Differential requirements for myogenic regulatory factors distinguish medial and lateral somitic, cranial and fin muscle fibre populations

Development

Volumn 136, Issue 3, 2009, Pages 403-414

  Hinits, Yaniv ^a   Osborn, Daniel P S ^a   Hughes, Simon M ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Fast; Fibre; Fin; Head; Hedgehog; Hsp90; Mef2d; Meox1; Mrf4 (myf6); Muscle; Myf5; Myod; Myogenin; Myosin; Pax3; Prdm1; Slow; Zebrafish

Indexed keywords

MYOD PROTEIN; MYOGENIC FACTOR 5; MYOGENIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BODY DISTRIBUTION; CELL DIFFERENTIATION; CELL POPULATION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; EMBRYO DEVELOPMENT; FAST MUSCLE FIBER; FISH GENETICS; GENE ACTIVITY; GENE FUNCTION; MUSCLE DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; SKULL DEVELOPMENT; SLOW MUSCLE FIBER; SOMITE; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BODY PATTERNING; EXTREMITIES; HEDGEHOG PROTEINS; LARVA; MUSCLE DEVELOPMENT; MUSCLE FIBERS, SKELETAL; MUTATION; MYOD PROTEIN; MYOGENIC REGULATORY FACTOR 5; MYOGENIC REGULATORY FACTORS; MYOGENIN; ORGAN SPECIFICITY; SOMITES; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO; ERINACEIDAE; MAMMALIA; MUS; VERTEBRATA;

EID: 64549085644     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.028019     Document Type: Article

References (71)

