The muscle regulatory factors MyoD and Myf-5 undergo distinct cell cycle-specific expression in muscle cells

Journal of Cell Biology

Volumn 142, Issue 6, 1998, Pages 1447-1459

  Kitzmann, Magali ^a   Carnac, Gilles ^a   Vandromme, Marie ^a   Primig, Michael ^b   Lamb, Ned J C ^a   Fernandez, Anne ^a  

^a INSTITUTE OF HUMAN GENETICS   (France)

^b INSTITUT PASTEUR   (France)

Author keywords

Cell cycle; Differentiation; Muscle; Myf 5; MyoD

Indexed keywords

MYOD1 PROTEIN; MYOGENIC FACTOR;

ANIMAL CELL; ARTICLE; CELL CYCLE; CELL DIFFERENTIATION; CELL POPULATION; DOWN REGULATION; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; MOUSE; MUSCLE CELL; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; REGULATORY MECHANISM;

ANIMALS; CELL CYCLE; CELL DIFFERENTIATION; CELL DIVISION; CELL LINE; CELLS, CULTURED; DNA-BINDING PROTEINS; METHIONINE; MICE; MICE, INBRED BALB C; MUSCLE PROTEINS; MUSCLES; MYOD PROTEIN; MYOGENIC REGULATORY FACTOR 5; TRANS-ACTIVATORS;

EID: 0032555944     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.142.6.1447     Document Type: Article

References (53)

