The E6E7 oncoproteins of cutaneous human papillomavirus type 38 interfere with the interferon pathway

Virology

Volumn 377, Issue 2, 2008, Pages 408-418

  Cordano, Pablo ^a   Gillan, Victoria ^a   Bratlie, Sigrid ^a   Bouvard, Veronique ^b   Banks, Lawrence ^c   Tommasino, Massimo ^b   Campo, M Saveria ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b INTERNATIONAL AGENCY FOR RESEARCH ON CANCER   (France)

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

Author keywords

E6; E7; HPV 38; Immunoevasion; Interferon pathway

Indexed keywords

BETA 2 MICROGLOBULIN; BETA1 INTERFERON; GAMMA INTERFERON; INTERFERON REGULATORY FACTOR 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; ONCOPROTEIN; PROTEIN E6; PROTEIN E7; STAT1 PROTEIN; TAPASIN; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING 1; VIRUS PROTEIN;

ARTICLE; CELL TRANSFORMATION; CONTROLLED STUDY; DOWN REGULATION; HEAVY CHAIN; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOSURVEILLANCE; IN VITRO STUDY; IN VIVO STUDY; KERATINOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SKIN PAPILLOMA; UPREGULATION; UTERINE CERVIX CARCINOMA; WART VIRUS;

CELL TRANSFORMATION, VIRAL; GENE EXPRESSION REGULATION, VIRAL; HUMANS; INTERFERONS; KERATINOCYTES; ONCOGENE PROTEINS; ONCOGENES; PAPILLOMAVIRIDAE;

HUMAN PAPILLOMAVIRUS; HUMAN PAPILLOMAVIRUS TYPE 38;

EID: 45049083616     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2008.04.036     Document Type: Article

References (44)

