Human papillomavirus 16-encoded E7 protein inhibits IFN-γ-mediated MHC class I antigen presentation and CTL-induced lysis by blocking IRF-1 expression in mouse keratinocytes

Journal of General Virology

Volumn 94, Issue PART 11, 2013, Pages 2504-2514

  Zhou, Fang ^a,b   Chen, JieZhong ^a   Zhao, Kong Nan ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ACTIN; GAMMA INTERFERON; INTERFERON REGULATORY FACTOR 1; JANUS KINASE 1; JANUS KINASE 2; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PROTEIN E7; STAT1 PROTEIN; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING 1;

ANIMAL CELL; ANTIGEN PRESENTATION; ARTICLE; CHROMIUM 51 RELEASE; CONTROLLED STUDY; CYTOLYSIS; CYTOTOXIC T LYMPHOCYTE; DOWN REGULATION; HUMAN PAPILLOMAVIRUS TYPE 16; IMMUNE RESPONSE; IMMUNOSURVEILLANCE; KERATINOCYTE; MOUSE; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TARGET CELL; TRANSGENIC MOUSE; UTERINE CERVIX CANCER;

ANIMALS; ANTIGEN PRESENTATION; FEMALE; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMAN PAPILLOMAVIRUS 16; HUMANS; INTERFERON REGULATORY FACTOR-1; INTERFERON-GAMMA; KERATINOCYTES; MICE; MICE, TRANSGENIC; PAPILLOMAVIRUS E7 PROTEINS; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84885611423     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.054486-0     Document Type: Article

References (57)

