Targeting the human papillomavirus E6 and E7 oncogenes through expression of the bovine papillomavirus type 1 E2 protein stimulates cellular motility

Journal of Virology

Volumn 85, Issue 20, 2011, Pages 10487-10498

  Morrison, Monique A ^a   Morreale, Richard J ^a   Akunuru, Shailaja ^a   Kofron, Matthew ^a   Zheng, Yi ^a   Wells, Susanne I ^a  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

E2 PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; BOVINE PAPILLOMAVIRUS TYPE 1; CELL AGING; CELL CONTACT; CELL CYCLE ARREST; CELL INVASION; CELL MIGRATION; CELL MOTILITY; CONTROLLED STUDY; E6 ONCOGENE; E7 ONCOGENE; EPITHELIAL MESENCHYMAL TRANSITION; GENE REPRESSION; HELA CELL; HUMAN; HUMAN CELL; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; RNA INTERFERENCE; WART VIRUS;

BOVINE PAPILLOMAVIRUS 1; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; DNA-BINDING PROTEINS; HUMANS; ONCOGENE PROTEINS, VIRAL; VIRAL PROTEINS;

BOVINE PAPILLOMAVIRUS TYPE 1; HUMAN PAPILLOMAVIRUS;

EID: 80054985859     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.05126-11     Document Type: Article

References (67)

