1. Cell Biology
  2. Physics of Living Systems

A mechanosensing mechanism controls plasma membrane shape homeostasis at the nanoscale

  1. Xarxa Quiroga
  2. Nikhil Walani
  3. Andrea Disanza
  4. Albert Chavero
  5. Alexandra Mittens
  6. Francesc Tebar
  7. Xavier Trepat
  8. Robert G Parton
  9. María Isabel Geli
  10. Giorgio Scita
  11. Marino Arroyo
  12. Anabel-Lise Le Roux  Is a corresponding author
  13. Pere Roca-Cusachs  Is a corresponding author
  1. Barcelona Institute for Science and Technology, Spain
  2. Indian Institute of Technology Delhi, India
  3. AIRC Institute of Molecular Oncology, Italy
  4. Universitat de Barcelona, Spain
  5. University of Queensland, Australia
  6. Institute for Molecular Biology of Barcelona, Spain
  7. Universitat Politècnica de Catalunya, Spain
https://doi.org/10.7554/eLife.72316
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Cite this article
  1. Xarxa Quiroga
  2. Nikhil Walani
  3. Andrea Disanza
  4. Albert Chavero
  5. Alexandra Mittens
  6. Francesc Tebar
  7. Xavier Trepat
  8. Robert G Parton
  9. María Isabel Geli
  10. Giorgio Scita
  11. Marino Arroyo
  12. Anabel-Lise Le Roux
  13. Pere Roca-Cusachs
(2023)
A mechanosensing mechanism controls plasma membrane shape homeostasis at the nanoscale
eLife 12:e72316.
https://doi.org/10.7554/eLife.72316
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  3. Download .RIS

Abstract

As cells migrate and experience forces from their surroundings, they constantly undergo mechanical deformations which reshape their plasma membrane (PM). To maintain homeostasis, cells need to detect and restore such changes, not only in terms of overall PM area and tension as previously described, but also in terms of local, nano-scale topography. Here we describe a novel phenomenon, by which cells sense and restore mechanically induced PM nano-scale deformations. We show that cell stretch and subsequent compression reshape the PM in a way that generates local membrane evaginations in the 100 nm scale. These evaginations are recognized by I-BAR proteins, which triggers a burst of actin polymerization mediated by Rac1 and Arp2/3. The actin polymerization burst subsequently re-flattens the evagination, completing the mechanochemical feedback loop. Our results demonstrate a new mechanosensing mechanism for PM shape homeostasis, with potential applicability in different physiological scenarios.

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Source data is provided for all figures in a corresponding source data file.

Article and author information

Author details

  1. Xarxa Quiroga

    Institute for Bioengineering of Catalonia, Barcelona Institute for Science and Technology, Barcelona, Spain
    Competing interests
    No competing interests declared.

  2. Nikhil Walani

    Department of Applied Mechanics, Indian Institute of Technology Delhi, Delhi, India
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5248-9181

  3. Andrea Disanza

    IFOM Foundation, AIRC Institute of Molecular Oncology, Milan, Italy
    Competing interests
    No competing interests declared.

  4. Albert Chavero

    Departament de Biomedicina, Universitat de Barcelona, Barcelona, Spain
    Competing interests
    No competing interests declared.

  5. Alexandra Mittens

    Institute for Bioengineering of Catalonia, Barcelona Institute for Science and Technology, Barcelona, Spain
    Competing interests
    No competing interests declared.

  6. Francesc Tebar

    Departament de Biomedicina, Universitat de Barcelona, Barcelona, Spain
    Competing interests
    No competing interests declared.

  7. Xavier Trepat

    Institute for Bioengineering of Catalonia, Barcelona Institute for Science and Technology, Barcelona, Spain
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7621-5214

  8. Robert G Parton

    Institute for Molecular Bioscience, University of Queensland, Brisbane, Australia
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7494-5248

  9. María Isabel Geli

    Institute for Molecular Biology of Barcelona, Barcelona, Spain
    Competing interests
    María Isabel Geli, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3452-6700

  10. Giorgio Scita

    IFOM Foundation, AIRC Institute of Molecular Oncology, Milan, Italy
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7984-1889

  11. Marino Arroyo

    Universitat Politècnica de Catalunya, Barcelona, Spain
    Competing interests
    No competing interests declared.

  12. Anabel-Lise Le Roux

    Institute for Bioengineering of Catalonia, Barcelona Institute for Science and Technology, Barcelona, Spain
    For correspondence
    aleroux@ibecbarcelona.eu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4152-5658

  13. Pere Roca-Cusachs

    Institute for Bioengineering of Catalonia, Barcelona Institute for Science and Technology, Barcelona, Spain
    For correspondence
    proca@ibecbarcelona.eu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6947-961X

Funding

Ministerio de Ciencia e Innovación (PID2019-110298GB-I00)

  • Pere Roca-Cusachs

Institució Catalana de Recerca i Estudis Avançats (ICREA Acadèmia Prize)

  • Marino Arroyo
  • Pere Roca-Cusachs

Ministerio de Ciencia e Innovación (PGC2018-099645-B-I00)

  • Xavier Trepat

Ministerio de Ciencia e Innovación (BFU2016-79916-P)

  • Xarxa Quiroga

European Commission (H2020-FETPROACT-01-2016-731957)

  • Xavier Trepat
  • Marino Arroyo
  • Pere Roca-Cusachs

Generalitat de Catalunya (2021 SGR 01425)

  • Xavier Trepat
  • Pere Roca-Cusachs

Fundació la Marató de TV3 (201936-30-31)

  • Pere Roca-Cusachs

'la Caixa' Foundation (LCF/PR/HR20/52400004)

  • Pere Roca-Cusachs

Ministerio de Ciencia e Innovación (BFU2015-66785-P)

  • Francesc Tebar

Associazione Italiana per la Ricerca sul Cancro (AIRC-IG 18621 and 1311 5XMille22759)

  • Giorgio Scita

italian ministry of university (PRIN 2017-Prot. 1313 2017HWTP2K)

  • Giorgio Scita

European Research Council (Adv-883739)

  • Xavier Trepat

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

Copyright

© 2023, Quiroga 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. Xarxa Quiroga
  2. Nikhil Walani
  3. Andrea Disanza
  4. Albert Chavero
  5. Alexandra Mittens
  6. Francesc Tebar
  7. Xavier Trepat
  8. Robert G Parton
  9. María Isabel Geli
  10. Giorgio Scita
  11. Marino Arroyo
  12. Anabel-Lise Le Roux
  13. Pere Roca-Cusachs
(2023)
A mechanosensing mechanism controls plasma membrane shape homeostasis at the nanoscale
eLife 12:e72316.
https://doi.org/10.7554/eLife.72316

Share this article

https://doi.org/10.7554/eLife.72316

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