Xenopus muscle development: From primary to secondary myogenesis

Developmental Dynamics

Volumn 226, Issue 1, 2003, Pages 12-23

  Chanoine, Christophe ^a   Hardy, Serge ^b  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b UNIVERSITÉ DE RENNES 1   (France)

Author keywords

Muscle development; Muscle fates; Myogenesis; Xenopus

Indexed keywords

BIOLOGICAL FACTOR; MESODERM INDUCING FACTOR; MYOGENIC DETERMINATION FACTOR XMYF5; MYOGENIC DETERMINATION FACTOR XMYOD; UNCLASSIFIED DRUG;

APOPTOSIS; CELL DEATH; EMBRYO DEVELOPMENT; FOWL; GENE EXPRESSION; MAMMAL; MESODERM; METAMORPHOSIS; MOLECULAR BIOLOGY; MULTINUCLEAR CELL; MUSCLE CELL; MUSCLE DEVELOPMENT; MYOTOME; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; XENOPUS;

ANIMALS; CELL DEATH; CELL DIFFERENTIATION; CELL LINEAGE; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MUSCLE PROTEINS; MUSCLE, SKELETAL; MUSCLES; MYOD PROTEIN; MYOGENIC REGULATORY FACTOR 5; TIME FACTORS; TRANS-ACTIVATORS; XENOPUS; XENOPUS PROTEINS;

AVES; MAMMALIA;

EID: 0037219768     PISSN: 10588388     EISSN: None     Source Type: Journal    
DOI: 10.1002/dvdy.10206     Document Type: Review

References (124)

