1. Physics of Living Systems

Epithelial colonies in vitro elongate through collective effects

  1. Jordi Comelles
  2. Soumya S S
  3. Linjie Lu
  4. Emilie Le-Maout
  5. Sudakar Anvitha
  6. Guillaume Salbreux
  7. Frank Jülicher
  8. Mandar M Inamdar  Is a corresponding author
  9. Daniel Riveline  Is a corresponding author
  1. Laboratory of Cell Physics ISIS/IGBMC, CNRS and University of Strasbourg, France
  2. Indian Institute of Technology Bombay, India
  3. The Francis Crick Institute, United Kingdom
  4. Max Planck Institute for the Physics of Complex Systems, Germany
https://doi.org/10.7554/eLife.57730
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  1. Jordi Comelles
  2. Soumya S S
  3. Linjie Lu
  4. Emilie Le-Maout
  5. Sudakar Anvitha
  6. Guillaume Salbreux
  7. Frank Jülicher
  8. Mandar M Inamdar
  9. Daniel Riveline
(2021)
Epithelial colonies in vitro elongate through collective effects
eLife 10:e57730.
https://doi.org/10.7554/eLife.57730
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Abstract

Epithelial tissues of the developing embryos elongate by different mechanisms, such as neighbor exchange, cell elongation, and oriented cell division. Since autonomous tissue self-organization is influenced by external cues such as morphogen gradients or neighboring tissues, it is difficult to distinguish intrinsic from directed tissue behavior. The mesoscopic processes leading to the different mechanisms remain elusive. Here, we study the spontaneous elongation behavior of spreading circular epithelial colonies in vitro. By quantifying deformation kinematics at multiple scales, we report that global elongation happens primarily due to cell elongations, and its direction correlates with the anisotropy of the average cell elongation. By imposing an external time-periodic stretch, the axis of this global symmetry breaking can be modified and elongation occurs primarily due to orientated neighbor exchange. These different behaviors are confirmed using a vertex model for collective cell behavior, providing a framework for understanding autonomous tissue elongation and its origins.

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All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Jordi Comelles

    Development and stem cells, Laboratory of Cell Physics ISIS/IGBMC, CNRS and University of Strasbourg, Illkirch CEDEX, France
    Competing interests
    The authors declare that no competing interests exist.

  2. Soumya S S

    Department of Civil Engineering, Indian Institute of Technology Bombay, Mumbai, India
    Competing interests
    The authors declare that no competing interests exist.

  3. Linjie Lu

    Development and stem cells, Laboratory of Cell Physics ISIS/IGBMC, CNRS and University of Strasbourg, Illkirch CEDEX, France
    Competing interests
    The authors declare that no competing interests exist.

  4. Emilie Le-Maout

    Development and stem cells, Laboratory of Cell Physics ISIS/IGBMC, CNRS and University of Strasbourg, Illkirch CEDEX, France
    Competing interests
    The authors declare that no competing interests exist.

  5. Sudakar Anvitha

    Department of Mechanical Engineering, Indian Institute of Technology Bombay, Mumbai, India
    Competing interests
    The authors declare that no competing interests exist.

  6. Guillaume Salbreux

    Theoretical Physics of Biology, The Francis Crick Institute, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7041-1292

  7. Frank Jülicher

    Max Planck Institute for the Physics of Complex Systems, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4731-9185

  8. Mandar M Inamdar

    Department of Civil Engineering, Indian Institute of Technology Bombay, Mumbai, India
    For correspondence
    minamdar@iitb.ac.in
    Competing interests
    The authors declare that no competing interests exist.

  9. Daniel Riveline

    Development and stem cells, Laboratory of Cell Physics ISIS/IGBMC, CNRS and University of Strasbourg, Illkirch CEDEX, France
    For correspondence
    riveline@unistra.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4632-011X

Funding

Department of Biotechnology, Ministry of Science and Technology, India (BT/06/IYBA/2012)

  • Mandar M Inamdar

Cancer Research UK (FC001317)

  • Guillaume Salbreux

Medical Research Council (FC001317)

  • Guillaume Salbreux

Wellcome Trust (FC001317)

  • Guillaume Salbreux

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

  • Guillaume Salbreux
  • Daniel Riveline

Agence Nationale de la Recherche (ANR-10-IDEX-0002-02)

  • Daniel Riveline

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

Reviewing Editor

  1. Irene Giardina, Università Sapienza, Italy

Version history

  1. Received: April 9, 2020
  2. Accepted: December 31, 2020
  3. Accepted Manuscript published: January 4, 2021 (version 1)
  4. Version of Record published: February 1, 2021 (version 2)

Copyright

© 2021, Comelles 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. Jordi Comelles
  2. Soumya S S
  3. Linjie Lu
  4. Emilie Le-Maout
  5. Sudakar Anvitha
  6. Guillaume Salbreux
  7. Frank Jülicher
  8. Mandar M Inamdar
  9. Daniel Riveline
(2021)
Epithelial colonies in vitro elongate through collective effects
eLife 10:e57730.
https://doi.org/10.7554/eLife.57730

Share this article

https://doi.org/10.7554/eLife.57730

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