1. Albagli-Curiel, O., G. Carnac, M. Vandromme, S. Vincent, P. Crepieux, and A. Bonnieu. 1993. Serum-induced inhibition of myogenesis is differentially relieved by retinoic acid and triiodolhyronine in C2 murine muscle cells. Differentiation. 52:201-210.
2. Alterio, J., Y. Courtois, J. Robelin, D. Bechet, and I. Martelly. 1990. Acidic and basic fibroblast growth factor mRNAs are expressed by skeletal muscle satellite cells. Biochem. Biophys. Res. Commun. 166:1205-1212.
3. Andrés, V., and K. Walsh. 1996. Myogenin expression, cell cycle withdrawal, and phenotypic differentiation are temporally separable events that precede cell fusion upon myogenesis. J. Cell Biol. 132:657-666.
4. Auradé, F., C. Pinset, P. Chaffey, F. Gros, and D. Montarras. 1994. Myf-5, MyoD, Myogenin and MRF4 myogenic derivatives of the embryonic mesenchymal cell line 10T1/2 exhibit the same adult phenotype. Differentiation. 55: 185-192.
5. Auradé, F., C.M. Pfarr, C. Lindon, A. Garcia, M. Primig, D. Montarras, and C. Pinset. 1997. The glucocorticoid receptor and AP-1 are involved in a positive regulation of the muscle regulatory gene Myf-5 in cultured myoblasts. J. Cell Sci. 110:2771-2779.
6. Bartek, J., J. Bartkova, and J. Lukas. 1996. The retinoblastoma protein pathway and the restriction point. Curr. Opin. Cell Biol. 8:805-814.
7. Carnac, G., O. Albagli-Curiel, M. Vandromme, C. Pinset, D. Montarras, V. Laudet, and A. Bonnieu. 1992. 3,5,3′-Triiodothyronine positively regulates both MyoD1 gene transcription and terminal differentiation in C2 inyoblasts. Mol. Endocrinol. 6:1185-1194.
8. Carnac, G., M. Primig, M. Kitzmann, P. Chafey, D. Tuil, N. Lamb, and A. Fernandez. 1998. RhoA GTPase and serum response factor control selectively the expression of MyoD without affecting Myf-5 in mouse myoblasts. Mol. Biol. Cell. 9:1891-1902.
9. Catala, G., J.F. Savouret, B. Mendez, B.L. West, M. Karin, J.A. Martial, and J.D. Baxter. 1983. A method for isolation of intact, translationally active ribonucleic acid. DNA. 2:329-335.
10. Chelappan, S.P., S. Hiebert, M. Mudryj, J.M. Horowitz, and J.R. Nevins. 1991. The E2F transcription factor is a cellular target of the RB protein. Cell. 65: 1053-1061.
11. Chu, C., J. Cogswell, and D.S. Kohtz. 1997. MyoD functions as a transcriptional repressor in proliferating myoblasts. J. Biol. Chem. 272:3145-3148.
12. Clegg, C.H., T.A. Linkhart, and B.B. Olwin. 1987. Growth factor control of skeletal muscle differentiation: commitment to terminal differentiation occurs in G1 phase and is repressed by fibroblast growth factor. J. Cell Biol. 105:949-956.
13. Coats, S., W.M. Flanagan, J. Nourse, and J.M. Roberts. 1996. Requirement of p27kip1 for restriction point control of the fibroblast cell cycle. Science. 272: 877-880.
14. Crescenzi, M., T.P. Fleming, A.B. Lassar, H. Weintraub, and S.A. Aaronson. 1990. MyoD induces growth arrest independent of differentiation in normal and transformed cells. Proc. Natl. Acad. Sci. USA. 87:8442-8446.
15. Cornelison, D.D.W., and B. Wold. 1997. Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev. Biol. 191:270-284.
16. Davis, R.L., H. Weintraub, and A.B. Lassar. 1987. Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell. 51:987-1000.
17. Dias, P., D.M. Parham, D.N. Shapiro, S.J. Tapscott, and P.J. Houghton. 1992. Monoclonal antibodies to the myogenic regulatory protein MyoD1: epitope mapping and diagnostic utility. Cancer. Res. 52:6431-6439.
18. Filvaroff, E.H., R. Ebner and R. Derynck 1994. Inhibition of myogenic differentiation in myoblast expressing a truncated type II TGF-β receptor. Development (Camb.). 120:1085-1095.
19. Florini, J.R., K.A. Magri, D.Z. Ewton, P.L. James, K. Grindstaff, and P.S. Rotwein. 1991. "Spontaneous" differentiation of skeletal myoblasts is dependent upon autocrine secretion of insulin-like growth factor-II. J. Biol. Chem. 24:15917-15923.
20. Floss, T., H.H. Arnold, and T. Braun. 1997. A role for FGF-6 in skeletal muscle regeneration. Genes Dev. 11:2040-2051.
21. Girard, F., U. Strausfeld, A. Fernandez, and N.J.C. Lamb. 1991. CyclinA is required for the onset of DNA replication in mammalian fibroblasts. Cell. 67: 1169-1179.
22. Gu, W., J.W. Schneider, and G. Condorelly. 1993. Interaction of myogenic factors and the retinoblastoma protein mediates muscle cell commitment and differentiation. Cell. 72:309-324.
23. Guo, K., J. Wang, V. Andres, R. Smith, and K. Walsh. 1995. MyoD-induced expression of p21 inhibits cyclin-dependent kinase activity upon myocyte terminal differentiation. Mol. Cell Biol. 15:3823-3829.
24. Halevy, O., B.G. Novitch, D.B. Spicer, S.X. Skapek, J. Rhee, G.J. Hannon, D. Beach, and A.B. Lassar. 1995. Correlation of terminal cell cycle arrest of skeletal muscle with induction of p21 by MyoD. Science. 1018-1021.
25. Hunter, T., and J. Pines. 1994. Cyclins and cancer II: cyclin D and CDK inhibitors come of age. Cell. 79:573-582.
