Disruption of the G1/S transition in human papillomavirus type 16 E7- expressing human cells is associated with altered regulation of cyclin E

Journal of Virology

Volumn 72, Issue 2, 1998, Pages 975-985

  Martin, Larry G ^a   William Demers, G ^a,b   Galloway, Denise A ^a  

^a Fred Hutchinson Cancer Research Center   (United States)

^b MERCK RESEARCH LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN E; ONCOGENE PROTEIN E7, HUMAN PAPILLOMAVIRUS TYPE 16; ONCOPROTEIN;

ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; VIRUS CELL INTERACTION; VIRUS REPLICATION; WART VIRUS; BIOSYNTHESIS; CELL CULTURE; EPITHELIUM CELL; FIBROBLAST; GENE EXPRESSION REGULATION; GENETICS; PAPILLOMA VIRUS; PATHOLOGY; VIROLOGY;

CELLS, CULTURED; CYCLIN E; EPITHELIAL CELLS; FIBROBLASTS; G1 PHASE; GENE EXPRESSION REGULATION, VIRAL; HUMANS; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRIDAE; S PHASE;

EID: 0031594586     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.72.2.975-985.1998     Document Type: Article

References (74)

1. Banks, L. M., C. Edmonds, and K. H. Vousden. 1990. Ability of the HPV16 E7 protein to bind RB and induce DNA synthesis is not sufficient for efficient transforming activity in NIH3T3 cells. Oncogene 5:1383-1389.
2. Blanton, R. A., M. D. Coltrera, A. M. Gown, C. L. Halbert, and J. K. 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.
3. Botz, J., K. Zerfass-Thome, D. Spitkovsky, H. Delius, B. Vogt, M. Eilers, A. Hatzigeorgiou, and P. Jansen-Durr. 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.
4. Boyer, S. N., D. E. Wazer, and V. Band. 1996. E7 protein of human papilloma virus-16 induces degradation of retinoblastoma protein through the ubiquitin-proteasome pathway. Cancer Res. 56:4620-4624.
5. Carr, A. M. 1996. Checkpoints take the next step. Science 271:314-315.
6. Cheng, S., D. C. Schmidt-Grimminger, T. Murant, T. R. Broker, and L. T. 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.
7. Chesters, P. M., K. H. Vousden, C. Edmonds, and D. J. McCance. 1990. Analysis of human papillomavirus type 16 open reading frame E7 immortalizing function in rat embryo fibroblast cells. J. Gen. Virol. 71:449-453.
8. 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.
9. Crook, T., J. A. Tidy, and K. H. Vousden. 1991. Degradation of p53 can be targeted by HPV E6 sequences distinct from those required for p53 binding and trans-activation. Cell 67:547-556.
10. 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.
11. Davies, R. C., and K. H. Vousden. 1992. Functional analysis of human papillomavirus type 16 E7 by complementation with adenovirus E1A mutants. J. Gen. Virol. 73:2135-2139.
12. Debbas, M., and E. White. 1993. Wild-type p53 mediates apoptosis by E1A, which is inhibited by E1B. Genes Dev. 7:546-554.
13. DeCaprio, J. A., J. W. Ludlow, D. Lynch, Y. Furukawa, J. D. Griffin, H. Piwnica-Worms, C. M. Huang, and D. M. Livingston. 1989. The product of the retinoblastoma susceptibility gene has properties of a cell cycle regulatory element. Cell 58:1085-1095.
14. 1/S-regulatory genes. Mol. Cell. Biol. 15:4215-4224.
15. Demers, G. W., E. Espling, J. B. Harry, B. G. Etscheid, and D. A. Galloway. 1996. Abrogation of growth arrest signals by human papillomavirus type 16 E7 is mediated by sequences required for transformation. J. Virol. 70:6862-6869.
