Neural tube-associated boundary caps are a major source of mural cells in the skin

  1. Gaspard Gerschenfeld
  2. Fanny Coulpier
  3. Aurélie Gresset
  4. Pernelle Pulh
  5. Bastien Job
  6. Thomas Topilko
  7. Julie Siegenthaler, Ph.D.
  8. Maria Eleni Kastriti
  9. Isabelle Brunet
  10. Patrick Charnay
  11. Piotr Topilko  Is a corresponding author
  1. Ecole normale supérieure, CNRS, Inserm, Université PSL, France
  2. Mondor Institute of Biomedical Research, France
  3. Institut Gustave Roussy, France
  4. Institut du Cerveau et de la Moelle Epinière, France
  5. University of Colorado Anschutz Medical Campus, United States
  6. Karolinska Institute, Sweden
  7. Collège de France, France

Abstract

In addition to their roles in protecting nerves and increasing conduction velocity, peripheral glia plays key functions in blood vessel development by secreting molecules governing arteries alignment and maturation with nerves. Here we show in mice that a specific, nerve-attached cell population, derived from boundary caps (BCs), constitutes a major source of mural cells for the developing skin vasculature. Using Cre-based reporter cell tracing and single-cell transcriptomics, we show that BC derivatives migrate into the skin along the nerves, detach from them and differentiate into pericytes and vascular smooth muscle cells. Genetic ablation of this population affects the organization of the skin vascular network. Our results reveal the heterogeneity and extended potential of the BC population in mice, which gives rise to mural cells, in addition to previously described neurons, Schwann cells and melanocytes. Finally, our results suggest that mural specification of BC derivatives takes place before their migration along nerves to the mouse skin.

Data availability

Single-cell RNA-seq data have been deposited in the ArrayExpress database at EMBL-EBI (www.ebi.ac.uk/arrayexpress) under accession number E-MTAB-8972.

The following data sets were generated

Article and author information

Author details

  1. Gaspard Gerschenfeld

    Developmental Biology, Ecole normale supérieure, CNRS, Inserm, Université PSL, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2456-704X
  2. Fanny Coulpier

    UMR U955 INSERM UPEC, Mondor Institute of Biomedical Research, Créteil, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Aurélie Gresset

    Developmental Biology, Ecole normale supérieure, CNRS, Inserm, Université PSL, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Pernelle Pulh

    Developmental Biology, Ecole normale supérieure, CNRS, Inserm, Université PSL, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Bastien Job

    Inserm US23, AMMICA, Institut Gustave Roussy, Villejuif, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Thomas Topilko

    Laboratoire de Plasticité Structurale, Institut du Cerveau et de la Moelle Epinière, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Julie Siegenthaler, Ph.D.

    Department of Pediatrics Section of Developmental Biology, University of Colorado Anschutz Medical Campus, Aurora, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Maria Eleni Kastriti

    Department of Physiology and Pharmacology, Karolinska Institute, Stockholm, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  9. Isabelle Brunet

    Center for Interdisciplinary Research in Biology, Collège de France, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5490-2937
  10. Patrick Charnay

    Developmental Biology, Ecole normale supérieure, CNRS, Inserm, Université PSL, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  11. Piotr Topilko

    UMR U955 INSERM UPEC, Mondor Institute of Biomedical Research, Créteil, France
    For correspondence
    piotr.topilko@inserm.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7381-6770

Funding

Agence Nationale de la Recherche (ANR-10-LABX-54 MEMOLIFE)

  • Patrick Charnay

Agence Nationale de la Recherche (ANR-11-IDEX-0001-02 PSL* Research University)

  • Patrick Charnay

Institut National de la Santé et de la Recherche Médicale

  • Patrick Charnay
  • Piotr Topilko

Centre National de la Recherche Scientifique

  • Patrick Charnay
  • Piotr Topilko

Institut National Du Cancer

  • Patrick Charnay
  • Piotr Topilko

Ministère de l'Enseignement Supérieur et de la Recherche Scientifique

  • Patrick Charnay
  • Piotr Topilko

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

Ethics

Animal experimentation: All animal manipulations were performed according to French and European Union regulations. According to these regulations, no ethics committee approval was required for this study which only used mouse embryos and newborns.

Copyright

© 2023, Gerschenfeld 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. Gaspard Gerschenfeld
  2. Fanny Coulpier
  3. Aurélie Gresset
  4. Pernelle Pulh
  5. Bastien Job
  6. Thomas Topilko
  7. Julie Siegenthaler, Ph.D.
  8. Maria Eleni Kastriti
  9. Isabelle Brunet
  10. Patrick Charnay
  11. Piotr Topilko
(2023)
Neural tube-associated boundary caps are a major source of mural cells in the skin
eLife 12:e69413.
https://doi.org/10.7554/eLife.69413

Share this article

https://doi.org/10.7554/eLife.69413

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