p21 and retinoblastoma protein control the absence of DNA replication in terminally differentiated muscle cells

Journal of Cell Biology

Volumn 149, Issue 2, 2000, Pages 281-292

  Mal, Asoke ^a   Chattopadhyay, Debasis ^a   Ghosh, Mrinal K ^a   Poon, Randy Y C ^b   Hunter, Tony ^c   Harter, Marian L ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b HONG KONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Hong Kong)

^c SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

C2C12 cells; Cell cycle; DNA replication; E1A; p21

Indexed keywords

CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE INHIBITOR; CYCLINE; DNA; GROWTH FACTOR; PROTEIN P21; RETINOBLASTOMA PROTEIN; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CELL CYCLE; CONTROLLED STUDY; DNA REPLICATION; ENZYME ACTIVITY; GENE CONTROL; MOUSE; MUSCLE DEVELOPMENT; MYOBLAST; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION;

ADENOVIRUS E1A PROTEINS; ANIMALS; CDC2-CDC28 KINASES; CELL DIFFERENTIATION; CELL LINE; CELL-FREE SYSTEM; CYCLIN E; CYCLIN-DEPENDENT KINASE 2; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLIN-DEPENDENT KINASES; CYCLINS; DNA REPLICATION; MICE; MUSCLE, SKELETAL; MUTAGENESIS; PROTEIN-SERINE-THREONINE KINASES; RECOMBINANT PROTEINS; RETINOBLASTOMA PROTEIN; TRANSFECTION;

ADENOVIRIDAE; ANIMALIA;

EID: 0034678364     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.149.2.281     Document Type: Article

References (72)

