The biological properties of E6 and E7 oncoproteins from human papillomaviruses (original) (raw)

References

  1. E.M. de Villiers, C. Fauquet, T.R. Broker, H.U. Bernard, H. zur Hausen, Classification of papillomaviruses. Virology 324, 17 (2004)
    Article PubMed CAS Google Scholar
  2. H. zur Hausen, Papillomaviruses and cancer: from basic studies to clinical application. Nat. Rev. Cancer 2, 342 (2002)
    Article CAS PubMed Google Scholar
  3. Z. Chen, M. Schiffman, R. Herrero, R. Desalle, R.D. Burk, Human papillomavirus (HPV) types 101 and 103 isolated from cervicovaginal cells lack an E6 open reading frame (ORF) and are related to gamma-papillomaviruses. Virology 360, 447 (2007)
    Article CAS PubMed Google Scholar
  4. R.J. Nobre, E. Herraez-Hernandez, J.W. Fei, L. Langbein, S. Kaden, H.J. Grone, E.M. de Villiers, E7 oncoprotein of novel human papillomavirus type 108 lacking the E6 gene induces dysplasia in organotypic keratinocyte cultures. J. Virol. 83, 2907 (2009)
    Article CAS PubMed PubMed Central Google Scholar
  5. N. Munoz, F.X. Bosch, S. de Sanjose, R. Herrero, X. Castellsague, K.V. Shah, P.J. Snijders, C.J. Meijer, Epidemiologic classification of human papillomavirus types associated with cervical cancer. N. Engl. J. Med. 348, 518 (2003)
    Article PubMed Google Scholar
  6. J.S. Smith, L. Lindsay, B. Hoots, J. Keys, S. Franceschi, R. Winer, G.M. Clifford, Human papillomavirus type distribution in invasive cervical cancer and high-grade cervical lesions: a meta-analysis update. Int. J. Cancer 121, 621 (2007)
    Article CAS PubMed Google Scholar
  7. A.R. Kreimer, G.M. Clifford, P. Boyle, S. Franceschi, Human papillomavirus types in head and neck squamous cell carcinomas worldwide: a systematic review. Cancer Epidemiol. Biomarkers Prev. 14, 467 (2005)
    Article CAS PubMed Google Scholar
  8. A.G. Ostor, Natural history of cervical intraepithelial neoplasia: a critical review. Int. J. Gynecol. Pathol. 12, 186 (1993)
    Article CAS PubMed Google Scholar
  9. N. Jones, Transcriptional regulation by dimerization: two sides to an incestuous relationship. Cell 61, 9 (1990)
    Article CAS PubMed Google Scholar
  10. P.K. Magnusson, P. Sparen, U.B. Gyllensten, Genetic link to cervical tumours. Nature 400, 6729 (1999)
    Article CAS Google Scholar
  11. V. Moreno, N. Munoz, F.X. Bosch, S. de Sanjose, L.C. Gonzalez, L. Tafur, M. Gili, I. Izarzugaza, C. Navarro, A. Vergara et al., Risk factors for progression of cervical intraepithelial neoplasm grade III to invasive cervical cancer. Cancer Epidemiol. Biomarkers Prev. 4, 459 (1995)
    CAS PubMed Google Scholar
  12. V. Moreno, F.X. Bosch, N. Munoz, C.J. Meijer, K.V. Shah, J.M. Walboomers, R. Herrero, S. Franceschi, Effect of oral contraceptives on risk of cervical cancer in women with human papillomavirus infection: the IARC multicentric case-control study. Lancet 359, 1085 (2002)
    Article CAS PubMed Google Scholar
  13. N. Munoz, S. Franceschi, C. Bosetti, V. Moreno, R. Herrero, J.S. Smith, K.V. Shah, C.J. Meijer, F.X. Bosch, Role of parity and human papillomavirus in cervical cancer: the IARC multicentric case-control study. Lancet 359, 1093 (2002)
    Article PubMed Google Scholar
  14. M.H. Schiffman, N.J. Haley, J.S. Felton, A.W. Andrews, R.A. Kaslow, W.D. Lancaster, R.J. Kurman, L.A. Brinton, L.B. Lannom, D. Hoffmann, Biochemical epidemiology of cervical neoplasia: measuring cigarette smoke constituents in the cervix. Cancer Res. 47, 3886 (1987)
