Actomyosin meshwork mechanosensing enables tissue shape to orient cell force

Nature Communications
Soline ChanetAdam C Martin

Abstract

Sculpting organism shape requires that cells produce forces with proper directionality. Thus, it is critical to understand how cells orient the cytoskeleton to produce forces that deform tissues. During Drosophila gastrulation, actomyosin contraction in ventral cells generates a long, narrow epithelial furrow, termed the ventral furrow, in which actomyosin fibres and tension are directed along the length of the furrow. Using a combination of genetic and mechanical perturbations that alter tissue shape, we demonstrate that geometrical and mechanical constraints act as cues to orient the cytoskeleton and tension during ventral furrow formation. We developed an in silico model of two-dimensional actomyosin meshwork contraction, demonstrating that actomyosin meshworks exhibit an inherent force orienting mechanism in response to mechanical constraints. Together, our in vivo and in silico data provide a framework for understanding how cells orient force generation, establishing a role for geometrical and mechanical patterning of force production in tissues.

References

Dec 31, 2002·Development·Change TanNorbert Perrimon
Mar 14, 2003·Physical Review Letters·E Cerda, L Mahadevan
Oct 28, 2003·Nature Cell Biology·Claudia VeigelJohn Kendrick-Jones
Dec 5, 2003·Current Biology : CB·Petros LigoxygakisJean-Marc Reichhart
Mar 20, 2004·Developmental Cell·Jennifer A Zallen, Eric Wieschaus
Dec 20, 2005·European Journal of Cell Biology·Alexander D BershadskyMichael M Kozlov
Mar 22, 2006·Cell Motility and the Cytoskeleton·Manuel ThéryMichel Bornens
Jun 6, 2007·Proceedings of the National Academy of Sciences of the United States of America·Mihály KovácsJames R Sellers
Nov 26, 2008·Nature·Adam C MartinEric F Wieschaus
Oct 7, 2009·Proceedings of the National Academy of Sciences of the United States of America·Démosthène MitrossilisAtef Asnacios
Nov 13, 2009·Development·Ivana ViktorinováChristian Dahmann
Mar 3, 2010·The Journal of Cell Biology·Adam C MartinEric F Wieschaus
May 12, 2010·Journal of Physics. Condensed Matter : an Institute of Physics Journal·A ZemelS A Safran
May 14, 2010·Proceedings of the National Academy of Sciences of the United States of America·Zhijun LiuChristopher S Chen
Sep 14, 2010·Developmental Cell·Sérgio de Matos SimõesJennifer A Zallen
Nov 26, 2010·Nature Cell Biology·Li HeDenise J Montell
Aug 5, 2011·Nature·Thierry SavinClifford J Tabin
Feb 24, 2012·Journal of Cell Science·Timothée VignaudManuel Théry
Jun 9, 2012·Science·Anne-Cécile ReymannLaurent Blanchoin
Oct 3, 2012·Trends in Cell Biology·Timothée VignaudManuel Théry
Nov 9, 2012·Proceedings of the National Academy of Sciences of the United States of America·Michael A GelbartMatthias Kaschube
Mar 5, 2013·Nature Cell Biology·Chiharu HigashidaNaoki Watanabe
May 7, 2013·Differentiation; Research in Biological Diversity·Rashmi PriyaGuillermo A Gomez
May 28, 2013·Developmental Cell·Pierre-Luc BardetYohanns Bellaïche
Aug 31, 2013·Science·Amy E ShyerL Mahadevan
Sep 21, 2013·Nature Reviews. Genetics·Callie Johnson Miller, Lance A Davidson
Sep 26, 2013·PloS One·Philipp Spahn, Rolf Reuter
Nov 14, 2013·Science Signaling·Alyssa J ManningStephen L Rogers
Jan 11, 2014·Journal of Applied Physiology·Harikrishnan ParameswaranBéla Suki
Jun 11, 2014·Developmental Cell·Matthew R StachowiakBen O'Shaughnessy
Jul 10, 2014·Development·Victor D Varner, Celeste M Nelson
Aug 2, 2014·Progress in Molecular Biology and Translational Science·Soline Chanet, Adam C Martin
Aug 21, 2014·Biophysical Journal·Patrick W OakesMargaret L Gardel

