Generality of vertebrate developmental patterns: evidence for a dermomyotome in fish

SUMMARY The somitic compartment that gives rise to trunk muscle and dermis in amniotes is an epithelial sheet on the external surface of the somite, and is known as the dermomyotome. However, despite its central role in the development of the trunk and limbs, the evolutionary history of the dermomyotome and its role in nonamniotes is poorly understood. We have tested whether a tissue with the morphological and molecular characteristics of a dermomyotome exists in nonamniotes. We show that representatives of the agnathans and of all major clades of gnathostomes each have a layer of cells on the surface of the somite, external to the embryonic myotome. These external cells do not show any signs of terminal myogenic or dermogenic differentiation. Moreover, in the embryos of bony fishes as diverse as sturgeons (Chondrostei) and zebrafish (Teleostei) this layer of cells expresses the pax3 and pax7 genes that mark myogenic precursors. Some of the pax7‐expressing cells also express the differentiation‐promoting myogenic regulatory factor Myogenin and appear to enter into the myotome. We therefore suggest that the dermomyotome is an ancient and conserved structure that evolved prior to the last common ancestor of all vertebrates. The identification of a dermomyotome in fish makes it possible to apply the powerful cellular and genetic approaches available in zebrafish to the understanding of this key developmental structure.

[1]  S. Kuratani,et al.  Evolution and developmental patterning of the vertebrate skeletal muscles: Perspectives from the lamprey , 2005, Developmental dynamics : an official publication of the American Association of Anatomists.

[2]  S. Hughes,et al.  Fgf8 drives myogenic progression of a novel lateral fast muscle fibre population in zebrafish , 2005, Development.

[3]  C. Cauty,et al.  Expression patterns of collagen I (α1) encoding gene and muscle‐specific genes reveal that the lateral domain of the fish somite forms a connective tissue surrounding the myotome , 2005, Developmental dynamics : an official publication of the American Association of Anatomists.

[4]  Chaya Kalcheim,et al.  Lineage analysis of the avian dermomyotome sheet reveals the existence of single cells with both dermal and muscle progenitor fates , 2005, Development.

[5]  S. Amacher,et al.  Zebrafish slow muscle cell migration induces a wave of fast muscle morphogenesis. , 2004, Developmental cell.

[6]  B. Christ,et al.  Formation and differentiation of the avian dermomyotome , 2004, Anatomy and Embryology.

[7]  T. Braun,et al.  Pax7 directs postnatal renewal and propagation of myogenic satellite cells but not their specification , 2004, The EMBO journal.

[8]  J. Klein,et al.  The phylogenetic relationship of tetrapod, coelacanth, and lungfish revealed by the sequences of forty-four nuclear genes. , 2004, Molecular biology and evolution.

[9]  A. Grimaldi,et al.  Hedgehog regulation of superficial slow muscle fibres in Xenopus and the evolution of tetrapod trunk myogenesis , 2004, Development.

[10]  C. Marcelle,et al.  A two-step mechanism for myotome formation in chick. , 2004, Developmental cell.

[11]  R. Latorre,et al.  The larval development of lateral musculature in gilthead sea bream Sparus aurata and sea bass Dicentrarchus labrax , 1995, Cell and Tissue Research.

[12]  A. Rowlerson,et al.  Hyperplastic and hypertrophic growth of lateral muscle in Dicentrarchus labrax (L.) , 1990, Anatomy and Embryology.

[13]  G. Morvan-Dubois,et al.  Skin development in bony fish with particular emphasis on collagen deposition in the dermis of the zebrafish (Danio rerio). , 2004, The International journal of developmental biology.

[14]  D. Dhouailly,et al.  Molecular mechanisms controlling dorsal dermis generation from the somitic dermomyotome. , 2004, The International journal of developmental biology.

[15]  J. Sire,et al.  Scale development in fish: a review, with description of sonic hedgehog (shh) expression in the zebrafish (Danio rerio). , 2004, The International journal of developmental biology.

[16]  Joel Cracraft,et al.  Assembling the tree of life , 2004 .

[17]  T. Rabbitts,et al.  Lmo2 and Scl/Tal1 convert non-axial mesoderm into haemangioblasts which differentiate into endothelial cells in the absence of Gata1 , 2003, Development.

