Human papillomavirus infection, cancer & therapy

Indian Journal of Medical Research

Volumn 130, Issue 3, 2009, Pages 277-285

  Grm, Helena Sterlinko ^a   Bergant, Martina ^a   Banks, Lawrence ^b  

^a UNIVERSITY OF NOVA GORICA   (Slovenia)

^b INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

Author keywords

E6; E7; Hpv; Protein targets; Therapy

Indexed keywords

PROTEIN E6; PROTEIN E7; WART VIRUS VACCINE;

CANCER SCREENING; CONDYLOMA ACUMINATUM; DRUG EFFICACY; DRUG RESEARCH; DRUG SAFETY; HUMAN; NONHUMAN; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; PUBLIC HEALTH PROBLEM; REVIEW; UTERINE CERVIX CANCER; UTERINE CERVIX CARCINOMA; VERRUCA VULGARIS; VIROGENESIS; VIRUS CARCINOGENESIS; VIRUS INFECTION; WART VIRUS;

ANIMALS; FEMALE; HUMANS; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; PAPILLOMAVIRUS VACCINES; UTERINE CERVICAL NEOPLASMS;

EID: 72649099241     PISSN: 09715916     EISSN: 09715916     Source Type: Journal    
DOI: None     Document Type: Review

References (100)

