The E6 Oncoproteins of High-Risk Papillomaviruses Bind to a Novel Putative GAP Protein, E6TP1, and Target It for Degradation

REFERENCES

• Altschuler, D. L., and J. Ribeiro-Neto 1998. Mitogenic and oncogenic properties of the small G protein Rap1b. Proc. Natl. Acad. Sci. USA 95:7475–7479.
   PubMed Web of Science ®Google Scholar
• Androphy, E. J., N. L. Hubbert, J. T. Schiller, and J. Lowy 1987. Identification of the HPV-16 E6 protein from transformed mouse cells and human cervical carcinoma cell lines. EMBO J. 6:989–992.
   PubMedGoogle Scholar
• Band, V., C. J. A. De, L. Delmolino, V. Kulesa, and J. Sager 1991. Loss of p53 protein in human papillomavirus type 16 E6-immortalized human mammary epithelial cells. J. Virol. 65:6671–6676.
   PubMedGoogle Scholar
• Band, V., D. Zajchowski, V. Kulesa, and J. Sager 1990. Human papilloma virus DNAs immortalize normal human mammary epithelial cells and reduce their growth factor requirements. Proc. Natl. Acad. Sci. USA 87:463–467.
   PubMed Web of Science ®Google Scholar
• Basu, T. N., D. H. Gutmann, J. A. Fletcher, T. W. Glover, F. S. Collins, and J. Downward 1992. Aberrant regulation of ras proteins in malignant tumour cells from type 1 neurofibromatosis patients. Nature 356:713–715.
   PubMed Web of Science ®Google Scholar
• Borg, J. P., J. Ooi, E. Levy, and J. Margolis 1996. The phosphotyrosine interaction domains of X11 and FE65 bind to distinct sites on the YENPTY motif of amyloid precursor protein. Mol. Cell. Biol. 16:6229–6241.
   PubMedGoogle Scholar
• Boyer, S. N., D. E. Wazer, and J. Band 1996. E7 protein of human papilloma virus-16 induces degradation of retinoblastoma protein through the ubiquitin-proteasome pathway. Cancer Res. 56:4620–4624.
   PubMed Web of Science ®Google Scholar
• Cao, Y., Q. Gao, D. E. Wazer, and J. Band 1997. Abrogation of wild-type p53-mediated transactivation is insufficient for mutant p53-induced immortalization of normal human mammary epithelial cells. Cancer Res. 57:5584–5589.
   PubMedGoogle Scholar
• Chen, F., M. Barkett, K. T. Ram, A. Quintanilla, and J. Hariharan 1997. Biological characterization of Drosophila Rapgap1, a GTPase activating protein for Rap1. Proc. Natl. Acad. Sci. USA 94:12485–12490.
   PubMedGoogle Scholar
• Chen, J. J., C. E. Reid, V. Band, and J. Androphy 1995. Interaction of papillomavirus E6 oncoproteins with a putative calcium-binding protein. Science 269:529–531.
   PubMed Web of Science ®Google Scholar
• Chenchik, A., F. Moqadam, P. Siebert 1996. A new method for full-length cDNA cloning by PCR, p. 273–321. In P. A. Krieg (ed.), A laboratory guide to RNA: isolation, analysis, and synthesis. John Wiley & Sons, Inc., New York, N.Y.
   Google Scholar
• Chien, C. T., P. L. Bartel, R. Sternglanz, and J. Fields 1991. The two-hybrid system: a method to identify and clone genes for proteins that interact with a protein of interest. Proc. Natl. Acad. Sci. USA 88:9578–9582.
   PubMed Web of Science ®Google Scholar
• Ciechanover, A. 1994. The ubiquitin-proteasome proteolytic pathway. Cell 79:13–21.
   PubMed Web of Science ®Google Scholar
• Dalal, S., Q. Gao, E. J. Androphy, and J. Band 1996. Mutational analysis of human papillomavirus type 16 E6 demonstrates that p53 degradation is necessary for immortalization of mammary epithelial cells. J. Virol. 70:683–688.
