Expression and interaction of muscle-related genes in the lamprey imply the evolutionary scenario for vertebrate skeletal muscle, in association with the acquisition of the neck and fins

Developmental Biology

Volumn 350, Issue 1, 2011, Pages 217-227

  Kusakabe, Rie ^a,b   Kuraku, Shigehiro ^b,c   Kuratani, Shigeru ^b  

^a KOBE UNIVERSITY   (Japan)

^b RIKEN Center for Biosystems Dynamics Research   (Japan)

^c UNIVERSITY OF KONSTANZ   (Germany)

Author keywords

Hypobranchial muscle; Lamprey; Lbx; Myogenic regulatory factors (MRF); Pax3 7; Skeletal muscle; Somites

Indexed keywords

MYOGENIC FACTOR; TRANSCRIPTION FACTOR PAX3; TRANSCRIPTION FACTOR PAX7;

ARTICLE; CONTROLLED STUDY; CYCLOSTOME; DEVELOPMENTAL BIOLOGY; EMBRYO DEVELOPMENT; GENE EXPRESSION; GENE INTERACTION; GENE SEQUENCE; LAMPREY; MOLECULAR EVOLUTION; MYOTOME; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; SEQUENCE HOMOLOGY; SKELETAL MUSCLE; SOMITE; TOPOGRAPHY;

GNATHOSTOMATA (VERTEBRATE); HAGFISH; PETROMYZONTIDAE; TELEOSTEI; VERTEBRATA;

EID: 78651237586     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2010.10.029     Document Type: Article

References (69)