1. Balagopalan, L., Keller, C. A. and Abmayr, S. M. (2001). Loss-of-function mutations reveal that the Drosophila nautilus gene is not essential for embryonic myogenesis or viability. Dev. Biol. 231, 374-382.
2. Baxendale, S., Davison, C., Muxworthy, C., Wolff, C., Ingham, P. W. and Roy, S. (2004). The B-cell maturation factor Blimp-1 specifies vertebrate slow-twitch muscle fiber identity in response to Hedgehog signaling. Nat. Genet. 36, 88-93.
3. Blagden, C. S., Currie, P. D., Ingham, P. W. and Hughes, S. M. (1997). Notochord induction of zebrafish slow muscle mediated by Sonic Hedgehog. Genes Dev. 11, 2163-2175.
4. Borycki, A.-G., Mendham, L. and Emerson, C. P., Jr (1998). Control of somite patterning by Sonic hedgehog and its downstream signal response genes. Development 125, 777-790.
5. Borycki, A.-G., Brunk, B., Tajbakhsh, S., Buckingham, M., Chiang, C. and Emerson, C. P., Jr (1999). Sonic hedgehog controls epaxial muscle determination through Myf5 activation. Development 126, 4053-4063.
6. Braun, T. and Arnold, H.-H. (1996). Myf-5 and myoD genes are activated in distinct mesenchymal stem cells and determine different skeletal muscle cell lineages. EMBO J. 15, 310-318.
7. Braun, T., Bober, E., Rudnicki, M. A., Jaenisch, R. and Arnold, H.-H. (1994). MyoD expression marks the onset of skeletal myogenesis in Myf-5 mutant mice. Development 120, 3083-3092.
8. Bryson-Richardson, R. J., Daggett, D. F., Cortes, F., Neyt, C., Keenan, D. G. and Currie, P. D. (2005). Myosin heavy chain expression in zebrafish and slow muscle composition. Dev. Dyn. 233, 1018-1022.
9. Burke, A. C. and Nowicki, J. L. (2003). A new view of patterning domains in the vertebrate mesoderm. Dev. Cell 4, 159-165.
10. Chen, L., Krause, M., Sepanski, M. and Fire, A. (1994). The Caenorhabditis elegans MYOD homologue HLH-1 is essential for proper muscle function and complete morphogenesis. Development 120, 1631-1641.
11. Chen, Y. H. and Tsai, H. J. (2002). Treatment with Myf5-morpholino results in somite patterning and brain formation defects in zebrafish. Differentiation 70, 447-456.
12. Chen, Y. H., Lee, W. C., Liu, C. F. and Tsai, H. J. (2001). Molecular structure, dynamic expression, and promoter analysis of zebrafish (Danio rerio) myf-5 gene. Genesis 29, 22-35.
13. Concordet, J.-P., Lewis, K. E., Moore, J. W., Goodrich, L. V., Johnson, R. L., Scott, M. P. and Ingham, P. W. (1996). Spatial regulation of a zebrafish patched homologue reflects the roles of sonic hedgehog and protein kinase A in neural tube and somite patterning. Development 122, 2835-2846.
14. Coutelle, O., Blagden, C. S., Hampson, R., Halai, C., Rigby, P. W. and Hughes, S. M. (2001). Hedgehog signalling is required for maintenance of myf5 and myoD expression and timely terminal differentiation in zebrafish adaxial myogenesis. Dev. Biol. 236, 136-150.
15. Devoto, S. H., Melancon, E., Eisen, J. S. and Westerfield, M. (1996). Identification of separate slow and fast muscle precursor cells in vivo, prior to somite formation. Development 122, 3371-3380.
16. Devoto, S. H., Stoiber, W., Hammond, C. L., Steinbacher, P., Haslett, J. R., Barresi, M. J., Patterson, S. E., Adiarte, E. G. and Hughes, S. M. (2006). Generality of vertebrate developmental patterns: evidence for a dermomyotome in fish. Evol. Dev. 8, 101-110.
17. Du, S. J., Li, H., Bian, Y. and Zhong, Y. (2008). Heat-shock protein 90alpha1 is required for organized myofibril assembly in skeletal muscles of zebrafish embryos. Proc. Natl. Acad. Sci. USA 105, 554-559.
18. Eisen, J. S. (1991). Determination of primary motoneuron identity in developing zebrafish embryos. Science 252, 569-571.
19. Ekker, M., Wegner, J., Akimenko, M. A. and Westerfield, M. (1992). Coordinate embryonic expression of three zebrafish engrailed genes. Development 116, 1001-1010.
20. Gensch, N., Borchardt, T., Schneider, A., Riethmacher, D. and Braun, T. (2008). Different autonomous myogenic cell populations revealed by ablation of Myf5-expressing cells during mouse embryogenesis. Development 135, 1597-1604.
21. Grimaldi, A., Tettamanti, G., Martin, B. L., Gaffield, W., Pownall, M. E. and Hughes, S. M. (2004). Hedgehog regulation of superficial slow muscle fibres in Xenopus and the evolution of tetrapod trunk myogenesis. Development 131, 3249-3262.
22. Groves, J. A., Hammond, C. L. and Hughes, S. M. (2005). Fgf8 drives myogenic progression of a novel lateral fast muscle fibre population in zebrafish. Development 132, 4211-4222.
23. Hacker, A. and Guthrie, S. (1998). A distinct developmental programme for the cranial paraxial mesoderm in the chick embryo. Development 125, 3461-3472.
