Notochord induction of zebrafish slow muscle mediated by sonic hedgehog

Genes and Development

Volumn 11, Issue 17, 1997, Pages 2163-2175

  Blagden, Chris S ^a   Currie, Peter D ^b   Ingham, Philip W ^b,c   Hughes, Simon M ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^c UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Adaxial cells; Fiber type; Muscle; Myoblast; Sonic hedgehog; Zebrafish

Indexed keywords

SONIC HEDGEHOG PROTEIN;

ARTICLE; CELL DIFFERENTIATION; EMBRYO; FAST MUSCLE; GENE EXPRESSION; GENE MUTATION; MESODERM; MYOBLAST; NONHUMAN; NOTOCHORD; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SLOW MUSCLE; ZEBRA FISH;

DANIO RERIO; ERINACEIDAE; VERTEBRATA;

EID: 0030885996     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.11.17.2163     Document Type: Article

References (77)

1. Baylies, M.K., A. Martinez-Arias, and M. Bate. 1995. wingless is required for the formation of a subset of muscle founder cells during Drosophila embryogenesis. Development 121: 3829-3837.
2. Bitgood, M.J. and A.P. McMahon. 1995. Hedgehog and Bmp genes are coexpressed at many diverse sites of cell-cell interaction in the mouse embryo. Dev. Biol. 172: 126-138.
3. Bober, E., B. Brand-Saberi, C. Ebensperger, J. Wilting, R. Balling, B.M. Paterson, H.-H. Arnold, and B. Christ. 1994. Initial steps of myogenesis in somites are independant of influence from axial structures. Development 120: 3073-3082.
4. Buffinger, N. and F.E. Stockdale. 1995. Myogenic specification of somites is mediated by diffusible factors. Dev. Biol. 169: 96-108.
5. Chiang, C., Y. Litingtung, E. Lee, K.E. Young, J.L. Corden, H. Westphal, and P.A. Beachy. 1996. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383: 407-413.
6. Cho, M., S.M. Hughes, I. Karsch-Mizrachi, M. Travis, L.A. Leinwand, and H.M. Blau. 1994. Fast myosin heavy chains expressed in secondary mammalian muscle fibres at the time of their inception. J. Cell Sci. 107: 2361-2371
7. Concordet, J.-P., K.E. Lewis, J.W. Moore, L.V. Goodrich, R.L. Johnson, M.P. Scott, and P.W. Ingham. 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.
8. Cossu, G., R. Kelly, S. Tajbakhsh, S. Di Donna, E. Vivarelli, and M. Buckingham. 1996a. Activation of different myogenic pathways: myf-5 is induced by the neural tube and MyoD by the dorsal ectoderm in mouse paraxial mesoderm. Development 122: 429-437.
9. Cossu, G., S. Tajbakhsh, and M. Buckingham. 1996b. How is myogenesis initiated in the embryo? Trends Genet. 12: 218-222.
10. Crow, M.T. and F.E. Stockdale. 1986. Myosin expression and specialization among the earliest muscle fibres of the developing avian limb. Dev. Biol. 113: 238-254.
11. Currie, P.D. and P.W. Ingham. 1996. Induction of a specific muscle cell type by a hedgehog-like protein in zebrafish. Nature 382: 452-455.
12. Dan-Goor, M., L. Silberstein, M. Kessel, and A. Muhlrad. 1990. Localization of epitopes and functional effects of two novel monoclonal antibodies against skeletal muscle myosin. J. Muscle Res. Cell Motil. 11: 216-226.
13. Devoto, S.H., E. Melancon, J.S. Eisen, and M. Westerfield. 1996. Identification of separate slow and fast muscle precursor cells in vivo, prior to somite formation. Development 122: 3371-3380.
