Terminally differentiated skeletal myotubes are not confined to G 0 but can enter G 1 upon growth factor stimulation

Cell Growth and Differentiation

Volumn 7, Issue 8, 1996, Pages 1039-1050

  Tiainen, Marianne ^a   Pajalunga, Deborah ^a   Ferrantelli, Flavia ^a   Soddu, Silvia ^a   Salvatori, Giovanni ^b   Sacchi, Ada ^a   Crescenzi, Marco ^a  

^a REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH FACTOR;

ARTICLE; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL DIFFERENTIATION; CELL GROWTH; DNA SYNTHESIS; GENE CONTROL; GENE EXPRESSION; HORMONAL REGULATION; MYOTUBE; PRIORITY JOURNAL; SKELETAL MUSCLE;

ADENOVIRUS E1A PROTEINS; ANIMALS; BLOTTING, NORTHERN; BLOTTING, WESTERN; CELL CYCLE PROTEINS; CELLS, CULTURED; DNA; G0 PHASE; G1 PHASE; GROWTH SUBSTANCES; HELIX-LOOP-HELIX MOTIFS; INHIBITOR OF DIFFERENTIATION PROTEIN 1; MICE; MUSCLE, SKELETAL; ONCOGENES; RECOMBINANT FUSION PROTEINS; REPRESSOR PROTEINS; RNA; S PHASE; TIME FACTORS; TRANSCRIPTION FACTORS; TRANSFECTION;

MAMMALIA;

EID: 0029842439     PISSN: 10449523     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (59)

