Perturbation of the p53 response by human papillomavirus type 16 E7

Journal of Virology

Volumn 71, Issue 5, 1997, Pages 3710-3718

  Hickman, Emma S ^a   Bates, Stewart ^a   Vousden, Karen H ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN P53;

APOPTOSIS; ARTICLE; CELL STRAIN MCF 7; CONTROLLED STUDY; DNA SYNTHESIS; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; TUMOR SUPPRESSOR GENE; WART VIRUS;

EID: 0030952369     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.71.5.3710-3718.1997     Document Type: Article

References (80)

1. Agarwal, M. L., A. Agarwal, W. R. Taylor, and G. R. Stark. 1995. p53 controls both the G2/M and the G1 cell cycle checkpoints and mediates reversible growth arrest in human fibroblasts. Proc. Natl. Acad. Sci. USA 92:8493-8497.
2. 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 G1. Genes Dev. 7:812-821.
3. Bates, S., and K. H. Vousden. 1996. p53 in signalling checkpoint arrest or apoptosis. Curr. Opin. Genet. Dev. 6:12-19.
4. 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.
5. Bookstein, R., J.-Y. Shew, P.-L. Chen, P. Scully, and W.-H. Lee. 1990. Suppression of tumourigenicity of human prostate carcinoma cells by replacing a mutated RB gene. Science 247:712-715.
6. Brugarolas, J., C. Chandrasekaran, J. I. Gordon, D. Beach, T. Jacks, and G. J. Hannon. 1995. Radiation-induced cell cycle arrest compromised by p21 deficiency. Nature 377:552-557.
7. 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.
8. Chellappan, S., V. B. Kraus, B. Kroger, K. Munger, P. M. Howley, W. C. Phelps, and J. R. 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 retinoblastoma gene product. Proc. Natl. Acad. Sci. USA 89:4549-4553.
9. Chen, P.-L., P. Scully, J.-Y. Shew, J. Y. J. 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.
10. Crook, T., N. J. Marston, E. A. Sara, and K. H. Vousden. 1994. Transcriptional activation by p53 correlates with suppression of growth but not transformation. Cell 79:817-827.
11. Crook, T., D. Wrede, J. Tidy, J. Scholefield, L. Crawford, and K. H. Vousden. 1991. Status of c-myc, p53 and retinoblastoma genes in human papillomavirus positive and negative squamous cell carcinomas of the anus. Oncogene 6:1251-1257.
12. Crook, T., D. Wrede, and K. H. Vousden. 1991. p53 point mutation in HPV negative human cervical carcinoma cell lines. Oncogene 6:873-875.
13. Cross, S. M., C. A. Sanchez, C. A. Morgan, M. K. Schimke, S. Ramel, R. L. Idzerda, W. H. Raskind, and B. J. Reid. 1995. A p53-dependent mouse spindle checkpoint. Science 267:1353-1356.
14. Davies, R., R. Hicks, T. Crook, J. Morris, and K. H. 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.
15. DeCaprio, J. A., J. W. Ludlow, D. Lynch, Y. Furukawa, J. 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.
16. DeGregori, J., G. Leone, K. Ohtani, A. Miron, and J. R. Nevins. 1995. E2F-1 accumulation bypasses a G1 arrest resulting from the inhibition of G1 cyclin-dependent kinase activity. Genes Dev. 9:2873-2887.
17. Demers, G. W., S. A. Foster, C. L. Halbert, and D. A. Galloway. 1994. Growth arrest by induction of p53 in DNA damaged keratinocytesis bypassed by human papillomavirus 16 E7. Proc. Natl. Acad. Sci. USA 91:4382-4386.
18. Deng, C., P. Zhang, J. W. Harper, S. J. Elledge, and P. Leder. 1995. Mice lacking p21CIP1/WAF1 undergo normal development, but are defective in G1 checkpoint control. Cell 82:675-684.
19. DiLeonardo, A., S. P. Linke, K. Clarkin, and G. M. Wahl. 1994. DNA damage triggers a prolonged p53-dependent G1 arrest and long-term induction of Cip1 in normal human fibroblasts. Genes Dev. 8:2540-2551.
