Inhibition of E2F activity by the cyclin-dependent protein kinase inhibitor p21 in cells expressing or lacking a functional retinoblastoma protein

Molecular and Cellular Biology

Volumn 16, Issue 6, 1996, Pages 2987-2997

  Dimri, Goberdhan P ^a   Nakanishi, Makoto ^b   Desprez, Pierre Yves ^a   Smith, James R ^b   Campisi, Judith ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE; PROTEIN P21; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR E2F;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL PROLIFERATION; DNA BINDING; DNA REPLICATION; DNA SYNTHESIS; GENETIC TRANSCRIPTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PHOSPHORYLATION; SIMIAN VIRUS 40; TRANSACTIVATION;

ANIMALIA; SIMIAE; SIMIAN VIRUS; SIMIAN VIRUS 40;

EID: 0030003153     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.16.6.2987     Document Type: Article

References (76)

1. Beijersbergen, R. L., L. Carlee, R. M. Kerkhoven, and R. Bernards. 1995. Regulation of the retinoblastoma protein-related p107 by G1 cyclin complexes. Genes Dev. 9:1340-1353.
2. Beijersbergen, R. L., R. M. Kerkhoven, L. Zhu, L. Carlee, P. M. Voorhoeve, and R. Bernards. 1994. E2F-4, a new member of the E2F gene family, has oncogenic activity and associates with p107 in vivo. Genes Dev. 8:2680-2690.
3. Buchkovich, K., L. A. Duffy, and E. Harlow. 1989. The retinoblastoma protein is phosphorylated during specific phases of the cell cycle. Cell 58:1097-1105.
4. Chellappan, S. P., S. Hiebert, M. Mudryj, J. M. Horowitz, and J. R. Nevins. 1991. The E2F transcription factor is a cellular target for the RB protein. Cell 65:1053-1061.
5. Chen, P. L., P. Scully, J. Y. Shew, J. Y. Wang, and W. H. Lee. 1989. Phosphorylation of the retinoblastoma gene product is modulated during the cell cycle and cellular differentiation. Cell 58:1193-1198.
6. 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.
7. Dalton, S. 1992. Cell cycle regulation of the human cdc2 gene. EMBO J. 11:1797-1804.
8. Datto, M. B., Y. Li, J. F. Panus, D. J. Howe, Y. Xiong, and X. F. Wang. 1995. Transforming growth factor beta induces the cyclin-dependent kinase inhibitor p21 through a p53-independent mechanism. Proc. Natl. Acad. Sci. USA 92:5545-5549.
9. DeCaprio, J., J. W. Ludlow, J. Figge, J. Y. Shew, C. M. Huang, W. H. Lee, E. Marsilio, E. Paucha, and D. M. Livingston. 1988. SV40 large tumor antigen forms a specific complex with the product of the retinoblastoma susceptibility gene. Cell 54:275-283.
10. 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.
11. 1/S-regulatory genes. Mol. Cell. Biol. 15:4215-4224.
12. Desprez, P. Y., C. Roskelley, J. Campisi, and M. J. Bissell. 1993. Isolation of functional cell lines from a mouse mammary epithelial cell strain: the importance of basement membrane and cell-cell interaction. Mol. Cell. Differ. 1:99-110.
13. Dignam, J. D., R. M. Lebovitz, and R. G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475-1489.
14. Dimri, G. P., and J. Campisi. 1994. Altered profile of transcription factor binding activities in senescent human fibroblasts. Exp. Cell Res. 212:132-140.
15. Dimri, G. P., and J. Campisi. 1994. Molecular and cell biology of replicative senescence. Cold Spring Harbor Symp. Quant. Biol. 59:67-73.
16. Dimri, G. P., E. Kara, and J. Campisi. 1994. Regulation of two E2F-related genes in presenescent and senescent human fibroblasts. J. Biol. Chem. 269: 16180-16186.
17. Draetta, G. F. 1994. Mammalian G1 cyclins. Curr. Opin. Cell Biol. 6:842-847.
