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

Mohi U. Ahmed, Ashish K. Maurya, Louise Cheng, Erika C. Jorge, Frank R. Schubert, Pascal Maire, M. Albert Basson, Philip W. Ingham, Susanne Dietrich

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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.
Original languageEnglish
JournalDevelopmental Biology
Early online date12 Aug 2017
DOIs
Publication statusE-pub ahead of print - 12 Aug 2017

Keywords

  • vertebrate development and evolution
  • locomotion and mobility
  • epaxial-hypaxial muscle
  • muscle innervation
  • spinal nerves
  • axon guidance
  • dorsal ramus
  • ventral ramus
  • Engrailed gene
  • mouse
  • chicken
  • zebrafish

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