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

Page view(s)
15
Checked on Jan 23, 2023
Engrailed controls epaxial-hypaxial muscle innervation and the establishment of vertebrate three-dimensional mobility
Title:
Engrailed controls epaxial-hypaxial muscle innervation and the establishment of vertebrate three-dimensional mobility
Other Titles:
Developmental Biology
Keywords:
Publication Date:
01 October 2017
Citation:
Mohi U. Ahmed, Ashish K. Maurya, Louise Cheng, Erika C. Jorge, Frank R. Schubert, Pascal Maire, M. Albert Basson, Philip W. Ingham, Susanne Dietrich, Engrailed controls epaxial-hypaxial muscle innervation and the establishment of vertebrate three-dimensional mobility, Developmental Biology, Volume 430, Issue 1, 2017, Pages 90-104, ISSN 0012-1606, https://doi.org/10.1016/j.ydbio.2017.08.011. (http://www.sciencedirect.com/science/article/pii/S0012160617304165) 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. 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
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.
License type:
http://creativecommons.org/licenses/by-nc-nd/4.0/
Funding Info:
We are most grateful to L. Alvares, M. Buckingham, J. Clack, P. Currie, L. Erskine, A. Graham, G. Kardon, S. Kuratani, M. Meredith-Smith, A. Prochiantz and S. Roy for inspiring discussions and critical comments to the manuscript, to H. Nakamura for the En siRNA knock down constructs, to Gail Martin for the En1cre/+ mouse line and to Hagen Schmidt and Samantha Martin for mouse husbandry. The work was supported by the Human Frontier Science Program, Grant No R6Y0056/2004-C201, the European Network of Excellence Myores, Grant No EU LSHG-CT-2004-511978 MYORES, the Association Française contre les Myopathies, Grant No 11378, the Wellcome Trust, Grant No. WT080470, the Medical Research Council, Grant No. G0601104 and funding from A*STAR.
Description:
ISSN:
0012-1606
Files uploaded:

File Size Format Action
66-1-s20-s0012160617304165-main.pdf 3.12 MB PDF Open