1. Alley KE. 1989 Myofiber turnover is used to retrofit frog jaw muscles during metamorphosis. Am J Anat 184:1-12.
2. Badiani P, Corbella P. Kioussis D, Marvel J. Weston K. 1994. Dominant interfering alleles define a role for c-Myb in T-cell development. Genes Dev 8:770-782.
3. Berry DL, Rose CS, Remo BF, Brown DD. 1998.The expression pattern of thyroid hormone response genes in remodeling tadpole tissues defines distinct growth and resorption gene expression programs. Dev Biol 203:24-35.
4. Blackshaw SE, Warner AE. 1976a, Low resistance junctions between mesoderm cells during development of trunk muscles, J Physiol 255:209-230.
5. Blackshaw S, Warner A, 1976b. Onset of acetylcholine sensitivity and endplate activity in developing myotome muscles of Xenopus. Nature 262:217-218.
6. Boudjelida, H, Muntz L, 1987. Multinucleation during myogenesis of the myotome of Xenopus laevis: A qualitative study. Development 101:583-590.
7. Brooke MH, Kaiser KK, 1970. Muscle fiber types: How many and what kind? Arch Neurol 23:369-379,
8. Caceres JF, Kornblihtt AR. 2002. Alternative splicing: Multiple control mechanisms and involvement in human disease. Trends Genet 18:186-193.
9. Chambers AE, Kotecha S, Towers N, Mohun TJ, 1992. Muscle-specific expression of SRF-related genes in the early embryo of Xenopus laevis, EMBO J 11:4981-4991.
10. Chanoine, C, d'Albis A, Lenfant-Guyot M, Janmot C, Gallien CL. 1987, Regulation by thyroid hormones of terminal differentiation in the skeletal dorsal muscle. II. Urodelan amphibians, Dev Biol 123:33-42.
11. Charbonnier F, Della Gaspera B, Armand As A, Van Der Laarse WJ, Launay T, Becker C, Gallien CL, Chanoine C. 2002. Two myogenin-related genes are differentially expressed in Xenopus laevis myogenesis and differ in their ability to trans-activate muscle-structural genes, J Biol Chem 277:1139-1147.
12. Chung HM, Neff AW, Malacinski GM. 1989, Autonomous death of amphibian (Xenopus laevis) cranial myotomes, J Exp Zool 251:290-299.
13. Chung HG, Chung HM. 1999, Neuregulin induces the expression of mesodermal genes in the ectoderm of Xenopus laevis, Mol Cells 9:497-503
14. Conlon FL, Sedgwick SG, Weston KM, Smith JC. 1996. Inhibition of Xbra transcription activation causes defects in mesodermal patterning and reveals autoregulation of Xbra in dorsal mesoderm. Development 122:2427-2435.
15. Cossu G, Borello U. 1999. Wnt signaling and the activation of myogenesis in mammals. EMBO J 18:6867-6872.
16. Dale L, Jones CM. 1999. BMP signalling in early Xenopus development. Bioessays 21:751-760.
17. Dale L, Slack JMW. 1987a. Fate map for the 32-cell stage of Xenopus laevis, Development 99:274-295.
18. Dale L, Slack JMW, 1987b. Regional specification within the mesoderm of early embryos of Xenopus laevis. Development 100:279-295.
19. Dhanarajan ZC, Atkinson BG. 1981. Thyroid-hormone-induced' differentiation and development of anuran tadpole hind limbs: Detection and quantitation of M-line protein and alpha-actinin synthesis. Dev Biol 82:317-328.
20. Dosch R, Gawantka V, Delius H, Blumenstock C, Niehrs C. 1997. Bmp-4 acts as a morphogen in dorsoventral mesoderm patterning in Xenopus. Development 124:2325-2334.
21. Duriez P, Lesimple M, Alio MR, Hardy S. 2000, Alternative splicing of Xenopus alphafast-tropomyosin pre-mRNA during development: Identification of determining sequences. DNA Cell Biol 19:365-376.
22. Elinson RP, Remo B, Brown DD. 1999. Novel structural elements identified during tail resorption in Xenopus laevis metamorphosis: Lessons from tailed frogs. Dev Biol 215:243-252.
23. Fisher ME, Isaacs HV, Pownall ME. 2002. eFGF is required for activation of XmyoD expression in the myogenic cell lineage of Xenopus laevis. Development 129:1307-1315.
24. Flood PR, Kryvi H, Totland GK. 1977. Ontophylogenetic aspects of muscle fibre types in the segmental trunk muscle of lower chordates. Folia Morphol 25:64-67.
25. Frank D, Harland RM. 1991. Transient expression of XMyoD in non-somitic mesoderm of Xenopus gastrulae. Development 113:1387-1393.
