The retinoblastoma gene product protects E2F-1 from degradation by the ubiquitin-proteasome pathway

Genes and Development

Volumn 10, Issue 23, 1996, Pages 2949-2959

  Hofmann, Francesco ^a   Martelli, Fabio ^a   Livingston, David M ^a   Wang, Zhiyan ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

cell cycle control; E2F; pRb; protein degradation; ubiquitin proteasome

Indexed keywords

GENE PRODUCT; PROTEASOME; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR; UBIQUITIN;

ANIMAL CELL; ARTICLE; CARCINOMA CELL; CELL CYCLE; COMPLEX FORMATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; REGULATORY MECHANISM;

ANIMALIA; MAMMALIA;

EID: 0029820095     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.10.23.2949     Document Type: Article

References (70)

1. Adnane, J., Z. Shao, and P.D. Robbins. 1995. The retinoblastoma susceptibility gene product represses transcription when directly bound to the promoter. J. Biol. Chem. 270: 8837-8843.
2. Amon, A., S. Irniger, and K. Nasmyth. 1994. Closing the cell cycle circle in yeast: G2 cyclin proteolysis initiated at mitosis persists until the activation of G1 cyclins in the next cycle. Cell 77: 1037-1050.
3. Asano, M., J.R. Nevins, and R.P. Wharton. 1996. Ectopic E2F expression induces S-phase and apoptosis in Drosophila imaginal discs. Genes & Dev. 10: 1422-1432.
4. Botz, J., K. Zerfass-Thome, D. Spitkovsky, H. Delius, B. Vogt, M. Eilers, A. Hatzigeorgiou, and P. Jansen-Dürr. 1996. Cell cycle regulation of the murine cyclin E gene depends on an E2F binding site in the promoter. Mol. Cell. Biol. 16: 3401-3409.
5. Bremner, R., B.L. Cohen, M. Sopta, P.A. Hamel, C.J. Ingles, B.L. Gallie, and R.A. Phillips. 1995. Direct transcriptional repression by pRb and its reversal by specific cyclins. Mol. Cell Biol. 15: 3256-3265.
6. Caruso M., F. Martelli, A. Giordano, and A. Felsani. 1993. Regulation of MyoD gene transcription and protein function by the transforming domains of the adeno virus E1A oncoprotein. Oncogene 8: 267-278.
7. Chen, C. and H. Okayama. 1987. High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 7: 2745-2752.
8. Ciechanover, A. 1994. The ubiquitin-proteasome proteolytic pathway. Cell 79: 13-21.
9. Clurman, B.E., R.J. Sheaff, K. Thress, M. Groudine and J.M. Roberts. 1996. Turnover of cyclin E by the ubiquitin-proteasome pathway is regulated by cdk2 binding and cyclin phosphorylation. Genes & Dev. 10: 1979-1990.
10. Cress, W.D., D.G. Johnson, and J.R. Nevins. 1993. A genetic analysis of the E2F-1 gene distinguishes regulation by pRb, p!07 and adenovirus E4. Mol. Cell. Biol. 13: 6314-6325.
11. De Gregori J., T. Kowalik, and J.R. Nevins. 1995. Cellular targets for activation by the E2F-1 transcription factor include DNA Synthesis- and G1/S-regulatory genes. Mol. Cell. Biol. 15: 4215-4224.
12. 1 cyclin Cln2p by a Cdc34p-dependent pathway. EMBO J. 14: 303-312.
13. 1 to S transition in Drosophila: Cyclin E is a limiting downstream target of E2F. Genes & Dev. 9: 1456-1468.
14. Ewen, M.E., H.K. Sluss, C.J. Sherr, H. Matsushime, J. Kato, and D.M. Livingston. 1993. Functional interactions of the retinoblastoma protein with mammalian D-type cyclins. Cell 73: 487-497.
15. Field, S.J., F.-Y. Tsai, F. Kuo, A.M. Zubiaga, W.G. Kaelin, D.M. Livingston, S.H. Orkin, and M.E. Greenberg. 1996. E2F-1 functions in mice to promote apoptosis and suppress proliferation. Cell 85: 549-561.
16. Flemington, E.K., S.H. Speck, and W.G. Kaelin. 1993. E2F-1-mediated transactivation is inhibited by complex formation with the retinoblastoma susceptibility gene product. Proc. Natl. Acad. Sci. 90: 6914-6918.
17. Geng, Y., 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
18. Ginsberg, D., G. Vairo, T. Chittenden, Z.-X. Xiao, G. Xu, K.L. Wydmer, 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.