18. 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.
19. El-Deiry, W. S., T. Tokino, V. E. Velculescu, D. B. Levy, R. Parsons, J. M. Trent, D. Lin, W. E. Mercer, K. W. Kinzler, and B. Vogelstein. 1993. WAF1, a potential mediator of p53 tumor suppression. Cell 75:817-825.
20. Ewen, M. E., J. W. Ludlow, E. Marsilio, J. A. DeCaprio, R. C. Milikan, S. H. Cheng, E. Paucha, and D. M. Livingston. 1989. An N-terminal transformation-governing sequence of SV40 large T antigen contributes to the binding of both p110Rb and a second cellular protein, p120. Cell 58:257-267.
21. Fanning, E., and R. Knippers. 1992. Structure and function of simian virus 40 large tumor antigen. Annu. Rev. Biochem. 61:55-85.
22. Farnham, P. J., J. E. Slansky, and R. Kollmar. 1993. The role of E2F in the mammalian cell cycle. Biochim. Biophys. Acta 1155:125-131.
23. Flores-Rozas, H., Z. Kelman, F. B. Dean, Z. Pan, J. W. Harper, S. J. Elledge, M. O'Donnell, and J. Hurwitz. 1994. Cdk-interacting protein 1 directly binds with proliferating cell nuclear antigen and inhibits DNA replication catalyzed by the DNA polymerase holoenzyme. Proc. Natl. Acad. Sci. USA 91:8655-8659.
24. Ginsberg, D., G. Vairo, T. Chittenden, Z. X. Xiao, G. Xu, K. L. Wydner, J. A. DeCaprio, J. B. Lawrence, and D. M. Livingston. 1994. E2F-4, a new member of the E2F transcription factor family, interacts with p107. Genes Dev. 8:2665-2679.
25. 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.
26. Gu, Y., C. W. Turek, and D. O. Morgan. 1993. Inhibition of CDK2 activity in vivo by an associated 20 K regulatory subunit. Nature (London) 366:707-710.
27. Hara, E., J. A. Uzman, G. P. Dimri, J. O. Nehlin, A. Testori, and J. Campisi. 1996. The helix-loop-helix protein Id-1 and a retinoblastoma protein binding mutant of SV40 T antigen synergize to reactivate DNA synthesis in senescent human fibroblasts. Dev. Genet. 18:161-172.
28. Harper, J. W., G. R. Adami, N. Wei, K. Keyomarsi, and S. J. Elledge. 1993. The p21 CDK-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 75:805-816.
29. Harper, J. W., S. J. Elledge, K. Keyomarsi, B. Dynlacht, L. H. Tsai, P. Zhang, S. Dobrowolski, C. Bai, L. Connell-Crowley, E. Swindell, M. P. Fox, and N. Wei. 1995. Inhibition of cyclin-dependent kinases by p21. Mol. Biol. Cell 6:387-400.
30. Helin, K., J. A. Lees, M. Vidal, N. Dyson, E. Harlow, and A. Fattaey. 1992. A cDNA encoding a pRB binding protein with properties of the transcription factor E2F. Cell 70:337-350.
31. Hijmans, E. M., P. M. Voorhoeve, R. L. Beijersbergen, L. J. van't Veer, and R. Bernards. 1995. E2F-5, a new E2F family member that interacts with p130 in vivo. Mol. Cell. Biol. 15:3082-3089.
32. Hollingsworth, R. E., P.-L. Chen, and W.-H. Lee. 1993. Integration of cell cycle control with transcriptional regulation by the retinoblastoma protein. Curr. Opin. Cell Biol. 5:194-200.
33. Ivey-Hoyle, M., R. Conroy, H. E. Huber, P. J. Goodhart, A. Oliff, and D. C. Heimbrook. 1993. Cloning and characterization of E2F-2, a novel protein with the biochemical properties of transcription factor E2F. Mol. Cell. Biol. 13:7802-7812.
34. Jackson, P. K., S. Chevalier, M. Philippe, and M. W. Kirschner. 1995. Early events in DNA replication require cyclin E and are blocked by p21. J. Cell Biol. 130:755-769.
35. Johnson, D. G., K. Ohtani, and J. R. Nevins. 1994. Autoregulatory control of E2F1 expression in response to positive and negative regulators of cell cycle progression. Genes Dev. 8:1514-1525.