26. Gaillard C, Theze N, Hardy S, Ailo MR, Ferrasson E, Thiebaud P. 1998. Alphatropomyosin gene expression in Xenopus laevis: Differential promoter usage during development and controlled expression by myogenic factors. Dev Genes Evol 207:435-445.
27. Gaillard C, Lerivray H, Theze N, Cooper B, Lepetit D, Mohun T, Thiebaud P, 1999. Differential expression of two skeletal muscle beta-tropomyosin mRNAs during Xenopus laevis development. Int J Dev Biol 43:175-178.
28. Grainger RM, Gurdon JB. 1989. Loss of competence in amphibian induction can take place in single nondividing cells. Proc Natl Acad Sci U S A 86:1900-1904.
29. Gurdon JB, Tiller E, Roberts J, Kato K. 1993a. A community effect in muscle development. Curr Biol 3:111.
30. Gurdon JB, Kato K, Lemaire P. 1993b. The community effect, dorsalization and mesoderm induction. Curr Opin Genet Dev 3:662-667.
31. Gurdon JB, Lemaire P, Mohun TJ, 1998. Myogenesis in Xenopus embryos. Methods Cell Biol 52:53-66.
32. Hamilton L. 1969. The formation of somites in Xenopus. J Embryol Exp Morphol 22:253-264.
33. Hardy S, Hamon S, Cooper B, Mohun T, Thiebaud P. 1999. Two skeletal alpha-tropomyosin transcripts with distinct 3'UTR have different temporal and spatial patterns of expression in the striated muscle lineages of Xenopus laevis, Mech Dev 87:199-202.
34. Harvey RP. 1990, The Xenopus MyoD gene: An unlocalised maternal mRNA predates lineage-restricted expression in the early embryo. Development 108:669-680.
35. Harvey RP. 1991. Widespread expression of MyoD genes in Xenopus embryos is amplified in presumptive muscle as a delayed response to mesoderm induction. Proc Natl Acad Sci U S A 88:9198-9202.
36. Hoppler S, Brown JD, Moon RT. 1996. Expression of a dominant-negative Wnt blocks induction of MyoD in Xenopus embryos. Genes Dev 10:2805-2817.
37. Hopwood ND, Pluck A, Gurdon JB, 1989. MyoD expression in the forming somites is an early response to mesoderm induction in Xenopus embryos. EMBO J 8:3409-3417.
38. Hopwood ND, Pluck A, Gurdon JB, 1991. Xenopus Myf-5 marks early muscle cells and can activate muscle genes ectopically in early embryos. Development 111:551-560.
39. Hopwood ND, Pluck A, Gurdon JB, Dilworth SM. 1992. Expression of XMyoD protein in early Xenopus laevis embryos, Development 114:31-38.
40. Jacobson AG. 1988. Somitomeres: Mesodermal segments of vertebrate embryos. Development 104(Suppl):209-220.
41. Jen WC, Wettstein D, Turner D, Chitnis A, Kintner C. 1997. The Notch ligand, X-Delta-2, mediates segmentation of the paraxial mesoderm in Xenopus embryos. Development. 124:1169-1178.
42. Jen WC, Gawantka V, Pollet N, Niehrs C, Kintner C, 1999. Periodic repression of Notch pathway genes governs the segmentation of Xenopus embryos. Genes Dev 13:1486-1499.
43. Jennings CG. 1992. Expression of the myogenic gene MRF4 during Xenopus development. Dev Biol 151:319-332.
44. Kahane N, Cinnamon Y, Kalcheim C, 2002. The roles of cell migration and myofiber intercalation in patterning formation of the postmitotic myotome. Development 129:2675-2687.
45. Kanamori A, Brown DD. 1992. The regulation of thyroid hormone receptor beta genes by thyroid hormone in Xenopus laevis. J Biol Chem 267:739-745.
46. Kato K, Gurdon JB. 1993. Single-cell transplantation determines the time when Xenopus muscle precursor cells acquire a capacity for autonomous differentiation. Proc Natl Acad Sci U S A 90:1310-1314.
47. Keller R. 2000. The origin and morphogenesis of amphibian somites. Curr Top Dev Biol 47:183-246.
48. Kielbowna L, 1966, Cytological and cytophotometrical studies on myogenesis in Xenopus laevis (Daudin), Zool Pol 17:247-255.
49. Kielbowna L. 1980. Two different types of myogenesis in Xenopus laevis Daudin, Zool Pol 27:377-395.
50. Kim SH, Jen WC, De Robertis EM, Kintner C. 2000. The protocadherin PAPC establishes segmental boundaries during somitogenesis in Xenopus embryos, Curr Biol 10:821-830.
51. Kimelman D, Griffin KJ. 2000. Vertebrate mesendoderm induction and patterning. Curr Opin Genet Dev 10:350-356.
