Modulation of apoptosis by human papillomavirus (HPV) oncoproteins

Archives of Virology

Volumn 151, Issue 12, 2006, Pages 2321-2335

  Garnett, T O ^a   Duerksen Hughes, P J ^a  

^a LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ONCOPROTEIN; VIRUS PROTEIN;

ALPHAPAPILLOMAVIRUS; APOPTOSIS; GENETICS; HUMAN; IMMUNOLOGY; OPEN READING FRAME; PATHOGENICITY; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; REVIEW; VIRUS INFECTION;

ALPHAPAPILLOMAVIRUS; APOPTOSIS; HUMANS; ONCOGENE PROTEINS; ONCOGENE PROTEINS, VIRAL; OPEN READING FRAMES; PAPILLOMAVIRUS INFECTIONS; VIRAL PROTEINS;

HUMAN PAPILLOMAVIRUS; PAPILLOMAVIRIDAE;

EID: 33751398479     PISSN: 03048608     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00705-006-0821-0     Document Type: Review

References (98)

1. W Al-Saleh P Delvenne JE Arrese AF Nikkels GE Pierard J Boniver 1995 Inverse modulation of intraepithelial Langerhans' cells and stromal macrophage/dendrocyte populations in human papillomavirus-associated squamous intraepithelial lesions of the cervix Virchows Arch 427 41 48
2. MJ Antinore MJ Birrer D Patel L Nader DJ [tmp] 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 1960
3. GH Ashrafi MR Haghshenas B Marchetti PM O'Brien MS Campo 2005 E5 protein of human papillomavirus type 16 selectively downregulates surface HLA class I Int J Cancer 113 276 283
4. E Berezutskaya S Bagchi 1997 The human papillomavirus E7 oncoprotein functionally interacts with the S4 subunit of the 26 S proteasome J Biol Chem 272 30135 30140
5. E Berezutskaya B Yu A Morozov P Raychaudhuri S Bagchi 1997 Differential regulation of the pocket domains of the retinoblastoma family proteins by the HPV16 E7 oncoprotein Cell Growth Differ 8 1277 1286
6. S Blachon S Bellanger C Demeret F Thierry 2005 Nucleo-cytoplasmic shuttling of high risk human Papillomavirus E2 proteins induces apoptosis J Biol Chem 280 36088 36098
7. HJ Bontkes TD de Gruijl JM Walboomers JT Schiller J Dillner TJ Helmerhorst RH Verheijen RJ Scheper CJ Meijer 1999 Immune responses against human papillomavirus (HPV) type 16 virus-like particles in a cohort study of women with cervical intraepithelial neoplasia. II. Systemic but not local IgA responses correlate with clearance of HPV-16 J Gen Virol 80 Pt 2 409 417
8. A Brehm SJ Nielsen EA Miska DJ [tmp] McCance JL Reid AJ Bannister T Kouzarides 1999 The E7 oncoprotein associates with Mi2 and histone deacetylase activity to promote cell growth EMBO J 18 2449 2458
9. JJ Chen CE Reid V Band EJ Androphy 1995 Interaction of papillomavirus E6 oncoproteins with a putative calcium-binding protein Science 269 529 531
10. SL Chen CH Huang TC Tsai KY Lu YP Tsao 1996 The regulation mechanism of c-jun and junB by human papillomavirus type 16 E5 oncoprotein Arch Virol 141 791 800
11. J Cohen 2005 Public health. High hopes and dilemmas for a cervical cancer vaccine Science 308 618 621
12. M Conrad VJ Bubb R Schlegel 1993 The human papillomavirus type 6 and 16 E5 proteins are membrane-associated proteins which associate with the 16-kilodalton pore-forming protein J Virol 67 6170 6178
13. SA Corden LJ Sant-Cassia AJ Easton AG Morris 1999 The integration of HPV-18 DNA in cervical carcinoma Mol Pathol 52 275 282
14. K Crusius E Auvinen B Steuer H Gaissert A Alonso 1998 The human papillomavirus type 16 E5-protein modulates ligand-dependent activation of the EGF receptor family in the human epithelial cell line HaCaT Exp Cell Res 241 76 83