   PubMed Web of Science ®Google Scholar
• DeCaprio, J. A., J. W. Ludlow, J. Figge, J. Y. Shew, C. M. Huang, W. H. Lee, E. Marsilio, E. Paucha, and J. Livingston 1988. SV40 large tumor antigen forms a specific complex with the product of the retinoblastoma susceptibility gene. Cell 54:275–283.
   PubMed Web of Science ®Google Scholar
• Dib, C., S. Faure, C. Fizames, D. Samson, N. Drouot, A. Vignal, P. Millasseau, S. Marc, J. Hazan, E. Seboun, M. Lathrop, G. Gyapay, J. Morissette, and J. Weissenbach 1996. A comprehensive genetic map of the human genome based on 5,264 microsatellites. Nature 380:152–154.
   PubMed Web of Science ®Google Scholar
• Duclos, F., U. Boschert, G. Sirugo, J. L. Mandel, R. Hen, and J. Koenig 1993. Gene in the region of the Friedreich ataxia locus encodes a putative transmembrane protein expressed in the nervous system. Proc. Natl. Acad. Sci. USA 90:109–113.
   PubMedGoogle Scholar
• Dyson, N., R. Bernards, S. H. Friend, L. R. Gooding, J. A. Hassell, E. O. Major, J. M. Pipas, T. Vandyke, and J. Harlow 1990. Large T antigens of many polyomaviruses are able to form complexes with the retinoblastoma protein. J. Virol. 64:1353–1356.
   PubMed Web of Science ®Google Scholar
• Dyson, N., P. M. Howley, K. Munger, and J. Harlow 1989. The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science 243:934–937.
   PubMed Web of Science ®Google Scholar
• Frech, M., J. John, V. Pizon, P. Chardin, A. Tavitian, R. Clark, F. McCormick, and J. Wittinghofer 1990. Inhibition of GTPase activating protein stimulation of Ras-p21 GTPase by the Krev-1 gene product. Science 249:169–171.
   PubMed Web of Science ®Google Scholar
• Gao, Q., S. H. Hauser, X. L. Liu, D. E. Wazer, H. Madoc-Jones, and J. Band 1996. Mutant p53-induced immortalization of primary human mammary epithelial cells. Cancer Res. 56:3129–3133.
   PubMed Web of Science ®Google Scholar
• Gao, Q., and V. Band. Unpublished data.
   Google Scholar
• Hata, Y., A. Kikuchi, T. Sasaki, M. D. Schaber, J. B. Gibbs, and J. Takai 1990. Inhibition of the ras p21 GTPase-activating protein-stimulated GTPase activity of c-Ha-ras p21 by smg p21 having the same putative effector domain as ras p21s. J. Biol. Chem. 265:7104–7107.
   PubMed Web of Science ®Google Scholar
• Hattori, M., N. Tsukamoto, M. S. Nur-e-Kamal, B. Rubinfeld, K. Iwai, H. Kubota, H. Maruta, and J. Minato 1995. Molecular cloning of a novel mitogen-inducible nuclear protein with a Ran GTPase-activating domain that affects cell cycle progression. Mol. Cell. Biol. 15:552–560.
   PubMedGoogle Scholar
• Hawley-Nelson, P., K. H. Vousden, N. L. Hubbert, D. R. Lowy, and J. Schiller 1989. HPV16 E6 and E7 proteins cooperate to immortalize human foreskin keratinocytes. EMBO J. 8:3905–3910.
   PubMed Web of Science ®Google Scholar
• Herrmann, C., G. Horn, M. Spaargaren, and J. Wittinghofer 1996. Differential interaction of the ras family GTP-binding proteins H-Ras, Rap1A, and R-Ras with the putative effector molecules Raf kinase and Ral-guanine nucleotide exchange factor. J. Biol. Chem. 271:6794–6800.
