Regulation of myogenic differentiation in the developing limb bud

Journal of Anatomy

Volumn 202, Issue 1, 2003, Pages 69-81

  Francis West, Philippa H ^a   Antoni, Laurent ^a   Anakwe, Kelly ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Bmp; Fibretype; Muscle; Shh; Wnt

Indexed keywords

MYOD PROTEIN; MYOGENIC FACTOR; MYOGENIC FACTOR 5; MYOSIN HEAVY CHAIN; UNCLASSIFIED DRUG;

BODY POSTURE; CELL DIFFERENTIATION; CELL MIGRATION; DERMOMYOTOME; FAST MUSCLE FIBER; LIMB DEVELOPMENT; MESODERM; MOLECULAR BIOLOGY; MUSCLE CELL; MUSCLE CONTRACTILITY; MUSCLE FORCE; MUSCLE FUNCTION; MYOGENIC CELL; MYOTOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; STEM CELL;

ANIMALS; EMBRYONIC INDUCTION; EXTREMITIES; GENE EXPRESSION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; MORPHOGENESIS; MUSCLE FIBERS, FAST-TWITCH; MUSCLE FIBERS, SLOW-TWITCH; MUSCLES; MYOGENIC REGULATORY FACTORS; TRANS-ACTIVATORS; VERTEBRATES;

EID: 0037278554     PISSN: 00218782     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1469-7580.2003.00136.x     Document Type: Review

References (121)

1. Akita K (1996) The effect of the ectoderm on the dorsoventral pattern of epidermis, muscles and joints in the developing chick leg: a new model. Anat. Embryol. (Berl.) 193, 377-386.
2. Amthor H, Christ Weil M, Patel K (1998) The importance of timing differentiation during limb muscle development. Curr. Biol. 8, 642-652.
3. Barresi MJ, Stickney H, Devoto SH (2000) The zebrafish slow-muscle-omitted gene product is required for Hedgehog signal transduction and the development of slow muscle identity. Development 127, 2189-2199.
4. Beddington RS, Martin P (1989) An in situ transgenic enzyme marker to monitor migration of cells in the mid-gestation mouse embryo. Somite contribution to the early forelimb bud. Mol. Biol. Med. 6, 263-274.
5. Bendall AJ, Ding J, Hu G, Shen MM, Abate-Shen C (1999) Msx1 antagonizes the myogenic activity of Pax3 in migrating limb muscle precursors. Development 126, 4965-4976.
6. Berk M, Desai SY, Heyman HC, Colmenares C (1997) Mice lacking the ski proto-oncogene have defects in neurulation, craniofacial, patterning, and skeletal muscle development. Genes Dev. 11, 2029-2039.
7. Bigard X, Sanchez H, Zoll J, Mateo P, Rousseau V, Veksler V, et al. (2000) Calcineurin co-regulates contractile and metabolic components of slow muscle phenotype. J. Biol. Chem. 275, 19653-19660.
8. Blagden CS, Currie PD, Ingham PW, Hughes SM (1997) Notochord induction of zebrafish slow muscle mediated by Sonic hedgehog. Genes Dev. 11, 2163-2175.
9. Borello U, Coletta M, Tajbakhsh S, Leyns L, De Robertis EM, Buckingham M, et al. (1999) Transplacental delivery of the Wnt antagonist Frzb1 inhibits development of caudal paraxial mesoderm and skeletal myogenesis in mouse embryos. Development 126, 4247-4255.
10. Brand-Saberi B, Krenn V, Grim M, Christ B (1993) Differences in the fibronectin-dependence of migrating cell populations. Anat. Embryol. (Berl.) 187, 17-26.
11. Brand-Saberi B, Wilting J, Ebensperger C, Christ B (1996) The formation of somite compartments in the avian embryo. Int. J. Dev. Biol. 40, 411-420.
12. Bren-Mattison Y, Olwin BB (2002) Sonic hedgehog inhibits the terminal differentiation of limb myoblasts committed to the slow muscle lineage. Dev. Biol. 242, 130-148.
13. Brohmann H, Jagla K, Birchmeier C (2000) The role of Lbx1 in migration of muscle precursor cells. Development 127, 437-445.
14. Cann GM, Lee JW, Stockdale FE (1999) Sonic hedgehog enhances somite cell viability and formation of primary slow muscle fibers in avian segmented mesoderm. Anat. Embryol. (Berl.) 200, 239-252.