    CAS PubMed Google Scholar
  15. H. Pfister, Chapter 8: human papillomavirus and skin cancer. J. Natl. Cancer Inst. Monogr. 31, 52 (2003)
    Article Google Scholar
  16. M.N. de Koning, S.J. Weissenborn, D. Abeni, J.N. Bouwes Bavinck, S. Euvrard, A.C. Green, C.A. Harwood, L. Naldi, R. Neale, I. Nindl, C.M. Proby, W.G. Quint, F. Sampogna, J. Ter Schegget, L. Struijk, U. Wieland, H.J. Pfister, M.C. Feltkamp, Prevalence and associated factors of betapapillomavirus infections in individuals without cutaneous squamous cell carcinoma. J. Gen. Virol. 90, 1611 (2009)
    Article PubMed CAS Google Scholar
  17. H.N. Ananthaswamy, S.M. Loughlin, P. Cox, R.L. Evans, S.E. Ullrich, M.L. Kripke, Sunlight and skin cancer: inhibition of p53 mutations in UV-irradiated mouse skin by sunscreens. Nat. Med. 3, 510 (1997)
    Article CAS PubMed Google Scholar
  18. B.K. Armstrong, A. Kricker, The epidemiology of UV induced skin cancer. J. Photochem. Photobiol. B 63, 8 (2001)
    Article CAS PubMed Google Scholar
  19. D.S. Preston, R.S. Stern, Nonmelanoma cancers of the skin. N. Engl. J. Med. 327, 1649 (1992)
    Article CAS PubMed Google Scholar
  20. C. Ateenyi-Agaba, E. Weiderpass, A. Smet, W. Dong, M. Dai, B. Kahwa, H. Wabinga, E. Katongole-Mbidde, S. Franceschi, M. Tommasino, Epidermodysplasia verruciformis human papillomavirus types and carcinoma of the conjunctiva: a pilot study. Br. J. Cancer 90, 1777 (2004)
    Article CAS PubMed PubMed Central Google Scholar
  21. R. Newton, A review of the aetiology of squamous cell carcinoma of the conjunctiva. Br. J. Cancer 74, 1511 (1996)
    Article CAS PubMed PubMed Central Google Scholar
  22. E. Schwarz, U.K. Freese, L. Gissmann, W. Mayer, B. Roggenbuck, A. Stremlau, H. zur Hausen, Structure and transcription of human papillomavirus sequences in cervical carcinoma cells. Nature 314, 111 (1985)
    Article CAS PubMed Google Scholar
  23. N. Wentzensen, S. Vinokurova, M. von Knebel Doeberitz, Systematic review of genomic integration sites of human papillomavirus genomes in epithelial dysplasia and invasive cancer of the female lower genital tract. Cancer Res. 64, 3878 (2004)
    Article CAS PubMed Google Scholar
  24. L.M. Alvarez-Salas, J.A. DiPaolo, Molecular approaches to cervical cancer therapy. Curr. Drug Discov. Technol. 4, 208 (2007)
    Article CAS PubMed Google Scholar
  25. M. Tommasino, L. Crawford, Human papillomavirus E6 and E7: proteins which deregulate the cell cycle. Bioessays 17, 509 (1995)
    Article CAS PubMed Google Scholar
  26. P.F. Lambert, S.J. Balsitis, A. Shai, S.J.S. Simonson, S.M.G. Williams, Transgenic mouse models for the in vivo analysis of papillomavirus oncogene function, in Papillomavirus Research: From Natural History to Vaccine and Beyond, ed. by M. Saveria Campo (Caister Academic Press, Norfolk, 2006), pp. 213–228
    Google Scholar
  27. M. Tommasino, R. Accardi, S. Caldeira, W. Dong, I. Malanchi, A. Smet, I. Zehbe, The role of TP53 in cervical carcinogenesis. Hum. Mutat. 21, 307 (2003)
    Article CAS PubMed Google Scholar
  28. J.M. Huibregtse, M. Scheffner, P.M. Howley, A cellular protein mediates association of p53 with the E6 oncoprotein of human papillomavirus types 16 or 18. EMBO J. 10, 4129 (1991)
    Article CAS PubMed PubMed Central Google Scholar
  29. M. Scheffner, B.A. Werness, J.M. Huibregtse, A.J. Levine, P.M. Howley, The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 63, 1129 (1990)