   PubMed Web of Science ®Google Scholar
• Huibregtse, J. M., M. Scheffner, and J. Howley 1991. A cellular protein mediates association of p53 with the E6 oncoprotein of human papillomavirus type 16 or 18. EMBO J. 10:4129–4135.
   PubMed Web of Science ®Google Scholar
• Huibregtse, J. M., M. Scheffner, and J. Howley 1993. Cloning and expression of the cDNA for E6-AP, a protein that mediates the interaction of the human papillomavirus E6 oncoprotein with p53. Mol. Cell. Biol. 13:775–784.
   PubMed Web of Science ®Google Scholar
• Huibregtse, J. M., M. Scheffner, and J. Howley 1993. Localization of the E6-AP regions that direct human papillomavirus E6 binding, association with p53, and ubiquitination of associated proteins. Mol. Cell. Biol. 13:4918–4927.
   PubMed Web of Science ®Google Scholar
• Jin, F., R. Wienecke, G. H. Xiao, J. C. Maize Jr., J. E. DeClue, and J. Yeung 1996. Suppression of tumorigenicity by the wild-type tuberous sclerosis 2 (Tsc2) gene and its C-terminal region. Proc. Natl. Acad. Sci. USA 93:9154–9159.
   PubMedGoogle Scholar
• Kaur, P., and J. McDougall 1988. Characterization of primary human keratinocytes transformed by human papillomavirus type 18. J. Virol. 62:1917–1924.
   PubMed Web of Science ®Google Scholar
• Kitayama, H., Y. Sugimoto, T. Matsuzaki, Y. Ikawa, and J. Noda 1989. A ras-related gene with transformation suppressor activity. Cell 56:77–84.
   PubMed Web of Science ®Google Scholar
• Kiyono, T., A. Hiraiwa, M. Fujita, Y. Hayashi, T. Akiyama, and J. Ishibashi 1997. Binding of high-risk human papillomavirus E6 oncoproteins to the human homologue of the Drosophila discs large tumor suppressor protein. Proc. Natl. Acad. Sci. USA 94:11612–11616.
   PubMed Web of Science ®Google Scholar
• Kobayashi, T., H. Mitani, R. Takahashi, M. Hirabayashi, M. Ueda, H. Tamura, and J. Hino 1997. Transgenic rescue from embryonic lethality and renal carcinogenesis in the Eker rat model by introduction of a wild-type Tsc2 gene. Proc. Natl. Acad. Sci. USA 94:3990–3993.
   PubMedGoogle Scholar
• Kurachi, H., Y. Wada, N. Tsukamoto, M. Maeda, H. Kubota, M. Hattori, K. Iwai, and J. Minato 1997. Human SPA-1 gene product selectively expressed in lymphoid tissues is a specific GTPase-activating protein for Rap1 and Rap2. Segregate expression profiles from a rap1GAP gene product. J. Biol. Chem. 272:28081–28088.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Lee, S. S., R. S. Weiss, and J. Javier 1997. Binding of human virus oncoproteins to hDlg/SAP97, a mammalian homolog of the Drosophila discs large tumor suppressor protein. Proc. Natl. Acad. Sci. USA 94:6670–6675.
   PubMed Web of Science ®Google Scholar
• Levine, A. J. 1997. p53, the cellular gatekeeper for growth and division. Cell 88:323–331.
   PubMed Web of Science ®Google Scholar
• Maki, C. G., J. M. Huibregtse, and J. Howley 1996. In vivo ubiquitination and proteasome-mediated degradation of p53. Cancer Res. 56:2649–2654.
   PubMed Web of Science ®Google Scholar
• Menon, A. G., J. L. Rutter, J. P. von Sattel, H. Synder, C. Murdoch, A. Blumenfeld, R. L. Martuza, A. von Deimling, J. F. Gusella, and J. Houseal 1997. Frequent loss of chromosome 14 in atypical and malignant meningioma: identification of a putative ‘tumor progression’ locus. Oncogene 14:611–616.