14. Dhoot, G.K. 1994. Mammalian myoblasts become fast or slow myocytes within the somitic myotome. J. Muscle Res. Cell Motil. 15: 617-622.
15. DiMario, J.X., S.E. Fernyak, and F.E. Stockdale. 1993. Myoblasts transferred to the limbs of embryos are committed to specific fibre fates. Nature 362: 165-167.
16. Duxson, M.J., Y. Usson, and A.J. Harris. 1989. The origin of secondary myotubes in mammalian skeletal muscles: Ultrastructural studies. Development 107: 743-750.
17. Echelard, Y., D.J. Epstein, B. St.-Jacques, L. Shen, J. Mohler, J.A. McMahon, and A.P. McMahon. 1993. Sonic hedgehog, a member of a family of putative signalling molecules implicated in regulation of CNS and limb polarity Cell 75: 1417-1430.
18. Ekker, S.C., L.L. McGrew, C.J. Lai, J.J. Lee, D.P. Von Kessler, R.T. Moon, and P.A. Beachy. 1995. Distinct expression and shared activities of members of the hedgehog gene family of Xenopus laevis. Development 121: 2337-2347.
19. Ericson, J., S. Morton, A. Kawakami, H. Roelink, and T.M. Jessell. 1996. Two critical periods of Sonic Hedgehog signaling required for the specification of motor neuron identity. Cell 87: 661-673.
20. Fan, C.-M. and M. Tessier-Lavigne. 1994. Patterning of mammalian somites by surface ectoderm and notochord: Evidence for sclerotome induction by a hedgehog homolog Cell 79: 1175-1186.
21. Fan, C.-M., J.A. Porter, C. Chiang, D.T. Chang, P.A. Beachy, and M. Tessier-Lavigne. 1995. Long-range sclerotome induction by sonic hedgehog: Direct role of the amino-termmal cleavage product and modulation by the cAMP signalling pathway. Cell 81: 457-465.
22. Felsenfeld, A.L., M. Curry, and C.B. Kimmel. 1991. The fub-1 mutation blocks initial myofibril formation in zebrafish muscle pioneer cells. Dev. Biol. 148: 23-30.
23. Gamel, A.J., B. Brand-Saberi, and B. Christ. 1995. Halves of epithelial somites and segmental plate show distinct muscle differentiation behavior in vitro compared to entire somites and segmental plate. Dev. Biol. 172: 625-639.
24. Gardahaut, M.F., J. Fontaine-Perus, T. Rouaud, E. Bandman, and R. Ferrand. 1992. Developmental modulation of myosin expression by thyroid hormone in avian skeletal muscle. Development 115: 1121-1131.
25. George-Weinstein, M., J.V. Gerhart, G.J. Foti, and J.W. Lash. 1994. Maturation of myogenic and chondrogenic cells in the presomitic mesoderm of the chick embryo. Exp. Cell Res. 211: 263-274.
26. Goulding, M., A. Lumsden, and A.J. Paquette. 1994. Regulation of Pax-3 expression in the dermamyotome and its role in muscle development. Development 120: 957-971.
27. Halpern, M.E., R.K. Ho, C. Walker, and C.B. Kimmel. 1993. Induction of muscle pioneers and floor plate is distinguished by the zebrafish no tail mutation. Cell 75: 99-111.
28. Halpern, M.E., C. Thisse, R.K. Ho, B. Thisse, B. Riggleman, B. Trevarrow, E.S. Weinberg, J.H. Postlethwait, and C.B. Kimmel. 1995. Cell-autonomous shift from axial to paraxial mesodermal development in zebrafish floating head mutants. Development 121: 4257-4264.
29. Hammerschmidt, M., M.J. Bitgood, and A.P. McMahon. 1996. Protein kinase A is a common negative regulator of hedgehog signalling in the vertebrate embryo. Genes & Dev. 10: 647-658.