24. Haines, L., Neyt, C., Gautier, P., Keenan, D. G., Bryson-Richardson, R. J., Hollway, G. E., Cole, N. J. and Currie, P. D. (2004). Met and Hgf signaling controls hypaxial muscle and lateral line development in the zebrafish. Development 131, 4857-4869.
25. Haldar, M., Karan, G., Tvrdik, P. and Capecchi, M. R. (2008). Two cell lineages, myf5-dependent and myf5-independent, participate in mouse skeletal myogenesis. Dev. Cell 14, 437-445.
26. Hamade, A., Deries, M., Begemann, G., Bally-Cuif, L., Genet, C., Sabatier, F., Bonnieu, A. and Cousin, X. (2006). Retinoic acid activates myogenesis in vivo through Fgf8 signalling. Dev. Biol. 289, 127-140.
27. Hammond, C. L., Hinits, Y., Osborn, D. P., Minchin, J. E., Tettamanti, G. and Hughes, S. M. (2007). Signals and myogenic regulatory factors restrict pax3 and pax7 expression to dermomyotome-like tissue in zebrafish. Dev. Biol. 302, 504-521.
28. Hasty, P., Bradley, A., Morris, J. H., Edmondson, D. G., Venuti, J. M., Olson, E. N. and Klein, W. H. (1993). Muscle deficiency and neonatal death in mice with targeted mutation in the myogenin gene. Nature 364, 501-506.
29. Hawkins, T. A., Haramis, A. P., Etard, C., Prodromou, C., Vaughan, C. K., Ashworth, R., Ray, S., Behra, M., Holder, N., Talbot, W. S. et al. (2008). The ATPase-dependent chaperoning activity of Hsp90a regulates thick filament formation and integration during skeletal muscle myofibrillogenesis. Development 135, 1147-1156.
30. Henry, C. A. and Amacher, S. L. (2004). Zebrafish slow muscle cell migration induces a wave of fast muscle morphogenesis. Dev. Cell 7, 917-923.
31. Higashijima, S., Nose, A., Eguchi, G., Hotta, Y. and Okamoto, H. (1997). Mindin/F-spondin family: novel ECM proteins expressed in the zebrafish embryonic axis. Dev. Biol. 192, 211-227.
32. Hinits, Y. and Hughes, S. M. (2007). Mef2s are required for thick filament formation in nascent muscle fibres. Development 134, 2511-2519.
33. Hinits, Y., Osborn, D. P., Carvajal, J. J., Rigby, P. W. and Hughes, S. M. (2007). Mrf4 (myf6) is dynamically expressed in differentiated zebrafish skeletal muscle. Gene Expr. Patterns 7, 738-745.
34. Hopwood, N. D., Pluck, A. and Gurdon, J. B. (1991). Xenopus Myf-5 marks early muscle cells and can activate muscle genes ectopically in early embryos. Development 111, 551-560.
35. Isken, O. and Maquat, L. E. (2007). Quality control of eukaryotic mRNA: safeguarding cells from abnormal mRNA function. Genes Dev. 21, 1833-1856.
36. Kablar, B., Krastel, K., Ying, C., Asakura, A., Tapscott, S. J. and Rudnicki, M. A. (1997). MyoD and Myf-5 differentially regulate the development of limb versus trunk skeletal muscle. Development 124, 4729-4738.
37. Kablar, B., Asakura, A., Krastel, K., Ying, C., May, L. L., Goldhamer, D. J. and Rudnicki, M. A. (1998). MyoD and Myf-5 define the specification of musculature of distinct embryonic origin. Biochem. Cell Biol. 76, 1079-1091.
38. Kahane, N., Cinnamon, Y., Bachelet, I. and Kalcheim, C. (2001). The third wave of myotome colonization by mitotically competent progenitors: regulating the balance between differentiation and proliferation during muscle development. Development 128, 2187-2198.
39. Kassar-Duchossoy, L., Gayraud-Morel, B., Gomes, D., Rocancourt, D., Buckingham, M., Shinin, V. and Tajbakhsh, S. (2004). Mrf4 determines skeletal muscle identity in Myf5:Myod double-mutant mice. Nature 431, 466-471.
40. Kaul, A., Koster, M., Neuhaus, H. and Braun, T. (2000). Myf-5 revisited: loss of early myotome formation does not lead to a rib phenotype in homozygous Myf-5 mutant mice. Cell 102, 17-19.
41. Koudijs, M. J., den Broeder, M. J., Groot, E. and van Eeden, F. J. (2008). Genetic analysis of the two zebrafish patched homologues identifies novel roles for the hedgehog signaling pathway. BMC Dev. Biol. 8, 15.
42. Lacalli, T. C. (2002). The dorsal compartment locomotory control system in amphioxus larvae. J. Morphol. 252, 227-237.
43. Liew, H. P., Choksi, S. P., Wong, K. N. and Roy, S. (2008). Specification of vertebrate slow-twitch muscle fiber fate by the transcriptional regulator Blimp1. Dev. Biol. 324, 226-235.
44. Lin, C. Y., Yung, R. F., Lee, H. C., Chen, W. T., Chen, Y. H. and Tsai, H. J. (2006). Myogenic regulatory factors Myf5 and Myod function distinctly during craniofacial myogenesis of zebrafish. Dev. Biol. 299, 594-608.
45. Maves, L., Waskiewicz, A. J., Paul, B., Cao, Y., Tyler, A., Moens, C. B. and Tapscott, S. J. (2007). Pbx homeodomain proteins direct Myod activity to promote fast-muscle differentiation. Development 134, 3371-3382.
46. Meedel, T. H., Chang, P. and Yasuo, H. (2007). Muscle development in Ciona intestinalis requires the b-HLH myogenic regulatory factor gene Ci-MRF. Dev. Biol. 302, 333-344.