1. Akgul B., Cooke J.C., and Storey A. HPV-associated skin disease. J. Pathol. 208 (2006) 165-175
2. Asgari M.M., Kiviat N.B., Critchlow C.W., Stern J.E., Argenyi Z.B., Raugi G.J., Berg D., Odland P.B., Hawes S.E., and de Villiers E.M. Detection of human papillomavirus DNA in cutaneous squamous cell carcinoma among immunocompetent individuals. J. Invest. Dermatol. (2008) Jan 10 [Electronic publication ahead of print]
3. Ashrafi G.H., Haghshenas M.R., Marchetti B., O'Brien P.M., and Campo M.S. E5 protein of human papillomavirus type 16 selectively downregulates surface HLA class I. Int. J. Cancer. 113 (2005) 276-283
4. Ashrafi G.H., Brown D.R., Fife K.H., and Campo M.S. Down-regulation of MHC class I is a property common to papillomavirus E5 proteins. Virus Res. 120 (2006) 208-211
5. Astori G., Lavergne D., Benton C., Hockmayr B., Egawa K., Garbe C., and de Villiers E.M. Human papillomaviruses are commonly found in normal skin of immunocompetent hosts. J. Invest. Dermatol. 110 (1998) 752-755
6. Barnard P., and McMillan N.A. The human papillomavirus E7 oncoprotein abrogates signaling mediated by interferon-alpha. Virology 259 (1999) 305-313
7. Boxman I.L., Berkhout R.J., Mulder L.H., Wolkers M.C., Bouwes Bavinck J.N., Vermeer B.J., and ter Schegget J. Detection of human papillomavirus DNA in plucked hairs from renal transplant recipients and healthy volunteers. J. Invest. Dermatol. 108 (1997) 712-715
8. Caldeira S., Zehbe I., Accardi R., Malanchi I., Dong W., Giarre M., de Villiers E.M., Filotico R., Boukamp P., and Tommasino M. The E6 and E7 proteins of the cutaneous human papillomavirus type 38 display transforming properties. J. Virol. 77 (2003) 2195-2206
9. Caldeira S., Filotico R., Accardi R., Zehbe I., Franceschi S., and Tommasino M. p53 mutations are common in human papillomavirus type 38-positive non-melanoma skin cancers. Cancer Lett. 209 (2004) 119-124
10. Chang Y.E., and Laimins L.A. Microarray analysis identifies interferon-inducible genes and Stat-1 as major transcriptional targets of human papillomavirus type 31. J. Virol. 74 (2000) 4174-4182
11. Chatterjee-Kishore M., Kishore R., Hicklin D.J., Marincola F.M., and Ferrone S. Different requirements for signal transducer and activator of transcription 1alpha and interferon regulatory factor 1 in the regulation of low molecular mass polypeptide 2 and transporter associated with antigen processing 1 gene expression. J. Biol. Chem. 273 (1998) 16177-16183
12. Chen Y.Y., Cheng M., and Tian Z.G. Hepatitis B virus down-regulates expressions of MHC class I molecules on hepatoplastoma cell line. Cell. Mol. Immunol. 3 (2006) 373-378
13. Cromme F.V., Airey J., Heemels M.T., Ploegh H.L., Keating P.J., Stern P.L., Meijer C.J., and Walboomers J.M. Loss of transporter protein, encoded by the TAP-1 gene, is highly correlated with loss of HLA expression in cervical carcinomas. J. Exp. Med. 179 (1994) 335-340
14. de Villiers E.M., Lavergne D., McLaren K., and Benton E.C. Prevailing papillomavirus types in non-melanoma carcinomas of the skin in renal allograft recipients. Int. J. Cancer 73 (1997) 356-361
15. Dong W., Kloz U., Accardi R., Caldeira S., Tong W.M., Wang Z.Q., Jansen L., Durst M., Sylla B.S., Gissmann L., and Tommasino M. Skin hyperproliferation and susceptibility to chemical carcinogenesis in transgenic mice expressing E6 and E7 of human papillomavirus type 38. J. Virol. 79 (2005) 14899-14908
16. Friedrich M.G., Chandrasoma S., Siegmund K.D., Weisenberger D.J., Cheng J.C., Toma M.I., Huland H., Jones P.A., and Liang G. Prognostic relevance of methylation markers in patients with non-muscle invasive bladder carcinoma. Eur. J. Cancer 41 (2005) 2769-2778
17. Gabet A.S., Accardi R., Bellopede A., Popp S., Boukamp P., Sylla B.S., Londoño-Vallejo J.A., and Tommasino M. Impairment of the telomere/telomerase system and genomic instability are associated with keratinocyte immortalization induced by the skin human papillomavirus type 38. FASEB J. 22 (2008) 622-632
18. Georgopoulos N.T., Proffitt J.L., and Blair G.E. Transcriptional regulation of the major histocompatibility complex (MHC) class I heavy chain, TAP1 and LMP2 genes by the human papillomavirus (HPV) type 6b, 16 and 18 E7 oncoproteins. Oncogene 19 (2000) 4930-4935
19. Goodbourn S., Didcock L., and Randall R.E. Interferons: cell signalling, immune modulation, antiviral response and virus countermeasures. J. Gen. Virol. 81 (2000) 2341-2364
20. Harwood C.A., Surentheran T., McGregor J.M., Spink P.J., Leigh I.M., Breuer J., and Proby C.M. Human papillomavirus infection and non-melanoma skin cancer in immunosuppressed and immunocompetent individuals. J. Med. Virol. 61 (2000) 289-297
