---
_id: '12875'
abstract:
- lang: eng
text: The superior colliculus (SC) in the mammalian midbrain is essential for multisensory
integration and is composed of a rich diversity of excitatory and inhibitory neurons
and glia. However, the developmental principles directing the generation of SC
cell-type diversity are not understood. Here, we pursued systematic cell lineage
tracing in silico and in vivo, preserving full spatial information, using genetic
mosaic analysis with double markers (MADM)-based clonal analysis with single-cell
sequencing (MADM-CloneSeq). The analysis of clonally related cell lineages revealed
that radial glial progenitors (RGPs) in SC are exceptionally multipotent. Individual
resident RGPs have the capacity to produce all excitatory and inhibitory SC neuron
types, even at the stage of terminal division. While individual clonal units show
no pre-defined cellular composition, the establishment of appropriate relative
proportions of distinct neuronal types occurs in a PTEN-dependent manner. Collectively,
our findings provide an inaugural framework at the single-RGP/-cell level of the
mammalian SC ontogeny.
acknowledged_ssus:
- _id: Bio
- _id: M-Shop
- _id: LifeSc
- _id: PreCl
acknowledgement: "We thank Liqun Luo for his continued support, for providing essential
resources for generating Fzd10-CreER mice which were generated in his laboratory,
and for comments on the manuscript; W. Zhong for providing Nestin-Cre transgenic
mouse line for this study; A. Heger for mouse colony management; R. Beattie and
T. Asenov for designing and producing components of acute slice recovery chamber
for MADM-CloneSeq experiments; and K. Leopold, J. Rodarte and N. Amberg for initial
experiments, technical support and/or assistance. This study was supported by the
Scientific Service Units (SSU) of IST Austria through resources provided by the
Imaging & Optics Facility (IOF), Laboratory Support Facility (LSF), Miba Machine
Shop, and Pre-clinical Facility (PCF). G.C. received funding from European Commission
(IST plus postdoctoral fellowship). This work was supported by ISTA institutional\r\nfunds;
the Austrian Science Fund Special Research Programmes (FWF SFB F78 Neuro Stem Modulation)
to S.H. "
article_processing_charge: Yes (via OA deal)
article_type: original
author:
- first_name: Giselle T
full_name: Cheung, Giselle T
id: 471195F6-F248-11E8-B48F-1D18A9856A87
last_name: Cheung
orcid: 0000-0001-8457-2572
- first_name: Florian
full_name: Pauler, Florian
id: 48EA0138-F248-11E8-B48F-1D18A9856A87
last_name: Pauler
orcid: 0000-0002-7462-0048
- first_name: Peter
full_name: Koppensteiner, Peter
id: 3B8B25A8-F248-11E8-B48F-1D18A9856A87
last_name: Koppensteiner
orcid: 0000-0002-3509-1948
- first_name: Thomas
full_name: Krausgruber, Thomas
last_name: Krausgruber
- first_name: Carmen
full_name: Streicher, Carmen
id: 36BCB99C-F248-11E8-B48F-1D18A9856A87
last_name: Streicher
- first_name: Martin
full_name: Schrammel, Martin
id: f13e7cae-e8bd-11ed-841a-96dedf69f46d
last_name: Schrammel
- first_name: Natalie Y
full_name: Özgen, Natalie Y
id: e68ece33-f6e0-11ea-865d-ae1031dcc090
last_name: Özgen
- first_name: Alexis
full_name: Ivec, Alexis
id: 1d144691-e8be-11ed-9b33-bdd3077fad4c
last_name: Ivec
- first_name: Christoph
full_name: Bock, Christoph
last_name: Bock
- first_name: Ryuichi
full_name: Shigemoto, Ryuichi
id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
last_name: Shigemoto
orcid: 0000-0001-8761-9444
- first_name: Simon
full_name: Hippenmeyer, Simon
id: 37B36620-F248-11E8-B48F-1D18A9856A87
last_name: Hippenmeyer
orcid: 0000-0003-2279-1061
citation:
ama: Cheung GT, Pauler F, Koppensteiner P, et al. Multipotent progenitors instruct
ontogeny of the superior colliculus. Neuron. 2024;112(2):230-246.e11. doi:10.1016/j.neuron.2023.11.009
apa: Cheung, G. T., Pauler, F., Koppensteiner, P., Krausgruber, T., Streicher, C.,
Schrammel, M., … Hippenmeyer, S. (2024). Multipotent progenitors instruct ontogeny
of the superior colliculus. Neuron. Elsevier. https://doi.org/10.1016/j.neuron.2023.11.009
chicago: Cheung, Giselle T, Florian Pauler, Peter Koppensteiner, Thomas Krausgruber,
Carmen Streicher, Martin Schrammel, Natalie Y Özgen, et al. “Multipotent Progenitors
Instruct Ontogeny of the Superior Colliculus.” Neuron. Elsevier, 2024.
https://doi.org/10.1016/j.neuron.2023.11.009.
ieee: G. T. Cheung et al., “Multipotent progenitors instruct ontogeny of
the superior colliculus,” Neuron, vol. 112, no. 2. Elsevier, p. 230–246.e11,
2024.
ista: Cheung GT, Pauler F, Koppensteiner P, Krausgruber T, Streicher C, Schrammel
M, Özgen NY, Ivec A, Bock C, Shigemoto R, Hippenmeyer S. 2024. Multipotent progenitors
instruct ontogeny of the superior colliculus. Neuron. 112(2), 230–246.e11.
mla: Cheung, Giselle T., et al. “Multipotent Progenitors Instruct Ontogeny of the
Superior Colliculus.” Neuron, vol. 112, no. 2, Elsevier, 2024, p. 230–246.e11,
doi:10.1016/j.neuron.2023.11.009.
short: G.T. Cheung, F. Pauler, P. Koppensteiner, T. Krausgruber, C. Streicher, M.
Schrammel, N.Y. Özgen, A. Ivec, C. Bock, R. Shigemoto, S. Hippenmeyer, Neuron
112 (2024) 230–246.e11.
date_created: 2023-04-27T09:41:48Z
date_published: 2024-01-17T00:00:00Z
date_updated: 2024-03-05T09:43:02Z
day: '17'
ddc:
- '570'
department:
- _id: SiHi
- _id: RySh
doi: 10.1016/j.neuron.2023.11.009
external_id:
pmid:
- '38096816'
file:
- access_level: open_access
checksum: 32b3788f7085cf44a84108d8faaff3ce
content_type: application/pdf
creator: dernst
date_created: 2024-02-06T13:56:15Z
date_updated: 2024-02-06T13:56:15Z
file_id: '14944'
file_name: 2024_Neuron_Cheung.pdf
file_size: 5942467
relation: main_file
success: 1
file_date_updated: 2024-02-06T13:56:15Z
has_accepted_license: '1'
intvolume: ' 112'
issue: '2'
language:
- iso: eng
month: '01'
oa: 1
oa_version: Published Version
page: 230-246.e11
pmid: 1
project:
- _id: 059F6AB4-7A3F-11EA-A408-12923DDC885E
grant_number: F07805
name: Molecular Mechanisms of Neural Stem Cell Lineage Progression
publication: Neuron
publication_identifier:
issn:
- 0896-6273
publication_status: published
publisher: Elsevier
quality_controlled: '1'
related_material:
link:
- description: News on ISTA Website
relation: press_release
url: https://ista.ac.at/en/news/the-pedigree-of-brain-cells/
scopus_import: '1'
status: public
title: Multipotent progenitors instruct ontogeny of the superior colliculus
tmp:
image: /images/cc_by.png
legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
short: CC BY (4.0)
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 112
year: '2024'
...
---
_id: '15084'
abstract:
- lang: eng
text: "GABAB receptor (GBR) activation inhibits neurotransmitter release in axon
terminals in the brain, except in medial habenula (MHb) terminals, which show
robust potentiation. However, mechanisms underlying this enigmatic potentiation
remain elusive. Here, we report that GBR activation on MHb terminals induces an
activity-dependent transition from a facilitating, tonic to a depressing, phasic
neurotransmitter release mode. This transition is accompanied by a 4.1-fold increase
in readily releasable vesicle pool (RRP) size and a 3.5-fold increase of docked
synaptic vesicles (SVs) at the presynaptic active zone (AZ). Strikingly, the depressing
phasic release exhibits looser coupling distance than the tonic release. Furthermore,
the tonic and phasic release are selectively affected by deletion of synaptoporin
(SPO) and Ca\r\n 2+\r\n -dependent
activator protein for secretion 2 (CAPS2), respectively. SPO modulates augmentation,
the short-term plasticity associated with tonic release, and CAPS2 retains the
increased RRP for initial responses in phasic response trains. The cytosolic protein
CAPS2 showed a SV-associated distribution similar to the vesicular transmembrane
protein SPO, and they were colocalized in the same terminals. We developed the
“Flash and Freeze-fracture” method, and revealed the release of SPO-associated
vesicles in both tonic and phasic modes and activity-dependent recruitment of
CAPS2 to the AZ during phasic release, which lasted several minutes. Overall,
these results indicate that GBR activation translocates CAPS2 to the AZ along
with the fusion of CAPS2-associated SVs, contributing to persistency of the RRP
increase. Thus, we identified structural and molecular mechanisms underlying tonic
and phasic neurotransmitter release and their transition by GBR activation in
MHb terminals."
acknowledged_ssus:
- _id: M-Shop
- _id: PreCl
- _id: EM-Fac
acknowledgement: We thank Erwin Neher and Ipe Ninan for critical comments on the manuscript.
This project has received funding from the European Research Council (ERC) and European
Commission, under the European Union’s Horizon 2020 research and innovation program
(ERC grant agreement no. 694539 to R.S. and the Marie Skłodowska-Curie grant agreement
no. 665385 to C.Ö.). This study was supported by the Cooperative Study Program of
Center for Animal Resources and Collaborative Study of NINS. We thank Kohgaku Eguchi
for statistical analysis, Yu Kasugai for additional EM imaging, Robert Beattie for
the design of the slice recovery chamber for Flash and Freeze experiments, Todor
Asenov from the ISTA machine shop for custom part preparations for high-pressure
freezing, the ISTA preclinical facility for animal caretaking, and the ISTA EM facilities
for technical support.
article_number: e2301449121
article_processing_charge: Yes (in subscription journal)
article_type: original
author:
- first_name: Peter
full_name: Koppensteiner, Peter
id: 3B8B25A8-F248-11E8-B48F-1D18A9856A87
last_name: Koppensteiner
orcid: 0000-0002-3509-1948
- first_name: Pradeep
full_name: Bhandari, Pradeep
id: 45EDD1BC-F248-11E8-B48F-1D18A9856A87
last_name: Bhandari
orcid: 0000-0003-0863-4481
- first_name: Hüseyin C
full_name: Önal, Hüseyin C
id: 4659D740-F248-11E8-B48F-1D18A9856A87
last_name: Önal
orcid: 0000-0002-2771-2011
- first_name: Carolina
full_name: Borges Merjane, Carolina
id: 4305C450-F248-11E8-B48F-1D18A9856A87
last_name: Borges Merjane
orcid: 0000-0003-0005-401X
- first_name: Elodie
full_name: Le Monnier, Elodie
id: 3B59276A-F248-11E8-B48F-1D18A9856A87
last_name: Le Monnier
- first_name: Utsa
full_name: Roy, Utsa
id: 4d26cf11-5355-11ee-ae5a-eb05e255b9b2
last_name: Roy
- first_name: Yukihiro
full_name: Nakamura, Yukihiro
last_name: Nakamura
- first_name: Tetsushi
full_name: Sadakata, Tetsushi
last_name: Sadakata
- first_name: Makoto
full_name: Sanbo, Makoto
last_name: Sanbo
- first_name: Masumi
full_name: Hirabayashi, Masumi
last_name: Hirabayashi
- first_name: JeongSeop
full_name: Rhee, JeongSeop
last_name: Rhee
- first_name: Nils
full_name: Brose, Nils
last_name: Brose
- first_name: Peter M
full_name: Jonas, Peter M
id: 353C1B58-F248-11E8-B48F-1D18A9856A87
last_name: Jonas
orcid: 0000-0001-5001-4804
- first_name: Ryuichi
full_name: Shigemoto, Ryuichi
id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
last_name: Shigemoto
orcid: 0000-0001-8761-9444
citation:
ama: Koppensteiner P, Bhandari P, Önal C, et al. GABAB receptors induce phasic release
from medial habenula terminals through activity-dependent recruitment of release-ready
vesicles. Proceedings of the National Academy of Sciences. 2024;121(8).
doi:10.1073/pnas.2301449121
apa: Koppensteiner, P., Bhandari, P., Önal, C., Borges Merjane, C., Le Monnier,
E., Roy, U., … Shigemoto, R. (2024). GABAB receptors induce phasic release from
medial habenula terminals through activity-dependent recruitment of release-ready
vesicles. Proceedings of the National Academy of Sciences. Proceedings
of the National Academy of Sciences. https://doi.org/10.1073/pnas.2301449121
chicago: Koppensteiner, Peter, Pradeep Bhandari, Cihan Önal, Carolina Borges Merjane,
Elodie Le Monnier, Utsa Roy, Yukihiro Nakamura, et al. “GABAB Receptors Induce
Phasic Release from Medial Habenula Terminals through Activity-Dependent Recruitment
of Release-Ready Vesicles.” Proceedings of the National Academy of Sciences.
Proceedings of the National Academy of Sciences, 2024. https://doi.org/10.1073/pnas.2301449121.
ieee: P. Koppensteiner et al., “GABAB receptors induce phasic release from
medial habenula terminals through activity-dependent recruitment of release-ready
vesicles,” Proceedings of the National Academy of Sciences, vol. 121, no.
8. Proceedings of the National Academy of Sciences, 2024.
ista: Koppensteiner P, Bhandari P, Önal C, Borges Merjane C, Le Monnier E, Roy U,
Nakamura Y, Sadakata T, Sanbo M, Hirabayashi M, Rhee J, Brose N, Jonas PM, Shigemoto
R. 2024. GABAB receptors induce phasic release from medial habenula terminals
through activity-dependent recruitment of release-ready vesicles. Proceedings
of the National Academy of Sciences. 121(8), e2301449121.
mla: Koppensteiner, Peter, et al. “GABAB Receptors Induce Phasic Release from Medial
Habenula Terminals through Activity-Dependent Recruitment of Release-Ready Vesicles.”
Proceedings of the National Academy of Sciences, vol. 121, no. 8, e2301449121,
Proceedings of the National Academy of Sciences, 2024, doi:10.1073/pnas.2301449121.
short: P. Koppensteiner, P. Bhandari, C. Önal, C. Borges Merjane, E. Le Monnier,
U. Roy, Y. Nakamura, T. Sadakata, M. Sanbo, M. Hirabayashi, J. Rhee, N. Brose,
P.M. Jonas, R. Shigemoto, Proceedings of the National Academy of Sciences 121
(2024).
date_created: 2024-03-05T09:23:55Z
date_published: 2024-02-20T00:00:00Z
date_updated: 2024-03-12T13:44:18Z
day: '20'
ddc:
- '570'
department:
- _id: RySh
- _id: PeJo
doi: 10.1073/pnas.2301449121
ec_funded: 1
external_id:
pmid:
- '38346189'
file:
- access_level: open_access
checksum: b25b2a057c266ff317a48b0d54d6fc8a
content_type: application/pdf
creator: dernst
date_created: 2024-03-12T13:42:42Z
date_updated: 2024-03-12T13:42:42Z
file_id: '15110'
file_name: 2024_PNAS_Koppensteiner.pdf
file_size: 13648221
relation: main_file
success: 1
file_date_updated: 2024-03-12T13:42:42Z
has_accepted_license: '1'
intvolume: ' 121'
issue: '8'
language:
- iso: eng
license: https://creativecommons.org/licenses/by-nc-nd/4.0/
month: '02'
oa: 1
oa_version: Published Version
pmid: 1
project:
- _id: 25CA28EA-B435-11E9-9278-68D0E5697425
call_identifier: H2020
grant_number: '694539'
name: 'In situ analysis of single channel subunit composition in neurons: physiological
implication in synaptic plasticity and behaviour'
- _id: 2564DBCA-B435-11E9-9278-68D0E5697425
call_identifier: H2020
grant_number: '665385'
name: International IST Doctoral Program
publication: Proceedings of the National Academy of Sciences
publication_identifier:
eissn:
- 1091-6490
issn:
- 0027-8424
publication_status: published
publisher: Proceedings of the National Academy of Sciences
quality_controlled: '1'
related_material:
link:
- description: News on ISTA Website
relation: press_release
url: https://ista.ac.at/en/news/neuronal-insights-flash-and-freeze-fracture/
record:
- id: '13173'
relation: research_data
status: public
status: public
title: GABAB receptors induce phasic release from medial habenula terminals through
activity-dependent recruitment of release-ready vesicles
tmp:
image: /images/cc_by_nc_nd.png
legal_code_url: https://creativecommons.org/licenses/by-nc-nd/4.0/legalcode
name: Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International
(CC BY-NC-ND 4.0)
short: CC BY-NC-ND (4.0)
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 121
year: '2024'
...