    Article CAS PubMed Google Scholar
  30. M. Scheffner, J.M. Huibregtse, R.D. Vierstra, P.M. Howley, The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell 75, 495 (1993)
    Article CAS PubMed Google Scholar
  31. P. Massimi, A. Shai, P. Lambert, L. Banks, HPV E6 degradation of p53 and PDZ containing substrates in an E6AP null background. Oncogene 27, 1800 (2008)
    Article CAS PubMed Google Scholar
  32. T. Hiller, S. Poppelreuther, F. Stubenrauch, T. Iftner, Comparative analysis of 19 genital human papillomavirus types with regard to p53 degradation, immortalization, phylogeny, and epidemiologic risk classification. Cancer Epidemiol. Biomarkers Prev. 15, 1262 (2006)
    Article CAS PubMed Google Scholar
  33. M.S. Lechner, L.A. Laimins, Inhibition of p53 DNA binding by human papillomavirus E6 proteins. J. Virol. 68, 4262 (1994)
    CAS PubMed PubMed Central Google Scholar
  34. K. Butz, C. Denk, A. Ullmann, M. Scheffner, F. Hoppe-Seyler, Induction of apoptosis in human papillomaviruspositive cancer cells by peptide aptamers targeting the viral E6 oncoprotein. Proc. Natl. Acad. Sci. USA 97, 6693 (2000)
    Article CAS PubMed Google Scholar
  35. H.C. Pan, A.E. Griep, Temporally distinct patterns of p53-dependent and p53-independent apoptosis during mouse lens development. Genes Dev. 9, 2157 (1995)
    Article CAS PubMed Google Scholar
  36. A.E. White, E.M. Livanos, T.D. Tlsty, Differential disruption of genomic integrity and cell cycle regulation in normal human fibroblasts by the HPV oncoproteins. Genes Dev. 8, 666 (1994)
    Article CAS PubMed Google Scholar
  37. U.M. Moll, S. Erster, A. Zaika, p53, p63 and p73—solos, alliances and feuds among family members. Biochim. Biophys. Acta 1552, 47 (2001)
    CAS PubMed Google Scholar
  38. J.S. Park, E.J. Kim, J.Y. Lee, H.S. Sin, S.E. NamKoong, S.J. Um, Functional inactivation of p73, a homolog of p53 tumor suppressor protein, by human papillomavirus E6 proteins. Int. J. Cancer 91, 822 (2001)
    Article CAS PubMed Google Scholar
  39. M.C. Marin, C.A. Jost, M.S. Irwin, J.A. DeCaprio, D. Caput, W. G. Kaelin Jr., Viral oncoproteins discriminate between p53 and the p53 homolog p73. Mol. Cell. Biol. 18, 6316 (1998)
    Article CAS PubMed PubMed Central Google Scholar
  40. D. Patel, S.M. Huang, L.A. Baglia, D.J. McCance, The E6 protein of human papillomavirus type 16 binds to and inhibits co- activation by CBP and p300. EMBO J. 18, 5061 (1999)
    Article CAS PubMed PubMed Central Google Scholar
  41. A. Muller-Schiffmann, J. Beckmann, G. Steger, The E6 protein of the cutaneous human papillomavirus type 8 can stimulate the viral early and late promoters by distinct mechanisms. J. Virol. 80, 8718 (2006)
    Article PubMed PubMed Central CAS Google Scholar
  42. D. Gardiol, C. Kuhne, B. Glaunsinger, S.S. Lee, R. Javier, L. Banks, Oncogenic human papillomavirus E6 proteins target the discs large tumour suppressor for proteasome-mediated degradation. Oncogene 18, 5487 (1999)
    Article CAS PubMed Google Scholar
  43. L. Funke, S. Dakoji, D.S. Bredt, Membrane-associated guanylate kinases regulate adhesion and plasticity at cell junctions. Annu. Rev. Biochem. 74, 219 (2005)
    Article CAS PubMed Google Scholar
  44. M.L. Nguyen, M.M. Nguyen, D. Lee, A.E. Griep, P.F. Lambert, The PDZ ligand domain of the human papillomavirus type 16 E6 protein is required for E6’s induction of epithelial hyperplasia in vivo. J. Virol. 77, 6957 (2003)
