Bovine papillomavirus E2 protein activates a complex growth-inhibitory program in p53-negative HT-3 cervical carcinoma cells that includes repression of cyclin A and cdc25A phosphatase genes and accumulation of hypophosphorylated retinoblastoma protein

Cell Growth and Differentiation

Volumn 10, Issue 6, 1999, Pages 413-422

  Naeger, Lisa K ^a,c   Goodwin, Edward C ^c   Hwang, Eun Seong ^b,c   DeFilippis, Rosa Anna ^c   Zhang, Hui ^c   DiMaio, Daniel ^c  

^a GILEAD SCIENCES   (United States)

^b University of Seoul   (South Korea)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE PROTEIN; CYCLIN A; CYCLIN DEPENDENT KINASE; HYDROXYUREA; MIMOSINE; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN E2; RETINOBLASTOMA PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; CELL GROWTH; CELL PROLIFERATION; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE EXPRESSION REGULATION; GROWTH INHIBITION; HUMAN; HUMAN CELL; PAPILLOMA VIRUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; UTERINE CERVIX CARCINOMA;

ANIMALS; CARRIER PROTEINS; CATTLE; CDC2-CDC28 KINASES; CDC25 PHOSPHATASE; CELL CYCLE PROTEINS; CELL DIVISION; CYCLIN A; CYCLIN-DEPENDENT KINASE 2; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLIN-DEPENDENT KINASES; CYCLINS; DNA-BINDING PROTEINS; E2F TRANSCRIPTION FACTORS; E2F1 TRANSCRIPTION FACTOR; ENZYME INHIBITORS; FEMALE; GENE EXPRESSION REGULATION; GROWTH INHIBITORS; HELA CELLS; HUMANS; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE-PHOSPHATASE; REPRESSOR PROTEINS; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR DP1; TRANSCRIPTION FACTORS; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEIN P53; UTERINE CERVICAL NEOPLASMS; VIRAL PROTEINS;

EID: 0033057438     PISSN: 10449523     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (68)

