The biological properties of E6 and E7 oncoproteins from human papillomaviruses

Virus Genes

Volumn 40, Issue 1, 2010, Pages 1-13

  Ghittoni, Raffaella ^a   Accardi, Rosita ^a   Hasan, Uzma ^a,b   Gheit, Tarik ^a   Sylla, Bakary ^a   Tommasino, Massimo ^a  

^a INTERNATIONAL AGENCY FOR RESEARCH ON CANCER   (France)

^b INSERM   (France)

Author keywords

Cellular transformation; E6 and E7 oncoproteins; Evasion immune response; Human carcinogenesis; Human papillomaviruses

Indexed keywords

GENE PRODUCT; PROTEIN E6; PROTEIN E7;

CARCINOGENESIS; HIGH RISK BEHAVIOR; IMMUNOSURVEILLANCE; NONHUMAN; PRIORITY JOURNAL; REVIEW; VIRUS IMMUNITY; WART VIRUS;

ANIMALS; HUMANS; NEOPLASMS; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS E7 PROTEINS; PAPILLOMAVIRUS INFECTIONS;

HUMAN PAPILLOMAVIRUS; HUMAN PAPILLOMAVIRUS TYPES; PAPILLOMAVIRIDAE;

EID: 77149149956     PISSN: 09208569     EISSN: 1572994X     Source Type: Journal    
DOI: 10.1007/s11262-009-0412-8     Document Type: Review

References (112)