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Citations

Jul 18, 2018·ELife·Yara E Sanchez-CorralesKatja Röper
Sep 1, 2018·Wiley Interdisciplinary Reviews. Developmental Biology·Hannah G Yevick, Adam C Martin
Sep 27, 2018·Journal of Cellular and Molecular Medicine·Gen ZhengJohn W Wiley
May 10, 2019·Cell Cycle·Tara M Finegan, Dan T Bergstralh
Nov 18, 2018·The EMBO Journal·Daniel KruegerStefano De Renzis
Aug 28, 2019·Nature Materials·Tom P J WyattGuillaume T Charras
Aug 25, 2020·Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences·Adam C Martin
Sep 12, 2018·Nature·Guy Blanchard
Apr 23, 2017·Development·Natalie C HeerAdam C Martin
Dec 1, 2017·Development·Natalie C Heer, Adam C Martin
May 12, 2018·Journal of Cell Science·Travis J ArmigerKris Noel Dahl
Sep 12, 2018·Nature Communications·Keisuke Ikawa, Kaoru Sugimura
Jul 22, 2018·Journal of Cell Science·Priyamvada Chugh, Ewa K Paluch
Aug 11, 2019·Development·Ramya BalajiAnne-Kathrin Classen
Mar 10, 2020·F1000Research·Ann Sutherland, Alyssa Lesko
Apr 15, 2020·Proceedings of the National Academy of Sciences of the United States of America·Jonathan FouchardGuillaume Charras
Sep 4, 2020·Development·Hui Miao, J Todd Blankenship
Jun 20, 2018·Nature Communications·Emiliano IzquierdoStefano De Renzis
Nov 19, 2017·Nature Communications·Gantas Perez-MockusFrançois Schweisguth
Dec 12, 2020·Journal of Cellular Physiology·Naruchit ThanuthanakhunMee-Hae Kim
May 4, 2018·Current Opinion in Cell Biology·Patrick W Oakes
Jun 12, 2018·Current Opinion in Cell Biology·Alişya A Anlaş, Celeste M Nelson
Mar 17, 2021·Soft Matter·Iaroslava GolovkovaLea-Laetitia Pontani
Mar 20, 2021·Frontiers in Cell and Developmental Biology·Anna PopkovaXiaobo Wang
Jul 3, 2020·Mechanisms of Development·Elham GheisariH-Arno J Müller
Dec 12, 2020·Wiley Interdisciplinary Reviews. Systems Biology and Medicine·Kathleen T DiNapoliPablo A Iglesias
Jun 8, 2021·Seminars in Cell & Developmental Biology·Giulia Paci, Yanlan Mao
Jul 7, 2021·PLoS Computational Biology·Michael C HolcombJerzy Blawzdziewicz
Jul 23, 2021·Biophysical Journal·R Marisol Herrera-PerezKaren E Kasza
Aug 28, 2021·The Journal of Cell Biology·Sourabh BhideMaria Leptin
Aug 20, 2021·Development·Mostafa Aakhte, Hans-Arno J Müller
Oct 14, 2021·Cell Reports·Vicki P Losick, Levi G Duhaime
Jun 2, 2021·Seminars in Cell & Developmental Biology·Yu-Chiun Wang
Jul 10, 2021·Seminars in Cell & Developmental Biology·Angus Inman, Michael Smutny
Dec 18, 2021·Development·Shari CarmonBen-Zion Shilo

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Methods Mentioned

BETA
Transgenic

Software Mentioned

MATLAB
Embryo Development Geometry Explorer ( EDGE )
EDGE
Zen
Fiji

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