Structural organization and dynamics of FCHo2 docking on membranes

  1. Fatima El Alaoui
  2. Ignacio Casuso
  3. David Sanchez-Fuentes
  4. Charlotte Arpin-Andre
  5. Raissa Rathar
  6. Volker Baecker
  7. Anna Castro
  8. Thierry Lorca
  9. Julien Viaud
  10. Stéphane Vassilopoulos
  11. Adrien Carretero-Genevrier
  12. Laura Picas  Is a corresponding author
  1. CNRS UMR 9004, Université de Montpellier, France
  2. U1067 INSERM, Aix-Marseille Université, France
  3. CNRS UMR 5214, Université de Montpellier, France
  4. CNRS, INSERM, University of Montpellier, France
  5. CNRS UMR Université de Montpellier, France
  6. UMR1297, University of Toulouse, France
  7. Sorbonne Université, INSERM, France

Abstract

Clathrin-mediated endocytosis (CME) is a central trafficking pathway in eukaryotic cells regulated by phosphoinositides. The plasma membrane phosphatidylinositol-4,5-bisphosphate (PI(4,5)P2) plays an instrumental role in driving CME initiation. The F-BAR domain only protein 1 and 2 complex (FCHo1/2) is among the early proteins that reach the plasma membrane, but the exact mechanisms triggering its recruitment remain elusive. Here, we show the molecular dynamics of FCHo2 self-assembly on membranes by combining minimal reconstituted in vitro and cellular systems. Our results indicate that PI(4,5)P2 domains assist FCHo2 docking at specific membrane regions, where it self-assembles into ring-like shape protein patches. We show that the binding of FCHo2 on cellular membranes promotes PI(4,5)P2 clustering at the boundary of cargo receptors and that this accumulation enhances clathrin assembly. Thus, our results provide a mechanistic framework that could explain the recruitment of early PI(4,5)P2-interacting proteins at endocytic sites.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting file. Datasets are available at Dryad, doi:10.5061/dryad.n8pk0p2wp

The following data sets were generated

Article and author information

Author details

  1. Fatima El Alaoui

    Institut de Recherche en Infectiologie de Montpellier (IRIM), CNRS UMR 9004, Université de Montpellier, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3298-4078
  2. Ignacio Casuso

    U1067 INSERM, Aix-Marseille Université, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  3. David Sanchez-Fuentes

    Institut d'Électronique et des Systèmes (IES), CNRS UMR 5214, Université de Montpellier, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Charlotte Arpin-Andre

    Institut de Recherche en Infectiologie de Montpellier (IRIM), CNRS UMR 9004, Université de Montpellier, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Raissa Rathar

    Institut d'Électronique et des Systèmes (IES), CNRS UMR 5214, Université de Montpellier, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8766-2186
  6. Volker Baecker

    Montpellier Ressources Imagerie, BioCampus Montpellier, CNRS, INSERM, University of Montpellier, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9129-6403
  7. Anna Castro

    Centre de Biologie Cellulaire de Montpellier (CRBM), CNRS UMR Université de Montpellier, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  8. Thierry Lorca

    Centre de Biologie Cellulaire de Montpellier (CRBM), CNRS UMR Université de Montpellier, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  9. Julien Viaud

    Institute of Metabolic and Cardiovascular Diseases (I2MC), UMR1297, University of Toulouse, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4406-5642
  10. Stéphane Vassilopoulos

    Sorbonne Université, INSERM, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0172-330X
  11. Adrien Carretero-Genevrier

    Institut d'Électronique et des Systèmes (IES), CNRS UMR 5214, Université de Montpellier, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0488-9452
  12. Laura Picas

    Institut de Recherche en Infectiologie de Montpellier (IRIM), CNRS UMR 9004, Université de Montpellier, Montpellier, France
    For correspondence
    laura.picas@irim.cnrs.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5619-5228

Funding

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

  • Volker Baecker

ATIP-Avenir (AO-2016)

  • Laura Picas

Agence Nationale de la Recherche (ANR-18-CE13-0015-02)

  • Laura Picas

European Research Council (No.803004)

  • Adrien Carretero-Genevrier

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

Reviewing Editor

  1. José D Faraldo-Gómez, National Heart, Lung and Blood Institute, National Institutes of Health, United States

Version history

  1. Preprint posted: April 20, 2021 (view preprint)
  2. Received: August 19, 2021
  3. Accepted: January 18, 2022
  4. Accepted Manuscript published: January 19, 2022 (version 1)
  5. Version of Record published: January 28, 2022 (version 2)

Copyright

© 2022, El Alaoui 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. Fatima El Alaoui
  2. Ignacio Casuso
  3. David Sanchez-Fuentes
  4. Charlotte Arpin-Andre
  5. Raissa Rathar
  6. Volker Baecker
  7. Anna Castro
  8. Thierry Lorca
  9. Julien Viaud
  10. Stéphane Vassilopoulos
  11. Adrien Carretero-Genevrier
  12. Laura Picas
(2022)
Structural organization and dynamics of FCHo2 docking on membranes
eLife 11:e73156.
https://doi.org/10.7554/eLife.73156

Share this article

https://doi.org/10.7554/eLife.73156

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