---
_id: '14843'
abstract:
- lang: eng
text: The coupling between Ca2+ channels and release sensors is a key factor defining
the signaling properties of a synapse. However, the coupling nanotopography at
many synapses remains unknown, and it is unclear how it changes during development.
To address these questions, we examined coupling at the cerebellar inhibitory
basket cell (BC)-Purkinje cell (PC) synapse. Biophysical analysis of transmission
by paired recording and intracellular pipette perfusion revealed that the effects
of exogenous Ca2+ chelators decreased during development, despite constant reliance
of release on P/Q-type Ca2+ channels. Structural analysis by freeze-fracture replica
labeling (FRL) and transmission electron microscopy (EM) indicated that presynaptic
P/Q-type Ca2+ channels formed nanoclusters throughout development, whereas docked
vesicles were only clustered at later developmental stages. Modeling suggested
a developmental transformation from a more random to a more clustered coupling
nanotopography. Thus, presynaptic signaling developmentally approaches a point-to-point
configuration, optimizing speed, reliability, and energy efficiency of synaptic
transmission.
acknowledged_ssus:
- _id: EM-Fac
- _id: PreCl
- _id: M-Shop
acknowledgement: We thank Drs. David DiGregorio and Erwin Neher for critically reading
an earlier version of the manuscript, Ralf Schneggenburger for helpful discussions,
Benjamin Suter and Katharina Lichter for support with image analysis, Chris Wojtan
for advice on numerical solution of partial differential equations, Maria Reva for
help with Ripley analysis, Alois Schlögl for programming, and Akari Hagiwara and
Toshihisa Ohtsuka for anti-ELKS antibody. We are grateful to Florian Marr, Christina
Altmutter, and Vanessa Zheden for excellent technical assistance and to Eleftheria
Kralli-Beller for manuscript editing. This research was supported by the Scientific
Services Units (SSUs) of ISTA (Electron Microscopy Facility, Preclinical Facility,
and Machine Shop). The project received funding from the European Research Council
(ERC) under the European Union’s Horizon 2020 research and innovation program (grant
agreement no. 692692), the Fonds zur Förderung der Wissenschaftlichen Forschung
(Z 312-B27, Wittgenstein award; P 36232-B), all to P.J., and a DOC fellowship of
the Austrian Academy of Sciences to J.-J.C.
article_processing_charge: No
article_type: original
author:
- first_name: JingJing
full_name: Chen, JingJing
id: 2C4E65C8-F248-11E8-B48F-1D18A9856A87
last_name: Chen
- first_name: Walter
full_name: Kaufmann, Walter
id: 3F99E422-F248-11E8-B48F-1D18A9856A87
last_name: Kaufmann
orcid: 0000-0001-9735-5315
- first_name: Chong
full_name: Chen, Chong
id: 3DFD581A-F248-11E8-B48F-1D18A9856A87
last_name: Chen
- first_name: Itaru
full_name: Arai, Itaru
id: 32A73F6C-F248-11E8-B48F-1D18A9856A87
last_name: Arai
- first_name: Olena
full_name: Kim, Olena
id: 3F8ABDDA-F248-11E8-B48F-1D18A9856A87
last_name: Kim
- first_name: Ryuichi
full_name: Shigemoto, Ryuichi
id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
last_name: Shigemoto
orcid: 0000-0001-8761-9444
- first_name: Peter M
full_name: Jonas, Peter M
id: 353C1B58-F248-11E8-B48F-1D18A9856A87
last_name: Jonas
orcid: 0000-0001-5001-4804
citation:
ama: Chen J, Kaufmann W, Chen C, et al. Developmental transformation of Ca2+ channel-vesicle
nanotopography at a central GABAergic synapse. Neuron. doi:10.1016/j.neuron.2023.12.002
apa: Chen, J., Kaufmann, W., Chen, C., Arai, itaru, Kim, O., Shigemoto, R., &
Jonas, P. M. (n.d.). Developmental transformation of Ca2+ channel-vesicle nanotopography
at a central GABAergic synapse. Neuron. Elsevier. https://doi.org/10.1016/j.neuron.2023.12.002
chicago: Chen, JingJing, Walter Kaufmann, Chong Chen, itaru Arai, Olena Kim, Ryuichi
Shigemoto, and Peter M Jonas. “Developmental Transformation of Ca2+ Channel-Vesicle
Nanotopography at a Central GABAergic Synapse.” Neuron. Elsevier, n.d.
https://doi.org/10.1016/j.neuron.2023.12.002.
ieee: J. Chen et al., “Developmental transformation of Ca2+ channel-vesicle
nanotopography at a central GABAergic synapse,” Neuron. Elsevier.
ista: Chen J, Kaufmann W, Chen C, Arai itaru, Kim O, Shigemoto R, Jonas PM. Developmental
transformation of Ca2+ channel-vesicle nanotopography at a central GABAergic synapse.
Neuron.
mla: Chen, JingJing, et al. “Developmental Transformation of Ca2+ Channel-Vesicle
Nanotopography at a Central GABAergic Synapse.” Neuron, Elsevier, doi:10.1016/j.neuron.2023.12.002.
short: J. Chen, W. Kaufmann, C. Chen, itaru Arai, O. Kim, R. Shigemoto, P.M. Jonas,
Neuron (n.d.).
date_created: 2024-01-21T23:00:56Z
date_published: 2024-01-11T00:00:00Z
date_updated: 2024-03-14T13:14:18Z
day: '11'
department:
- _id: PeJo
- _id: EM-Fac
- _id: RySh
doi: 10.1016/j.neuron.2023.12.002
ec_funded: 1
external_id:
pmid:
- '38215739'
language:
- iso: eng
month: '01'
oa_version: None
pmid: 1
project:
- _id: 25B7EB9E-B435-11E9-9278-68D0E5697425
call_identifier: H2020
grant_number: '692692'
name: Biophysics and circuit function of a giant cortical glumatergic synapse
- _id: 25C5A090-B435-11E9-9278-68D0E5697425
call_identifier: FWF
grant_number: Z00312
name: The Wittgenstein Prize
- _id: bd88be38-d553-11ed-ba76-81d5a70a6ef5
grant_number: P36232
name: Mechanisms of GABA release in hippocampal circuits
- _id: 26B66A3E-B435-11E9-9278-68D0E5697425
grant_number: '25383'
name: Development of nanodomain coupling between Ca2+ channels and release sensors
at a central inhibitory synapse
publication: Neuron
publication_identifier:
eissn:
- 1097-4199
issn:
- 0896-6273
publication_status: inpress
publisher: Elsevier
quality_controlled: '1'
related_material:
link:
- description: News on ISTA Website
relation: press_release
url: https://ista.ac.at/en/news/synapses-brought-to-the-point/
record:
- id: '15101'
relation: dissertation_contains
status: public
scopus_import: '1'
status: public
title: Developmental transformation of Ca2+ channel-vesicle nanotopography at a central
GABAergic synapse
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
year: '2024'
...
---
_id: '12809'
abstract:
- lang: eng
text: "Understanding the mechanisms of learning and memory formation has always
been one of\r\nthe main goals in neuroscience. Already Pavlov (1927) in his early
days has used his classic\r\nconditioning experiments to study the neural mechanisms
governing behavioral adaptation.\r\nWhat was not known back then was that the
part of the brain that is largely responsible for\r\nthis type of associative
learning is the cerebellum.\r\nSince then, plenty of theories on cerebellar learning
have emerged. Despite their differences,\r\none thing they all have in common
is that learning relies on synaptic and intrinsic plasticity.\r\nThe goal of my
PhD project was to unravel the molecular mechanisms underlying synaptic\r\nplasticity
in two synapses that have been shown to be implicated in motor learning, in an\r\neffort
to understand how learning and memory formation are processed in the cerebellum.\r\nOne
of the earliest and most well-known cerebellar theories postulates that motor
learning\r\nlargely depends on long-term depression at the parallel fiber-Purkinje
cell (PC-PC) synapse.\r\nHowever, the discovery of other types of plasticity in
the cerebellar circuitry, like long-term\r\npotentiation (LTP) at the PC-PC synapse,
potentiation of molecular layer interneurons (MLIs),\r\nand plasticity transfer
from the cortex to the cerebellar/ vestibular nuclei has increased the\r\npopularity
of the idea that multiple sites of plasticity might be involved in learning.\r\nStill
a lot remains unknown about the molecular mechanisms responsible for these types
of\r\nplasticity and whether they occur during physiological learning.\r\nIn the
first part of this thesis we have analyzed the variation and nanodistribution
of voltagegated calcium channels (VGCCs) and α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic
acid\r\ntype glutamate receptors (AMPARs) on the parallel fiber-Purkinje cell
synapse after vestibuloocular reflex phase reversal adaptation, a behavior that
has been suggested to rely on PF-PC\r\nLTP. We have found that on the last day
of adaptation there is no learning trace in form of\r\nVGCCs nor AMPARs variation
at the PF-PC synapse, but instead a decrease in the number of\r\nPF-PC synapses.
These data seem to support the view that learning is only stored in the\r\ncerebellar
cortex in an initial learning phase, being transferred later to the vestibular
nuclei.\r\nNext, we have studied the role of MLIs in motor learning using a relatively
simple and well characterized behavioral paradigm – horizontal optokinetic reflex
(HOKR) adaptation. We\r\nhave found behavior-induced MLI potentiation in form
of release probability increase that\r\ncould be explained by the increase of
VGCCs at the presynaptic side. Our results strengthen\r\nthe idea of distributed
cerebellar plasticity contributing to learning and provide a novel\r\nmechanism
for release probability increase. "
acknowledged_ssus:
- _id: EM-Fac
- _id: Bio
- _id: PreCl
alternative_title:
- ISTA Thesis
article_processing_charge: No
author:
- first_name: Catarina
full_name: Alcarva, Catarina
id: 3A96634C-F248-11E8-B48F-1D18A9856A87
last_name: Alcarva
citation:
ama: 'Alcarva C. Plasticity in the cerebellum: What molecular mechanisms are behind
physiological learning. 2023. doi:10.15479/at:ista:12809'
apa: 'Alcarva, C. (2023). Plasticity in the cerebellum: What molecular mechanisms
are behind physiological learning. Institute of Science and Technology Austria.
https://doi.org/10.15479/at:ista:12809'
chicago: 'Alcarva, Catarina. “Plasticity in the Cerebellum: What Molecular Mechanisms
Are behind Physiological Learning.” Institute of Science and Technology Austria,
2023. https://doi.org/10.15479/at:ista:12809.'
ieee: 'C. Alcarva, “Plasticity in the cerebellum: What molecular mechanisms are
behind physiological learning,” Institute of Science and Technology Austria, 2023.'
ista: 'Alcarva C. 2023. Plasticity in the cerebellum: What molecular mechanisms
are behind physiological learning. Institute of Science and Technology Austria.'
mla: 'Alcarva, Catarina. Plasticity in the Cerebellum: What Molecular Mechanisms
Are behind Physiological Learning. Institute of Science and Technology Austria,
2023, doi:10.15479/at:ista:12809.'
short: 'C. Alcarva, Plasticity in the Cerebellum: What Molecular Mechanisms Are
behind Physiological Learning, Institute of Science and Technology Austria, 2023.'
date_created: 2023-04-06T07:54:09Z
date_published: 2023-04-06T00:00:00Z
date_updated: 2023-04-26T12:16:56Z
day: '06'
ddc:
- '570'
degree_awarded: PhD
department:
- _id: GradSch
- _id: RySh
doi: 10.15479/at:ista:12809
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date_updated: 2023-04-07T06:18:05Z
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file_date_updated: 2023-04-07T06:18:05Z
has_accepted_license: '1'
language:
- iso: eng
month: '04'
oa_version: Published Version
page: '115'
project:
- _id: 267DFB90-B435-11E9-9278-68D0E5697425
name: 'Plasticity in the cerebellum: Which molecular mechanisms are behind physiological
learning?'
publication_identifier:
issn:
- 2663 - 337X
publication_status: published
publisher: Institute of Science and Technology Austria
status: public
supervisor:
- first_name: Ryuichi
full_name: Shigemoto, Ryuichi
id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
last_name: Shigemoto
orcid: 0000-0001-8761-9444
title: 'Plasticity in the cerebellum: What molecular mechanisms are behind physiological
learning'
type: dissertation
user_id: 8b945eb4-e2f2-11eb-945a-df72226e66a9
year: '2023'
...
---
_id: '14253'
abstract:
- lang: eng
text: Junctions between the endoplasmic reticulum (ER) and the plasma membrane (PM)
are specialized membrane contacts ubiquitous in eukaryotic cells. Concentration
of intracellular signaling machinery near ER-PM junctions allows these domains
to serve critical roles in lipid and Ca2+ signaling and homeostasis. Subcellular
compartmentalization of protein kinase A (PKA) signaling also regulates essential
cellular functions, however, no specific association between PKA and ER-PM junctional
domains is known. Here, we show that in brain neurons type I PKA is directed to
Kv2.1 channel-dependent ER-PM junctional domains via SPHKAP, a type I PKA-specific
anchoring protein. SPHKAP association with type I PKA regulatory subunit RI and
ER-resident VAP proteins results in the concentration of type I PKA between stacked
ER cisternae associated with ER-PM junctions. This ER-associated PKA signalosome
enables reciprocal regulation between PKA and Ca2+ signaling machinery to support
Ca2+ influx and excitation-transcription coupling. These data reveal that neuronal
ER-PM junctions support a receptor-independent form of PKA signaling driven by
membrane depolarization and intracellular Ca2+, allowing conversion of information
encoded in electrical signals into biochemical changes universally recognized
throughout the cell.
acknowledgement: We thank Kayla Templeton and Peter Turcanu for technical assistance,
Michelle Salemi for assistance with LC-MS data acquisition and analysis, Dr. Belvin
Gong for advice on monoclonal antibody generation, Drs. Maria Casas Prat and Eamonn
Dickson for assistance with super-resolution TIRF microscopy, Dr. Oscar Cerda for
assistance with the design of TAT-FFAT peptides, Dr. Fernando Santana for helpful
discussions, and Dr. Jodi Nunnari for a careful reading of our manuscript. We also
thank Dr. Alan Howe, Dr. Sohum Mehta, and Dr. Jin Zhang for providing plasmids used
in this study. This project was funded by NIH Grants R01NS114210 and R21NS101648
(J.S.T.), and F32NS108519 (N.C.V.).
article_number: '5231'
article_processing_charge: Yes
article_type: original
author:
- first_name: Nicholas C.
full_name: Vierra, Nicholas C.
last_name: Vierra
- first_name: Luisa
full_name: Ribeiro-Silva, Luisa
last_name: Ribeiro-Silva
- first_name: Michael
full_name: Kirmiz, Michael
last_name: Kirmiz
- first_name: Deborah
full_name: Van Der List, Deborah
last_name: Van Der List
- first_name: Pradeep
full_name: Bhandari, Pradeep
id: 45EDD1BC-F248-11E8-B48F-1D18A9856A87
last_name: Bhandari
orcid: 0000-0003-0863-4481
- first_name: Olivia A.
full_name: Mack, Olivia A.
last_name: Mack
- first_name: James
full_name: Carroll, James
last_name: Carroll
- first_name: Elodie
full_name: Le Monnier, Elodie
id: 3B59276A-F248-11E8-B48F-1D18A9856A87
last_name: Le Monnier
- first_name: Sue A.
full_name: Aicher, Sue A.
last_name: Aicher
- first_name: Ryuichi
full_name: Shigemoto, Ryuichi
id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
last_name: Shigemoto
orcid: 0000-0001-8761-9444
- first_name: James S.
full_name: Trimmer, James S.
last_name: Trimmer
citation:
ama: Vierra NC, Ribeiro-Silva L, Kirmiz M, et al. Neuronal ER-plasma membrane junctions
couple excitation to Ca2+-activated PKA signaling. Nature Communications.
2023;14. doi:10.1038/s41467-023-40930-6
apa: Vierra, N. C., Ribeiro-Silva, L., Kirmiz, M., Van Der List, D., Bhandari, P.,
Mack, O. A., … Trimmer, J. S. (2023). Neuronal ER-plasma membrane junctions couple
excitation to Ca2+-activated PKA signaling. Nature Communications. Springer
Nature. https://doi.org/10.1038/s41467-023-40930-6
chicago: Vierra, Nicholas C., Luisa Ribeiro-Silva, Michael Kirmiz, Deborah Van Der
List, Pradeep Bhandari, Olivia A. Mack, James Carroll, et al. “Neuronal ER-Plasma
Membrane Junctions Couple Excitation to Ca2+-Activated PKA Signaling.” Nature
Communications. Springer Nature, 2023. https://doi.org/10.1038/s41467-023-40930-6.
ieee: N. C. Vierra et al., “Neuronal ER-plasma membrane junctions couple
excitation to Ca2+-activated PKA signaling,” Nature Communications, vol.