20. Dulic, V., W. K. Kaufmann, S. J. Wilson, T. D. Tlsty, E. Lees, J. W. Harper, S. J. Elledge, and S. I. Reed. 1994. p53-dependent inhibition of cyclin-dependent kinase activities in human fibroblasts during radiation-induced G1 arrest. Cell 76:1013-1023.
21. Durst, M., L. Gissman, H. Ikenberg, and H. zur Hausen. 1983. A papillomavirus DNA from cervical carcinoma and its prevalence in cancer biopsy samples from different geographic regions. Proc. Natl. Acad. Sci. USA 80: 3812-3816.
22. El-Deiry, W. S., S. E. Kern, J. A. Pietenpol, K. W. Kinzler, and B. Vogelstein. 1992. Definition of a consensus binding site for p53. Nat. Genet. 1:45-49.
23. 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.
24. Fritsche, M., C. Haessler, and G. Brandner. 1993. Induction of nuclear accumulation of the tumor-suppressor protein p53 by DNA-damaging agents. Oncogene 8:307-318. (Erratum, 8:2605.)
25. Funk, W. D., D. T. Pak, R. H. Karas, W. E. Wright, and J. W. Shay. 1992. A transcriptionally active DNA-binding site for human p53 protein complexes. Mol. Cell. Biol. 12:2866-2871.
26. Girard, F., U. Strausfeld, A. Fernandez, and N. J. Lamb. 1991. Cyclin A is required for the onset of DNA replication in mammalian fibroblasts. Cell 67:1169-1179.
27. Gissman, L., M. Boshart, M. Durst, H. Ikenberg, D. Wagner, and H. zur Hausen. 1984. Presence of human papillomavirus in genital tumors. J. Invest. Dermatol. 83:26S-28S.
28. 1-phase checkpoint by low-oxygen conditions is independent of p53 status. Mol. Cell. Biol. 14:6264-6277.
29. Guillouf, C., F. Rosselli, K. Krishnaraju, E. Moustacchi, B. Hoffman, and D. A. Liebermann. 1995. p53 involvement in control of G2 exit of the cell cycle: role in DNA damage-induced apoptosis. Oncogene 10:2263-2270.
30. Hall, P. A., P. H. McKee, H. P. Menage, R. Dover, and D. P. Lane. 1993. High levels of p53 protein in UV-irradiated normal human skin. Oncogene 8:203-207.
31. 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.
32. Hickman, E. S., S. M. Picksley, and K. H. Vousden. 1994. Cells expressing HPV16 E7 continue cell cycle progression following DNA damage induced p53 activation. Oncogene 9:2177-2181.
33. Hinds, P. W., S. F. Dowdy, E. N. Eaton, A. Arnold, and R. A. Weinberg. 1994. Function of a human cyclin gene as an oncogene. Proc. Natl. Acad. Sci. USA 91:709-713.
34. 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.
35. Hollstein, M., D. Sidransky, B. Vogelstein, and C. C. Harris. 1991. p53 mutations in human cancers. Science 253:49-53.
36. Jiang, W., Y.-J. Zhang, S. M. Kahn, M. C. Hollstein, R. M. Santella, S.-H. Lu, C. C. Harris, R. Montesano, and I. B. Weinstein. 1993. Altered expression of the cyclin D1 and retinoblastoma genes in human esophageal cancer. Proc. Natl. Acad. Sci. USA 90:9026-9030.
37. Kamb, A., N. A. Gruis, J. Weaver-Feldhaus, Q. Liu, K. Harshamn, S. V. Tavtigian, E. Stockert, R. S. Day III, B. E. Johnson, and M. H. Skolnick. 1994. A cell cycle regulator potentially involved in genesis of many tumour types. Science 264:436-440.
38. Kastan, M. B., O. Onyekwere, D. Sidransky, B. Vogelstein, and R. W. Craig. 1991. Participation of p53 protein in the cellular response to DNA damage. Cancer Res. 51:6304-6311.
39. Kessis, T. D., R. J. Slebos, W. G. Nelson, M. B. Kastan, B. S. Plunkett, S. M. Han, A. T. Lorincz, L. Hedrick, and K. R. Cho. 1993. Human papillomavirus 16 E6 expression disrupts the p53-mediated cellular response to DNA damage. Proc. Natl. Acad. Sci. USA 90:3988-3992.