30. Hatta, K., T.F. Schilling, R.A. BreMiller, and C.B. Kimmel. 1990. Specification of jaw muscle identity in zebrafish: Correlation with engrailed-homeoprotein expression. Science 250: 802-805.
31. Hatta, K., R. Bremiller, M. Westerfield, and C.B. Kimmel. 1991. Diversity of expression of engrailed-like antigens in zebrafish. Development 112: 821-832.
32. Holland, L.Z., D.A. Pace, M.L. Blink, M. Kene, and N.D. Holland. 1995. Sequence and expression of amphioxus alkali myosin light chain (AmphiMLC-alk) throughout development: Implications for vertebrate myogenesis. Dev. Biol. 171: 665-676.
33. Huang, Z. and S. Kunes. 1996. Hedgehog, transmitted along retinal axons, triggers neurogenesis in the developing visual centers of the Drosophila brain. Cell 86: 411-422.
34. Hughes, S.M. and H.M. Blau. 1992. Muscle fiber pattern is independent of cell lineage in postnatal rodent development. Cell 68: 659-671.
35. Hughes, S.M., M. Cho, I. Karsch-Mizrachi, M. Travis, L. Silberstein, L.A. Leinwand, and H.M. Blau. 1993. Three slow myosin heavy chains sequentially expressed in developing mammalian skeletal muscle. Dev. Biol. 158: 183-199.
36. Johnson, R.L., E. Laufer, R.D. Riddle, and C. Tabin. 1994. Ectopic expression of Sonic hedgehog alters dorsal-ventral patterning of somites. Cell 79: 1165-1173.
37. Kelly, A.M. and N.A. Rubinstein. 1980. Why are fetal muscles slow? Nature 288: 266-269.
38. Kenny-Mobbs, T. and P. Thorogood. 1987. Autonomy of differentiation in avian brachial somites and the influence of adjacent tissues. Development 100: 449-462.
39. Kimmel, C.B. and R.M. Warga. 1987. Cell lineages generating axial muscle in the zebrafish embryo. Nature 327: 234-237.
40. Krauss, S., J.-P. Concordet, and P.W. Ingham. 1993. A functionally conserved homologue of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos. Cell 75: 1431-1444.
41. Lassar, A.B. and A.E. Munsterberg. 1996. The role of positive and negative signals in somite patterning. Curr. Opin. Neurobiol. 6: 57-63.
42. Lin-Jones, J. and S.D. Hauschka. 1996. Myogenic determination factor expression in the developing avian limb bud: An RT-PCR analysis. Dev. Biol. 174: 407-422.
43. Marigo, V. and C.J. Tabin. 1996. Regulation of patched by sonic hedgehog in the developing neural tube. Proc. Natl. Acad. Sci. 93: 9346-9351.
44. Maroto, M., R. Reshef, A.E. Münsterberg, S. Koester, M. Goulding, and A.B. Lassar. 1997. Ectopic Pax-3 activates MyoD and Myf-5 expression in embryonic mesoderrn and neural tissue. Cell 89: 139-148.
45. Marti, E., R. Takada, D.A. Bumcrot, H. Sasaki, and A.P. McMahon. 1995. Distribution of Sonic hedgehog peptides in the developing chick and mouse embryo. Development 121: 2537-2547.
46. Miller, J.B. and F.E. Stockdale. 1986. Developmental origins of skeletal muscle fibres: Clonal analysis of myogenic cell lineages based on expression of fast and slow myosin heavy chains. Proc. Natl. Acad. Sci. 83: 3860-3864.
47. Morin-Kensicki, E.M. and J.S. Eisen. 1997. Sclerotome development and peripheral nervous system segmentation in embryonic zebrafish. Development 124: 159-167.
