[{"oa_version":"Published Version","file":[{"file_id":"13246","relation":"main_file","success":1,"checksum":"8e88cb0e5a6433a2f1939a9030bed384","date_created":"2023-07-18T07:59:58Z","date_updated":"2023-07-18T07:59:58Z","access_level":"open_access","file_name":"2023_PloSBiology_Shamipour.pdf","creator":"dernst","file_size":4431723,"content_type":"application/pdf"}],"intvolume":" 21","status":"public","title":"Yolk granule fusion and microtubule aster formation regulate cortical granule translocation and exocytosis in zebrafish oocytes","ddc":["570"],"user_id":"4359f0d1-fa6c-11eb-b949-802e58b17ae8","_id":"13229","issue":"6","abstract":[{"lang":"eng","text":"Dynamic reorganization of the cytoplasm is key to many core cellular processes, such as cell division, cell migration, and cell polarization. Cytoskeletal rearrangements are thought to constitute the main drivers of cytoplasmic flows and reorganization. In contrast, remarkably little is known about how dynamic changes in size and shape of cell organelles affect cytoplasmic organization. Here, we show that within the maturing zebrafish oocyte, the surface localization of exocytosis-competent cortical granules (Cgs) upon germinal vesicle breakdown (GVBD) is achieved by the combined activities of yolk granule (Yg) fusion and microtubule aster formation and translocation. We find that Cgs are moved towards the oocyte surface through radially outward cytoplasmic flows induced by Ygs fusing and compacting towards the oocyte center in response to GVBD. We further show that vesicles decorated with the small Rab GTPase Rab11, a master regulator of vesicular trafficking and exocytosis, accumulate together with Cgs at the oocyte surface. This accumulation is achieved by Rab11-positive vesicles being transported by acentrosomal microtubule asters, the formation of which is induced by the release of CyclinB/Cdk1 upon GVBD, and which display a net movement towards the oocyte surface by preferentially binding to the oocyte actin cortex. We finally demonstrate that the decoration of Cgs by Rab11 at the oocyte surface is needed for Cg exocytosis and subsequent chorion elevation, a process central in egg activation. Collectively, these findings unravel a yet unrecognized role of organelle fusion, functioning together with cytoskeletal rearrangements, in orchestrating cytoplasmic organization during oocyte maturation."}],"type":"journal_article","date_published":"2023-06-08T00:00:00Z","page":"e3002146","article_type":"original","citation":{"ama":"Shamipour S, Hofmann L, Steccari I, Kardos R, Heisenberg C-PJ. Yolk granule fusion and microtubule aster formation regulate cortical granule translocation and exocytosis in zebrafish oocytes. PLoS Biology. 2023;21(6):e3002146. doi:10.1371/journal.pbio.3002146","ieee":"S. Shamipour, L. Hofmann, I. Steccari, R. Kardos, and C.-P. J. Heisenberg, “Yolk granule fusion and microtubule aster formation regulate cortical granule translocation and exocytosis in zebrafish oocytes,” PLoS Biology, vol. 21, no. 6. Public Library of Science, p. e3002146, 2023.","apa":"Shamipour, S., Hofmann, L., Steccari, I., Kardos, R., & Heisenberg, C.-P. J. (2023). Yolk granule fusion and microtubule aster formation regulate cortical granule translocation and exocytosis in zebrafish oocytes. PLoS Biology. Public Library of Science. https://doi.org/10.1371/journal.pbio.3002146","ista":"Shamipour S, Hofmann L, Steccari I, Kardos R, Heisenberg C-PJ. 2023. Yolk granule fusion and microtubule aster formation regulate cortical granule translocation and exocytosis in zebrafish oocytes. PLoS Biology. 