1. Okazaki, K., and Holtzer, H. Myogenesis: fusion, myosin synthesis, and the mitotic cycle. Proc. Natl. Acad. Sci. USA, 56: 1484-1490, 1966.
2. Weintraub, H., Davis, R., Tapscott, S., Thayer, M., Krause, M., Benezra, R., Blackwell, K. T., Turner, D., Rupp, R., Hollenberg, S., Zhuang, Y., and Lassar, A. The myoD gene family: nodal point during specification of the muscle cell lineage. Science (Washington DC), 251: 761-766, 1991.
3. Olson, E. N. MyoD family: a paradigm for development? Genes Dev., 4: 1454-1461, 1990.
4. Crescenzi, M., Soddu, S., Sacchi, A., and Tató, F. Adenovirus infection induces reentry into the cell cycle of terminally differentiated skeletal muscle cells. Ann. N. Y. Acad. Sci., 752: 9-18, 1995.
5. Crescenzi, M., Soddu, S., and Tató, F. Mitotic cycle reactivation in terminally differentiated cells by adenovirus infection. J. Cell. Physiol., 1 62: 26-35, 1995.
6. Cardoso, M. C., Leonhardt, H., and Nadal-Ginard, B. Reversal of terminal differentiation and control of DNA replication: cyclin A and cdk2 specifically localize at subnuclear sites of DNA replication. Cell, 74: 979-992, 1993.
7. Endo, T., and Nadal-Ginard, B. SV40 large T antigen induces reentry of terminally differentiated myotubes into the cell cycle. In: L. H. Kedes and F. E. Stockdale (eds.),. Cellular and Molecular Biology of Muscle Development, pp. 95-104. New York: Alan R. Liss, Inc., 1989.
8. Yaffe, D., and Gershon, D. Multinucleated muscle fibres: induction of DNA synthesis and mitosis by polyoma virus infection. Nature (Lond.), 215: 421-424, 1967.
9. Endo, T., and Nadal-Ginard, B. Transcriptional and posttranscriptional control of c-myc during myogenesis: its mRNA remains inducible in dif- ferentiated cells and does not suppress the differentiated phenotype. Mol. Cell. Biol., 6: 1412-1421, 1986.
10. Crescenzi, M., Fleming, T. P., Lassar, A. B., Weintraub, H., and Aaronson, S. A. MyoD induces growth arrest independent of differentiation in normal and transformed cells. Proc. Natl. Acad. Sci. USA, 87: 8442-8446, 1990.
11. Sorrentino, V., Pepperkok, R., Davis, R. L., Ansorge, W., and Philipson, L. Cell proliferation inhibited by MyoD1 independently of myogenic differentiation. Nature (Lond.), 345: 813-815, 1990.
12. -/- muscle cells. Science (Washington DC), 2 64: 1467-1471, 1994.
13. Gu, W., Schneider, J. W., Condorelli, G., Kaushal, S., Mahdavi, V., and Nadal-Ginard, B. Interaction of myogenic factors and the retinoblastoma protein mediates muscle cell commitment and differentiation. Cell, 72: 309-324, 1993.
14. Guo, K., Wang, J., Andres, V., Smith, R. C., and Walsh, K. MyoD-induced expression of p21 inhibits cyclin-dependent kinase activity upon myocyte terminal differentiation. Mol. Cell. Biol., 1 5: 3823-3829, 1995.
15. Halevy, O., Novitch, B. G., Spicer, D. B., Skapek, S. X., Rhee, J., Hannon, G. J., Beach, D., and Lassar, A. B. Correlation of terminal cell cycle arrest of skeletal muscle with induction of p21 by MyoD. Science (Washington DC), 2 67: 1018-1021, 1995.
16. Jiang, H., Lin, J., Su, Z-z., Collart, F. R., Huberman, E., and Fisher, P. B. Induction of differentiation in human promyelocytic HL-60 leukemia cells activates p21, WAF1/CIP1, expression in the absence of p53. Oncogene, 9: 3397-3406, 1994.
17. Missero, C., Calautti, E., Eckner, R., Chin, J., Tsai, L. H., Livingston, D. M., and Dotto, G. P. Involvement of the cell-cycle inhibitor Cip1/MAF1 and the E1A-associated p300 protein in terminal differentiation. Proc. Natl. Acad. Sci. USA, 92: 5451-5455, 1995.
18. Cip1 in muscle and other terminally differentiated cells. Science (Washington DC), 2 67: 1024-1027, 1995.
19. Skapek, S. S., Rhee, J., Spicer, D. B., and Lassar, A. B. Inhibition of myogenic differentiation in proliferating myoblasts by cyclin D1-dependent kinase. Science (Washington DC), 2 67: 1022-1024, 1995.
20. Steinman, R. A., Hoffman, B., Iro, A., Guillouf, C., Liebermann, D. A., and El-Houseini, M. E. Induction of p21 (WAF-1/CIP1) during differentiation. Oncogene, 9: 3389-3396, 1994.
21. Baserga, R. The biology of cell reproduction. Cambridge: Harvard University Press, 1985.
22. v-src in postmitotic quail myotubes. Mol. Cell. Biol., 1 1: 3331-3338, 1991.
23. Gosset, L. A., Zhang, W., and Olson, E. N. Dexamethasone-dependent inhibition of differentiation of C2 myoblasts bearing steroid-inducible N-ras oncogenes. J. Cell Biol., 1 06: 2127-2137, 1988.
24. Crescenzi, M., Crouch, D. H., and Tató, F. Transformation by myc prevents fusion but not biochemical differentiation of C2C12 myoblasts: mechanisms of phenotypic correction in mixed culture with normal cells. J. Cell Biol., 125: 1137-1145, 1994.
25. Wolff, J. A., Dowty, M. E., Jiao, S., Repetto, G., Berg, R. K., Ludtke, J. J., and Williams, P. Expression of naked plasmids by cultured myotubes and entry of plasmids into T tubules and caveolae of mammalian skeletal muscle. J. Cell Sci., 1 03: 1249-1259, 1992.
26. Johnson, D. G., Schwarz, J. K., Cress, D. W., and Nevins, J. R. Expression of transcription factor E2F1 induces quiescent cells to enter S phase. Nature (Lond.), 365: 349-352, 1993.
27. Shan, B., and Lee, W-H. Deregulated expression of E2F-1 induces S-phase entry and leads to apoptosis. Mol. Cell. Biol., 1 4: 8166-8173, 1994.
28. Weinberg, R. A. The retinoblastoma protein and cell cycle control. Cell, 81: 323-330, 1995.
29. Barone, M. V., Pepperkok, R., Peverali, F. A., and Philipson, L. Id proteins control growth induction in mammalian cells. Proc. Natl. Acad. Sci. USA, 91: 4985-4988, 1994.