   PubMed Web of Science ®Google Scholar
• Munger, K., W. C. Phelps, V. Bubb, P. M. Howley, and J. Schlegel 1989. The E6 and E7 genes of the human papillomavirus type 16 together are necessary and sufficient for transformation of primary human keratinocytes. J. Virol. 63:4417–4421.
   PubMed Web of Science ®Google Scholar
• Munger, K., B. A. Werness, N. Dyson, W. C. Phelps, E. Harlow, and J. Howley 1989. Complex formation of human papillomavirus E7 proteins with the retinoblastoma tumor suppressor gene product. EMBO J. 8:4099–4105.
   PubMed Web of Science ®Google Scholar
• Pirisi, L., S. Yasumoto, M. Feller, J. Doniger, and J. DiPaolo 1987. Transformation of human fibroblasts and keratinocytes with human papillomavirus type 16 DNA. J. Virol. 61:1061–1066.
   PubMed Web of Science ®Google Scholar
• Polakis, P., B. Rubinfeld, and J. McCormick 1992. Phosphorylation of rap1GAP in vivo and by cAMP-dependent kinase and the cell cycle p34cdc2 kinase in vitro. J. Biol. Chem. 267:10780–10785.
   PubMedGoogle Scholar
• Ponting, C. P., C. Phillips, K. E. Davies, and J. Blake 1997. PDZ domains: targeting signalling molecules to sub-membranous sites. Bioessays 19:469–479.
   PubMedGoogle Scholar
• Rubinfeld, B., W. J. Crosier, I. Albert, L. Conroy, R. Clark, F. McCormick, and J. Polakis 1992. Localization of the rap1GAP catalytic domain and sites of phosphorylation by mutational analysis. Mol. Cell. Biol. 12:4634–4642.
   PubMedGoogle Scholar
• Rubinfeld, B., S. Munemitsu, R. Clark, L. Conroy, K. Watt, W. J. Crosier, F. McCormick, and J. Polakis 1991. Molecular cloning of a GTPase activating protein specific for the Krev-1 protein p21rap1. Cell 65:1033–1042.
   PubMed Web of Science ®Google Scholar
• Scheffner, M., J. M. Huibregtse, R. D. Vierstra, and J. 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.
   PubMed Web of Science ®Google Scholar
• Scheffner, M., B. A. Werness, J. M. Huibregtse, A. J. Levine, and J. Howley 1990. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 63:1129–1136.
   PubMed Web of Science ®Google Scholar
• Schuler, G. D., M. S. Boguski, E. A. Stewart, L. D. Stein, G. Gyapay, K. Rice, R. E. White, P. Rodriguez-Tome, A. Aggarwal, E. Bajorek, S. Bentolila, B. B. Birren, A. Butler, A. B. Castle, N. Chiannilkulchai, A. Chu, C. Clee, S. Cowles, P. J. Day, T. Dibling, N. Drouot, I. Dunham, S. Duprat, C. East, T. J. Hudson et al.. 1996. A gene map of the human genome. Science 274:540–546.
   PubMed Web of Science ®Google Scholar
• Simon, M., A. von Deimling, J. J. Larson, R. Wellenreuther, P. Kaskel, A. Waha, R. E. Warnick, J. M. Tew Jr., and J. Menon 1995. Allelic losses on chromosomes 14, 10, and 1 in atypical and malignant meningiomas: a genetic model of meningioma progression. Cancer. Res. 55:4696–4701.
   PubMed Web of Science ®Google Scholar
• Stubdal, H., J. Zalvide, K. S. Campbell, C. Schweitzer, T. M. Roberts, and J. DeCaprio 1997. Inactivation of pRB-related proteins p130 and p107 mediated by the J domain of simian virus 40 large T antigen. Mol. Cell. Biol. 17:4979–4990.
   PubMedGoogle Scholar
• The European Chromosome 16 Tuberous Sclerosis Consortium. 1993. Identification and characterization of the tuberous sclerosis gene on chromosome 16. Cell 75:1305–1315.