52. Kobel HR, DuPasquier L. 1986. Genetics of polyploid Xenopus. Trends Genet 2:310-315.
53. Kolm PJ, Sive HL, 1995, Efficient hormone-inducible protein function in Xenopus laevis, Dev Biol 171:267-272.
54. Kordylewski L. 1986. Differentiation of tail and trunk musculature in the tadpoles of Xenopus laevis. Z Mikrosk Anat Forsch 100:767-789.
55. Kordylewski L, Faber J, Gorlich A, Kilarski W. 1989. Histochemistry and isomyosins of tail musculature in Xenopus. J Muscle Res Cell Motil 10:290-296.
56. Kroll KL, Amaya E. 1996. Transgenic Xenopus embryos from sperm nuclear transplantations reveal FGF signaling requirements during gastrulation. Development 122:3173-3183.
57. Kullberg RW, Lentz TL, Cohen MW. 1977. Development of the myotomal neuromuscular junction in Xenopus laevis: An electrophysiological and fine-structural study Dev Biol 60:101-129.
58. Lane MC, Smith WC. 1999. The origins of primitive blood in Xenopus: Implications for axial patterning. Development 126:423-434.
59. Lännergren J, Smith RS. 1966. Types of muscle fibres in toad skeletal muscle, Acta Physiol Scand 68:263-274.
60. Lännergren J, Hoh JF. 1984. Myosin isoenzymes in single muscle fibres of Xenopus laevis: Analysis of five different functional types. Proc R Soc Lond B Biol Sci 222:401-408.
61. Lännergren J. 1987. Contractile properties and myosin isoenzymes of various kinds of Xenopus twitch muscle fibres, J Muscle Res Cell Motil 8:260-273.
62. L'Ecuyer TJ, Tompach PC, Morris E, Fulton AB. 1995. Transdifferentiation of chicken embryonic cells into muscle cells by the 3' untranslated region of muscle tropomyosin. Proc Natl Acad Sci U S A 92:7520-7524.
63. Ludolph DC, Neff AW, Mescher AL, Malacinski GM, Parker MA, Smith RC. 1994, Overexpression of XMyoD or XMyf5 in Xenopus embryos induces the formation of enlarged myotomes through recruitment of cells of nonsomitic lineage. Dev Biol 166:18-33.
64. Martin BL, Harland RM. 2001. Hypaxial muscle migration during primary myogenesis in Xenopus laevis. Dev Biol 239:270-280.
65. Matsui M, Mizuseki K, Nakatani J, Nakanishi S, Sasai Y, 2000. Xenopus kielin: A dorsalizing factor containing multiple chordin-type repeats secreted from the embryonic midline. Proc Natl Acad Sci U S A 97:5291-5296.
66. McDowell N, Gurdon JB. 1999. Activin as a morphogen in Xenopus mesoderm induction, Semin Cell Dev Biol 10:311-317.
67. Mei W, Yang J, Tao Q, Geng X, Rupp RA, Ding X. 2001. An interferon regulatory factor-like binding element restricts Xmyf-5 expression in the posterior somites during Xenopus laevis myogenesis. FEBS Lett 505:47-52.
68. Mohun T, Garrett N, Stutz F, Sophr G. 1988. A third striated muscle actin gene is expressed during early development in the amphibian Xenopus laevis. J Mol Biol 202:67-76.
69. Mohun T, Wilson R, Gonti E, Longan M. 1994. Myogenesis in Xenopus laevis, Trends Cardiovasc Med 4:146-151.
70. Muntz L. 1975. Myogenesis in the trunk and leg during development of the tadpole of Xenopus laevis (Daudin). J Embryol Exp Morphol 33:757-774.
71. Myer A, Wagner DS, Vivian JL, Olson EN, Klein WH. 1997. Wild-type myoblasts rescue the ability of myogenin-null myoblasts to fuse in vivo. Dev Biol 185:127-138.
72. Newport J, Kirschner M. 1982, A major developmental transition in early Xenopus embryos. II. Control of the onset of transcription. Cell 30:687-696.
73. Nicolas N, Gallien CL, Chanoine C, 1996. Analysis of MyoD, myogenin, and muscle-specific gene mRNAs in regenerating Xenopus skeletal muscle. Dev Dyn 207:60-68.
74. Nicolas N, Gallien CL, Chanoine C. 1998. Expression of myogenic regulatory factors during muscle development of Xenopus: Myogenin mRNA accumulation is limited strictly to secondary myogenesis. Dev Dyn 213:309-321.
75. Nicolas N, Mira JC, Gallien CL, Chanoine C. 1999. Long-term denervation modulates differentially the accumulation of myogenin and MRF4 mRNA in adult Xenopus muscle, Neurosci Lett 277:107-110.
76. Nishikawa A, Hayashi H. 1994. Isoform transition of contractile proteins related to muscle remodeling with an axial gradient during metamorphosis in Xenopus laevis. Dev Biol 165:86-94.