1. Au, W. W., S. Abdou-Salama, and A. Al-Hendy. 2007. Inhibition of growth of cervical cancer cells using a dominant negative estrogen receptor gene. Gynecol. Oncol. 104:276-280.
2. Bechtold, V., P. Beard, and K. Raj. 2003. Human papillomavirus type 16 E2 protein has no effect on transcription from episomal viral DNA. J. Virol. 77:2021-2028.
3. Butz, K., C. Denk, A. Ullmann, M. Scheffner, and F. Hoppe-Seyler. 2000. Induction of apoptosis in human papillomavirus positive cancer cells by peptide aptamers targeting the viral E6 oncoprotein. Proc. Natl. Acad. Sci. U. S. A. 97:6693-6697.
4. Chen, L., et al. 11 January 2011, posting date. Down-regulation of HPV18 E6, E7, or VEGF expression attenuates malignant biological behavior of human cervical cancer cells. Med. Oncol. [Epub ahead of print.] doi:10.1007/s12032-010-9690-1.
5. Corona Gutierrez, C. M., et al. 2004. Therapeutic vaccination with MVA E2 can eliminate precancerous lesions (CIN 1, CIN 2, and CIN 3) associated with infection by oncogenic human papillomavirus. Hum. Gene Ther. 15: 421-431.
6. DeFilippis, R. A., E. C. Goodwin, L. Wu, and 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.
7. Desaintes, C., C. Demeret, S. Goyat, M. Yaniv, and F. Thierry. 1997. Expression of the papillomavirus E2 protein in HeLa cells leads to apoptosis. EMBO J. 16:504-514.
8. DiMaio, D., and J. Settleman. 1988. Bovine papillomavirus mutant temperature sensitive for transformation, replication and transactivation. EMBO J. 7:1197-1204.
9. Dimri, G. P., et al. 1995. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc. Natl. Acad. Sci. U. S. A. 92:9363-9367.
10. Dowhanick, J. J., A. A. McBride, and P. M. Howley. 1995. Suppression of cellular proliferation by the papillomavirus E2 protein. J. Virol. 69:7791-7799.
11. Dyson, N., P. M. Howley, K. Munger, and E. Harlow. 1989. The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science 243:934-937.
12. Flores, E. R., B. L. Allen-Hoffmann, D. Lee, C. A. Sattler, and P. F. Lambert. 1999. Establishment of the human papillomavirus type 16 (HPV-16) life cycle in an immortalized human foreskin keratinocyte cell line. Virology 262:344-354.
13. Fujii, T., et al. 2006. Intratumor injection of small interfering RNA-targeting human papillomavirus 18 E6 and E7 successfully inhibits the growth of cervical cancer. Int. J. Oncol. 29:541-548.
14. Gammoh, N., H. S. Grm, P. Massimi, and 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.
15. Garcia-Hernandez, E., et al. 2006. Regression of papilloma high-grade lesions (CIN 2 and CIN 3) is stimulated by therapeutic vaccination with MVA E2 recombinant vaccine. Cancer Gene Ther. 13:592-597.
16. Geiger, T., H. Sabanay, N. Kravchenko-Balasha, B. Geiger, and A. Levitzki. 2008. Anomalous features of EMT during keratinocyte transformation. PLoS One 3:e1574.
17. Goodwin, E. C., et al. 2000. Rapid induction of senescence in human cervical carcinoma cells. Proc. Natl. Acad. Sci. U. S. A. 97:10978-10983.
18. Gu, W., et al. 2006. Inhibition of cervical cancer cell growth in vitro and in vivo with lentiviral-vector delivered short hairpin RNA targeting human papillomavirus E6 and E7 oncogenes. Cancer Gene Ther. 13:1023-1032.
19. Guo, F., and Y. Zheng. 2004. Involvement of Rho family GTPases in p19Arfand p53-mediated proliferation of primary mouse embryonic fibroblasts. Mol. Cell Biol. 24:1426-1438.
20. Hall, A. H., and K. A. Alexander. 2003. RNA interference of human papillomavirus type 18 E6 and E7 induces senescence in HeLa cells. J. Virol. 77:6066-6069.
21. Hellner, K., J. Mar, F. Fang, J. Quackenbush, and K. Munger. 2009. HPV16 E7 oncogene expression in normal human epithelial cells causes molecular changes indicative of an epithelial to mesenchymal transition. Virology 391: 57-63.
22. Helt, A. M., and D. A. Galloway. 2003. Mechanisms by which DNA tumor virus oncoproteins target the Rb family of pocket proteins. Carcinogenesis 24:159-169.
23. Johung, K., E. C. Goodwin, and D. DiMaio. 2007. Human papillomavirus E7 repression in cervical carcinoma cells initiates a transcriptional cascade driven by the retinoblastoma family, resulting in senescence. J. Virol. 81: 2102-2116.
24. Cip1-mediated inhibition of cdk2. Genes Dev. 11:2101-2111.
25. Jonson, A. L., L. M. Rogers, S. Ramakrishnan, and L. S. Downs, Jr. 2008. Gene silencing with siRNA targeting E6/E7 as a therapeutic intervention in a mouse model of cervical cancer. Gynecol. Oncol. 111:356-364.
26. Karstensen, B., et al. 2006. Gene expression profiles reveal an upregulation of E2F and downregulation of interferon targets by HPV18 but no changes between keratinocytes with integrated or episomal viral genomes. Virology 353:200-209.
27. Kiyono, T., et al. 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. U. S. A. 94:11612-11616.
28. Klingelhutz, A. J., S. A. Foster, and J. K. McDougall. 1996. Telomerase activation by the E6 gene product of human papillomavirus type 16. Nature 380:79-82.
29. Kondo, H., and Y. Yonezawa. 1992. Changes in the migratory ability of human lung and skin fibroblasts during in vitro aging and in vivo cellular senescence. Mech. Ageing Dev. 63:223-233.
30. Lea, J. S., et al. 2007. Silencing of HPV 18 oncoproteins With RNA interference causes growth inhibition of cervical cancer cells. Reprod. Sci. 14:20-28.
31. Le Beyec, J., et al. 1997. A complete epithelial organization of Caco-2 cells induces I-FABP and potentializes apolipoprotein gene expression. Exp. Cell Res. 236:311-320.
32. Lee, S. S., R. S. Weiss, and R. T. 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. U. S. A. 94:6670-6675.