1. Ahmad, F., Li, P. M., Meyerovitch, J. & Goldstein, B. J. (1995). Osmotic loading of neutralizing antibodies demonstrates a role for protein-tyrosine phosphatase 1B in negative regulation of the insulin action pathway. J Biol Chem 270, 20503-20508.
2. Antonsson, A., Payne, E., Hengst, K. & McMillan, N. A. (2006). The human papillomavirus type 16 E7 protein binds human interferon regulatory factor-9 via a novel PEST domain required for transformation. J Interferon Cytokine Res 26, 455-461.
3. Barnabas, R. V., Laukkanen, P., Koskela, P., Kontula, O., Lehtinen, M. & Garnett, G. P. (2006). Epidemiology of HPV 16 and cervical cancer in Finland and the potential impact of vaccination: mathematical modelling analyses. PLoS Med 3, e138.
4. Barnard, P. & McMillan, N. A. (1999). The human papillomavirus E7 oncoprotein abrogates signaling mediated by interferon-α. Virology 259, 305-313.
5. Berger, K. L., Barriga, F., Lace, M. J., Turek, L. P., Zamba, G. J., Domann, F. E., Lee, J. H. & Klingelhutz, A. J. (2006). Cervical keratinocytes containing stably replicating extrachromosomal HPV-16 are refractory to transformation by oncogenic H-Ras. Virology 356, 68-78.
6. Bhat, P., Mattarollo, S. R., Gosmann, C., Frazer, I. H. & Leggatt, G. R. (2011). Regulation of immune responses to HPV infection and during HPV-directed immunotherapy. Immunol Rev 239, 85-98.
7. Brucet, M., Marqués, L., Sebastián, C., Lloberas, J. & Celada, A. (2004). Regulation of murine Tap1 and Lmp2 genes in macrophages by interferon gamma is mediated by STAT1 and IRF-1. Genes Immun 5, 26-35.
8. Conzelmann, M., Wagner, A. H., Hildebrandt, A., Rodionova, E., Hess, M., Zota, A., Giese, T., Falk, C. S., Ho, A. D. & other authors (2010). IFN-γ activated JAK1 shifts CD40-induced cytokine profiles in human antigen-presenting cells toward high IL-12p70 and low IL-10 production. Biochem Pharmacol 80, 2074-2086.
9. Cordano, P., Gillan, V., Bratlie, S., Bouvard, V., Banks, L., Tommasino, M. & Campo, M. S. (2008). The E6E7 oncoproteins of cutaneous human papillomavirus type 38 interfere with the interferon pathway. Virology 377, 408-418.
10. Darji, A., Chakraborty, T., Wehland, J. & Weiss, S. (1997). TAPdependent major histocompatibility complex class I presentation of soluble proteins using listeriolysin. Eur J Immunol 27, 1353-1359.
11. Drew, P. D., Franzoso, G., Carlson, L. M., Biddison, W. E., Siebenlist, U. & Ozato, K. (1995). Interferon regulatory factor-2 physically interacts with NF-κB in vitro and inhibits NF-κB induction of major histocompatibility class I and β2-microglobulin gene expression in transfected human neuroblastoma cells. J Neuroimmunol 63, 157-162.
12. Dürst, M., Croce, C. M., Gissmann, L., Schwarz, E. & Huebner, K. (1987). Papillomavirus sequences integrate near cellular oncogenes in some cervical carcinomas. Proc Natl Acad Sci U S A 84, 1070-1074.
13. Flores, E. R., Allen-Hoffmann, B. L., Lee, D., Sattler, C. A. & Lambert, P. F. (1999). Establishment of the human papillomavirus type 16 (HPV-16) life cycle in an immortalized human foreskin keratinocyte cell line. Virology 262, 344-354.
14. Frazer, I. H. (2004). Prevention of cervical cancer through papillomavirus vaccination. Nat Rev Immunol 4, 46-55.
15. Frazer, I. H. (2007). HPV immunisation: a significant advance in cancer control. Gynecol Oncol 107 (Suppl. 1), S1.
16. Frazer, I. H., De Kluyver, R., Leggatt, G. R., Guo, H. Y., Dunn, L., White, O., Harris, C., Liem, A. & Lambert, P. (2001). Tolerance or immunity to a tumor antigen expressed in somatic cells can be determined by systemic proinflammatory signals at the time of first antigen exposure. J Immunol 167, 6180-6187.
17. Frazer, I. H., Leggatt, G. R. & Mattarollo, S. R. (2011). Prevention and treatment of papillomavirus-related cancers through immunization. Annu Rev Immunol 29, 111-138.
18. Guan, P., Howell-Jones, R., Li, N., Bruni, L., de Sanjosé, S., Franceschi, S. & Clifford, G. M. (2012). Human papillomavirus types in 115,789 HPV-positive women: a meta-analysis from cervical infection to cancer. Int J Cancer 131, 2349-2359.