1. EM de Villiers C Fauquet TR Broker HU Bernard H zur Hausen 2004 Classification of papillomaviruses Virology 324 17 15183049
2. H zur Hausen 2002 Papillomaviruses and cancer: from basic studies to clinical application Nat. Rev. Cancer 2 342 12044010
3. Z Chen M Schiffman R Herrero R Desalle RD Burk 2007 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 17125811
4. RJ Nobre E Herraez-Hernandez JW Fei L Langbein S Kaden HJ Grone EM de Villiers 2009 E7 oncoprotein of novel human papillomavirus type 108 lacking the E6 gene induces dysplasia in organotypic keratinocyte cultures J. Virol. 83 2907 19153227
5. N Munoz FX Bosch S de Sanjose R Herrero X Castellsague KV Shah PJ Snijders CJ Meijer 2003 Epidemiologic classification of human papillomavirus types associated with cervical cancer N. Engl. J. Med. 348 518 12571259
6. JS Smith L Lindsay B Hoots J Keys S Franceschi R Winer GM Clifford 2007 Human papillomavirus type distribution in invasive cervical cancer and high-grade cervical lesions: a meta-analysis update Int. J. Cancer 121 621 17405118
7. AR Kreimer GM Clifford P Boyle S Franceschi 2005 Human papillomavirus types in head and neck squamous cell carcinomas worldwide: a systematic review Cancer Epidemiol. Biomarkers Prev. 14 467 15734974
8. AG Ostor 1993 Natural history of cervical intraepithelial neoplasia: a critical review Int. J. Gynecol. Pathol. 12 186 8463044
9. N Jones 1990 Transcriptional regulation by dimerization: two sides to an incestuous relationship Cell 61 9 2180585
10. PK Magnusson P Sparen UB Gyllensten 1999 Genetic link to cervical tumours Nature 400 6729
11. V Moreno N Munoz FX Bosch S de Sanjose LC Gonzalez L Tafur M Gili I Izarzugaza C Navarro A Vergara, et al. 1995 Risk factors for progression of cervical intraepithelial neoplasm grade III to invasive cervical cancer Cancer Epidemiol. Biomarkers Prev. 4 459 7549800
12. V Moreno FX Bosch N Munoz CJ Meijer KV Shah JM Walboomers R Herrero S Franceschi 2002 Effect of oral contraceptives on risk of cervical cancer in women with human papillomavirus infection: the IARC multicentric case-control study Lancet 359 1085 11943255
13. N Munoz S Franceschi C Bosetti V Moreno R Herrero JS Smith KV Shah CJ Meijer FX Bosch 2002 Role of parity and human papillomavirus in cervical cancer: the IARC multicentric case-control study Lancet 359 1093 11943256
14. MH Schiffman NJ Haley JS Felton AW Andrews RA Kaslow WD Lancaster RJ Kurman LA Brinton LB Lannom D Hoffmann 1987 Biochemical epidemiology of cervical neoplasia: measuring cigarette smoke constituents in the cervix Cancer Res. 47 3886 3594446
15. H Pfister 2003 Chapter 8: human papillomavirus and skin cancer J. Natl. Cancer Inst. Monogr. 31 52 12807946
16. MN de Koning SJ Weissenborn D Abeni JN Bouwes Bavinck S Euvrard AC Green CA Harwood L Naldi R Neale I Nindl CM Proby WG Quint F Sampogna J Ter Schegget L Struijk U Wieland HJ Pfister MC Feltkamp 2009 Prevalence and associated factors of betapapillomavirus infections in individuals without cutaneous squamous cell carcinoma J. Gen. Virol. 90 1611 19321753
17. HN Ananthaswamy SM Loughlin P Cox RL Evans SE Ullrich ML Kripke 1997 Sunlight and skin cancer: inhibition of p53 mutations in UV-irradiated mouse skin by sunscreens Nat. Med. 3 510 9142118
18. BK Armstrong A Kricker 2001 The epidemiology of UV induced skin cancer J. Photochem. Photobiol. B 63 8 11684447
19. DS Preston RS Stern 1992 Nonmelanoma cancers of the skin N. Engl. J. Med. 327 1649 1435901
20. C Ateenyi-Agaba E Weiderpass A Smet W Dong M Dai B Kahwa H Wabinga E Katongole-Mbidde S Franceschi M Tommasino 2004 Epidermodysplasia verruciformis human papillomavirus types and carcinoma of the conjunctiva: a pilot study Br. J. Cancer 90 1777 15150602
21. R Newton 1996 A review of the aetiology of squamous cell carcinoma of the conjunctiva Br. J. Cancer 74 1511 8932327
22. E Schwarz UK Freese L Gissmann W Mayer B Roggenbuck A Stremlau H zur Hausen 1985 Structure and transcription of human papillomavirus sequences in cervical carcinoma cells Nature 314 111 2983228
23. N Wentzensen S Vinokurova M von Knebel Doeberitz 2004 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 15172997
24. LM Alvarez-Salas JA DiPaolo 2007 Molecular approaches to cervical cancer therapy Curr. Drug Discov. Technol. 4 208 17986003
25. M Tommasino L Crawford 1995 Human papillomavirus E6 and E7: proteins which deregulate the cell cycle Bioessays 17 509 7575492
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
27. M Tommasino R Accardi S Caldeira W Dong I Malanchi A Smet I Zehbe 2003 The role of TP53 in cervical carcinogenesis Hum. Mutat. 21 307 12619117
