Destabilization of the RB tumor suppressor protein and stabilization of p53 contribute to HPV type 16 E7-induced apoptosis

Virology

Volumn 239, Issue 1, 1997, Pages 97-107

  Jones, D Leanne ^a   Thompson, David A ^a   Münger, Karl ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASEIN KINASE II; ONCOPROTEIN; PROTEIN P53; RETINOBLASTOMA PROTEIN; VIRUS PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DEATH; CELL TRANSFORMATION; CELL VIABILITY; CONTROLLED STUDY; HUMAN; HUMAN CELL; LENS EPITHELIUM; LUNG FIBROBLAST; NONHUMAN; PHOTORECEPTOR CELL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN STABILITY; PROTEIN TARGETING; TRANSGENIC MOUSE; TUMOR SUPPRESSOR GENE; WART VIRUS;

ADENOVIRIDAE; ANIMALIA; DNA VIRUSES; HUMAN PAPILLOMAVIRUS; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN PAPILLOMAVIRUS TYPES; MUS MUSCULUS; PAPOVAVIRIDAE; RNA VIRUSES;

EID: 0031438309     PISSN: 00426822     EISSN: None     Source Type: Journal    
DOI: 10.1006/viro.1997.8851     Document Type: Article

References (58)

1. Almasan A., Yin Y. X., Kelly R. E., Lee E.-Y. H.-P., Bradley A., Li W. W., Bertino J. R., Wahl G. M. Deficiency of retinoblastoma protein leads to inappropriate S-phase entry, activation of E2F-responsive genes, and apoptosis. Proc. Natl. Acad. Sci. USA. 92:1995;5436-5440.
2. An B., Dou Q. P. Cleavage of retinoblastoma protein during apoptosis: An interleukin 1 beta-converting enzyme-like protease as candidate. Cancer Res. 56:1996;438-442.
3. Banks L., Edmonds C., Vousden K. Ability of the HPV-16 E7 protein to bind RB and induce DNA synthesis is not sufficient for efficient transforming activity in NIH 3T3 cells. Oncogene. 5:1990;1383-1389.
4. Barbosa M. S., Edmonds C., Fisher C., Schiller J. T., Lowy D. R., Vousden K. H. The region of the HPV E7 oncoprotein homologous to adenovirus E1a and SV40 large T antigen contains separate domains for Rb binding and casein kinase II. EMBO J. 9:1990;153-160.
5. Boyer S. N., Wazer D. E., Band V. E7 protein of human papilloma virus-16 induces degradation of retinoblastoma protein through the ubiquitin-proteasome pathway. Cancer Res. 56:1996;4620-4624.
6. Brokaw J. L., Yee C. L., Münger K. A mutational analysis of the amino terminal domain of the human papillomavirus type 16 E7 oncoprotein. Virology. 205:1994;603-607.
7. Chiou S.-K., White E. p300 binding by E1A co-segregates with p53 induction but is dispensable for apoptosis. J. Virol. 71:1997;3515-3525.
8. Clarke A. R., Maandag E. R., Van Roon M., Van derLugt N. M. T., Van der Valk M., Hooper M. L., Berns A., Te Riele H. Requirement for a functional Rb-1 gene in murine development. Nature. 359:1992;328-330.
9. Conzen S. D., Snay C. A., Cole C. N. Identification of a novel antiapoptotic functional domain in simian virus 40 large T antigen. J. Virol. 71:1997;4536-4543.
10. Davies R. C., Vousden K. H. Functional analysis of human papillomavirus type 16 E7 by complementation with adenovirus E1A mutants. J. Gen. Virol. 73:1992;2135-2139.
11. Demers G. W., Espling E., Harry J. B., Etscheid B. G., Galloway D. A. Abrogation of growth arrest signals by human papillomavirus type 16 E7 is mediated by sequences required for transformation. J. Virol. 70:1996;6862-6869.
12. Demers G. W., Halbert C. L., Galloway D. A. Elevated wild-type p53 protein levels in human epithelial cell lines immortalized by the human papillomavirus type 16 E7 gene. Virology. 198:1994;169-174.
13. Edmonds C., Vousden K. H. A point mutational analysis of human papillomavirus type 16 E7 protein. J. Virol. 63:1989;2650-2656.
14. Evan G. I., Wyllie A. H., Gilbert C. S., Littlewood T. D., Land H., Brooks M., Waters C. M., Penn L. Z., Hancock D. C. Induction of apoptosis in fibroblasts by c-myc protein. Cell. 69:1992;119-128.
