The expression and regulation of Follistatin and a Follistatin-like gene during avian somite compartmentalization and myogenesis

Developmental Biology

Volumn 178, Issue 2, 1996, Pages 343-362

  Amthor, Helge ^a,c   Connolly, David ^b   Patel, Ketan ^b   Brand Saberi, Beate ^a   Wilkinson, David G ^b   Cooke, Jonathan ^b   Christ, Bodo ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^c ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FOLLISTATIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHICKEN; EMBRYO; EMBRYO DEVELOPMENT; GENE EXPRESSION REGULATION; IN SITU HYBRIDIZATION; MUSCLE DEVELOPMENT; NONHUMAN; NOTOCHORD; PRIORITY JOURNAL; SOMITE;

ANIMALIA; AVES; ERINACEIDAE; GALLUS GALLUS;

EID: 0030587619     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.1996.0223     Document Type: Article

References (79)

1. Aoyma, H., and Asamoto, K. (1988). Determination of somite cells: Independence of cell differentiation and morphogenesis. Development 104, 15-28.
2. Basler, K., Edlung, T., Jessell, T. M., and Yamada, T. (1993). Control of cell pattern in the neural tube: regulation of cell differentiation by dorsalin-1, a novel TGF-β family member. Cell 73, 687-702.
3. Bellairs, R. (1963). The development of somites in the chick embryo. J. Embryol. Exp. Morphol. 11, 697-714.
4. Bellairs, R. (1979). The mechanism of somite segmentation in the chick embryo. J. Embryol. Exp. Morphol. 51, 227-243.
5. Bober, E., Brand-Saberi, B., Ebensberger, C., Wilting, J., Balling, R., Paterson, B. M., Arnold, H. H., and Christ, B. (1994). Initial steps of myogenesis in somites are independent of influence form axial structures. Development 120, 3073-3082.
6. Brand-Saberi, B., Ebensberger, C., Wilting, J., Balling, R., and Christ, B. (1993). The ventralizing effect of the notochord on somite differentiation in chick embryos. Anat. Embryol. 188, 239-245.
7. Buffinger, N., and Stockdale, F. E. (1994). Myogenic specification in somites: Induction by axial structures. Development 120, 1443-1452.
8. Buffinger, N., and Stockdale, F. E. (1995). Myogenic specification of somites is mediated by diffusible factors. Dev. Biol. 169, 96-108.
9. Bumcrot,D. A.,Takada, R., and McMahon, A. P. (1995). Proteolytic processing yields two secreted forms of sonic hedgehog. Mol. Cell. Biol. 15, 2294-303.
10. Christ, B., Jacob, H. J., and Jacob, M. (1972). Experimentelle Untersuchungen zur Somitenentstehung beim Hühnerembryo. Z. Anat. Entwickl.-Gesch. 138, 82-97.
11. Christ, B., Jacob, H. J., and Jacob, M. (1974a). Experimentelle Untersuchungen zur Entwicklung der Brustwand beim Hühnerembryo. Experientia 30, 1449-1451.
12. Christ, B., Jacob, H. J., and Jacob, M. (1974b). Über den Ursprung der Flügelmuskulatur. Experimentelle Untersuchungen mit Wachtel-und Hühnerembryonen. Experientia 30, 1446-1449.
13. Christ, B., Jacob, H. J., and Jacob, M. (1977). Experimental analysis of the origin of the wing musculature in avian embryos. Anat. Embryol. 150, 171-186.
14. Christ, B., Jacob, M., and Jacob, H. J. (1983). On the origin and development of the ventroabdominal muscles in the avian embryo. Anat. Embryol. 166, 87-101.
15. Christ, B., and Wilting, J. (1992). From somites to vertebral column. Ann. Anat. 174, 23-32.
16. Christ, B., Brand-Saberi, B., Grim, M., and Wilting, J. (1992). Local signalling in dermomyotomal cell type specification. Anat. Embryol. 186, 239-245.
17. Connolly, D. J., Patel, K., Seleiro, E. A. P., Wilkinson, D. G., and Cooke, J. (1995). Cloning, sequencing, and expressional analysis of the chick homologue of Follistatin. Dev. Gen. 17, 65-77.
18. Deuchar, E. M. (1958). Experimental demonstration of tongue muscle origin in chick embryos. J. Embryol. Exp. Morph. 6, 527-529.