    Article CAS PubMed PubMed Central Google Scholar
  45. R.A. Watson, M. Thomas, L. Banks, S. Roberts, Activity of the human papillomavirus E6 PDZ-binding motif correlates with an enhanced morphological transformation of immortalized human keratinocytes. J. Cell Sci. 116, 4925 (2003)
    Article CAS PubMed Google Scholar
  46. S. Jackson, C. Harwood, M. Thomas, L. Banks, A. Storey, Role of Bak in UV-induced apoptosis in skin cancer and abrogation by HPV E6 proteins. Genes Dev. 14, 3065 (2000)
    Article CAS PubMed PubMed Central Google Scholar
  47. M. Thomas, L. Banks, Inhibition of Bak-induced apoptosis by HPV-18 E6. Oncogene 17, 2943 (1998)
    Article CAS PubMed Google Scholar
  48. C.M. Sorenson, Bcl-2 family members and disease. Biochim. Biophys. Acta 1644, 169 (2004)
    Article CAS PubMed Google Scholar
  49. A.A. Borbely, M. Murvai, J. Konya, Z. Beck, L. Gergely, F. Li, G. Veress, Effects of human papillomavirus type 16 oncoproteins on surviving gene expression. J. Gen. Virol. 87, 287 (2006)
    Article CAS PubMed Google Scholar
  50. M.A. James, J.H. Lee, A.J. Klingelhutz, Human papillomavirus type 16 E6 activates NF-kappaB, induces cIAP-2 expression, and protects against apoptosis in a PDZ binding motif-dependent manner. J. Virol. 80, 5301 (2006)
    Article CAS PubMed PubMed Central Google Scholar
  51. H. Yuan, F. Fu, J. Zhuo, W. Wang, J. Nishitani, D.S. An, I.S. Chen, X. Liu, Human papillomavirus type 16 E6 and E7 oncoproteins upregulate c-IAP2 gene expression and confer resistance to apoptosis. Oncogene 24, 5069 (2005)
    Article CAS PubMed Google Scholar
  52. A.J. Klingelhutz, S.A. Foster, J.K. McDougall, Telomerase activation by the E6 gene product of human papillomavirus type 16. Nature 380, 79 (1996)
    Article CAS PubMed Google Scholar
  53. J.W. Shay, W.E. Wright, Senescence and immortalization: role of telomeres and telomerase. Carcinogenesis 26, 867 (2005)
    Article CAS PubMed Google Scholar
  54. L. Gewin, H. Myers, T. Kiyono, D.A. Galloway, Identification of a novel telomerase repressor that interacts with the human papillomavirus type-16 E6/E6-AP complex. Genes Dev. 18, 2269 (2004)
    Article CAS PubMed PubMed Central Google Scholar
  55. K.M. Bedard, M.P. Underbrink, H.L. Howie, D.A. Galloway, The E6 oncoproteins from human betapapillomaviruses differentially activate telomerase through an E6AP-dependent mechanism and prolong the lifespan of primary keratinocytes. J. Virol. 82, 3894 (2008)
    Article CAS PubMed PubMed Central Google Scholar
  56. X. Liu, H. Yuan, B. Fu, G.L. Disbrow, T. Apolinario, V. Tomaic, M.L. Kelley, C.C. Baker, J. Huibregtse, R. Schlegel, The E6AP ubiquitin ligase is required for transactivation of the hTERT promoter by the human papillomavirus E6 oncoprotein. J. Biol. Chem. 280, 10807 (2005)
    Article CAS PubMed Google Scholar
  57. T. Veldman, X. Liu, H. Yuan, R. Schlegel, Human papillomavirus E6 and Myc proteins associate in vivo and bind to and cooperatively activate the telomerase reverse transcriptase promoter. Proc. Natl. Acad. Sci. USA 100, 8211 (2003)
    Article CAS PubMed Google Scholar
  58. P. Sekaric, J.J. Cherry, E.J. Androphy, Binding of human papillomavirus type 16 E6 to E6AP is not required for activation of hTERT. J. Virol. 82, 71 (2008)
    Article CAS PubMed Google Scholar
  59. X. Liu, J. Roberts, A. Dakic, Y. Zhang, R. Schlegel, HPV E7 contributes to the telomerase activity of immortalized and tumorigenic cells and augments E6-induced hTERT promoter function. Virology 375, 611 (2008)