15. K Crusius M Kaszkin V Kinzel A Alonso 1999 The human papillomavirus type 16 E5 protein modulates phospholipase C-gamma-1 activity and phosphatidyl inositol turnover in mouse fibroblasts Oncogene 18 6714 6718
16. K Crusius I Rodriguez A Alonso 2000 The human papillomavirus type 16 E5 protein modulates ERK1/2 and p38 MAP kinase activation by an EGFR-independent process in stressed human keratinocytes Virus Genes 20 65 69
17. RA DeFilippis EC Goodwin L Wu D DiMaio 2003 Endogenous human papillomavirus E6 and E7 proteins differentially regulate proliferation, senescence, and apoptosis in HeLa cervical carcinoma cells J Virol 77 1551 1563
18. YY Degenhardt SJ Silverstein 2001 Gps2, a protein partner for human papillomavirus E6 proteins J Virol 75 151 160
19. J Du GG Chen AC Vlantis PK Chan RK Tsang CA van Hasselt 2004 Resistance to apoptosis of HPV 16-infected laryngeal cancer cells is associated with decreased Bak and increased Bcl-2 expression Cancer Lett 205 81 88
20. M Du X Fan E Hong JJ Chen 2002 Interaction of oncogenic papillomavirus E6 proteins with fibulin-1 Biochem Biophys Res Commun 296 962 969
21. PJ Duerksen-Hughes J Yang SB Schwartz 1999 HPV 16 E6 blocks TNF-mediated apoptosis in mouse fibroblast LM cells Virology 264 55 65
22. N Dyson PM Howley K Munger E Harlow 1989 The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product Science 243 934 937
23. M Filippova H Song JL Connolly TS Dermody PJ Duerksen-Hughes 2002 The human papillomavirus 16 E6 protein binds to tumor necrosis factor (TNF) R1 and protects cells from TNF-induced apoptosis J Biol Chem 277 21730 21739
24. M Filippova L Parkhurst PJ Duerksen-Hughes 2004 The human papillomavirus 16 E6 protein binds to Fas-associated death domain and protects cells from Fas-triggered apoptosis J Biol Chem 279 25729 25744
25. M Filippova TA Brown-Bryan CA Casiano PJ Duerksen-Hughes 2005 The human papillomavirus 16 E6 protein can either protect or further sensitize cells to TNF: effect of dose Cell Death Differ 12 1622 1635
26. P Finzer A Aguilar-Lemarroy F Rosl 2002 The role of human papillomavirus oncoproteins E6 and E7 in apoptosis Cancer Lett 188 15 24
27. N Gammoh HS Grm P Massimi L Banks 2006 Regulation of human papillomavirus type 16 E7 activity through direct protein interaction with the E2 transcriptional activator J Virol 80 1787 1797
28. Q Gao S Srinivasan SN Boyer DE Wazer V Band 1999 The E6 oncoproteins of high-risk papillomaviruses bind to a novel putative GAP protein, E6TP1, and target it for degradation Mol Cell Biol 19 733 744
29. Garnett TO, Filippova M, Duerksen-Hughes PJ (2006) Accelerated degradation of FADD and procaspase 8 in cells expressing human papilloma virus 16 E6 impairs TRAIL-mediated apoptosis. Cell Death Differ [Epub ahead of print] Doi: 10.1038/sj.cdd.4401886
30. U Gaur BB Aggarwal 2003 Regulation of proliferation, survival and apoptosis by members of the TNF superfamily Biochem Pharmacol 66 1403 1408
31. BA Glaunsinger SS Lee M Thomas L Banks R Javier 2000 Interactions of the PDZ-protein MAGI-1 with adenovirus E4-ORF1 and high-risk papillomavirus E6 oncoproteins Oncogene 19 5270 5280
32. EC Goodwin E Yang CJ Lee HW Lee D DiMaio ES Hwang 2000 Rapid induction of senescence in human cervical carcinoma cells Proc Natl Acad Sci USA 97 10978 10983
33. DR Green 2006 At the gates of death Cancer Cell 9 328 330
34. S Gross-Mesilaty E Reinstein B Bercovich KE Tobias AL Schwartz C Kahana A Ciechanover 1998 Basal and human papillomavirus E6 oncoprotein-induced degradation of Myc proteins by the ubiquitin pathway Proc Natl Acad Sci USA 95 8058 8063
