The interplay of stiffness and force anisotropies drive embryo elongation

  1. Thanh Thi Kim Vuong-Brender  Is a corresponding author
  2. Martine Ben Amar
  3. Julien Pontabry
  4. Michel Labouesse  Is a corresponding author
  1. Sorbonne Universités, UPMC Univ Paris 06, CNRS, France
  2. Ecole Normale Supérieure, UPMC Université Pierre et Marie Curie, Université Paris Diderot, CNRS, France
  3. Institute of Epigenetics and Stem Cells, Germany

Abstract

The morphogenesis of tissues, like the deformation of an object, results from the interplay between their material properties and the mechanical forces exerted on them. Whereas the importance of mechanical forces in influencing cell behaviour is widely recognized, the importance of tissue material properties, in particular stiffness, has received much less attention. Using C. elegans as a model, we examine how both aspects contribute to embryonic elongation. Measuring the opening shape of the epidermal actin cortex after laser nano-ablation, we assess the spatiotemporal changes of actomyosin-dependent force and stiffness along the antero-posterior and dorso-ventral axis. Experimental data and analytical modelling show that myosin II-dependent force anisotropy within the lateral epidermis, and stiffness anisotropy within the fiber-reinforced dorso-ventral epidermis are critical to drive embryonic elongation. Together, our results establish a quantitative link between cortical tension, material properties and morphogenesis of an entire embryo.

Article and author information

Author details

  1. Thanh Thi Kim Vuong-Brender

    Laboratoire de Biologie du Développement - Institut de Biologie Paris-Seine, Sorbonne Universités, UPMC Univ Paris 06, CNRS, Paris, France
    For correspondence
    vuongthikimthanh@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6594-2881
  2. Martine Ben Amar

    Laboratoire de Physique Statistique, Ecole Normale Supérieure, UPMC Université Pierre et Marie Curie, Université Paris Diderot, CNRS, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Julien Pontabry

    Helmholtz Zentrum, Institute of Epigenetics and Stem Cells, München, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Michel Labouesse

    Laboratoire de Biologie du Développement - Institut de Biologie Paris-Seine, Sorbonne Universités, UPMC Univ Paris 06, CNRS, Paris, France
    For correspondence
    michel.labouesse@upmc.fr
    Competing interests
    The authors declare that no competing interests exist.

Funding

European Research Council (#294744)

  • Michel Labouesse

Centre National de la Recherche Scientifique (ANR-10-LABX-0030-INRT)

  • Michel Labouesse

Université de Strasbourg (ANR-10-IDEX-0002-02)

  • Michel Labouesse

Université Pierre et Marie Curie (ANR-10-LABX-0030-INRT)

  • Michel Labouesse

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. K VijayRaghavan, National Centre for Biological Sciences, Tata Institute of Fundamental Research, India

Version history

  1. Received: December 2, 2016
  2. Accepted: January 27, 2017
  3. Accepted Manuscript published: February 9, 2017 (version 1)
  4. Accepted Manuscript updated: February 15, 2017 (version 2)
  5. Version of Record published: March 29, 2017 (version 3)

Copyright

© 2017, Vuong-Brender et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Thanh Thi Kim Vuong-Brender
  2. Martine Ben Amar
  3. Julien Pontabry
  4. Michel Labouesse
(2017)
The interplay of stiffness and force anisotropies drive embryo elongation
eLife 6:e23866.
https://doi.org/10.7554/eLife.23866

Share this article

https://doi.org/10.7554/eLife.23866

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