14. Springer Nature, 2023.
ista: Vierra NC, Ribeiro-Silva L, Kirmiz M, Van Der List D, Bhandari P, Mack OA,
Carroll J, Le Monnier E, Aicher SA, Shigemoto R, Trimmer JS. 2023. Neuronal ER-plasma
membrane junctions couple excitation to Ca2+-activated PKA signaling. Nature Communications.
14, 5231.
mla: Vierra, Nicholas C., et al. “Neuronal ER-Plasma Membrane Junctions Couple Excitation
to Ca2+-Activated PKA Signaling.” Nature Communications, vol. 14, 5231,
Springer Nature, 2023, doi:10.1038/s41467-023-40930-6.
short: N.C. Vierra, L. Ribeiro-Silva, M. Kirmiz, D. Van Der List, P. Bhandari, O.A.
Mack, J. Carroll, E. Le Monnier, S.A. Aicher, R. Shigemoto, J.S. Trimmer, Nature
Communications 14 (2023).
date_created: 2023-09-03T22:01:14Z
date_published: 2023-08-26T00:00:00Z
date_updated: 2023-09-06T06:53:32Z
day: '26'
ddc:
- '570'
department:
- _id: RySh
doi: 10.1038/s41467-023-40930-6
external_id:
pmid:
- '37633939'
file:
- access_level: open_access
checksum: 6ab8aab4e957f626a09a1c73db3388fb
content_type: application/pdf
creator: dernst
date_created: 2023-09-06T06:50:07Z
date_updated: 2023-09-06T06:50:07Z
file_id: '14270'
file_name: 2023_NatureComm_Vierra.pdf
file_size: 9412549
relation: main_file
success: 1
file_date_updated: 2023-09-06T06:50:07Z
has_accepted_license: '1'
intvolume: ' 14'
language:
- iso: eng
month: '08'
oa: 1
oa_version: Published Version
pmid: 1
publication: Nature Communications
publication_identifier:
eissn:
- 2041-1723
publication_status: published
publisher: Springer Nature
quality_controlled: '1'
scopus_import: '1'
status: public
title: Neuronal ER-plasma membrane junctions couple excitation to Ca2+-activated PKA
signaling
tmp:
image: /images/cc_by.png
legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
short: CC BY (4.0)
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 14
year: '2023'
...
---
_id: '13202'
abstract:
- lang: eng
text: Phosphatidylinositol-4,5-bisphosphate (PI(4,5)P2) plays an essential role
in neuronal activities through interaction with various proteins involved in signaling
at membranes. However, the distribution pattern of PI(4,5)P2 and the association
with these proteins on the neuronal cell membranes remain elusive. In this study,
we established a method for visualizing PI(4,5)P2 by SDS-digested freeze-fracture
replica labeling (SDS-FRL) to investigate the quantitative nanoscale distribution
of PI(4,5)P2 in cryo-fixed brain. We demonstrate that PI(4,5)P2 forms tiny clusters
with a mean size of ∼1000 nm2 rather than randomly distributed in cerebellar neuronal
membranes in male C57BL/6J mice. These clusters show preferential accumulation
in specific membrane compartments of different cell types, in particular, in Purkinje
cell (PC) spines and granule cell (GC) presynaptic active zones. Furthermore,
we revealed extensive association of PI(4,5)P2 with CaV2.1 and GIRK3 across different
membrane compartments, whereas its association with mGluR1α was compartment specific.
These results suggest that our SDS-FRL method provides valuable insights into
the physiological functions of PI(4,5)P2 in neurons.
acknowledged_ssus:
- _id: EM-Fac
acknowledgement: This work was supported by The Institute of Science and Technology
(IST) Austria, the European Union's Horizon 2020 Research and Innovation Program
under the Marie Skłodowska-Curie Grant Agreement No. 793482 (to K.E.) and by the
European Research Council (ERC) Grant Agreement No. 694539 (to R.S.). We thank Nicoleta
Condruz (IST Austria, Klosterneuburg, Austria) for technical assistance with sample
preparation, the Electron Microscopy Facility of IST Austria (Klosterneuburg, Austria)
for technical support with EM works, Natalia Baranova (University of Vienna, Vienna,
Austria) and Martin Loose (IST Austria, Klosterneuburg, Austria) for advice on liposome
preparation, and Yugo Fukazawa (University of Fukui, Fukui, Japan) for comments.
article_processing_charge: No
article_type: original
author:
- first_name: Kohgaku
full_name: Eguchi, Kohgaku
id: 2B7846DC-F248-11E8-B48F-1D18A9856A87
last_name: Eguchi
orcid: 0000-0002-6170-2546
- first_name: Elodie
full_name: Le Monnier, Elodie
id: 3B59276A-F248-11E8-B48F-1D18A9856A87
last_name: Le Monnier
- first_name: Ryuichi
full_name: Shigemoto, Ryuichi
id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
last_name: Shigemoto
orcid: 0000-0001-8761-9444
citation:
ama: Eguchi K, Le Monnier E, Shigemoto R. Nanoscale phosphoinositide distribution
on cell membranes of mouse cerebellar neurons. The Journal of Neuroscience.
2023;43(23):4197-4216. doi:10.1523/JNEUROSCI.1514-22.2023
apa: Eguchi, K., Le Monnier, E., & Shigemoto, R. (2023). Nanoscale phosphoinositide
distribution on cell membranes of mouse cerebellar neurons. The Journal of
Neuroscience. Society for Neuroscience. https://doi.org/10.1523/JNEUROSCI.1514-22.2023
chicago: Eguchi, Kohgaku, Elodie Le Monnier, and Ryuichi Shigemoto. “Nanoscale Phosphoinositide
Distribution on Cell Membranes of Mouse Cerebellar Neurons.” The Journal of
Neuroscience. Society for Neuroscience, 2023. https://doi.org/10.1523/JNEUROSCI.1514-22.2023.
ieee: K. Eguchi, E. Le Monnier, and R. Shigemoto, “Nanoscale phosphoinositide distribution
on cell membranes of mouse cerebellar neurons,” The Journal of Neuroscience,
vol. 43, no. 23. Society for Neuroscience, pp. 4197–4216, 2023.
ista: Eguchi K, Le Monnier E, Shigemoto R. 2023. Nanoscale phosphoinositide distribution
on cell membranes of mouse cerebellar neurons. The Journal of Neuroscience. 43(23),
4197–4216.
mla: Eguchi, Kohgaku, et al. “Nanoscale Phosphoinositide Distribution on Cell Membranes
of Mouse Cerebellar Neurons.” The Journal of Neuroscience, vol. 43, no.
23, Society for Neuroscience, 2023, pp. 4197–216, doi:10.1523/JNEUROSCI.1514-22.2023.
short: K. Eguchi, E. Le Monnier, R. Shigemoto, The Journal of Neuroscience 43 (2023)
4197–4216.
date_created: 2023-07-09T22:01:12Z
date_published: 2023-06-07T00:00:00Z
date_updated: 2023-10-18T07:12:47Z
day: '07'
ddc:
- '570'
department:
- _id: RySh
doi: 10.1523/JNEUROSCI.1514-22.2023
ec_funded: 1
external_id:
isi:
- '001020132100005'
pmid:
- '37160366'
file:
- access_level: open_access
checksum: 70b2141870e0bf1c94fd343e18fdbc32
content_type: application/pdf
creator: alisjak
date_created: 2023-07-10T09:04:58Z
date_updated: 2023-07-10T09:04:58Z
file_id: '13205'
file_name: 2023_JN_Eguchi.pdf
file_size: 7794425
relation: main_file
success: 1
file_date_updated: 2023-07-10T09:04:58Z
has_accepted_license: '1'
intvolume: ' 43'
isi: 1
issue: '23'
language:
- iso: eng
month: '06'
oa: 1
oa_version: Published Version
page: 4197-4216
pmid: 1
project:
- _id: 2659CC84-B435-11E9-9278-68D0E5697425
call_identifier: H2020
grant_number: '793482'
name: 'Ultrastructural analysis of phosphoinositides in nerve terminals: distribution,
dynamics and physiological roles in synaptic transmission'
- _id: 25CA28EA-B435-11E9-9278-68D0E5697425
call_identifier: H2020
grant_number: '694539'
name: 'In situ analysis of single channel subunit composition in neurons: physiological
implication in synaptic plasticity and behaviour'
publication: The Journal of Neuroscience
publication_identifier:
eissn:
- 1529-2401
issn:
- 0270-6474
publication_status: published
publisher: Society for Neuroscience
quality_controlled: '1'
scopus_import: '1'
status: public
title: Nanoscale phosphoinositide distribution on cell membranes of mouse cerebellar
neurons
tmp:
image: /images/cc_by.png
legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
short: CC BY (4.0)
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 43
year: '2023'
...
---
_id: '13126'
abstract:
- lang: eng
text: Mapping the complex and dense arrangement of cells and their connectivity
in brain tissue demands nanoscale spatial resolution imaging. Super-resolution
optical microscopy excels at visualizing specific molecules and individual cells
but fails to provide tissue context. Here, we developed Comprehensive Analysis
of Tissues across Scales (CATS), a technology to densely map brain tissue architecture
from millimeter regional to nanometer synaptic scales in diverse chemically fixed
brain preparations, including rodent and human. CATS uses fixation-compatible
extracellular labeling and optical imaging, including stimulated emission depletion
or expansion microscopy, to comprehensively delineate cellular structures. It
enables three-dimensional reconstruction of single synapses and mapping of synaptic
connectivity by identification and analysis of putative synaptic cleft regions.
Applying CATS to the mouse hippocampal mossy fiber circuitry, we reconstructed
and quantified the synaptic input and output structure of identified neurons.
We furthermore demonstrate applicability to clinically derived human tissue samples,
including formalin-fixed paraffin-embedded routine diagnostic specimens, for visualizing
the cellular architecture of brain tissue in health and disease.
acknowledged_ssus:
- _id: ScienComp
- _id: Bio
- _id: PreCl
- _id: LifeSc
- _id: M-Shop
- _id: E-Lib
acknowledgement: "We thank Jakob Vorlaufer, Nathalie Agudelo-Dueñas, Wiebke Jahr,
Andreas Wartak for microscope maintenance and troubleshooting, Caroline Kreuzinger,
Anna Freeman, and Irene Erber for technical assistance and Matthias Tomschik for
support with obtaining human samples. We gratefully acknowledge Eder Miguel for
setting up webKnossos and Marek Šuplata for computational support and hardware control.
We are grateful to Ryuichi Shigemoto and Bernd Bickel for generous support, and
Michael Sixt and Scott Boyd (Stanford University) for discussions and critical reading
of the manuscript. PSD95-HaloTag mice were kindly provided by Seth Grant (University
of Edinburgh). We acknowledge expert support by IST Austria’s scientific computing,
imaging and optics, preclinical, and lab support facilities, and by the Library
and Miba machine shop.\r\nWe gratefully acknowledge funding by the following sources:
\r\nAustrian Science Fund (FWF) grant I3600-B27 (JGD)\r\nAustrian Science Fund (FWF)
grant DK W1232 (JGD, JMM)\r\nAustrian Science Fund (FWF) grant Z 312-B27, Wittgenstein
award (PJ)\r\nAustrian Science Funds (FWF) projects I4685-B, I6565-B (SYNABS) and
DOC 33-B27 (RH)\r\nGesellschaft für Forschungsförderung NÖ (NFB) grant LSC18-022
(JGD)\r\nEuropean Union’s Horizon 2020 research and innovation programme, European
Research Council (ERC) grant 715508 – REVERSEAUTISM (GN)\r\nEuropean Union’s Horizon
2020 research and innovation programme, European Research Council (ERC) grant 692692
– GIANTSYN (PJ)\r\nMarie Skłodowska-Curie Actions Fellowship GA no. 665385 under
the EU Horizon 2020 program (JMM, JL)\r\nMarie Skłodowska-Curie Actions Individual
Fellowship 101026635 under the EU Horizon 2020 program (JFW)"
article_processing_charge: No
author:
- first_name: Johann G
full_name: Danzl, Johann G
id: 42EFD3B6-F248-11E8-B48F-1D18A9856A87
last_name: Danzl
orcid: 0000-0001-8559-3973
citation:
ama: Danzl JG. Research data for the publication “Imaging brain tissue architecture
across millimeter to nanometer scales.” 2023. doi:10.15479/AT:ISTA:13126
apa: Danzl, J. G. (2023). Research data for the publication “Imaging brain tissue
architecture across millimeter to nanometer scales.” Institute of Science and
Technology Austria. https://doi.org/10.15479/AT:ISTA:13126
chicago: Danzl, Johann G. “Research Data for the Publication ‘Imaging Brain Tissue
Architecture across Millimeter to Nanometer Scales.’” Institute of Science and
Technology Austria, 2023. https://doi.org/10.15479/AT:ISTA:13126.
ieee: J. G. Danzl, “Research data for the publication ‘Imaging brain tissue architecture
across millimeter to nanometer scales.’” Institute of Science and Technology Austria,
2023.
ista: Danzl JG. 2023. Research data for the publication ‘Imaging brain tissue architecture
across millimeter to nanometer scales’, Institute of Science and Technology Austria,
10.15479/AT:ISTA:13126.
mla: Danzl, Johann G. Research Data for the Publication “Imaging Brain Tissue
Architecture across Millimeter to Nanometer Scales.” Institute of Science
and Technology Austria, 2023, doi:10.15479/AT:ISTA:13126.
short: J.G. Danzl, (2023).
contributor:
- first_name: Julia M
id: 443DB6DE-F248-11E8-B48F-1D18A9856A87
last_name: Michalska
- first_name: Julia
id: 46E28B80-F248-11E8-B48F-1D18A9856A87
last_name: Lyudchik
- first_name: Philipp
id: 39BDC62C-F248-11E8-B48F-1D18A9856A87
last_name: Velicky
orcid: 0000-0002-2340-7431
- first_name: Hana
id: ee3cb6ca-ec98-11ea-ae11-ff703e2254ed
last_name: Stefanickova
- first_name: Jake
id: 63836096-4690-11EA-BD4E-32803DDC885E
last_name: Watson
orcid: 0000-0002-8698-3823
- first_name: Alban
id: 9ac8f577-2357-11eb-997a-e566c5550886
last_name: Cenameri
- first_name: Christoph M
id: 4DF26D8C-F248-11E8-B48F-1D18A9856A87
last_name: Sommer
orcid: 0000-0003-1216-9105
- first_name: Nicole
id: 4CD6AAC6-F248-11E8-B48F-1D18A9856A87
last_name: Amberg
orcid: 0000-0002-3183-8207
- first_name: Alessandro
id: 41CB84B2-F248-11E8-B48F-1D18A9856A87
last_name: Venturino
orcid: 0000-0003-2356-9403
- first_name: Karl
last_name: Roessler
- first_name: Thomas
last_name: Czech
- first_name: Romana
last_name: Höftberger
- first_name: Sandra
id: 36ACD32E-F248-11E8-B48F-1D18A9856A87
last_name: Siegert
orcid: 0000-0001-8635-0877
- first_name: Gaia
id: 3E57A680-F248-11E8-B48F-1D18A9856A87
last_name: Novarino
orcid: 0000-0002-7673-7178
- first_name: Peter M
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name: Probing the Reversibility of Autism Spectrum Disorders by Employing in vivo
and in vitro Models
- _id: 25B7EB9E-B435-11E9-9278-68D0E5697425
call_identifier: H2020
grant_number: '692692'
name: Biophysics and circuit function of a giant cortical glumatergic synapse
- _id: 2564DBCA-B435-11E9-9278-68D0E5697425
call_identifier: H2020
grant_number: '665385'
name: International IST Doctoral Program
- _id: fc2be41b-9c52-11eb-aca3-faa90aa144e9
call_identifier: H2020
grant_number: '101026635'
name: Synaptic computations of the hippocampal CA3 circuitry
publisher: Institute of Science and Technology Austria
related_material:
link:
- description: 'Original data for Fig. 5d, Fig. 5d (N2V) and Fig. 5f-i, provided
via an external link due to the large size (>10GB) of the datasets. '
relation: research_data
url: https://pub.ista.ac.at/group_danzl/data/CATS/
record:
- id: '14257'
relation: used_in_publication
status: public
status: public
title: Research data for the publication "Imaging brain tissue architecture across
millimeter to nanometer scales"
tmp:
image: /images/cc_by_nc_sa.png
legal_code_url: https://creativecommons.org/licenses/by-nc-sa/4.0/legalcode
name: Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC
BY-NC-SA 4.0)
short: CC BY-NC-SA (4.0)
type: research_data
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
year: '2023'
...