19. Halbert, C. L., Demers, G. W. & Galloway, D. A. (1991). The E7 gene of human papillomavirus type 16 is sufficient for immortalization of human epithelial cells. J Virol 65, 473-478.
20. + CTL. J Immunol 154, 6140-6156.
21. Hong, S., Mehta, K. P. & Laimins, L. A. (2011). Suppression of STAT-1 expression by human papillomaviruses is necessary for differentiation-dependent genome amplification and plasmid maintenance. J Virol 85, 9486-9494.
22. Jarosinski, K. W. & Massa, P. T. (2002). Interferon regulatory factor-1 is required for interferon-γ-induced MHC class I genes in astrocytes. J Neuroimmunol 122, 74-84.
23. Korkolopoulou, P., Kaklamanis, L., Pezzella, F., Harris, A. L. & Gatter, K. C. (1996). Loss of antigen-presenting molecules (MHC class I and TAP-1) in lung cancer. Br J Cancer 73, 148-153.
24. Lace, M. J., Anson, J. R., Klussmann, J. P., Wang, D. H., Smith, E. M., Haugen, T. H. & Turek, L. P. (2011). Human papillomavirus type 16 (HPV-16) genomes integrated in head and neck cancers and in HPV-16-immortalized human keratinocyte clones express chimeric viruscell mRNAs similar to those found in cervical cancers. J Virol 85, 1645-1654.
25. Lambert, P. F., Pan, H., Pitot, H. C., Liem, A., Jackson, M. & Griep, A. E. (1993). Epidermal cancer associated with expression of human papillomavirus type 16 E6 and E7 oncogenes in the skin of transgenic mice. Proc Natl Acad Sci U S A 90, 5583-5587.
26. Lee, S. H., Kim, J. W., Lee, H. W., Cho, Y. S., Oh, S. H., Kim, Y. J., Jung, C. H., Zhang, W. & Lee, J. H. (2003). Interferon regulatory factor-1 (IRF-1) is a mediator for interferon-γ induced attenuation of telomerase activity and human telomerase reverse transcriptase (hTERT) expression. Oncogene 22, 381-391.
27. Leggatt, G. R. & Frazer, I. H. (2007). HPV vaccines: the beginning of the end for cervical cancer. Curr Opin Immunol 19, 232-238.
28. Leggatt, G. R., Dunn, L. A., De Kluyver, R. L., Stewart, T. & Frazer, I. H. (2002). Interferon-gamma enhances cytotoxic T lymphocyte recognition of endogenous peptide in keratinocytes without lowering the requirement for surface peptide. Immunol Cell Biol 80, 415-424.
29. Lehtonen, A., Matikainen, S. & Julkunen, I. (1997). Interferons upregulate STAT1, STAT2, and IRF family transcription factor gene expression in human peripheral blood mononuclear cells and macrophages. J Immunol 159, 794-803.
30. Li, S., Labrecque, S., Gauzzi, M. C., Cuddihy, A. R., Wong, A. H., Pellegrini, S., Matlashewski, G. J. & Koromilas, A. E. (1999). The human papilloma virus (HPV)-18 E6 oncoprotein physically associates with Tyk2 and impairs Jak-STAT activation by interferon-α. Oncogene 18, 5727-5737.
31. Li, W., Deng, X. M., Wang, C. X., Zhang, X., Zheng, G. X., Zhang, J. & Feng, J. B. (2010). Down-regulation of HLA class I antigen in human papillomavirus type 16 E7 expressing HaCaT cells: correlate with TAP-1 expression. Int J Gynecol Cancer 20, 227-232.
32. Marquis, J. F., Kapoustina, O., Langlais, D., Ruddy, R., Dufour, C. R., Kim, B. H., MacMicking, J. D., Giguère, V. & Gros, P. (2011). Interferon regulatory factor 8 regulates pathways for antigen presentation in myeloid cells and during tuberculosis. PLoS Genet 7, e1002097.
33. Merzougui, N., Kratzer, R., Saveanu, L. & van Endert, P. (2011). A proteasome-dependent, TAP-independent pathway for crosspresentation of phagocytosed antigen. EMBO Rep 12, 1257-1264.
34. Mori, K., Stone, S., Khaodhiar, L., Braverman, L. E. & DeVito, W. J. (1999). Induction of transcription factor interferon regulatory factor-1 by interferon-γ (IFNγ) and tumor necrosis factor-α (TNFα) in FRTL-5 cells. J Cell Biochem 74, 211-219.
35. Münger, K. & Howley, P. M. (2002). Human papillomavirus immortalization and transformation functions. Virus Res 89, 213-228.
36. Nakanishi, G., Fujimoto, W. & Arata, J. (1997). IRF-1 expression in normal human epidermal keratinocytes. Arch Dermatol Res 289, 415-420.
