Unique morphogenetic signatures define mammalian neck muscles and associated connective tissues
- Institut Pasteur, France
- Brno University of Technology, Czech Republic
- University of Utah, United States
- 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
Elizabeth M Sefton
Shahragim Tajbakhsh
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.
Reviewing Editor
- Clare Blackburn, MRC Centre for Regenerative Medicine, University of Edinburgh, United Kingdom
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)
Version history
- Received: July 17, 2018
- Accepted: November 17, 2018
- Accepted Manuscript published: November 19, 2018 (version 1)
- Version of Record published: December 28, 2018 (version 2)
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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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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