Unique morphogenetic signatures define mammalian neck muscles and associated connective tissues

  1. Eglantine Heude
  2. Marketa Tesarova
  3. Elizabeth M Sefton
  4. Estelle Jullian
  5. Noritaka Adachi
  6. Alexandre Grimaldi
  7. Tomas Zikmund
  8. Jozef Kaiser
  9. Gabrielle Kardon
  10. Robert G Kelly
  11. Shahragim Tajbakhsh  Is a corresponding author
  1. Institut Pasteur, France
  2. Brno University of Technology, Czech Republic
  3. University of Utah, United States
  4. Aix-Marseille Université, France

Abstract

In vertebrates, head and trunk muscles develop from different mesodermal populations and are regulated by distinct genetic networks. Neck muscles at the head-trunk interface remain poorly defined due to their complex morphogenesis and dual mesodermal origins. Here, we use genetically modified mice to establish a 3D model that integrates regulatory genes, cell populations and morphogenetic events that define this transition zone. We show that the evolutionary conserved cucullaris-derived muscles originate from posterior cardiopharyngeal mesoderm, not lateral plate mesoderm, and we define new boundaries for neural crest and mesodermal contributions to neck connective tissue. Furthermore, lineage studies and functional analysis of Tbx1- and Pax3-null mice reveal a unique developmental program for somitic neck muscles that is distinct from that of somitic trunk muscles. Our findings unveil the embryological and developmental requirements underlying tetrapod neck myogenesis and provide a blueprint to investigate how muscle subsets are selectively affected in some human myopathies.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Eglantine Heude

    Department of Developmental and Stem Cell Biology, Institut Pasteur, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Marketa Tesarova

    Central European Institute of Technology, Brno University of Technology, Brno, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  3. Elizabeth M Sefton

    Department of Human Genetics, University of Utah, Salt Lake City, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6481-612X
  4. Estelle Jullian

    CNRS UMR 7288, Aix-Marseille Université, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Noritaka Adachi

    CNRS UMR 7288, Aix-Marseille Université, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9482-8436
  6. Alexandre Grimaldi

    Department of Developmental and Stem Cell Biology, Institut Pasteur, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Tomas Zikmund

    Central European Institute of Technology, Brno University of Technology, Brno, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  8. Jozef Kaiser

    Central European Institute of Technology, Brno University of Technology, Brno, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  9. Gabrielle Kardon

    Department of Human Genetics, University of Utah, Salt Lake City, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Robert G Kelly

    CNRS UMR 7288, Aix-Marseille Université, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
  11. Shahragim Tajbakhsh

    Department of Developmental & Stem Cell Biology, Institut Pasteur, Paris, France
    For correspondence
    shahragim.tajbakhsh@pasteur.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1809-7202

Funding

Institut Pasteur

  • Eglantine Heude
  • Alexandre Grimaldi
  • Shahragim Tajbakhsh

National Institutes of Health

  • Elizabeth M Sefton
  • Gabrielle Kardon

Agence Nationale de la Recherche

  • Eglantine Heude
  • Alexandre Grimaldi
  • Shahragim Tajbakhsh

Centre National de la Recherche Scientifique

  • Eglantine Heude
  • Estelle Jullian
  • Noritaka Adachi
  • Alexandre Grimaldi
  • Robert G Kelly
  • Shahragim Tajbakhsh

Association Française contre les Myopathies

  • Eglantine Heude
  • Alexandre Grimaldi
  • Shahragim Tajbakhsh

Central European Institute of Technology

  • Marketa Tesarova
  • Tomas Zikmund
  • Jozef Kaiser

March of Dimes Foundation

  • Elizabeth M Sefton
  • Gabrielle Kardon

Fondation pour la Recherche Médicale

  • Estelle Jullian
  • Noritaka Adachi
  • Robert G Kelly

Fondation Leducq

  • Estelle Jullian
  • Noritaka Adachi
  • Robert G Kelly

Yamada Science Foundation

  • Noritaka Adachi
  • Robert G Kelly

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

Ethics

Animal experimentation: Animals were handled as per European Community guidelines and the ethics committee of the Institut Pasteur (CTEA) approved protocols. (APAFIS#6354-20160809l2028839)

Copyright

© 2018, Heude 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. Eglantine Heude
  2. Marketa Tesarova
  3. Elizabeth M Sefton
  4. Estelle Jullian
  5. Noritaka Adachi
  6. Alexandre Grimaldi
  7. Tomas Zikmund
  8. Jozef Kaiser
  9. Gabrielle Kardon
  10. Robert G Kelly
  11. Shahragim Tajbakhsh
(2018)
Unique morphogenetic signatures define mammalian neck muscles and associated connective tissues
eLife 7:e40179.
https://doi.org/10.7554/eLife.40179

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https://doi.org/10.7554/eLife.40179