Myosin II isoforms play distinct roles in adherens junction biogenesis

  1. Mélina L Heuze  Is a corresponding author
  2. Gautham Sankara
  3. Joseph D'Alessandro
  4. Victor Cellerin
  5. Tien Dang
  6. David S Williams
  7. Jan CM Van Hest
  8. Philippe Marcq
  9. René-Marc Mège  Is a corresponding author
  10. Benoit Ladoux  Is a corresponding author
  1. CNRS, France
  2. Swansea University, United Kingdom
  3. Eindhoven University of Technology, Netherlands
  4. Sorbonne Université, France

Abstract

Adherens junction (AJ) assembly under force is essential for many biological processes like epithelial monolayer bending, collective cell migration, cell extrusion and wound healing. The acto-myosin cytoskeleton acts as a major force-generator during the de novo formation and remodelling of AJ. Here, we investigated the role of myosinII isoforms in epithelial junction assembly. Myosin IIA (NMIIA) and Myosin IIB (NMIIB) differentially regulate biogenesis of adherens junction through association with distinct actin networks. Analysis of junction dynamics, actin organization, and mechanical forces of control and knockdown cells for myosins revealed that NMIIA provides the mechanical tugging force necessary for cell-cell junction reinforcement and maintenance. NMIIB is involved in E-cadherin clustering, maintenance of a branched actin layer connecting E-cadherin complexes and perijunctional actin fibres leading to the building-up of anisotropic stress. These data reveal unanticipated complementary functions of NMIIA and NMIIB in the biogenesis and integrity of AJ.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for the main figures and figure supplements.

Article and author information

Author details

  1. Mélina L Heuze

    Institut Jacques Monod, CNRS, Paris, France
    For correspondence
    melina.heuze@ijm.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4271-2706
  2. Gautham Sankara

    Institut Jacques Monod, CNRS, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Joseph D'Alessandro

    Institut Jacques Monod, CNRS, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1585-3255
  4. Victor Cellerin

    Institut Jacques Monod, CNRS, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Tien Dang

    Institut Jacques Monod, CNRS, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  6. David S Williams

    Department of Chemistry, Swansea University, Swansea, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  7. Jan CM Van Hest

    Biomedical Engineering, Eindhoven University of Technology, Eindhoven, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  8. Philippe Marcq

    Laboratoire Physique et Mécanique des Milieux Hétérogènes, Sorbonne Université, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  9. René-Marc Mège

    Institut Jacques Monod, CNRS, Paris, France
    For correspondence
    rene-marc.mege@ijm.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8128-5543
  10. Benoit Ladoux

    Institut Jacques Monod, CNRS, Paris, France
    For correspondence
    benoit.ladoux@ijm.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2086-1556

Funding

Seventh Framework Programme (CoG-617233)

  • Benoit Ladoux

Agence Nationale de la Recherche (ANR-17-CE13-0013)

  • René-Marc Mège

Agence Nationale de la Recherche (ANR-10-INBS-04)

  • René-Marc Mège
  • Benoit Ladoux

Agence Nationale de la Recherche (ANR‐11‐LABX‐0071)

  • René-Marc Mège
  • Benoit Ladoux

Agence Nationale de la Recherche (ANR-11-LABX-0071)

  • Benoit Ladoux

Agence Nationale de la Recherche (ANR-17-CE13-0012)

  • Benoit Ladoux

Ligue Contre le Cancer (Equipe Labellisée)

  • René-Marc Mège

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

Reviewing Editor

  1. William I Weis, Stanford University School of Medicine, United States

Version history

  1. Received: March 6, 2019
  2. Accepted: September 5, 2019
  3. Accepted Manuscript published: September 5, 2019 (version 1)
  4. Version of Record published: September 23, 2019 (version 2)

Copyright

© 2019, Heuze 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. Mélina L Heuze
  2. Gautham Sankara
  3. Joseph D'Alessandro
  4. Victor Cellerin
  5. Tien Dang
  6. David S Williams
  7. Jan CM Van Hest
  8. Philippe Marcq
  9. René-Marc Mège
  10. Benoit Ladoux
(2019)
Myosin II isoforms play distinct roles in adherens junction biogenesis
eLife 8:e46599.
https://doi.org/10.7554/eLife.46599

Share this article

https://doi.org/10.7554/eLife.46599

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