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

Journal of Virology

Volumn 71, Issue 3, 1997, Pages 2217-2224

  Tedesco, Donato ^a   Baron, Livio ^a   Fischer Fantuzzi, Lia ^a   Vesco, Cesare ^a  

^a CNR   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN A; CYCLIN D1; CYCLIN DEPENDENT KINASE; CYCLIN E; MITOGENIC AGENT; MYOGENIN; VIRUS LARGE T ANTIGEN;

ANIMAL CELL; ARTICLE; CELL CYCLE; CELL DIFFERENTIATION; CELL TRANSFORMATION; IMMUNOBLOTTING; MOUSE; MUSCLE DEVELOPMENT; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; SIMIAN VIRUS 40;

EID: 0031041892     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.71.3.2217-2224.1997     Document Type: Article

References (87)

1. cdk2. J. Virol. 67:6551-6557.
2. Alemà, S., and F. Tatò. 1994. Oncogenes and muscle differentiation: multiple mechanisms of interference. Semin. Cancer Biol. 5:147-156.
3. Aprelikova, O., Y. Xiong, and E. T. Liu. 1995. Both p16 and p21 families of cyclin-dependent kinase (CDK) inhibitors block the phosphorylation of cyclin-dependent kinases by the CDK-activating kinase. J. Biol. Chem. 270: 18195-18197.
4. Bader, D. T., T. Masaki, and D. Fischman. 1982. Immunochemical analysis of myosin heavy chain during avian myogenesis in vivo and in vitro. J. Cell Biol. 95:763-770.
5. Baldin, V., J. Lukas, M. J. Marcote, M. Pagano, and G. Draetta. 1993. Cyclin D1 is a nuclear protein required for cell cycle progression in G(1). Genes Dev. 7:812-821.
6. Bernards, R., G. M. Schackleford, M. R. Gerber, J. M. Horowitz, S. H. Friend, M. Schartl, E. Bogenmann, J. M. Rapaport, T. McGee, T. P. Dryja, et al. 1989. Structure and expression of the murine retinoblastoma gene and characterization of its encoded protein. Proc. Natl. Acad. Sci. USA 86:6474-6478.
7. Buchberger, A., K. Ragge, and H. H. Arnold. 1994. The myogenin gene is activated during myocyte differentiation by pre-existing, not newly synthesized transcription factor MEF-2. J. Biol. Chem. 269:17289-17296.
8. Buckingham, M. 1994. Molecular biology of muscle development. Cell 78: 15-21.
9. Cao, L., B. Faha, M. Dembski, L. H. Tsai, E. Harlow, and N. Dyson. 1992. Independent binding of the retinoblastoma protein and p107 to the transcription factor E2F. Nature 355:176-179.
10. Cobrinik, D., P. Whyte, D. S. Peeper, T. Jacks, and R. A. Weinberg. 1993. Cell cycle-specific association of E2F with the p130 E1A-binding protein. Genes Dev. 7:2392-2404.
11. Coppola, J. A., B. A. Lewis, and M. D. Cole. 1990. Increased retinoblastoma gene expression is associated with late stages of differentiation in many different cell types. Oncogene 5:1731-1733.
12. Davis, R. L., H. Weintraub, and A. B. Lassar. 1987. Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell 51:987-1000.
13. DeCaprio, J. A., Y. Furukawa, F. Ajchenbaum, J. D. Griffin, and D. M. Livingston. 1992. The retinoblastoma-susceptibility gene product becomes phosphorylated in multiple stages during cell cycle entry and progression. Proc. Natl. Acad. Sci. USA 89:1795-1798.
14. 1/S-regulatory genes. Mol. Cell. Biol. 15:4215-4224.
15. Dynlacht, B. D., O. Flores, J. A. Lees, and E. Harlow. 1994. Differential regulation of E2F trans-activation by cyclin/cdk2 complexes. Genes Dev. 8:1772-1786.
16. Dyson, N., M. Dembski, A. Fattaey, C. Ngwu, M. Ewen, and K. Helin. 1993. Analysis of p107-associated proteins - p107 associates with a form of E2F that differs from pRB-associated E2F-1. J. Virol. 67:7641-7647.