48. Munsterberg, A.E., J. Kitajewski, D.A. Bumcrot, A.P, McMahon, and A.B. Lassar. 1995. Combinatorial signaling by sonic hedgehog and Wnt family members induces myogenic bHLH gene expression in the somite. Genes & Dev. 9: 2911-2922.
49. Odenthal, J., P. Haffter, E. Vogelsang, M. Brand, F.J.M. Van Eeden, M. Furutani-Seiki, M. Granato, M. Hammerschmidt, C.P. Heisenberg, Y.J. Jiang, D.A. Kane, R.N. Kelsh, M.C. Mullins, R.M. Warga, M.L. Allende, E.S. Weinberg, and C. Nüsslein-Volhard. 1996. Mutations affecting the formation of the notochord in the zebrafish, Danio rerio. Development 123: 103-115.
50. Ott, M.-O., E. Bober, G. Lyons, H. Arnold, and M. Buckingham. 1991. Early expression of the myogenic regulatory gene, myf-5, in precursor cells of skeletal muscle in the mouse embryo. Development 111: 1097-1107.
51. Page, S., J.B. Miller, J.X. DiMario, E.J. Hager, A. Moser, and F.E. Stockdale. 1992. Developmentally regulated expression of three slow isoforms of myosin heavy chain: Diversity among the first fibers to form in avian muscle. Dev. Biol. 154: 118-128.
52. Pownall, M.E., K.E. Strunk, and C.P. Emerson, Jr. 1996. Notochord signals control the transriptional cascade of myogenic bHLH genes in somites of quail embryos. Development 122: 1475-1488.
53. Pourquie, O., M. Coltey, M.-A. Teillet, C. Ordahl, and N.M. Le Douarin. 1993. Control of dorsoventral patterning of somitic derivatives by notochord and floor plate. Proc. Natl. Acad. Sci. 90: 5242-5246.
54. Pourquie, O., C.-M. Fan, M. Coltey, E. Hirsinger, Y. Watanabe, C. Breant, P. Francis-West, P. Brickell, M. Tessier-Lavigne, and N.M. Le Douarin. 1996. Lateral and axial signals involved in avian somite patterning: A role for BMP4. Cell 84: 461-471.
55. Quinn, L.S., H. Holtzer, and M. Nameroff. 1985. Generation of chick skeletal muscle cells in groups of 16 from stem cells. Nature 313: 692-694.
56. Roelink, H., A. Augsburger, J. Heemskerk, V. Korzh, S. Norlin, A. Ruiz i Altaba, Y. Tanabe, M. Placzek, T. Edlund, T.M. Jessell, and f. Dodd. 1994. Floor plate and motor neuron induction by vhh-1, a vertebrate homologue of hedgehog expressed by the notochord. Cell 76: 761-775.
57. Rong, P.M., A.-M. Teillet, C. Ziller, and N.M. Le Douarin. 1992. The neural tube/notochord complex is necessary for vertebral but not limb and body wall striated muscle differentiation. Development 115: 657-672.
58. Rudnicki, M.A., P.N.J. Schnegelsberg, R.H. Stead, T. Braun, H.-H. Arnold, and R. Jaenisch. 1993. MyoD or Myf-5 is required for the formation of skeletal muscle. Cell 75: 1351-1359.
59. Schafer, D.A., J.B. Miller, and F.E. Stockdale. 1987. Cell diversification within the myogenic lineage: In vitro generation of two types of myoblasts from a single myogenic progenitor cell. Cell 48: 659-670.
60. Schier, A.F., S.C.F. Neuhauss, K.A. Heide, W.S. Talbot, and W. Driever. 1997. The one-eyed pinhead gene functions in mesoderm and endoderm formation in zebrafish and interacts with no tail. Development 124: 327-342.
61. Schiaffino, S., L. Gorza, S. Sartore, L. Saggin, S. Ausoni, M. Vianello, K. Gundersen, and T. Lomo. 1989. Three myosin heavy chain isoforms in type 2 skeletal muscle fibres. J. Muscle Res. Cell Motil. 10: 197-205.