1. Andres, 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.
2. Bader, B., I. Masaki, and D.A. Fischman. 1982. Biochemical analysis of myosin heavy chain during avian myogenesis in vivo and in vitro. J. Cell Biol. 95: 763-770.
3. Cardoso, M.C., H. Leonhardt, and B. Nadal-Ginard. 1993. 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.
4. Cenciarelli, C., F. De Santa, P.L. Puri, E. Mattei, L. Ricci, F. Bucci, A. Felsani, and M. Caruso. 1999. Critical role played by cyclin D3 in the MyoD-mediated arrest of cell cycle during myoblast differentiation. Mol. Cell. Biol. 19: 5203-5217.
5. Clurman, B.E., R.J. Sheaff, K. Thress, M. Groudine, and J.M. Roberts. 1996. Turnover of cyclin E by the ubiquitin-proleasome pathway is regulated by cdk2 binding and cyclin phosphorylation. Genes Dev. 10:1979-1990.
6. Crescenzi, M., S. Soddu, and F. Tato. 1995. Mitotic cycle reactivation in terminally differentiated cells by adenovirus infection. J. Cell. Physiol. 162:26-35.
7. 1-S phase protein kinase. Science. 257:1958-1961.
8. Dutta, A., and S.P. Bell. 1997. Initiation of DNA replication in eukaryotic cells. Annu. Rev. Cell Dev. Biol. 13:293-332.
9. Dyson, N. 1998. The regulation of E2F by pRB-family proteins. Genes Dev. 12: 2245-2262.
10. Endo, T., and B. Nadal-Ginard. 1989. SV40 large T antigen induces reentry of terminally differentiated myotubes into the cell cycle. In Cellular and Molecular Biology of Muscle Development. L.H. Kedes and F.E. Stockdale, editors. Alan R. Liss, Inc, New York. 95-104.
11. Flint, J., and T. Shenk. 1997. Viral transactivating proteins. Annu. Rev. Genet. 31:177-212.
12. INK4c and its predominant association with CDK4 and CDK6 during myogenic differentiation. Mol. Biol. Cell. 7:1587-1599.
13. Funk, J.O., S. Waga, J.B. Harry, E. Espling, B. Stillman, and D.A. Galloway. 1997. Inhibition of CDK activity and PCNA-dependent DNA replication by p21 is blocked by interaction with the HPV-16 E7 oncoprotein. Genes Dev. 11:2090-2100.
14. Gao, C.Y., and P.S. Zelenka. 1997. Cyclins, cyclin-dependent kinases and differentiation. Bioessays. 19:307-314.
15. Gu, W., J.W. Schneider, G. Condorelli, S. Kaushal, V. Mahdavi, and B. Nadal-Ginard. 1993. Interaction of myogenic factors and the retinoblastoma protein mediates muscle cell commitment and differentiation. Cell. 72:309-324.
16. Guo, K., J. Wang, V. Andres, R.C. 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.
17. 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. 267:1018-1021.
18. Harlow, E., B.R. Franza, Jr., and C. Schley. 1985. Monoclonal antibodies specific for adenovirus early region IA proteins: extensive heterogeneity in early region 1A products. J. Virol. 55:533-546.
19. Harper, J.W., S.J. Elledge, K. Keyomarsi, B. Dynlacht, L.-H. Tsai, P. Zhang, S. Dobrowolski, C. Bai, L. Connell-Crowley, E. Swindell, et al. 1995. Inhibition of cyclin-dependent kinases by p21. Mol. Biol. Cell. 6:387-400.
20. Cip1. Genes Dev. 24:3882-3888.
21. Herwig, S., and M. Strauss. 1997. The retinoblastoma protein: a master regulator of cell cycle, differentiation and apoptosis. Eur. J. Biochem. 246:581-601.
22. Iujvidin, S., O. Fuchs, U. Nudel, and D. Yaffe. 1990. SV40 immortalizes myogenic cells: DNA synthesis and mitosis in differentiating myotubes. Differentiation. 43:192-203.
23. Jahn, L., J.-I. Sadoshima, and S. Izumo. 1994. Cyclins and cyclin-dependent kinases are differentially regulated during terminal differentiation of C2C12 muscle cells. Exp. Cell Res. 212:297-307.
24. Cip1-mediated inhibition of cdk2. Genes Dev. 11:2101-2111.
25. Knudsen, E.S., and J.Y.J. Wang. 1996. Differential regulation of retinoblastoma protein function by specific cdk phosphorylation sites. J. Biol. Chem. 271: 8313-8320.
26. 1/S transition and S-phase progression. Genes Dev. 12:2278-2292.
27. Koff, A. 1991. Human cyclin E, a new cyclin that interacts with two members of the CDC2 gene family. Cell. 66:1217-1224.
28. 1 phase of the human cell cycle. Science. 257:1689-1693.
29. Kowalik, T.F., J. DeGregori, J.K. Schwarz, and J.R. Nevins. 1995. E2F1 overexpression in quiescent fibroblasts leads to induction of cellular DNA synthesis and apoptosis. J. Virol. 69:2491-2500.
30. Lassar, A.B., S.X. Skapek, and B. Novitch. 1994. Regulatory mechanisms that coordinate skeletal muscle differentiation and cell cycle withdrawal. Curr. Opin. Cell Biol. 6:788-794.
31. Lees, E., B. Faha, V. Dulic, S.I. Reed, and E. Harlow. 1992. Cyclin E/cdk2 and cyclin A/cdk2 kinases associate with p107 and E2F in a temporally distinct manner. Genes Dev. 6:1874-1885.
32. Lundblad, J.R., R.P.S. Kwok, M.E. Laurance, M.L. Harter, and R.H. Goodman. 1995. Adenoviral E1A-associated p300 is a functional homologue of the transcriptional co-activator CBP. Nature. 374:85-88.
33. Kip1 in TGF-b treated cells. Nature. 380:262-265.
34. Missero, C., E. Calautti, R. Eckner, J. Chin, L.H. Tsai, D.M. Livingston, and G.P. Dotto. 1995. Involvement of the cell-cycle inhibitor Cip1/WAF1 and the E1A-associated p300 protein in terminal differentiation. Proc. Natl. Acad. Sci. USA. 92:5451-5455.
35. Cip1/WAF1 alters keratinocyte growth and differentiation and promotes ras-tumor progression. Genes Dev. 10:3065-3075.
36. Morgan, D.O. 1995. Principles of CDK regulation. Nature. 374:131-134.
37. Morgan, D.O. 1997. Cyclin-dependent kinases: engines, clocks, and microprocessors. Annu. Rev. Cell Dev. Biol. 13:261-291.
38. Mumberg, D., K. Haas, T. Moroy, R. Niedenthal, J.H. Hegemann, M. Funk, and R. Muller. 1996. Uncoupling of DNA replication and cell cycle progression by human cyclin E. Oncogene. 13:2493-2497.
