PUBLICATION

Engrailed controls epaxial-hypaxial muscle innervation and the establishment of vertebrate three-dimensional mobility

Authors
Ahmed, M.U., Maurya, A.K., Cheng, L., Jorge, E.C., Schubert, F.R., Maire, P., Basson, M.A., Ingham, P.W., Dietrich, S.
ID
ZDB-PUB-170817-16
Date
2017
Source
Developmental Biology   430(1): 90-104 (Journal)
Registered Authors
Ingham, Philip, Maurya, Ashish
Keywords
Engrailed gene, axon guidance, chicken, dorsal ramus, epaxial-hypaxial muscle, locomotion and mobility, mouse, muscle innervation, spinal nerves, ventral ramus, vertebrate development and evolution, zebrafish
MeSH Terms
  • Animals
  • Animals, Newborn
  • Axons/metabolism
  • Biomarkers/metabolism
  • Body Patterning/genetics
  • Chickens/metabolism*
  • Gene Expression Regulation, Developmental
  • Homeodomain Proteins/metabolism*
  • Mice
  • Movement*
  • Muscle Development/genetics
  • Muscle, Skeletal/innervation*
  • Muscle, Skeletal/metabolism*
  • Myoblasts/cytology
  • Myoblasts/metabolism
  • Phenotype
  • Somites/metabolism
  • Transcription Factors/metabolism*
  • Zebrafish/embryology*
  • Zebrafish/metabolism*
PubMed
28807781 Full text @ Dev. Biol.
Abstract
Chordates are characterised by contractile muscle on either side of the body that promotes movement by side-to-side undulation. In the lineage leading to modern jawed vertebrates (crown group gnathostomes), this system was refined: body muscle became segregated into distinct dorsal (epaxial) and ventral (hypaxial) components that are separately innervated by the medial and hypaxial motors column, respectively, via the dorsal and ventral ramus of the spinal nerves. This allows full three-dimensional mobility, which in turn was a key factor in their evolutionary success. How the new gnathostome system is established during embryogenesis and how it may have evolved in the ancestors of modern vertebrates is not known. Vertebrate Engrailed genes have a peculiar expression pattern as they temporarily demarcate a central domain of the developing musculature at the epaxial-hypaxial boundary. Moreover, they are the only genes known with this particular expression pattern. The aim of this study was to investigate whether Engrailed genes control epaxial-hypaxial muscle development and innervation. Investigating chick, mouse and zebrafish as major gnathostome model organisms, we found that the Engrailed expression domain was associated with the establishment of the epaxial-hypaxial boundary of muscle in all three species. Moreover, the outgrowing epaxial and hypaxial nerves orientated themselves with respect to this Engrailed domain. In the chicken, loss and gain of Engrailed function changed epaxial-hypaxial somite patterning. Importantly, in all animals studied, loss and gain of Engrailed function severely disrupted the pathfinding of the spinal motor axons, suggesting that Engrailed plays an evolutionarily conserved role in the separate innervation of vertebrate epaxial-hypaxial muscle.
Genes / Markers
Figures
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Expression
Phenotype
Mutations / Transgenics
Human Disease / Model
Sequence Targeting Reagents
Fish
Antibodies
Orthology
Engineered Foreign Genes
Mapping