[18]  N. Kahane,et al.  Coherent development of dermomyotome and dermis from the entire mediolateral extent of the dorsal somite , 2003, Development.

[19]  P. Currie,et al.  Myotome meanderings , 2003, EMBO reports.

[20]  S. Tajbakhsh.  Stem cells to tissue: molecular, cellular and anatomical heterogeneity in skeletal muscle. , 2003, Current opinion in genetics & development.

[21]  P. Rigby,et al.  Analysis of a key regulatory region upstream of the Myf5 gene reveals multiple phases of myogenesis, orchestrated at each site by a combination of elements dispersed throughout the locus , 2003, Development.

[22]  Ruijin Huang,et al.  Three different fates of cells migrating from somites into the limb bud , 2003, Anatomy and Embryology.

[23]  M. Buckingham,et al.  The formation of skeletal muscle: from somite to limb , 2003, Journal of anatomy.

[24]  M. D. Pai-Silva,et al.  Morphological and histochemical study of the myotomal muscle in pacu (Piaractus mesopotamicus Holmberg, 1887) during the initial growth phases , 2003 .

[25]  C. Tabin,et al.  Local extrinsic signals determine muscle and endothelial cell fate and patterning in the vertebrate limb. , 2002, Developmental cell.

[26]  P. Holland,et al.  Bayesian Phylogenetic Analysis Supports Monophyly of Ambulacraria and of Cyclostomes , 2002, Zoological science.

[27]  C. Emerson,et al.  Myogenic regulatory factors and the specification of muscle progenitors in vertebrate embryos. , 2002, Annual review of cell and developmental biology.

[28]  A. Rowlerson,et al.  5. Cellular mechanisms of post-embryonic muscle growth in aquaculture species , 2001 .

[29]  P. Rigby,et al.  Hedgehog signalling is required for maintenance of myf5 and myoD expression and timely terminal differentiation in zebrafish adaxial myogenesis. , 2001, Developmental biology.

[30]  P. Rescan.  Regulation and functions of myogenic regulatory factors in lower vertebrates. , 2001, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[31]  I. Bachelet,et al.  The third wave of myotome colonization by mitotically competent progenitors: regulating the balance between differentiation and proliferation during muscle development. , 2001, Development.

[32]  G. Goldspink,et al.  Red and white muscle development in the trout (Oncorhynchus mykiss) as shown by in situ hybridisation of fast and slow myosin heavy chain transcripts. , 2001, The Journal of experimental biology.

[33]  R. Spörle.  Epaxial-adaxial-hypaxial regionalisation of the vertebrate somite: evidence for a somitic organiser and a mirror-image duplication , 2001, Development Genes and Evolution.

[34]  I. Johnston.  Muscle development and growth , 2001 .

[35]  Matthew J. Hayden.  Embryology: Constructing the Organism , 2001, The Yale Journal of Biology and Medicine.

[36]  B. Thisse,et al.  Evolutionary origins of vertebrate appendicular muscle , 2000, Nature.

[37]  M. Barresi,et al.  DEVELOPMENTAL DYNAMICS 219:287–303 (2000) REVIEWS A PEER REVIEWED FORUM Somite Development in Zebrafish , 2022 .

[38]  Ruijin Huang,et al.  Origin of the epaxial and hypaxial myotome in avian embryos , 2000, Anatomy and Embryology.

[39]  M. Dal Pai-Silva,et al.  Morphological, Histochemical and Morphometric Study of the Myotomal Muscle Tissue of the Pacu (Piaractus mesopotamicus Holmberg 1887: Serrasalminae, Characidae, Teleostei) , 2000, Anatomia, histologia, embryologia.

[40]  M. Rudnicki,et al.  Pax7 Is Required for the Specification of Myogenic Satellite Cells , 2000, Cell.

[41]  W. Denetclaw,et al.  The growth of the dermomyotome and formation of early myotome lineages in thoracolumbar somites of chicken embryos. , 2000, Development.

[42]  S. Morris,et al.  Lower Cambrian vertebrates from south China , 1999, Nature.

[43]  T. Lacalli,et al.  Somatic motoneurones in amphioxus larvae: cell types, cell position and innervation patterns , 1999 .

[44]  Y. Cinnamon,et al.  Myotome formation: a multistage process , 1999, Cell and Tissue Research.

