Roadmap for the multiscale coupling of biochemical and mechanical signals during development

Lenne PF, Munro E, Heemskerk I, Warmflash A, Bocanegra L, Kishi K, Kicheva A, Long Y, Fruleux A, Boudaoud A, Saunders TE, Caldarelli P, Michaut A, Gros J, Maroudas-Sacks Y, Keren K, Hannezo EB, Gartner ZJ, Stormo B, Gladfelter A, Rodrigues A, Shyer A, Minc N, Maître JL, Di Talia S, Khamaisi B, Sprinzak D, Tlili S. 2021. Roadmap for the multiscale coupling of biochemical and mechanical signals during development. Physical biology. 18(4), 041501.

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Author
Lenne, Pierre François; Munro, Edwin; Heemskerk, Idse; Warmflash, Aryeh; Bocanegra, LauraIST Austria; Kishi, KasumiIST Austria; Kicheva, AnnaIST Austria ; Long, Yuchen; Fruleux, Antoine; Boudaoud, Arezki; Saunders, Timothy E.; Caldarelli, Paolo
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Abstract
The way in which interactions between mechanics and biochemistry lead to the emergence of complex cell and tissue organization is an old question that has recently attracted renewed interest from biologists, physicists, mathematicians and computer scientists. Rapid advances in optical physics, microscopy and computational image analysis have greatly enhanced our ability to observe and quantify spatiotemporal patterns of signalling, force generation, deformation, and flow in living cells and tissues. Powerful new tools for genetic, biophysical and optogenetic manipulation are allowing us to perturb the underlying machinery that generates these patterns in increasingly sophisticated ways. Rapid advances in theory and computing have made it possible to construct predictive models that describe how cell and tissue organization and dynamics emerge from the local coupling of biochemistry and mechanics. Together, these advances have opened up a wealth of new opportunities to explore how mechanochemical patterning shapes organismal development. In this roadmap, we present a series of forward-looking case studies on mechanochemical patterning in development, written by scientists working at the interface between the physical and biological sciences, and covering a wide range of spatial and temporal scales, organisms, and modes of development. Together, these contributions highlight the many ways in which the dynamic coupling of mechanics and biochemistry shapes biological dynamics: from mechanoenzymes that sense force to tune their activity and motor output, to collectives of cells in tissues that flow and redistribute biochemical signals during development.
Publishing Year
Date Published
2021-04-14
Journal Title
Physical biology
Acknowledgement
The AK group is supported by IST Austria and by the ERC under European Union Horizon 2020 research and innovation programme Grant 680037. Apologies to those whose work could not be mentioned due to limited space. We thank all my lab members, both past and present, for stimulating discussion. This work was funded by a Singapore Ministry of Education Tier 3 Grant, MOE2016-T3-1-005. We thank Francis Corson for continuous discussion and collaboration contributing to these views and for figure 4(A). PC is sponsored by the Institut Pasteur and the European Union's Horizon 2020 research and innovation programme under the Marie Sklodowska-Curie Grant Agreement No. 665807. Research in JG's laboratory is funded by the European Research Council under the European Union's Seventh Framework Programme (FP7/2007-2013)/ERC Grant Agreement No. 337635, Institut Pasteur, CNRS, Cercle FSER, Fondation pour la Recherche Medicale, the Vallee Foundation and the ANR-19-CE-13-0024 Grant. We thank Erez Braun and Alex Mogilner for comments on the manuscript and Niv Ierushalmi for help with figure 5. This project has received funding from the European Union's Horizon 2020 research and innovation programme under Grant Agreement No. ERC-2018-COG Grant 819174-HydraMechanics awarded to KK. EH thanks all lab members, as well as Pierre Recho, Tsuyoshi Hirashima, Diana Pinheiro and Carl-Philip Heisenberg, for fruitful discussions on these topics—and apologize for not being able to cite many very relevant publications due to the strict 10-reference limit. EH acknowledges the support of Austrian Science Fund (FWF) (P 31639) and the European Research Council under the European Union's Horizon 2020 Research and Innovation Programme Grant Agreements (851288). The authors acknowledge the inspiring scientists whose work could not be cited in this perspective due to space constraints; the members of the Gartner Lab for helpful discussions; the Barbara and Gerson Bakar Foundation, the Chan Zuckerberg Biohub Investigators Programme, the National Institute of Health, and the Centre for Cellular Construction, an NSF Science and Technology Centre. The Minc laboratory is currently funded by the CNRS and the European Research Council (CoG Forcaster No. 647073). Research in the lab of J-LM is supported by the Institut Curie, the Centre National de la Recherche Scientifique (CNRS), the Institut National de la Santé Et de la Recherche Médicale (INSERM), and is funded by grants from the ATIP-Avenir programme, the Fondation Schlumberger pour l'Éducation et la Recherche via the Fondation pour la Recherche Médicale, the European Research Council Starting Grant ERC-2017-StG 757557, the European Molecular Biology Organization Young Investigator programme (EMBO YIP), the INSERM transversal programme Human Development Cell Atlas (HuDeCA), Paris Sciences Lettres (PSL) 'nouvelle équipe' and QLife (17-CONV-0005) grants and Labex DEEP (ANR-11-LABX-0044) which are part of the IDEX PSL (ANR-10-IDEX-0001-02). We acknowledge useful discussions with Massimo Vergassola, Sebastian Streichan and my lab members. Work in my laboratory on Drosophila embryogenesis is partly supported by NIH-R01GM122936. The authors acknowledge the support by a grant from the European Research Council (Grant No. 682161). Lenne group is funded by a grant from the 'Investissements d'Avenir' French Government programme managed by the French National Research Agency (ANR-16-CONV-0001) and by the Excellence Initiative of Aix-Marseille University—A*MIDEX, and ANR projects MechaResp (ANR-17-CE13-0032) and AdGastrulo (ANR-19-CE13-0022).
Volume
18
Issue
4
Article Number
041501
eISSN
IST-REx-ID