35. AH Hall KA Alexander 2003 RNA interference of human papillomavirus type 18 E6 and E7 induces senescence in HeLa cells J Virol 77 6066 6069
36. R Herber A Liem H Pitot PF Lambert 1996 Squamous epithelial hyperplasia and carcinoma in mice transgenic for the human papillomavirus type 16 E7 oncogene J Virol 70 1873 1881
37. P Hubert SL Giannini A Vanderplasschen E Franzen-Detrooz N Jacobs J Boniver P Delvenne 2001 Dendritic cells induce the death of human papillomavirus-transformed keratinocytes FASEB J 15 2521 2523
38. 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 4135
39. MA James JH Lee AJ Klingelhutz 2006 Human papillomavirus type 16 E6 activates NF-κB, induces cIAP-2 expression, and protects against apoptosis in a PDZ binding motif-dependent manner J Virol 80 5301 5307
40. K Kabsch A Alonso 2002 The human papillomavirus type 16 E5 protein impairs TRAIL- and FasL-mediated apoptosis in HaCaT cells by different mechanisms J Virol 76 12162 12172
41. DW Kaznelson S Bruun A Monrad S Gjerlov J Birk C Ropke B Norrild 2004 Simultaneous human papilloma virus type 16 E7 and cdk inhibitor p21 expression induces apoptosis and cathepsin B activation Virology 320 301 312
42. T Kiyono A Hiraiwa M Fujita Y Hayashi T Akiyama M 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
43. C Kuhne L Banks 1998 E3-ubiquitin ligase/E6-AP links multicopy maintenance protein 7 to the ubiquitination pathway by a novel motif, the L2G box J Biol Chem 273 34302 34309
44. I Kukimoto S Aihara K Yoshiike T Kanda 1998 Human papillomavirus oncoprotein E6 binds to the C-terminal region of human minichromosome maintenance 7 protein Biochem Biophys Res Commun 249 258 262
45. SS Lee RS Weiss RT 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
46. SS Lee B Glaunsinger F Mantovani L Banks RT Javier 2000 Multi-PDZ domain protein MUPP1 is a cellular target for both adenovirus E4-ORF1 and high-risk papillomavirus type 18 E6 oncoproteins J Virol 74 9680 9693
47. Y Liu V Tergaonkar S Krishna EJ Androphy 1999 Human papillomavirus type 16 E6-enhanced susceptibility of L929 cells to tumor necrosis factor alpha correlates with increased accumulation of reactive oxygen species J Biol Chem 274 24819 24827
48. MS Longworth LA Laimins 2004 Pathogenesis of human papillomaviruses in differentiating epithelia Microbiol Mol Biol Rev 68 362 372
49. MS Longworth LA Laimins 2004 The binding of histone deacetylases and the integrity of zinc finger-like motifs of the E7 protein are essential for the life cycle of human papillomavirus type 31 J Virol 78 3533 3541
50. B Mannhardt SA Weinzimer M Wagner M Fiedler P Cohen P Jansen-Durr W Zwerschke 2000 Human papillomavirus type 16 E7 oncoprotein binds and inactivates growth-inhibitory insulin-like growth factor binding protein 3 Mol Cell Biol 20 6483 6495
51. F Mantovani L Banks 2001 The human papillomavirus E6 protein and its contribution to malignant progression Oncogene 20 7874 7887
52. P Massimi D Pim A Storey L Banks 1996 HPV-16 E7 and adenovirus E1a complex formation with TATA box binding protein is enhanced by casein kinase II phosphorylation Oncogene 12 2325 2330
53. P Massimi L Banks 2005 Transformation assays for HPV oncoproteins Methods Mol Med 119 381 395
54. S Mazurek W Zwerschke P Jansen-Durr E Eigenbrodt 2001 Metabolic cooperation between different oncogenes during cell transformation: interaction between activated ras and HPV-16 E7 Oncogene 20 6891 6898
55. JM Mazzarelli GB Atkins JV Geisberg RP Ricciardi 1995 The viral oncoproteins Ad5 E1A, HPV16 E7 and SV40 TAg bind a common egion of the TBP-associated factor-110 Oncogene 11 1859 1864
