1. Physics of Living Systems
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Ezrin enrichment on curved membranes requires a specific conformation or interaction with a curvature-sensitive partner

  1. Feng-Ching Tsai  Is a corresponding author
  2. Aurelie Bertin
  3. Hugo Bousquet
  4. John Manzi
  5. Yosuke Senju
  6. Meng-Chen Tsai
  7. Laura Picas
  8. Stephanie Miserey-Lenkei
  9. Pekka Lappalainen
  10. Emmanuel Lemichez
  11. Evelyne Coudrier  Is a corresponding author
  12. Patricia Bassereau  Is a corresponding author
  1. Institut Curie, France
  2. University of Helsinki, Finland
  3. Université Côte d'Azur, France
  4. Institut de Recherche en Infectiologie de Montpellier (IRIM), France
  5. Institut Pasteur, France
Research Article
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Cite this article as: eLife 2018;7:e37262 doi: 10.7554/eLife.37262

Abstract

One challenge in cell biology is to decipher the biophysical mechanisms governing protein enrichment on curved membranes and the resulting membrane deformation. The ERM protein ezrin is abundant and associated with cellular membranes that are flat, positively or negatively curved. Using in vitro and cell biology approaches, we assess mechanisms of ezrin's enrichment on curved membranes. We evidence that wild-type ezrin (ezrinWT) and its phosphomimetic mutant T567D (ezrinTD) do not deform membranes but self-assemble anti-parallelly, zipping adjacent membranes. EzrinTD's specific conformation reduces intermolecular interactions, allows binding to actin filaments, which reduces membrane tethering, and promotes ezrin binding to positively-curved membranes. While neither ezrinTD nor ezrinWT senses negative curvature alone, we demonstrate that interacting with curvature-sensing I-BAR-domain proteins facilitates ezrin enrichment in negatively-curved membrane protrusions. Overall, our work demonstrates that ezrin can tether membranes, or be targeted to curved membranes, depending on conformations and interactions with actin and curvature-sensing binding partners.

Article and author information

Author details

  1. Feng-Ching Tsai

    Laboratoire Physico Chimie Curie, Institut Curie, Paris, France
    For correspondence
    feng-ching.tsai@curie.fr
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6869-5254
  2. Aurelie Bertin

    Laboratoire Physico Chimie Curie, Institut Curie, Paris, France
    Competing interests
    No competing interests declared.
  3. Hugo Bousquet

    UMR 144, Institut Curie, Paris, France
    Competing interests
    No competing interests declared.
  4. John Manzi

    Laboratoire Physico Chimie Curie, Institut Curie, Paris, France
    Competing interests
    No competing interests declared.
  5. Yosuke Senju

    Program in Cell and Molecular Biology, Institute of Biotechnology, University of Helsinki, Helsinki, Finland
    Competing interests
    No competing interests declared.
  6. Meng-Chen Tsai

    CNRS, Institut de Pharmacologie Moléculaire et Cellulaire, Université Côte d'Azur, Valbonne, France
    Competing interests
    No competing interests declared.
  7. Laura Picas

    CNRS UMR 9004, Institut de Recherche en Infectiologie de Montpellier (IRIM), Montpellier, France
    Competing interests
    No competing interests declared.
  8. Stephanie Miserey-Lenkei

    UMR 144, Institut Curie, Paris, France
    Competing interests
    No competing interests declared.
  9. Pekka Lappalainen

    Program in Cell and Molecular Biology, Institute of Biotechnology, University of Helsinki, Helsinki, Finland
    Competing interests
    Pekka Lappalainen, Reviewing editor, eLife.
  10. Emmanuel Lemichez

    Département de Microbiologie, Unité des Toxines Bactériennes, Institut Pasteur, Paris, France
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9080-7761
  11. Evelyne Coudrier

    UMR 144, Institut Curie, Paris, France
    For correspondence
    Evelyne.Coudrier@curie.fr
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6011-8922
  12. Patricia Bassereau

    Laboratoire Physico Chimie Curie, Institut Curie, Paris, France
    For correspondence
    patricia.bassereau@curie.fr
    Competing interests
    Patricia Bassereau, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8544-6778

Funding

Agence Nationale de la Recherche (ANR-15-CE18-0016-03)

  • Meng-Chen Tsai
  • Emmanuel Lemichez
  • Patricia Bassereau

H2020 European Research Council (339847)

  • Stephanie Miserey-Lenkei
  • Evelyne Coudrier
  • Patricia Bassereau

Human Frontier Science Program (RGP0005/2016)

  • Yosuke Senju
  • Pekka Lappalainen
  • Evelyne Coudrier
  • Patricia Bassereau

European Molecular Biology Organization (ALTF 1527-2014)

  • Feng-Ching Tsai

H2020 Marie Skłodowska-Curie Actions (H2020-MSCA-IF-2014)

  • Feng-Ching Tsai

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

Reviewing Editor

  1. Anna Akhmanova, Utrecht University, Netherlands

Publication history

  1. Received: April 4, 2018
  2. Accepted: September 14, 2018
  3. Accepted Manuscript published: September 20, 2018 (version 1)
  4. Version of Record published: October 1, 2018 (version 2)

Copyright

© 2018, Tsai 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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