E2F-Rb Complexes Assemble and Inhibit cdc25A Transcription in Cervical Carcinoma Cells following Repression of Human Papillomavirus Oncogene Expression

REFERENCES

• Berezutskaya, E., Yu, B., Morozov, A., Raychaudhuri, P., and Bagchi, S.. 1997. Differential regulation of the pocket domains of the retinoblastoma family proteins by the HPV16 E7 oncoprotein. Cell Growth Differ. 8:1277–1286
   PubMedGoogle Scholar
• Bernard, B. A., Bailly, C., Lenoir, M.-C., Darmon, M., Thierry, F., and Yaniv, M.. 1989. 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
   PubMedGoogle Scholar
• Boyer, S. N., Wazer, D. E., and Band, V.. 1996. E7 protein of human papilloma virus-16 induces degradation of retinoblastoma protein through the ubiquitin-proteosome pathway. Cancer Res. 56:4620–4624
   PubMed Web of Science ®Google Scholar
• Chellappan, S., Kraus, V. B., Kroger, B., Münger, K., Howley, P. M., Phelps, W. C., and Nevins, J. R.. 1992. Adenovirus E1A, simian virus 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
   PubMed Web of Science ®Google Scholar
• Chen, X., and Prywes, R.. 1999. Serum-induced expression of the cdc25A gene by relief of E2F-mediated repression. Mol. Cell. Biol. 19:4695–4702
   PubMed Web of Science ®Google Scholar
• Cobrinik, D., Whyte, P., Peeper, D. S., Jacks, T., and Weinberg, R. A.. 1993. Cell cycle-specific association of E2F with the p130 E1A-binding protein. Genes Dev. 7:2392–2404
   PubMed Web of Science ®Google Scholar
• Crook, T., Wrede, D., and Vousden, K. H.. 1991. p53 point mutation in HPV-negative human cervical carcinoma cell lines. Oncogene 6:873–875
   PubMed Web of Science ®Google Scholar
• DeGregori, J., Leone, G., Miron, A., Jakoi, L., and Nevins, J. R.. 1997. Distinct roles for E2F proteins in cell growth control and apoptosis. Proc. Natl. Acad. Sci. USA 94:7245–7250
   PubMed Web of Science ®Google Scholar
• DeGregori, J., Kowalik, T., and Nevins, J. R.. 1995. Cellular targets for activation by the E2F1 transcription factor include DNA synthesis and G1/S regulatory genes. Mol. Cell. Biol. 15:4215–4224
   PubMed Web of Science ®Google Scholar
• Demers, G., Espling, E., Harry, J., Etscheid, B., and Galloway, D.. 1996. Abrogation of growth arrest signals by human papillomavirus type 16E7 is mediated by sequences required for transformation. J. Virol. 70:6862–6869
   PubMedGoogle Scholar
• Demers, G. W., Foster, S. A., Halbert, C. L., and Galloway, D. A.. 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
   PubMed Web of Science ®Google Scholar
• Desaintes, C., Demeret, C., Goyat, S., Yaniv, M., and Thierry, F.. 1997. Expression of the papillomavirus E2 protein in HeLa cells leads to apoptosis. EMBO J. 16:504–514
   PubMed Web of Science ®Google Scholar
• Dowhanick, J. J., McBride, A. A., and Howley, P. M.. 1995. Suppression of cellular proliferation by the papillomavirus E2 protein. J. Virol. 69:7791–7799
   PubMedGoogle Scholar
• Draetta, G., and Eckstein, J.. 1997. Cdc25 protein phosphatases in cell proliferation. Biochim. Biophys. Acta 1332:M53–M63
   PubMed Web of Science ®Google Scholar
• Dyson, N.. 1998. The regulation of E2F by pRB-family proteins. Genes Dev. 12:2245–2262
   PubMed Web of Science ®Google Scholar
• Dyson, N., Howley, P., Münger, K., and Harlow, E.. 1989. The human papillomavirus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science 243:934–936