15. Chevallier A, Kieny M, Mauger A (1977) Limb-somite relationship: origin of the limb musculature. J. Embryol. Exp. Morph. 41, 245-258.
16. Chin ER, Olson EN, Richardson JA, Yang Q, Humphries C, Shelton JM, et al. (1998) A calcineurin-dependent transcriptional pathway controls skeletal muscle fiber type. Genes Dev. 12, 2499-2509.
17. Christ B, Jacob HJ, Jacob M (1977) [Experimental findings on muscle development in the limbs of the chick embryo]. Verh. Anat. Ges. 71, 1231-1237.
18. Clase KL, Mitchell PJ, Ward PJ, Dorman CM, Johnson SE, Hannon K (2000) FGF5 stimulates expansion of connective tissue fibroblasts and inhibits skeletal muscle development in the limb. Dev. Dyn. 219, 368-380.
19. Cossu G, Molinaro M (1987) Cell heterogeneity in the myogenic lineage. Curr. Top. Dev. Biol. 23, 185-208.
20. Currie PD, Ingham PW (1996) Induction of a specific muscle cell type by a hedgehog-like protein in zebrafish. Nature 382, 452-455.
21. Daston G, Lamar E, Olivier M, Goulding M (1996) Pax-3 is necessary for migration but not differentiation of limb muscle precursors in the mouse. Development 122, 1017-1027.
22. Delfini M, Hirsinger E, Pourquie O, Duprez D (2000) Delta 1-activated notch inhibits muscle differentiation without affecting Myf5 and Pax3 expression in chick limb myogenesis. Development 127, 5213-5224.
23. Delling U, Tureckova J, Lim HW, De Windt LJ, Rotwein P, Molkentin JD (2000) A calcineurin-NFATc3-dependent pathway regulates skeletal muscle differentiation and slow myosin heavy-chain expression. Mol. Cell Biol. 20, 6600-6611.
24. DiMario JX, Fernyak SE, Stockdale FE (1993) Myoblasts transferred to the limbs of embryos are committed to specific fibre fates. Nature 362, 165-167.
25. DiMario JX, Stockdale FE (1995) Differences in the developmental fate of cultured and noncultured myoblasts when transplanted into embryonic limbs. Exp. Cell Res. 216, 431-442.
26. DiMario JX, Stockdale FE (1997) Both myoblast lineage and innervation determine fiber type and are required for expression of the slow myosin heavy chain 2 gene. Dev. Biol. 188, 167-180.
27. Du SJ, Devoto SH, Westerfield M, Moon RT (1997) Positive and negative regulation of muscle cell identity by members of the hedgehog and TGF-beta gene families. J. Cell Biol. 139, 145-156.
28. Dunn SE, Burns JL, Michel RN (1999) Calcineurin is required for skeletal muscle hypertrophy. J. Biol. Chem. 274, 21908-21912.
29. Duprez D, Fournier-Thibault C, Le Douarin N (1998) Sonic Hedgehog induces proliferation of committed skeletal muscle cells in the chick limb. Development 125, 495-505.
30. Duxson MJ, Usson Y, Harris AJ (1989) The origin of secondary myotubes in mammalian skeletal muscles: ultrastructural studies. Development 107, 743-750.
31. Edom-Vovard F, Bonnin MA, Duprez D (2001) Misexpression of Fgf-4 in the chick limb inhibits myogenesis by down-regulating Frek expression. Dev. Biol. 233, 56-71.
32. Epstein JA, Shapiro DN, Cheng J, Lam PY, Maas RL (1996) Pax3 modulates expression of the c-Met receptor during limb muscle development. Proc. Natl Acad. Sci. USA 93, 4213-4218.
33. Evans D, Baillie H, Caswell A, Wigmore P (1994) During fetal muscle development clones of cells contribute to both primary and secondary fibers. Dev. Biol. 162 (2), 348-353.
34. Faerman A, Goldhamer DJ, Puzis R, Emerson CP Jr, Shani M (1995) The distal human myoD enhancer sequences direct unique muscle-specific patterns of lacZ. expression during mouse development. Dev. Biol. 171, 27-38.
35. Flanagan-Steet H, Hannon K, McAvoy MJ, Hullinger R, Olwin BB (2000) Loss of FGF receptor 1 signaling reduces skeletal muscle mass and disrupts myofiber organization in the developing limb. Dev. Biol. 218, 21-37.