---
_id: '14257'
abstract:
- lang: eng
text: Mapping the complex and dense arrangement of cells and their connectivity
in brain tissue demands nanoscale spatial resolution imaging. Super-resolution
optical microscopy excels at visualizing specific molecules and individual cells
but fails to provide tissue context. Here we developed Comprehensive Analysis
of Tissues across Scales (CATS), a technology to densely map brain tissue architecture
from millimeter regional to nanometer synaptic scales in diverse chemically fixed
brain preparations, including rodent and human. CATS uses fixation-compatible
extracellular labeling and optical imaging, including stimulated emission depletion
or expansion microscopy, to comprehensively delineate cellular structures. It
enables three-dimensional reconstruction of single synapses and mapping of synaptic
connectivity by identification and analysis of putative synaptic cleft regions.
Applying CATS to the mouse hippocampal mossy fiber circuitry, we reconstructed
and quantified the synaptic input and output structure of identified neurons.
We furthermore demonstrate applicability to clinically derived human tissue samples,
including formalin-fixed paraffin-embedded routine diagnostic specimens, for visualizing
the cellular architecture of brain tissue in health and disease.
acknowledged_ssus:
- _id: ScienComp
- _id: Bio
- _id: PreCl
- _id: LifeSc
- _id: M-Shop
- _id: E-Lib
acknowledgement: 'We thank J. Vorlaufer, N. Agudelo-Dueñas, W. Jahr and A. Wartak
for microscope maintenance and troubleshooting; C. Kreuzinger, A. Freeman and I.
Erber for technical assistance; and M. Tomschik for support with obtaining human
samples. We gratefully acknowledge E. Miguel for setting up webKnossos and M. Šuplata
for computational support and hardware control. We are grateful to R. Shigemoto
and B. Bickel for generous support and M. Sixt and S. Boyd (Stanford University)
for discussions and critical reading of the paper. PSD95-HaloTag mice were kindly
provided by S. Grant (University of Edinburgh). We acknowledge expert support by
Institute of Science and Technology Austria’s scientific computing, imaging and
optics, preclinical and lab support facilities and by the Miba machine shop and
library. We gratefully acknowledge funding by the following sources: Austrian Science
Fund (FWF) grant I3600-B27 (J.G.D.); Austrian Science Fund (FWF) grant DK W1232
(J.G.D. and J.M.M.); Austrian Science Fund (FWF) grant Z 312-B27, Wittgenstein award
(P.J.); Austrian Science Fund (FWF) projects I4685-B, I6565-B (SYNABS) and DOC 33-B27
(R.H.); Gesellschaft für Forschungsförderung NÖ (NFB) grant LSC18-022 (J.G.D.);
European Union’s Horizon 2020 research and innovation programme, European Research
Council (ERC) grant 715508 – REVERSEAUTISM (G.N.); European Union’s Horizon 2020
research and innovation programme, European Research Council (ERC) grant 692692
– GIANTSYN (P.J.); Marie Skłodowska-Curie Actions Fellowship GA no. 665385 under
the EU Horizon 2020 program (J.M.M. and J.L.); and Marie Skłodowska-Curie Actions
Individual Fellowship no. 101026635 under the EU Horizon 2020 program (J.F.W.).'
article_processing_charge: Yes (in subscription journal)
article_type: original
author:
- first_name: Julia M
full_name: Michalska, Julia M
id: 443DB6DE-F248-11E8-B48F-1D18A9856A87
last_name: Michalska
orcid: 0000-0003-3862-1235
- first_name: Julia
full_name: Lyudchik, Julia
id: 46E28B80-F248-11E8-B48F-1D18A9856A87
last_name: Lyudchik
- first_name: Philipp
full_name: Velicky, Philipp
id: 39BDC62C-F248-11E8-B48F-1D18A9856A87
last_name: Velicky
orcid: 0000-0002-2340-7431
- first_name: Hana
full_name: Korinkova, Hana
id: ee3cb6ca-ec98-11ea-ae11-ff703e2254ed
last_name: Korinkova
- first_name: Jake
full_name: Watson, Jake
id: 63836096-4690-11EA-BD4E-32803DDC885E
last_name: Watson
orcid: 0000-0002-8698-3823
- first_name: Alban
full_name: Cenameri, Alban
id: 9ac8f577-2357-11eb-997a-e566c5550886
last_name: Cenameri
- first_name: Christoph M
full_name: Sommer, Christoph M
id: 4DF26D8C-F248-11E8-B48F-1D18A9856A87
last_name: Sommer
orcid: 0000-0003-1216-9105
- first_name: Nicole
full_name: Amberg, Nicole
id: 4CD6AAC6-F248-11E8-B48F-1D18A9856A87
last_name: Amberg
orcid: 0000-0002-3183-8207
- first_name: Alessandro
full_name: Venturino, Alessandro
id: 41CB84B2-F248-11E8-B48F-1D18A9856A87
last_name: Venturino
orcid: 0000-0003-2356-9403
- first_name: Karl
full_name: Roessler, Karl
last_name: Roessler
- first_name: Thomas
full_name: Czech, Thomas
last_name: Czech
- first_name: Romana
full_name: Höftberger, Romana
last_name: Höftberger
- first_name: Sandra
full_name: Siegert, Sandra
id: 36ACD32E-F248-11E8-B48F-1D18A9856A87
last_name: Siegert
orcid: 0000-0001-8635-0877
- first_name: Gaia
full_name: Novarino, Gaia
id: 3E57A680-F248-11E8-B48F-1D18A9856A87
last_name: Novarino
orcid: 0000-0002-7673-7178
- first_name: Peter M
full_name: Jonas, Peter M
id: 353C1B58-F248-11E8-B48F-1D18A9856A87
last_name: Jonas
orcid: 0000-0001-5001-4804
- first_name: Johann G
full_name: Danzl, Johann G
id: 42EFD3B6-F248-11E8-B48F-1D18A9856A87
last_name: Danzl
orcid: 0000-0001-8559-3973
citation:
ama: Michalska JM, Lyudchik J, Velicky P, et al. Imaging brain tissue architecture
across millimeter to nanometer scales. Nature Biotechnology. 2023. doi:10.1038/s41587-023-01911-8
apa: Michalska, J. M., Lyudchik, J., Velicky, P., Korinkova, H., Watson, J., Cenameri,
A., … Danzl, J. G. (2023). Imaging brain tissue architecture across millimeter
to nanometer scales. Nature Biotechnology. Springer Nature. https://doi.org/10.1038/s41587-023-01911-8
chicago: Michalska, Julia M, Julia Lyudchik, Philipp Velicky, Hana Korinkova, Jake
Watson, Alban Cenameri, Christoph M Sommer, et al. “Imaging Brain Tissue Architecture
across Millimeter to Nanometer Scales.” Nature Biotechnology. Springer
Nature, 2023. https://doi.org/10.1038/s41587-023-01911-8.
ieee: J. M. Michalska et al., “Imaging brain tissue architecture across millimeter
to nanometer scales,” Nature Biotechnology. Springer Nature, 2023.
ista: Michalska JM, Lyudchik J, Velicky P, Korinkova H, Watson J, Cenameri A, Sommer
CM, Amberg N, Venturino A, Roessler K, Czech T, Höftberger R, Siegert S, Novarino
G, Jonas PM, Danzl JG. 2023. Imaging brain tissue architecture across millimeter
to nanometer scales. Nature Biotechnology.
mla: Michalska, Julia M., et al. “Imaging Brain Tissue Architecture across Millimeter
to Nanometer Scales.” Nature Biotechnology, Springer Nature, 2023, doi:10.1038/s41587-023-01911-8.
short: J.M. Michalska, J. Lyudchik, P. Velicky, H. Korinkova, J. Watson, A. Cenameri,
C.M. Sommer, N. Amberg, A. Venturino, K. Roessler, T. Czech, R. Höftberger, S.
Siegert, G. Novarino, P.M. Jonas, J.G. Danzl, Nature Biotechnology (2023).
date_created: 2023-09-03T22:01:15Z
date_published: 2023-08-31T00:00:00Z
date_updated: 2024-02-21T12:18:18Z
day: '31'
department:
- _id: SaSi
- _id: GaNo
- _id: PeJo
- _id: JoDa
- _id: Bio
- _id: RySh
doi: 10.1038/s41587-023-01911-8
ec_funded: 1
external_id:
isi:
- '001065254200001'
isi: 1
language:
- iso: eng
main_file_link:
- open_access: '1'
url: https://doi.org/10.1038/s41587-023-01911-8
month: '08'
oa: 1
oa_version: Published Version
project:
- _id: 265CB4D0-B435-11E9-9278-68D0E5697425
call_identifier: FWF
grant_number: I03600
name: Optical control of synaptic function via adhesion molecules
- _id: 2548AE96-B435-11E9-9278-68D0E5697425
call_identifier: FWF
grant_number: W1232-B24
name: Molecular Drug Targets
- _id: 25C5A090-B435-11E9-9278-68D0E5697425
call_identifier: FWF
grant_number: Z00312
name: The Wittgenstein Prize
- _id: 23889792-32DE-11EA-91FC-C7463DDC885E
name: High content imaging to decode human immune cell interactions in health and
allergic disease
- _id: 25444568-B435-11E9-9278-68D0E5697425
call_identifier: H2020
grant_number: '715508'
name: Probing the Reversibility of Autism Spectrum Disorders by Employing in vivo
and in vitro Models
- _id: 25B7EB9E-B435-11E9-9278-68D0E5697425
call_identifier: H2020
grant_number: '692692'
name: Biophysics and circuit function of a giant cortical glumatergic synapse
- _id: 2564DBCA-B435-11E9-9278-68D0E5697425
call_identifier: H2020
grant_number: '665385'
name: International IST Doctoral Program
- _id: fc2be41b-9c52-11eb-aca3-faa90aa144e9
call_identifier: H2020
grant_number: '101026635'
name: Synaptic computations of the hippocampal CA3 circuitry
publication: Nature Biotechnology
publication_identifier:
eissn:
- 1546-1696
issn:
- 1087-0156
publication_status: epub_ahead
publisher: Springer Nature
quality_controlled: '1'
related_material:
link:
- relation: software
url: https://github.com/danzllab/CATS
record:
- id: '13126'
relation: research_data
status: public
scopus_import: '1'
status: public
title: Imaging brain tissue architecture across millimeter to nanometer scales
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
year: '2023'
...
---
_id: '13173'
abstract:
- lang: eng
text: GABAB receptor (GBR) activation inhibits neurotransmitter release in axon
terminals in the brain, except in medial habenula (MHb) terminals, which show
robust potentiation. However, mechanisms underlying this enigmatic potentiation
remain elusive. Here, we report that GBR activation on MHb terminals induces an
activity-dependent transition from a facilitating, tonic to a depressing, phasic
neurotransmitter release mode. This transition is accompanied by a 4.1-fold increase
in readily releasable vesicle pool (RRP) size and a 3.5-fold increase of docked
synaptic vesicles at the presynaptic active zone (AZ). Strikingly, tonic and phasic
release exhibit distinct coupling distances and are selectively affected by deletion
of synaptoporin (SPO) and Ca2+-dependent activator protein for secretion 2 (CAPS2),
respectively. SPO modulates augmentation, the short-term plasticity associated
with tonic release, and CAPS2 retains the increased RRP for initial responses
in phasic response trains. Double pre-embedding immunolabeling confirmed the co-localization
of CAPS2 and SPO inside the same terminal. The cytosolic protein CAPS2 showed
a synaptic vesicle (SV)-associated distribution similar to the vesicular transmembrane
protein SPO. A newly developed “Flash and Freeze-fracture” method revealed the
release of SPO-associated vesicles in both tonic and phasic modes and activity-dependent
recruitment of CAPS2 to the AZ during phasic release, which lasted several minutes.
Overall, these results indicate that GBR activation translocates CAPS2 to the
AZ along with the fusion of CAPS2-associated SVs, contributing to a persistent
RRP increase. Thus, we discovered structural and molecular mechanisms underlying
tonic and phasic neurotransmitter release and their transition by GBR activation
in MHb terminals.
article_processing_charge: No
author:
- first_name: Ryuichi
full_name: Shigemoto, Ryuichi
id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
last_name: Shigemoto
orcid: 0000-0001-8761-9444
citation:
ama: Shigemoto R. Transition from tonic to phasic neurotransmitter release by presynaptic
GABAB receptor activation in medial habenula terminals. 2023. doi:10.15479/AT:ISTA:13173
apa: Shigemoto, R. (2023). Transition from tonic to phasic neurotransmitter release
by presynaptic GABAB receptor activation in medial habenula terminals. Institute
of Science and Technology Austria. https://doi.org/10.15479/AT:ISTA:13173
chicago: Shigemoto, Ryuichi. “Transition from Tonic to Phasic Neurotransmitter Release
by Presynaptic GABAB Receptor Activation in Medial Habenula Terminals.” Institute
of Science and Technology Austria, 2023. https://doi.org/10.15479/AT:ISTA:13173.
ieee: R. Shigemoto, “Transition from tonic to phasic neurotransmitter release by
presynaptic GABAB receptor activation in medial habenula terminals.” Institute
of Science and Technology Austria, 2023.
ista: Shigemoto R. 2023. Transition from tonic to phasic neurotransmitter release
by presynaptic GABAB receptor activation in medial habenula terminals, Institute
of Science and Technology Austria, 10.15479/AT:ISTA:13173.
mla: Shigemoto, Ryuichi. Transition from Tonic to Phasic Neurotransmitter Release
by Presynaptic GABAB Receptor Activation in Medial Habenula Terminals. Institute
of Science and Technology Austria, 2023, doi:10.15479/AT:ISTA:13173.
short: R. Shigemoto, (2023).
date_created: 2023-06-29T13:16:42Z
date_published: 2023-07-29T00:00:00Z
date_updated: 2024-03-12T13:44:18Z
day: '29'
ddc:
- '571'
department:
- _id: RySh
doi: 10.15479/AT:ISTA:13173
file:
- access_level: closed
checksum: ed59170869ba621f89f7c1894092192f
content_type: application/x-zip-compressed
creator: shigemot
date_created: 2023-06-29T13:11:22Z
date_updated: 2023-11-17T14:30:44Z
description: After review an updated version of the data is provided
file_id: '13174'
file_name: Raw data for Koppensteiner et al.zip
file_size: 542873672
relation: main_file
title: Outdated Version
- access_level: open_access
checksum: c07860eb82b4d367245f1b589fe5c250
content_type: application/vnd.openxmlformats-officedocument.spreadsheetml.sheet
creator: patrickd
date_created: 2023-11-17T14:13:02Z
date_updated: 2023-11-17T14:13:02Z
file_id: '14550'
file_name: 11-17-23 Updated Koppensteiner et al. raw data.xlsx
file_size: 915079
relation: main_file
success: 1
- access_level: open_access
checksum: abf84b1699edac4349dc3a92d466fb7b
content_type: application/x-zip-compressed
creator: dernst
date_created: 2024-02-06T07:21:43Z
date_updated: 2024-02-06T07:21:43Z
file_id: '14942'
file_name: EM_Images.zip
file_size: 544868924
relation: main_file
success: 1
file_date_updated: 2024-02-06T07:21:43Z
has_accepted_license: '1'
keyword:
- medial habenula
- GABAB receptor
- vesicle release
- Flash and Freeze
- Flash and Freeze-fracture
month: '07'
oa: 1
oa_version: Published Version
publisher: Institute of Science and Technology Austria
related_material:
record:
- id: '15084'
relation: used_in_publication
status: public
status: public
title: Transition from tonic to phasic neurotransmitter release by presynaptic GABAB
receptor activation in medial habenula terminals
tmp:
image: /images/cc_by_nc.png
legal_code_url: https://creativecommons.org/licenses/by-nc/4.0/legalcode
name: Creative Commons Attribution-NonCommercial 4.0 International (CC BY-NC 4.0)
short: CC BY-NC (4.0)
type: research_data
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
year: '2023'
...