   PubMed Web of Science ®Google Scholar
• Francis, D. A., Schmid, S. I., and Howley, P. M.. 2000. Repression of the integrated papillomavirus E6/E7 promoter is required for growth suppression of cervical cancer cells. J. Virol. 74:2679–2686
   PubMed Web of Science ®Google Scholar
• Galaktionov, K., Chen, X., and Beach, D.. 1996. Cdc25 cell-cycle phosphatase as a target of c-myc. Nature 382:511–517
   PubMed Web of Science ®Google Scholar
• Ginsberg, D., Vairo, G., Chittenden, T., Xiao, Z. X., Xu, G., Wydner, K. L., DeCaprio, J. A., Lawrence, J. B., and Livingston, D. M.. 1994. E2F-4, a new member of the E2F transcription factor family, interacts with p107. Genes Dev. 8:2665–2679
   PubMed Web of Science ®Google Scholar
• Goodwin, E. C., Naeger, L. K., Breiding, D. E., Androphy, E. J., and DiMaio, D.. 1998. 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
   PubMedGoogle Scholar
• Hamel, P. A., Gill, R. M., Phillips, R. A., and Gallie, B. L.. 1992. Transcriptional repression of the E2-containing promoters EIIaE, c-myc, and RB1 by the product of the RB1 gene. Mol. Cell. Biol. 12:3431–3438
   PubMed Web of Science ®Google Scholar
• Hateboer, G., Kerkhoven, R. M., Shvarts, A., Bernards, R., and Beijersbergen, R. L.. 1996. Degradation of E2F by the ubiquitin-proteasome pathway: regulation by retinoblastoma family proteins and adenovirus transforming proteins. Genes Dev. 10:2960–2970
   PubMed Web of Science ®Google Scholar
• Havre, P. A., Yuan, J., Hedrick, L., Cho, K. R., and Glazer, P. M.. 1995. p53 inactivation by HPV16 E6 results in increased mutagenesis in human cells. Cancer Res. 55:4420–4424
   PubMed Web of Science ®Google Scholar
• Hickman, E., Picksley, S., and Vousden, K.. 1994. Cells expressing HPV16 E7 continue cycle progression following DNA damage-induced p53 activation. Oncogene 9:2177–2181
   PubMed Web of Science ®Google Scholar
• Hiebert, S., Chellappan, S., Horowitz, J., and Nevins, J.. 1992. The interaction of Rb with E2F coincides with an inhibition of the transcriptional activity of E2F. Genes Dev. 6:177–185
   PubMed Web of Science ®Google Scholar
• Hofmann, F., Martelli, F., Livingston, D. M., and Wang, Z.. 1996. The retinoblastoma gene product protects E2F1 from degradation by the ubiquitin-proteasome pathway. Genes Dev. 10:2949–2959
   PubMed Web of Science ®Google Scholar
• Hsiao, K., McMahon, S. L., and Farnham, P. J.. 1994. Multiple DNA elements are required for the growth regulation of the mouse E2F1 promoter. Genes Dev. 8:1526–1537
   PubMed Web of Science ®Google Scholar
• Hurford, R. K.Jr., Cobrinik, D., Lee, M. H., and Dyson, N.. 1997. pRB and p107/p130 are required for the regulated expression of different sets of E2F responsive genes. Genes Dev. 11:1447–1463
   PubMed Web of Science ®Google Scholar
• Hwang, E.-S., Naeger, L. K., and DiMaio, D.. 1996. 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
   PubMedGoogle Scholar
• Hwang, E.-S., Riese, D. J.II, Settleman, J., Nilson, L. A., Honig, J., Flynn, S., and DiMaio, D.. 1993. Inhibition of cervical carcinoma cell line proliferation by introduction of a bovine papillomavirus regulatory gene. J. Virol. 67:3720–3729
   PubMedGoogle Scholar