56. K Munger PM Howley 2002 Human papillomavirus immortalization and transformation functions Virus Res 89 213 228
57. S Nakagawa JM Huibregtse 2000 Human scribble (Vartul) is targeted for ubiquitin-mediated degradation by the high-risk papillomavirus E6 proteins and the E6AP ubiquitin-protein ligase Mol Cell Biol 20 8244 8253
58. 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 6964
59. I Oelze J Kartenbeck K Crusius A Alonso 1995 Human papillomavirus type 16 E5 protein affects cell-cell communication in an epithelial cell line J Virol 69 4489 4494
60. JL Parish A Kowalczyk HT Chen GE Roeder R Sessions M Buckle K Gaston 2006 E2 proteins from high- and low-risk human papillomavirus types differ in their ability to bind p53 and induce apoptotic cell death J Virol 80 4580 4590
61. 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 6769
62. DM Parkin F Bray J Ferlay P Pisani 2001 Estimating the world cancer burden: Globocan 2000 Int J Cancer 94 153 156
63. D Patel SM Huang LA Baglia DJ [tmp] McCance 1999 The E6 protein of human papillomavirus type 16 binds to and inhibits co-activation by CBP and p300 EMBO J 18 5061 5072
64. 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 Pt 4 905 909
65. D Pim M Collins L Banks 1992 Human papillomavirus type 16 E5 gene stimulates the transforming activity of the epidermal growth factor receptor Oncogene 7 27 32
66. D Pim P Massimi SM Dilworth L Banks 2005 Activation of the protein kinase B pathway by the HPV-16 E7 oncoprotein occurs through a mechanism involving interaction with PP2A Oncogene 24 7830 7838
67. P Pisani F Bray DM Parkin 2002 Estimates of the world-wide prevalence of cancer for 25 sites in the adult population International Journal of Cancer 97 72 81
68. T Prathapam C Kuhne L Banks 2001 The HPV-16 E7 oncoprotein binds Skip and suppresses its transcriptional activity Oncogene 20 7677 7685
69. 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 2072
70. CM Rudin CB Thompson 1997 Apoptosis and disease: regulation and clinical relevance of programmed cell death Annu Rev Med 48 267 281
71. 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 1136
72. S Song HC Pitot PF Lambert 1999 The human papillomavirus type 16 E6 gene alone is sufficient to induce carcinomas in transgenic animals J Virol 73 5887 5893
73. KS Srivenugopal F Ali-Osman 2002 The DNA repair protein, O(6)-methylguanine-DNA methyltransferase is a proteolytic target for the E6 human papillomavirus oncoprotein Oncogene 21 5940 5945
74. MH Stoler CR Rhodes A Whitbeck SM Wolinsky LT Chow TR Broker 1992 Human papillomavirus type 16 and 18 gene expression in cervical neoplasias Hum Pathol 23 117 128
75. H Stoppler MC Stoppler E Johnson CM Simbulan-Rosenthal ME Smulson S Iyer DS Rosenthal R Schlegel 1998 The E7 protein of human papillomavirus type 16 sensitizes primary human keratinocytes to apoptosis Oncogene 17 1207 1214
76. MC Stoppler SW Straight G Tsao R Schlegel DJ [tmp] McCance 1996 The E5 gene of HPV-16 enhances keratinocyte immortalization by full-length DNA Virology 223 251 254
77. SW Straight PM Hinkle RJ Jewers DJ [tmp] McCance 1993 The E5 oncoprotein of human papillomavirus type 16 transforms fibroblasts and effects the downregulation of the epidermal growth factor receptor in keratinocytes J Virol 67 4521 4532
78. S Tang M Tao JP [tmp] McCoy Jr ZM Zheng 2006 The E7 oncoprotein is translated from spliced E6*I transcripts in high-risk human papillomavirus type 16- or type 18-positive cervical cancer cell lines via translation reinitiation J Virol 80 4249 4263