36. Fredette BJ, Landmesser LT (1991) Relationship of primary and secondary myogenesis to fiber type development in embryonic chick muscle. Dev. Biol. 143, 1-18.
37. Goldhamer DJ, Brunk BP, Faerman A, King A, Shani M, Emerson CP Jr (1995) Embryonic activation of the myoD gene is regulated by a highly conserved distal control element. Development 121, 637-649.
38. Grobet L, Martin LJ, Poncelet D, Pirottin D, Brouwers B, Riquet J, et al. (1997) A deletion in the bovine myostatin gene causes the double-muscled phenotype in cattle. Nature Genet 17, 71-74.
39. Gross MK, Moran-Rivard L, Velasquez T, Nakatsu MN, Jagla K, Goulding M (2000) Lbx1 is required for muscle precursor migration along a lateral pathway into the limb. Development 127, 413-424.
40. Hasty P, Bradley A, Morris JH, Edmondson DG, Venuti JM, Olson EN, et al. (1993) Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature 364, 501-506.
41. Haub O, Goldfarb M (1991) Expression of the fibroblast growth factor-5 gene in the mouse embryo. Development 112, 397-406.
42. Hayashi K, Ozawa E (1995) Myogenic cell migration from somites is induced by tissue contact with medial region of the presumptive limb mesoderm in chick embryos. Development 121, 661-669.
43. Heymann S, Koudrova M, Arnold H, Koster M, Braun T (1996) Regulation and function of SF/HGF during migration of limb muscle precursor cells in chicken. Dev. Biol. 180, 566-578.
44. Hilfer SR, Searls RL, Fonte VG (1973) An ultrastructural study of early myogenesis in the chick wing bud. Dev. Biol. 30, 374-391.
45. Houzelstein D, Auda-Boucher G, Cheraud Y, Rouaud T, Blanc I, Tajbakhsh S, et al. (1999) The homeobox gene Msx1 is expressed in a subset of somites, and in muscle progenitor cells migrating into the forelimb. Development 126, 2689-2701.
46. Hughes SM, Blau HM (1992) Muscle fiber pattern is independent of cell lineage in postnatal rodent development. Cell 68, 659-671.
47. Hughes SM, Koishi K, Rudnicki M, Maggs AM (1997) MyoD protein is differentially accumulated in fast and slow skeletal muscle fibres and required for normal fibre type balance in rodents. Mech. Dev. 61, 151-163.
48. Hughes SM, Chi MM, Lowry OH, Gundersen K (1999) Myogenin induces a shift of enzyme activity from glycolytic to oxidative metabolism in muscles of transgenic mice. J. Cell Biol. 145, 633-642.
49. Hughes SM, Salinas PC (1999) Control of muscle fibre and motoneuron diversification. Curr. Opin. Neurobiol. 9, 54-64.
50. Itoh N, Mima T, Mikawa T (1996) Loss of fibroblast growth factor receptors is necessary for terminal differentiation of embryonic limb muscle. Development 122, 291-300.
51. Jacob M, Christ B, Jacob HJ (1978) On the migration of myogenic stem cells into the prospective wing region of chick embryos. A scanning and transmission electron microscope study. Anat. Embryol. (Berl.) 153, 179-193.
52. Jaffredo T, Horwitz AF, Buck CA, Rong PM, Dieterlen-Lievre F (1988) Myoblast migration specifically inhibited in the chick embryo by grafted CSAT hybridoma cells secreting an anti-integrin antibody. Development 103, 431-446.
53. Kablar B, Krastel K, Ying C, Tapscott SJ, Goldhamer DJ, Rudnicki MA (1999) Myogenic determination occurs independently in somites and limb buds. Dev. Biol. 206, 219-231.
54. Kambadur R, Sharma M, Smith TP, Bass JJ (1997) Mutations in myostatin (GDF8) in double-muscled Belgian Blue and Piedmontese cattle. Genome Res. 7, 910-916.
55. Kardon G (1998) Muscle and tendon morphogenesis in the avian hind limb. Development 125, 4019-4032.
56. Kardon G, Campbell JK, Tabin CJ (2002) Local extrinsic signals determine muscle and endothelial cell fate and patterning in the vertebrate limb. Dev. Cell 3, 533-545.
57. Krüger M, Mennerich D, Fees S, Schafer R, Mundlos S, Braun T (2001) Sonic hedgehog is a survival factor for hypaxial muscles during mouse development. Development 128, 743-752.