1. Villa, L. L. Human papillomaviruses and cervical cancer. Adv. Cancer Res., 77: 321-341, 1997.
2. Adams, P. D., and Kaelin, W. G., Jr. Transcriptional control by E2F. Semin. Cancer Biol., 6; 99-108, 1995.
3. Chellappan, S., Kraus, V. B., Kroger, B., Münger, K., Howley, P. M., Phelps, W. C., and Nevins, J. R. Adenovirus E1A, simian vims 40 tumor antigen, and human papillomavirus E7 protein share the capacity to disrupt the interaction between the transcription factor E2F and the retinoblastoma gene product. Proc. Natl. Acad. Sci. USA, 89: 4549-4553, 1992.
4. Chellappan, S. P., Hiebert, S., Mudryj, M., Horowitz, J. M., and Nevins, J. R. The E2F transcription factor is a cellular target for the RB protein. Cell, 65: 1053-1061, 1991.
5. Hinds, P. W., Mittnacht, S., Dulic, V., Arnold, A., Reed, S. I., and Weinberg, R. A. Regulation of retinoblastoma protein functions by ectopic expression of human cyclins. Cell, 70: 993-1006, 1992.
6. Morgan, D. O. Principles of CDK regulation. Nature (Lond.), 374: 131-134, 1995.
7. Okayama, H., Nagata, A., Jinno, S., Murakami, H., Tanaka, K., and Nakashima, N. Cell cycle control in fission yeast and mammals: identification of new regulatory mechanisms. Adv. Cancer Res., 69: 17-62, 1996.
8. Weintraub, S. J., Prater, C. A., and Dean, D. C. Retinoblastoma protein switches the E2F site from positive to negative element. Nature (Lond.), 358: 259-261, 1992.
9. Weintraub, S. J., Chow, K. N., Luo, R. X., Zhang, S. H., He, S., and Dean, D. C. Mechanism of active transcriptional repression by the retinoblastoma protein. Nature (Lond.), 375: 812-815, 1995.
10. Nevins, J. R. E2F: a link between the Rb tumor suppressor protein and viral oncoproteins. Science (Washington DC), 258: 424-429, 1992.
11. El-Deiry, W. S., Tokino, T., Velculescu, V. E., Levy, D. B., Parsons, R., Trent, J. M., Lin, D., Mercer, W. E., Kinzler, K. W., and Vogelstein, B. WAF1, a potential mediator of p53 tumor suppression. Cell, 75: 817-825, 1993.
12. 1 cyclin-dependent kinases. Cell, 75: 805-816, 1993.
13. Draetta, G., and Eckstein, J. Cdc25 protein phosphatases in cell proliferation. Biochim. Biophys. Acta, 1332: M53-M63, 1997.
14. Galaktionov, K., and Beach, D. Specific activation of cdc25 tyrosine phosphatases by B-type cyclins: evidence for multiple roles of mitotic cyclins. Cell, 67: 1181-1194, 1991.
15. cdc2, Cell, 67: 197-211, 1991.
16. 1/S transition. EMBO J., 13: 4302-4310, 1994.
17. Jinno, S., Suto, K., Nagata, A., Igarashi, M., Kanaoka, Y., Nojima, H., and Okayama, H. Cdc25A is a novel phosphatase functioning early in the cell cycle. EMBO J., 13: 1549-1556, 1994.
18. Sebastian, B., Kakizuka, A., and Hunter, T. Cdc25M2 activation of cyclin-dependent kinases by dephosphorylation of threonine-14 and tyrosine-15. Proc. Natl. Acad. Sci. USA, 90: 3521-3524, 1993.
19. Sexl, V., Diehl, J. A., Sherr, C. J., Ashmun, R., Beach, D., and Roussel, M. F. A rate-limiting function of cdc25A for S phase entry inversely correlates with tyrosine dephosphorylation of Cdk2. Oncogene, 18: 573-582, 1999.
20. Bernard, B. A., Bailly, C., Lenoir, M-C., Dadrmon, M., Thierry, F., and Yaniv, M. The human papillomavirus type 18 (HPV18) E2 gene product is a repressor of the HPV18 regulatory region in human keratinocytes. J. Virol., 63: 4317-4324, 1989.
21. Thierry, F., and Yaniv, M. The BPV1-E2 trans-acting protein can be either an activator or a represser of the HPV18 regulatory region. EMBO J., 6: 3391-3397, 1987.
22. Hwang, E., Riese, D. R., Settleman, J., Nilson, L., Honig, J., Flynn, S., and DiMaio, D. Inhibition of cervical carcinoma cell line proliferation by introduction of a bovine papillomavirus regulatory gene. J. Virol., 67: 3720-3729, 1993.
23. Dowhanick, J. J., McBride, A. A., and Howley, P. M. Suppression of cellular proliferation by the papillomavirus E2 protein. J. Virol., 69: 7791-7799, 1995.