---
_id: '10890'
abstract:
- lang: eng
text: Upon the arrival of action potentials at nerve terminals, neurotransmitters
are released from synaptic vesicles (SVs) by exocytosis. CaV2.1, 2.2, and 2.3
are the major subunits of the voltage-gated calcium channel (VGCC) responsible
for increasing intraterminal calcium levels and triggering SV exocytosis in the
central nervous system (CNS) synapses. The two-dimensional analysis of CaV2 distributions
using sodium dodecyl sulfate (SDS)-digested freeze-fracture replica labeling (SDS-FRL)
has revealed their numbers, densities, and nanoscale clustering patterns in individual
presynaptic active zones. The variation in these properties affects the coupling
of VGCCs with calcium sensors on SVs, synaptic efficacy, and temporal precision
of transmission. In this study, we summarize how the morphological parameters
of CaV2 distribution obtained using SDS-FRL differ depending on the different
types of synapses and could correspond to functional properties in synaptic transmission.
acknowledgement: "This work was supported by the European Research Council advanced
grant No. 694539 and the joint German-Austrian DFG and FWF project SYNABS (FWF:
I-4638-B) to RS.\r\nThe authors thank Walter Kaufmann for his critical comments
on the manuscript."
article_number: '846615'
article_processing_charge: No
article_type: original
author:
- first_name: Kohgaku
full_name: Eguchi, Kohgaku
id: 2B7846DC-F248-11E8-B48F-1D18A9856A87
last_name: Eguchi
orcid: 0000-0002-6170-2546
- first_name: Jacqueline-Claire
full_name: Montanaro-Punzengruber, Jacqueline-Claire
id: 3786AB44-F248-11E8-B48F-1D18A9856A87
last_name: Montanaro-Punzengruber
- first_name: Elodie
full_name: Le Monnier, Elodie
id: 3B59276A-F248-11E8-B48F-1D18A9856A87
last_name: Le Monnier
- first_name: Ryuichi
full_name: Shigemoto, Ryuichi
id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
last_name: Shigemoto
orcid: 0000-0001-8761-9444
citation:
ama: Eguchi K, Montanaro-Punzengruber J-C, Le Monnier E, Shigemoto R. The number
and distinct clustering patterns of voltage-gated Calcium channels in nerve terminals.
Frontiers in Neuroanatomy. 2022;16. doi:10.3389/fnana.2022.846615
apa: Eguchi, K., Montanaro-Punzengruber, J.-C., Le Monnier, E., & Shigemoto,
R. (2022). The number and distinct clustering patterns of voltage-gated Calcium
channels in nerve terminals. Frontiers in Neuroanatomy. Frontiers. https://doi.org/10.3389/fnana.2022.846615
chicago: Eguchi, Kohgaku, Jacqueline-Claire Montanaro-Punzengruber, Elodie Le Monnier,
and Ryuichi Shigemoto. “The Number and Distinct Clustering Patterns of Voltage-Gated
Calcium Channels in Nerve Terminals.” Frontiers in Neuroanatomy. Frontiers,
2022. https://doi.org/10.3389/fnana.2022.846615.
ieee: K. Eguchi, J.-C. Montanaro-Punzengruber, E. Le Monnier, and R. Shigemoto,
“The number and distinct clustering patterns of voltage-gated Calcium channels
in nerve terminals,” Frontiers in Neuroanatomy, vol. 16. Frontiers, 2022.
ista: Eguchi K, Montanaro-Punzengruber J-C, Le Monnier E, Shigemoto R. 2022. The
number and distinct clustering patterns of voltage-gated Calcium channels in nerve
terminals. Frontiers in Neuroanatomy. 16, 846615.
mla: Eguchi, Kohgaku, et al. “The Number and Distinct Clustering Patterns of Voltage-Gated
Calcium Channels in Nerve Terminals.” Frontiers in Neuroanatomy, vol. 16,
846615, Frontiers, 2022, doi:10.3389/fnana.2022.846615.
short: K. Eguchi, J.-C. Montanaro-Punzengruber, E. Le Monnier, R. Shigemoto, Frontiers
in Neuroanatomy 16 (2022).
date_created: 2022-03-20T23:01:39Z
date_published: 2022-02-24T00:00:00Z
date_updated: 2023-08-03T06:07:18Z
day: '24'
ddc:
- '570'
department:
- _id: RySh
doi: 10.3389/fnana.2022.846615
ec_funded: 1
external_id:
isi:
- '000766662700001'
pmid:
- '35280978'
file:
- access_level: open_access
checksum: 51ec9b90e7da919e22c01a15489eaacd
content_type: application/pdf
creator: dernst
date_created: 2022-03-21T09:41:19Z
date_updated: 2022-03-21T09:41:19Z
file_id: '10911'
file_name: 2022_FrontiersNeuroanatomy_Eguchi.pdf
file_size: 2416395
relation: main_file
success: 1
file_date_updated: 2022-03-21T09:41:19Z
has_accepted_license: '1'
intvolume: ' 16'
isi: 1
language:
- iso: eng
month: '02'
oa: 1
oa_version: Published Version
pmid: 1
project:
- _id: 25CA28EA-B435-11E9-9278-68D0E5697425
call_identifier: H2020
grant_number: '694539'
name: 'In situ analysis of single channel subunit composition in neurons: physiological
implication in synaptic plasticity and behaviour'
- _id: 05970B30-7A3F-11EA-A408-12923DDC885E
grant_number: I04638
name: LGI1 antibody-induced pathophysiology in synapses
publication: Frontiers in Neuroanatomy
publication_identifier:
eissn:
- '16625129'
publication_status: published
publisher: Frontiers
quality_controlled: '1'
scopus_import: '1'
status: public
title: The number and distinct clustering patterns of voltage-gated Calcium channels
in nerve terminals
tmp:
image: /images/cc_by.png
legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
short: CC BY (4.0)
type: journal_article
user_id: 4359f0d1-fa6c-11eb-b949-802e58b17ae8
volume: 16
year: '2022'
...
---
_id: '10889'
abstract:
- lang: eng
text: Genetically encoded tags have introduced extensive lines of application from
purification of tagged proteins to their visualization at the single molecular,
cellular, histological and whole-body levels. Combined with other rapidly developing
technologies such as clustered regularly interspaced palindromic repeats (CRISPR)/CRISPR-associated
protein 9 (Cas9) system, proteomics, super-resolution microscopy and proximity
labeling, a large variety of genetically encoded tags have been developed in the
last two decades. In this review, I focus on the current status of tag development
for electron microscopic (EM) visualization of proteins with metal particle labeling.
Compared with conventional immunoelectron microscopy using gold particles, tag-mediated
metal particle labeling has several advantages that could potentially improve
the sensitivity, spatial and temporal resolution, and applicability to a wide
range of proteins of interest (POIs). It may enable researchers to detect single
molecules in situ, allowing the quantitative measurement of absolute numbers and
exact localization patterns of POI in the ultrastructural context. Thus, genetically
encoded tags for EM could revolutionize the field as green fluorescence protein
did for light microscopy, although we still have many challenges to overcome before
reaching this goal.
acknowledgement: European Research Council Advanced Grant (694539 to R.S.).
article_processing_charge: No
article_type: original
author:
- first_name: Ryuichi
full_name: Shigemoto, Ryuichi
id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
last_name: Shigemoto
orcid: 0000-0001-8761-9444
citation:
ama: Shigemoto R. Electron microscopic visualization of single molecules by tag-mediated
metal particle labeling. Microscopy. 2022;71(Supplement_1):i72-i80. doi:10.1093/jmicro/dfab048
apa: Shigemoto, R. (2022). Electron microscopic visualization of single molecules
by tag-mediated metal particle labeling. Microscopy. Oxford Academic. https://doi.org/10.1093/jmicro/dfab048
chicago: Shigemoto, Ryuichi. “Electron Microscopic Visualization of Single Molecules
by Tag-Mediated Metal Particle Labeling.” Microscopy. Oxford Academic,
2022. https://doi.org/10.1093/jmicro/dfab048.
ieee: R. Shigemoto, “Electron microscopic visualization of single molecules by tag-mediated
metal particle labeling,” Microscopy, vol. 71, no. Supplement_1. Oxford
Academic, pp. i72–i80, 2022.
ista: Shigemoto R. 2022. Electron microscopic visualization of single molecules
by tag-mediated metal particle labeling. Microscopy. 71(Supplement_1), i72–i80.
mla: Shigemoto, Ryuichi. “Electron Microscopic Visualization of Single Molecules
by Tag-Mediated Metal Particle Labeling.” Microscopy, vol. 71, no. Supplement_1,
Oxford Academic, 2022, pp. i72–80, doi:10.1093/jmicro/dfab048.
short: R. Shigemoto, Microscopy 71 (2022) i72–i80.
date_created: 2022-03-20T23:01:39Z
date_published: 2022-03-01T00:00:00Z
date_updated: 2023-08-03T06:08:01Z
day: '01'
department:
- _id: RySh
doi: 10.1093/jmicro/dfab048
ec_funded: 1
external_id:
isi:
- '000768384100011'
pmid:
- '35275179'
intvolume: ' 71'
isi: 1
issue: Supplement_1
language:
- iso: eng
main_file_link:
- open_access: '1'
url: https://doi.org/10.1093/jmicro/dfab048
month: '03'
oa: 1
oa_version: Published Version
page: i72-i80
pmid: 1
project:
- _id: 25CA28EA-B435-11E9-9278-68D0E5697425
call_identifier: H2020
grant_number: '694539'
name: 'In situ analysis of single channel subunit composition in neurons: physiological
implication in synaptic plasticity and behaviour'
publication: Microscopy
publication_identifier:
eissn:
- 2050-5701
issn:
- 2050-5698
publication_status: published
publisher: Oxford Academic
quality_controlled: '1'
scopus_import: '1'
status: public
title: Electron microscopic visualization of single molecules by tag-mediated metal
particle labeling
type: journal_article
user_id: 4359f0d1-fa6c-11eb-b949-802e58b17ae8
volume: 71
year: '2022'
...
---
_id: '11419'
abstract:
- lang: eng
text: Elevation of soluble wild-type (WT) tau occurs in synaptic compartments in
Alzheimer’s disease. We addressed whether tau elevation affects synaptic transmission
at the calyx of Held in slices from mice brainstem. Whole-cell loading of WT human
tau (h-tau) in presynaptic terminals at 10–20 µM caused microtubule (MT) assembly
and activity-dependent rundown of excitatory neurotransmission. Capacitance measurements
revealed that the primary target of WT h-tau is vesicle endocytosis. Blocking
MT assembly using nocodazole prevented tau-induced impairments of endocytosis
and neurotransmission. Immunofluorescence imaging analyses revealed that MT assembly
by WT h-tau loading was associated with an increased MT-bound fraction of the
endocytic protein dynamin. A synthetic dodecapeptide corresponding to dynamin
1-pleckstrin-homology domain inhibited MT-dynamin interaction and rescued tau-induced
impairments of endocytosis and neurotransmission. We conclude that elevation of
presynaptic WT tau induces de novo assembly of MTs, thereby sequestering free
dynamins. As a result, endocytosis and subsequent vesicle replenishment are impaired,
causing activity-dependent rundown of neurotransmission.
acknowledgement: We thank Yasuo Ihara, Nobuyuki Nukina, and Takeshi Sakaba for comments
and Patrick Stoney for editing this paper. We also thank Shota Okuda and Mikako
Matsubara for their contributions in the early stage of this study, and Satoko Wada-Kakuda
for technical assistant with in vitro analysis of tau. This research was supported
by funding from Okinawa Institute of Science and Technology and from Technology
(OIST) and Core Research for the Evolutional Science and Technology of Japan Science
and Technology Agency (CREST) to TT, and by Scientific Research on Innovative Areas
to TM (Brain Protein Aging and Dementia Control 26117004).
article_number: e73542
article_processing_charge: No
article_type: original
author:
- first_name: Tetsuya
full_name: Hori, Tetsuya
last_name: Hori
- first_name: Kohgaku
full_name: Eguchi, Kohgaku
id: 2B7846DC-F248-11E8-B48F-1D18A9856A87
last_name: Eguchi
orcid: 0000-0002-6170-2546
- first_name: Han Ying
full_name: Wang, Han Ying
last_name: Wang
- first_name: Tomohiro
full_name: Miyasaka, Tomohiro
last_name: Miyasaka
- first_name: Laurent
full_name: Guillaud, Laurent
last_name: Guillaud
- first_name: Zacharie
full_name: Taoufiq, Zacharie
last_name: Taoufiq
- first_name: Satyajit
full_name: Mahapatra, Satyajit
last_name: Mahapatra
- first_name: Hiroshi
full_name: Yamada, Hiroshi
last_name: Yamada
- first_name: Kohji
full_name: Takei, Kohji
last_name: Takei
- first_name: Tomoyuki
full_name: Takahashi, Tomoyuki
last_name: Takahashi
citation:
ama: Hori T, Eguchi K, Wang HY, et al. Microtubule assembly by tau impairs endocytosis
and neurotransmission via dynamin sequestration in Alzheimer’s disease synapse
model. eLife. 2022;11. doi:10.7554/eLife.73542
apa: Hori, T., Eguchi, K., Wang, H. Y., Miyasaka, T., Guillaud, L., Taoufiq, Z.,
… Takahashi, T. (2022). Microtubule assembly by tau impairs endocytosis and neurotransmission
via dynamin sequestration in Alzheimer’s disease synapse model. ELife.
eLife Sciences Publications. https://doi.org/10.7554/eLife.73542
chicago: Hori, Tetsuya, Kohgaku Eguchi, Han Ying Wang, Tomohiro Miyasaka, Laurent
Guillaud, Zacharie Taoufiq, Satyajit Mahapatra, Hiroshi Yamada, Kohji Takei, and
Tomoyuki Takahashi. “Microtubule Assembly by Tau Impairs Endocytosis and Neurotransmission
via Dynamin Sequestration in Alzheimer’s Disease Synapse Model.” ELife.
eLife Sciences Publications, 2022. https://doi.org/10.7554/eLife.73542.
ieee: T. Hori et al., “Microtubule assembly by tau impairs endocytosis and
neurotransmission via dynamin sequestration in Alzheimer’s disease synapse model,”
eLife, vol. 11. eLife Sciences Publications, 2022.
ista: Hori T, Eguchi K, Wang HY, Miyasaka T, Guillaud L, Taoufiq Z, Mahapatra S,
Yamada H, Takei K, Takahashi T. 2022. Microtubule assembly by tau impairs endocytosis
and neurotransmission via dynamin sequestration in Alzheimer’s disease synapse
model. eLife. 11, e73542.
mla: Hori, Tetsuya, et al. “Microtubule Assembly by Tau Impairs Endocytosis and
Neurotransmission via Dynamin Sequestration in Alzheimer’s Disease Synapse Model.”
ELife, vol. 11, e73542, eLife Sciences Publications, 2022, doi:10.7554/eLife.73542.
short: T. Hori, K. Eguchi, H.Y. Wang, T. Miyasaka, L. Guillaud, Z. Taoufiq, S. Mahapatra,
H. Yamada, K. Takei, T. Takahashi, ELife 11 (2022).
date_created: 2022-05-29T22:01:54Z
date_published: 2022-05-05T00:00:00Z
date_updated: 2023-08-03T07:15:49Z
day: '05'
ddc:
- '616'
department:
- _id: RySh
doi: 10.7554/eLife.73542
external_id:
isi:
- '000876231600001'
pmid:
- '35471147 '
file:
- access_level: open_access
checksum: ccddbd167e00ff8375f12998af497152
content_type: application/pdf
creator: cchlebak
date_created: 2022-05-30T08:09:16Z
date_updated: 2022-05-30T08:09:16Z
file_id: '11421'
file_name: elife-73542-v2.pdf
file_size: 2466296
relation: main_file
success: 1
file_date_updated: 2022-05-30T08:09:16Z
has_accepted_license: '1'
intvolume: ' 11'
isi: 1
language:
- iso: eng
month: '05'
oa: 1
oa_version: Published Version
pmid: 1
publication: eLife
publication_identifier:
eissn:
- 2050-084X
publication_status: published
publisher: eLife Sciences Publications
quality_controlled: '1'
scopus_import: '1'
status: public
title: Microtubule assembly by tau impairs endocytosis and neurotransmission via dynamin
sequestration in Alzheimer's disease synapse model
tmp:
image: /images/cc_by.png
legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
short: CC BY (4.0)
type: journal_article
user_id: 4359f0d1-fa6c-11eb-b949-802e58b17ae8
volume: 11
year: '2022'
...
---
_id: '12212'
abstract:
- lang: eng
text: Alzheimer’s disease (AD) is characterized by a reorganization of brain activity
determining network hyperexcitability and loss of synaptic plasticity. Precisely,
a dysfunction in metabotropic GABAB receptor signalling through G protein-gated
inwardly rectifying K+ (GIRK or Kir3) channels on the hippocampus has been postulated.
Thus, we determined the impact of amyloid-β (Aβ) pathology in GIRK channel density,
subcellular distribution, and its association with GABAB receptors in hippocampal
CA1 pyramidal neurons from the APP/PS1 mouse model using quantitative SDS-digested
freeze-fracture replica labelling (SDS-FRL) and proximity ligation in situ assay
(P-LISA). In wild type mice, single SDS-FRL detection revealed a similar dendritic
gradient for GIRK1 and GIRK2 in CA1 pyramidal cells, with higher densities in
spines, and GIRK3 showed a lower and uniform distribution. Double SDS-FRL showed
a co-clustering of GIRK2 and GIRK1 in post- and presynaptic compartments, but
not for GIRK2 and GIRK3. Likewise, double GABAB1 and GIRK2 SDS-FRL detection displayed
a high degree of co-clustering in nanodomains (40–50 nm) mostly in spines and
axon terminals. In APP/PS1 mice, the density of GIRK2 and GIRK1, but not for GIRK3,
was significantly reduced along the neuronal surface of CA1 pyramidal cells and
in axon terminals contacting them. Importantly, GABAB1 and GIRK2 co-clustering
was not present in APP/PS1 mice. Similarly, P-LISA experiments revealed a significant
reduction in GABAB1 and GIRK2 interaction on the hippocampus of this animal model.
