Initiation of DNA synthesis by human papillomavirus E7 oncoproteins is resistant to p21-mediated inhibition of cyclin E-cdk2 activity

Journal of Virology

Volumn 71, Issue 7, 1997, Pages 5570-5578

  Ruesch, Margaret N ^a   Laimins, Laimonis A ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN E; ONCOPROTEIN; PROTEIN P21; PROTEIN P53;

ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL IMMORTALIZATION; DNA DAMAGE; DNA SYNTHESIS; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; KERATINOCYTE; PAPILLOMA VIRUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METABOLISM; TUMOR SUPPRESSOR GENE;

EID: 0030973383     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.71.7.5570-5578.1997     Document Type: Article

References (69)

1. Arroyo, M., S. Bagchi, and P. Raychaudhuri. 1993. Association of the human papillomavirus type 16 E7 protein with the S-phase-specific E2F-cyclin A complex. Mol. Cell. Biol. 13:6537-6546.
2. Ausubel, F., R. Brent, R. Kingston, D. Moore, J. Seidman, J. Smith, and K. Struhl (ed.). 1995. Current protocols in molecular biology, vol. 1. John Wiley & Sons, New York, N.Y.
3. Blanton, R., M. Coltrera, A. Gown, C. Halbert, and J. McDougall. 1992. Expression of the HPV16 E7 gene generates proliferation in stratified squamous cell cultures which is independent of endogenous p53 levels. Cell Growth Differ. 3:791-802.
4. Brokaw. J., C. Yee, and K. Hunger. 1994. A mutational analysis of the amino terminal domain of the human papillomavirus type 16 E7 oncoprotein. Virology 205:603-607.
5. Chellappan, S., S. Hiebert, M. Mudryj, J. Horowitz, and J. Nevins. 1991. The E2F transcription factor is a cellular target for the Rb protein. Cell 65:1053-1061.
6. Chellappan, S., V. Kraus, B. Kroger, K. Munger, P. Howley, W. Phelps, and J. Nevins. 1992. Adenovirus E1A, simian virus 40 tumor antigen, and human papillomavirus E7 protein share the capacity to disrupt the interaction between transcription factor E2F and the rctinoblastoma gene product. Proc. Natl. Acad. Sci. USA 89:4549-4553.
7. Chen, J., P. Jackson, M. Kirschner, and A. Dutta. 1995. Separate domains of p21 involved in the inhibition of cdk kinase and PCNA. Nature 374:386-388.
8. Cheng, S., D. Schmidt-Grimminger, T. Murant, T. Broker, and L. Chow. 1995. Differentiation-dependent up-regulation of the human papillomavirus E7 gene reactivates cellular DNA replication in suprabasal differentiated keratinocytes. Genes Dev. 9:2335-2349.
9. Davies, R., R. Hicks, T. Crook, J. Morris, and K. Vousden. 1993. Human papillomavirus type 16 E7 associates with a histone H1 kinase and with p107 through sequences necessary for transformation. J. Virol. 67:2521-2528.
10. DeGregori, J., G. Leone, K. Ohtani, A. Miron, and J. Nevins. 1995. E2F-1 accumulation bypasses a G1 arrest resulting from the inhibition of G1 cyclin-dependent kinase activity. Genes Dev. 9:2873-2887.
11. Demers, G., E. Espling, J. Harry, B. Etscheid, and D. Galloway. 1996. Abrogation of growth arrest signals by human papillomavirus type 16E7 is mediated by sequences required for transformation. J. Virol. 70:6862-6869.
12. Demers, G., S. Foster, C. Halbert, and D. Galloway. 1994. Growth arrest by induction of p53 in DNA damaged keratinocytes is bypassed by human papillomavirus 16 E7 protein. Proc. Natl. Acad. Sci. USA 91:4382-4386.
13. CIPI/WAFI underg0 normal development, but are defective in G1 check-point control. Cell 82:675-684.
14. Dimri, G., M. Nakanishsi, P. Desprez, J. Smith, and J. Campisi. 1996. Inhibition of E2F activity by the cyclin-dependent protein kinase inhibitor p21 in cells expressing or lacking a functional retinoblastoma protein. Mol. Cell. Biol. 16:2987-2997.
15. Dulic, V., W. Kaufmann, S. Wilson, T. Tlsty, E. Lees, J. W. Harper, S. Elledge, and S. Reed. 1994. p53-dependent inhibition of cyclin-dependent kinase activities in human fibroblasts during radiation-induced G1 arrest. Cell 78:1013-1023.
16. Duronio, R., A. Brook, N. Dyson, and P. O'Farrell. 1996. E2F-induced S phase requires cyclin E. Genes Dev. 10:2505-2513.