• Iavarone, A., and Massague, J.. 1999. E2F and histone deacetylase mediate transforming growth factor β repression of cdc25A during keratinocyte cell cycle arrest. Mol. Cell. Biol. 19:916–922
   PubMed Web of Science ®Google Scholar
• Ikeda, M.-A., Jakoi, L., and Nevins, J. R.. 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
   PubMedGoogle Scholar
• Johnson, D. G., Ohtani, K., and Nevins, J. R.. 1994. Autoregulatory control of E2F1 expression in response to positive and negative regulators of cell cycle progression. Genes Dev. 8:1514–1525
   PubMed Web of Science ®Google Scholar
• Jones, D. L., and Münger, K.. 1997. Analysis of the p53-mediated G1 growth arrest pathway in cells expressing the human papillomavirus type 16 E7 oncoprotein. J. Virol. 71:2905–2912
   PubMedGoogle Scholar
• Lam, E. W., and Watson, R. J.. 1993. An E2F-binding site mediates cell-cycle regulated repression of mouse B-myb transcription. EMBO J. 12:2705–2713
   PubMed Web of Science ®Google Scholar
• Li, J.-M., Hu, P. P.-C., Shen, X., Yu, Y., and Wang, X.-F.. 1997. E2F4-RB and E2F4-p107 complexes suppress gene expression by transforming growth factor β through E2F binding sites. Proc. Natl. Acad. Sci. USA 94:4948–4953
   PubMedGoogle Scholar
• Lindeman, G. J., Gaubatz, S., Livingston, D. M., and Ginsberg, D.. 1997. The subcellular localization of E2F-4 is cell-cycle dependent. Proc. Natl. Acad. Sci. USA 94:5095–5100
   PubMedGoogle Scholar
• Magae, J., Wu, C. L., Illenye, S., Harlow, E., and Heintz, N. H.. 1996. Nuclear localization of DP and E2F transcription factors by heterodimeric partners and retinoblastoma protein family members. J. Cell Sci. 109:1717–1726
   PubMedGoogle Scholar
• Moberg, K., Starz, M. A., and Lees, J. A.. 1996. E2F-4 switches from p130 to p107 and pRB in response to cell cycle reentry. Mol. Cell. Biol. 16:1436–1449
   PubMed Web of Science ®Google Scholar
• Morkel, M., Wenkel, J., Bannister, A. J., Kouzarides, T., and Hagemeier, C.. 1997. An E2F-like repressor of transcription. Nature 390:567–568
   PubMedGoogle Scholar
• Naeger, L. K., Goodwin, E. C., Hwang, E.-S., DeFilippis, R. A., Zhang, H., and DiMaio, D.. 1999. 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 Differ. 10:413–422
   PubMedGoogle Scholar
• Neuman, E., Flemington, E. K., Sellers, W. R., Kaelin, W. G.Jr.. 1994. Transcription of the E2F-1 gene is rendered cell cycle dependent by E2F DNA-binding sites within its promoter. Mol. Cell. Biol. 14:6607–6615
   PubMed Web of Science ®Google Scholar
• Nevins, J. R.. 1998. Toward an understanding of the functional complexity of the E2F and retinoblastoma families. Cell Growth Differ. 9:585–593
   PubMedGoogle Scholar
• Nevins, J. R.. 1992. E2F: a link between the Rb tumor suppressor protein and viral oncoproteins. Science 258:424–429
   PubMed Web of Science ®Google Scholar
• Romanczuk, H., Thierry, F., and Howley, P. M.. 1990. Mutations analysis of cis elements involved in E2 modulation of human papillomavirus type 16 P97 and type 18 P105 promoters. J. Virol. 64:2849–2859
   PubMed Web of Science ®Google Scholar
• Scheffner, M., Münger, K., Byrne, J. C., and Howley, P. M.. 1991. The state of the p53 and retinoblastoma genes in human cervical carcinoma cell lines. Proc. Natl. Acad. Sci. USA 88:5523–5527
   PubMed Web of Science ®Google Scholar
• Scheffner, M., Huibregtse, J. M., Vierstra, R. D., and Howley, P. M.. 1993. The HPV-16 E6 and EP-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell 75:495–505