    Article CAS PubMed PubMed Central Google Scholar
  60. S. Lowell, P. Jones, R. Le, I.J. Dunne, F.M. Watt, Stimulation of human epidermal differentiation by delta-notch signalling at the boundaries of stem-cell clusters. Curr. Biol. 10, 491 (2000)
    Article Google Scholar
  61. T. Yugawa, K. Handa, M. Narisawa-Saito, S. Ohno, M. Fujita, T. Kiyono, Regulation of Notch1 gene expression by p53 in epithelial cells. Mol. Cell. Biol. 27, 3732 (2007)
    Article CAS PubMed PubMed Central Google Scholar
  62. C. Talora, D.C. Sgroi, C.P. Crum, G.P. Dotto, Specific down-modulation of Notch1 signaling in cervical cancer cells is required for sustained HPV-E6/E7 expression and late steps of malignant transformation. Genes Dev. 16, 2252 (2002)
    Article CAS PubMed PubMed Central Google Scholar
  63. I. Malanchi, S. Caldeira, M. Krutzfeldt, M. Giarre, M. Alunni-Fabbroni, M. Tommasino, Identification of a novel activity of human papillomavirus type 16 E6 protein in deregulating the G1/S transition. Oncogene 21, 5665 (2002)
    Article CAS PubMed Google Scholar
  64. I. Malanchi, R. Accardi, F. Diehl, A. Smet, E. Androphy, J. Hoheisel, M. Tommasino, Human papillomavirus type 16 E6 promotes retinoblastoma protein phosphorylation and cell cycle progression. J. Virol. 78, 13769 (2004)
    Article CAS PubMed PubMed Central Google Scholar
  65. J. An, D. Mo, H. Liu, M.S. Veena, E.S. Srivatsan, R. Massoumi, M.B. Rettig, Inactivation of the CYLD deubiquitinase by HPV E6 mediates hypoxia-induced NF-kappaB activation. Cancer Cell 14, 394 (2008)
    Article CAS PubMed PubMed Central Google Scholar
  66. H.L. Howie, R.A. Katzenellenbogen, D.A. Galloway, Papillomavirus E6 proteins. Virology 384, 324 (2009)
    Article CAS PubMed Google Scholar
  67. F. Mantovani, L. Banks, The human papillomavirus E6 protein and its contribution to malignant progression. Oncogene 20, 7874 (2001)
    Article CAS PubMed Google Scholar
  68. S.S. Tungteakkhun, M. Filippova, J.W. Neidigh, N. Fodor, P.J. Duerksen-Hughes, The interaction between human papillomavirus type 16 and FADD is mediated by a novel E6 binding domain. J. Virol. 82, 9600 (2008)
    Article CAS PubMed PubMed Central Google Scholar
  69. R.M. Vos, J. Altreuter, E.A. White, P.M. Howley, The ubiquitin-specific peptidase USP15 regulates human papillomavirus type 16 E6 protein stability. J. Virol. 83, 8885 (2009)
    Article CAS PubMed PubMed Central Google Scholar
  70. K. Munger, J.R. Basile, S. Duensing, A. Eichten, S.L. Gonzalez, M. Grace, V.L. Zacny, Biological activities and molecular targets of the human papillomavirus E7 oncoprotein. Oncogene 20, 7888 (2001)
    Article CAS PubMed Google Scholar
  71. D. Cobrinik, Pocket proteins and cell cycle control. Oncogene 24, 2796 (2005)
    Article CAS PubMed Google Scholar
  72. D.K. Dimova, N.J. Dyson, The E2F transcriptional network: old acquaintances with new faces. Oncogene 24, 2810 (2005)
    Article CAS PubMed Google Scholar
  73. S.G. Hwang, D. Lee, J. Kim, T. Seo, J. Choe, Human papillomavirus type 16 E7 binds to E2F1 and activates E2F1-driven transcription in a retinoblastoma protein-independent manner. J. Biol. Chem. 277, 2923 (2002)
    Article CAS PubMed Google Scholar
  74. M.J. Antinore, M.J. Birrer, D. Patel, L. Nader, D.J. McCance, The human papillomavirus type 16 E7 gene product interacts with and trans-activates the AP1 family of transcription factors. EMBO J. 15, 1950 (1996)