19. Duprez, D. M., Coltey, M., Amthor, H., Brickell, P. M., and Tickle, C. (1996). Bone morphogenetic protein-2 (BMP-2) inhibits muscle development and promotes cartilage formation in chick limb bud cultures. Dev. Biol. 174, 448-452.
20. Ebensperger, C., Wilting, J., Brand-Saberi, B., Mizutani, Y., Christ, B., Balling, R., and Koseki, H. (1995). Pax-1, a regulator of sclerotome development is induced by notochord and floor plate signals in avian embryos. Anat. Embryol. 191, 297-310.
21. Emerson, C. P. (1993a). Skeletal myogenesis: Genetics and embryology to the fore. Curr. Opin. Genet. Dev. 3, 265-274.
22. Emerson, C. P. (1993b). Embryonic signals for skeletal myogenesis: arriving at the beginning. Curr. Opin. Cell Biol. 5, 1057-1064.
23. Epstein, J. A., Lam, P., Jepeal, L., Maas, R. L., and Shapiro, D. N. (1995). Pax-3 inhibits myogenic differentiation of cultured myoblast cells. J. Biol. Chem. 270, 11719-11722.
24. Epstein, D. J., Vekemaus, M., and Gruss, P. (1991). Splotch (Sp2h), a mutation affecting development of the mouse neural tube, shows a deletion within the paired homeodeomain of Pax -3. Cell 67, 767-774.
25. Fan, C. M., and Tessier-Lavigne, M. (1994). Patterning of mammalian somites by surface ectoderm and notochord: Evidence for sclerotome induction by a hedgehog homolog. Cell 79, 1175-1186.
26. Florini, J. R., Ewton, D. Z., and Magrik, A. (1991). Hormones, growth factors and myogenic differentiation. Annu. Rev. Physiol. 53, 201-216.
27. Franz, T., Kothary, R., Surani, M. A. H., Halata, Z., and Grim, M. (1993). The Splotch mutation interferes with muscle development in the limbs. Anat. Embryol. 187, 153-160.
28. Gamel, A. J., Brand-Saberi, B., and Christ, B. (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.
29. Goulding, M., Lumsden, A., and Paquette, A. J. (1994). Regulation of Pax-3 expression in the dermomyotome and its role in muscle development. Development 120, 957-971.
30. Graham, A., Francis-West, P., Brickell, P., and Lumsden, A. (1994). The signalling molecule BMP-4 mediates apoptosis in the rhombencephalic neural crest. Nature 372, 684-686.
31. Hamburger, V., and Hamilton, H. L. (1951). A series of normal stages in the development of the chick embryo. J. Morphol. 88, 49-92.
32. Hazelton, R. D. (1970). A radioautographic analysis of the migration and fate of cells derived from the occipital somites in the chick embryo with spezific reference to the development of the hypoglossal musculature. J. Embryol. Exp. Morph. 24, 455-466.
33. Hemmati-Brivanlou, A., Kelly, O. G., and Melton, D. A. (1994). Follistatin, an antagonist of activin, is expressed in the Spemann organizer and displays direct neuralizing activity. Cell 77, 283-295.
34. Hemmati-Brivanlou, A., and Melton, D. A. (1994). Inhibition of activin receptor signalling promotes neuralization in Xenopus. Cell 77, 273-281.
35. Holley, S. A., Jackson, P. J., Sasai, Y., Lu, B., De Robertis, E. M., Hoffman, F. M., and Ferguson, E. L. (1995). A conserved system for dorsal-ventral patterning in insects and vertebrates involving sog and chordin. Nature 376, 249-253.
36. Jacowley, S. B., Ciment, G., Tuan, R. S., Sporn, M. B., and Roberts, A. B. (1994). Expression of transforming growth factors-2 and 3 mRNAs and proteins in the developing chicken embryo. Differentiation 55, 105-118.
37. Johnson, R. L., Laufer, E., Riddle, R. D., and Tabin, C. (1994). Ectopic expression of sonic hedgehog alters dorsal-ventral patterning of somites. Cell 79, 1165-1173.
38. Jones, C. M., Bringas, P., Santos, V., Shum, L., and Slavkin, H. C. (1992). Involvement of BMP-4 and Vgr-1 in morphogenesis and neurogenesis in the mouse. Development 111, 531-542.