16. Demers, G. W., S. A. Foster, C. L. Halbert, and D. A. Galloway. 1994. Growth arrest by induction of p53 in DNA damaged keratinocytes is bypassed by human papillomavirus 16 E7. Proc. Natl. Acad. Sci. USA 91:4382-4386.
17. Demers, G. W., C. L. Halbert, and D. A. Galloway. 1994. Elevated wild-type p53 protein levels in human epithelial cell lines immortalized by the human papillomavirus type 16 E7 gene. Virology 198:169-174.
18. Dyson, N., P. M. Howley, K. Munger, and E. Harlow. 1989. The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science 243:934-937.
19. El-Deiry, W. S., J. W. Harper, P. M. O'Connor, V. E. Velculescu, C. E. Canman, J. Jackman, J. A. Pietenpol, M. Burrell, D. E. Hill, Y. Wang, K. G. Wiman, W. E. Mercer, M. B. Kastan, K. W. Kohn, S. J. Elledge, K. W. Kinzler, and B. Vogelstein. 1994. WAF1/CIP1 is induced in p53-mediated G1 arrest and apoptosis. Cancer Res. 54:1169-1174.
20. El-Deiry, W. S., T. Tokino, V. E. Velculescu, D. B. Levy, R. Parsons, J. M. Trent, D. Lin, E. Mercer, K. W. Kinzler, and B. Vogelstein. 1993. WAF1, a potential mediator of p53 tumor suppression. Cell 75:817-825.
21. Etscheid, B. G., S. A. Foster, and D. A. Galloway. 1994. The E6 protein of human papillomavirus type 16 functions as a transcriptional repressor in a mechanism independent of the tumor suppressor protein, p53. Virology 205:583-585.
22. Ewen, M. E. 1994. The cell cycle and the retinoblastoma protein family. Cancer Metastasis Rev. 13:45-66.
23. Firzlaff, J. M., C. N. L. Hsia, C. L. Halbert, S. A. Jenison, and D. A. Galloway. 1987. Polyclonal antibodies to human papillomavirus type 6b and type 16 bacterially derived fusion proteins. Cancer Cells 5:105-113.
24. Foster, S. A., G. W. Demers, B. G. Etscheid, and D. A. 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.
25. 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.
26. Gage, J. R., C. Meyers, and F. O. Wettstein. 1990. The E7 proteins of the nononcogenic human papillomavirus type 6b (HPV-6b) and of the oncogenic HPV-16 differ in retinoblastoma protein binding and other properties. J. Virol. 64:723-730.
27. 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.
28. Gray-Bablin, J., J. Zalvide, M. P. Fox, C. J. Knickerbocker, J. A. DeCaprio, and K. Keyomarsi. 1996. Cyclin E, a redundant cyclin in breast cancer. Proc. Natl. Acad. Sci. USA 93:15215-15220.
29. Halbert, C. L., G. W. Demers, and D. A. Galloway. 1991. The E7 gene of human papillomavirus type 16 is sufficient for immortalization of human epithelial cells. J. Virol. 65:473-478.
30. Halbert, C. L., G. W. Demers, and D. A. 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.
31. Hawkins, D. S., G. W. Demers, and D. A. Galloway. 1996. Inactivation of p53 enhances sensitivity to multiple chemotherapeutic agents. Cancer Res. 56: 892-898.
32. 1 restriction point regulation in Rb-deficient fibroblasts. Mol. Cell. Biol. 16:2402-2407.
33. Huang, P. S., D. R. Patrick, G. Edwards, P. J. Goodhart, H. E. Huber, L. Miles, V. M. Garsky, A. Oliff, and D. C. Heimbrook. 1993. Protein domains governing interactions between E2F, the retinohlastoma gene product, and human papillomavirus type 16 E7 protein. Mol. Cell. Biol. 13:953-960.