21(6), e3002146.","short":"S. Shamipour, L. Hofmann, I. Steccari, R. Kardos, C.-P.J. Heisenberg, PLoS Biology 21 (2023) e3002146.","mla":"Shamipour, Shayan, et al. “Yolk Granule Fusion and Microtubule Aster Formation Regulate Cortical Granule Translocation and Exocytosis in Zebrafish Oocytes.” PLoS Biology, vol. 21, no. 6, Public Library of Science, 2023, p. e3002146, doi:10.1371/journal.pbio.3002146.","chicago":"Shamipour, Shayan, Laura Hofmann, Irene Steccari, Roland Kardos, and Carl-Philipp J Heisenberg. “Yolk Granule Fusion and Microtubule Aster Formation Regulate Cortical Granule Translocation and Exocytosis in Zebrafish Oocytes.” PLoS Biology. Public Library of Science, 2023. https://doi.org/10.1371/journal.pbio.3002146."},"publication":"PLoS Biology","article_processing_charge":"No","has_accepted_license":"1","day":"08","scopus_import":"1","volume":21,"date_created":"2023-07-16T22:01:09Z","date_updated":"2023-08-02T06:33:14Z","author":[{"id":"40B34FE2-F248-11E8-B48F-1D18A9856A87","last_name":"Shamipour","first_name":"Shayan","full_name":"Shamipour, Shayan"},{"id":"b88d43f2-dc74-11ea-a0a7-e41b7912e031","last_name":"Hofmann","first_name":"Laura","full_name":"Hofmann, Laura"},{"full_name":"Steccari, Irene","last_name":"Steccari","first_name":"Irene","id":"2705C766-9FE2-11EA-B224-C6773DDC885E"},{"first_name":"Roland","last_name":"Kardos","id":"4039350E-F248-11E8-B48F-1D18A9856A87","full_name":"Kardos, Roland"},{"orcid":"0000-0002-0912-4566","id":"39427864-F248-11E8-B48F-1D18A9856A87","last_name":"Heisenberg","first_name":"Carl-Philipp J","full_name":"Heisenberg, Carl-Philipp J"}],"publisher":"Public Library of Science","department":[{"_id":"CaHe"}],"publication_status":"published","pmid":1,"year":"2023","acknowledgement":"This work was supported by funding from the European Union (European Research Council Advanced grant 742573) to C.-P.H. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.","ec_funded":1,"file_date_updated":"2023-07-18T07:59:58Z","language":[{"iso":"eng"}],"doi":"10.1371/journal.pbio.3002146","project":[{"_id":"260F1432-B435-11E9-9278-68D0E5697425","grant_number":"742573","call_identifier":"H2020","name":"Interaction and feedback between cell mechanics and fate specification in vertebrate gastrulation"}],"quality_controlled":"1","isi":1,"external_id":{"pmid":["37289834"],"isi":["001003199100005"]},"tmp":{"name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","short":"CC BY (4.0)","image":"/images/cc_by.png"},"oa":1,"publication_identifier":{"eissn":["1545-7885"]},"month":"06"},{"publisher":"Springer Nature","department":[{"_id":"CaHe"},{"_id":"EdHa"}],"publication_status":"published","year":"2022","acknowledgement":"We thank K. Sampath, A. Pauli and Y. Bellaїche for feedback on the manuscript. We also thank the members of the Heisenberg group, in particular A. Schauer and F. Nur Arslan, for help, technical advice and discussions, and the Bioimaging and Life Science facilities at IST\r\nAustria for continuous support. We thank C. Flandoli for the artwork in the figures. This work was supported by postdoctoral fellowships from EMBO (LTF-850-2017) and HFSP (LT000429/2018-L2) to D.P. and the European Union (European Research Council starting grant 851288 to É.H. and European Research Council advanced grant 742573 to C.