21. Haspel R.L., Salditt-Georgieff M., and Darnell Jr. J.E. The rapid inactivation of nuclear tyrosine phosphorylated Stat1 depends upon a protein tyrosine phosphatase. EMBO J. 15 (1996) 6262-6268
22. Hazard K., Eliasson L., Dillner J., and Forslund O. Subtype HPV38b[FA125] demonstrates heterogeneity of human papillomavirus type 38. Int. J. Cancer 119 (2006) 1073-1077
23. Hughes E.A., Hammond C., and Cresswell P. Misfolded major histocompatibility complex class I heavy chains are translocated into the cytoplasm and degraded by the proteasome. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 1896-1901
24. IARC Monographs. Human Papillomaviruses. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. vol 90 (2005), Lyon, France
25. Ivanov S.V., Salnikow K., Ivanova A.V., Bai L., and Lerman M.I. Hypoxic repression of STAT1 and its downstream genes by a pVHL/HIF-1 target DEC1/STRA13. Oncogene 26 (2006) 802-812
26. Jablonska S. Epidermodysplasia verruciformis. In: Friedman R.J. (Ed). Skin Cancers (1991), WB Saunders Co., Philadelphia, Pa. 101-113
27. Jong-Tieben L.M., Berkhout R.J., Smits H.L., Bouwes Bavinck J.N., Vermeer B.J., van der Woude F.J., and ter Schegget J. High frequency of detection of epidermodysplasia verruciformis-associated human papillomavirus DNA in biopsies from malignant and premalignant skin lesions from renal transplant recipients. J. Invest. Dermatol. 105 (1995) 367-371
28. Kroger A., Koster M., Schroeder K., Hauser H., and Mueller P.P. Activities of IRF-1. J. Interferon Cytokine Res. 22 (2002) 5-14
29. Li S., Labrecque S., Gauzzi M.C., Cuddihy A.R., Wong A.H., Pellegrini S., Matlashewski G.J., and Koromilas A.E. The human papilloma virus (HPV)-18 E6 oncoprotein physically associates with Tyk2 and impairs Jak-STAT activation by interferon-alpha. Oncogene 18 (1999) 5727-5737
30. Livak K.J., and Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25 (2001) 402-408
31. Mantovani F., and Banks L. The human papillomavirus E6 protein and its contribution to malignant progression. Oncogene 20 (2001) 7874-7887
32. Massimi P., Thomas M., Bouvard V., Ruberto I., Campo M.S., Tommasino M., and Banks L. Comparative transforming potential of different human papillomaviruses associated with non-melanoma skin cancer. Virology 371 (2008) 374-379
33. Nees M., Geoghegan J.M., Hyman T., Frank S., Miller L., and Woodworth C.D. Papillomavirus type 16 oncogenes downregulate expression of interferon-responsive genes and upregulate proliferation-associated and NF-kappaB-responsive genes in cervical keratinocytes. J. Virol. 75 (2001) 4283-4296
34. O'Brien P.M., and Campo M.S. Papillomaviruses: a correlation between immune evasion and oncogenicity?. Trends Microbiol. 11 (2003) 300-305
35. Ohmori Y., Schreiber R.D., and Hamilton T.A. Synergy between interferon-gamma and tumor necrosis factor-alpha in transcriptional activation is mediated by cooperation between signal transducer and activator of transcription 1 and nuclear factor kappaB. J. Biol. Chem. 272 (1997) 14899-14907
36. Park J.S., Kim E.J., Kwon H.J., Hwang E.S., Namkoong S.E., and Um S.J. 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 (2000) 6764-6769
37. Pear W.S., Nolan G.P., Scott M.L., and Baltimore D. Production of high-titer helper-free retroviruses by transient transfection. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 8392-8396
38. Perea S.E., Massimi P., and Banks L. Human papillomavirus type 16 E7 impairs the activation of the interferon regulatory factor-1. Int. J. Mol. Med. 5 (2000) 661-666
39. Proffitt J.A., and Blair G.E. The MHC-encoded TAP1/LMP2 bidirectional promoter is down-regulated in highly oncogenic adenovirus type 12 transformed cells. FEBS Lett. 400 (1997) 141-144
40. Ronco L.V., Karpova A.Y., Vidal M., and Howley P.M. Human papillomavirus 16 E6 oncoprotein binds to interferon regulatory factor-3 and inhibits its transcriptional activity. Genes Dev. 12 (1998) 2061-2072
41. Tang S., Tao M., McCoy Jr. J.P., and Zheng Z.M. 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 (2006) 4249-4263
42. Wang J., and Michalak T.I. Inhibition by woodchuck hepatitis virus of class I major histocompatibility complex presentation on hepatocytes is mediated by virus envelope pre-S2 protein and can be reversed by treatment with gamma interferon. J. Virol. 80 (2006) 8541-8553
43. White L.C., Wright K.L., Felix N.J., Ruffner H., Reis L.F., Pine R., and Ting J.P. Regulation of LMP2 and TAP1 genes by IRF-1 explains the paucity of CD8+ T cells in IRF-1-/- mice. Immunity 5 (1996) 365-376
44. Wright K.L., White L.C., Kelly A., Beck S., Trowsdale J., and Ting J.P. Coordinate regulation of the human TAP1 and LMP2 genes from a shared bidirectional promoter. J. Exp. Med. 181 (1995) 1459-1471