77. Nishikawa A, Hayashi H. 1995. Spatial, temporal and hormonal regulation of programmed muscle cell death during metamorphosis of the frog Xenopus laevis. Differentiation 59:207-214.
78. Nishikawa A. 1997. Induction of cell differentiation and programmed cell death in amphibian metamorphosis. Hum Cell 10:167-174.
79. Nishikawa A, Murata E, Akita M, Kaneko K, Moriya O, Tomita M, Hayashi H. 1998. Roles of macrophages in programmed cell death and remodeling of tail and body muscle of Xenopus laevis during metamorphosis. Histochem Cell Biol 109:11-17.
80. Oppenheimer JH, Schwartz HL, Mariash CN, Kinlaw WB, Wong NCW, Freake HC. 1987. Advances in our understanding of thyroid hormone action at the cellular level. Endocr Rev 8:288-308.
81. Radice GP, Malacinski GM. 1989. Expression of myosin heavy chain transcripts during Xenopus laevis development. Dev Biol 133:562-568.
82. Radice GP, Neff AW, Shim YH, Brustis JJ, Malacinski GM. 1989. Developmental histories in amphibian myogenesis, Int J Dev Biol 33:325-343.
83. Radice GP, 1995. Spatial expression of two tadpole stage specific myosin heavy chains in Xenopus laevis. Acta Anat (Basel) 153:254-262.
84. Rashbass J, Taylor MV, Gurdon JB. 1992. The DNA-binding protein E12 co-operates with XMyoD in the activation of muscle-specific gene expression in Xenopus embryos. EMBO J 11:2981-2990.
85. Rastinejad F, Blau HM. 1993. Genetic complementation reveals a novel regulatory role for 3' untranslated regions in growth and differentiation. Cell 72:903-917.
86. Rastinejad F, Conboy MJ, Rando TA, Blau HM. 1993. Tumor suppression by RNA from the 3' untranslated region of alpha-tropomyosin. Cell 75:1107-1117.
87. Regel ED, Epstein SM. 1972. Segmentation of interauricular skull region in anura. Zool Zh 51:1517-1528.
88. Re'em-Kalma Y, Lamb T, Frank D. 1995. Competition between noggin and bone morphogenetic protein 4 activities may regulate dorsalization during Xenopus development. Proc Natl Acad Sci U S A 92:12141-12145.
89. Rupp RA, Weintraub H, 1991. Ubiquitous MyoD transcription at the midblastula transition precedes induction-dependent MyoD expression in presumptive mesoderm of X. laevis. Cell 65:927-937.
90. Rupp RA, Snider L, Weintraub H. 1994. Xenopus embryos regulate the nuclear localization of XMyoD. Genes Dev 8:1311-1323.
91. Ryke PA. 1938. The ontogenetic development of the somatic musculature of the trunk of the aglossal anuran Xenopus. Acta Zool 34:1-17.
92. Sachs L, de Luze A, Lebrun JJ, Kelly PA, Demeneix BA. 1996. Use of heterologous DNA-based gene transfer to follow physiological, T3-dependent regulation of myosin heavy chain genes in Xenopus tadpoles. Endocrinology 137:2191-2194.
93. Sachs LM, Abdallah B, Hassan A, Levi G, De Luze A, Reed JC, Demeneix BA, 1997a. Apoptosis in Xenopus tadpole tail muscles involves Bax-dependent pathways. FASEB J 11:801-808.
94. Sachs LM, Lebrun JJ, de Luze A, Kelly PA, Demeneix BA, 1997b, Tail regression, apoptosis and thyroid hormone regulation of myosin heavy chain isoforms in Xenopus tadpoles. Mol Cell Endocrinol 131:211-219.
95. Sasaki F. 1974. Histochemical and ultra-structural studies of tail muscles in the anuran tadpole. Acta Histochem Cytochem 7:239-256.
96. Sasaki F. 1977. Histochemical and biochemical investigation of the tail muscle of anuran tadpoles during metamorphosis. Acta Histochem Cytochem 10:413-425.
97. Sassoon DA, 1993. Myogenic regulatory factors: Dissecting their role and regulation during vertebrate embryogenesis. Dev Biol 156:11-23.
98. Scales JB, Olson EN, Perry M. 1990. Two distinct Xenopus genes with homology to MyoD1 are expressed before somite formation in early embryogenesis. Mol Cell Biol 10:1516-1524.
99. Schwartz LM, Kay BK. 1988. Differential expression of the Ca2+-binding protein parvalbumin during myogenesis in Xenopus laevis. Dev Biol 128:441-452.
100. Shi DL, Bourdelas A, Umbhauer M, Boucaut JC. 2002. Zygotic Wnt/beta-catenin signaling preferentially regulates the expression of Myf5 gene in the mesoderm of Xenopus. Dev Biol 245:124-135.