19. Glotzer, M., A.W. Murray, and M.W. Kirschner. 1991. Cyclin is degraded by the ubiquitin pathway. Nature 349: 132-138.
20. Hamel, P.A., B.L. Cohen, L.M. Sorce, B.L. Gallie, and R.A. Phillips. 1990. Hyperphosphorylation of the retinoblastoma gene product is determined by domains outside the Simian virus 40 large T antigen-binding region. Mol. Cell Biol. 10: 6586-6595.
21. 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.
22. Herrera, R., V.P. Sah, B.O. Williams, T.P. Mäkelä, R.A. Weinberg, and T. Jacks. 1996. Altered cell cycle kinetics, gene expression, and G1 restriction point regulation in Rb-deficient fibroblast. Mol. Cell. Biol. 16: 2402-2407.
23. 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 p 130 in vivo. Mol. Cell. Biol. 15: 3082-3089.
24. Hochstrasser, M. 1995. Ubiquitin, proteasomes, and the regulation of intracellular protein degradation. Curr. Opin. Cell Biol. 7: 215-223.
25. 1 exit. Genes & Dev. 10: 851-861.
26. Hsiao, K.-M., S.L. McMahon, and P.J. Farnham. 1994. Multiple DNA elements are required for the growth regulation of the mouse E2F-1 promoter. Genes & Dev. 8: 1526-1537.
27. Johnson, D.G., J.K. Schwarz, W.D. Cress, and J.R. Nevins. 1993. Expression of E2F-1 induces quiescent cells to enter S-phase. Nature 365: 349-352.
28. Johnson, D.G., W. Cress, L. Jakoi, and J.R. Nevins. 1994a. Oncogenic capacity of the E2F-1 gene. Proc. Natl. Acad. Sci. 91: 12823-12827.
29. Johnson, D.G., K. Ohtani, and J.R. Nevins. 1994b. Autoregulatory control of E2F-1 expression in response to positive and negative regulators of cell cycle progression. Genes & Dev. 8: 1514-1525.
30. Kaelin, W.G. Jr., 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.
31. 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.
32. Krek, W., G. Xu, and D.M. Livingston. 1995. Cyclin A kinase regulation of E2F-1 DNA binding function underlies suppression of an S phase checkpoint. Cell 83: 1149-1158.
33. Lam, E.W.-F. and N.B. La Thangue. 1994. DP and E2F proteins: Coordinating transcription with cell cycle progression. Curr. Opin. Cell Biol. 6: 859-866.
34. Lam, E.W.-F. and R.J. Watson. 1993. An E2F-bindmg site mediates cell cycle regulated repression of mouse b-myb transcription. EMBO J. 12: 2705-2752.
35. Lanker, S., M.H. Valdivieso, and C. Wittenberg. 1996. Rapid degradation of the G1 cyclin Cln2 induced by cdk-dependent phosphorylation. Science 271: 1597-1600.
36. 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.
37. Nefsky, B. and D. Beach. 1996. Publ acts as an E6-AP-like protein ubiquitin ligase in the degradation of cdc25. EMBO J. 15: 1301-1312.
38. 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.
39. Nevins, J.R. 1992. A link between the Rb tumor suppressor protein and viral oncoproteins. Science 258: 424-429.
40. Nurse, P. 1994. Ordering S phase and M phase in the cell cycle. Cell 79: 547-550.
41. Ohtani, K., J. De Gregori, and J.R. Nevins. 1995. Regulation of the cyclin E gene by transcription factor E2F-1. Proc. Natl. Acad. Sci. 92: 12146-12150.
42. Ormondroyd, E., S. de la Luna, and N.B. La Thangue. 1995. A new member of the DP family, DP-3, with distinct protein products suggests a regulatory role for alternative splicing in the cell cycle transcription factor DRTF1/E2F. Oncogene 11: 1437-1446
43. Otterson, G.A., S.N. Khleif, W. Chen, A. Coxon, and F.J. Kaye. 1995. CDK2N gene silencing in lung cancer by DNA hypermethylation and kinetics of p16INK4 protein induction by 5-aza-2′-deoxycytidine. Oncogene 11: 1211-1216.
44. Pagano, M., S.W. Tam, A.M. Theodoras, P. Beer-Romero, G. Dal Sal, V. Chau, P.R. Yew, G.F. Draetta, and M. Rolfe. 1995. Role of the Ubiquitin-proteosome pathway in regulating abundance of the cyclin-dependent kinase inhibitor p27. Science 269: 682-685.
