Extra-cellular matrix in multicellular aggregates acts as a pressure sensor controlling cell proliferation and motility

  1. Monika E Dolega
  2. Sylvain Monnier
  3. Benjamin Brunel
  4. Jean-François Joanny
  5. Pierre Recho  Is a corresponding author
  6. Giovanni Cappello  Is a corresponding author
  1. Université Grenoble Alpes, France
  2. Université Claude Bernard Lyon 1, CNRS, France
  3. Collège de France, France
  4. Institut Curie, France

Abstract

Imposed deformations play an important role in morphogenesis and tissue homeostasis, both in normal and pathological conditions. To perceive mechanical perturbations of different types and magnitudes, tissues need appropriate detectors, with a compliance that matches the perturbation amplitude. By comparing results of selective osmotic compressions of CT26 cells within multicellular aggregates and global aggregate compressions, we show that global compressions have a strong impact on the aggregates growth and internal cell motility, while selective compressions of same magnitude have almost no effect. Both compressions alter the volume of individual cells in the same way over a shor-timescale, but, by draining the water out of the extracellular matrix, the global one imposes a residual compressive mechanical stress on the cells over a long-timescale, while the selective one does not. We conclude that the extracellular matrix is as a sensor that mechanically regulates cell proliferation and migration in a 3D environment.

Data availability

Data concerning figures 2, 3, 4, 5 and appendix B are available at the following URL: https://osf.io/n6ra2/?view_only=059da2ebcd064b75bd12c0c2008b9a6a

The following data sets were generated

Article and author information

Author details

  1. Monika E Dolega

    Physics, Université Grenoble Alpes, St. Martin d'Hères, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Sylvain Monnier

    Institut Lumière Matière, Université Claude Bernard Lyon 1, CNRS, F-69622 VILLEURBANNE, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Benjamin Brunel

    Physics, Université Grenoble Alpes, St. Martin d'Hères, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2858-5074
  4. Jean-François Joanny

    PSL Research University, Collège de France, 75005 Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Pierre Recho

    Department of Physico-Chemistry of Living Matter, Institut Curie, Paris, France
    For correspondence
    pierre.recho@univ-grenoble-alpes.fr
    Competing interests
    The authors declare that no competing interests exist.
  6. Giovanni Cappello

    Physics, Université Grenoble Alpes, St. Martin d'Hères, France
    For correspondence
    giovanni.cappello@univ-grenoble-alpes.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5012-367X

Funding

Agence Nationale de la Recherche (ANR-13-BSV5-0008-01)

  • Giovanni Cappello

Centre National de la Recherche Scientifique (MechanoBio 2018)

  • Giovanni Cappello

Ligue Contre le Cancer

  • Sylvain Monnier

Institut National de la Santé et de la Recherche Médicale (PC201407)

  • Giovanni Cappello

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

Reviewing Editor

  1. Chase P. Broedersz, Arnold Sommerfeld Center for Theoretical Physics, LMU Munich, Germany

Version history

  1. Received: September 19, 2020
  2. Accepted: March 8, 2021
  3. Accepted Manuscript published: March 11, 2021 (version 1)
  4. Version of Record published: April 23, 2021 (version 2)

Copyright

© 2021, Dolega 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. Monika E Dolega
  2. Sylvain Monnier
  3. Benjamin Brunel
  4. Jean-François Joanny
  5. Pierre Recho
  6. Giovanni Cappello
(2021)
Extra-cellular matrix in multicellular aggregates acts as a pressure sensor controlling cell proliferation and motility
eLife 10:e63258.
https://doi.org/10.7554/eLife.63258

Share this article

https://doi.org/10.7554/eLife.63258

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