36. Johnson, D. G., J. K. Schwarz, W. D. Cress, and J. R. Nevins. 1993. Expression of transcription factor E2F induces quiescent cells to enter S phase. Nature (London) 365:349-352.
37. Kaelin, W. G., W. Krek, W. R. Sellers, J. A. DeCaprio, F. Ajchenbaum, C. S. Fuchs, T. Chittenden, Y. Li, P. J. Farnham, M. A. Blanar, D. M. Livingston, and E. K. Flemington. 1992. Expression cloning of a cDNA encoding a retinoblastoma binding protein with E2F-like properties. Cell 70:351-364.
38. Kierstead, T. D., and M. J. Tevethia. 1993. Association of p53 binding and immortalization of primary C57BL/6 mouse embryo fibroblasts by using simian virus 40 T-antigen mutants bearing internal overlapping deletion mutations. J. Virol. 67:1817-1829.
39. Kowalik, T. F., J. DeGregori, J. K. Schwarz, and J. R. Nevins. 1995. E2F-1 overexpression in quiescent fibroblasts leads to induction of cellular DNA synthesis and apoptosis. J. Virol. 69:2491-2500.
40. 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.
41. La Thangue, N. B. 1994. DP and E2F proteins: components of a heterodimeric transcription factor implicated in cell cycle control. Curr. Opin. Cell Biol. 6:443-450.
42. Lees, J. A., M. Saito, M. Vidal, M. Valentine, T. Look, E. Harlow, N. Dyson, and K. Helin. 1993. The retinoblastoma protein binds to a family of E2F transcription factors. Mol. Cell. Biol. 13:7813-7825.
43. Lim, K., and C. B. Chae. 1989. A simple assay for DNA transfection by incubation of the cells in culture dishes with substrates for beta-galactosidase. BioTechniques 7:576-579.
44. Lu, K., R. A. Levine, and J. Campisi. 1989. c-ras-Ha gene expression is regulated by insulin or insulinlike growth factor and by epidermal growth factor in murine fibroblasts. Mol. Cell. Biol. 9:3411-3417.
45. Meyerson, M., G. H. Enders, C. Wu, L. Su, C. Gorka, C. Nelson, E. Harlow, and L. Tsai. 1992. A family of human cdc2-related protein kinases. EMBO J. 11:2909-2917.
46. Mihara, K., X. R. Cao, A. Yen, S. Chandler, B. Driscoll, A. L. Murphree, A. T'Ang, and Y. K. T. Fung. 1989. Cell cycle dependent regulation of phosphorylation of the human retinoblastoma gene product. Science 246:1300-1303.
47. Morgan, D. O. 1994. Principles of CDK regulation. Nature (London) 374: 131-134.
48. Nakanishi, M., G. R. Adami, R. S. Robetorye, A. Noda, S. F. Venable, D. Dimitrov, O. M. Pereira-Smith, and J. R. Smith. 1995. Exit from G0 and entry into the cell cycle of cells expressing p21/sdi1 antisense RNA. Proc. Natl. Acad. Sci. USA 92:4352-4356.
49. Sdi1/CIP1/WAF1. EMBO J. 14:555-563.
50. Neuman, E., E. K. Flemington, W. R. Sellers, and W. G. Kaelin. 1994. Transcription of the E2F-1 gene is rendered cell cycle dependent by E2F DNA-binding sites within its promoter. Mol. Cell. Biol. 14:6607-6615.
51. Nevins, J. R. 1994. Cell cycle targets of the DNA tumor viruses. Curr. Opin. Genet. Dev. 4:130-134.
52. Noda, A., Y. Ning, S. F. Venable, O. M. Pereira-Smith, and J. R. Smith. 1994. Cloning of senescent cell-derived inhibitors of DNA synthesis using an expression screen. Exp. Cell Res. 211:90-98.
53. Ohtsubo, M., and J. M. Roberts. 1993. Cyclin-dependent regulation of G1 in mammalian cells. Science 259:1908-1912.
54. Pardee, A. B. 1989. G1 events and regulation of cell proliferation. Science 246:603-608.
55. Pines, J. 1994. The cell cycle kinases. Semin. Cell Biol. 5:305-313.