Cite this

Lenne PF, Munro E, Heemskerk I, et al. Roadmap for the multiscale coupling of biochemical and mechanical signals during development. Physical biology. 2021;18(4). doi:10.1088/1478-3975/abd0db
Lenne, P. F., Munro, E., Heemskerk, I., Warmflash, A., Bocanegra, L., Kishi, K., … Tlili, S. (2021). Roadmap for the multiscale coupling of biochemical and mechanical signals during development. Physical Biology. IOP Publishing. https://doi.org/10.1088/1478-3975/abd0db
Lenne, Pierre François, Edwin Munro, Idse Heemskerk, Aryeh Warmflash, Laura Bocanegra, Kasumi Kishi, Anna Kicheva, et al. “Roadmap for the Multiscale Coupling of Biochemical and Mechanical Signals during Development.” Physical Biology. IOP Publishing, 2021. https://doi.org/10.1088/1478-3975/abd0db.
P. F. Lenne et al., “Roadmap for the multiscale coupling of biochemical and mechanical signals during development,” Physical biology, vol. 18, no. 4. IOP Publishing, 2021.
Lenne PF, Munro E, Heemskerk I, Warmflash A, Bocanegra L, Kishi K, Kicheva A, Long Y, Fruleux A, Boudaoud A, Saunders TE, Caldarelli P, Michaut A, Gros J, Maroudas-Sacks Y, Keren K, Hannezo EB, Gartner ZJ, Stormo B, Gladfelter A, Rodrigues A, Shyer A, Minc N, Maître JL, Di Talia S, Khamaisi B, Sprinzak D, Tlili S. 2021. Roadmap for the multiscale coupling of biochemical and mechanical signals during development. Physical biology. 18(4), 041501.
Lenne, Pierre François, et al. “Roadmap for the Multiscale Coupling of Biochemical and Mechanical Signals during Development.” Physical Biology, vol. 18, no. 4, 041501, IOP Publishing, 2021, doi:10.1088/1478-3975/abd0db.
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