39. Katagiri, T., Yamaguchi, A., Komaki, M., Abe, E., Takahashi, N., Ikeda, T., Rosen, V., Wozney, J. M., Fujisawa-Sehara, A., and Suda, T. (1994). Bone morphogenetic protein-2 converts the differentiation pathway of C2C12 myoblasts into the osteoblast lineage. J. Cell. Biol. 127, 1755-1766.
40. Kenny-Mobbs, T., and Thorogood, P. (1987). Autonomy of differentiation in avian brachial somites and the influence of adjacent tissues. Development 100, 449-462.
41. Keynes, R. J., and Stern, C. D. (1988). Mechanism of vertebrate segmentation. Development 103, 413-429.
42. Krenn, V., Brand-Saberi, B., and Wachtler, F. (1991). Hyaluronic acid influences the migration of myoblasts within the avian embryonic wing bud. Am. J. Anat. 192, 400-406.
43. Lassar, A. B., and Münsterberg, A. E. (1994). Wiring diagrams: Regulatory circuits and the control of skeletal myogenesis. Curr. Opin. Cell Biol. 5, 1057-1064.
44. Matzuk, M. M., Naifang, L., Vogel, H., Sellheyer, K., Roop, D. R., and Bradley, A. (1995). Multiple defects and perinatal death in mice deficient in Follistatin. Nature 374, 360-363.
45. Michel, U., Farnworth, P., and Findlay, J. K. (1993). Follistatins: more than follicle-stimulating hormone suppressing proteins. Mol. Cell. Endocrinol. 91, 1-11.
46. Münsterberg, A. E., and Lassar, A. B. (1995). Combinatorial signals from the neural tube, floor plate and notochord induce myogenic bHLH gene expression in the somite. Development 121, 651-660.
47. Nieto,M. A.,Patel, K., and Wilkinson, D. G. (1996). In situ hybridisation of chick embryos in whole mount and tissue sections. In "Methods in Cell Biology" (M. Bronner-Fraser, Ed.), Vol. 51, pp. 219-235. Acedemic Press, San Diego.
48. Olson, E. N. (1992). Interplay between proliferation and differentiation within the myogenic lineage. Dev. Biol. 154, 261-272.
49. Olwin, B. B., Hannon, K., and Kudla, A. J. (1994). Are fibroblast growth factors regulators of myogenesis in vivo? Prog. Growth Factor Res. 5, 145-158.
50. Ordahl, C. P., and Le Douarin, N. M. (1992). Two myogenic lineages within the developing somite. Development 114, 339-353.
51. Ordahl, C. P. (1993). Myogenic lineages within the developing somite. In "Molecular Basis of Morphogenesis," pp. 165-176. Liss, New York.
52. Ott, M.-O., Bober, E., Lyons, G., Arnold, H., and Buckingham, M. (1991). Early expression of the myogenic regulatory gene, myf-5, in precursor cells of skeletal muscle in the mouse embryo. Development 111, 1097-1107.
53. Packard, D. S., and Jacobson, A. G. (1976). The influence of axial structures on chick somite formation. Dev. Biol. 53, 36-48.
54. Patel, K., Connolly, D. J., Amthor, H., Nose, K., and Cooke, J. (1996). Cloning and early dorsal-axial expression of Flik, a chick Follistatin related gene; evidence for involvement in dorsalisation/neural induction. Dev. Biol., submitted for publication.
55. Pourquié, O., Coltey, M., Bréant, C., and Le Douarin, N. M. (1995). Control of somite patterning by signals from the lateral plate. Proc. Natl. Acad. Sci. USA 92, 3219-3223.
56. Pourquié, O., Coltey, M., Teillet, M.-A., Ordahl, C., and Le Douarin, N. M. (1993). Control of dorsoventral patterning of somite derivatives by notochord and floor plate. Proc. Natl. Acad. Sci. USA 90, 5242-5246.
57. Pourquié, O., Fan, C. M., Coltey, M., Hirsinger, E., Watanabe, Y., Breant, C., Francis-West, P., Brickell, P., Tessier-Lavigne, M., and Le Douarin, N. M. (1996). Lateral and axial signals involved in avian somite patterning: A role for BMP-4. Cell 84, 461-471.
58. Pownall, M. E., and Emerson, C. P. (1992). Sequential activation of three myogenic regulatory genes during somite morphogenesis in quail embryos. Dev. Biol. 151, 67-79.
59. Robson, L. G., Kara, T., Crawley, A., and Tickle, C. (1994). Tissue and cellular patterning of the musculature in chick wings. Development 120, 1265-1276.