40. Krek, W., G. Xu, and D. M. Livingston. 1995. Cyclin A-kinase regulation of E2F1 DNA binding function underlies suppression of an S phase checkpoint. Cell 83:1149-1158.
41. Latham, K. M., S. W. Eastman, A. Wong, and P. W. Hinds. 1996. Inhibition of p53-mediated growth arrest by overexpression of cyclin-dependent kinases. Mol. Cell. Biol. 16:4445-4455.
42. Lee, W. H., R. Bookstein, and E. Y. Lee. 1988. Studies on the human retinoblastoma susceptibility gene. J. Cell. Biochem. 38:213-227.
43. Lee, W. Y.-H., J.-Y. Shew, R. Bookstein, P. Scully, and W.-H. Lee. 1988. Inactivation of the retinoblastoma susceptibility gene in human breast cancers. Science 241:218-221.
44. Lees, J. A., K. 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.
45. Lin, B. T.-Y., S. Gruenwald, A. O. Morla, W.-H. Lee, and J. Y. Wang. 1991. Retinoblastoma cancer suppressor gene product is a substrate of the cell cycle regulator cdc2 kinase. EMBO J. 10:857-864.
46. Lin, D., M. T. Shields, S. J. Ullrich, E. Appella, and W. E. Mercer. 1992. Growth arrest induced by wild-type p53 protein blocks cells prior to or near the restriction point in late G1 phase. Proc. Natl. Acad. Sci. USA 89:9210-9214.
47. Livingstone, L. R., A. White, J. Sprouse, E. Livanos, T. Jacks, and T. D. Tlsty. 1992. Altered cell cycle arrest and gene amplification potential accompany loss of wild-type p53. Cell 70:923-935.
48. Mal, A., R. Y. C. Poon, P. H. Howe, H. Toyoshima, T. Hunter, and M. L. Harter. 1996. Inactivation of p27Kip1 by the viral E1A oncoprotein in TGFB-treated cells. Nature 380:262-265.
49. Malzman, W., and L. Czyzyk. 1984. UV irradiation stimulates levels of p53 cellular tumor antigen in nontransformed mouse cells. Mol. Cell. Biol. 4:1689-1694.
50. McIntyre, M. C., M. N. Ruesch, and L. A. Laimins. 1996. Human papillomavirus E7 oncoproteins bind a single form of cyclin E in a complex with cdk2 and p107. Virology 215:73-82.
51. 1 kinase activity for cdk6, a novel cyclin D partner. Mol. Cell. Biol. 14:2077-2086.
52. Morris, J. D., T. Crook, L. R. Bandara, R. Davies, N. B. LaThangue, and K. H. Vousden. 1993. Human papillomavirus type 16 E7 regulates E2F and contributes to mitogenic signalling. Oncogene 8:893-898.
53. Nelson, W. G., and M. B. Kastan. 1994. DNA strand breaks: the DNA template alterations that trigger p53-dependent DNA damage response pathways. Mol. Cell. Biol. 14:1815-1823.
54. Nigg, E. A. 1993. Targets of cydin-dependent protein kinases. Curr. Biol. 5:187-193.
55. Nobori, T., K. Miura, D. J. Wu, A. Lois, K. Takabayashi, and D. A. Carson. 1994. Deletions of the cyclin-dependent kinase-4 inhibitor gene in multiple human cancers. Nature 368:753-756.
56. 1-to-S phase transition. Mol. Cell. Biol. 15:2612-2624.
57. Pagano, M., R. Pepperkok, J. Lukas, V. Baldin, W. Ansorge, J. Bartek, and G. Draetta. 1993. Regulation of the cell cycle by the cdk2 protein kinase in cultured human fibroblasts. J. Cell Biol. 121:101-111.
58. Pagano, M., R. Pepperkok, F. Verde, W. Ansorge, and G. Draetta. 1992. Cyclin A is required at two points in the human cell cycle. EMBO J. 11:961-971.
59. Pan, H., and A. E. Griep. 1994. Altered cell cycle regulation in the lens of HPV-16 E6 or E7 transgenic mice: implications for tumour suppressor gene function in development. Genes Dev. 8:1285-1299.
60. Pietenpol, J. A., T. Tokino, S. Thiagalingam, W. S. el-Deiry, K. W. Kinzler, and B. Vogelstein. 1994. Sequence-specific transcriptional activation is essential for growth suppression by p53. Proc. Natl. Acad. Sci. USA 91:1998-2002.