[45]  S. Cordes,et al.  Expression of Zkrml2, a homologue of the Krml1/val segmentation gene, during embryonic patterning of the zebrafish (Danio rerio) , 1999, Mechanisms of Development.

[46]  M. C. Candia Carnevali,et al.  Muscle growth in response to changing demands of functions in the teleost Sparus aurata (L.) during development from hatching to juvenile , 1998, Anatomy and Embryology.

[47]  I. Johnston,et al.  Molecular cloning and developmental expression patterns of the MyoD and MEF2 families of muscle transcription factors in the carp. , 1998, The Journal of experimental biology.

[48]  R. Latorre,et al.  Muscle Development in Gilthead Sea Bream (Sparus aurata, L.) and Sea Bass (Dicentrarchus labrax, L.): Further Histochemical and Ultrastructural Aspects , 1998, Anatomia, histologia, embryologia.

[49]  J. Haslett,et al.  Patterns of superficial fibre formation in the European pearlfish (Rutilus frisii meidingeri) provide a general template for slow muscle development in teleost fish , 1998, Anatomy and Embryology.

[50]  B. Håvik,et al.  The zebrafish Pax3 and Pax7 homologues are highly conserved, encode multiple isoforms and show dynamic segment-like expression in the developing brain , 1998, Mechanisms of Development.

[51]  Bruce B. Collette,et al.  The Diversity of Fishes , 1997 .

[52]  P. Ingham,et al.  Notochord induction of zebrafish slow muscle mediated by Sonic hedgehog. , 1997, Genes & development.

[53]  E. Davidson,et al.  Set-aside cells in maximal indirect development: evolutionary and developmental significance. , 1997, BioEssays : news and reviews in molecular, cellular and developmental biology.

[54]  Scott F. Gilbert,et al.  Embryology : constructing the organism , 1997 .

[55]  M. Westerfield,et al.  Identification of separate slow and fast muscle precursor cells in vivo, prior to somite formation. , 1996, Development.

[56]  S. Krauss,et al.  Zebrafish Pax9 Encodes Two Proteins with Distinct C-terminal Transactivating Domains of Different Potency Negatively Regulated by Adjacent N-terminal Sequences* , 1996, The Journal of Biological Chemistry.

[57]  M. Allende,et al.  Developmental regulation of zebrafish MyoD in wild-type, no tail and spadetail embryos. , 1996, Development.

[58]  B. Brand-Saberi,et al.  Angiogenic potential of the avian somite , 1995, Developmental dynamics : an official publication of the American Association of Anatomists.

[59]  I. Johnston.  Temperature influences muscle differentiation and the relative timing of organogenesis in herring (Clupea harengus) larvae , 1993 .

[60]  P. R. Flood,et al.  Origin and differentiation of muscle fibre types in the trunk of the sturgeon, Acipenser stellatus Pallas , 1987 .

[61]  S. R. Hilfer,et al.  Development of the eye of the chick embryo. , 1983, Scanning electron microscopy.

[62]  M. Kieny,et al.  Origin of satellite cells in avian skeletal muscles. , 1983, Archives d'anatomie microscopique et de morphologie experimentale.

[63]  I. Johnston,et al.  Molecular plasticity in the myo fibrillar protein complex of the mummichog fundulus heteroclitus , 1982 .

[64]  O. Hertwig.  Handbuch der Vergleichenden und Experimentellen Entwickelungslehre der Wirbeltiere , 1981 .

[65]  A. Kelly,et al.  Why are fetal muscles slow? , 1980, Nature.

[66]  T. Nakao.  Electron microscopic studies on the myotomes of larval lamprey, Lampetra japonica , 1977, The Anatomical record.

[67]  L. Hamilton.  The formation of somites in Xenopus. , 1969, Journal of embryology and experimental morphology.

[68]  R. Waterman.  Development of the lateral musculature in the teleost, Brachydanio rerio: a fine structural study. , 1969, The American journal of anatomy.

[69]  Armand Louis Jean Sunier.  Les premiers stades de la différentiation interne du myotome et la formation des éléments sclérotomatiques chez les acraniens les sélaciens et les téléostéens , 1911 .

[70]  B..  The Development of the Chick , 1909, Nature.