Overall, our results provide compelling evidence showing a significant reduction
on the cell surface density of pre- and postsynaptic GIRK1 and GIRK2, but not
GIRK3, and a decline in GABAB receptors and GIRK2 channels co-clustering in hippocampal
pyramidal neurons from APP/PS1 mice, thus suggesting that a disruption in the
GABAB receptor–GIRK channel membrane assembly causes dysregulation in the GABAB
signalling via GIRK channels in this AD animal model.
acknowledgement: "We thank Ms. Diane Latawiec for the English revision of the manuscript.
Funding sources were the Spanish Ministerio de Economía y Competitividad, Junta
de Comunidades de Castilla-La Mancha (Spain), and Life Science Innovation Center
at University of Fukui. We thank Centres de Recerca de Catalunya (CERCA) Programme/Generalitat
de Catalunya for IDIBELL institutional support. We thank Hitoshi Takagi and Takako
Maegawa at the University of Fukui for their technical assistance on SDS-FRL experiments.\r\nThis
work was supported by grants from the Spanish Ministerio de Economía y Competitividad
(BFU2015-63769-R, RTI2018-095812-B-I00, and PID2021-125875OB-I00) and Junta de Comunidades
de Castilla-La Mancha (SBPLY/17/180501/000229 and SBPLY/21/180501/000064) to RL,
Life Science Innovation Center at University of Fukui and JSPS KAKENHI (Grant Numbers
16H04662, 19H03323, and 20H05058) to YF, and Margarita Salas fellowship from Ministerio
de Universidades and Universidad de Castilla-La Mancha to AMB."
article_number: '136'
article_processing_charge: No
article_type: original
author:
- first_name: Alejandro
full_name: Martín-Belmonte, Alejandro
last_name: Martín-Belmonte
- first_name: Carolina
full_name: Aguado, Carolina
last_name: Aguado
- first_name: Rocío
full_name: Alfaro-Ruiz, Rocío
last_name: Alfaro-Ruiz
- first_name: Ana Esther
full_name: Moreno-Martínez, Ana Esther
last_name: Moreno-Martínez
- first_name: Luis
full_name: de la Ossa, Luis
last_name: de la Ossa
- first_name: Ester
full_name: Aso, Ester
last_name: Aso
- first_name: Laura
full_name: Gómez-Acero, Laura
last_name: Gómez-Acero
- first_name: Ryuichi
full_name: Shigemoto, Ryuichi
id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
last_name: Shigemoto
orcid: 0000-0001-8761-9444
- first_name: Yugo
full_name: Fukazawa, Yugo
last_name: Fukazawa
- first_name: Francisco
full_name: Ciruela, Francisco
last_name: Ciruela
- first_name: Rafael
full_name: Luján, Rafael
last_name: Luján
citation:
ama: Martín-Belmonte A, Aguado C, Alfaro-Ruiz R, et al. Nanoscale alterations in
GABAB receptors and GIRK channel organization on the hippocampus of APP/PS1 mice.
Alzheimer’s Research & Therapy. 2022;14. doi:10.1186/s13195-022-01078-5
apa: Martín-Belmonte, A., Aguado, C., Alfaro-Ruiz, R., Moreno-Martínez, A. E., de
la Ossa, L., Aso, E., … Luján, R. (2022). Nanoscale alterations in GABAB receptors
and GIRK channel organization on the hippocampus of APP/PS1 mice. Alzheimer’s
Research & Therapy. Springer Nature. https://doi.org/10.1186/s13195-022-01078-5
chicago: Martín-Belmonte, Alejandro, Carolina Aguado, Rocío Alfaro-Ruiz, Ana Esther
Moreno-Martínez, Luis de la Ossa, Ester Aso, Laura Gómez-Acero, et al. “Nanoscale
Alterations in GABAB Receptors and GIRK Channel Organization on the Hippocampus
of APP/PS1 Mice.” Alzheimer’s Research & Therapy. Springer Nature,
2022. https://doi.org/10.1186/s13195-022-01078-5.
ieee: A. Martín-Belmonte et al., “Nanoscale alterations in GABAB receptors
and GIRK channel organization on the hippocampus of APP/PS1 mice,” Alzheimer’s
Research & Therapy, vol. 14. Springer Nature, 2022.
ista: Martín-Belmonte A, Aguado C, Alfaro-Ruiz R, Moreno-Martínez AE, de la Ossa
L, Aso E, Gómez-Acero L, Shigemoto R, Fukazawa Y, Ciruela F, Luján R. 2022. Nanoscale
alterations in GABAB receptors and GIRK channel organization on the hippocampus
of APP/PS1 mice. Alzheimer’s Research & Therapy. 14, 136.
mla: Martín-Belmonte, Alejandro, et al. “Nanoscale Alterations in GABAB Receptors
and GIRK Channel Organization on the Hippocampus of APP/PS1 Mice.” Alzheimer’s
Research & Therapy, vol. 14, 136, Springer Nature, 2022, doi:10.1186/s13195-022-01078-5.
short: A. Martín-Belmonte, C. Aguado, R. Alfaro-Ruiz, A.E. Moreno-Martínez, L. de
la Ossa, E. Aso, L. Gómez-Acero, R. Shigemoto, Y. Fukazawa, F. Ciruela, R. Luján,
Alzheimer’s Research & Therapy 14 (2022).
date_created: 2023-01-16T09:45:51Z
date_published: 2022-09-21T00:00:00Z
date_updated: 2023-08-04T09:23:10Z
day: '21'
ddc:
- '570'
department:
- _id: RySh
doi: 10.1186/s13195-022-01078-5
external_id:
isi:
- '000857985500001'
file:
- access_level: open_access
checksum: 88e49715ad6a1abf0fdb27efd65368dc
content_type: application/pdf
creator: dernst
date_created: 2023-01-27T07:53:18Z
date_updated: 2023-01-27T07:53:18Z
file_id: '12413'
file_name: 2022_AlzheimersResearch_MartinBelmont.pdf
file_size: 11013325
relation: main_file
success: 1
file_date_updated: 2023-01-27T07:53:18Z
has_accepted_license: '1'
intvolume: ' 14'
isi: 1
keyword:
- Cognitive Neuroscience
- Neurology (clinical)
- Neurology
language:
- iso: eng
month: '09'
oa: 1
oa_version: Published Version
publication: Alzheimer's Research & Therapy
publication_identifier:
issn:
- 1758-9193
publication_status: published
publisher: Springer Nature
quality_controlled: '1'
scopus_import: '1'
status: public
title: Nanoscale alterations in GABAB receptors and GIRK channel organization on the
hippocampus of APP/PS1 mice
tmp:
image: /images/cc_by.png
legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
short: CC BY (4.0)
type: journal_article
user_id: 4359f0d1-fa6c-11eb-b949-802e58b17ae8
volume: 14
year: '2022'
...
---
_id: '11333'
abstract:
- lang: eng
text: Adenosine triphosphate (ATP) is the energy source for various biochemical
processes and biomolecular motors in living things. Development of ATP antagonists
and their stimuli-controlled actions offer a novel approach to regulate biological
processes. Herein, we developed azobenzene-based photoswitchable ATP antagonists
for controlling the activity of motor proteins; cytoplasmic and axonemal dyneins.
The new ATP antagonists showed reversible photoswitching of cytoplasmic dynein
activity in an in vitro dynein-microtubule system due to the trans and cis photoisomerization
of their azobenzene segment. Importantly, our ATP antagonists reversibly regulated
the axonemal dynein motor activity for the force generation in a demembranated
model of Chlamydomonas reinhardtii. We found that the trans and cis isomers of
ATP antagonists significantly differ in their affinity to the ATP binding site.
article_number: e202200807
article_processing_charge: No
article_type: original
author:
- first_name: Sampreeth
full_name: Thayyil, Sampreeth
last_name: Thayyil
- first_name: Yukinori
full_name: Nishigami, Yukinori
last_name: Nishigami
- first_name: Muhammad J
full_name: Islam, Muhammad J
id: C94881D2-008F-11EA-8E08-2637E6697425
last_name: Islam
- first_name: P. K.
full_name: Hashim, P. K.
last_name: Hashim
- first_name: Ken'Ya
full_name: Furuta, Ken'Ya
last_name: Furuta
- first_name: Kazuhiro
full_name: Oiwa, Kazuhiro
last_name: Oiwa
- first_name: Jian
full_name: Yu, Jian
last_name: Yu
- first_name: Min
full_name: Yao, Min
last_name: Yao
- first_name: Toshiyuki
full_name: Nakagaki, Toshiyuki
last_name: Nakagaki
- first_name: Nobuyuki
full_name: Tamaoki, Nobuyuki
last_name: Tamaoki
citation:
ama: Thayyil S, Nishigami Y, Islam MJ, et al. Dynamic control of microbial movement
by photoswitchable ATP antagonists. Chemistry - A European Journal. 2022;28(30).
doi:10.1002/chem.202200807
apa: Thayyil, S., Nishigami, Y., Islam, M. J., Hashim, P. K., Furuta, K., Oiwa,
K., … Tamaoki, N. (2022). Dynamic control of microbial movement by photoswitchable
ATP antagonists. Chemistry - A European Journal. Wiley. https://doi.org/10.1002/chem.202200807
chicago: Thayyil, Sampreeth, Yukinori Nishigami, Muhammad J Islam, P. K. Hashim,
Ken’Ya Furuta, Kazuhiro Oiwa, Jian Yu, Min Yao, Toshiyuki Nakagaki, and Nobuyuki
Tamaoki. “Dynamic Control of Microbial Movement by Photoswitchable ATP Antagonists.”
Chemistry - A European Journal. Wiley, 2022. https://doi.org/10.1002/chem.202200807.
ieee: S. Thayyil et al., “Dynamic control of microbial movement by photoswitchable
ATP antagonists,” Chemistry - A European Journal, vol. 28, no. 30. Wiley,
2022.
ista: Thayyil S, Nishigami Y, Islam MJ, Hashim PK, Furuta K, Oiwa K, Yu J, Yao M,
Nakagaki T, Tamaoki N. 2022. Dynamic control of microbial movement by photoswitchable
ATP antagonists. Chemistry - A European Journal. 28(30), e202200807.
mla: Thayyil, Sampreeth, et al. “Dynamic Control of Microbial Movement by Photoswitchable
ATP Antagonists.” Chemistry - A European Journal, vol. 28, no. 30, e202200807,
Wiley, 2022, doi:10.1002/chem.202200807.
short: S. Thayyil, Y. Nishigami, M.J. Islam, P.K. Hashim, K. Furuta, K. Oiwa, J.
Yu, M. Yao, T. Nakagaki, N. Tamaoki, Chemistry - A European Journal 28 (2022).
date_created: 2022-04-24T22:01:44Z
date_published: 2022-05-25T00:00:00Z
date_updated: 2023-10-03T10:58:31Z
day: '25'
department:
- _id: RySh
doi: 10.1002/chem.202200807
external_id:
isi:
- '000781658800001'
pmid:
- '35332959'
intvolume: ' 28'
isi: 1
issue: '30'
language:
- iso: eng
main_file_link:
- open_access: '1'
url: https://doi.org/10.1002/chem.202200807
month: '05'
oa: 1
oa_version: Published Version
pmid: 1
publication: Chemistry - A European Journal
publication_identifier:
eissn:
- '15213765'
issn:
- '09476539'
publication_status: published
publisher: Wiley
quality_controlled: '1'
scopus_import: '1'
status: public
title: Dynamic control of microbial movement by photoswitchable ATP antagonists
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 28
year: '2022'
...
---
_id: '11393'
abstract:
- lang: eng
text: "AMPA receptors (AMPARs) mediate fast excitatory neurotransmission and their
role is\r\nimplicated in complex processes such as learning and memory and various
neurological\r\ndiseases. These receptors are composed of different subunits and
the subunit composition can\r\naffect channel properties, receptor trafficking
and interaction with other associated proteins.\r\nUsing the high sensitivity
SDS-digested freeze-fracture replica labeling (SDS-FRL) for\r\nelectron microscopy
I investigated the number, density, and localization of AMPAR subunits,\r\nGluA1,
GluA2, GluA3, and GluA1-3 (panAMPA) in pyramidal cells in the CA1 area of mouse\r\nhippocampus.
I have found that the immunogold labeling for all of these subunits in the\r\npostsynaptic
sites was highest in stratum radiatum and lowest in stratum lacunosummoleculare.
The labeling density for the all subunits in the extrasynaptic sites showed a
gradual\r\nincrease from the pyramidal cell soma towards the distal part of stratum
radiatum. The densities\r\nof extrasynaptic GluA1, GluA2 and panAMPA labeling
reached 10-15% of synaptic densities,\r\nwhile the ratio of extrasynaptic labeling
for GluA3 was significantly lower compared than those\r\nfor other subunits. The
labeling patterns for GluA1, GluA2 and GluA1-3 are similar and their\r\ndensities
were higher in the periphery than center of synapses. In contrast, the GluA3-\r\ncontaining
receptors were more centrally localized compared to the GluA1- and GluA2-\r\ncontaining
receptors.\r\nThe hippocampus plays a central role in learning and memory. Contextual
learning has been\r\nshown to require the delivery of AMPA receptors to CA1 synapses
in the dorsal hippocampus.\r\nHowever, proximodistal heterogeneity of this plasticity
and particular contribution of different\r\nAMPA receptor subunits are not fully
understood. By combining inhibitory avoidance task, a\r\nhippocampus-dependent
contextual fear-learning paradigm, with SDS-FRL, I have revealed an\r\nincrease
in synaptic density specific to GluA1-containing AMPA receptors in the CA1 area.\r\nThe
intrasynaptic distribution of GluA1 also changed from the periphery to center-preferred\r\npattern.
Furthermore, this synaptic plasticity was evident selectively in stratum radiatum
but\r\nnot stratum oriens, and in the CA1 subregion proximal but not distal to
CA2. These findings\r\nfurther contribute to our understanding of how specific
hippocampal subregions and AMPA\r\nreceptor subunits are involved in physiological
learning.\r\nAlthough the immunolabeling results above shed light on subunit-specific
plasticity in\r\nAMPAR distribution, no tools to visualize and study the subunit
composition at the single\r\nchannel level in situ have been available. Electron
microscopy with conventional immunogold\r\nlabeling approaches has limitations
in the single channel analysis because of the large size of\r\nantibodies and
steric hindrance hampering multiple subunit labeling of single channels. I\r\nmanaged
to develop a new chemical labeling system using a short peptide tag and small\r\nsynthetic
probes, which form specific covalent bond with a cysteine residue in the tag fused
to\r\nproteins of interest (reactive tag system). I additionally made substantial
progress into adapting\r\nthis system for AMPA receptor subunits."
acknowledged_ssus:
- _id: EM-Fac
alternative_title:
- ISTA Thesis
article_processing_charge: No
author:
- first_name: Marijo
full_name: Jevtic, Marijo
id: 4BE3BC94-F248-11E8-B48F-1D18A9856A87
last_name: Jevtic
citation:
ama: Jevtic M. Contextual fear learning induced changes in AMPA receptor subtypes
along the proximodistal axis in dorsal hippocampus. 2022. doi:10.15479/at:ista:11393
apa: Jevtic, M. (2022). Contextual fear learning induced changes in AMPA receptor
subtypes along the proximodistal axis in dorsal hippocampus. Institute of
Science and Technology Austria. https://doi.org/10.15479/at:ista:11393
chicago: Jevtic, Marijo. “Contextual Fear Learning Induced Changes in AMPA Receptor
Subtypes along the Proximodistal Axis in Dorsal Hippocampus.” Institute of Science
and Technology Austria, 2022. https://doi.org/10.15479/at:ista:11393.
ieee: M. Jevtic, “Contextual fear learning induced changes in AMPA receptor subtypes
along the proximodistal axis in dorsal hippocampus,” Institute of Science and
Technology Austria, 2022.
ista: Jevtic M. 2022. Contextual fear learning induced changes in AMPA receptor
subtypes along the proximodistal axis in dorsal hippocampus. Institute of Science
and Technology Austria.
mla: Jevtic, Marijo. Contextual Fear Learning Induced Changes in AMPA Receptor
Subtypes along the Proximodistal Axis in Dorsal Hippocampus. Institute of
Science and Technology Austria, 2022, doi:10.15479/at:ista:11393.
short: M. Jevtic, Contextual Fear Learning Induced Changes in AMPA Receptor Subtypes
along the Proximodistal Axis in Dorsal Hippocampus, Institute of Science and Technology
Austria, 2022.
date_created: 2022-05-17T08:57:41Z
date_published: 2022-05-16T00:00:00Z
date_updated: 2023-09-07T14:53:44Z
day: '16'
ddc:
- '570'
degree_awarded: PhD
department:
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- _id: RySh
doi: 10.15479/at:ista:11393
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date_updated: 2023-05-17T22:30:03Z
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file_id: '11395'
file_name: MJ thesis.docx
file_size: 56427603
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language:
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month: '05'
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page: '108'
publication_identifier:
issn:
- 2663-337X
publication_status: published
publisher: Institute of Science and Technology Austria
related_material:
record:
- id: '7391'
relation: part_of_dissertation
status: public
status: public
supervisor:
- first_name: Ryuichi
full_name: Shigemoto, Ryuichi
id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
last_name: Shigemoto
orcid: 0000-0001-8761-9444
title: Contextual fear learning induced changes in AMPA receptor subtypes along the
proximodistal axis in dorsal hippocampus
type: dissertation
user_id: 8b945eb4-e2f2-11eb-945a-df72226e66a9
year: '2022'
...