28. JM Huibregtse M Scheffner PM Howley 1991 A cellular protein mediates association of p53 with the E6 oncoprotein of human papillomavirus types 16 or 18 EMBO J. 10 4129 1661671
29. M Scheffner BA Werness JM Huibregtse AJ Levine PM Howley 1990 The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53 Cell 63 1129 2175676
30. M Scheffner JM Huibregtse RD Vierstra PM Howley 1993 The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53 Cell 75 495 8221889
31. P Massimi A Shai P Lambert L Banks 2008 HPV E6 degradation of p53 and PDZ containing substrates in an E6AP null background Oncogene 27 1800 17934525
32. T Hiller S Poppelreuther F Stubenrauch T Iftner 2006 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 16835321
33. MS Lechner LA Laimins 1994 Inhibition of p53 DNA binding by human papillomavirus E6 proteins J. Virol. 68 4262 8207801
34. K Butz C Denk A Ullmann M Scheffner F Hoppe-Seyler 2000 Induction of apoptosis in human papillomaviruspositive cancer cells by peptide aptamers targeting the viral E6 oncoprotein Proc. Natl. Acad. Sci. USA 97 6693 10829072
35. HC Pan AE Griep 1995 Temporally distinct patterns of p53-dependent and p53-independent apoptosis during mouse lens development Genes Dev. 9 2157 7657167
36. AE White EM Livanos TD Tlsty 1994 Differential disruption of genomic integrity and cell cycle regulation in normal human fibroblasts by the HPV oncoproteins Genes Dev. 8 666 7926757
37. UM Moll S Erster A Zaika 2001 p53, p63 and p73-solos, alliances and feuds among family members Biochim. Biophys. Acta 1552 47 11825686
38. JS Park EJ Kim JY Lee HS Sin SE NamKoong SJ Um 2001 Functional inactivation of p73, a homolog of p53 tumor suppressor protein, by human papillomavirus E6 proteins Int. J. Cancer 91 822 11275986
39. MC Marin CA Jost MS Irwin JA DeCaprio D Caput WG Kaelin Jr 1998 Viral oncoproteins discriminate between p53 and the p53 homolog p73 Mol. Cell. Biol. 18 6316 9774648
40. D Patel SM Huang LA Baglia DJ McCance 1999 The E6 protein of human papillomavirus type 16 binds to and inhibits co- activation by CBP and p300 EMBO J. 18 5061 10487758
41. A Muller-Schiffmann J Beckmann G Steger 2006 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 16912319
42. D Gardiol C Kuhne B Glaunsinger SS Lee R Javier L Banks 1999 Oncogenic human papillomavirus E6 proteins target the discs large tumour suppressor for proteasome-mediated degradation Oncogene 18 5487 10523825
43. L Funke S Dakoji DS Bredt 2005 Membrane-associated guanylate kinases regulate adhesion and plasticity at cell junctions Annu. Rev. Biochem. 74 219 15952887
44. ML Nguyen MM Nguyen D Lee AE Griep PF Lambert 2003 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 12768014
45. RA Watson M Thomas L Banks S Roberts 2003 Activity of the human papillomavirus E6 PDZ-binding motif correlates with an enhanced morphological transformation of immortalized human keratinocytes J. Cell Sci. 116 4925 14625386
46. S Jackson C Harwood M Thomas L Banks A Storey 2000 Role of Bak in UV-induced apoptosis in skin cancer and abrogation by HPV E6 proteins Genes Dev. 14 3065 11114894
47. M Thomas L Banks 1998 Inhibition of Bak-induced apoptosis by HPV-18 E6 Oncogene 17 2943 9881696
48. CM Sorenson 2004 Bcl-2 family members and disease Biochim. Biophys. Acta 1644 169 14996501
49. AA Borbely M Murvai J Konya Z Beck L Gergely F Li G Veress 2006 Effects of human papillomavirus type 16 oncoproteins on surviving gene expression J. Gen. Virol. 87 287 16432013
50. MA James JH Lee AJ Klingelhutz 2006 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 16699010
51. H Yuan F Fu J Zhuo W Wang J Nishitani DS An IS Chen X Liu 2005 Human papillomavirus type 16 E6 and E7 oncoproteins upregulate c-IAP2 gene expression and confer resistance to apoptosis Oncogene 24 5069 15856013
52. AJ Klingelhutz SA Foster JK McDougall 1996 Telomerase activation by the E6 gene product of human papillomavirus type 16 Nature 380 79 8598912
53. JW Shay WE Wright 2005 Senescence and immortalization: role of telomeres and telomerase Carcinogenesis 26 867 15471900
54. L Gewin H Myers T Kiyono DA Galloway 2004 Identification of a novel telomerase repressor that interacts with the human papillomavirus type-16 E6/E6-AP complex Genes Dev. 18 2269 15371341
55. KM Bedard MP Underbrink HL Howie DA Galloway 2008 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 18256157
56. X Liu H Yuan B Fu GL Disbrow T Apolinario V Tomaic ML Kelley CC Baker J Huibregtse R Schlegel 2005 The E6AP ubiquitin ligase is required for transactivation of the hTERT promoter by the human papillomavirus E6 oncoprotein J. Biol. Chem. 280 10807 15655249