30. 1 progression by E2A and Id helix-loop-helix proteins. EMBO J., 1 3: 4291-4301, 1994.
31. Benezra, R., Davis, R. L., Lockshon, D., Turner, D. L., and Weintraub, H. The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell, 61: 49-59, 1990.
32. Jen, Y., Weintraub, H., and Benezra, R. Overexpression of Id protein inhibits the muscle differentiation program: in vivo association of Id with E2A proteins. Genes Dev., 6: 1466-1479, 1992.
33. 1/S phosphorylation of the retinoblastoma protein is associated with an altered affinity for the nuclear compartment. Cell, 65: 381-393, 1991.
34. Kelly, K., Cochran, B. H., Stiles, C. D., and Leder, P. Cell-specific regulation of the c-myc gene by lymphocyte mitogens and platelet-derived growth factor. Cell, 35: 603-610, 1983.
35. Lamph, W. W., Wamsley, P., Sassone-Corsi, P., and Verma, I. M. Induction of proto-oncogene JUN/AP-1 by serum and TPA. Nature (Lond.), 334: 629-631, 1988.
36. Müller, R., Bravo, R., and Burckhardt, J. Induction of c-fos gene and protein by growth factors precedes activation of c-myc. Nature (Lond.), 372: 716-720, 1984.
37. Spitkovsky, D., Sleiner, P., Lukas, J., Lees, E., Pagano, M., Schulze, A., Joswig, S., Picard, D., Tommasino, M., Eilers, M., and Jansen-Dürr, P. Modulation of cyclin gene expression by adenovirus E1A in a cell line with E1A-dependent conditional proliferation. J. Virol., 68: 2206-2214, 1994.
38. Nevins, J. R. E2F: a link between the Rb tumor suppressor protein and viral oncoproteins. Science (Washington DC), 258: 424-429, 1992.
39. Chellappan, S. P., Hiebert, S., Mudryi, M., Horowitz, J. M., and Nevins, J. R. The E2F transcription factor is a cellular target for the RB protein. Cell, 65: 1053-1061, 1991.
40. Hara, E., Ohshima, T., Ishii, T., Sugino, W., Tsutsui, K., Nakada, S., Tsuchida, N., and Oda, K. Mechanism of induction of cellular DNA synthesis by the adenovirus E1A 12S cDNA product. Exp. Cell Res., 1 98: 250-258, 1992.
41. Goldstein, S. Replicative senescence: the human fibroblast comes of age. Science (Washington DC), 249: 1129-1133, 1990.
42. Clegg, C. H., and Hauschka, S. D. Heterokaryon analysis of muscle differentiation: regulation of the postmitotic state. J. Cell Biol., 105: 937-947, 1987.
43. Ringertz, N. R., and Savage, R. E. Cell hybrids. New York: Academic Press, 1976.
44. Seshadri, T., and Campisi, J. Repression of c-fos transcription and an altered genetic program in senescent human fibroblasts. Science (Washington DC), 2 47: 205-209, 1990.
45. 1 progression and are repressed in senescent human fibroblasts. J. Biol. Chem., 2 69: 2139-2145, 1994.
46. 1 cyclins in senescent human diploid fibroblasts: accumulation of inactive cyclin E-Cdk2 and cyclin D1-Cdk2 complexes. Proc. Natl. Acad. Sci. USA, 90: 11034-11038, 1993.
47. Duprey, P., and Lesens, C. Control of skeletal muscle-specific transcription: involvement of paired homeodomain and MADS domain transcription factors. Int. J. Dev. Biol., 38: 591-604, 1994.
48. Gosset, L. A., Kelvin, D. J., Sternberg, E. A., and Olson, E. N. A new myocyte-specific enhancer-binding factor that recognizes a conserved element associated with multiple muscle-specific genes. Mol. Cell. Biol., 9: 5022-5033, 1989.
49. Blau, H. M., Pavlath, G. K., Hardeman, E. C., Chiu, C-P., Silberstein, L., Webster, S. G., Miller, S. C., and Webster, C. Plasticity of the differentiated state. Science (Washington DC), 2 30: 758-766, 1985.
50. Yaffe, D., and Saxel, O. Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature (Lond.), 2 70: 725-727, 1977.
51. Rando, T. A., and Blau, H. M. Primary mouse myoblast purification, characterization, and transplantation for cell-mediated gene therapy. J. Cell Biol., 1 25: 1275-1287, 1994.
52. Di Fiore, P. P., Pierce, J. H., Fleming, T. P., Hazan, R., Ullrich, A., King, C. R., Schlessinger, J., and Aaronson, S. A. Overexpression of the human EGF receptor confers an EGF-dependent transformed phenotype to NIH 3T3 cells. Cell, 51: 1063-1070, 1987.
53. Santos, E., Tronick, S. R., Aaronson, S. A., Pulciani, S., and Barbacid, M. T24 human bladder carcinoma oncogene is an activated form of the normal human homologue of BALB- and Harvey-MSV transforming genes. Nature (Lond.), 2 98: 343-347, 1982.
54. Sala, A., and Calabretta, B. Regulation of BALB/c 3T3 fibroblast proliferation by B-myb is accompanied by selective activation of cdc2 and cyclin D1 expression. Proc. Natl. Acad. Sci. USA, 89: 10415-10419, 1992.
55. Bernards, R., Houweling, A., Schrier, P. I., Bos, J. L., and van der Eb, A. J. Characterization of cells transformed by Ad5/Ad12 hybrid early region I plasmids. Virology, 1 20: 422-432, 1982.
56. Jiao, S., Schultz, E., and Wolff, J. A. Intracerebral transplants of primary muscle cells: a potential "platform" for transgene expression in the brain. Brain Res., 575: 143-147, 1992.
57. Digiesi, G., Giacomini, P., Fraioli, R., Mariani, M., Nicotra, M. R., Segatto, O., and Natali, P. G. Production and characterization of murine mAbs to the extracellular domain of human neu oncogene product GP185HER2. Hybridoma, 1 1: 519-527, 1992.
58. Bader, D., Masaki, T., and Fischman, D. A. Immunochemical analysis of myosin heavy chain during avian myogenesis in vivo and in vitro. J. Cell Biol., 95: 763-770, 1982.
59. Sambrook, J., Fritsch, E. F., and Maniatis, T. Molecular Cloning. A Laboratory Manual. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory, 1989.