58. Kühl M, Sheldahl LC, Malbon CC, Moon RT (2000) Ca(2+)/ calmodulin-dependent protein kinase II is stimulated by Wnt and Frizzled homologs and promotes ventral cell fates in Xenopus. J. Biol. Chem. 275, 12701-12711.
59. Lee SJ, McPherron AC (2001) Regulation of myostatin activity and muscle growth. Proc. Natl Acad. Sci. USA 98, 9306-9311.
60. Lee KKH, Wong CC, Webb SE, Tang MK, Leung AKC, Kwok PF, et al. (1999) Hepatocyte growth factor stimulates chemotactic response in mouse embryonic limb myogenic cells in vitro. J. Exp. Zool. 283, 170-180.
61. Lewis KE, Currie PD, Roy S, Schauerte H, Haffter P, Ingham PW (1999) Control of muscle cell-type specification in the zebrafish embryo by Hedgehog signalling. Dev. Biol. 216, 469-480.
62. Lin J, Wu H, Tarr PT, Zhang CY, Wu Z, Boss O, et al. (2002) Transcriptional co-activator PGC-1alpha drives the formation of slow-twitch muscle fibres. Nature 418, 797-801.
63. Liu D, Black BL, Derynck R (2001) TGF-beta inhibits muscle differentiation through functional repression of myogenic transcription factors by Smad3. Genes Dev. 15, 2950-2966.
64. Luo K, Stroschein SL, Wang W, Chen D, Martens E, Zhou S, et al. (1999) The Ski oncoprotein interacts with the Smad proteins to repress TGFbeta signaling. Genes Dev. 13, 2196-2206.
65. Mankoo BS, Collins NS, Ashby P, Grigorieva E, Pevny LH, Candia A, et al. (1999) Mox2 is a component of the genetic hierarchy controlling limb muscle development. Nature 400, 69-73.
66. Marics I, Padilla F, Guillemot J-F, Scaal M, Marcelle C (2002) FGFR4 signaling is a necessary step in limb muscle differentiation. Development 129, 4559-4569.
67. Maroto M, Reshef R, Münsterberg AE, Koester S, Goulding M, Lassar AB (1997) Ectopic Pax-3 activates MyoD and Myf-5 expression in embryonic mesoderm and neural tissue. Cell 89, 139-148.
68. Matzuk MM, Lu N, Vogel H, Sellheyer K, Roop DR, Bradley A (1995) Multiple defects and perinatal death in mice deficient in follistatin. Nature 374, 360-363.
69. McPherron AC, Lee SJ (1997) Double muscling in cattle due to mutations in the myostatin gene. Proc. Natl Acad. Sci. USA 94, 12457-12461.
70. Mennerich D, Schafer K, Braun T (1998) Pax-3 is necessary but not sufficient for lbx1 expression in myogenic precursor cells of the limb. Mech. Dev. 73, 147-158.
71. Miller JB, Stockdale FE (1986a) Developmental origins of skeletal muscle fibers: clonal analysis of myogenic cell lineages based on expression of fast and slow myosin heavy chains. Proc. Natl Acad. Sci. USA 83, 3860-3864.
72. Miller JB, Stockdale FE (1986b) Developmental regulation of the multiple myogenic cell lineages of the avian embryo. J. Cell Biol. 103, 2197-2208.
73. Münsterberg AE, Kitajewski J, Bumcrot DA, McMahon AP, Lassar AB (1995) Combinatorial signaling by Sonic hedgehog and Wnt family members induces myogenic bHLH gene expression in the somite. Genes Dev. 9, 2911-2922.
74. Nabeshima Y, Hanaoka K, Hayasaka M, Esumi E, Li S, Nonaka I (1993) Myogenin gene disruption results in perinatal lethality because of severe muscle defect. Nature 364, 532-535.
75. Naya FJ, Mercer B, Shelton J, Richardson JA, Williams RS, Olson EN (2000) Stimulation of slow skeletal muscle fiber gene expression by calcineurin in vivo. J. Biol. Chem. 275, 4545-4548.
76. Nikovits W Jr, Cann GM, Huang R, Christ B, Stockdale FE (2001) Patterning of fast and slow fibers within embryonic muscles is established independently of signals from the surrounding mesenchyme. Development 128, 2537-2544.
77. Niswander L, Martin GR (1992) Fgf-4 expression during gastrulation, myogenesis, limb and tooth development in the mouse. Development 114, 755-768.