1. zur Hausen H. Papillomaviruses and cancer: from basic studies to clinical application. Nat Rev Cancer 2002; 2: 342-50.
2. zur Hausen H. Papillomavirus infections-a major cause of human cancers. Biochim Biophys Acta 1996; 1288: F55-78.
3. Bosch Fx, Lorincz A, Muñoz N, Meijer CJ, Shah KV. The causal relation between human papillomavirus and cervical cancer. J Clin Pathol 2002; 55: 244-65.
4. Clifford GM, Smith JS, Aguado T, Franceschi S. Comparison of HPV type distribution in high-grade cervical lesions and cervical cancer: a meta-analysis. Br J Cancer 2003; 89: 101-5.
5. Zielinski GD, Snijders PJ, Rozendaal L, Daalmeijer NF, Risse EK, Voorhorst FJ, et al. The presence of high-risk HPV combined with specific p53 and p16INK4a expression patterns points to high-risk HPV as the main causative agent for adenocarcinoma in situ and adenocarcinoma of the cervix. J Pathol 2003; 201: 535-43.
6. Bosch Fx, Manos MM, Munoz N, Sherman M, Jansen AM, Peto J, et al. Prevalence of human papillomavirus in cervical cancer: a world-wide perspective. International biological study on cervical cancer (IBSCC) study group. J Natl Cancer Inst 1995; 87: 796-801.
7. Bosch Fx, Lorincz A, Munoz N, Meijer CJ, Shah KV. The causal relation between human papillomavirus and cervical cancer. J Clin Pathol 2002; 55: 244-65.
8. Watt FM. Epidermal stem cells: markers, patterning and the control of stem cell fate. Philos Trans R Soc Lond B Biol Sci 1998; 353: 831-7.
9. Doorbar J. The papillomavirus life cycle. J Clin Virol 2005; 32 (Suppl 1): S7-15
10. Hebner CM, Laimins LA. Human papillomaviruses: basic mechanisms of pathogenesis and oncogenicity. Rev Med Virol 2006; 16: 83-97.
11. Zhang B, Chen W, Roman A. The E7 proteins of low- and high-risk human papillomaviruses share the ability to target the pRB family member p130 for degradation. Proc Natl Acad Sci USA 2006; 103: 437-42.
12. Genovese NJ, Banerjee NS, Broker TR, Chow LT. Casein kinase II motif-dependent phosphorylation of the human papillomavirus E7 protein promotes p130 degradation and S-phase induction in differentiated human keratinocytes. J Virol 2008; 82: 4862-73.
13. Brehm A, Nielsen SJ, Miska EA, McCance DJ, Reid JL, Bannister AJ, et al. The E7 oncoprotein associates with Mi2 and histone deacetylase activity to promote cell growth. EMBO J 1999; 18: 2449-58.
14. McCance DJ. The human papillomavirus type 16 E7 gene product interacts with and trans-activates the AP1 family of transcription factors. EMBO J 1996; 15:1950-60.
15. Funk JO, Waga S, Harry JB, Espling E, Stillman B, Galloway DA. Inhibition of CDK activity and PCNA-dependent DNA replication by p21 is blocked by interaction with the HPV16 E7 oncoprotein. Genes Dev 1997; 11: 2090-100.
16. Coote JH, Arrand JR. Leaky scanning is the predominant mechanism for translation of human papillomavirus type 16 E7 oncoprotein from E6/E7 bicistronic mRNA. J Virol 2000; 74: 7284-97.
17. Scheffner M, Werness BA, Huibregtse JM, Levine AJ, Howley PM. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 1990; 63: 1129-36.
18. Thomas M, Pim D, Banks L. The role of the E6-p53 interaction in the molecular pathogenesis of HPV. Oncogene 1999; 18: 7690-700.
19. Thomas M, Banks L. Inhibition of Bak-induced apoptosis by HPV-18 E6. Oncogene 1998; 17: 2943-54.
20. Li B, Dou QP. Bax degradation by the ubiquitin/proteasome- dependent pathway: involvement in tumor survival and progression. Proc Natl Acad Sci USA 2000; 97: 3850-5.
21. Mantovani F, Banks L. The human papillomavirus E6 protein and its contribution to malignant progression. Oncogene 2001; 20: 7874-87.
22. Nguyen ML, Nguyen MM, Lee D, Griep AE, Lambert PF. 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 2003; 77: 6957-64.
