Unique morphogenetic signatures define mammalian neck muscles and associated connective tissues.

Eglantine Heude,Marketa Tesarova,Tomas Zikmund,Shahragim Tajbakhsh,Noritaka Adachi,Estelle Jullian,Alexandre Grimaldi,Elizabeth M Sefton,Gabrielle Kardon,Robert G Kelly,Jozef Kaiser

doi:10.7554/elife.40179

Eglantine Heude, Marketa Tesarova + Show 9 more

Open Access

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

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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.

Highlights

The neck is composed of approximately 80 skeletal muscles in humans that allow head mobility, respiration, swallowing and vocalization processes, containing essential elements such as the trachea, esophagus, larynx, and cervical vertebrae
Head and trunk muscles arise from different mesodermal origins and their development depends on distinct myogenic programs
The embryological origins of neck muscles and connective tissues at the head-trunk interface have been poorly defined largely due to their localization at a transition zone that involves multiple embryonic populations

Summary

Introduction

The neck is composed of approximately 80 skeletal muscles in humans that allow head mobility, respiration, swallowing and vocalization processes, containing essential elements such as the trachea, esophagus, larynx, and cervical vertebrae. While the somitic origin of epaxial/hypaxial neck muscles and CPM origin of pharyngeal, laryngeal and esophagus striated muscles are well defined (Gopalakrishnan et al, 2015; Noden, 1983; Tabler et al, 2017), the embryological origin of cucullaris-derived muscles has remained a subject of controversy (Couly et al, 1993; Edgeworth, 1935; Greil, 1913; Huang et al, 1997; Huang et al, 2000; Matsuoka et al, 2005; Noden, 1983; Piatt, 1938; Piekarski and Olsson, 2007) This muscle group was reported to originate either from lateral plate mesoderm (LPM) or CPM populations adjacent to the first three somites in chick and axolotl (Nagashima et al, 2016; Sefton et al, 2016; Theis et al, 2010). We identify a unique genetic network involving both Mesp and Pax genes for somite-derived neck muscles and we define a new limit of neural crest contribution to neck connective tissue and shoulder components

Results

Discussion

Materials and methods

Funding Funder Institut Pasteur