    Article CAS PubMed PubMed Central Google Scholar
  75. E. Maldonado, M.E. Cabrejos, L. Banks, J.E. Allende, Human papillomavirus-16 E7 protein inhibits the DNA interaction of the TATA binding transcription factor. J. Cell. Biochem. 85, 663 (2002)
    Article CAS PubMed Google Scholar
  76. P. Massimi, D. Pim, L. Banks, Human papillomavirus type 16 E7 binds to the conserved carboxy-terminal region of the TATA box binding protein and this contributes to E7 transforming activity. J. Gen. Virol. 78, 2607 (1997)
    Article CAS PubMed Google Scholar
  77. A.C. Phillips, K.H. Vousden, Analysis of the interaction between human papillomavirus type 16 E7 and the TATA-binding protein, TBP. J. Gen. Virol. 78, 905 (1997)
    Article CAS PubMed Google Scholar
  78. J.O. Funk, S. Waga, J.B. Harry, E. Espling, B. Stillman, D.A. Galloway, Inhibition of CDK activity and PCNA-dependent DNA replication by p21 is blocked by interaction with the HPV-16 E7 oncoprotein. Genes Dev. 11, 2090 (1997)
    Article CAS PubMed PubMed Central Google Scholar
  79. D.L. Jones, R.M. Alani, K. Munger, The human papillomavirus E7 oncoprotein can uncouple cellular differentiation and proliferation in human keratinocytes by abrogating p21Cip1-mediated inhibition of cdk2. Genes Dev. 11, 2101 (1997)
    Article CAS PubMed PubMed Central Google Scholar
  80. K. Zerfaß-Thome, W. Zwerschke, B. Mannhardt, R. Tindle, J. Botz, P. Jansen-Dürr, Inactivation of the cdk inhibitor p27KIP1 by the human papillomavirus type 16 E7 oncoprotein. Oncogene 13, 2323 (1996)
    PubMed Google Scholar
  81. M. Arroyo, S. Bagchi, P. Raychaudhuri, Association of the human papillomavirus type-16 E7 protein with the S-phase-specific E2F-cyclin-A complex. Mol. Cell. Biol. 13, 6537 (1993)
    Article CAS PubMed PubMed Central Google Scholar
  82. R. Davies, R. Hicks, T. Crook, J. Morris, K. Vousden, Human papillomavirus type-16 E7 associates with a histone H1 kinase and with p107 through sequences necessary for transformation. J. Virol. 67, 2521 (1993)
    CAS PubMed PubMed Central Google Scholar
  83. M. Tommasino, J.P. Adamczewski, F. Carlotti, C.F. Barth, R. Manetti, M. Contorni, F. Cavalieri, T. Hunt, L. Crawford, HPV16 E7 protein associates with the protein kinase p33CDK2 and cyclin A. Oncogene 8, 195 (1993)
    CAS PubMed Google Scholar
  84. W. He, D. Staples, C. Smith, C. Fisher, Direct activation of cyclin-dependent kinase 2 by human papillomavirus E7. J. Virol. 77, 10566 (2003)
    Article CAS PubMed PubMed Central Google Scholar
  85. K. Munger, B.A. Werness, N. Dyson, W.C. Phelps, E. Harlow, P.M. Howley, Complex formation of human papillomavirus E7 proteins with the retinoblastoma tumor suppressor gene product. EMBO J. 8, 4099 (1989)
    Article CAS PubMed PubMed Central Google Scholar
  86. D.V. Heck, C.L. Yee, P.M. Howley, K. Munger, Efficiency of binding the retinoblastoma protein correlates with the transforming capacity of the E7 oncoproteins of the human papillomaviruses. Proc. Natl. Acad. Sci. USA 89, 4442 (1992)
    Article CAS PubMed Google Scholar
  87. B.C. Sang, M.S. Barbosa, Single amino acid substitutions in “low-risk” human papillomavirus (HPV) type 6 E7 protein enhance features characteristic of the “high-risk” HPV E7 oncoproteins. Proc. Natl. Acad. Sci. USA 89, 8063 (1992)
    Article CAS PubMed Google Scholar
  88. S. Caldeira, W. Dong, P. Tomakidi, A. Paradiso, M. Tommasino, Human papillomavirus type 32 does not display in vitro transforming properties. Virology 301, 157 (2002)
