Microtubule plus-end dynamics link wound repair to the innate immune response

  1. Clara Taffoni
  2. Shizue Omi
  3. Caroline Huber
  4. Sébastien Mailfert
  5. Matthieu Fallet
  6. Jean-François Rupprecht
  7. Jonathan Ewbank
  8. Nathalie Pujol  Is a corresponding author
  1. Aix Marseille Université, INSERM, CNRS, France
  2. Aix Marseille Université, CNRS UMR7332, France

Abstract

The skin protects animals from infection and physical damage. In C. elegans, wounding the epidermis triggers an immune reaction and a repair response, but it is not clear how these are coordinated. Previous work implicated the microtubule cytoskeleton in the maintenance of epidermal integrity (Chuang et al, 2016). Here, by establishing a simple wounding system, we show that wounding provokes a reorganisation of plasma membrane subdomains. This is followed by recruitment of the microtubule plus end-binding protein EB1/EBP-2 around the wound and actin ring formation, dependant on ARP2/3 branched actin polymerisation. We show that microtubule dynamics are required for the recruitment and closure of the actin ring, and for the trafficking of the key signalling protein SLC6/SNF-12 towards the injury site. Without SNF-12 recruitment, there is an abrogation of the immune response. Our results suggest that microtubule dynamics coordinate the cytoskeletal changes required for wound repair and the concomitant activation of innate immunity.

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 all quantitative Figures.

Article and author information

Author details

  1. Clara Taffoni

    CIML, Centre d'Immunologie de Marseille-Luminy, Turing Centre for Living Systems, Aix Marseille Université, INSERM, CNRS, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9265-5909
  2. Shizue Omi

    CIML, Centre d'Immunologie de Marseille-Luminy, Turing Centre for Living Systems, Aix Marseille Université, INSERM, CNRS, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2711-2016
  3. Caroline Huber

    CIML, Centre d'Immunologie de Marseille-Luminy, Turing Centre for Living Systems, Aix Marseille Université, INSERM, CNRS, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3767-2719
  4. Sébastien Mailfert

    CIML, Centre d'Immunologie de Marseille-Luminy, Turing Centre for Living Systems, Aix Marseille Université, INSERM, CNRS, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0409-0432
  5. Matthieu Fallet

    CIML, Centre d'Immunologie de Marseille-Luminy, Turing Centre for Living Systems, Aix Marseille Université, INSERM, CNRS, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8144-6159
  6. Jean-François Rupprecht

    CPT, Turing Centre for Living Systems, Aix Marseille Université, CNRS UMR7332, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8904-5878
  7. Jonathan Ewbank

    CIML, Centre d'Immunologie de Marseille-Luminy, Turing Centre for Living Systems, Aix Marseille Université, INSERM, CNRS, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1257-6862
  8. Nathalie Pujol

    CIML, Centre d'Immunologie de Marseille-Luminy, Turing Centre for Living Systems, Aix Marseille Université, INSERM, CNRS, Marseille, France
    For correspondence
    pujol@ciml.univ-mrs.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8889-3197

Funding

Agence Nationale de la Recherche (ANR-16-CE15-0001-01)

  • Clara Taffoni
  • Sébastien Mailfert
  • Matthieu Fallet
  • Jonathan Ewbank
  • Nathalie Pujol

Institut National de la Santé et de la Recherche Médicale

  • Jonathan Ewbank

Centre National de la Recherche Scientifique

  • Shizue Omi
  • Sébastien Mailfert
  • Matthieu Fallet
  • Jean-François Rupprecht
  • Nathalie Pujol

Aix-Marseille Université

  • Clara Taffoni
  • Caroline Huber

Agence Nationale de la Recherche (ANR-12-BSV3-0001-01)

  • Clara Taffoni
  • Sébastien Mailfert
  • Matthieu Fallet
  • Jonathan Ewbank
  • Nathalie Pujol

Agence Nationale de la Recherche (ANR-11-LABX-0054)

  • Clara Taffoni
  • Sébastien Mailfert
  • Matthieu Fallet
  • Jonathan Ewbank
  • Nathalie Pujol

Agence Nationale de la Recherche (ANR-11-IDEX-0001-02)

  • Clara Taffoni
  • Sébastien Mailfert
  • Matthieu Fallet
  • Jonathan Ewbank
  • Nathalie Pujol

Agence Nationale de la Recherche (ANR-10-INBS-04-01)

  • Clara Taffoni
  • Sébastien Mailfert
  • Matthieu Fallet
  • Jonathan Ewbank
  • Nathalie Pujol

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

Reviewing Editor

  1. Terry Lechler, Duke University, United States

Publication history

  1. Received: January 11, 2019
  2. Accepted: January 27, 2020
  3. Accepted Manuscript published: January 29, 2020 (version 1)
  4. Version of Record published: February 26, 2020 (version 2)

Copyright

© 2020, Taffoni 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. Clara Taffoni
  2. Shizue Omi
  3. Caroline Huber
  4. Sébastien Mailfert
  5. Matthieu Fallet
  6. Jean-François Rupprecht
  7. Jonathan Ewbank
  8. Nathalie Pujol
(2020)
Microtubule plus-end dynamics link wound repair to the innate immune response
eLife 9:e45047.
https://doi.org/10.7554/eLife.45047

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