---
_id: '7551'
abstract:
- lang: eng
text: Novelty facilitates formation of memories. The detection of novelty and storage
of contextual memories are both mediated by the hippocampus, yet the mechanisms
that link these two functions remain to be defined. Dentate granule cells (GCs)
of the dorsal hippocampus fire upon novelty exposure forming engrams of contextual
memory. However, their key excitatory inputs from the entorhinal cortex are not
responsive to novelty and are insufficient to make dorsal GCs fire reliably. Here
we uncover a powerful glutamatergic pathway to dorsal GCs from ventral hippocampal
mossy cells (MCs) that relays novelty, and is necessary and sufficient for driving
dorsal GCs activation. Furthermore, manipulation of ventral MCs activity bidirectionally
regulates novelty-induced contextual memory acquisition. Our results show that
ventral MCs activity controls memory formation through an intra-hippocampal interaction
mechanism gated by novelty.
acknowledgement: We thank Peter Jonas and Peter Somogyi for critically reading the
manuscript, Satoshi Kida for helpful discussion, Taijia Makinen for providing the
Prox1-creERT2 mouse line, and Hiromu Yawo for the VAMP2-Venus construct. We also
thank Vivek Jayaraman, Ph.D.; Rex A. Kerr, Ph.D.; Douglas S. Kim, Ph.D.; Loren L.
Looger, Ph.D.; and Karel Svoboda, Ph.D. from the GENIE Project, Janelia Farm Research
Campus, Howard Hughes Medical Institute for the viral constructs used for GCaMP6s
expression. We also thank Jacqueline Montanaro, Vanessa Zheden, David Kleindienst,
and Laura Burnett for technical assistance, as well as Robert Beattie for imaging
assistance. This work was supported by a European Research Council Advanced Grant
694539 to R.S.
article_processing_charge: No
article_type: original
author:
- first_name: Felipe A
full_name: Fredes Tolorza, Felipe A
id: 384825DA-F248-11E8-B48F-1D18A9856A87
last_name: Fredes Tolorza
- first_name: Maria A
full_name: Silva Sifuentes, Maria A
id: 371B3D6E-F248-11E8-B48F-1D18A9856A87
last_name: Silva Sifuentes
- first_name: Peter
full_name: Koppensteiner, Peter
id: 3B8B25A8-F248-11E8-B48F-1D18A9856A87
last_name: Koppensteiner
- first_name: Kenta
full_name: Kobayashi, Kenta
last_name: Kobayashi
- first_name: Maximilian A
full_name: Jösch, Maximilian A
id: 2BD278E6-F248-11E8-B48F-1D18A9856A87
last_name: Jösch
orcid: 0000-0002-3937-1330
- first_name: Ryuichi
full_name: Shigemoto, Ryuichi
id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
last_name: Shigemoto
orcid: 0000-0001-8761-9444
citation:
ama: Fredes Tolorza FA, Silva Sifuentes MA, Koppensteiner P, Kobayashi K, Jösch
MA, Shigemoto R. Ventro-dorsal hippocampal pathway gates novelty-induced contextual
memory formation. Current Biology. 2021;31(1):P25-38.E5. doi:10.1016/j.cub.2020.09.074
apa: Fredes Tolorza, F. A., Silva Sifuentes, M. A., Koppensteiner, P., Kobayashi,
K., Jösch, M. A., & Shigemoto, R. (2021). Ventro-dorsal hippocampal pathway
gates novelty-induced contextual memory formation. Current Biology. Elsevier.
https://doi.org/10.1016/j.cub.2020.09.074
chicago: Fredes Tolorza, Felipe A, Maria A Silva Sifuentes, Peter Koppensteiner,
Kenta Kobayashi, Maximilian A Jösch, and Ryuichi Shigemoto. “Ventro-Dorsal Hippocampal
Pathway Gates Novelty-Induced Contextual Memory Formation.” Current Biology.
Elsevier, 2021. https://doi.org/10.1016/j.cub.2020.09.074.
ieee: F. A. Fredes Tolorza, M. A. Silva Sifuentes, P. Koppensteiner, K. Kobayashi,
M. A. Jösch, and R. Shigemoto, “Ventro-dorsal hippocampal pathway gates novelty-induced
contextual memory formation,” Current Biology, vol. 31, no. 1. Elsevier,
p. P25–38.E5, 2021.
ista: Fredes Tolorza FA, Silva Sifuentes MA, Koppensteiner P, Kobayashi K, Jösch
MA, Shigemoto R. 2021. Ventro-dorsal hippocampal pathway gates novelty-induced
contextual memory formation. Current Biology. 31(1), P25–38.E5.
mla: Fredes Tolorza, Felipe A., et al. “Ventro-Dorsal Hippocampal Pathway Gates
Novelty-Induced Contextual Memory Formation.” Current Biology, vol. 31,
no. 1, Elsevier, 2021, p. P25–38.E5, doi:10.1016/j.cub.2020.09.074.
short: F.A. Fredes Tolorza, M.A. Silva Sifuentes, P. Koppensteiner, K. Kobayashi,
M.A. Jösch, R. Shigemoto, Current Biology 31 (2021) P25–38.E5.
date_created: 2020-02-28T10:56:18Z
date_published: 2021-01-11T00:00:00Z
date_updated: 2023-08-04T10:47:11Z
day: '11'
ddc:
- '570'
department:
- _id: MaJö
- _id: RySh
doi: 10.1016/j.cub.2020.09.074
ec_funded: 1
external_id:
isi:
- '000614361000020'
file:
- access_level: open_access
checksum: b7b9c8bc84a08befce365c675229a7d1
content_type: application/pdf
creator: dernst
date_created: 2020-10-19T13:31:28Z
date_updated: 2020-10-19T13:31:28Z
file_id: '8678'
file_name: 2021_CurrentBiology_Fredes.pdf
file_size: 4915964
relation: main_file
success: 1
file_date_updated: 2020-10-19T13:31:28Z
has_accepted_license: '1'
intvolume: ' 31'
isi: 1
issue: '1'
language:
- iso: eng
month: '01'
oa: 1
oa_version: Published Version
page: P25-38.E5
project:
- _id: 25CA28EA-B435-11E9-9278-68D0E5697425
call_identifier: H2020
grant_number: '694539'
name: 'In situ analysis of single channel subunit composition in neurons: physiological
implication in synaptic plasticity and behaviour'
publication: Current Biology
publication_status: published
publisher: Elsevier
quality_controlled: '1'
related_material:
link:
- description: News on IST Homepage
relation: press_release
url: https://ist.ac.at/en/news/remembering-novelty/
status: public
title: Ventro-dorsal hippocampal pathway gates novelty-induced contextual memory formation
tmp:
image: /images/cc_by_nc_nd.png
legal_code_url: https://creativecommons.org/licenses/by-nc-nd/4.0/legalcode
name: Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International
(CC BY-NC-ND 4.0)
short: CC BY-NC-ND (4.0)
type: journal_article
user_id: 4359f0d1-fa6c-11eb-b949-802e58b17ae8
volume: 31
year: '2021'
...
---
_id: '9330'
abstract:
- lang: eng
text: In nerve cells the genes encoding for α2δ subunits of voltage-gated calcium
channels have been linked to synaptic functions and neurological disease. Here
we show that α2δ subunits are essential for the formation and organization of
glutamatergic synapses. Using a cellular α2δ subunit triple-knockout/knockdown
model, we demonstrate a failure in presynaptic differentiation evidenced by defective
presynaptic calcium channel clustering and calcium influx, smaller presynaptic
active zones, and a strongly reduced accumulation of presynaptic vesicle-associated
proteins (synapsin and vGLUT). The presynaptic defect is associated with the downscaling
of postsynaptic AMPA receptors and the postsynaptic density. The role of α2δ isoforms
as synaptic organizers is highly redundant, as each individual α2δ isoform can
rescue presynaptic calcium channel trafficking and expression of synaptic proteins.
Moreover, α2δ-2 and α2δ-3 with mutated metal ion-dependent adhesion sites can
fully rescue presynaptic synapsin expression but only partially calcium channel
trafficking, suggesting that the regulatory role of α2δ subunits is independent
from its role as a calcium channel subunit. Our findings influence the current
view on excitatory synapse formation. First, our study suggests that postsynaptic
differentiation is secondary to presynaptic differentiation. Second, the dependence
of presynaptic differentiation on α2δ implicates α2δ subunits as potential nucleation
points for the organization of synapses. Finally, our results suggest that α2δ
subunits act as transsynaptic organizers of glutamatergic synapses, thereby aligning
the synaptic active zone with the postsynaptic density.
acknowledged_ssus:
- _id: EM-Fac
acknowledgement: "We thank Arnold Schwartz for providing α2δ-1 knockout mice; Ariane
Benedetti, Sabine Baumgartner, Sandra Demetz, and Irene Mahlknecht for technical
support; Nadine Ortner and Andreas Lieb for electrophysiological experiments; the
team of the Electron Microscopy Facility at the Institute of Science and Technology
Austria for technical support related to ultrastructural analysis; Hermann Dietrich
and Anja Beierfuß and her team for animal care; Jutta Engel and Jörg Striessnig
for critical discussions; and Bruno Benedetti and Bernhard Flucher for critical
discussions and reading the manuscript. This study was supported by Austrian Science
Fund Grants P24079, F44060, F44150, and DOC30-B30 (to G.J.O.) and T855 (to M.C.),
European Research Council Grant AdG 694539 (to R.S.), Deutsche Forschungsgemeinschaft\r\nGrant
SFB1348-TP A03 (to M.M.), and Interdisziplinäre Zentrum für Klinische Forschung
Münster Grant Mi3/004/19 (to M.M.). This work is part of the PhD theses of C.L.S.,
S.M.G., and C.A."
article_processing_charge: No
article_type: original
author:
- first_name: Clemens L.
full_name: Schöpf, Clemens L.
last_name: Schöpf
- first_name: Cornelia
full_name: Ablinger, Cornelia
last_name: Ablinger
- first_name: Stefanie M.
full_name: Geisler, Stefanie M.
last_name: Geisler
- first_name: Ruslan I.
full_name: Stanika, Ruslan I.
last_name: Stanika
- first_name: Marta
full_name: Campiglio, Marta
last_name: Campiglio
- first_name: Walter
full_name: Kaufmann, Walter
id: 3F99E422-F248-11E8-B48F-1D18A9856A87
last_name: Kaufmann
orcid: 0000-0001-9735-5315
- first_name: Benedikt
full_name: Nimmervoll, Benedikt
last_name: Nimmervoll
- first_name: Bettina
full_name: Schlick, Bettina
last_name: Schlick
- first_name: Johannes
full_name: Brockhaus, Johannes
last_name: Brockhaus
- first_name: Markus
full_name: Missler, Markus
last_name: Missler
- first_name: Ryuichi
full_name: Shigemoto, Ryuichi
id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
last_name: Shigemoto
orcid: 0000-0001-8761-9444
- first_name: Gerald J.
full_name: Obermair, Gerald J.
last_name: Obermair
citation:
ama: Schöpf CL, Ablinger C, Geisler SM, et al. Presynaptic α2δ subunits are key
organizers of glutamatergic synapses. PNAS. 2021;118(14). doi:10.1073/pnas.1920827118
apa: Schöpf, C. L., Ablinger, C., Geisler, S. M., Stanika, R. I., Campiglio, M.,
Kaufmann, W., … Obermair, G. J. (2021). Presynaptic α2δ subunits are key organizers
of glutamatergic synapses. PNAS. National Academy of Sciences. https://doi.org/10.1073/pnas.1920827118
chicago: Schöpf, Clemens L., Cornelia Ablinger, Stefanie M. Geisler, Ruslan I. Stanika,
Marta Campiglio, Walter Kaufmann, Benedikt Nimmervoll, et al. “Presynaptic Α2δ
Subunits Are Key Organizers of Glutamatergic Synapses.” PNAS. National
Academy of Sciences, 2021. https://doi.org/10.1073/pnas.1920827118.
ieee: C. L. Schöpf et al., “Presynaptic α2δ subunits are key organizers of
glutamatergic synapses,” PNAS, vol. 118, no. 14. National Academy of Sciences,
2021.
ista: Schöpf CL, Ablinger C, Geisler SM, Stanika RI, Campiglio M, Kaufmann W, Nimmervoll
B, Schlick B, Brockhaus J, Missler M, Shigemoto R, Obermair GJ. 2021. Presynaptic
α2δ subunits are key organizers of glutamatergic synapses. PNAS. 118(14).
mla: Schöpf, Clemens L., et al. “Presynaptic Α2δ Subunits Are Key Organizers of
Glutamatergic Synapses.” PNAS, vol. 118, no. 14, National Academy of Sciences,
2021, doi:10.1073/pnas.1920827118.
short: C.L. Schöpf, C. Ablinger, S.M. Geisler, R.I. Stanika, M. Campiglio, W. Kaufmann,
B. Nimmervoll, B. Schlick, J. Brockhaus, M. Missler, R. Shigemoto, G.J. Obermair,
PNAS 118 (2021).
date_created: 2021-04-18T22:01:40Z
date_published: 2021-04-06T00:00:00Z
date_updated: 2023-08-08T13:08:47Z
day: '06'
ddc:
- '570'
department:
- _id: EM-Fac
- _id: RySh
doi: 10.1073/pnas.1920827118
ec_funded: 1
external_id:
isi:
- '000637398300002'
file:
- access_level: open_access
checksum: dd014f68ae9d7d8d8fc4139a24e04506
content_type: application/pdf
creator: dernst
date_created: 2021-04-19T10:10:56Z
date_updated: 2021-04-19T10:10:56Z
file_id: '9340'
file_name: 2021_PNAS_Schoepf.pdf
file_size: 2603911
relation: main_file
success: 1
file_date_updated: 2021-04-19T10:10:56Z
has_accepted_license: '1'
intvolume: ' 118'
isi: 1
issue: '14'
language:
- iso: eng
month: '04'
oa: 1
oa_version: Published Version
project:
- _id: 25CA28EA-B435-11E9-9278-68D0E5697425
call_identifier: H2020
grant_number: '694539'
name: 'In situ analysis of single channel subunit composition in neurons: physiological
implication in synaptic plasticity and behaviour'
publication: PNAS
publication_identifier:
eissn:
- 1091-6490
publication_status: published
publisher: National Academy of Sciences
quality_controlled: '1'
scopus_import: '1'
status: public
title: Presynaptic α2δ subunits are key organizers of glutamatergic synapses
tmp:
image: /images/cc_by.png
legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
short: CC BY (4.0)
type: journal_article
user_id: 4359f0d1-fa6c-11eb-b949-802e58b17ae8
volume: 118
year: '2021'
...
---
_id: '9641'
abstract:
- lang: eng
text: At the encounter with a novel environment, contextual memory formation is
greatly enhanced, accompanied with increased arousal and active exploration. Although
this phenomenon has been widely observed in animal and human daily life, how the
novelty in the environment is detected and contributes to contextual memory formation
has lately started to be unveiled. The hippocampus has been studied for many decades
for its largely known roles in encoding spatial memory, and a growing body of
evidence indicates a differential involvement of dorsal and ventral hippocampal
divisions in novelty detection. In this brief review article, we discuss the recent
findings of the role of mossy cells in the ventral hippocampal moiety in novelty
detection and put them in perspective with other novelty-related pathways in the
hippocampus. We propose a mechanism for novelty-driven memory acquisition in the
dentate gyrus by the direct projection of ventral mossy cells to dorsal dentate
granule cells. By this projection, the ventral hippocampus sends novelty signals
to the dorsal hippocampus, opening a gate for memory encoding in dentate granule
cells based on information coming from the entorhinal cortex. We conclude that,
contrary to the presently accepted functional independence, the dorsal and ventral
hippocampi cooperate to link the novelty and contextual information, and this
dorso-ventral interaction is crucial for the novelty-dependent memory formation.
acknowledgement: This work was supported by a European Research Council Advanced Grant
694539 to Ryuichi Shigemoto.
article_number: '107486'
article_processing_charge: No
article_type: original
author:
- first_name: Felipe
full_name: Fredes, Felipe
last_name: Fredes
- first_name: Ryuichi
full_name: Shigemoto, Ryuichi
id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
last_name: Shigemoto
orcid: 0000-0001-8761-9444
citation:
ama: Fredes F, Shigemoto R. The role of hippocampal mossy cells in novelty detection.