78. Norris W, Neyt C, Ingham PW, Currie PD (2000) Slow muscle induction by Hedgehog signalling in vitro. J. Cell Sci. 113, 2695-2703.
79. Ordahl CP, Le Douarin NM (1992) Two myogenic lineages within the developing somite. Development 114, 339-353.
80. Parr BA, McMahon AP (1995) Dorsalizing signal Wnt-7a required for normal polarity of D-V and A-P axes of mouse limb. Nature 374, 350-353.
81. Petropoulos H, Skerjanc IS (2002) Beta-catenin is essential and sufficient for skeletal myogenesis in P19 cells. J. Biol. Chem. 277, 15393-15399.
82. Pin CL, Merrifield PA (1997) Regionalized expression of myosin isoforms in heterotypic myotubes formed from embryonic and fetal rat myoblasts in vitro. Dev. Dyn. 208, 420-431.
83. Pourquie O, Fan CM, Coltey M, Hirsinger E, Watanabe Y, Breant C, et al. (1996) Lateral and axial signals involved in avian somite patterning: a role for BMP4. Cell 84, 461-471.
84. Pownall ME, Gustafsson MK, Emerson CP Jr (2002) Myogenic Regulatory Factors and the Specification of Muscle Progenitors in Vertebrate Embryos. Annu. Rev. Cell Dev. Biol. 18, 18.
85. Rees E, Young RD, Evans DJR (2003) Spatial and temporal contribution of somitic myoblasts to avian limb muscles. Dev. Biol. in press.
86. Robson LG, Hughes SM (1996) The distal limb environment regulates MyoD accumulation and muscle differentiation in mouse-chick chimaeric limbs. Development 122, 3899-3910.
87. Robson LG, Hughes SM (1999) Local signals in the chick limb bud can override myoblast lineage commitment: induction of slow myosin heavy chain in fast myoblasts. Mech. Dev. 85, 59-71.
88. Robson LG, Kara T, Crawley A, Tickle C (1994) Tissue and cellular patterning of the musculature in chick wings. Development 120, 1265-1276.
89. Roy S, Wolff C, Ingham PW (2001) The u-boot mutation identifies a Hedgehog-regulated myogenic switch for fiber-type diversification in the zebrafish embryo. Genes Dev. 15, 1563-1576.
90. Rudnicki MA, Schnegelsberg PN, Stead RH, Braun T, Arnold HH, Jaenisch R (1993) MyoD or Myf-5 is required for the formation of skeletal muscle. Cell 75, 1351-1359.
91. Sachs M, Brohmann H, Zechner D, Muller T, Hulsken J, Walther I, et al. (2000) Essential role of Gab1 for signaling by the c-Met receptor in vivo. J. Cell Biol. 150, 1375-1384.
92. Scaal M, Bonafede A, Dathe V, Sachs M, Cann G, Christ B, Brand-Saberi B (1999) SF/HGF is a mediator between limb patterning and muscle development. Development 126, 4885-4893.
93. Schäfer K, Braun T (1999) Early specification of limb muscle precursor cells by the homeobox gene Lbx1h. Nat. Genet. 23, 213-216.
94. Schmidt M, Tanaka M, Munsterberg A (2000) Expression of (beta)-catenin in the developing chick myotome is regulated by myogenic signals. Development 127, 4105-4113.
95. Schramm C, Solursh M (1990) The formation of premuscle masses during chick wing bud development. Anat. Embryol. 182, 235-247.
96. Seed J, Hauschka SD (1984) Temporal separation of the migration of distinct myogenic precursor populations into the developing chick wing bud. Dev. Biol. 106, 389-393.
97. Seed J, Hauschka SD (1988) Clonal analysis of vertebrate myogenesis. VIII. Fibroblasts growth factor (FGF)-dependent and FGF-independent muscle colony types during chick wing development. Dev. Biol. 128, 40-49.
98. 2+-dependent calcineurin signalling pathway. Nature 400, 576-581.
99. Serrano AL, Murgia M, Pallafacchina G, Calabria E, Coniglio P, Lomo T, et al. (2001) Calcineurin controls nerve activity-dependent specification of slow skeletal muscle fibers but not muscle growth. Proc. Natl Acad. Sci. USA 98, 13108-13113.