47. Moore, C. A., Parkin, C. A., Bidet, Y. and Ingham, P. W. (2007). A role for the Myoblast city homologues Dock1 and Dock5 and the adaptor proteins Crk and Crk-like in zebrafish myoblast fusion. Development 134, 3145-3153.
48. Morin-Kensicki, E. M. and Eisen, J. S. (1997). Sclerotome development and peripheral nervous system segmentation in embryonic zebrafish. Development 124, 159-167.
49. Nabeshima, Y., Hanaoka, K., Hayasaka, M., Esumi, E., Li, S., Nonaka, I. and Nabeshima, Y.-i. (1993). Myogenin gene disruption results in perinatal lethality owing to severe muscle defect. Nature 364, 532-535.
50. Neyt, C., Jagla, K., Thisse, C., Thisse, B., Haines, L. and Currie, P. D. (2000). Evolutionary origins of vertebrate appendicular muscle. Nature 408, 82-86.
51. Patterson, S. E., Mook, L. B. and Devoto, S. H. (2008). Growth in the larval zebrafish pectoral fin and trunk musculature. Dev. Dyn. 237, 307-315.
52. Penn, B. H., Bergstrom, D. A., Dilworth, F. J., Bengal, E. and Tapscott, S. J. (2004). A MyoD-generated feed-forward circuit temporally patterns gene expression during skeletal muscle differentiation. Genes Dev. 18, 2348-2353.
53. Rawls, A., Morris, J. H., Rudnicki, M., Braun, T., Arnold, H.-H., Klein, W. H. and Olson, E. N. (1995). Myogenin's functions do not overlap with those of MyoD or Myf-5 during mouse embryogenesis. Dev. Biol. 172, 37-50.
54. Rawls, A., Valdez, M. R., Zhang, W., Richardson, J., Klein, W. H. and Olson, E. N. (1998). Overlapping functions of the myogenic bHLH genes MRF4 and MyoD revealed in double mutant mice. Development 125, 2349-2358.
55. Rudnicki, M. A., Braun, T., Hinuma, S. and Jaenisch, R. (1992). Inactivation of MyoD in mice leads to up-regulation of the myogenic HLH gene Myf-5 and results in apparently normal muscle development. Cell 71, 383-390.
56. Rudnicki, M. A., Schnegelsberg, P. N., Stead, R. H., Braun, T., Arnold, H.-H. and Jaenisch, R. (1993). MyoD or Myf-5 is required for the formation of skeletal muscle. Cell 75, 1351-1359.
57. Sambasivan, R. and Tajbakhsh, S. (2007). Skeletal muscle stem cell birth and properties. Semin. Cell Dev. Biol. 18, 870-882.
58. Stellabotte, F., Dobbs-McAuliffe, B., Fernandez, D. A., Feng, X. and Devoto, S. H. (2007). Dynamic somite cell rearrangements lead to distinct waves of myotome growth. Development 134, 1253-1257.
59. Stemple, D. L. (2004). TILLING-a high-throughput harvest for functional genomics. Nat. Rev. Genet. 5, 145-150.
60. Tajbakhsh, S., Rocancourt, D., Cossu, G. and Buckingham, M. (1997). Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf-5 act upstream of MyoD. Cell 89, 127-138.
61. Ticho, B. S., Stainier, D. Y. R., Fishman, M. C. and Breitbart, R. E. (1996). Three zebrafish MEF2 genes delineate somitic and cardiac muscle development in wildtype and mutant embryos. Mech. Dev. 59, 205-218.
62. Valdez, M. R., Richardson, J. A., Klein, W. H. and Olson, E. N. (2000). Failure of Myf5 to support myogenic differentiation without myogenin, MyoD, and MRF4. Dev. Biol. 219, 287-298.
63. Venuti, J. M., Morris, J. H., Vivian, J. L., Olson, E. N. and Klein, W. H. (1995). Myogenin is required for late but not early aspects of myogenesis during mouse development. J. Cell Biol. 128, 563-576.
64. Wang, Y. H., Li, C. K., Lee, G. H., Tsay, H. J., Tsai, H. J. and Chen, Y. H. (2008). Inactivation of zebrafish mrf4 leads to myofibril misalignment and motor axon growth disorganization. Dev. Dyn. 237, 1043-1050.
65. Weinberg, E. S., Allende, M. L., Kelly, C. S., Abdelhamid, A., Murakami, T., Andermann, P., Doerre, O. G., Grunwald, D. J. and Riggleman, B. (1996). Developmental regulation of zebrafish MyoD in wild-type, no tail and spadetail embryos. Development 122, 271-280.
66. Weintraub, H. (1993). The MyoD family and myogenesis: redundancy, networks, and thresholds. Cell 75, 1241-1244.
67. Westerfield, M. (1995). The Zebrafish Book. A Guide for the Laboratory Use of Zebrafish (Danio rerio). Eugene, OR: University of Oregon Press.
68. Wolff, C., Roy, S. and Ingham, P. W. (2003). Multiple muscle cell identities induced by distinct levels and timing of hedgehog activity in the zebrafish embryo. Curr. Biol. 13, 1169-1181.
69. Wotton, K. R., Weierud, F. K., Dietrich, S. and Lewis, K. E. (2008). Comparative genomics of Lbx loci reveals conservation of identical Lbx ohnologs in bony vertebrates. BMC Evol. Biol. 8, 171.
70. Xu, Y., He, J., Wang, X., Lim, T. M. and Gong, Z. (2000). Asynchronous activation of 10 muscle-specific protein (MSP) genes during zebrafish somitogenesis. Dev. Dyn. 219, 201-215.
71. Zhang, W., Behringer, R. R. and Olson, E. N. (1995). Inactivation of the myogenic bHLH gene MRF4 results in up-regulation of myogenin and rib anomalies. Genes Dev. 9, 1388-1399.