Talin-activated vinculin interacts with branched actin networks to initiate bundles

  1. Rajaa Boujemaa-Paterski  Is a corresponding author
  2. Bruno Martins
  3. Matthias Eibauer
  4. Charlie T Beals
  5. Benjamin Geiger
  6. Ohad Medalia  Is a corresponding author
  1. University of Zurich, Switzerland
  2. University of Zürich, Switzerland
  3. Weizmann Institute of Science, Israel

Abstract

Vinculin plays a fundamental role in integrin-mediated cell adhesion. Activated by talin, it interacts with diverse adhesome components, enabling mechanical coupling between the actin cytoskeleton and the extracellular matrix. Here we studied the interactions of activated full-length vinculin with actin and the way it regulates the organization and dynamics of the Arp2/3 complex-mediated branched actin network. Through a combination of surface patterning and light microscopy experiments we show that vinculin can bundle dendritic actin networks through rapid binding and filament crosslinking. We show that vinculin promotes stable but flexible actin bundles having a mixed-polarity organization, as confirmed cryo-electron tomography. Adhesion-like synthetic design of vinculin activation by surface-bound talin revealed that clustered vinculin can initiate and immobilize bundles from mobile Arp2/3-branched networks. Our results provide a molecular basis for coordinate actin bundle formation at nascent adhesions.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. The structural data is deposited to the EMD , access number EMD-10737, and two tomographic volumes were deposited in EMPIAR under the accession number EMPIAR-10548.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Rajaa Boujemaa-Paterski

    Department of Biochemistry, University of Zurich, Zurich, Switzerland
    For correspondence
    r.boujemaa@bioc.uzh.ch
    Competing interests
    The authors declare that no competing interests exist.
  2. Bruno Martins

    Biochemistry, University of Zürich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  3. Matthias Eibauer

    Biochemistry, University of Zürich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  4. Charlie T Beals

    Biochemistry, University of Zürich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  5. Benjamin Geiger

    Department of Molecular Cell Biology, Weizmann Institute of Science, Rehovot, Israel
    Competing interests
    The authors declare that no competing interests exist.
  6. Ohad Medalia

    Biochemistry, University of Zürich, Zurich, Switzerland
    For correspondence
    omedalia@bioc.uzh.ch
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0994-2937

Funding

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (31003A_179418)

  • Ohad Medalia

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

Reviewing Editor

  1. Edward H Egelman, University of Virginia, United States

Publication history

  1. Received: November 26, 2019
  2. Accepted: November 12, 2020
  3. Accepted Manuscript published: November 13, 2020 (version 1)
  4. Version of Record published: November 23, 2020 (version 2)

Copyright

© 2020, Boujemaa-Paterski 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. Rajaa Boujemaa-Paterski
  2. Bruno Martins
  3. Matthias Eibauer
  4. Charlie T Beals
  5. Benjamin Geiger
  6. Ohad Medalia
(2020)
Talin-activated vinculin interacts with branched actin networks to initiate bundles
eLife 9:e53990.
https://doi.org/10.7554/eLife.53990

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