24. Frattini, M. G., Hurst, S. D., Lim, H. B., Swaminathan, S., and Laimins, L. A. Abrogation of a mitotic checkpoint by E2 proteins from oncogenic human papillomaviruses correlates with increased turnover of the p53 tumor suppressor protein. EMBO J., 16: 318-331, 1997.
25. Desaintes, C., Demeret, C., Goyat, S., Yaniv, M., and Thierry, F. Expression of the papillomavirus E2 protein in HeLa cells leads to apoptosis. EMBO J., 16: 504-514, 1997.
26. Sanchez-Perez, A-M., Soriano, S., Clarke, A. R., and Gaston, K. Disruption of the human papillomavirus type 16 E2 gene protects cervical carcinoma cells from E2F-induced apoptosis. J. Gen. Virol., 78: 3009-3018, 1997.
27. Hwang, E-S., Naeger, L. K., and DiMaio, D. Activation of the endogenous p53 growth inhibitory pathway in HeLa cervical carcinoma cells by expression of the bovine papillomavirus E2 gene. Oncogene, 12: 795-803, 1996.
28. Crook, T., Marston, N. J., Sara, E. A., and Vousden, K. H. Transcriptional activation by p53 correlates with suppression of growth but not transformation. Cell, 79: 817-827, 1994.
29. Crook, T., Wrede, D., and Vousden, K. H. p53 point mutation in HPV-negative human cervical carcinoma cell lines. Oncogene, 6: 873-875, 1991.
30. Scheffner, M., Münger, K., Byrne, J. C., and Howley, P. M. The state of the p53 and retinoblastoma genes in human cervical carcinoma cell lines. Proc. Natl. Acad. Sci. USA, 88: 5523-5527, 1991.
31. Pater, M. M., and Pater, A. Human papiHomavirus types 16 and 18 sequences in carcinoma cell lines of the cervix. Virology, 145: 313-318, 1985.
32. Yee, C. I., Krishnan-Hewlett, I., Baker, C. C., Schlegel, R., and Howley, P. M. Presence and expression of human papillomavirus sequences in human cervical carcinoma cell lines. Am. J. Pathol., 119: 361-366, 1985.
33. Delius, H., and Hofmann, B. Primer-directed sequencing of human papiHomavirus types. Curr. Top. Microbiol. Immunol., 186: 13-31, 1994.
34. Varma, V. A., Sanchez-Lanier, M., Unger, E. R., Clark, C., Tickman, R., Hewan-Lowe, K., Chenggis, M. L., and Swan, D. C. Association of human papillomavirus with penile carcinoma: a study using polymerase chain reaction and in situ hybridization. Hum. Pathol., 22: 908-913, 1991.
35. Goodwin, E. C., Naeger, L. K., Breiding, D. E., Androphy, E. J., and DiMaio, D. Transactivation-competent bovine papillomavirus E2 protein is specifically required for efficient repression of human papillomavirus oncogene expression and for acute growth inhibition of cervical carcinoma cell lines. J. Virol., 72: 3925-3934, 1998.
36. Kip1. Mot. Cell. Biol., 15: 4347-4352, 1995.
37. Ewen, M. E., Sluss, H. K., Sherr, C. J., Matsushime, H., Kato, J., and Livingston, D. M. Functional interactions of the retinoblastoma protein with mammalian D-type cyclins. Cell, 73: 487-497, 1993.
38. 105 promoters. J. Virol., 64: 2849-2859, 1990.
39. 105 promoter. New Biol., 3: 90-100, 1991.
40. - loma virus-16 induces degradation of retinoblastoma protein through the ubiquitin-proteosome pathway. Cancer Res., 56: 4620-4624, 1996.
41. Demers, G. W., Foster, S. A., Halbert, C. L., and Galloway, D. A. 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, 1994.
42. 1 growth arrest pathway in cells expressing the human papillomavirus type 16 E7 oncoprotein. J. Virol., 71: 2905-2912, 1997.
43. Pines, J., and Hunter, T. Cyclins A and B1 in the human cell cycle. Ciba Found. Symp., 170: 187-204, 1992.
44. Pines, J., and Hunter, T. Human cyclin A is adenovirus E1A-associated protein p60 and behaves differently from cyclin B. Nature (Lond.), 346: 760-763, 1990.
45. Schulze, A., Zerfass, K., Spitkovsky, D., Berges, J., Middendorp, S., Jansen-Dürr, P., and Henglein, B. Cell cycle regulation of cyclin A gene transcription is mediated by a variant E2F binding site. Proc. Natl. Acad. Sci. USA, 92: 11264-11268, 1995.