17. Edmondson, D. G., T. C. Cheng, P. Cserjesi, T. Chakraborty, and E. N. Olson. 1992. Analysis of the myogenin promoter reveals an indirect pathway for positive autoregulation mediated by the muscle-specific enhancer factor MEF-2. Mol. Cell. Biol. 12:3665-3677.
18. Endo, T. 1992. SV40 large T inhibits myogenic differentiation partially through inducing c-jun. J. Biochem. (Tokyo) 112:321-329.
19. Endo, T., and S. Goto. 1992. Retinoblastoma gene product Rb accumulates during myogenic differentiation and is deinduced by the expression of SV40 large T antigen. J. Biochem. (Tokyo) 112:427-430.
20. Geng, Y., E. N. Eaton, M. Picon, J. M. Roberts, A. S. Lundberg, A. Gifford, C. Sardet, and R. A. Weinberg. 1996. Regulation of cyclin E transcription by E2Fs and retinoblastoma protein. Oncogene 12:1173-1180.
21. Giordano, A., P. Whyte, E. Harlow, B. R. Franza, D. Beach, and G. Draetta. 1989. A 60 kd cdc2-associated polypeptide complexes with the E1A proteins in Adenovirus-infected cells. Cell 58:981-990.
22. Grana, X., and E. P. Reddy. 1995. Cell cycle control in mammalian cells: role of cyclins, cyclin dependent kinases (CDKs), growth suppressor genes and cyclin-dependent kinase inhibitors (CKIs). Oncogene 11:211-219.
23. Gu, W., J. W. Schneider, G. Condorelli, S. Kaushal, V. Mahdavi, and B. Nadalginard. 1993. Interaction of myogenic factors and the retinoblastoma protein mediates muscle cell commitment and differentiation. Cell 72:309-324.
24. Guo, K., J. A. 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.
25. Haider, S. R., W. Wang, and S. J. Kaufman. 1994. SV40 T antigen inhibits expression of MyoD and myogenin, up-regulates Myf-5, but does not affect early expression of desmin or alpha 7 integrin during muscle development. Exp. Cell Res. 210:278-286.
26. 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.
27. Harper, J. W., S. J. Elledge, K. Keyomarsi, B. Dynlacht, L. H. Tsai, P. Zhang, S. Dobrowolski, C. Bai, L. Connell-Crowley, and E. Swindell. 1995. Inhibition of cyclin-dependent kinases by p21. Mol. Biol. Cell 6:387-400.
28. Hasty, P., A. Bradley, J. H. Morris, D. G. Edmondson, J. M. Venuti, E. N. Olson, and W. H. Klein. 1993. Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature 364:501-506.
29. 1, restriction point regulation in Rb-deficient fibroblasts. Mol. Cell. Biol. 16:2402-2407.
30. Hollenberg, S. M., P. F. Cheng, and H. Weintraub. 1993. Use of a conditional MyoD transcription factor in studies of Myod trans-activation and muscle determination. Proc. Natl. Acad. Sci. USA 90:8028-8032.
31. Hunter, T. 1991. Cooperation between oncogenes. Cell 64:249-270.
32. 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.
33. Jahn, L., J. 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.
34. Kato, J. Y., M. Matsuoka, D. K. Strom, and C. J. Sherr. 1994. Regulation of cyclin D-dependent kinase 4 (cdk4) by cdk4-activating kinase. Mol. Cell. Biol. 14:2713-2721.
35. Kiess, M., R. M. Gill, and P. A. Hamel. 1995. Expression and activity of the retinoblastoma protein (pRB)-family proteins, p107 and p130, during L(6) myoblast differentiation. Cell Growth Differ. 6:1287-1298.
36. Kiess, M., R. M. Gill, and P. A. Hamel. 1995. Expression of the positive regulator of cell cycle progression, cyclin D3, is induced during differentiation of myoblasts into quiescent myotubes. Oncogene 10:159-166.
