A mechano-osmotic feedback couples cell volume to the rate of cell deformation

  1. Larisa Venkova
  2. Amit Singh Vishen
  3. Sergio Lembo
  4. Nishit Srivastava
  5. Baptiste Duchamp
  6. Artur Ruppel
  7. Alice Williart
  8. Stéphane Vassilopoulos
  9. Alexandre Deslys
  10. Juan-Manuel Garcia Arcos
  11. Alba Diz-Muñoz
  12. Martial Balland
  13. Jean-François Joanny
  14. Damien Cuvelier
  15. Pierre Sens  Is a corresponding author
  16. Matthieu Piel  Is a corresponding author
  1. Institut Curie, CNRS, UMR 144, France
  2. European Molecular Biology Laboratory, Germany
  3. Laboratoire Interdisciplinaire de Physique, France
  4. Sorbonne Université, INSERM, France
  5. Institut Curie, CNRS UMR168, France

Abstract

Mechanics has been a central focus of physical biology in the past decade. In comparison, how cells manage their size is less understood. Here we show that a parameter central to both the physics and the physiology of the cell, its volume, depends on a mechano-osmotic coupling. We found that cells change their volume depending on the rate at which they change shape, when they spontaneously spread are externally deformed. Cells undergo slow deformation at constant volume, while fast deformation leads to volume loss. We propose a mechano-sensitive pump and leak model to explain this phenomenon. Our model and experiments suggest that volume modulation depends on the state of the actin cortex and the coupling of ion fluxes to membrane tension. This mechano-osmotic coupling defines a membrane tension homeostasis module constantly at work in cells, causing volume fluctuations associated with fast cell shape changes, with potential consequences on cellular physiology.

Data availability

All data generated or analysed during this study are included in themanuscript and supporting file; all the raw analysed data shown in thefigure panels in the article are available in the accompanying SourceData files

Article and author information

Author details

  1. Larisa Venkova

    PSL Research University, Institut Curie, CNRS, UMR 144, Paris, France
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5721-7962
  2. Amit Singh Vishen

    PSL Research University, Institut Curie, CNRS, UMR 144, Paris, France
    Competing interests
    No competing interests declared.
  3. Sergio Lembo

    Cell Biology and Biophysics Unit, European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2253-8771
  4. Nishit Srivastava

    PSL Research University, Institut Curie, CNRS, UMR 144, Paris, France
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4177-6123
  5. Baptiste Duchamp

    PSL Research University, Institut Curie, CNRS, UMR 144, Paris, France
    Competing interests
    No competing interests declared.
  6. Artur Ruppel

    Laboratoire Interdisciplinaire de Physique, Grenoble, France
    Competing interests
    No competing interests declared.
  7. Alice Williart

    PSL Research University, Institut Curie, CNRS, UMR 144, Paris, France
    Competing interests
    No competing interests declared.
  8. Stéphane Vassilopoulos

    Sorbonne Université, INSERM, Paris, France
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0172-330X
  9. Alexandre Deslys

    PSL Research University, Institut Curie, CNRS, UMR 144, Paris, France
    Competing interests
    No competing interests declared.
  10. Juan-Manuel Garcia Arcos

    PSL Research University, Institut Curie, CNRS, UMR 144, Paris, France
    Competing interests
    No competing interests declared.
  11. Alba Diz-Muñoz

    Cell Biology and Biophysics Unit, European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6864-8901
  12. Martial Balland

    Laboratoire Interdisciplinaire de Physique, Grenoble, France
    Competing interests
    No competing interests declared.
  13. Jean-François Joanny

    PSL Research University, Institut Curie, CNRS UMR168, Paris, France
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6966-3222
  14. Damien Cuvelier

    PSL Research University, Institut Curie, CNRS, UMR 144, Paris, France
    Competing interests
    No competing interests declared.
  15. Pierre Sens

    Laboratoire Physico Chimie Curie, Institut Curie, CNRS UMR168, Paris, France
    For correspondence
    pierre.sens@curie.fr
    Competing interests
    Pierre Sens, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4523-3791
  16. Matthieu Piel

    PSL Research University, Institut Curie, CNRS, UMR 144, Paris, France
    For correspondence
    matthieu.piel@curie.fr
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2848-177X

Funding

Agence Nationale de la Recherche (ANR-19-CE13-0030)

  • Matthieu Piel

Agence Nationale de la Recherche (ANR-10-EQPX-34)

  • Matthieu Piel

Agence Nationale de la Recherche (ANR-10-IDEX-0001-02 PSL)

  • Matthieu Piel

Agence Nationale de la Recherche (ANR-10-LABX-31)

  • Matthieu Piel

Fondation pour la Recherche Médicale (FDT201805005592)

  • Larisa Venkova

Human Frontier Science Program (LT000305/2018-L)

  • Nishit Srivastava

Agence Nationale de la Recherche (ANR‐17‐CE13‐0020‐02)

  • Amit Singh Vishen

European Union's Horizon 2020 research and innovation programme (Marie Sklodowska-Curie grant agreement no. 641639)

  • Larisa Venkova

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

Reviewing Editor

  1. Felix Campelo, Institute of Photonic Sciences, Spain

Publication history

  1. Preprint posted: June 8, 2021 (view preprint)
  2. Received: July 21, 2021
  3. Accepted: April 8, 2022
  4. Accepted Manuscript published: April 13, 2022 (version 1)
  5. Version of Record published: May 10, 2022 (version 2)

Copyright

© 2022, Venkova 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. Larisa Venkova
  2. Amit Singh Vishen
  3. Sergio Lembo
  4. Nishit Srivastava
  5. Baptiste Duchamp
  6. Artur Ruppel
  7. Alice Williart
  8. Stéphane Vassilopoulos
  9. Alexandre Deslys
  10. Juan-Manuel Garcia Arcos
  11. Alba Diz-Muñoz
  12. Martial Balland
  13. Jean-François Joanny
  14. Damien Cuvelier
  15. Pierre Sens
  16. Matthieu Piel
(2022)
A mechano-osmotic feedback couples cell volume to the rate of cell deformation
eLife 11:e72381.
https://doi.org/10.7554/eLife.72381

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