45. Porcu, P., X. Grana, S. Li, J. Swantek, A. De Luca, A. Giordano, and R. Baserga. 1994. An E2F binding sequence negatively regulates the response of the insulin-like growth factor 1 (IGF-I) promoter to simian virus 40 T antigen and to serum. Oncogene 9: 2125-2134.
46. Qin, X.Q., D.M. Livingston, W.G. Kaelin, and P. Adams. 1994. Deregulated E2F-1 expression leads to S-phase entry and p53-mediated apoptosis. Proc. Natl. Acad. Sci. 91: 10918-10922.
47. Qin, X.Q., D.M. Livingston, D.M. Ewen, W.R. Sellers, Z. Arany, and W.G. Kaelin. 1995. The transcription factor E2F-1 is a downstream target of RB action. Mol. Cell. Biol. 15: 742-755.
48. Rock, K.L., C. Gramm, L. Rothstein, K. Clark, R. Stein, L. Dick, D. Hwang, and A.L. Goldberg. 1994. Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell 78: 761-777.
49. 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 phase of the cell cycle. Proc. Natl. Acad. Sci. 92: 2403-2407.
50. Scheffner, M., J.M. Huigregste, R.D. Vierstra, and P.M. Howley. 1993. The HPV E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell 75: 495-505.
51. Scheffner, M., U. Nuber, and J.M. Huibregste. 1995. Protein ubiquitination involving an E1-E2-E3 enzyme ubiquitin thioester cascade. Nature 373: 81-83.
52. Schulze, A., K. Zerfass, D. Spitovsky, J. Berges, S. Middendrop, P.Jansen-Dürr, and B. Henglein. 1995. Cell cycle regulation of cyclin A gene transcription by a variant E2F binding site. Proc. Natl. Acad. Sci. 92: 11264-11268.
53. 1 to S transition in S. cerevisiae. Cell 79: 233-244.
54. Sellers, W.R., J.W. Rodgers, and W.G. Kaelin. 1995. A potent transrepression domain in the retinoblastoma protein induces a cell cycle arrest when bound to E2F sites. Proc. Natl. Acad. Sci. 92: 11544-11548.
55. Seufert, W., B. Futcher, and S. Jentsch. 1995. A ubiquitin-conjugating enzyme involved in the degradation of both S- and M-phase cyclins. Nature 373: 78-81.
56. Singh, P., S. Wong, and W. Hong. 1994. Overexpression of E2F-1 in rat embryo fibroblasts leads to neoplastic transformation. EMBO J. 13: 3329-3338.
57. Shan, B. and W.-H. Lee. 1994. Deregulated expression of E2F-1 induces S-phase entry and leads to apoptosis. Mol. Cell. Biol. 14: 8166-8173.
58. 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. 13: 5620-5631.
59. 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.
60. Ward, C.L., S. Omura, and R.R. Kopito. 1995. Degradation of CFTR by the ubiquitin-proteasome pathway. Cell 83: 121-127.
61. Weinberg, R.A. 1995. The retinoblastoma protein and cell cycle control. Cell 81: 323-330.
62. Weinberg, R.A. 1996. E2F and cell proliferation: A world turned upside down. Cell 85: 457-459.
63. Weintraub, S.J., C.A. Prater, and D.C. Dean. 1992. Retinoblastoma protein switches the E2F site from positive to negative element. Nature 358: 259-261.
64. Weintraub, S.J., K.N.B. Chow, R.X. Luo, S. Zhang, S. He, and D.C. Dean. 1995. Mechanisms of active transcriptional repression by the retinoblastoma protein. Nature 375: 812-815.
65. Won, K.-A. and S.I. Reed. 1996. Activation of cyclin E/cdk2 is coupled to site-specific autophosphorylation and ubiquitin-dependent degradation of cyclin E. EMBO J. 15: 4182-4193.
66. Wu, X. and A.J. Levine. 1994. p53 and E2F-1 cooperate to mediate apoptosis. Proc. Natl. Acad. Sci. 91: 3602-3606.
67. Wuarin, J. and P. Nurse. 1996. Regulating S-phase: CDKs, licensing and proteolysis. Cell 85: 785-787.
68. Xu, G., D.M. Livingston, and W. Krek. 1995. Multiple members of the E2F transcription factor family are the products of oncogenes. Proc. Natl. Acad. Sci. 92: 1357-1361.
69. cdc28-mediated control of Cln3 cyclin degradation. Mol. Cell. Biol. 15: 731-741.
70. Yamasaki, L., T. Jacks, R. Bromson, E. Goillot, E. Harlow, and N.J. Dyson. 1996. Tumor induction and tissue atrophy in mice lacking E2F-1. Cell 85: 537-548.