79. M Thomas L Banks 1998 Inhibition of Bak-induced apoptosis by HPV-18 E6 Oncogene 17 2943 2954
80. M Thomas L Banks 1999 Human papillomavirus (HPV) E6 interactions with Bak are conserved amongst E6 proteins from high and low risk HPV types J Gen Virol 80 Pt 6 1513 1517
81. M Thomas B Glaunsinger D Pim R Javier L Banks 2001 HPV E6 and MAGUK protein interactions: determination of the molecular basis for specific protein recognition and degradation Oncogene 20 5431 5439
82. M Thomas R Laura K Hepner E Guccione C Sawyers L Lasky L Banks 2002 Oncogenic human papillomavirus E6 proteins target the MAGI-2 and MAGI-3 proteins for degradation Oncogene 21 5088 5096
83. DA Thompson V Zacny GS Belinsky M Classon DL Jones R Schlegel K Munger 2001 The HPV E7 oncoprotein inhibits tumor necrosis factor alpha-mediated apoptosis in normal human fibroblasts Oncogene 20 3629 3640
84. P Thomsen B van Deurs B Norrild L Kayser 2000 The HPV16 E5 oncogene inhibits endocytic trafficking Oncogene 19 6023 6032
85. L Thyrell O Sangfelt B Zhivotovsky K Pokrovskaja Y Wang S Einhorn D Grander 2005 The HPV-16 E7 oncogene sensitizes malignant cells to IFN-alpha-induced apoptosis J Interferon Cytokine Res 25 63 72
86. 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 8 195 202
87. X Tong PM Howley 1997 The bovine papillomavirus E6 oncoprotein interacts with paxillin and disrupts the actin cytoskeleton Proc Natl Acad Sci USA 94 4412 4417
88. YP Tsao LY Li TC Tsai SL Chen 1996 Human papillomavirus type 11 and 16 E5 represses p21(WafI/SdiI/CipI) gene expression in fibroblasts and keratinocytes J Virol 70 7535 7539
89. J Viac Y Chardonnet MC Chignol D Schmitt 1993 Papilloma viruses, warts, carcinoma and Langerhans cells In Vivo 7 207 212
90. F Vikhanskaya C Falugi P Valente P Russo 2002 Human papillomavirus type 16 E6-enhanced susceptibility to apoptosis induced by TNF in A2780 human ovarian cancer cell line Int J Cancer 97 732 739
91. Vogt M, Butz K, Dymalla S, Semzow J, Hoppe-Seyler F (2006) Inhibition of Bax activity is crucial for the antiapoptotic function of the human papillomavirus E6 oncoprotein. Oncogene [Epub] Doi: 10.1038/sj.onc.1209429
92. 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 4934
93. MJ Welters A de Jong SJ van den Eeden JM van der Hulst KM Kwappenberg S Hassane KL Franken JW Drijfhout GJ Fleuren G Kenter CJ Melief R Offringa SH van der Burg 2003 Frequent display of human papillomavirus type 16 E6-specific memory t-Helper cells in the healthy population as witness of previous viral encounter Cancer Res 63 636 641
94. MJ Welters P van der Logt SJ van den Eeden KM Kwappenberg JW Drijfhout GJ Fleuren GG Kenter CJ Melief SH van der Burg R Offringa 2006 Detection of human papillomavirus type 18 E6 and E7-specific CD4+ T-helper 1 immunity in relation to health versus disease Int J Cancer 118 950 956
95. BA Werness AJ Levine PM Howley 1990 Association of human papillomavirus types 16 and 18 E6 proteins with p53 Science 248 76 79
96. 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 5078
97. M Zeng A Kumar G Meng Q Gao G Dimri D Wazer H Band V Band 2002 Human papilloma virus 16 E6 oncoprotein inhibits retinoic X receptor-mediated transactivation by targeting human ADA3 coactivator J Biol Chem 277 45611 45618
98. H Zimmermann R Degenkolbe HU Bernard MJ O'Connor 1999 The human papillomavirus type 16 E6 oncoprotein can down-regulate p53 activity by targeting the transcriptional coactivator CBP/p300 J Virol 73 6209 6219