101. Shi YB, Yaoita Y, Brown DD. 1992. Genomic organization and alternative promoter usage of the two thyroid hormone receptor beta genes in Xenopus laevis. J Biol Chem 267:733-738.
102. Smit AL. 1953. The ontogenesis of the vertebral column of Xenopus laevis (Daudin) with special reference to the segmentation of the meitotic region of the skull. Ann Univ Stellen-bosch 29:81-136.
103. Smith JC. 1995. Mesoderm-inducing factors and mesodermal patterning. Curr Opin Cell Biol 7:856-861.
104. Smith RS, Ovalle WK Jr. 1973. Varieties of fast and slow extrafusal muscle fibres in amphibian hind limb muscles. J Anat 116:1-24.
105. Sparrow DB, Jen WC, Kotecha S, Towers N, Kintner C, Mohun TJ. 1998. Thylacine 1 is expressed segmentally within the paraxial mesoderm of the Xenopus embryo and interacts with the Notch pathway. Development, 125:2041-2051.
106. Sperry DG. 1981. Fiber type composition and postmetamorphic growth of anuran hindlimb muscles. J Morphol 170:321-345.
107. Standley HJ, Zorn AM, Gurdon JB. 2001. eFGF and its mode of action in the community effect during Xenopus myogenesis. Development 128:1347-1357.
108. Steinbach OC, Wolffe AP, Rupp RA. 1997. Somatic linker histones cause loss of mesodermal competence in Xenopus. Nature 389:395-399.
109. Steinbach OC, Ulshofer A, Authaler A, Rupp RA. 1998.Temporal restriction of MyoD induction and autocatalysis during Xenopus mesoderm formation. Dev Biol 202:280-292.
110. Steinbac OC, Wolffe AP, Rupp RA. 2000. Histone deacetylase activity is required for the induction of the MyoD muscle cell lineage in Xenopus. Biol Chem 381:1013-1016.
111. Stennard F, Ryan K, Gurdon JB, 1997. Markers of vertebrate mesoderm induction. Curr Opin Genet Dev 7:620-627.
112. Su XL, Woodland HR. 1993. The MyoD binding site is dispensable for cardiac actin gene expression in the somites of later stage Xenopus embryos. FEBS Lett 335:41-46.
113. Tajbakhsh S, Buckingham M. 2000. The birth of muscle progenitor cells in the mouse: Spatiotemporal considerations. Curr Top Dev Biol:225-268.
114. Tata JR, Kawahara A, Baker BS. 1991. Prolactin inhibits both thyroid hormone-induced morphogenesis and cell death in cultured amphibian larval tissues. Dev Biol 146:72-80.
115. Taylor MV, Gurdon JB, Hopwood ND, Towers N, Mohun TJ. 1991. Xenopus embryos contain a somite-specific, MyoD-like protein that binds to a promoter site required for muscle actin expression. Genes Dev 5:1149-1160.
116. Thayer MJ, Tapscott SJ, Davis RL, Wright WE, Lassar AB, Weintraub H. 1989. Positive autoregulation of the myogenic determination gene MyoD1. Cell 58:241-248.
117. Theze N, Hardy S, Wilson R, Allo MR, Mohun T, Thiebaud P. 1995. The MLClf/3f gene is an early marker of somitic muscle differentiation in Xenopus laevis embryo. Dev Biol 171:352-362.
118. Tucker AS, Slack JM, 1995. Tail bud determination in the vertebrate embryo, Curr Biol 5:807-813.
119. Watanabe K, Khan MA, Sasaki F, Iseki H. 1978. Light and electron microscopic investigation of ATPase activity in musculature during anuran tail resorption. Histochemistry 58:13-22.
120. Wittenberger T, Steinbach OC, Authaler A, Kopan R, Rupp RA. 1999. MyoD stimulates delta-1 transcription and triggers notch signaling in the Xenopus gastrula. EMBO J 18:1915-1922.
121. Yaoita Y, Shi Y, Brown D. 1990. Xenopus laevis alpha and beta thyroid hormone receptors. Proc Natl Acad Sci U S A 87:7090-7094.
122. Yaoita Y, Nakajima K. 1997. Induction of apoptosis and CPP32 expression by thyroid hormone in a myoblastic cell line derived from tadpole tail. J Biol Chem 272:5122-5127.
123. Youn WB, Malacinski GM. 1981a. Somitogenesis in the amphibian Xenopus laevis: Scanning electron microscopic analysis of intrasomitic cellular arrangements during somite rotation. J Embryol Exp Morphol 64:22-43.
124. Youn WB, Malacinski GM. 1981b. Comparative analysis of amphibian somite morphogenesis: Cell rearrangement patterns during rosette formation and myoblast fusion. J Embryol Exp Morphol 66:1-26.