1. Alvares L.E., Schubert F.R., Thorpe C., Mootoosamy R.C., Cheng L., Parkyn G., Lumsden A., Dietrich S. Intrinsic, Hox-dependent cues determine the fate of skeletal muscle precursors. Dev. Cell 2003, 5:379-390.
2. Araki I., Terazawa K., Satoh N. Duplication of an amphioxus myogenic bHLH gene is independent of vertebrate myogenic bHLH gene duplication. Gene 1996, 171:231-236.
3. Bajard L., Relaix F., Lagha M., Rocancourt D., Daubas P., Buckingham M.E. A novel genetic hierarchy functions during hypaxial myogenesis: Pax3 directly activates Myf5 in muscle progenitor cells in the limb. Genes Dev. 2006, 20:2450-2464.
4. Barresi M.J., D'Angelo J.A., Hernandez L.P., Devoto S.H. Distinct mechanisms regulate slow-muscle development. Curr. Biol. 2001, 11:1432-1438.
5. Bladt F., Riethmacher D., Isenmann S., Aguzzi A., Birchmeier C. Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud. Nature 1995, 376:768-771.
6. Brohmann H., Jagla K., Birchmeier C. The role of Lbx1 in migration of muscle precursor cells. Development 2000, 127:437-445.
7. Burke A.C., Nowicki J.L. A new view of patterning domains in the vertebrate mesoderm. Dev. Cell 2003, 4:159-165.
8. Devoto S.H., Melancon E., Eisen J.S., Westerfield M. Identification of separate slow and fast muscle precursor cells in vivo, prior to somite formation. Development 1996, 122:3371-3380.
9. Dietrich S., Schubert F.R., Healy C., Sharpe P.T., Lumsden A. Specification of the hypaxial musculature. Development 1998, 125:2235-2249.
10. Dietrich S., Abou-Rebyeh F., Brohmann H., Bladt F., Sonnenberg-Riethmacher E., Yamaai T., Lumsden A., Brand-Saberi B., Birchmeier C. The role of SF/HGF and c-Met in the development of skeletal muscle. Development 1999, 126:1621-1629.
11. Freitas R., Zhang G., Cohn M.J. Evidence that mechanisms of fin development evolved in the midline of early vertebrates. Nature 2006, 442:1033-1037.
12. Goulding M.D., Chalepakis G., Deutsch U., Erselius J.R., Gruss P. Pax-3, a novel murine DNA binding protein expressed during early neurogenesis. EMBO J. 1991, 10:1135-1147.
13. Goulding M., Lumsden A., Paquette A.J. Regulation of Pax-3 expression in the dermomyotome and its role in muscle development. Development 1994, 120:957-971.
14. Grimaldi A., Tettamanti G., Martin B.L., Gaffield W., Pownall M.E., Hughes S.M. Hedgehog regulation of superficial slow muscle fibres in Xenopus and the evolution of tetrapod trunk myogenesis. Development 2004, 131:3249-3262.
15. Gross M.K., Moran-Rivard L., Velasquez T., Nakatsu M.N., Jagla K., Goulding M. Lbx1 is required for muscle precursor migration along a lateral pathway into the limb. Development 2000, 127:413-424.
16. Guindon S., Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 2003, 52:696-704.
17. Haines L., Neyt C., Gautier P., Keenan D.G., Bryson-Richardson R.J., Hollway G.E., Cole N.J., Currie P.D. Met and Hgf signaling controls hypaxial muscle and lateral line development in the zebrafish. Development 2004, 131:4857-4869.
18. Holland L.Z., Schubert M., Kozmik Z., Holland N.D. AmphiPax3/7, an amphioxus paired box gene: insights into chordate myogenesis, neurogenesis, and the possible evolutionary precursor of definitive vertebrate neural crest. Evol. Dev. 1999, 1:153-165.
19. Hollway G.E., Currie P.D. Myotome meanderings. Cellular morphogenesis and the making of muscle. EMBO Rep. 2003, 4:855-860.
20. Jagla K., Dolle P., Mattei M.G., Jagla T., Schuhbaur B., Dretzen G., Bellard F., Bellard M. Mouse Lbx1 and human LBX1 define a novel mammalian homeobox gene family related to the Drosophila lady bird genes. Mech. Dev. 1995, 53:345-356.
21. Jostes B., Walther C., Gruss P. The murine paired box gene, Pax7, is expressed specifically during the development of the nervous and muscular system. Mech. Dev. 1990, 33:27-37.
22. Kablar B., Krastel K., Ying C., Asakura A., Tapscott S.J., Rudnicki M.A. MyoD and Myf-5 differentially regulate the development of limb versus trunk skeletal muscle. Development 1997, 124:4729-4738.
23. Kassar-Duchossoy L., Gayraud-Morel B., Gomes D., Rocancourt D., Buckingham M., Shinin V., Tajbakhsh S. Mrf4 determines skeletal muscle identity in Myf5:Myod double-mutant mice. Nature 2004, 431:466-471.