37. Pamment, J., Ramsay, E., Kelleher, M., Dornan, D. & Ball, K. L. (2002). Regulation of the IRF-1 tumour modifier during the response to genotoxic stress involves an ATM-dependent signalling pathway. Oncogene 21, 7776-7785.
38. Park, J. S., Kim, E. J., Kwon, H. J., Hwang, E. S., Namkoong, S. E. & Um, S. J. (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.
39. Perea, S. E., Massimi, P. & Banks, L. (2000). Human papillomavirus type 16 E7 impairs the activation of the interferon regulatory factor-1. Int J Mol Med 5, 661-666.
40. Romanczuk, H., Villa, L. L., Schlegel, R. & Howley, P. M. (1991). The viral transcriptional regulatory region upstream of the E6 and E7 genes is a major determinant of the differential immortalization activities of human papillomavirus types 16 and 18. J Virol 65, 2739-2744.
41. Saito, H., Morita, Y., Fujimoto, M., Narazaki, M., Naka, T. & Kishimoto, T. (2000). IFN regulatory factor-1-mediated transcriptional activation of mouse STAT-induced STAT inhibitor-1 gene promoter by IFN-γ. J Immunol 164, 5833-5843.
42. Sasagawa, T., Takagi, H. & Makinoda, S. (2012). Immune responses against human papillomavirus (HPV) infection and evasion of host defense in cervical cancer. J Infect Chemother 18, 807-815.
43. Schroder, K., Hertzog, P. J., Ravasi, T. & Hume, D. A. (2004). Interferon-γ: an overview of signals, mechanisms and functions. J Leukoc Biol 75, 163-189.
44. Stanley, M. A. (2005). Establishing HPV-containing keratinocyte cell lines from tissue biopsies. Methods Mol Med 119, 129-139.
45. Stanley, M. A., Pett, M. R. & Coleman, N. (2007). HPV: from infection to cancer. Biochem Soc Trans 35, 1456-1460.
46. Storm van's Gravesande, K., Layne, M. D., Ye, Q., Le, L., Baron, R. M., Perrella, M. A., Santambrogio, L., Silverman, E. S. & Riese, R. J. (2002). IFN regulatory factor-1 regulates IFN-γ-dependent cathepsin S expression. J Immunol 168, 4488-4494.
47. Tennant, L. M., Renard, C., Chardon, P. & Powell, P. P. (2007). Regulation of porcine classical and nonclassical MHC class I expression. Immunogenetics 59, 377-389.
48. Tey, S. K. & Khanna, R. (2012). Autophagy mediates transporter associated with antigen processing-independent presentation of viral epitopes through MHC class I pathway. Blood 120, 994-1004.
49. Um, S. J., Rhyu, J. W., Kim, E. J., Jeon, K. C., Hwang, E. S. & Park, J. S. (2002). Abrogation of IRF-1 response by high-risk HPV E7 protein in vivo. Cancer Lett 179, 205-212.
50. Vambutas, A., DeVoti, J., Pinn, W., Steinberg, B. M. & Bonagura, V. R. (2001). Interaction of human papillomavirus type 11 E7 protein with TAP-1 results in the reduction of ATP-dependent peptide transport. Clin Immunol 101, 94-99.
51. Van Doorslaer, K. & Burk, R. D. (2010). Evolution of human papillomavirus carcinogenicity. Adv Virus Res 77, 41-62.
52. Wang, X., Liu, J., Zhao, W. M. & Zhao, K. N. (2009). Expression of HPV 58 long and short L1 capsid proteins in primary mouse keratinocyte cultures. Protein Pept Lett 16, 65-74.
53. Yewdell, J. W., Snyder, H. L., Bacik, I., Antón, L. C., Deng, Y., Behrens, T. W., Bachi, T. & Bennink, J. R. (1998). TAP-independent delivery of antigenic peptides to the endoplasmic reticulum: therapeutic potential and insights into TAP-dependent antigen processing. J Immunother 21, 127-131.
54. Zhou, F. (2009a). Molecular mechanisms of IFN-gamma to upregulate MHC class I antigen processing and presentation. Int Rev Immunol 28, 239-260.
55. Zhou, F. (2009b). Molecular mechanisms of viral immune evasion proteins to inhibit MHC class I antigen processing and presentation. Int Rev Immunol 28, 376-393.
56. Zhou, F., Frazer, I. H. & Leggatt, G. R. (2009). Keratinocytes efficiently process endogenous antigens for cytotoxic T-cell mediated lysis. Exp Dermatol 18, 1053-1059.
57. Zhou, F., Leggatt, G. R. & Frazer, I. H. (2011). Human papillomavirus 16 E7 protein inhibits interferon-γ-mediated enhancement of keratinocyte antigen processing and T-cell lysis. FEBS J 278, 955-963.