60. Rong, P. M., Teillet, M. A., and Ziller, C. (1990). Differential influence of the neural primordium on muscle development in myotome and limb. In "The Avian Model in Developmental Biology: From Organism to Genes," edition du CNRS-1990, pp. 153-164.
61. Rong, P. M., Teillet, M.-A., Ziller, C., and Le Douarin, N.M. (1992). The neural tube/notochord complex is necessary for vertebral but not limb and body wall striated muscle differentiation. Development 115, 657-672.
62. Sassoon, P. A. (1993). Myogenic regulatory factors: dissecting their role and regulation during vertebrate embryogenesis. Dev. Biol. 156, 11-23.
63. Salzberg, S., Mandelbaum, M., Zaleberg, M., and Shainberg, A. (1995). Interruption of myogenesis by transforming growth factor beta 1 or EGTA inhibits expression and activity of the myogenic-associated (2′-5′) oligoadenylate synthetase and PKR. Exp. Cell. Res. 219, 223-232.
64. Sasai, Y., Lu, B., Steinbeisser, H., and De Robertis, E. M. (1995). Regulation of neural induction by the Chd and Bmp-4 antagonistic patterning signals in xenopus. Nature 376, 333-336.
65. Schemainda, H. (1979). Über die Entwicklung der occipitalen Somiten. Experimentelle Untersuchungen an Wachtel-und Hühnerembryonen. Verh. Anat. Ges. 73, 527-532.
66. Schmidt, J. E., Suzuki, A., Ueno, N., and Kimelman, D. (1995). Localized BMP-4 mediates dorsal/ventral patterning in the early Xenopus embryo. Dev. Biol. 169, 37-50.
67. Shibanuma, M., Jashimo, J., Mita, A., Kuroki, T., and Nose, K. (1993). Cloning from a mouse osteoblastic cell line of a set of transforming-growth-factors-regulated genes, one of which seems to encode a Follistatin-related polypeptide. Eur. J. Biochem. 217, 13-19.
68. Smith, T. H., Kachinsky, A. M., and Miller, J. B. (1994). Somite subdomains, muscle cell origins, and the four muscle regulatory factor proteins. J. Cell Biol. 127, 95-105.
69. Sosic, D., Christ, B., Brand-Saberi, B., Martin, J. F., and Olson, E. N. (1996). Mef2 and myogenic bMLH genes respond to different axial signals in the somites, submitted for publication.
70. Spence, M. S., Yip, J., and Erickson, C. A. (1996). The dorsal neural tube organizes the dermamyotome and induces axial myocytes in the avian embryo. Development 122, 231-241.
71. Stern, M. H., and Hauschka, S. D. (1995). Neural tube and notochord promote in vitro myogenesis in single somite explants. Dev. Biol. 167, 87-103.
72. Suzuki, A., Thies, R. S., Yamaji, N., Song, J. J., Wozney, J. M., Murakami, K., and Ueno, N. (1994). A truncated bone morphogenic protein receptor affects dorsal-ventral patterning in the early Xenopus embryo. Proc. Natl. Acad. Sci. USA 91, 10255-10259.
73. Trelstad, R. L., Hay, E. D., and Revel, J. P. (1967). Cell contact during early morphogenesis in the embryo. Dev. Biol. 16, 78-106.
74. van Bemmelen, J. F. (1889). Über die Herkunft der Extremitäten-und Zungenmuskulatur bei Eidechsen. Anat. Anz. 4, 240-255.
75. Veini, M., and Bellairs, R. (1991). Early mesoderm differentiation in the chick embryo. Anat. Embryol. 183, 143-149.
76. von Kirschhofer, K., Grim, M., Christ, B., and Wachtler, F. (1994). Emergence of myogenic and endothelial cell lineages in avian embryos. Dev. Biol. 163, 270-278.
77. Weintraub, H., Davis, R., Tapscott, S., Thayer, M., Krause, M., Benezra, R., Blackwell, T. K., Turner, D., Rupp, R., and Hollenberg, S. (1991). The myoD gene family: Nodal point during specification of the muscle cell lineage. Science 251, 761-766.
78. Williams, B. A., and Ordahl, C. P. (1994). Pax-3 expression in segmental plate marks early stages in myogenic cell specification. Development 120, 785-796.
79. Wilson, P. A., and Hemmati-Brivanlou, A. (1995). Induction of epidermis and inhibition of neural fate by BMP-4. Nature 376, 331-333.