15. Firzlaff J. M., Lüscher B., Eisenman R. N. Negative charge at the casein kinase phosphorylation site is important for transformation but not for RB binding by the E7 protein of the human papillomavirus type 16. Proc. Natl. Acad. Sci. USA. 88:1991;5187-5191.
16. Haas Kogan D. A., Kogan S. C., Levi D., Dazin P., Tang A., Fung Y. K. T., Israel M. A. Inhibition of apoptosis by the retinoblastoma gene product. EMBO J. 14:1995;461-472.
17. Halbert C. L., Demers W., Galloway D. A. The E7 gene of human papillomavirus type 16 is sufficient for immortalization of human epithelial cells. J. Virol. 65:1991;473-478.
18. Hateboer G., Kerkhoven R. M., Shvarts A., Bernards R., Beijersbergen R. L. Degradation of E2F by the ubiquitin-proteasome pathway: Regulation by retinoblastoma family proteins and adenovirus transforming proteins. Genes Dev. 10:1996;2960-2970.
19. Haupt Y., Rowan S., Oren M. p53-mediated apoptosis in HeLa cells can be overcome by excess pRB. Oncogene. 10:1995;1563-1571.
20. Hawley-Nelson P., Vousden K. H., Hubbert N. L., Lowy D. R., Schiller J. T. HPV16 E6 and E7 proteins cooperate to immortalize human foreskin keratinocytes. EMBO J. 8:1989;3905-3910.
21. Hickman E. S., Bates S., Vousden K. H. Perturbation of the p53 response by human papillomavirus type 16 E7. J. Virol. 71:1997;3710-3718.
22. Hofmann F., Martelli F., Livingston D. M., Wang Z. The retinoblastoma gene product protects E2F-1 from degradation by the ubiquitin-proteasome pathway. Genes Dev. 10:1996;2949-2959.
23. Howes K. A., Ransom L. N., Papermaster D. S., Lasudry J. G. H., Albert D. M., Windle J. J. Apoptosis or retinoblastoma: Alternative fates of photoreceptors expressing the HPV-16 E7 gene in the presence or absence of p53. Genes Dev. 8:1994;1300-1310.
24. Howley P. M. Papillomavirinae: The viruses and their replication. Fundamental Virology. 1996;Lippincott-Raven, Philadelphia. p. 947-978.
25. Hsieh J.-K., Fredersdorf S., Kouzarides T., Martin K., Lu X. E2F1-induced apoptosis requires DNA binding but not transactivation and is inhibited by the retinoblastoma protein through direct interaction. Genes Dev. 11:1997;1840-1852.
26. Hudson J. B., Bedell M. A., McCance D. J., Laimins L. A. Immortalization and altered differentiation of human keratinocytes in vitro by the E6 and E7 open reading frames of human papillomavirus type 18. J. Virol. 64:1990;519-526.
27. Jacks T., Fazeli A., Schmitt E. M., Bronson R. T., Goodell M. A., Weinberg R. A. Effects of an Rb mutation in the mouse. Nature. 359:1992;295-300.
28. Jacobson M. D., Weil M., Raff M. Programmed cell death in animal development. Cell. 88:1997;347-354.
29. Janicke R. U., Walker P. A., Lin X. Y., Porter A. G. Specific cleavage of the retinoblastoma protein by an ICE-like protease in apoptosis. EMBO J. 15:1996;6969-6978.
30. Jewers R. J., Hildebrandt P., Ludlow J. W., Kell B., McCance D. J. Regions of human papillomavirus type 16 E7 oncoprotein required for immortalization of human keratinocytes. J. Virol. 66:1992;1329-1335.
31. Jones D. L., Münger K. Analysis of the p53-mediated G1 growth arrest pathway in cells expressing the human papillomavirus type 16 E7 oncoprotein. J. Virol. 71:1997;2905-2912.
32. Kauffmann-Zeh A., Rodriguez-Viciana P., Ulrich E., Gilbert C., Coffer P., Downward J., Evan G. Suppression of c-Myc induced apoptosis by Ras signalling through PI(3)K and PKB. Nature. 385:1997;544-548.
33. Kowalik T. F., Degregori J., Schwarz J. K., Nevins J. R. E2F1 overexpression in quiescent fibroblasts leads to induction of cellular DNA synthesis and apoptosis. J. Virol. 69:1995;2491-2500.
34. Lane D. P. Cancer. p53, guardian of the genome. Nature. 358:1992;15-16.
35. Lee E.-Y. H.-P., Chang C. Y., Hu N., Wang Y. C.-J., Lai C. C., Herrup K., Lee W. H., Bradley A. Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis. Nature. 359:1992;288-294.
36. Levine A. J. p53, cellular gatekeeper for growth and division. Cell. 88:1997;323-331.