37. Kitagawa, M., H. Higashi, I. Suzuki-Takahashi, K. Segawa, S. K. Hanks, Y. Taya, S. Nishimura, and A. Okuyama. 1995. Phosphorylation of E2F-1 by cyclin A-cdk2. Oncogene 10:229-236.
38. Krek, W., M. E. Ewen, S. Shirodkar, Z. Arany, W. G. Kaelin, and D. M. Livingston. 1994. Negative regulation of the growth-promoting transcription factor E2F-1 by a stably bound cyclin A-dependent protein kinase. Cell 78:161-172.
39. Lees, J. A., K. J. Buchkovich, D. R. Marshak, C. W. Anderson, and E. Harlow. 1991. The retinoblastoma protein is phosphorylated on multiple sites by human cdc2. EMBO J. 10:4279-4290.
40. Lin, S. Y., A. R. Black, D. Kostic, S. Pajovic, C. N. Hoover, and J. C. Azizkhan. 1996. Cell cycle-regulated association of E2F1 and Sp1 is related to their functional interaction. Mol. Cell. Biol. 16:1668-1675.
41. Lukas, J., J. Bartkova, H. Muller, D. Spitkovsky, A. A. Kjerulff, P. Jansendurr, M. Strauss, and J. Bartek. 1994. DNA tumor virus oncoproteins and retinoblastoma gene mutations share the ability to relieve the cells requirement for cyclin D1 function in G1. J. Cell Biol. 125:625-638.
42. Maione, R., and G. M. Fimia. Personal communication.
43. Maione, R., G. M. Fimia, and P. Amati. 1992. Inhibition of in vitro myogenic differentiation by a polyomavirus early function. Oncogene 7:85-93.
44. Mal, A., R. Y. C. Poon, P. H. Howe, H. Toyoshima, T. Hunter, and M. L. Harter. 1996. Inactivation of p27(Kip1) by the viral E1A oncoprotein in TGF beta-treated cells. Nature 380:262-265.
45. Manfredi, J. J., and C. Prives. 1994. The transforming activity of simian virus 40 large tumor antigen. Biochim. Biophys. Acta 1198:65-83.
46. Martelli, F., C. Cenciarelli, G. Santarelli, B. Polikar, A. Felsani, and M. Caruso. 1994. MyoD induces retinoblastoma gene expression during myogenic differentiation. Oncogene 9:3579-3590.
47. Mayol, X., X. Grana, A. Baldi, N. L. Sang, Q. J. Hu, and A. Giordano. 1993. Cloning of a new member of the retinoblastoma gene family (pRb2) which binds to the E1A transforming domain. Oncogene 8:2561-2566.
48. Moberg, K., M. A. Starz, and J. A. Lees. 1996. E2F-4 switches from p130 to p107 and pRB in response to cell cycle reentry. Mol. Cell. Biol. 16:1436-1449.
49. Morgan, D. O. 1995. Principles of CDK regulation. Nature 374:131-134.
50. Mudrak, I., E. Ogris, H. Rotheneder, and E. Wintersberger. 1994. Coordinated trans activation of DNA synthesis-and precursor-producing enzymes by polyomavirus LT antigen through interaction with the retinoblastoma protein. Mol. Cell. Biol. 14:1886-1892.
51. Ohkubo, Y., T. Kishimoto, T. Nakata, H. Yasuda, and T. Endo. 1994. SV40 large T antigen reinduces the cell cycle in terminally differentiated myotubes through inducing Cdk2, Cdc2, and their partner cyclins. Exp. Cell Res. 214:270-278.
52. Ohtani, K., J. Degregori, and J. R. Nevins. 1995. Regulation of the cyclin E gene by transcription factor E2F1. Proc. Natl. Acad. Sci. USA 92:12146-12150.
53. Olson, E. N. 1992. Interplay between proliferation and differentiation within the myogenic lineage. Dev. Biol. 154:261-272.
54. Olson, E. N., and W. H. Klein. 1994. bHLH factors in muscle development -dead lines and commitments, what to leave in and what to leave out. Genes Dev. 8:1-8.