34. Hunter, T., and J. Pines. 1994. Cyclins and cancer II: cyclin D and CDK inhibitors come of age. Cell 79:573-582.
35. 1 growth arrest pathway in cells expressing the human papillomavirus type 16 E7 oncoprotein. J. Virol. 71:2905-2912.
36. Kamb, A. 1995. Cell-cycle regulators and cancer. Trends Genet. 11:136-140.
37. Kaur, P., and J. K. McDougall. 1989. HPV-18 immortalization of human keratinocytes. Virology 173:302-310.
38. Koff, A., F. Cross, A. Fisher, J. Schumacher, K. Leguellec, M. Philippe, and J. M. Roberts. 1991. Human cyclin E, a new cyclin that interacts with two members of the CDC2 gene family. Cell 66:1217-1228.
39. Koff, A., A. Giordano, D. Desai, K. Yamashita, J. W. Harper, S. J. Elledge, T. Nishimoto, D. O. Morgan, B. R. Franza, and J. M. Roberts. 1992. Formation and activation of a cyclin E-cdk2 complex during the G1 phase of the human cell cycle. Science 257:1689-1694.
40. Koff, A., M. Ohtsuki, P. Kornelia, J. M. Roberts, and J. Massague. 1993. Negative regulation of G1 in mammalian cells: inhibition of cyclin E-dependent kinase by TGF-beta. Science 260:536-539.
41. 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.
42. Laborda, J. 1991. 36B4 cDNA used as an estradiol-independent mRNA control is the cDNA for human acidic ribosomal phosphoprotein PO. Nucleic Acids Res. 19:3998.
43. Li, Y., M. A. Nichols, J. W. Shay, and Y. Xiong. 1994. Transcriptional repression of the D-type cyclin-dependent kinase inhibitor p16 by the retinoblastoma susceptibility gene product. Cancer Res. 54:6078-6082.
44. Matlashewski, G. 1989. The cell biology of human papillomavirus transformed cells. Anticancer Res. 9:1447-1456.
45. Miller, A. D., and G. J. Rosman. 1989. Improved retroviral vectors for gene transfer and expression. BioTechniques 7:980-990.
46. Munger, K., B. A. Werness, N. Dyson, W. C. Phelps, E. Harlow, and P. M. Howley. 1989. Complex formation of the human papillomavirus E7 proteins with the retinoblastoma tumor suppressor gene product. EMBO J. 8:4099-4105.
47. Nass, S. J., and R. B. Dickson. 1977. Detection of cyclin messenger RNAs by nonradioactive ribonuclease protection assay: a comparison of four detection methods. BioTechniques 19:772-776.
48. 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.
49. 1 in mammalian fibroblasts. Science 259:1908-1912.
50. 1-to-S phase transition. Mol. Cell. Biol. 15:2612-2624.
51. Pan, H., and A. E. Griep. 1995. Temporally distinct patterns of p53-dependent and p53-independent apoptosis during mouse lens development. Genes Dev. 9:2157-2169.
52. Parry, D., S. Bates, D. J. Mann, and G. Peters. 1995. Lack of cyclin D-Cdk complexes in Rh-negative cells correlates with high levels of p16INK4/MTS1 tumour suppressor gene product. EMBO J. 14:503-511.
53. Kip1, a cyclin-Cdk inhibitor, links transforming growth factor-b and contact inhibition to cell cycle arrest. Genes Dev. 8:9-22.
54. Quelle, D. E., R. A. Ashmun, S. A. Shurtleff, J.-Y. Kato, D. Bar-Sagi, M. F. Roussell, and C. J. Sherr. 1993. Overexpression of mouse D-type cyclins accelerates G1 phase in rodent fibroblasts. Genes Dev. 7:1559-1571.
55. 1-to-S transition. Mol. Cell. Biol. 15:3463-3469.