24. Kuraku S., Kuratani S. Time scale for cyclostome evolution inferred with a phylogenetic diagnosis of hagfish and lamprey cDNA sequences. Zoolog Sci. 2006, 23:1053-1064.
25. Kuraku S., Takio Y., Tamura K., Aono H., Meyer A., Kuratani S. Noncanonical role of Hox14 revealed by its expression patterns in lamprey and shark. Proc. Natl Acad. Sci. USA 2008, 105:6679-6683.
26. Kuraku S., Meyer A., Kuratani S. Timing of genome duplications relative to the origin of the vertebrates: did cyclostomes diverge before or after?. Mol. Biol. Evol. 2009, 26:47-59.
27. Kuratani S. Evolutionary developmental studies of cyclostomes and the origin of the vertebrate neck. Dev. Growth Differ. 2008, 50(Suppl 1):S189-S194.
28. Kuratani S., Ota K.G. Primitive versus derived traits in the developmental program of the vertebrate head: views from cyclostome developmental studies. J. Exp. Zool. B Mol. Dev. Evol. 2008, 310:294-314.
29. Kuratani S., Ueki T., Aizawa S., Hirano S. Peripheral development of cranial nerves in a cyclostome, Lampetra japonica: morphological distribution of nerve branches and the vertebrate body plan. J. Comp. Neurol. 1997, 384:483-500.
30. Kuratani S., Horigome N., Hirano S. Developmental morphology of the head mesoderm and reevaluation of segmental theories of the vertebrate head: evidence from embryos of an agnathan vertebrate, Lampetra japonica. Dev. Biol. 1999, 210:381-400.
31. Kusakabe R., Kuratani S. Evolution and developmental patterning of the vertebrate skeletal muscles: perspectives from the lamprey. Dev. Dyn. 2005, 234:824-834.
32. Kusakabe R., Kuratani S. Evolutionary perspectives from development of mesodermal components in the lamprey. Dev. Dyn. 2007, 236:2410-2420.
33. Kusakabe R., Takechi M., Tochinai S., Kuratani S. Lamprey contractile protein genes mark different populations of skeletal muscles during development. J. Exp. Zoolog. B, Mol. Dev. Evol. 2004, 302:121-133.
34. Martin B.L., Harland R.M. Hypaxial muscle migration during primary myogenesis in Xenopus laevis. Dev. Biol. 2001, 239:270-280.
35. Martin B.L., Harland R.M. A novel role for lbx1 in Xenopus hypaxial myogenesis. Development 2006, 133:195-208.
36. Matsuoka T., Ahlberg P.E., Kessaris N., Iannarelli P., Dennehy U., Richardson W.D., McMahon A.P., Koentges G. Neural crest origins of the neck and shoulder. Nature 2005, 436:347-355.
37. Matsuura M., Nishihara H., Onimaru K., Kokubo N., Kuraku S., Kusakabe R., Okada N., Kuratani S., Tanaka M. Identification of four engrailed genes in the Japanese lamprey, Lethenteron japonicum. Dev. Dyn. 2008, 237:1581-1589.
38. McCauley D.W., Bronner-Fraser M. Conservation of Pax gene expression in ectodermal placodes of the lamprey. Gene 2002, 287:129-139.
39. Mennerich D., Schafer K., Braun T. Pax-3 is necessary but not sufficient for lbx1 expression in myogenic precursor cells of the limb. Mech. Dev. 1998, 73:147-158.
40. Nagai T., Aruga J., Takada S., Gunther T., Sporle R., Schughart K., Mikoshiba K. The expression of the mouse Zic1, Zic2, and Zic3 gene suggests an essential role for Zic genes in body pattern formation. Dev. Biol. 1997, 182:299-313.
41. Nakao T. Electron microscopic studies on the myotomes of larval lamprey, Lampetra japonica. Anat. Rec. 1977, 187:383-404.
42. Neyt C., Jagla K., Thisse C., Thisse B., Haines L., Currie P.D. Evolutionary origins of vertebrate appendicular muscle. Nature 2000, 408:82-86.
43. Noden D.M., Francis-West P. The differentiation and morphogenesis of craniofacial muscles. Dev. Dyn. 2006, 235:1194-1218.
44. Nowicki J.L., Takimoto R., Burke A.C. The lateral somitic frontier: dorso-ventral aspects of anterio-posterior regionalization in avian embryos. Mech. Dev. 2003, 120:227-240.
45. Ochi H., Westerfield M. Lbx2 regulates formation of myofibrils. BMC Dev. Biol. 2009, 9:13.
46. Ohtani K., Yao T., Kobayashi M., Kusakabe R., Kuratani S., Wada H. Expression of Sox and fibrillar collagen genes in lamprey larval chondrogenesis with implications for the evolution of vertebrate cartilage. J. Exp. Zoolog. B, Mol. Dev. Evol. 2008, 310:596-607.