55. Olson, E. N., M. Perry, and R. A. Schulz. 1995. Regulation of muscle differentiation by the MEF2 family of MADS box transcription factors. Dev. Biol. 172:2-14.
56. Pagano, M., S. W. Tam, A. M. Theodoras, P. Beerromero, G. Delsal, V. Chau, P. R. Yew, G. F. Draetta, and M. Rolfe. 1995. Role of the ubiquitin-proteasome pathway in regulating abundance of the cyclin-dependent kinase inhibitor p27. Science 269:682-685.
57. Parker, S. B., G. Eichele, P. M. Zhang, A. Rawls, A. T. Sands, A. Bradley, E. N. Olson, J. W. Harper, and S. J. Elledge. 1995. P53-independent expression of p21(Cip)1 in muscle and other terminally differentiating cells. Science 267:1024-1027.
58. Peeper, D. S., P. Keblusek, K. Helin, M. Toebes, A. J. Vandereb, and A. Zantema. 1995. Phosphorylation of a specific cdk site in E2F-1 affects its electrophoretic mobility and promotes pRB-binding in vitro. Oncogene 10: 39-48.
59. Peterson, S. R., D. M. Gadbois, E. M. Bradbury, and P. M. Kraemer. 1995. Immortalization of human fibroblasts by SV40 large T antigen results in the reduction of cyclin d1 expression and subunit association with proliferating cell nuclear antigen and Waf1(1). Cancer Res. 55:4651-4657.
60. Polyak, K., M. H. Lee, H. Erdjumentbromage, A. Koff, J. M. Roberts, P. Tempst, and J. Massague. 1994. Cloning of p27(Kip1), a cyclin-dependent kinase inhibitor and a potential mediator of extracellular antimitogenic signals. Cell 78:59-66.
61. Poon, R. Y., H. Toyoshima, and T. Hunter. 1995. Redistribution of the CDK inhibitor p27 between different cyclin. CDK complexes in the mouse fibroblast cell cycle and in cells arrested with lovastatin or ultraviolet irradiation. Mol. Biol. Cell 6:1197-1213.
62. Poon, R. Y. C., and T. Hunter. 1995. Dephosphorylation of Cdk2 Thr(160) by the cyclin-dependent kinase-interacting phosphatase KAP in the absence of cyclin. Science 270:90-93.
63. Rao, S. S., C. Chu, and D. S. Kohtz. 1994. Ectopic expression of cyclin D1 prevents activation of gene transcription by myogenic basic helix-loop-helix regulators. Mol. Cell. Biol. 14:5259-5267.
64. Rao, S. S., and D. S. Kohtz. 1995. Positive and negative regulation of D-type cyclin expression in skeletal myoblasts by basic fibroblast growth factor and transforming growth factor beta-A role for cyclin D1 in control of myoblast differentiation. J. Biol. Chem. 270:4093-4100.
65. 1-to-S transition. Mol. Cell. Biol. 15:3463-3469.
66. Sala, A., N. C. Nicolaides, A. Engelhard, T. Bellon, D. C. Lawe, A. Arnold, X. Grana, A. Giordano, and B. Calabretta. 1994. Correlation between E2F-1 requirement in the S phase and E2F-1 transactivation of cell cycle-related genes in human cells. Cancer Res. 54:1402-1406.
67. Sardet, C., M. Vidal, D. Cobrinik, Y. Geng, C. Onufryk, A. Chen, and R. A. Weinberg. 1995. E2F-4 and E2F-5, two members of the E2F family, are expressed in the early phases of the cell cycle. Proc. Natl. Acad. Sci. USA 92:2403-2407.
68. Schneider, J. W., W. Gu, L. Zhu, V. Mahdavi, and B. Nadal-Ginard. 1994. Reversal of terminal differentiation mediated by p107 in Rh(-/-) muscle cells. Science 264:1467-1471.
69. Schwarz, J. K., S. H. Devoto, E. J. Smith, S. P. Chellappan, L. Jakoi, and J. R. Nevins. 1993. Interactions of the p107 and Rb proteins with E2F during the cell proliferation response. EMBO J. 12:1013-1020.