23. Nguyen MM, Nguyen ML, Caruana G, Bernstein A, Lambert PF, Griep AE. Requirement of PDZ-containing proteins for cell cycle regulation and differentiation in the mouse lens epithelium. Mol Cell Biol 2003; 23: 8970-81.
24. Doorbar J, Foo C, Coleman N, Medcalf L, Hartley O, Prospero T, et al. Characterization of events during the late stages of HPV16 infection in vivo using high-affinity synthetic Fabs to E4. Virology 1997; 238: 40-52.
25. Munger K, Phelps WC, Bubb V, Howley PM, Schlegel R. The E6 and E7 genes of human papillomavirus type 16 are necessary and sufficient for transformation of primary human keratinocytes. J Virol 1989; 63: 4417-23.
26. Hawley-Nelson P, Vousden KH, Hubbert NL, Lowy DR, Schiller JT. HPV 16 E6 and E7 proteins cooperate to immortalize human foreskin keratinocytes. EMBO J 1989; 8: 3905-10.
27. Barbosa MS, Schlegel R. The E6 and E7 genes of HPV-18 are sufficient for inducing two-stage in vitro transformation of human keratinocytes. Oncogene 1989; 4: 1529-32.
28. Münger K, Baldwin A, Edwards KM, Hayakawa H, Nguyen CL, Owens M, et al. Mechanisms of human papillomavirus-induced oncogenesis. J Virol 2004; 78: 11451-60.
29. von Knebel Doeberitz M. New markers for cervical dysplasia to visualise the genomic chaos created by aberrant oncogenic papillomavirus infections. Eur J Cancer 2002; 38: 2229-42.
30. Pett M, Coleman N. Integration of high-risk human papillomavirus: a key event in cervical carcinogenesis? J Pathol 2007; 212: 356-67.
31. Vinokurova S, Wentzensen N, Kraus I, Klaes R, Driesch C, Melsheimer P, et al. Type-dependent integration frequency of human papillomavirus genomes in cervical lesions. Cancer Res 2008; 68: 307-13.
32. Yee C, Krishnan-Hewlett I, Baker CC, Schlegel R, Howley PM. Presence and expression of human papillomavirus sequences in human cervical carcinoma cell lines. Am J Pathol 1985; 119: 361-6.
33. Schwarz E, Freese U, Gissmann L, Mayer W, Roggenbuck B, Stremlau A, et al. Structure and transcription of human papillomavirus sequences in cervical carcinoma cells. Nature 1985; 314: 111-4.
34. Baker CC, Phelps WC, Lindgren V, Braun MJ, Gonda MA, Howley PM. Structural and transcriptional analysis of human papillomavirus type 16 sequences in cervical carcinoma cell lines. J Virol 1987; 61: 962-71.
35. Auewarakul P, Gissmann L, Cid-Arregui A. Targeted expression of the E6 and E7 oncogenes of human papillomavirus type 16 in the epidermis of transgenic mice elicits generalized epidermal hyperplasia involving autocrine factors. Mol Cell Biol 1994; 14: 8250-8.
36. Arbeit JM, Münger K, Howley PM, Hanahan D. Neuroepithelial carcinomas in mice transgenic with human papillomavirus type 16 E6/E7 ORFs. Am J Pathol 1993; 142: 1187-97.
37. Griep AE, Herber R, Jeon S, Lohse JK, Dubielzig RR, Lambert PF. Tumorigenicity by human papillomavirus type 16 E6 and E7 in transgenic mice correlates with alterations in epithelial cell growth and differentiation. J Virol 1993; 67: 1373-84.
38. Comerford SA, Maika SD, Laimins LA, Messing A, Elsässer HP, Hammer RE. E6 and E7 expression from the HPV 18 LCR: development of genital hyperplasia and neoplasia in transgenic mice. Oncogene 1995; 10: 587-97.
39. Arbeit JM, Münger K, Howley PM, Hanahan D. Progressive squamous epithelial neoplasia in K14-human papillomavirus type 16 transgenic mice. J Virol 1994; 68: 4358-68.
40. Herber R, Liem A, Pitot H, Lambert PF. Squamous epithelial hyperplasia and carcinoma in mice transgenic for the human papillomavirus type 16 E7 oncogene. J Virol 1996; 70: 1873-81.
41. Song S, Pitot HC, Lambert PF. The human papillomavirus type 16 E6 gene alone is sufficient to induce carcinomas in transgenic animals. J Virol 1999; 73: 5887-93.
42. Simonson SJ, Difilippantonio MJ, Lambert PF. Two distinct activities contribute to human papillomavirus 16 E6's oncogenic potential. Cancer Res 2005; 65: 8266-73.