47. Ohtsuka M., Kikuchi N., Ozato K., Inoko H., Kimura M. Comparative analysis of a 229-kb medaka genomic region, containing the zic1 and zic4 genes, with Fugu, human, and mouse. Genomics 2004, 83:1063-1071.
48. Ohtsuka M., Kikuchi N., Yokoi H., Kinoshita M., Wakamatsu Y., Ozato K., Takeda H., Inoko H., Kimura M. Possible roles of zic1 and zic4, identified within the medaka Double anal fin (Da) locus, in dorsoventral patterning of the trunk-tail region (related to phenotypes of the Da mutant). Mech. Dev. 2004, 121:873-882.
49. Ota K.G., Kuraku S., Kuratani S. Hagfish embryology with reference to the evolution of the neural crest. Nature 2007, 446:672-675.
50. Patterson S.E., Mook L.B., Devoto S.H. Growth in the larval zebrafish pectoral fin and trunk musculature. Dev. Dyn. 2008, 237:307-315.
51. Peters A., Mackay B. The structure and innervation of the myotomes of the lamprey. J. Anat. 1961, 95:575-585.
52. Pownall M.E., Gustafsson M.K., Emerson C.P. Myogenic regulatory factors and the specification of muscle progenitors in vertebrate embryos. Annu. Rev. Cell Dev. Biol. 2002, 18:747-783.
53. Prunotto C., Crepaldi T., Forni P.E., Ieraci A., Kelly R.G., Tajbakhsh S., Buckingham M., Ponzetto C. Analysis of Mlc-lacZ Met mutants highlights the essential function of Met for migratory precursors of hypaxial muscles and reveals a role for Met in the development of hyoid arch-derived facial muscles. Dev. Dyn. 2004, 231:582-591.
54. Relaix F., Rocancourt D., Mansouri A., Buckingham M. Divergent functions of murine Pax3 and Pax7 in limb muscle development. Genes Dev. 2004, 18:1088-1105.
55. Relaix F., Rocancourt D., Mansouri A., Buckingham M. A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature 2005, 435:948-953.
56. Sauka-Spengler T., Meulemans D., Jones M., Bronner-Fraser M. Ancient evolutionary origin of the neural crest gene regulatory network. Dev. Cell 2007, 13:405-420.
57. Scaal M., Wiegreffe C. Somite compartments in anamniotes. Anat Embryol. (Berl) 2006, 211(Suppl 1):9-19.
58. Schubert F.R., Dietrich S., Mootoosamy R.C., Chapman S.C., Lumsden A. Lbx1 marks a subset of interneurons in chick hindbrain and spinal cord. Mech. Dev. 2001, 101:181-185.
59. Steinbacher P., Haslett J.R., Obermayer A., Marschallinger J., Bauer H.C., Sanger A.M., Stoiber W. MyoD and myogenin expression during myogenic phases in brown trout: a precocious onset of mosaic hyperplasia is a prerequisite for fast somatic growth. Dev. Dyn. 2007, 236:1106-1114.
60. Stickney H.L., Barresi M.J., Devoto S.H. Somite development in zebrafish. Dev. Dyn. 2000, 219:287-303.
61. Sun Rhodes L.S., Merzdorf C.S. The zic1 gene is expressed in chick somites but not in migratory neural crest. Gene Expr. Patterns 2006, 6:539-545.
62. Tahara Y. Normal stages of development in the lamprey, Lampetra reissneri (Dybowski). Zool. Sci. 1988, 5:109-118.
63. Tajbakhsh S., Rocancourt D., Cossu G., Buckingham M. Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf-5 act upstream of MyoD. Cell 1997, 89:127-138.
64. Takio Y., Kuraku S., Murakami Y., Pasqualetti M., Rijli F.M., Narita Y., Kuratani S., Kusakabe R. Hox gene expression patterns in Lethenteron japonicum embryos-insights into the evolution of the vertebrate Hox code. Dev. Biol. 2007, 308:606-620.
65. Uchiyama K., Ishikawa A., Hanaoka K. Expression of lbx1 involved in the hypaxial musculature formation of the mouse embryo. J. Exp. Zool. 2000, 286:270-279.
66. Venkatesh B., Kirkness E.F., Loh Y.H., Halpern A.L., Lee A.P., Johnson J., Dandona N., Viswanathan L.D., Tay A., Venter J.C., Strausberg R.L., Brenner S. Survey sequencing and comparative analysis of the elephant shark (Callorhinchus milii) genome. PLoS Biol. 2007, 5:e101.
67. Wada H., Holland P.W., Sato S., Yamamoto H., Satoh N. Neural tube is partially dorsalized by overexpression of HrPax-37: the ascidian homologue of Pax-3 and Pax-7. Dev. Biol. 1997, 187:240-252.
68. Weintraub H. The MyoD family and myogenesis: redundancy, networks, and thresholds. Cell 1993, 75:1241-1244.
69. Wotton K.R., Weierud F.K., Dietrich S., Lewis K.E. Comparative genomics of Lbx loci reveals conservation of identical Lbx ohnologs in bony vertebrates. BMC Evol. Biol. 2008, 8:171.