-P.H.).","volume":18,"date_updated":"2023-08-04T09:15:58Z","date_created":"2023-01-16T09:45:19Z","author":[{"first_name":"Diana C","last_name":"Nunes Pinheiro","id":"2E839F16-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0003-4333-7503","full_name":"Nunes Pinheiro, Diana C"},{"last_name":"Kardos","first_name":"Roland","id":"4039350E-F248-11E8-B48F-1D18A9856A87","full_name":"Kardos, Roland"},{"id":"3A9DB764-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0001-6005-1561","first_name":"Edouard B","last_name":"Hannezo","full_name":"Hannezo, Edouard B"},{"orcid":"0000-0002-0912-4566","id":"39427864-F248-11E8-B48F-1D18A9856A87","last_name":"Heisenberg","first_name":"Carl-Philipp J","full_name":"Heisenberg, Carl-Philipp J"}],"ec_funded":1,"file_date_updated":"2023-01-27T07:32:01Z","project":[{"name":"Coordination of mesendoderm cell fate specification and internalization during zebrafish gastrulation","grant_number":"ALTF 850-2017","_id":"26520D1E-B435-11E9-9278-68D0E5697425"},{"grant_number":"ALTF 850-2017","_id":"26520D1E-B435-11E9-9278-68D0E5697425","name":"Coordination of mesendoderm cell fate specification and internalization during zebrafish gastrulation"},{"_id":"05943252-7A3F-11EA-A408-12923DDC885E","grant_number":"851288","name":"Design Principles of Branching Morphogenesis","call_identifier":"H2020"},{"_id":"260F1432-B435-11E9-9278-68D0E5697425","grant_number":"742573","name":"Interaction and feedback between cell mechanics and fate specification in vertebrate gastrulation","call_identifier":"H2020"}],"isi":1,"quality_controlled":"1","tmp":{"name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","short":"CC BY (4.0)","image":"/images/cc_by.png"},"oa":1,"external_id":{"isi":["000871319900002"]},"language":[{"iso":"eng"}],"acknowledged_ssus":[{"_id":"Bio"},{"_id":"LifeSc"}],"doi":"10.1038/s41567-022-01787-6","publication_identifier":{"issn":["1745-2473"],"eissn":["1745-2481"]},"month":"12","intvolume":" 18","title":"Morphogen gradient orchestrates pattern-preserving tissue morphogenesis via motility-driven unjamming","status":"public","ddc":["570"],"user_id":"4359f0d1-fa6c-11eb-b949-802e58b17ae8","_id":"12209","file":[{"relation":"main_file","file_id":"12412","date_created":"2023-01-27T07:32:01Z","date_updated":"2023-01-27T07:32:01Z","checksum":"c86a8e8d80d1bfc46d56a01e88a2526a","success":1,"file_name":"2022_NaturePhysics_Pinheiro.pdf","access_level":"open_access","content_type":"application/pdf","file_size":36703569,"creator":"dernst"}],"oa_version":"Published Version","type":"journal_article","issue":"12","abstract":[{"lang":"eng","text":"Embryo development requires biochemical signalling to generate patterns of cell fates and active mechanical forces to drive tissue shape changes. However, how these processes are coordinated, and how tissue patterning is preserved despite the cellular flows occurring during morphogenesis, remains poorly understood. Gastrulation is a crucial embryonic stage that involves both patterning and internalization of the mesendoderm germ layer tissue. Here we show that, in zebrafish embryos, a gradient in Nodal signalling orchestrates pattern-preserving internalization movements by triggering a motility-driven unjamming transition. In addition to its role as a morphogen determining embryo patterning, graded Nodal signalling mechanically subdivides the mesendoderm into a small fraction of highly protrusive leader cells, able to autonomously internalize via local unjamming, and less protrusive followers, which need to be pulled inwards by the leaders. The Nodal gradient further enforces a code of preferential adhesion coupling leaders to their immediate followers, resulting in a collective and ordered mode of internalization that preserves mesendoderm patterning. Integrating this dual mechanical role of Nodal signalling into minimal active particle simulations quantitatively predicts both physiological and experimentally perturbed internalization movements. This provides a quantitative framework for how a morphogen-encoded unjamming transition can bidirectionally couple tissue mechanics with patterning during complex three-dimensional morphogenesis."