100. Slusarski DC, Corces VG, Moon RT (1997a) Interaction of Wnt and a Frizzled homologue triggers G-protein-linked phosphatidylinositol signalling. Nature 390, 410-413.
101. 2+ signaling by Wnt-5A. Dev. Biol. 182, 114-120.
102. Solursh M, Drake C, Meier S (1987) The migration of myogenic cells from the somites at the wing level in avian embryos. Dev. Biol. 121, 389-396.
103. Song K, Wang Y, Sassoon D (1992) Expression of Hox-7.1 in myoblasts inhibits terminal differentiation and induces cell transformation. Nature 360, 477-481.
104. Stockdale FE (1990) Myoblast diversity and the formation of the early limb musculature. Ann. NY Acad. Sci. 599, 111-118.
105. Stockdale FE (1992) Myogenic cell lineages. Dev. Biol. 154, 284-298.
106. Sutrave P, Leferovich JM, Kelly AM, Hughes SH (2000) The induction of skeletal muscle hypertrophy by a ski transgene is promoter-dependent. Gene 241, 107-116.
107. Swartz ME, Eberhart J, Pasquale EB, Krull CE (2001) EphA4/ephrin-A5 interactions in muscle precursor cell migration in the avian forelimb. Development 128, 4669-4680.
108. Sweeney LJ, Kennedy JM, Zak R, Kokjohn K, Kelley SW (1989) Evidence for expression of a common myosin heavy chain phenotype in future fast and slow skeletal muscle during initial stages of avian embryogenesis. Dev. Biol. 133, 361-374
109. Takayama H, LaRochelle WJ, Anver M, Bockman DE, Merlino G (1996) Scatter factor/hepatocyte growth factor as a regulator of skeletal muscle and neural crest development. Proc. Natl Acad. Sci. USA 93, 5866-5871.
110. Thomas M, Langley B, Berry C, Sharma M, Kirk S, Bass J, Kambadur R (2000) Myostatin, a negative regulator of muscle growth, functions by inhibiting myoblast proliferation. J. Biol. Chem. 275, 40235-40243.
111. Tiidus PM, Bombardier E, Xeni J, Bestic NM, Vandenboom R, Rudnicki MA, et al. (1996) Elevated catalase activity in red and white muscles of MyoD gene- inactivated mice. Biochem. Mol. Biol. Int. 39, 1029-1035.
112. Tremblay P, Dietrich S, Mericskay M, Schubert FR, Li Z, Paulin D (1998) A crucial role for Pax3 in the development of the hypaxial musculature and the long-range migration of muscle precursors. Dev. Biol. 203, 49-61.
113. Uchiyama K, Ishikawa A, Hanaoka K (2000) Expression of lbx1 involved in the hypaxial musculature formation of the mouse embryo. J. Exp. Zool. 286, 270-279.
114. Van Swearingen J, Lance-Jones C (1995) Slow and fast muscle fibers are preferentially derived from myoblasts migrating into the chick limb bud at different developmental times. Dev. Biol. 170, 321-337.
115. Webb SE, Lee KK, Tang MK, Ede DA (1997) Fibroblast growth factors 2 and 4 stimulate migration of mouse embryonic limb myogenic cells. Dev. Dyn. 209, 206-216.
116. Wigmore PM, Evans DJ (2002) Molecular and cellular mechanisms involved in the generation of fiber diversity during myogenesis. Int. Rev. Cytol. 216, 175-232.
117. Wilting J, Brand-Saberi B, Huang R, Zhi Q, Kontges G, Ordahl CP, et al. (1995) Angiogenic potential of the avian somite. Dev. Dyn. 202, 165-171.
118. Woloshin P, Song K, Degnin C, Killary AM, Goldhamer DJ, Sassoon D, et al. (1995) MSX1 inhibits myoD expression in fibroblast x 10T1/2 cell hybrids. Cell 82, 611-620.
119. Yamamoto M, Gotoh Y, Tamura K, Tanaka M, Kawakami A, Ide H, et al. (1998) Coordinated expression of Hoxa-11 and Hoxa-13 during limb muscle patterning. Development 125, 1325-1335.
120. Yang XM, Vogan K, Gros P, Park M (1996) Expression of the met receptor tyrosine kinase in muscle progenitor cells in somites and limbs is absent in Splotch mice. Development 122, 2163-2171.
121. Zhang M, McLennan IS (1998) Primary myotubes preferentially mature into either the fastest or slowest muscle fibers. Dev. Dyn. 213, 147-157.