    Article CAS PubMed Google Scholar
  89. F. Ciccolini, G. Di Pasquale, F. Carlotti, L. Crawford, M. Tommasino, Functional studies of E7 proteins from different HPV types. Oncogene 9, 2342 (1994)
    Google Scholar
  90. W.L. Dong, S. Caldeira, P. Sehr, M. Pawlita, M. Tommasino, Determination of the binding affinity of different human papillomavirus E7 proteins for the tumour suppressor pRb by a plate-binding assay. J. Virol. Methods 98, 91 (2001)
    Article CAS PubMed Google Scholar
  91. A. Schmitt, J.B. Harry, B. Rapp, F.O. Wettstein, T. Iftner, Comparison of the properties of the E6 and E7 genes of low- and high-risk cutaneous papillomaviruses reveals strongly transforming and high Rb-binding activity for the E7 protein of the low-risk human papillomavirus type 1. J. Virol. 68, 7051 (1994)
    CAS PubMed PubMed Central Google Scholar
  92. S.N. Boyer, D.E. Wazer, V. Band, E7 protein of human papilloma virus-16 induces degradation of retinoblastoma protein through the ubiquitin-proteasome pathway. Cancer Res. 56, 4620 (1996)
    CAS PubMed Google Scholar
  93. D.L. Jones, K. Munger, Analysis of the p53-mediated G1 growth arrest pathway in cells expressing the human papillomavirus type 16 E7 oncoprotein. J. Virol. 71, 2905 (1997)
    CAS PubMed PubMed Central Google Scholar
  94. M. Giarre, S. Caldeira, I. Malanchi, F. Ciccolini, M.J. Leao, M. Tommasino, Induction of pRb degradation by the human papillomavirus type 16 E7 protein is essential to efficiently overcome p16INK4a-imposed G1 cell cycle arrest. J. Virol. 75, 4705 (2001)
    Article CAS PubMed PubMed Central Google Scholar
  95. S.L. Gonzalez, M. Stremlau, X. He, J.R. Basile, K. Munger, Degradation of the retinoblastoma tumor suppressor by the human papillomavirus type 16 E7 oncoprotein is important for functional inactivation and is separable from proteasomal degradation of E7. J. Virol. 75, 7583 (2001)
    Article CAS PubMed PubMed Central Google Scholar
  96. G.A. Darnell, W.A. Schroder, T.M. Antalis, E. Lambley, L. Major, J. Gardner, G. Birrell, A. Cid-Arregui, A. Suhrbier, Human papillomavirus E7 requires the protease calpain to degrade the retinoblastoma protein. J. Biol. Chem. 282, 37492 (2007)
    Article CAS PubMed Google Scholar
  97. K. Huh, X. Zhou, H. Hayakawa, J.Y. Cho, T.A. Libermann, J. Jin, J.W. Harper, K. Munger, Human papillomavirus type 16 E7 oncoprotein associates with the cullin 2 ubiquitin ligase complex, which contributes to degradation of the retinoblastoma tumor suppressor. J. Virol. 81, 9737 (2007)
    Article CAS PubMed PubMed Central Google Scholar
  98. S.J. Reshkin, A. Bellizzi, S. Caldeira, V. Albarani, I. Malanchi, M. Poignee, M. Alunni-Fabbroni, V. Casavola, M. Tommasino, Na+/H+ exchanger-dependent intracellular alkalinization is an early event in malignant transformation and plays an essential role in the development of subsequent transformation-associated phenotypes. FASEB J. 14, 2185 (2000)
    Article CAS PubMed Google Scholar
  99. M.E. McLaughlin-Drubin, K. Munger, The human papillomavirus E7 oncoprotein. Virology 384, 335 (2009)
    Article CAS PubMed Google Scholar
  100. A.C. Rodriguez, M. Schiffman, R. Herrero, S. Wacholder, A. Hildesheim, P.E. Castle, D. Solomon, R. Burk, Rapid clearance of human papillomavirus and implications for clinical focus on persistent infections. J. Natl. Cancer Inst. 100, 513 (2008)
