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Actomyosin meshwork mechanosensing enables tissue shape to orient cell force

Author

Listed:
  • Soline Chanet

    (Massachusetts Institute of Technology)

  • Callie J. Miller

    (University of Pittsburgh)

  • Eeshit Dhaval Vaishnav

    (Massachusetts Institute of Technology)

  • Bard Ermentrout

    (University of Pittsburgh)

  • Lance A. Davidson

    (University of Pittsburgh
    University of Pittsburgh
    University of Pittsburgh)

  • Adam C. Martin

    (Massachusetts Institute of Technology)

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.

Suggested Citation

  • Soline Chanet & Callie J. Miller & Eeshit Dhaval Vaishnav & Bard Ermentrout & Lance A. Davidson & Adam C. Martin, 2017. "Actomyosin meshwork mechanosensing enables tissue shape to orient cell force," Nature Communications, Nature, vol. 8(1), pages 1-13, August.
  • Handle: RePEc:nat:natcom:v:8:y:2017:i:1:d:10.1038_ncomms15014
    DOI: 10.1038/ncomms15014
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    Cited by:

    1. Hannah J. Gustafson & Nikolas Claussen & Stefano Renzis & Sebastian J. Streichan, 2022. "Patterned mechanical feedback establishes a global myosin gradient," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    2. Miho Matsuda & Jan Rozman & Sassan Ostvar & Karen E. Kasza & Sergei Y. Sokol, 2023. "Mechanical control of neural plate folding by apical domain alteration," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    3. Kazunori Sunadome & Alek G. Erickson & Delf Kah & Ben Fabry & Csaba Adori & Polina Kameneva & Louis Faure & Shigeaki Kanatani & Marketa Kaucka & Ivar Dehnisch Ellström & Marketa Tesarova & Tomas Zikmu, 2023. "Directionality of developing skeletal muscles is set by mechanical forces," Nature Communications, Nature, vol. 14(1), pages 1-24, December.
    4. Aurélien Villedieu & Lale Alpar & Isabelle Gaugué & Amina Joudat & François Graner & Floris Bosveld & Yohanns Bellaïche, 2023. "Homeotic compartment curvature and tension control spatiotemporal folding dynamics," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    5. Ana Sousa-Ortega & Javier Vázquez-Marín & Estefanía Sanabria-Reinoso & Jorge Corbacho & Rocío Polvillo & Alejandro Campoy-López & Lorena Buono & Felix Loosli & María Almuedo-Castillo & Juan R. Martíne, 2023. "A Yap-dependent mechanoregulatory program sustains cell migration for embryo axis assembly," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    6. Julien Fierling & Alphy John & Barthélémy Delorme & Alexandre Torzynski & Guy B. Blanchard & Claire M. Lye & Anna Popkova & Grégoire Malandain & Bénédicte Sanson & Jocelyn Étienne & Philippe Marmottan, 2022. "Embryo-scale epithelial buckling forms a propagating furrow that initiates gastrulation," Nature Communications, Nature, vol. 13(1), pages 1-14, December.

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