56. Qin, X.-Q., D. M. Livingston, M. Ewen, W. R. Sellers, Z. Arany, and W. G. Kaelin, Jr. 1995. The transcription factor E2F-1 is a downstream target of RB action. Mol. Cell. Biol. 15:742-755.
57. Qin, X. Q., D. M. Livingston, W. G. Kaelin, and P. D. Adams. 1994. Deregulated transcription factor E2F-1 expression leads to S-phase entry and p53-mediated apoptosis. Proc. Natl. Acad. Sci. USA 91:10918-10922.
58. 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.
59. Seshadri, T., and J. Campisi. 1990. c-fos repression and an altered genetic program in senescent human fibroblasts. Science 247:205-209.
60. Schwarz, J. K., C. H. Bassing, I. Kovesdi, M. B. Datto, M. Blazing, S. George, X. F. Wang, and J. R. Nevins. 1995. Expression of the E2F1 transcription factor overcomes type beta transforming growth factor-mediated growth suppression. Proc. Natl. Acad. Sci. USA 92:483-487.
61. 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 proliferative response. EMBO J. 12:1013-1020.
62. Shan, B., X. Zhu, P. L. Chen, T. Durfee, Y. Yang, D. Sharp, and W. H. Lee. 1992. Molecular cloning of cellular genes encoding retinoblastoma-associated proteins: identification of a gene with properties of the transcription factor E2F. Mol. Cell. Biol. 12:5620-5631.
63. Sheng, M., S. T. Dougan, G. McFadden, and M. E. Greenberg. 1988. Calcium and growth factor pathways of c-fos transcriptional activation require distinct upstream regulatory sequences. Mol. Cell. Biol. 8:2787-2796.
64. Sherr, C. J. 1994. G1 phase progression: cycling on cue. Cell 79:551-555.
65. Sherr, C. J., and J. M. Roberts. 1995. Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev. 9:1149-1163.
66. Slansky, J. E., Y. Li, W. G. Kaelin, and P. J. Farnham. 1993. A protein synthesis dependent increase in E2F-1 mRNA correlates with growth regulation of the dihydrofolate reductase promoter. Mol. Cell. Biol. 13:1610-1618.
67. Smith, D. B., and K. S. Johnson. 1988. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene 67:31-40.
68. Stein, G. H., M. Beeson, and L. Gordon. 1990. Failure to phosphorylate the retinoblastoma gene product in senescent human fibroblasts. Science 249: 666-669.
69. Takahashi, R., T. Hashimoto, H. J. Xu, T. Matsui, T. Miki, H. Bigo-Marshall, S. A. Aaronson, and W. F. Benedict. 1991. The retinoblastoma gene functions as a growth and tumor suppressor in human bladder carcinoma cells. Proc. Natl. Acad. Sci. USA 88:5257-5261.
70. 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.
71. Wade, M., T. F. Kowalik, M. Mudryj, E. S. Huang, and J. C. Azizkhan. 1992. E2F mediates dihydrofolate reductase promoter activation and multiprotein complex formation in human cytomegalovirus infection. Mol. Cell. Biol. 12:4364-4374.
72. Waga, S., G. J. Hannon, D. Beach, and B. Slillman. 1994. The p21 inhibitor of cyclin-dependent kinases controls DNA replication by interaction with PCNA. Nature (London) 366:701-704.
73. Weinberg, R. A. 1995. The retinoblastoma protein and cell cycle control. Cell 81:323-330.
74. Weintraub, S. J., C. A. Prater, and D. C. Dean. 1992. Retinoblastoma protein switches the E2F site from positive to negative element. Nature (London) 358:259-261.
75. Xiong, Y., G. Hannon, H. Zhang, D. Casso, R. Kobayashi, and D. Beach. 1993. p21 is a universal inhibitor of cyclin kinases. Nature (London) 366: 701-704.
76. Zhu, L., E. Harlow, and B. D. Dynlacht. 1995. p107 uses a p21/Cip1-related domain to bind cyclin/cdk2 and regulate interactions with E2F. Genes Dev. 9:1740-1752.