    Article PubMed PubMed Central Google Scholar
  101. M.H. Einstein, J.T. Schiller, R.P. Viscidi, H.D. Strickler, P. Coursaget, T. Tan, N. Halsey, D. Jenkins, Clinician’s guide to human papillomavirus immunology: knowns and unknowns. Lancet Infect. Dis. 9, 347 (2009)
    Article CAS PubMed Google Scholar
  102. U.A. Hasan, E. Bates, F. Takeshita, A. Biliato, R. Accardi, V. Bouvard, M. Mansour, I. Vincent, L. Gissmann, T. Iftner, M. Sideri, F. Stubenrauch, M. Tommasino, TLR9 expression and function is abolished by the cervical cancer-associated human papillomavirus type 16. J. Immunol. 178, 3186 (2007)
    Article CAS PubMed Google Scholar
  103. L.V. Ronco, A.Y. Karpova, M. Vidal, P.M. Howley, Human papillomavirus 16 E6 oncoprotein binds to interferon regulatory factor-3 and inhibits its transcriptional activity. Genes Dev. 12, 2061 (1998)
    Article CAS PubMed PubMed Central Google Scholar
  104. J.S. Park, E.J. Kim, H.J. Kwon, E.S. Hwang, S.E. NamKoong, S.J. Um, Inactivation of interferon regulatory factor-1 tumor suppressor protein by HPV E7 oncoprotein. Implication for the E7-mediated immune evasion mechanism in cervical carcinogenesis. J. Biol. Chem. 275, 6764 (2000)
    Article CAS PubMed Google Scholar
  105. S.E. Perea, P. Massimi, L. Banks, Human papillomavirus type 16 E7 impairs the activation of the interferon regulatory factor-1. Int. J. Mol. Med. 5, 661 (2000)
    CAS PubMed Google Scholar
  106. J.H. Caberg, P.M. Hubert, D.Y. Begon, M.F. Herfs, P.J. Roncarati, J.J. Boniver, P.O. Delvenne, Silencing of E7 oncogene restores functional E-cadherin expression in human papillomavirus 16-transformed keratinocytes. Carcinogenesis 29, 1441 (2008)
    Article CAS PubMed Google Scholar
  107. P. Hubert, J.H. Caberg, C. Gilles, L. Bousarghin, E. Franzen-Detrooz, J. Boniver, P. Delvenne, E-cadherin-dependent adhesion of dendritic and Langerhans cells to keratinocytes is defective in cervical human papillomavirus-associated (pre)neoplastic lesions. J. Pathol. 206, 346 (2005)
    Article CAS PubMed Google Scholar
  108. F.V. Cromme, P.J. Snijders, A.J. van den Brule, P. Kenemans, C.J. Meijer, J.M. Walboomers, MHC class I expression in HPV 16 positive cervical carcinomas is post-transcriptionally controlled and independent from c-myc overexpression. Oncogene 8, 2969 (1993)
    CAS PubMed Google Scholar
  109. A. Vambutas, V.R. Bonagura, B.M. Steinberg, Altered expression of TAP-1 and major histocompatibility complex class I in laryngeal papillomatosis: correlation of TAP-1 with disease. Clin. Diagn. Lab. Immunol. 7, 79 (2000)
    CAS PubMed PubMed Central Google Scholar
  110. A. Vambutas, J. DeVoti, W. Pinn, B.M. Steinberg, V.R. Bonagura, Interaction of human papillomavirus type 11 E7 protein with TAP-1 results in the reduction of ATP-dependent peptide transport. Clin. Immunol. 101, 94 (2001)
    Article CAS PubMed Google Scholar
  111. F. Mota, N. Rayment, S. Chong, A. Singer, B. Chain, The antigen-presenting environment in normal and human papillomavirus (HPV)-related premalignant cervical epithelium. Clin. Exp. Immunol. 116, 33 (1999)
    Article CAS PubMed PubMed Central Google Scholar
  112. L.L. Villa, K.B. Vieira, X.F. Pei, R. Schlegel, Differential effect of tumor necrosis factor on proliferation of primary human keratinocytes and cell lines containing human papillomavirus types 16 and 18. Mol. Carcinog. 6, 5 (1992)
    Article CAS PubMed Google Scholar

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