17. Dyson, N., P. Guida, K. Munger, and E. Harlow. 1992. Homologous sequences in adenovirus E1A and human papillomavirus E7 proteins mediate interaction with the same set of cellular proteins. J. Virol. 66:6893-6902.
18. Dyson, N., P. Howley, K. Munger, and E. Harlow. 1989. The human papillomavirus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science 243:934-936.
19. El-Deiry, W., T. Tokino, V. Velculescu, D. Levy, R. Parsons, J. Trent, D. Lin, W. Mercer, K. Kinzler, and B. Vogelstein. 1993. WAF1, a potential mediator of p53 tumor suppression. Cell 75:817-825.
20. Ewen, M., B. Faha, E. Harlow, and D. Livingston. 1992. Interaction of p107 with cyclin A independent of complex formation with viral oncoproteins. Science 255:85-90.
21. Foster, S., G. Demers, B. Etscheid, and D. Galloway. 1994. The ability of human papillomavirus E6 proteins to target p53 for degradation in vivo correlates with their ability to abrogate actinomycin D-induced growth arrest. J. Virol. 68:5698-5705.
22. Ginsberg, D., G. Vairo, T. Chittenden, A. Xiao, G. Xu, K. Wydner, J. DeCaprio, J. Lawrence, and D. Livingston. 1994. E2F-4, a new member of the E2F transcription factor family, interacts with p107. Genes Dev. 8:2665-2679.
23. Halbert, C., G. Demers, and D. Galloway. 1992. The E6 and E7 genes of human papillomavirus type 6 have weak immortalizing activity in human epithelial cells. J. Virol. 66:2125-2134.
24. Halbert, C., G. Demers, and D. Galloway. 1991. The E7 gene of human papillomavirus type 16 is sufficient for immortalization of human epithelial cells. J. Virol. 65:473-478.
25. Harper, J., G. Adami, N. Wei, K. Keyomarsi, and S. Elledge. 1993. The p21 cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 75:805-816.
26. Heck, D., C. Yee, P. Howley, and K. Munger. 1992. Efficiency of binding the retinoblastoma protein correlates with the transforming capacity of the E7 oncoproteins of the human papillomaviruses. Proc. Natl. Acad. Sci. USA 89:4442-4446.
27. Hickman, E., S. Picksley, and K. Vousden. 1994. Cells expressing HPV16 E7 continue cell cycle progression following DNA damage induced p53 activation. Oncogene 9:2177-2181.
28. Hiebert, S., S. Chellappan, J. Horowitz, and J. Nevins. 1992. The interaction of Rb with E2F coincides with an inhibition of the transcriptional activity of E2F. Genes Dev. 6:177-185.
29. Howley, P. M. 1991. Papillomavirinae and their replication, vol. 2. Raven Press, New York, N.Y.
30. Ikeda, M., L. Jakoi, and J. Nevins. 1996. A unique role for the Rb protein in controlling E2F accumulation during cell growth and differentiation. Proc. Natl. Acad. Sci. USA 93:3215-3220.
31. Johnson, D., J. Schwarz, W. Cress, and J. Nevins. 1993. Expression of transcription factor E2F1 induces quiescent cells to enter S phase. Nature 365:349-352.
32. Kessis, T., R. Slebos, W. Nelson, M. Kastan, B. Plunkett, S. Han, A. Lorincz, L. Hedrick, and K. Cho. 1993. Human papillomavirus 16 E6 disrupts the p53-mediated cellular response to DNA damage. Proc. Natl. Acad. Sci. USA 90:3988-3992.
33. Koff, A., F. Cross, A. Fisher, J. Schumacher, K. Leguellec, M. Philippe, and J. Roberts. 1991. Human cyclin E, a new cyclin that interacts with two members of the cdc2 gene family. Cell 66:1217-1228.
34. Laimins, L. 1993. The biology of human papillomaviruses: from warts to cancer. Infect. Agents Dis. 2:74-86.
35. LaThangue, N. 1994. DRTF1/E2F: an expanding family of heterodimeric transcription factor implicated in cell cycle control. Trends Biochem. Sci. 19:108-114.
36. Lees, E., B. Faha, V. Dulic, S. 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.
37. Li, Y., C. Graham, S. Lacy, A. Duncan, and P. Whyte. 1993. The adenovirus E1A-associated 130-kD protein is encoded by a member of the retinoblastoma gene family and physically interacts with cyclins A and E. Genes Dev. 7:2366-2377.
38. Lowy, D., R. Kernbauer, and J. Schiller. 1994. Genital human papillomavirus infection. Proc. Natl. Acad. Sci. USA 91:2436-2440.
39. McIntyre, M., M. Frattini, S. Grossman, and L. Laimins. 1993. Human papillomavirus type 18 E7 protein requires intact Cys-X-X-Cys motifs for zinc binding, dimerization, and transformation but not for Rb binding. J. Virol. 67:3142-3150.