}],"page":"1482-1493","article_type":"original","citation":{"chicago":"Nunes Pinheiro, Diana C, Roland Kardos, Edouard B Hannezo, and Carl-Philipp J Heisenberg. “Morphogen Gradient Orchestrates Pattern-Preserving Tissue Morphogenesis via Motility-Driven Unjamming.” Nature Physics. Springer Nature, 2022. https://doi.org/10.1038/s41567-022-01787-6.","mla":"Nunes Pinheiro, Diana C., et al. “Morphogen Gradient Orchestrates Pattern-Preserving Tissue Morphogenesis via Motility-Driven Unjamming.” Nature Physics, vol. 18, no. 12, Springer Nature, 2022, pp. 1482–93, doi:10.1038/s41567-022-01787-6.","short":"D.C. Nunes Pinheiro, R. Kardos, E.B. Hannezo, C.-P.J. Heisenberg, Nature Physics 18 (2022) 1482–1493.","ista":"Nunes Pinheiro DC, Kardos R, Hannezo EB, Heisenberg C-PJ. 2022. Morphogen gradient orchestrates pattern-preserving tissue morphogenesis via motility-driven unjamming. Nature Physics. 18(12), 1482–1493.","apa":"Nunes Pinheiro, D. C., Kardos, R., Hannezo, E. B., & Heisenberg, C.-P. J. (2022). Morphogen gradient orchestrates pattern-preserving tissue morphogenesis via motility-driven unjamming. Nature Physics. Springer Nature. https://doi.org/10.1038/s41567-022-01787-6","ieee":"D. C. Nunes Pinheiro, R. Kardos, E. B. Hannezo, and C.-P. J. Heisenberg, “Morphogen gradient orchestrates pattern-preserving tissue morphogenesis via motility-driven unjamming,” Nature Physics, vol. 18, no. 12. Springer Nature, pp. 1482–1493, 2022.","ama":"Nunes Pinheiro DC, Kardos R, Hannezo EB, Heisenberg C-PJ. Morphogen gradient orchestrates pattern-preserving tissue morphogenesis via motility-driven unjamming. Nature Physics. 2022;18(12):1482-1493. doi:10.1038/s41567-022-01787-6"},"publication":"Nature Physics","date_published":"2022-12-01T00:00:00Z","keyword":["General Physics and Astronomy"],"scopus_import":"1","has_accepted_license":"1","article_processing_charge":"No","day":"01"},{"publication_identifier":{"eissn":["10974172"],"issn":["00928674"]},"month":"05","external_id":{"isi":["000469415100013"],"pmid":["31080065"]},"oa":1,"main_file_link":[{"open_access":"1","url":"https://doi.org/10.1016/j.cell.2019.04.030"}],"project":[{"grant_number":"742573","_id":"260F1432-B435-11E9-9278-68D0E5697425","call_identifier":"H2020","name":"Interaction and feedback between cell mechanics and fate specification in vertebrate gastrulation"},{"grant_number":"P31639","_id":"268294B6-B435-11E9-9278-68D0E5697425","call_identifier":"FWF","name":"Active mechano-chemical description of the cell cytoskeleton"}],"isi":1,"quality_controlled":"1","doi":"10.1016/j.cell.2019.04.030","language":[{"iso":"eng"}],"acknowledged_ssus":[{"_id":"Bio"},{"_id":"PreCl"}],"ec_funded":1,"file_date_updated":"2020-10-21T07:22:34Z","pmid":1,"year":"2019","acknowledgement":"We would like to thank Pierre Recho, Guillaume Salbreux, and Silvia Grigolon for advice on the theory, Lila Solnica-Krezel for kindly providing us with zebrafish dachsous mutants, members of the Heisenberg and Hannezo groups for fruitful discussions, and the Bioimaging and zebrafish facilities at IST Austria for their continuous support. This project has received funding from the European Union (European Research Council Advanced Grant 742573 to C.P.H.) and from the Austrian Science Fund (FWF) (P 