62. Schulte-Merker, S., F.J.M. van Eeden, M.E. Halpern, C.B. Kimmel, and C. Nusslein-Volhard. 1994. no tail [ntl] is the zebrafish homologue of the mouse T (Brachyury) gene. Development 120: 1009-1015.
63. Solnica-Krezel, L., D.L. Stemple, E. Mountcastle-Shah, Z. Rangini, S.C.F. Neuhauss, J. Malicki, A.F. Schier, D.Y.R. Stainier, F. Zwartkruis, S. Abdelilah, and W. Driever. 1996. Mutations affecting cell fates and cellular rearrangements during gastrulation in zebrafish. Development 123: 67-80.
64. Stern, H.M. and S.D. Hauschka. 1995. Neural tube and notochord promote in vitro myogenesis in single somite explants. Dev. Biol. 167: 87-103.
65. Stern, H.M., A.M.C. Brown, and S.D. Hauschka. 1995. Myogenesis in paraxial mesoderm: Preferential induction by dorsal neural tube and by cells expressing Wnt-1. Development 121: 3675-3686.
66. Stone, D.M., M. Hynes, M. Armanini, T.A. Swanson, Q. Gu, R.L. Johnson, M.P. Scott, D. Pennica, A. Goddard, H. Phillips, M. Noll, J.E. Hooper, F. De Sauvage, and A. Rosenthal. 1996. The tumour-suppressor gene patched encodes a candidate receptor for Sonic hedgehog. Nature 384: 129-134.
67. Tajhakhsh, S., D. Rocancourt, G. Cossu, and M. Buckingham. 1997. Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf-5 act upstream of MyoD. Cell 89: 127-138.
68. Talbot, W.B., B. Trevarrow, M.E. Halpern, A.E. Melby, G. Farr, T.J. Postlethwait, C.B. Kimmel, and D. Kimmelman. 1995. A homeobox gene essential for zebrafish notochord development. Nature 378: 150-157.
69. Teillet, M.-A. and N.M. Le Douarin. 1983. Consequences of neural tube and notochord excision on the development of the peripheral nervous system in chick embryos. Dev. Biol. 98: 192-211.
70. Ticho, B.S., D.Y.R. Stainier, and M.C. Fishman. 1996. Three zebrafish MEF2 genes delineate somitic and cardiac muscle development in wild-type and mutant embryos. Mech. Dev. 59: 205-218.
71. van Eeden, F.J.M., M. Granato, U. Schach, M. Brand, M. Furutani-Seiki, P. Haffter, M. Hammerschmidt, C.P. Heisenberg, Y.-J. Jiang, D.A. Kane, R.N. Kelsh, M.C. Mullins, J. Odenthal, R.M. Warga, M.L. Allende, E.S. Weinberg, and C. Nüsslein-Volhard. 1996. Mutations affecting somite formation and patterning in the zebrafish, Danio rerio. Development 123: 153-164.
72. van Raamsdonk, W., C.W. Pool, and G. te Kronnie. 1978. Differentiation of muscle fibre types in the teleost Brachydanio rerio. Anat. Embryol. 153: 137-155.
73. Vivarelli, E., W.E. Brown, R.G. Whalen, and G. Cossu. 1988. The expression of slow myosin during mammalian somitogenesis and limb bud differentiation. J. Cell Biol. 107: 2191-2197.
74. Vortkamp, A., K. Lee, B. Lanske, G.V. Segre, H.M. Kronenberg, and C.J. Tabin. 1996. Regulation of rate of cartilage differentiation by Indian Hedgehog and PTH-related protein. Science 273: 613-622.
75. Webster, C., L. Silberstein, A.P. Hays, and H.M. Blau. 1988. Fast muscle fibers are preferentially affected in Duchenne muscular dystrophy. Cell 52: 503-513.
76. Weinberg, E.S., M.L. Allende, C.S. Kelly, A. Abdelhamid, T. Murakami, P. Andermann, O.G. Doerre, D.J. Grunwald, and B. Riggleman. 1996. Developmental regulation of zebrafish MyoD in wild-type, no tail, and spadetail embryos. Development 122: 271-280.
77. Westerfield, M. 1995. The zebrafish book. University of Oregon Press. Eugene, OR.