37. Macleod K. F., Hu Y., Jacks T. Loss of Rb activates both p53-dependent and independent cell death pathways in the developing mouse nervous system. EMBO J. 15:1996;6178-6188.
38. McCance D. J., Kopan R., Fuchs E., Laimins L. A. Human papillomavirus type 16 alters human epithelial cell differentiation in vitro. Proc. Natl. Acad. Sci. USA. 85:1988;7169-7173.
39. McIntyre M. C., Frattini M. G., Grossman S. R., Laimins L. A. 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. 67:1993;3142-3150.
40. Miller A. D., Rosman G. J. Improved retroviral vectors for gene transfer and expression. BioTechniques. 7:1989;980-982.
41. Morozov A., Shiyanov P., Barr E., Leiden J. M., Raychaudhuri P. Accumulation of human papillomavirus type 16 E7 protein bypasses G1 arrest induced by serum deprivation and by the cell cycle inhibitor p21. J. Virol. 71:1997;3451-3457.
42. Münger K., Phelps W. C. The human papillomavirus-E7 protein as a transforming and transactivating factor. Biochem. Biophys. Acta. 1155:1993;111-123.
43. Münger K., Phelps W. C., Bubb V., Howley P. M., Schlegel R. The E6 and E7 genes of the human papillomavirus type 16 together are necessary and sufficient for transformation of primary human keratinocytes. J. Virol. 63:1989;4417-4421.
44. Münger K., Scheffner M., Huibregtse J. M., Howley P. M. Interactions of HPV E6 and E7 with tumour suppressor gene products. Cancer Surv. 12:1992;197-217.
45. Nichols W. W., Murphy D. G., Cristofaldo V. J., Toji L. H., Greene A. E., Dwight S. A. Characterization of a new human diploid cell strain, IMR-90. Science. 196:1977;60-63.
46. Pan H. C., Griep A. E. Altered cell cycle regulation in the lens of HPV-16 E6 or E7 transgenic mice: Implications for tumor suppressor gene function in development. Genes Dev. 8:1994;1285-1299.
47. Pan H. C., Griep A. E. Temporally distinct patterns of p53-dependent and p53-independent apoptosis during mouse lens development. Genes Dev. 9:1995;2157-2169.
48. Phelps W. C., Münger K., Yee C. L., Barnes J. A., Howley P. M. Structure-function analysis of the human papillomavirus E7 oncoprotein. J. Virol. 66:1992;2418-2427.
49. Phelps W. C., Yee C. L., Münger K., Howley P. M. The human papillomavirus type 16 E7 gene encodes transactivation and transformation functions similar to adenovirus E1a. Cell. 53:1988;539-547.
50. Phillips A. C., Bates S., Ryan K. M., Helin K., Vousden K. H. Induction of DNA synthesis and apoptosis are separable functions of E2F-1. Genes Dev. 11:1997;1853-1863.
51. Qin X. Q., Livingston D. M., Kaelin W. G., Adams P. D. Deregulated transcription factor E2F-1 expression leads to S-phase entry and p53-mediated apoptosis. Proc. Natl. Acad. Sci. USA. 91:1994;10918-10922.
52. Rao L., Debbas M., Sabbatini P., Hockenbery D., Korsmayer S., White E. The adenovirus E1A proteins induce apoptosis, which is inhibited by the E1B 19-kDa and Bcl-2 proteins. Proc. Natl. Acad. Sci. USA. 89:1992;7742-7746.
53. Thompson D. A., Belinski G., Chang T., Jones D. L., Schlegel R., Münger K. Human papillomavirus type 16 E6 protein decreases the vigilance of mitotic checkpoints. Oncogenem. 1997.
54. Weinberg R. A. The cat and mouse games that genes, viruses, and cells play. Cell. 88:1997;573-575.
55. White A. E., Livanos E. M., Tlsty T. D. Differential Disruption of Genomic Integrity and Cell Cycle Regulation in Normal Human Fibroblasts by the HPV Oncoproteins. Genes Dev. 8:1994;666-677.
56. Wu X. W., Levine A. J. P53 and E2F-1 cooperate to mediate apoptosis. Proc. Natl. Acad. Sci. USA. 91:1994;3602-3606.
57. Zacksenhaus E., Jiang Z., Chung D. D., M. J., Phillips R. A., Gallie B. L. pRb controls proliferation, differentiation, and death of skeletal muscle cells and other lineages during embryogenesis. Genes Dev. 10:1996;3051-3064.
58. zur Hausen H. Viruses in human cancer. Science. 254:1991;1167-1172.