46. Zerfass, K., Schulze, A., Spitkovsky, D., Friedman, V., Henglein, B., and Jansen-Durr, P. 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, 1995.
47. Zwicker, J., and Müller, R. Cell-cycle regulation of gene expression by transcriptional repression. Trends Genet., 13: 3-6, 1997.
48. Ohtani, K., DeGregori, J., and Nevins, J. R. Regulation of the cyclin E gene by transcription factor E2F1. Proc. Natl. Acad. Sci. USA, 92: 12146-12150, 1995.
49. Geng, G., Eaton, E. N., Picon, M., Roberts, J. M., Lundberg, A. S., Gifford, A., Sardet, C. and Weinberg, R. A. Regulation of cyclin E transcription by E2Fs and retinoblastoma protein. Oncogene, 12: 1173-1180.
50. Iavarone, A., and Massagué, J. E2F and histone deacetylase mediate transforming growth factor β repression of cdc25A during keratinocyte cell cycle arrest. Mol. Cell. Biol., 19: 916-922, 1999.
51. Girard, F., Strausfeld, U., Fernandez, A., and Lamb, N. J. C. Cyclin A is required for the onset of DNA replication in mammalian fibroblasts. Cell, 67: 1169-1179, 1991.
52. Pagano, M., Pepperkok, R., Verde, F., Ansorge, W., and Draetta, G. Cyclin A is required at two points in the human cell cycle. EMBO J., 11: 961-971, 1992.
53. Zindy, F., Lamas, E., Chenivesse, X., Sobczak, J., Wang, J., Fesquet, D., Henglein, B., and Brechot, C. Cyclin A is required in S phase in normal epithelial cells. Biochem. Biophys. Res. Commun., 182; 1144-1154, 1992.
54. Dynlacht, B. D., Flores, O., Lees, J. A., and Harlow, E. Differential regulation of E2F trans-activation by cyclin/cdk2 complexes. Genes Dev., 8: 1772-1786, 1994.
55. Spitkovsky, D., Jansen-Dürr, P., Karsenti, E., and Hoffmann, I. S-phase induction by adenovirus E1A requires activation of cdc25a tyrosine phosphatase. Oncogene, 12: 2549-2554, 1996.
56. Iavarone, A., and Massagué, J. Repression of the CDK activator Cdc25A and cell-cycle arrest by cytokine TGF-β in cells lacking the CDK inhibitor p15. Nature (Lond.), 387: 417-422, 1997.
57. 0-like arrest. Mol. Cell. Biol., 16: 3934-3944, 1996.
58. Buchmann, A. M., Swaminathan, S., and Thimmapaya, B. Regulation of cellular genes in a chromosomal context by the retinoblastoma tumor suppressor protein. Mol. Cell. Biol., 18: 4565-4576, 1998.
59. Funk, J. O., Waga, S., Harry, J. B., Espling, E., Stillman, B., and Galloway, D. A. Inhibition of CDK activity and PCNA-dependent DNA replication by p21 is blocked by interaction with the HPV-16 E7 onco-protein. Genes Dev., 11: 2090-2100, 1997.
60. Teodoro, J. G., and Branton, P. E. Regulation of apoptosis by viral gene products. J. Virol., 71: 1739-1746, 1997.
61. WAF1 is required for survival of differentiating neuroblastoma cells. Mol. Cell. Biol., 16: 1335-1341, 1996.
62. Polyak, K., Waldman, T., He, T-C., Kinzler, K. W., and Vogelstein, B. Genetic determinants of p53-induced apoptosis and growth arrest. Genes Dev., 10: 1945-1952, 1996.
63. Wang, J., and Walsh, K. Resistance to apoptosis conferred by cdk inhibitors during myocyte differentiation. Science (Washington DC), 273: 359-361, 1996.
64. Galaktionov, K., Chen, X., and Beach, D. Cdc25 cell-cycle phosphatase as a target of c-myc. Nature (Lond.), 382: 511-517, 1996.
65. Galaktionov, K., Lee, A. K., Eckstein, J., Draetta, G., Meckler, J., Loda, M., and Beach, D. CDC25 phosphatases as potential human oncogenes. Science (Washington DC), 269: 1575-1577, 1995.
66. Gasparotto, D., Maestro, R., Piccinin, S., Vukosavljevic, T., Barzan, L., Sulfaro, S., and Boiocchi, M. Overexpression of CDC25A and CDC25B in head and neck cancers. Cancer Res., 57: 2366-2368, 1997.
67. 1 in mammalian cells: inhibition of cyclin E-dependent kinase by TGF-β. Science (Washington DC), 260: 536-539, 1993.
68. Zhang, H., Hannon, G. J., and Beach, D. p21-containing cyclin kinases exist in both active and inactive states. Genes Dev., 8: 1750-1758, 1994.