43. Arbeit JM, Howley PM, Hanahan D. Chronic estrogen-induced cervical and vaginal squamous carcinogenesis in human papillomavirus type 16 transgenic mice. Proc Natl Acad Sci USA 1996; 93: 2930-5.
44. Elson DA, Riley RR, Lacey A, Thordarson G, Talamantes FJ, Arbeit JM. Sensitivity of the cervical transformation zone to estrogen-induced squamous carcinogenesis. Cancer Res 2000; 60: 1267-75.
45. Riley RR, Duensing S, Brake T, Münger K, Lambert PF, Arbeit JM. Dissection of human papillomavirus E6 and E7 function in transgenic mouse models of cervical carcinogenesis. Cancer Res 2003; 63: 4862-71.
46. Doorbar J, Cubie H. Molecular basis for advances in cervical screening. Mol Diagn 2005; 9: 129-42.
47. Lin YY, Alphs H, Hung CF, Roden RB, Wu TC. Vaccines against human papillomavirus. Front Biosci 2007; 12: 246-64.
48. Wright TC, Bosch Fx, Franco EL, Cuzick J, Schiller JT, Garnett GP, et al. Chapter 30: HPV vaccines and screening in the prevention of cervical cancer; conclusions from a 2006 workshop of international experts. Vaccine 2006; 24 Suppl 3: 251-61.
49. Sterlinko Grm H, Banks L. HPV proteins as targets for therapeutic intervention. Antivir Ther 2004; 9: 665-78.
50. Kim SW, Yang JS. Human papillomavirus type 16 E5 protein as a therapeutic target. Yonsei Med J 2006; 47: 1-14.
51. Schaal TD, Mallet WG, McMinn DL, Nguyen NV, Sopko MM, John S, et al. Inhibition of human papilloma virus E2 DNA binding protein by covalently linked polyamides. Nucleic Acids Res 2003; 31: 1282-91.
52. White PW, Titolo S, Brault K, Thauvette L, Pelletier A, Welchner E, et al. Inhibition of human papillomavirus DNA replication by small molecule antagonists of the E1-E2 protein interaction. J Biol Chem 2003; 278: 26765-72.
53. Mino T, Hatono T, Matsumoto N, Mori T, Mineta Y, Aoyama Y, et al. Inhibition of DNA replication of human papillomavirus by artificial zinc finger proteins. J Virol 2006; 80: 5405-12.
54. Smotkin D, Wettstein FO. Transcription of human papillomavirus type 16 early genes in a cervical cancer and a cancer-derived cell line and identification of the E7 protein. Proc Natl Acad Sci USA 1986; 83: 4680-4.
55. Androphy EJ, Hubbert NL, Schiller JT, Lowy DR. Identification of the HPV-16 E6 protein from transformed mouse cells and human cervical carcinoma cell lines. EMBO J 1987; 6: 989-92.
56. Banks L, Spence P, Androphy E, Hubbert N, Matlashewski G, Murray A, et al. Identification of human papillomavirus type 18 E6 polypeptide in cells derived from human cervical carcinomas. J Gen Virol 1987; 68: 1351-9.
57. von Knebel Doeberitz M, Oltersdorf T, Schwarz E, Gissmann L. Correlation of modified human papilloma virus early gene expression with altered growth properties in C4-1 cervical carcinoma cells. Cancer Res 1988; 48: 3780-6.
58. Crook T, Morgenstern JP, Crawford L, Banks L. Continued expression of HPV-16 E7 protein is required for maintenance of the transformed phenotype of cells co-transformed by HPV-16 plus EJ-ras. EMBO J 1989; 8: 513-9.
59. Storey A, Massimi P, Dawson K, Banks L. Conditional immortalization of primary cells by human papillomavirus type 18 E6 and EJ-ras defines an E6 activity in G0/G1 phase which can be substituted for mutations in p53. Oncogene 1995; 11: 653-61.
60. Flores ER, Allen-Hoffmann BL, Lee D, Lambert PF. The human papillomavirus type 16 E7 oncogene is required for the productive stage of the viral life cycle. J Virol 2000; 74: 6622-31.
61. Thomas JT, Hubert WG, Ruesch MN, Laimins LA. Human papillomavirus type 31 oncoproteins E6 and E7 are required for the maintenance of episomes during the viral life cycle in normal human keratinocytes. Proc Natl Acad Sci USA 1999; 96: 8449-54.
62. Park RB, Androphy EJ. Genetic analysis of high-risk e6 in episomal maintenance of human papillomavirus genomes in primary human keratinocytes. J Virol 2002; 76: 11359-64.