Neurobiology of Learning and Memory. 2021;183. doi:10.1016/j.nlm.2021.107486
apa: Fredes, F., & Shigemoto, R. (2021). The role of hippocampal mossy cells
in novelty detection. Neurobiology of Learning and Memory. Elsevier. https://doi.org/10.1016/j.nlm.2021.107486
chicago: Fredes, Felipe, and Ryuichi Shigemoto. “The Role of Hippocampal Mossy Cells
in Novelty Detection.” Neurobiology of Learning and Memory. Elsevier, 2021.
https://doi.org/10.1016/j.nlm.2021.107486.
ieee: F. Fredes and R. Shigemoto, “The role of hippocampal mossy cells in novelty
detection,” Neurobiology of Learning and Memory, vol. 183. Elsevier, 2021.
ista: Fredes F, Shigemoto R. 2021. The role of hippocampal mossy cells in novelty
detection. Neurobiology of Learning and Memory. 183, 107486.
mla: Fredes, Felipe, and Ryuichi Shigemoto. “The Role of Hippocampal Mossy Cells
in Novelty Detection.” Neurobiology of Learning and Memory, vol. 183, 107486,
Elsevier, 2021, doi:10.1016/j.nlm.2021.107486.
short: F. Fredes, R. Shigemoto, Neurobiology of Learning and Memory 183 (2021).
date_created: 2021-07-11T22:01:16Z
date_published: 2021-06-30T00:00:00Z
date_updated: 2023-08-10T14:10:37Z
day: '30'
ddc:
- '610'
department:
- _id: RySh
doi: 10.1016/j.nlm.2021.107486
ec_funded: 1
external_id:
isi:
- '000677694900004'
pmid:
- '34214666'
file:
- access_level: open_access
checksum: 8e8298a9e8c7df146ad23f32c2a63929
content_type: application/pdf
creator: cziletti
date_created: 2021-07-19T13:46:06Z
date_updated: 2021-07-19T13:46:06Z
file_id: '9694'
file_name: 2021_NeurobLearnMemory_Fredes.pdf
file_size: 1994793
relation: main_file
success: 1
file_date_updated: 2021-07-19T13:46:06Z
has_accepted_license: '1'
intvolume: ' 183'
isi: 1
language:
- iso: eng
month: '06'
oa: 1
oa_version: Published Version
pmid: 1
project:
- _id: 25CA28EA-B435-11E9-9278-68D0E5697425
call_identifier: H2020
grant_number: '694539'
name: 'In situ analysis of single channel subunit composition in neurons: physiological
implication in synaptic plasticity and behaviour'
publication: Neurobiology of Learning and Memory
publication_identifier:
eissn:
- '10959564'
issn:
- '10747427'
publication_status: published
publisher: Elsevier
quality_controlled: '1'
scopus_import: '1'
status: public
title: The role of hippocampal mossy cells in novelty detection
tmp:
image: /images/cc_by_nc_nd.png
legal_code_url: https://creativecommons.org/licenses/by-nc-nd/4.0/legalcode
name: Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International
(CC BY-NC-ND 4.0)
short: CC BY-NC-ND (4.0)
type: journal_article
user_id: 4359f0d1-fa6c-11eb-b949-802e58b17ae8
volume: 183
year: '2021'
...
---
_id: '10051'
abstract:
- lang: eng
text: 'Rab-interacting molecule (RIM)-binding protein 2 (BP2) is a multidomain protein
of the presynaptic active zone (AZ). By binding to RIM, bassoon (Bsn), and voltage-gated
Ca2+ channels (CaV), it is considered to be a central organizer of the topography
of CaV and release sites of synaptic vesicles (SVs) at the AZ. Here, we used RIM-BP2
knock-out (KO) mice and their wild-type (WT) littermates of either sex to investigate
the role of RIM-BP2 at the endbulb of Held synapse of auditory nerve fibers (ANFs)
with bushy cells (BCs) of the cochlear nucleus, a fast relay of the auditory pathway
with high release probability. Disruption of RIM-BP2 lowered release probability
altering short-term plasticity and reduced evoked EPSCs. Analysis of SV pool dynamics
during high-frequency train stimulation indicated a reduction of SVs with high
release probability but an overall normal size of the readily releasable SV pool
(RRP). The Ca2+-dependent fast component of SV replenishment after RRP depletion
was slowed. Ultrastructural analysis by superresolution light and electron microscopy
revealed an impaired topography of presynaptic CaV and a reduction of docked and
membrane-proximal SVs at the AZ. We conclude that RIM-BP2 organizes the topography
of CaV, and promotes SV tethering and docking. This way RIM-BP2 is critical for
establishing a high initial release probability as required to reliably signal
sound onset information that we found to be degraded in BCs of RIM-BP2-deficient
mice in vivo. SIGNIFICANCE STATEMENT: Rab-interacting molecule (RIM)-binding proteins
(BPs) are key organizers of the active zone (AZ). Using a multidisciplinary approach
to the calyceal endbulb of Held synapse that transmits auditory information at
rates of up to hundreds of Hertz with submillisecond precision we demonstrate
a requirement for RIM-BP2 for normal auditory signaling. Endbulb synapses lacking
RIM-BP2 show a reduced release probability despite normal whole-terminal Ca2+
influx and abundance of the key priming protein Munc13-1, a reduced rate of SV
replenishment, as well as an altered topography of voltage-gated (CaV)2.1 Ca2+
channels, and fewer docked and membrane proximal synaptic vesicles (SVs). This
hampers transmission of sound onset information likely affecting downstream neural
computations such as of sound localization.'
acknowledgement: This work was supported by the Deutsche Forschungsgemeinschaft (DFG,
German Research Foundation) through the Collaborative Sensory Research Center 1286
[to C.W. (A4) and T.M. (B5)] and under Germany’s Excellence Strategy Grant EXC 2067/1-390729940.
We thank S. Gerke, A.J. Goldak, and C. Senger-Freitag for expert technical assistance;
G. Hoch for developing image analysis routines; and S. Chepurwar and N. Strenzke
for technical support and discussion regarding in vivo experiments. We also thank
Dr. Christian Rosenmund, Dr. Katharina Grauel, and Dr. Stephan Sigrist for providing
RIM-BP2 KO mice and Dr. Masahiko Watanabe for providing the anti-neurexin-antibody,
and Dr. Toshihisa Ohtsuka for the anti-ELKS-antibody. J. Neef for help with the
STED imaging and image analysis; E. Neher and S. Rizzoli for discussion and comments
on the manuscript; K. Eguchi for help with the statistical analysis; and C. H. Huang
and J. Neef for constant support and scientific discussion.
article_processing_charge: No
article_type: original
author:
- first_name: Tanvi
full_name: Butola, Tanvi
last_name: Butola
- first_name: Theocharis
full_name: Alvanos, Theocharis
last_name: Alvanos
- first_name: Anika
full_name: Hintze, Anika
last_name: Hintze
- first_name: Peter
full_name: Koppensteiner, Peter
id: 3B8B25A8-F248-11E8-B48F-1D18A9856A87
last_name: Koppensteiner
orcid: 0000-0002-3509-1948
- first_name: David
full_name: Kleindienst, David
id: 42E121A4-F248-11E8-B48F-1D18A9856A87
last_name: Kleindienst
- first_name: Ryuichi
full_name: Shigemoto, Ryuichi
id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
last_name: Shigemoto
orcid: 0000-0001-8761-9444
- first_name: Carolin
full_name: Wichmann, Carolin
last_name: Wichmann
- first_name: Tobias
full_name: Moser, Tobias
last_name: Moser
citation:
ama: Butola T, Alvanos T, Hintze A, et al. RIM-binding protein 2 organizes Ca21
channel topography and regulates release probability and vesicle replenishment
at a fast central synapse. Journal of Neuroscience. 2021;41(37):7742-7767.
doi:10.1523/JNEUROSCI.0586-21.2021
apa: Butola, T., Alvanos, T., Hintze, A., Koppensteiner, P., Kleindienst, D., Shigemoto,
R., … Moser, T. (2021). RIM-binding protein 2 organizes Ca21 channel
topography and regulates release probability and vesicle replenishment at a fast
central synapse. Journal of Neuroscience. Society for Neuroscience. https://doi.org/10.1523/JNEUROSCI.0586-21.2021
chicago: Butola, Tanvi, Theocharis Alvanos, Anika Hintze, Peter Koppensteiner, David
Kleindienst, Ryuichi Shigemoto, Carolin Wichmann, and Tobias Moser. “RIM-Binding
Protein 2 Organizes Ca21 Channel Topography and Regulates Release Probability
and Vesicle Replenishment at a Fast Central Synapse.” Journal of Neuroscience.
Society for Neuroscience, 2021. https://doi.org/10.1523/JNEUROSCI.0586-21.2021.
ieee: T. Butola et al., “RIM-binding protein 2 organizes Ca21
channel topography and regulates release probability and vesicle replenishment
at a fast central synapse,” Journal of Neuroscience, vol. 41, no. 37. Society
for Neuroscience, pp. 7742–7767, 2021.
ista: Butola T, Alvanos T, Hintze A, Koppensteiner P, Kleindienst D, Shigemoto R,
Wichmann C, Moser T. 2021. RIM-binding protein 2 organizes Ca21 channel
topography and regulates release probability and vesicle replenishment at a fast
central synapse. Journal of Neuroscience. 41(37), 7742–7767.
mla: Butola, Tanvi, et al. “RIM-Binding Protein 2 Organizes Ca21 Channel
Topography and Regulates Release Probability and Vesicle Replenishment at a Fast
Central Synapse.” Journal of Neuroscience, vol. 41, no. 37, Society for
Neuroscience, 2021, pp. 7742–67, doi:10.1523/JNEUROSCI.0586-21.2021.
short: T. Butola, T. Alvanos, A. Hintze, P. Koppensteiner, D. Kleindienst, R. Shigemoto,
C. Wichmann, T. Moser, Journal of Neuroscience 41 (2021) 7742–7767.
date_created: 2021-09-27T14:33:13Z
date_published: 2021-09-15T00:00:00Z
date_updated: 2023-08-14T06:56:30Z
day: '15'
ddc:
- '570'
department:
- _id: RySh
doi: 10.1523/JNEUROSCI.0586-21.2021
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- '34353898'
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publication: Journal of Neuroscience
publication_identifier:
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publication_status: published
publisher: Society for Neuroscience
quality_controlled: '1'
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title: RIM-binding protein 2 organizes Ca21 channel topography and regulates
release probability and vesicle replenishment at a fast central synapse
tmp:
image: /images/cc_by.png
legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
short: CC BY (4.0)
type: journal_article
user_id: 4359f0d1-fa6c-11eb-b949-802e58b17ae8
volume: 41
year: '2021'
...
---
_id: '10403'
abstract:
- lang: eng
text: Synaptic transmission, connectivity, and dendritic morphology mature in parallel
during brain development and are often disrupted in neurodevelopmental disorders.
Yet how these changes influence the neuronal computations necessary for normal
brain function are not well understood. To identify cellular mechanisms underlying
the maturation of synaptic integration in interneurons, we combined patch-clamp
recordings of excitatory inputs in mouse cerebellar stellate cells (SCs), three-dimensional
reconstruction of SC morphology with excitatory synapse location, and biophysical
modeling. We found that postnatal maturation of postsynaptic strength was homogeneously
reduced along the somatodendritic axis, but dendritic integration was always sublinear.
However, dendritic branching increased without changes in synapse density, leading
to a substantial gain in distal inputs. Thus, changes in synapse distribution,
rather than dendrite cable properties, are the dominant mechanism underlying the
maturation of neuronal computation. These mechanisms favor the emergence of a
spatially compartmentalized two-stage integration model promoting location-dependent
integration within dendritic subunits.
acknowledgement: This study was supported by the Centre National de la Recherche Scientifique
and the Agence Nationale de la Recherche (ANR-13-BSV4-00166, to LC and DAD). TA
was supported by fellowships from the Fondation pour la Recherche Medicale and the
Swedish Research Council. We thank Dmitry Ershov from the Image Analysis Hub of
the Institut Pasteur, Elodie Le Monnier, Elena Hollergschwandtner, Vanessa Zheden,
and Corinne Nantet for technical support and Haining Zhong for providing the Venus-tagged
PSD95 mouse line. We would like to thank Alberto Bacci, Ann Lohof, and Nelson Rebola
for comments on the manuscript.
article_number: e65954
article_processing_charge: No
article_type: original
author:
- first_name: Celia
full_name: Biane, Celia
last_name: Biane
- first_name: Florian
full_name: Rückerl, Florian
last_name: Rückerl
- first_name: Therese
full_name: Abrahamsson, Therese
last_name: Abrahamsson
- first_name: Cécile
full_name: Saint-Cloment, Cécile
last_name: Saint-Cloment
- first_name: Jean
full_name: Mariani, Jean
last_name: Mariani
- first_name: Ryuichi
full_name: Shigemoto, Ryuichi
id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
last_name: Shigemoto
orcid: 0000-0001-8761-9444
- first_name: David A.
full_name: Digregorio, David A.
last_name: Digregorio
- first_name: Rachel M.
full_name: Sherrard, Rachel M.
last_name: Sherrard
- first_name: Laurence
full_name: Cathala, Laurence
last_name: Cathala
citation:
ama: Biane C, Rückerl F, Abrahamsson T, et al. Developmental emergence of two-stage
nonlinear synaptic integration in cerebellar interneurons. eLife. 2021;10.
doi:10.7554/eLife.65954
apa: Biane, C., Rückerl, F., Abrahamsson, T., Saint-Cloment, C., Mariani, J., Shigemoto,
R., … Cathala, L. (2021). Developmental emergence of two-stage nonlinear synaptic
integration in cerebellar interneurons. ELife. eLife Sciences Publications.
https://doi.org/10.7554/eLife.65954
chicago: Biane, Celia, Florian Rückerl, Therese Abrahamsson, Cécile Saint-Cloment,
Jean Mariani, Ryuichi Shigemoto, David A. Digregorio, Rachel M. Sherrard, and
Laurence Cathala. “Developmental Emergence of Two-Stage Nonlinear Synaptic Integration
in Cerebellar Interneurons.” ELife. eLife Sciences Publications, 2021.
https://doi.org/10.7554/eLife.65954.
ieee: C. Biane et al., “Developmental emergence of two-stage nonlinear synaptic
integration in cerebellar interneurons,” eLife, vol. 10. eLife Sciences
Publications, 2021.
ista: Biane C, Rückerl F, Abrahamsson T, Saint-Cloment C, Mariani J, Shigemoto R,
Digregorio DA, Sherrard RM, Cathala L. 2021. Developmental emergence of two-stage
nonlinear synaptic integration in cerebellar interneurons. eLife. 10, e65954.
mla: Biane, Celia, et al. “Developmental Emergence of Two-Stage Nonlinear Synaptic
Integration in Cerebellar Interneurons.” ELife, vol. 10, e65954, eLife
Sciences Publications, 2021, doi:10.7554/eLife.65954.
short: C. Biane, F. Rückerl, T. Abrahamsson, C. Saint-Cloment, J. Mariani, R. Shigemoto,
D.A. Digregorio, R.M. Sherrard, L. Cathala, ELife 10 (2021).
date_created: 2021-12-05T23:01:40Z
date_published: 2021-11-03T00:00:00Z
date_updated: 2023-08-14T13:12:07Z
day: '03'
ddc:
- '570'
department:
- _id: RySh
doi: 10.7554/eLife.65954
external_id:
isi:
- '000715789500001'
file:
- access_level: open_access
checksum: c7c33c3319428d56e332e22349c50ed3
content_type: application/pdf
creator: cchlebak
date_created: 2021-12-10T08:31:41Z
date_updated: 2021-12-10T08:31:41Z
file_id: '10528'
file_name: 2021_eLife_Biane.pdf
file_size: 13131322
relation: main_file
success: 1
file_date_updated: 2021-12-10T08:31:41Z
has_accepted_license: '1'
intvolume: ' 10'
isi: 1
language:
- iso: eng
month: '11'
oa: 1
oa_version: Published Version
publication: eLife
publication_identifier:
eissn:
- 2050-084X
publication_status: published
publisher: eLife Sciences Publications
quality_controlled: '1'
scopus_import: '1'
status: public
title: Developmental emergence of two-stage nonlinear synaptic integration in cerebellar
interneurons
tmp:
image: /images/cc_by.png
legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
short: CC BY (4.0)
type: journal_article
user_id: 4359f0d1-fa6c-11eb-b949-802e58b17ae8
volume: 10
year: '2021'
...