31639 to E.H.).","publisher":"Elsevier","department":[{"_id":"CaHe"},{"_id":"EdHa"},{"_id":"BjHo"}],"publication_status":"published","related_material":{"record":[{"id":"8350","relation":"dissertation_contains","status":"public"}],"link":[{"description":"News on IST Homepage","relation":"press_release","url":"https://ist.ac.at/en/news/how-the-cytoplasm-separates-from-the-yolk/"}]},"author":[{"full_name":"Shamipour, Shayan","first_name":"Shayan","last_name":"Shamipour","id":"40B34FE2-F248-11E8-B48F-1D18A9856A87"},{"last_name":"Kardos","first_name":"Roland","id":"4039350E-F248-11E8-B48F-1D18A9856A87","full_name":"Kardos, Roland"},{"full_name":"Xue, Shi-lei","id":"31D2C804-F248-11E8-B48F-1D18A9856A87","last_name":"Xue","first_name":"Shi-lei"},{"full_name":"Hof, Björn","id":"3A374330-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0003-2057-2754","first_name":"Björn","last_name":"Hof"},{"full_name":"Hannezo, Edouard B","orcid":"0000-0001-6005-1561","id":"3A9DB764-F248-11E8-B48F-1D18A9856A87","last_name":"Hannezo","first_name":"Edouard B"},{"full_name":"Heisenberg, Carl-Philipp J","first_name":"Carl-Philipp J","last_name":"Heisenberg","id":"39427864-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0002-0912-4566"}],"volume":177,"date_created":"2019-06-02T21:59:12Z","date_updated":"2024-03-28T23:30:39Z","scopus_import":"1","article_processing_charge":"No","has_accepted_license":"1","day":"30","citation":{"ama":"Shamipour S, Kardos R, Xue S, Hof B, Hannezo EB, Heisenberg C-PJ. Bulk actin dynamics drive phase segregation in zebrafish oocytes. Cell. 2019;177(6):1463-1479.e18. doi:10.1016/j.cell.2019.04.030","ista":"Shamipour S, Kardos R, Xue S, Hof B, Hannezo EB, Heisenberg C-PJ. 2019. Bulk actin dynamics drive phase segregation in zebrafish oocytes. Cell. 177(6), 1463–1479.e18.","apa":"Shamipour, S., Kardos, R., Xue, S., Hof, B., Hannezo, E. B., & Heisenberg, C.-P. J. (2019). Bulk actin dynamics drive phase segregation in zebrafish oocytes. Cell. Elsevier. https://doi.org/10.1016/j.cell.2019.04.030","ieee":"S. Shamipour, R. Kardos, S. Xue, B. Hof, E. B. Hannezo, and C.-P. J. Heisenberg, “Bulk actin dynamics drive phase segregation in zebrafish oocytes,” Cell, vol. 177, no. 6. Elsevier, p. 1463–1479.e18, 2019.","mla":"Shamipour, Shayan, et al. “Bulk Actin Dynamics Drive Phase Segregation in Zebrafish Oocytes.” Cell, vol. 177, no. 6, Elsevier, 2019, p. 1463–1479.e18, doi:10.1016/j.cell.2019.04.030.","short":"S. Shamipour, R. Kardos, S. Xue, B. Hof, E.B. Hannezo, C.-P.J. Heisenberg, Cell 177 (2019) 1463–1479.e18.","chicago":"Shamipour, Shayan, Roland Kardos, Shi-lei Xue, Björn Hof, Edouard B Hannezo, and Carl-Philipp J Heisenberg. “Bulk Actin Dynamics Drive Phase Segregation in Zebrafish Oocytes.” Cell. Elsevier, 2019. https://doi.org/10.1016/j.cell.2019.04.030."},"publication":"Cell","page":"1463-1479.e18","article_type":"original","date_published":"2019-05-30T00:00:00Z","type":"journal_article","issue":"6","abstract":[{"lang":"eng","text":"Segregation of maternal determinants within the oocyte constitutes the first step in embryo patterning. In zebrafish oocytes, extensive ooplasmic streaming leads to the segregation of ooplasm from yolk granules along the animal-vegetal axis of the oocyte. Here, we show that this process does not rely on cortical actin reorganization, as previously thought, but instead on a cell-cycle-dependent bulk actin polymerization wave traveling from the animal to the vegetal pole of the oocyte. This wave functions in segregation by both pulling ooplasm animally and pushing yolk granules vegetally. Using biophysical experimentation and theory, we show that ooplasm pulling is mediated by bulk actin network flows exerting friction forces on the ooplasm, while yolk granule pushing is achieved by a mechanism closely resembling actin comet formation on yolk granules. Our study defines a novel role of cell-cycle-controlled bulk actin polymerization waves in oocyte polarization via ooplasmic segregation."