70. Sherr, C. J. 1994. G1 phase progression: cycling on cue. Cell 79:551-555.
71. Sherr, C. J., and J. M. Roberts. 1995. Inhibitors of mammalian G(1) cyclin-dependent kinases. Genes Dev. 9:1149-1163.
72. Shin, E. K., A. Shin, C. Paulding, B. Schaffhausen, and A. S. Yee. 1995. Multiple changes in E2F function and regulation occur upon muscle differentiation. Mol. Cell. Biol. 15:2252-2262.
73. Slack, R. S., P. A. Hamel, T. S. Bladon, R. M. Gill, and M. W. Mcburney. 1993. Regulated expression of the retinoblastoma gene in differentiating embryonal carcinoma cells. Oncogene 8:1585-1591.
74. Spitkovsky, D., P. Steiner, J. Lukas, E. Lees, M. Pagano, A. Schulze, S. Joswig, D. Picard, M. Tommasino, M. Eilers, and P. Jansendurr. 1994. Modulation of cyclin gene expression by adenovirus E1A in a cell line with E1A-dependent conditional proliferation. J. Virol. 68:2206-2214.
75. Suzukitakahashi, I., M. Kitagawa, M. Saijo, H. Higashi, H. Ogino, H. Matsumoto, Y. Taya, S. Nishimura, and A. Okuyama. 1995. The interactions of E2F with pRB and with p107 are regulated via the phosphorylation of pRB and p107 by a cyclin-dependent kinase. Oncogene 10:1691-1698.
76. Tam, S. W., J. W. Shay, and M. Pagano. 1994. Differential expression and cell cycle regulation of the cyclin-dependent kinase 4 inhibitor p16(Ink4). Cancer Res. 54:5816-5820.
77. Tedesco, D., M. Caruso, L. Fischer-Fantuzzi, and C. Vesco. 1995. The inhibition of cultured myoblast differentiation by the simian virus 40 large T antigen occurs after myogenin expression and Rb up-regulation and is not exerted by transformation-competent cytoplasmic mutants. J. Virol. 69: 6947-6957.
78. Tedesco, D., L. Fischer-Fantuzzi, and C. Vesco. 1993. Limits of transforming competence of SV40 nuclear and cytoplasmic large T-mutants with altered Rb-binding sequences. Oncogene 8:549-557.
79. Toyoshima, H., and T. Hunter. 1994. p27, a novel inhibitor of G1 cyclin-Cdk protein kinase activity, is related to p21. Cell 78:67-74.
80. Vairo, G., D. M. Livingston, and D. Ginsberg. 1995. Functional interaction between E2F-4 and p130: evidence for distinct mechanisms underlying growth suppression by different retinoblastoma protein family members. Genes Dev. 9:869-881.
81. Wang, J., and B. Nadal-Ginard. 1995. Regulation of cyclins and p34CDC2 expression during terminal differentiation of C2C12 myocytes. Biochem. Biophys. Res. Commun. 206:82-88.
82. Weinberg, R. 1995. The retinoblastoma protein and cell cycle control. Cell 81:323-330.
83. Weintraub, H. 1993. The MyoD family and myogenesis - redundancy, networks, and thresholds. Cell 75:1241-1244.
84. Wright, W. E., M. Binder, and W. D. Funk. 1991. Cyclic amplification, and selection of targets (CASTing)-for the myogenin consensus binding site. Mol. Cell. Biol. 11:4104-4110.
85. Xiong, Y., G. J. Hannon, H. Zhang, D. Casso, R. Kobayashi, and D. Beach. 1993. p21 is a universal inhibitor of cyclin kinases. Nature 366:701-704.
86. Xu, M., K. A. Sheppard, C. Y. Peng, A. S. Yee, and H. Piwnicaworms. 1994. Cyclin A CDK2 hinds directly to E2F-1 and inhibits the DNA-binding activity of E2F-1/DP-1 by phosphorylation. Mol. Cell. Biol. 14:8420-8431.
87. Yaffe, D., and O. Saxel. 1977. Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 270:725-727.