56. Reznikoff, C. A., C. Belair, E. Savelieva, Y. Zhai, K. Pfeifer, T. Yeager, K. J. Thompson, S. De Vries, C. Bindley, M. A. Newton, G. Sekhon, and F. Waldman. 1994. Long-term genome stability and minimal genotypic and phenotypic alterations in HPV16 E7-, but not E6-, immortalized human uroepithehal cells. Genes Dev. 8:2227-2240.
57. Ruesch, M. N., and L. A. Laimins. 1997. Initiation of DNA synthesis by human papillomavirus E7 oncoproteins is resistant to p21-mediated inhibition of cyclin E-cdk2 activity. J. Virol. 71:5570-5578.
58. Scheffner, M., J. M. Huibregtse, R. D. Vierstra, and P. M. Howley. 1993. The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell 75:495-505.
59. Schulze, A., K. Zerfass, D. Spitkovsky, S. Middendorp, J. Berges, K. Helin, P. Jansen-Durr, and B. Henglein. 1995. Cell cycle regulation of the cyclin A gene promoter is mediated by a variant E2F site. Proc. Natl. Acad. Sci. USA 92:11264-11268.
60. Sherr, C. J. 1994. G1 phase progression: cycling on cue. Cell 79:551-555.
61. Soos, T. J., H. Kiyokawa, J. S. Yan, M. S. Rubin, A. Giordano, A. DeBlasio, S. Bottega, B. Wong, J. Mendelsohn, and A. Koff. 1996. Formation of p27-CDK complexes during the human mitotic cell cycle. Cell Growth Differ. 7:135-146.
62. Spitkovsky, D., P. Jansen-Durr, E. Karsenti, and I. Hoffman. 1996. S-phase induction by adenovirus E1A requires activation of cdc25a tyrosine phosphatase. Oncogene 12:2549-2554.
63. Tommasino, M., and L. Crawford. 1995. Human papillomavirus E6 and E7: proteins which deregulate the cell cycle. Bioessays 17:509-518.
64. Van Dyke, T. A. 1994. Analysis of viral-host protein interactions and tumorigenesis in transgenic mice. Semin. Cancer Biol. 5:47-60.
65. Watanabe, S., H. Sato, N. Komiyama, T. Kanda, and K. Yoshiike. 1992. The E7 functions of human papillomaviruses in rat 3Y1 cells. Virology 187:107-114.
66. Weinberg, R. A. 1995. The retinoblastoma protein and cell cycle control. Cell 81:323-330.
67. Werness, B. A., A. J. Levine, and P. M. Howley. 1990. Association of human papillomavirus types 16 and 18 E6 proteins with p53. Science 248:76-79.
68. 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.
69. Xiong, Y., D. Kuppuswamy, Y. Li, E. M. Livanos, M. Hixon, A. White, D. Beach, and T. D. Tlsty. 1996. Alteration of cell cycle complexes in human papillomavirus E6-and E7-expressing fibroblasts precedes neoplastic transformation. J. Virol. 70:999-1008.
70. Yeager, T., W. Stadler, C. Belair, J. Puthenveettil, O. Olopade, and C. A. Reznikoff. 1995. Increased p16 levels correlate with pRb alterations in human urothelial cells. Cancer Res. 55:493-497.
71. Zerfass, K., A. Schulze, D. Spitkovsky, V. Friedman, B. Henglein, and P. Jansen-Durr. 1995. Sequential activation of cyclin E and cyclin A gene expression by human papillomavirus type 16 E7 through sequences necessary for transformation. J. Virol. 69:6389-6399.
72. Zerfass-Thome, K., W. Zwerschke, B. Mannhardt, R. Tindle, J. W. Botz, and P. Jansen-Durr. 1996. Inactivation of the cdk inhibitor p27KIP1 by the human papillomavirus type 16 E7 oncoprotein. Oncogene 13:2323-2330.
73. Zhang, H., G. J. Hannon, and D. Beach. 1995. p21-containing cyclin kinases exist in both active and inactive states. Genes Dev. 8:1750-1758.
74. zur Hausen, H. 1991. Human papillomaviruses in the pathogenesis of anogenital cancer. Virology 184:9-13.