57. T Veldman X Liu H Yuan R Schlegel 2003 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 12821782
58. P Sekaric JJ Cherry EJ Androphy 2008 Binding of human papillomavirus type 16 E6 to E6AP is not required for activation of hTERT J. Virol. 82 71 17942561
59. X Liu J Roberts A Dakic Y Zhang R Schlegel 2008 HPV E7 contributes to the telomerase activity of immortalized and tumorigenic cells and augments E6-induced hTERT promoter function Virology 375 611 18367227
60. S Lowell P Jones R Le IJ Dunne FM Watt 2008 Stimulation of human epidermal differentiation by delta-notch signalling at the boundaries of stem-cell clusters Curr. Biol. 10 491
61. T Yugawa K Handa M Narisawa-Saito S Ohno M Fujita T Kiyono 2007 Regulation of Notch1 gene expression by p53 in epithelial cells Mol. Cell. Biol. 27 3732 17353266
62. C Talora DC Sgroi CP Crum GP Dotto 2002 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 12208848
63. I Malanchi S Caldeira M Krutzfeldt M Giarre M Alunni-Fabbroni M Tommasino 2002 Identification of a novel activity of human papillomavirus type 16 E6 protein in deregulating the G1/S transition Oncogene 21 5665 12173036
64. I Malanchi R Accardi F Diehl A Smet E Androphy J Hoheisel M Tommasino 2004 Human papillomavirus type 16 E6 promotes retinoblastoma protein phosphorylation and cell cycle progression J. Virol. 78 13769 15564485
65. J An D Mo H Liu MS Veena ES Srivatsan R Massoumi MB Rettig 2008 Inactivation of the CYLD deubiquitinase by HPV E6 mediates hypoxia-induced NF-kappaB activation Cancer Cell 14 394 18977328
66. HL Howie RA Katzenellenbogen DA Galloway 2009 Papillomavirus E6 proteins Virology 384 324 19081593
67. F Mantovani L Banks 2001 The human papillomavirus E6 protein and its contribution to malignant progression Oncogene 20 7874 11753670
68. SS Tungteakkhun M Filippova JW Neidigh N Fodor PJ Duerksen-Hughes 2008 The interaction between human papillomavirus type 16 and FADD is mediated by a novel E6 binding domain J. Virol. 82 9600 18632871
69. RM Vos J Altreuter EA White PM Howley 2009 The ubiquitin-specific peptidase USP15 regulates human papillomavirus type 16 E6 protein stability J. Virol. 83 8885 19553310
70. K Munger JR Basile S Duensing A Eichten SL Gonzalez M Grace VL Zacny 2001 Biological activities and molecular targets of the human papillomavirus E7 oncoprotein Oncogene 20 7888 11753671
71. D Cobrinik 2005 Pocket proteins and cell cycle control Oncogene 24 2796 15838516
72. DK Dimova NJ Dyson 2005 The E2F transcriptional network: old acquaintances with new faces Oncogene 24 2810 15838517
73. SG Hwang D Lee J Kim T Seo J Choe 2002 Human papillomavirus type 16 E7 binds to E2F1 and activates E2F1-driven transcription in a retinoblastoma protein-independent manner J. Biol. Chem. 277 2923 11713253
74. MJ Antinore MJ Birrer D Patel L Nader DJ McCance 1996 The human papillomavirus type 16 E7 gene product interacts with and trans-activates the AP1 family of transcription factors EMBO J. 15 1950 8617242
75. E Maldonado ME Cabrejos L Banks JE Allende 2002 Human papillomavirus-16 E7 protein inhibits the DNA interaction of the TATA binding transcription factor J. Cell. Biochem. 85 663 11968006
76. P Massimi D Pim L Banks 1997 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 9349482
77. AC Phillips KH Vousden 1997 Analysis of the interaction between human papillomavirus type 16 E7 and the TATA-binding protein, TBP J. Gen. Virol. 78 905 9129664
78. JO Funk S Waga JB Harry E Espling B Stillman DA Galloway 1997 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 9284048
79. DL Jones RM Alani K Munger 1997 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 9284049
80. K Zerfa-Thome W Zwerschke B Mannhardt R Tindle J Botz P Jansen-Dürr 1996 Inactivation of the cdk inhibitor p27KIP1 by the human papillomavirus type 16 E7 oncoprotein Oncogene 13 2323 8957073
81. M Arroyo S Bagchi P Raychaudhuri 1993 Association of the human papillomavirus type-16 E7 protein with the S-phase-specific E2F-cyclin-A complex Mol. Cell. Biol. 13 6537 8413252
82. R Davies R Hicks T Crook J Morris K Vousden 1993 Human papillomavirus type-16 E7 associates with a histone H1 kinase and with p107 through sequences necessary for transformation J. Virol. 67 2521 8386265
83. M Tommasino JP Adamczewski F Carlotti CF Barth R Manetti M Contorni F Cavalieri T Hunt L Crawford 1993 HPV16 E7 protein associates with the protein kinase p33CDK2 and cyclin A Oncogene 8 195 8380917
84. W He D Staples C Smith C Fisher 2003 Direct activation of cyclin-dependent kinase 2 by human papillomavirus E7 J. Virol. 77 10566 12970441