}],"user_id":"4359f0d1-fa6c-11eb-b949-802e58b17ae8","_id":"6508","intvolume":" 177","status":"public","title":"Bulk actin dynamics drive phase segregation in zebrafish oocytes","ddc":["570"],"file":[{"access_level":"open_access","file_name":"2019_Cell_Shamipour_accepted.pdf","file_size":3356292,"content_type":"application/pdf","creator":"dernst","relation":"main_file","file_id":"8686","checksum":"aea43726d80e35ce3885073a5f05c3e3","success":1,"date_created":"2020-10-21T07:22:34Z","date_updated":"2020-10-21T07:22:34Z"}],"oa_version":"Published Version"},{"related_material":{"record":[{"relation":"part_of_dissertation","status":"public","id":"7186"}]},"author":[{"full_name":"Schwayer, Cornelia","orcid":"0000-0001-5130-2226","id":"3436488C-F248-11E8-B48F-1D18A9856A87","last_name":"Schwayer","first_name":"Cornelia"},{"id":"2F74BCDE-F248-11E8-B48F-1D18A9856A87","first_name":"Mateusz K","last_name":"Sikora","full_name":"Sikora, Mateusz K"},{"full_name":"Slovakova, Jana","last_name":"Slovakova","first_name":"Jana","id":"30F3F2F0-F248-11E8-B48F-1D18A9856A87"},{"full_name":"Kardos, Roland","last_name":"Kardos","first_name":"Roland","id":"4039350E-F248-11E8-B48F-1D18A9856A87"},{"id":"39427864-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0002-0912-4566","first_name":"Carl-Philipp J","last_name":"Heisenberg","full_name":"Heisenberg, Carl-Philipp J"}],"volume":37,"oa_version":"None","date_updated":"2023-09-07T12:56:41Z","date_created":"2018-12-11T11:50:07Z","_id":"1096","year":"2016","user_id":"3E5EF7F0-F248-11E8-B48F-1D18A9856A87","department":[{"_id":"CaHe"}],"intvolume":" 37","publisher":"Cell Press","title":"Actin rings of power","publication_status":"published","status":"public","publist_id":"6279","issue":"6","type":"journal_article","doi":"10.1016/j.devcel.2016.05.024","date_published":"2016-06-20T00:00:00Z","language":[{"iso":"eng"}],"citation":{"chicago":"Schwayer, Cornelia, Mateusz K Sikora, Jana Slovakova, Roland Kardos, and Carl-Philipp J Heisenberg. “Actin Rings of Power.” Developmental Cell. Cell Press, 2016. https://doi.org/10.1016/j.devcel.2016.05.024.","mla":"Schwayer, Cornelia, et al. “Actin Rings of Power.” Developmental Cell, vol. 37, no. 6, Cell Press, 2016, pp. 493–506, doi:10.1016/j.devcel.2016.05.024.","short":"C. Schwayer, M.K. Sikora, J. Slovakova, R. Kardos, C.-P.J. Heisenberg, Developmental Cell 37 (2016) 493–506.","ista":"Schwayer C, Sikora MK, Slovakova J, Kardos R, Heisenberg C-PJ. 2016. Actin rings of power. Developmental Cell. 37(6), 493–506.","ieee":"C. Schwayer, M. K. Sikora, J. Slovakova, R. Kardos, and C.-P. J. Heisenberg, “Actin rings of power,” Developmental Cell, vol. 37, no. 6. Cell Press, pp. 493–506, 2016.","apa":"Schwayer, C., Sikora, M. K., Slovakova, J., Kardos, R., & Heisenberg, C.-P. J. (2016). Actin rings of power. Developmental Cell. Cell Press. https://doi.org/10.1016/j.devcel.2016.05.024","ama":"Schwayer C, Sikora MK, Slovakova J, Kardos R, Heisenberg C-PJ. Actin rings of power. Developmental Cell. 2016;37(6):493-506. doi:10.1016/j.devcel.2016.05.024"},"publication":"Developmental Cell","page":"493 - 506","quality_controlled":"1","day":"20","month":"06","scopus_import":1}]