63. Oh ST, Longworth MS, Laimins LA. Roles of the E6 and E7 proteins in the life cycle of low-risk human papillomavirus type 11. J Virol 2004; 78: 2620-6.
64. Goodwin EC, DiMaio D. Repression of human papillomavirus oncogenes in HeLa cervical carcinoma cells causes the orderly reactivation of dormant tumor suppressor pathways. Proc Natl Acad Sci USA 2000; 97: 12513-8.
65. Hamada K, Sakaue M, Alemany R, Zhang W, Horio Y, Roth J, et al. Adenovirus-mediated transfer of HPV 16 E6/E7 antisense RNA to human cervical cancer cells. Gynecol Oncol 1996; 63: 219-27.
66. Márquez-Gutiérrez MA, Benítez-Hess ML, DiPaolo JA, Alvarez-Salas LM. Effect of combined antisense oligodeoxynucleotides directed against the human papillomavirus type 16 on cervical carcinoma cells. Arch Med Res 2007; 38: 730-8.
67. Alvarez-Salas LM, Arpawong TE, DiPaolo JA. Growth inhibition of cervical tumor cells by antisense oligodeoxynucleotides directed to the human papillomavirus type 16 E6 gene. Antisense Nucleic Acid Drug Dev 1999; 9: 441-50.
68. Alvarez-Salas L. Cullinan A, Siwkowski A, Hampel A, DiPaolo D. Inhibition of HPV-16 E6/E7 immortalization of normal keratinocytes by hairpin ribozymes. Proc Natl Acad Sci USA 1998; 95: 1189-94.
69. Zheng Y, Zhang J, Rao Z. Ribozyme targeting HPV16 E6E7 transcripts in cervical cancer cells suppresses cell growth and sensitizes cells to chemotherapy and radiotherapy. Cancer Biol Ther 2004; 3: 1129-34.
70. Alvarez-Salas LM, Benítez-Hess ML, DiPaolo JA. Advances in the development of ribozymes and antisense oligodeoxynucleotides as antiviral agents for human papillomaviruses. Antivir Ther 2003; 8: 265-78.
71. Hall AHS, Alexsander KA. RNA interference of human papillomavirus type 18 E6 and E7 induces senescence in HeLa cells. J Virol 2003; 77: 6066-9.
72. Butz K, Ristriani T, Hengstermann A, Denk C, Scheffner M, Hoppe-Seyler F. siRNA targeting of the viral E6 oncogene efficiently kills human papillomavirus-positive cancer cells. Oncogene 2003; 22: 5938-45.
73. Yamato K, Yamada T, Kizaki M, Ui-Tei K, Natori Y, Fujino M, et al. New highly potent and specific E6 and E7 siRNAs for treatment of HPV16 positive cervical cancer. Cancer Gene Ther 2008; 15: 140-53.
74. Sima N, Wang W, Kong D, Deng D, xu Q, Zhou J, et al. RNA interference against HPV16 E7 oncogene leads to viral E6 and E7 suppression in cervical cancer cells and apoptosis via upregulation of Rb and p53. Apoptosis 2008; 13: 273-81.
75. Goodwin EC, DiMaio D. Repression of human papillomavirus oncogenes in HeLa cervical carcinoma cells causes the orderly reactivation of dormant tumor suppressor pathways. Proc Natl Acad Sci USA 2000; 97: 12513-8.
76. Wells SI, Francis DA, Karpova AY, Dowhanick JJ, Benson JD, Howley PM. Papillomavirus E2 induces senescence in HPV-positive cells via pRB- and p21(CIP)-dependent pathways. EMBO J 2000; 19: 5762-71.
77. Butz K, Denk C, Ullmann A, Scheffner M, Hoppe-Seyler F. Induction of apoptosis in human papillomaviruspositive cancer cells by peptide aptamers targeting the viral E6 oncoprotein. Proc Natl Acad Sci USA 2000; 97:6693-7.
78. Griffin H, Elston R, Jackson D, Ansell K, Coleman M, Winter G, et al. Inhibition of papillomavirus protein function in cervical cancer cells by intrabody targeting. J Mol Biol 2006; 355: 360-78.
79. Butz K, Shahabeddin L, Geisen C, Spitkovsky D, Ullmann A, Hoppe-Seyler F. Functional p53 protein in human papillomavirus-positive cancer cells. Oncogene 1995; 10: 927-36.
80. Butz K, Whitaker N, Denk C, Ullmann A, Geisen C, Hoppe-Seyler F. Induction of the p53-target gene GADD45 in HPV-positive cancer cells. Oncogene 1999; 18: 2381-6.