85. K Munger BA Werness N Dyson WC Phelps E Harlow PM Howley 1989 Complex formation of human papillomavirus E7 proteins with the retinoblastoma tumor suppressor gene product EMBO J. 8 4099 2556261
86. DV Heck CL Yee PM Howley K Munger 1992 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 1316608
87. BC Sang MS Barbosa 1992 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 1325643
88. S Caldeira W Dong P Tomakidi A Paradiso M Tommasino 2002 Human papillomavirus type 32 does not display in vitro transforming properties Virology 301 157 12359456
89. F Ciccolini G Di Pasquale F Carlotti L Crawford M Tommasino 1994 Functional studies of E7 proteins from different HPV types Oncogene 9 2342
90. WL Dong S Caldeira P Sehr M Pawlita M Tommasino 2001 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 11543887
91. A Schmitt JB Harry B Rapp FO Wettstein T Iftner 1994 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 7933087
92. SN Boyer DE Wazer V Band 1996 E7 protein of human papilloma virus-16 induces degradation of retinoblastoma protein through the ubiquitin-proteasome pathway Cancer Res. 56 4620 8840974
93. DL Jones K Munger 1997 Analysis of the p53-mediated G1 growth arrest pathway in cells expressing the human papillomavirus type 16 E7 oncoprotein J. Virol. 71 2905 9060648
94. M Giarre S Caldeira I Malanchi F Ciccolini MJ Leao M Tommasino 2001 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 11312342
95. SL Gonzalez M Stremlau X He JR Basile K Munger 2001 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 11462030
96. GA Darnell WA Schroder TM Antalis E Lambley L Major J Gardner G Birrell A Cid-Arregui A Suhrbier 2007 Human papillomavirus E7 requires the protease calpain to degrade the retinoblastoma protein J. Biol. Chem. 282 37492 17977825
97. K Huh X Zhou H Hayakawa JY Cho TA Libermann J Jin JW Harper K Munger 2007 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 17609271
98. SJ Reshkin A Bellizzi S Caldeira V Albarani I Malanchi M Poignee M Alunni-Fabbroni V Casavola M Tommasino 2000 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 11053239
99. ME McLaughlin-Drubin K Munger 2009 The human papillomavirus E7 oncoprotein Virology 384 335 19007963
100. AC Rodriguez M Schiffman R Herrero S Wacholder A Hildesheim PE Castle D Solomon R Burk 2008 Rapid clearance of human papillomavirus and implications for clinical focus on persistent infections J. Natl. Cancer Inst. 100 513 18364507
101. MH Einstein JT Schiller RP Viscidi HD Strickler P Coursaget T Tan N Halsey D Jenkins 2009 Clinician's guide to human papillomavirus immunology: knowns and unknowns Lancet Infect. Dis. 9 347 19467474
102. UA 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 2007 TLR9 expression and function is abolished by the cervical cancer-associated human papillomavirus type 16 J. Immunol. 178 3186 17312167
103. LV Ronco AY Karpova M Vidal PM Howley 1998 Human papillomavirus 16 E6 oncoprotein binds to interferon regulatory factor-3 and inhibits its transcriptional activity Genes Dev. 12 2061 9649509
104. JS Park EJ Kim HJ Kwon ES Hwang SE NamKoong SJ Um 2000 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 10702232
105. SE Perea P Massimi L Banks 2000 Human papillomavirus type 16 E7 impairs the activation of the interferon regulatory factor-1 Int. J. Mol. Med. 5 661 10812019
106. JH Caberg PM Hubert DY Begon MF Herfs PJ Roncarati JJ Boniver PO Delvenne 2008 Silencing of E7 oncogene restores functional E-cadherin expression in human papillomavirus 16-transformed keratinocytes Carcinogenesis 29 1441 18566017
107. P Hubert JH Caberg C Gilles L Bousarghin E Franzen-Detrooz J Boniver P Delvenne 2005 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 15852499
108. FV Cromme PJ Snijders AJ van den Brule P Kenemans CJ Meijer JM Walboomers 1993 MHC class I expression in HPV 16 positive cervical carcinomas is post-transcriptionally controlled and independent from c-myc overexpression Oncogene 8 2969 8414499
109. A Vambutas VR Bonagura BM Steinberg 2000 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 10618282
110. A Vambutas J DeVoti W Pinn BM Steinberg VR Bonagura 2001 Interaction of human papillomavirus type 11 E7 protein with TAP-1 results in the reduction of ATP-dependent peptide transport Clin. Immunol. 101 94 11580231
111. F Mota N Rayment S Chong A Singer B Chain 1999 The antigen-presenting environment in normal and human papillomavirus (HPV)-related premalignant cervical epithelium Clin. Exp. Immunol. 116 33 10209502
112. LL Villa KB Vieira XF Pei R Schlegel 1992 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 1323969