   PubMedGoogle Scholar
• Tong, X., and J. Howley 1997. The bovine papillomavirus E6 oncoprotein interacts with paxillin and disrupts the actin cytoskeleton. Proc. Natl. Acad. Sci. USA 94:4412–4417.
   PubMedGoogle Scholar
• Tse, J. Y., H. K. Ng, K. M. Lau, K. W. Lo, W. S. Poon, and J. Huang 1997. Loss of heterozygosity of chromosome 14q in low- and high-grade meningiomas. Hum. Pathol. 28:779–785.
   PubMed Web of Science ®Google Scholar
• Vossler, M. R., H. Yao, R. D. York, M. G. Pan, C. S. Rim, and J. Stork 1997. cAMP activates MAP kinase and Elk-1 through a B-Raf- and Rap1-dependent pathway. Cell 89:73–82.
   PubMed Web of Science ®Google Scholar
• Wazer, D. E., X. L. Liu, Q. Chu, Q. Gao, and J. Band 1995. Immortalization of distinct human mammary epithelial cell types by human papilloma virus 16 E6 or E7. Proc. Natl. Acad. Sci. USA 92:3687–3691.
   PubMed Web of Science ®Google Scholar
• Weinberg, R. A. 1995. The retinoblastoma protein and cell cycle control. Cell 81:323–330.
   PubMed Web of Science ®Google Scholar
• Werness, B. A., A. J. Levine, and J. Howley 1990. Association of human papillomavirus types 16 and 18 E6 proteins with p53. Science 248:76–79.
   PubMed Web of Science ®Google Scholar
• Whyte, P., K. J. Buchkovich, J. M. Horowitz, S. H. Friend, M. Raybuck, R. A. Weinberg, and J. Harlow 1988. Association between an oncogene and an anti-oncogene: the adenovirus E1A proteins bind to the retinoblastoma gene product. Nature 334:124–129.
   PubMed Web of Science ®Google Scholar
• Wienecke, R., A. Konig, and J. DeClue 1995. Identification of tuberin, the tuberous sclerosis-2 product. Tuberin possesses specific Rap1GAP activity. J. Biol. Chem. 270:16409–16414.
   PubMed Web of Science ®Google Scholar
• Woodworth, C. D., J. Doniger, and J. DiPaolo 1989. Immortalization of human foreskin keratinocytes by various human papillomavirus DNAs corresponds to their association with cervical carcinoma. J. Virol. 63:159–164.
   PubMed Web of Science ®Google Scholar
• Xiao, G. H., F. Shoarinejad, F. Jin, E. A. Golemis, and J. Yeung 1997. The tuberous sclerosis 2 gene product, tuberin, functions as a Rab5 GTPase activating protein (GAP) in modulating endocytosis. J. Biol. Chem. 272:6097–6100.
   PubMed Web of Science ®Google Scholar
• Yeung, R. S., G. H. Xiao, F. Jin, W. C. Lee, J. R. Testa, and J. Knudson 1994. Predisposition to renal carcinoma in the Eker rat is determined by germ-line mutation of the tuberous sclerosis 2 (TSC2) gene. Proc. Natl. Acad. Sci. USA 91:11413–11416.
   PubMed Web of Science ®Google Scholar
• Yoshida, Y., M. Kawata, Y. Miura, T. Musha, T. Sasaki, A. Kikuchi, and J. Takai 1992. Microinjection of smg/rap1/Krev-1 p21 into Swiss 3T3 cells induces DNA synthesis and morphological changes. Mol. Cell. Biol. 12:3407–3414.
   PubMedGoogle Scholar
• Zur Hausen, H. 1987. Papillomaviruses in human cancer. Appl. Pathol. 5:19–24.
   PubMedGoogle Scholar
• Zur Hausen, H., and J. Schneider 1987. The Papillomaviruses The papovaviridae In P. M. Howley, N. P. Salzman (ed.), 2:245–263 Plenum, New York, N.Y.
   Google Scholar