40. McIntyre, M., M. Ruesch, and L. Laimins. 1996. Human papillomavirus E7 oncoproteins bind a single form of cyclin E in a complex with cdk2 and p107. Virology 215:73-82.
41. Meyers, C., M. Frattini, J. Hudson, and L. Laimins. 1992. Biosynthesis of human papillomavirus from a continuous cell line upon epithelial differentiation. Science 257:971-973.
42. Missero, C., E. Calautti, R. Eckner, J. Chin, L. Tsai, D. Livingston, and G. 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.
43. Moberg, K., M. Starz, and J. Lees. 1996. E2F-4 switches from p130 to p107 and pRb in response to cell cycle reentry. Mol. Cell. Biol. 16:1436-1449.
44. Munger, K., B. Werness, N. Dyson, W. Phelps, E. Harlow, and P. Howley. 1989. Complex formation of human papillomavirus E7 proteins with the retinoblastoma tumor suppressor gene product. EMBO J. 8:4099-4105.
45. Munger, K., C. Yee, W. Phelps, J. Peitenpol, H. Moses, and P. Howley. 1991. Biochemical and biological differences between E7 oncoproteins of the high-and low-risk human papillomavirus types are determined by amino-terminal sequences. J. Virol. 65:3943-3948.
46. sdi1/CIP1/WAF1. EMBO J 14:555-563.
47. Ohtani, K., J. DeGregori, and J. Nevins. 1995. Regulation of the cyclin E gene by transcription factor E2F1. Proc. Natl. Acad. Sci. USA 92:12146-12150.
48. CIP1 in muscle and other terminally differentiating cells. Science 267:1024-1027.
49. Peeper, D., A. van der Eb, and A. Zantema. 1994. The G1/S cell-cycle checkpoint in eukaryotic cells. Biochim. Biophys. Acta 1198:215-230.
50. Phelps, W., K. Munger, C. Yee, J. Barnes, and P. Howley. 1992. Structure-function analysis of the human papillomavirus type 16 E7 oncoprotein. J. Virol. 66:2418-2427.
51. Potter, H. 1996. Transfection of DNA into eukaryotic cells, vol. 1.1. John Wiley and Sons, Inc., New York, N.Y.
52. Qin, X., D. Livingston, W. Kaelin, and P. 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.
53. 52a. Ruesch, M. N., and L. A. Laimins. Unpublished data.
54. Sardet, C., M. Vidal, D. Cobrinik, Y. Geng, C. Onufryk, A. Chen, and R. 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.
55. Scheffner, M., B. Werness, J. Huibregtse, A. Levine, and P. Howley. 1990. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 63:1129-1136.
56. Sherr, C. 1994. G1 phase progression: cycling on cue. Cell 79:551-555.
57. Slebos, R., M. Lee, B. Plunkett, T. Kessis, B. Williams, T. Jacks, L. Hedrick, M. Kastan, and K. Cho. 1994. p53-dependent G1 arrest involves pRB-related proteins and is disrupted by the human papillomavirus 16 E7 oncoprotein. Proc. Natl. Acad. Sci. USA 91:5320-5324.
58. 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.
59. Vairo, G., D. 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.
60. Vousden, K. 1994. Interactions between papillomavirus proteins and tumor suppressor gene products. Adv. Cancer Res. 64:1-24.
61. Watanabe, S., T. Kanda, H. Sato, A. Furuno, and K. Yoshike. 1990. Mutational analysis of human papillomavirus type 16 E7 functions. J. Virol. 64:207-214.
62. Weinberg, R. 1995. The retinoblastoma protein and cell cycle control. Cell 81:323-330.
63. Weintraub, S., C. Prater, and D. Dean. 1992. Retinoblastoma protein switches the E2F site from positive to negative element. Nature 358:259-261.
64. Werness, B., A. Levine, and P. Howley. 1990. Association of human papillomavirus types 16 and 18 E6 proteins with p53. Science 248:76.
65. Wu, C.-L., L. Zukerberg, C. Ngwu, E. Harlow, and J. Lees. 1995. In vivo association of E2F and DP family proteins. Mol. Cell. Biol. 15:2536-2546.
66. Wu, X., and A. Levine. 1994. p53 and E2F-1 cooperate to mediate apoptosis. Proc. Natl. Acad. Sci. USA 91:3602-3606.
67. Zhang, H., G. Hannon, and D. Beach. 1994. p21-containing cyclin kinases exist in both active and inactive states. Genes Dev. 8:1750-1758.
68. CIP1-related domain to bind cyclin/cdk2 and regulate interactions with E2F. Genes Dev. 9:1740-1752.
69. zur Hausen, A., and E. de Villiers. 1994. Human papillomaviruses. Annu. Rev. Microbiol. 48:427-447.