26. Krek, W., and J.A. DeCaprio. 1995. Cell synchronization. Methods Enzymol. 254:114-125.
27. Lamb, J.C., A. Fernandez, A. Watrin, J.C. Labée, and J.C. Cavadore. 1992. Microinjection of p34cdc2 kinase induces marked changes in cell shape, cytoskeletal organisation, and chromatin structure in mammalian fibroblasts. Cell. 60:151-165.
28. Lindon, C., D. Montarras, and C. Pinset. 1998. Cell cycle-regulated expression of the muscle determination factor Myf-5 in proliferating myoblasts. J. Cell Biol. 140:111-118.
29. Montarras, D., F. Aurade, T. Johnson, J. Ilan, F. Gros, and C. Pinset. 1996. Autonomous differentiation in the mouse myogenic cell line, C2, involves a mutual positive control between insulin like growth factor II and MyoD, operating as early as the myoblast stage. J Cell Sci. 109:551-560.
30. Nadal-Ginard, B. 1978. Commitment, fusion and biochemical differentiation of a myogenic cell line in the absence of DNA synthesis. Cell. 15:855-864.
31. Novitch, B.G., G.J. Mulligan, T. Jacks, and A.B. Lassar. 1996. Skeletal muscle cells lacking the retinoblasloma protein display defects in muscle gene expression and accumulate in S and G2 phases of the cell cycle. J. Cell Biol. 135:441-456.
32. Nurse, P. 1994. Ordering S phase and M phase in the cell cycle. Cell. 79:547-555.
33. Pagano, M., R. Pepperkok, J. Lukas, V. Baldin, W. Ansorge, J. Bartek, and G. Draetta. 1993. Regulation of the cell cycle by the cdk2 protein kinase in cultured human fibroblasts. J. Cell Biol. 121:101-111.
34. Pinset, C., and D. Montarras. 1994. A system for ex vivo studies of myogenesis: a protocol for the isolation of stable muscle cell populations from newborn adult mice. In Cell Biology: A Laboratory Handbook. J. Cells, editor. Academic Press, Inc., San Diego, CA. 199-206.
35. Pinsel, C., and R.G. Whalen. 1984. Manipulation of medium conditions and differentiation in the rat myogenic cell line L6. Dev. Biol. 102:269-277.
36. Pinsel, C., D. Montarras, J. Chenevert, A. Minty, P. Barton, C. Laurent, and F. Gros. 1988. Control of myogenesis in the mouse myogenic C2 cell line by medium composition and by insulin: characterisation of permissive and inductible C2 myoblasts. Differentiation, 38:28-34.
37. Polyak, K., M.H. Lee, H. Erdjument-Bromage, A. Koff, J.M. Roberts, P. Tempst, and J. Massague 1994. Cloning of P27Kip1, a cyclin dependent kinase inhibitor and a potential mediator of extracellular antimitogenic signals. Cell. 78:59-66.
38. Rao, S., and D.S. Kohtz. 1994. Positive and negative regulation of D-type cyclin expression in skeletal myoblasts by basic fibroblast growth factor and transforming growth factor β. J. Biol. Chem. 270:4093-4100.
39. Rudnicki, M.A., T. Braun, S. Hinuma, and R. Jaenisch. 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.
40. -/- muscle cells. Science. 264:1467-1471.
41. Schultz, E., and K.M. McCormick. 1994. Skeletal muscle satellite cells. Rev. Physiol. Biochem. Pharmacol. 123:213-257.
42. Skapek, S.X., J. Rhee, D.B. Spicer, and A.B. Lassar. 1995. Inhibition of myogenic differentiation in proliferating myoblasts by cyclin D1-dependent kinase. Science. 267:1022-1024.
43. Smith, C.K., M.J. Janney, and R.E. Allen. 1994. Temporal expression of myogenic regulatory genes during activation, proliferation, and differentiation of rat skeletal muscle satellite cells. J. Cell Physiol. 159:379-385.
44. Sorrentino, V., R. Pepperkok, R.L. Davis, W. Ansorge, and L. Pilipson. 1990. Cell proliferation inhibited by myoD1 independently of myogenic differentiation. Nature. 345:813-815.
45. Tapscott, S.J., R.J. Davis, M.J. Thayr, P. Cheng, H. Weintraub, and A.B. Lassar. 1988. MyoD1: a nuclear phosphoprotein requiring a myc homology region to convert fibroblasts to myoblasts. Science. 242:405-411.
46. Thorburn, A.M., P.A. Walton, and J.R. Feramisco. 1993. MyoD induced cell cycle arrest is associated with increased nuclear affinity of the Rb protein. Mol. Biol. Cell. 4:705-713.
47. Walsh, K., and H. Perlman. 1997. Cell cycle exit upon myogenic differentiation. Curr. Opin. Gen. Der. 7:597-602.
48. Weintraub, H., V.J. Dwarki, I. Verma, R. Davis, S. Hollemberg, L. Snider, A.B. Lassar, and S.J. Tapscott. 1991. Muscle-specific transcriptional activation by MyoD. Genes Dev. 5:1377-1386.
49. Weintraub, H. 1993. The MyoD family and myogenesis: redundancy, networks. and thresholds. Cell. 75:1241-1244.
50. Wright, W.E., D.A. Sassoon, and V.K. Lin. 1989. Myogenin, a factor regulating myogenesis, has a domain homologous to MyoD. Cell. 56:607-617.
51. Yablonka-Reuveni, Z., and A.J. Rivera. 1994. Temporal expression of regulatory and structural muscle proteins during myogenesis of satellite cells on isolated adult rat fibers. Dev. Biol. 164:588-603.
52. Yaffe, D., and O. Saxel. 1977. Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature. 270:725-727.
53. Zetterberg, A., O. Larsson, and K.G. Wiman. 1995. What is the restriction point? Curr. Opin. Cell Biol. 7:835-842.