61. Puthenveettil, J. A., S. M. Frederickson, and C. A. Reznikoff. 1996. Apoptosis in human papillomavirus 16 E7-, but not E6-immortalised human uroepithelial cells. Oncogene 13:1123-1131.
62. Quelle, D. E., R. A. Ashmun, S. A. Shurtleff, J.-Y. Kato, D. Bar-Sagi, M. F. Roussel, and C. J. Sherr. 1993. Overexpression of mouse D type cyclins accelerates G1 phase in rodent libroblasts. Genes Dev. 7:1559-1571.
63. Sabbatini, P., J. Lin, A. J. Levine, and E. White. 1995. Essential role for p53-mediated transcription in E1A-induced apoptosis. Genes Dev. 9:2184-2192.
64. Scheffner, M., K. Munger, J. C. Byrne, and P. M. Howley. 1991. The state of the p53 and retinoblastoma genes in human cervical carcinoma cell lines. Proc. Natl. Acad. Sci. USA 88:5523-5527.
65. Scheffner, M., B. A. Werness, J. M. Huibregtse, A. J. Levine, and P. M. Howley. 1990. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 63:1129-1136.
66. Slebos, R. J., M. H. Lee, B. S. Plunkett, T. D. Kessis, B. O. Williams, T. Jacks, L. Hedrick, M. B. Kastan, and K. R. Cho. 1994. p53-dependent G1 arrest involves pRB-related proteins and is disrupted by the human papillomavirus 16 E7 oncoproiein. Proc. Natl. Acad. Sci. USA 91:5320-5324.
67. Stewart, N., G. G. Hicks, F. Paraskevas, and M. Mowat. 1995. Evidence for a second cell cycle block at G2/M by p53. Oncogene 10:109-115.
68. Thomas, M., G. Matlashewski, D. Pim, and L. Banks. 1996. Induction of apoptocic by p53 is independent of its oligomeric state and can be abolished by HPV-18 E6 through ubiquitin mediated degradation. Oncogene 13:265-273.
69. Tommasino, M., J. P. Adamczewski, F. Carlotti, C. F. Barth, R. Manetti, M. Contorni, F. Cavalieri, T. Hunt, and L. Crawford. 1993. HPV16 E7 protein associates with the protein kinase p33cdk2 and cyclin A. Oncogene 8:195-202.
70. Tsai, L.-H., E. Lees, B. Faha, E. Harlow, and K. Riabowol. 1993. The cdk2 kinase is required for the G1-to-S transition in mammalian cells. Oncogene 8:1593-1602.
71. Venter, D. J., K. L. Bevan, R. L. Ludwig, T. E. Riley, P. S. Jat, D. G. Thomas, and M. D. Noble. 1991. Retinoblastoma gene deletions in human glioblastomas. Oncogene 6:445-448.
72. Vousden, K. H. 1993. Interactions of human papillomavirus transforming proteins with the products of tumour suppressor genes. FASEB J. 7:872-879.
73. Waldman, T., K. W. Kinzler, and B. Vogelstein. 1995. p21 is necessary for the p53-mediated G1 arrest in human cancer cells. Cancer Res. 55:5187-5190.
74. Waldman, T., C. Lengauer, K. W. Kinzler, and B. Vogelstein. 1996. Uncoupling of S phase and mitosis induced by anticancer agents in cells lacking p21. Nature 381:713-716.
75. Wang, Y., I. Okan, K. Pokrovskaja, and K. G. Wiman. 1996. Abrogation of p53-induced G1 arrest by the HPV16 E7 protein does not inhibit p53-induced apoptosis. Oncogene 12:2731-2735.
76. 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.
77. 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.
78. Yokota, J., T. Akiyama, Y. K. Fung, W. F. Benedict, Y. Namba, M. Hanaoka, M. Wada, T. Terasaki, Y. Shimosato, T. Sugimura, et al. 1988. Altered expression of the retinoblastoma (RB) gene in small-cell carcinoma of the lung. Oncogene 3:471-475.
79. KIP1 by the human papillomavirus type 16 E7 oncoprotein. Oncogene 13:2323-2330.
80. Zhu, L., E. Harlow, and B. D. Dynlacht. 1995. p107 uses a p21CIP1-related domain to bind cyclin/cdk2 and regulate interactions with E2F. Genes Dev. 9:1740-1752.