   PubMed Web of Science ®Google Scholar
• Schulze, A., Zerfass, K., Spitkovsky, D., Berges, J., Middendorp, S., Jansen-Dürr, P., and Henglein, B.. 1995. Cell cycle regulation of cyclin A gene transcription is mediated by a variant E2F binding site. Proc. Natl. Acad. Sci. USA 92:11264–11268
   PubMedGoogle Scholar
• Sidle, A., Palaty, C., Dirks, P., Wiggan, O'N., Kiess, M., Gill, R. M., Wong, A. K., and Hamel, P. A.. 1996. Activity of the retinoblastoma family proteins, pRB, p107, and p130, during cellular proliferation and differentiation. Crit. Rev. Biochem. Mol. Biol. 31:237–271
   PubMed Web of Science ®Google Scholar
• Slebos, R., Lee, M., Plunkett, B., Kessis, T., Williams, B., Jacks, T., Hedrick, L., Kastan, M., and Cho, K.. 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
   PubMed Web of Science ®Google Scholar
• Smith, E. J., Leone, G., DeGregori, J., Jakoi, L., and Nevins, J. R.. 1996. The accumulation of an E2F-p130 transcriptional repressor distinguishes a G0 cell state from a G1 cell state. Mol. Cell. Biol. 16:6965–6976
   PubMed Web of Science ®Google Scholar
• Thomas, N. S. B., Pizzey, A. R., Tiwari, S., Williams, C. D., and Yang, J.. 1998. p130, p107, and pRB are differentially regulated in proliferating cells and during cell cycle arrest by α-interferon. J. Biol. Chem. 273:23659–23667
   PubMed Web of Science ®Google Scholar
• Tommasi, S., and Pfeifer, G. P.. 1995. In vivo structure of the human cdc2 promoter: release of a p130–E2F-4 complex from sequences immediately upstream of the transcription initiation site coincides with induction of cdc2 expression. Mol. Cell. Biol. 15:6901–6913
   PubMedGoogle Scholar
• Vairo, G., Livingston, D. M., and Ginsberg, D.. 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
   PubMed Web of Science ®Google Scholar
• Vigo, E., Müller, H., Prosperini, E., Hateboer, G., Cartwright, P., Moroni, M. C., and Helin, K.. 1999. CDC25A phosphatase is a target of E2F and is required for efficient E2F-induced S phase. Mol. Cell. Biol. 19:6379–6395
   PubMed Web of Science ®Google Scholar
• Villa, L. L.. 1997. Human papillomaviruses and cervical cancer. Adv. Cancer Res. 71:321–341
   PubMed Web of Science ®Google Scholar
• Weintraub, S. J., Chow, K. N., Luo, R. X., Zhang, S. H., He, S., and Dean, D. C.. 1995. Mechanism of active transcriptional repression by the retinoblastoma protein. Nature 375:812–815
   PubMed Web of Science ®Google Scholar
• Weintraub, S. J., Prater, C. A., and Dean, D. C.. 1992. Retinoblastoma protein switches the E2F site from positive to negative element. Nature 358:259–261
   PubMed Web of Science ®Google Scholar
• White, A. E., Livanos, E. M., and Tlsty, T. D.. 1994. Differential disruption of genomic integrity and cell cycle regulation in normal human fibroblasts by the HPV oncoprotein. Genes Dev. 8:666–677
   PubMed Web of Science ®Google Scholar
• Zerfass, K., Schulze, A., Spitkovsky, D., Friedman, V., Henglein, B., and Jansen-Durr, P.. 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
   PubMedGoogle Scholar
• Zwicker, J., Liu, N., Engeland, K., Lucibello, F. C., and Muller, R.. 1996. Cell cycle regulation of E2F site occupation in vivo. Science 271:1595–1596
   PubMed Web of Science ®Google Scholar