39. Neville, C., N. Rosenthal, M. McGrew, N. Bogdanova, and S. Hauschka. 1997. Skeletal muscle cultures. In Methods in Muscle Biology. C.P. Emerson, Jr. and H.L. Sweeney, editors. Academic Press, New York. 85-114.
40. Nomura, H., Y. Sawada, and S. Ohtaki. 1998. Interaction of p27 with E1A and its effect on cdk kinase activity. Biochem. Biophys. Res. Commun. 248:228-234.
41. 2 phases of the cell cycle. J. Cell Biol. 135:441-456.
42. 1-to-S phase transition. Mol. Cell. Biol. 15:2612-2624.
43. Olson, E.N., H.-H. Arnold, P.W.J. Rigby, and B.J. Wold. 1996. Know your neighbors: three phenotypes in null mutants of the myogenic bHLH gene MRF4. Cell. 85:1-4.
44. Kip1 in anchorage-independent cells. Oncogene. 16:2575-2583.
45. Otten, A.D., E.J. Firpo, A.N. Gerber, L.L. Brody, J.M. Roberts, and S.J. Tapscott. 1997. Inactivation of MyoD-mediated expression of p21 in tumor cell lines. Cell Growth Diff. 8:1151-1160.
46. Pajalunga, D., D. Tognozzi, M. Tiainen, M. D'Angelo, F. Ferranteli, D. Helin, A. Sacchi, and M. Crescenzi. 1999. E2F activates late-G1 events but cannot replace E1A in inducing S phase in terminally differentiated skeletal muscle cells. Oncogene. 18:5054-5062.
47. Cip1 in muscle and other terminally differentiating cells. Science. 267: 1024-1027.
48. Kip1, a cyclin-dependent kinase inhibitor and a potential mediator of extracellular antimitogenic signals. Cell. 78:59-66.
49. Cip1/WAF1 in UV-irradiated and transformed cells. Oncogene. 16:1333-1343.
50. Puri, P.L., C. Balsano, V.L. Burgio, P. Chirillo, G. Natoli, L. Ricci, E. Mattei, A. Graessmann, and M. Levrero. 1997. MyoD prevents cyclin A/cdk2 containing E2F complexes formation in terminally differentiated myocytes. Oncogene. 14:1171-1184.
51. Puri, P.L., L. Cimino, M. Fulco, C. Zimmerman, N.B. La Thangue, A. Giordano, A. Graessmann, and M. Levrero. 1998. Regulation of E2F4 mitogenic activity during terminal differentiation by its heterodimerization partners for nuclear translocation. Cancer Res. 58:1325-1331.
52. Raychaudhuri, P., S. Bagchi, S.H. Devoto, V.B. Kraus, E. Morgan, and J.R. Nevins. 1991. Domains of the adenovirus E1A protein required for oncogenic activity are also required for dissociation of E2F transcription factor complexes. Genes Dev. 5:1200-1211.
53. / muscle cells. Science. 264:1467-1471.
54. Sherr, C.J. 1994. G1 phase progression: cycling on cue. Cell. 79:551-555.
55. 1 cyclin-dependent kinases. Genes Dev. 9:1149-1163.
56. 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.
57. Skapek, S.X., J. Rhee, P.S. Kim, B.G. Novitch, and A.B. Lassar. 1996. Cyclin-mediated inhibition of muscle gene expression via a mechanism that is independent of pRB hyperphosphorylation. Mol. Cell. Biol. 16:7043-7053.
58. Stein, R.W., M. Corrigan, P. Yaciuk, J. Whelan, and E. Moran. 1990. Analysis of E1A-mediated growth regulation functions: binding of the 300-kilodalton cellular product correlates with E1A enhancer repression function and DNA synthesis-inducing activity. J. Virol. 64:4421-4427.
59. Sterner, J.M., S. Dew-Knight, C. Musahl, S. Kornbluth, and J.M. Horowitz, 1998. Negative regulation of DNA replication by the retinoblastoma protein is mediated by its association with MCM7. Mol. Cell. Biol. 18:2748-2757.
60. Tedesco, D., L. Baron, L. Fischer-Fantuzzi, and C. Vesco. 1997. Induction of cyclins E and A in response to mitogen removal: a basic alteration associated with the arrest of differentiation of C2 myoblasts transformed by simian virus 40 large T antigen. J. Virol. 71:2217-2224.
61. 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.
62. 1 upon growth factor stimulation. Cell Growth Diff. 7:1039-1050.
63. Tiainen, M., D. Spitkovsky, P. Jansen-Durr, A. Sacchi, and M. Crescenzi. 1996b. Expression of E1A in terminally differentiated muscle cells reactivates the cell cycle and suppresses tissue-specific genes by separable mechanisms. Mol. Cell. Biol. 16:5302-5312.
64. Wang, D.-M., B. Dalie, and M.L. Harter. 1992. The adenovirus E1A 243R protein purified from Escherichia coli under nondenaturing conditions is found in association with dnaK. Protein Expr. Purif. 3:8-17.
65. Wang, H.-G.H., Y. Rikitake, M.C. Carter, P. Yaciuk, S.E. Abraham, B. Zerler, and E. Moran. 1993. Identification of specific adenovirus E1A N-terminal residues critical to the binding of cellular proteins and the control of cell growth. J. Virol. 67:476-488.
66. Wang, J., and K. Walsh. 1996. Inhibition of retinohlastoma protein phosphorylation by myogenesis-indueed changes in the subunit composition of the cyclin-dependent kinase 4 complex. Cell Growth Diff. 7:1471-1478.
67. Wang, J., K. Helin, P. Jin, and B. Nadal-Ginard. 1995. Inhibition of in vitro myogenic differentiation by cellular transcription factor E2F1. Cell Growth Diff. 6:1299-1306.
68. Wang, J., K. Guo, K.N. Wills, and K. Walsh. 1997. Rb functions to inhibit apoptosis during myocyte differentiation. Cancer Res. 57:351-354.
69. Weintraub, H. 1993. The MyoD family and myogenesis: Redundancy, networks, and thresholds. Cell. 75:1241-1244.
70. Wolff, J.A., M.E. Dowty, S. Jiao, G. Repetto, R.K. Berg, J.J. Ludtke, P. Williams, and D.B. Slautterback. 1992. Expression of naked plasmids by cultured myotubes and entry of plasmids into T tubules and caveolae of mammalian skeletal muscle. J. Cell Sci. 103:1249-1259.
71. Yaffe, D., and O. Saxel. 1977. Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature. 270:725-727.
72. Zacksenhaus, E., Z. Jiang, D. Chung, J.D. Marth, R.A. Phillips, and B.L. Gallie. 1996. pRb controls proliferation, differentiation, and death of skeletal muscle cells and other lineages during embryogenesis. Genes Dev. 10:3051-3064.