33. Liu, X., et al. 2009. HPV E6 protein interacts physically and functionally with the cellular telomerase complex. Proc. Natl. Acad. Sci. U. S. A. 106:18780-18785.
34. Lleonart, M. E., A. Artero-Castro, and H. Kondoh. 2009. Senescence induction; a possible cancer therapy. Mol. Cancer 8:3.
35. Ma, B., Yijie Xu, Chien-Fu Hung, and T.-C. Wu. 2010. HPV and therapeutic vaccines: where are we in 2010? Curr. Cancer Ther. Rev. 6:81-103.
36. McCormack, P. L., and E. A. Joura. 2010. Quadrivalent human papillomavirus (types 6, 11, 16, 18) recombinant vaccine (Gardasil): a review of its use in the prevention of premalignant genital lesions, genital cancer and genital warts in women. Drugs 70:2449-2474.
37. McLaughlin-Drubin, M. E., and K. Munger. 2009. The human papillomavirus E7 oncoprotein. Virology 384:335-344.
38. Moody, C. A., and L. A. Laimins. 2010. Human papillomavirus oncoproteins: pathways to transformation. Nat. Rev. Cancer 10:550-560.
39. Moon, M. S., et al. 2001. Effect of BPV1 E2-mediated inhibition of E6/E7 expression in HPV16-positive cervical carcinoma cells. Gynecol. Oncol. 80: 168-175.
40. Munger, K. 2002. The role of human papillomaviruses in human cancers. Front. Biosci. 7:d641-d649.
41. Nakagawa, S., and J. M. 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.
42. Nakahara, T., W. L. Peh, J. Doorbar, D. Lee, and P. F. Lambert. 2005. Human papillomavirus type 16 E1^E4 contributes to multiple facets of the papillomavirus life cycle. J. Virol. 79:13150-13165.
43. Nauenburg, S., W. Zwerschke, and P. Jansen-Durr. 2001. Induction of apoptosis in cervical carcinoma cells by peptide aptamers that bind to the HPV-16 E7 oncoprotein. FASEB J. 15:592-594.
44. Nishimura, A., et al. 2000. Mechanisms of human papillomavirus E2-mediated repression of viral oncogene expression and cervical cancer cell growth inhibition. J. Virol. 74:3752-3760.
45. Niu, X. Y., Z. L. Peng, W. Q. Duan, H. Wang, and P. Wang. 2006. Inhibition of HPV 16 E6 oncogene expression by RNA interference in vitro and in vivo. Int. J. Gynecol. Cancer. 16:743-751.
46. Psyrri, A., et al. 2004. Role of the retinoblastoma pathway in senescence triggered by repression of the human papillomavirus E7 protein in cervical carcinoma cells. Cancer Res. 64:3079-3086.
47. Raftopoulou, M., and A. Hall. 2004. Cell migration: Rho GTPases lead the way. Dev. Biol. 265:23-32.
48. Rampias, T., C. Sasaki, P. Weinberger, and A. Psyrri. 2009. E6 and e7 gene silencing and transformed phenotype of human papillomavirus 16-positive oropharyngeal cancer cells. J. Natl. Cancer Inst. 101:412-423.
49. Ridley, A. J. 2001. Rho family proteins: coordinating cell responses. Trends Cell Biol. 11:471-477.
50. Ruutu, M., P. Peitsaro, B. Johansson, and S. Syrjanen. 2002. Transcriptional profiling of a human papillomavirus 33-positive squamous epithelial cell line which acquired a selective growth advantage after viral integration. Int. J. Cancer 100:318-326.
51. Schauner, S., and C. Lyon. 2010. Bivalent HPV recombinant vaccine (Cervarix) for the prevention of cervical cancer. Am. Fam. Physician 82:1541-1542.
52. Scheffner, M., J. M. Huibregtse, R. D. Vierstra, and P. M. 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.
53. Scheffner, M., B. A. Werness, J. M. Huibregtse, A. J. Levine, and P. M. Howley. 1990. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 63:1129-1136.
54. Tan, T. M., and R. C. Ting. 1995. In vitro and in vivo inhibition of human papillomavirus type 16 E6 and E7 genes. Cancer Res. 55:4599-4605.
55. Thierry, F., et al. 2004. A genomic approach reveals a novel mitotic pathway in papillomavirus carcinogenesis. Cancer Res. 64:895-903.
56. Thierry, F., and M. Yaniv. 1987. The BPV1-E2 trans-acting protein can be either an activator or a repressor of the HPV18 regulatory region. EMBO J. 6:3391-3397.
57. Thomas, M., et al. 2008. Human papillomaviruses, cervical cancer and cell polarity. Oncogene 27:7018-7030.
58. Veldman, T., I. Horikawa, J. C. Barrett, and R. Schlegel. 2001. Transcriptional activation of the telomerase hTERT gene by human papillomavirus type 16 E6 oncoprotein. J. Virol. 75:4467-4472.
59. von Knebel Doeberitz, M., C. Rittmuller, H. zur Hausen, and M. Durst. 1992. Inhibition of tumorigenicity of cervical cancer cells in nude mice by HPV E6-E7 anti-sense RNA. Int. J. Cancer 51:831-834.
60. Wang, W., et al. 2010. Selective targeting of HPV-16 E6/E7 in cervical cancer cells with a potent oncolytic adenovirus and its enhanced effect with radiotherapy in vitro and vivo. Cancer Lett. 291:67-75.
61. Wei, J., et al. 2008. Microenvironment determines lineage fate in a human model of MLL-AF9 leukemia. Cancer Cell 13:483-495.
62. Wells, S. I., et al. 2003. Transcriptome signature of irreversible senescence in human papillomavirus-positive cervical cancer cells. Proc. Natl. Acad. Sci. U. S. A. 100:7093-7098.
63. Wells, S. I., et al. 2000. Papillomavirus E2 induces senescence in HPVpositive cells via pRB- and p21(CIP)-dependent pathways. EMBO J. 19: 5762-5771.
64. Werness, B. A., A. J. Levine, and P. M. Howley. 1990. Association of human papillomavirus types 16 and 18 E6 proteins with p53. Science 248:76-79.
65. Wilding, J., et al. 1996. E-cadherin transfection down-regulates the epidermal growth factor receptor and reverses the invasive phenotype of human papilloma virus-transfected keratinocytes. Cancer Res. 56:5285-5292.
66. Wise-Draper, T. M., et al. 2006. Apoptosis inhibition by the human DEK oncoprotein involves interference with p53 functions. Mol. Cell. Biol. 26: 7506-7519.
67. Wise-Draper, T. M., et al. 2005. The human DEK proto-oncogene is a senescence inhibitor and an upregulated target of high-risk human papillomavirus E7. J. Virol. 79:14309-14317.