Unique morphogenetic signatures define mammalian neck muscles and associated connective tissues

Elife. 2018 Nov 19:7:e40179. doi: 10.7554/eLife.40179.

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.

Keywords: cranial mesoderm; developmental biology; mouse; neck myogenesis; neural crest; somite.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Connective Tissue / diagnostic imaging
  • Connective Tissue / embryology*
  • Connective Tissue / metabolism
  • Female
  • Gene Expression Regulation, Developmental
  • Male
  • Mammals / embryology*
  • Mammals / genetics
  • Mammals / metabolism
  • Mesoderm / diagnostic imaging
  • Mesoderm / embryology
  • Mesoderm / metabolism
  • Mice, Knockout
  • Mice, Transgenic
  • Microscopy, Confocal
  • Morphogenesis*
  • Muscle, Skeletal / diagnostic imaging
  • Muscle, Skeletal / embryology
  • Muscle, Skeletal / metabolism
  • Neck Muscles / diagnostic imaging
  • Neck Muscles / embryology*
  • Neck Muscles / metabolism
  • Somites / diagnostic imaging
  • Somites / embryology
  • Somites / metabolism
  • T-Box Domain Proteins / genetics
  • T-Box Domain Proteins / metabolism
  • X-Ray Microtomography

Substances

  • T-Box Domain Proteins
  • Tbx1 protein, mouse

Grants and funding

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