81. Huibregtse JM, Scheffner M, Howley PM. Localization of the E6-AP regions that direct human papillomavirus E6 binding, association with p53, and ubiquitination of associated proteins. Mol Cell Biol 1993; 13: 4918-27.
82. Huibregtse JM, Scheffner M, Howley PM. 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 1993; 13: 775-84.
83. Hengstermann A, Linares LK, Ciechanover A, Whitaker NJ, Scheffner M. Complete switch from Mdm2 to human papillomavirus E6-mediated degradation of p53 in cervical cancer cells. Proc Natl Acad of Sci USA 2001; 98: 1218-23.
84. Beer-Romero P, Glass S, Rolfe M. Antisense targeting of E6AP elevates p53 in HPV-infected cells but not in normal cells. Oncogene 1997; 14: 595-602.
85. Mantovani F, Banks L. Inhibition of E6 induced degradation of p53 is not sufficient for stabilization of p53 protein in cervical tumour derived cell lines. Oncogene 1999; 18: 3309-15.
86. Narisawa-Saito M, Kiyono T. Basic mechanisms of high-risk human papillomavirus-induced carcinogenesis: roles of E6 and E7 proteins. Cancer Sci 2007; 98: 1505-11.
87. Liu Y, Chen JJ, Gao Q, Dalal S, Hong Y, Mansur CP, et al. Multiple functions of human papillomavirus type 16 E6 contribute to the immortalization of mammary epithelial cells. J Virol 1999; 73: 7297-307.
88. Nakagawa S, Watanabe S, Yoshikawa H, Taketani Y, Yoshiike K, Kanda T. Mutational analysis of human papillomavirus type 16 E6 protein: transforming function for human cells and degradation of p53 in vitro. Virology 1995; 212: 535-42.
89. Pan H, Griep AE. Temporally distinct patterns of p53-dependent and p53-independent apoptosis during mouse lens development. Genes Dev 1995; 9: 2157-69.
90. Pim D, Storey A, Thomas M, Massimi P, Banks L. Mutational analysis of HPV-18 E6 identifies domains required for p53 degradation in vitro, abolition of p53 transactivation in vivo and immortalisation of primary BMK cells. Oncogene 1994; 9: 1869-76.
91. Kiyono T, Foster SA, Koop JI, McDougall JK, Galloway DA, Klingelhutz AJ. Both Rb/p16INK4a inactivation and telomerase activity are required to immortalize human epithelial cells. Nature 1998; 396: 84-8.
92. Kiyono T, Hiraiwa A, Fujita M, Hayashi Y, Akiyama T, Ishibashi M. 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 1997; 94: 11612-6.
93. Elbel M, Carl S, Spaderna S, Iftner T. A comparative analysis of the interactions of the E6 proteins from cutaneous and genital papillomaviruses with p53 and E6AP in correlation to their transforming potential. Virology 1997; 239: 132-49.
94. Kemp CJ, Donehower LA, Bradley A, Balmain A. Reduction of p53 gene dosage does not increase initiation or promotion but enhances malignant progression of chemically induced skin tumors. Cell 1993; 74: 813-22.
95. Chen JJ, Reid CE, Band V, Androphy EJ. Interaction of papillomavirus E6 oncoproteins with a putative calcium-binding protein. Science 1995; 269: 529-31.
96. Morais Cabral JH, Petosa C, Sutcliffe MJ, Raza S, Byron O, Poy F, et al. Crystal structure of a PDZ domain. Nature 1996; 382: 649-52.
97. Doyle DA, Lee A, Lewis J, Kim E, Sheng M, MacKinnon R. Crystal structures of a complexed and peptide-free membrane protein-binding domain: molecular basis of peptide recognition by PDZ. Cell 1996; 85: 1067-76.
98. Hillier BJ, Christopherson KS, Prehoda KE, Bredt DS, Lim WA. Unexpected modes of PDZ domain scaffolding revealed by structure of nNOS-syntrophin complex. Science 1999; 284: 812-5.
99. Zhang Y, Dasgupta J, Ma RZ, Banks L, Thomas M, Chen xS. Structures of a human papillomavirus (HPV) E6 polypeptide bound to MAGUK proteins: mechanisms of targeting tumor suppressors by a high-risk HPV oncoprotein. J Virol 2007; 81: 3618-26.
100. Sterlinko Grm H, Weber M, Elston R, McIntosh P, Griffin H, Banks L, et al. Inhibition of E6-induced degradation of its cellular substrates by novel blocking peptides. J Mol Biol 2004; 335: 971-85.