HLA class I binding promiscuity of the CD8 T-cell epitopes of human papillomavirus type 16 E6 protein

Journal of Virology

Volumn 81, Issue 3, 2007, Pages 1412-1423

  Nakagawa, Mayumi ^a,c   Kim, Kevin H ^a   Gillam, Tiffany M ^a   Moscicki, Anna Barbara ^b  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; HLA A ANTIGEN; HLA ANTIGEN CLASS 1; HLA B ANTIGEN; PEPTIDE; PHENYLALANYLALANYLPHENYLALANYLARGINYLASPARTYLLEUCYLCYSTEINYLISOLEUCYLVALYLTYROSINE; PROTEIN E6; THREONYLISOLEUCYLHISTIDYLASPARTYLISOLEUCYLISOLEUCYLLEUCYLGLUTAMYLCYSTEINE; THREONYLISOLEUCYLHISTIDYLASPARTYLISOLEUCYLISOLEUCYLLEUCYLGLUTAMYLCYSTEINYLVALINE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CD8+ T LYMPHOCYTE; CYTOTOXIC T LYMPHOCYTE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN PAPILLOMAVIRUS TYPE 16; NONHUMAN; PERSISTENT VIRUS INFECTION; PRIORITY JOURNAL; PROTEIN BINDING; UTERINE CERVIX CANCER;

BINDING, COMPETITIVE; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; EPITOPES, T-LYMPHOCYTE; GENES, MHC CLASS I; HLA ANTIGENS; HUMANS; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; REPRESSOR PROTEINS; T-LYMPHOCYTES, CYTOTOXIC;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN PAPILLOMAVIRUS; HUMAN PAPILLOMAVIRUS TYPE 16;

EID: 33846534656     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01768-06     Document Type: Article

References (46)

1. Adams, M., L. Borysiewicz, A. Fiander, S. Man, B. Jasani, H. Navabi, C. Lipetz, A. S. Evans, and M. Mason. 2001. Clinical studies of human papilloma vaccines in pre-invasive and invasive cancer. Vaccine 19:2549-2556.
2. Alexander, M., M. L. Salgaller, E. Celis, A. Sette, W. A. Barnes, S. A. Rosenberg, and M. A. Steller. 1996. Generation of tumor-specific cytolytic T lymphocytes from peripheral blood of cervical cancer patients by in vitro stimulation with a synthetic human papillomavirus type 16 E7 epitope. Am. J. Obstet. Gynecol. 175:1586-1593.
3. Borysiewicz, L. K., A. Fiander, M. Nimako, S. Man, G. W. Wilkinson, D. Westmorland, A. S. Evans, M. Adams, S. N. Stacey, M. E. Boursnell, E. Rutherford, J. K. Hickling, and S. C. Inglis. 1996. A recombinant vaccinia virus encoding human papillomavirus types 16 and 18, E6 and E7 proteins as immunotherapy for cervical cancer. Lancet 347:1523-1527.
4. Bourgault Villada, I., N. Beneton, C. Bony, F. Connan, J. Monsonego, A. Bianchi, P. Saiag, J. P. Levy, J. G. Guillet, and J. Choppin. 2000. Identification in humans of HPV-16 E6 and E7 protein epitopes recognized by cytolytic T lymphocytes in association with HLA-B18 and determination of the HLA-B18-specific binding motif. Eur. J. Immunol. 30:2281-2289.
5. Boursnell, M. E., E. Rutherford, J. K. Hickling, E. A. Rollinson, A. J. Munro, N. Rolley, C. S. McLean, L. K. Borysiewicz, K. Vousden, and S. C. Inglis. 1996. Construction and characterisation of a recombinant vaccinia virus expressing human papillomavirus proteins for immunotherapy of cervical cancer. Vaccine 14:1485-1494.
6. Brown, S. A., T. D. Lockey, C. Slaughter, K. S. Slobod, S. Surman, A. Zirkel, A. Mishra, V. R. Pagala, C. Coleclough, P. C. Doherty, and J. L. Hurwitz. 2005. T cell epitope "hotspots" on the HIV type 1 gp120 envelope protein overlap with tryptic fragments displayed by mass spectrometry. AIDS Res. Hum. Retroviruses 21:165-170.
7. Crook, T., J. A. Tidy, and K. H. Vousden. 1991. Degradation of p53 can be targeted by HPV E6 sequences distinct from those required for p53 binding and trans-activation. Cell 67:547-556.
8. Davidson, E. J., R. L. Faulkner, P. Sehr, M. Pawlita, L. J. Smyth, D. J. Burt, A. E. Tomlinson, J. Hickling, H. C. Kitchener, and P. L. Stern. 2004. Effect of TA-CIN (HPV 16 L2E6E7) booster immunisation in vulval intraepithelial neoplasia patients previously vaccinated with TA-HPV (vaccinia virus encoding HPV 16/18 E6E7). Vaccine 22:2722-2729.
9. de Jong, A., T. O'Neill, A. Y. Khan, K. M. Kwappenberg, S. E. Chisholm, N. R. Whittle, J. A. Dobson, L. C. Jack, J. A. St Clair Roberts, R. Offringa, S. H. van der Burg, and J. K. Hickling. 2002. Enhancement of human papillomavirus (HPV) type 16 E6 and E7-specific T-cell immunity in healthy volunteers through vaccination with TA-CIN, an HPV16 L2E7E6 fusion protein vaccine. Vaccine 20:3456-3464.
10. Evans, E. M., S. Man, A. S. Evans, and L. K. Borysiewicz. 1997. Infiltration of cervical cancer tissue with human papillomavirus-specific cytotoxic T-lymphocytes. Cancer Res. 57:2943-2950.
11. Feltkamp, M. C., H. L. Smits, M. P. Vierboom, R. P. Minnaar, B. M. de Jongh, J. W. Drijfhout, J. ter Schegget, C. J. Melief, and W. M. Kast. 1993. Vaccination with cytotoxic T lymphocyte epitope-containing peptide protects against a tumor induced by human papillomavirus type 16-transformed cells. Eur. J. Immunol. 23:2242-2249.
12. Feltkamp, M. C., G. R. Vreugdenhil, M. P. Vierboom, E. Ras, S. H. van der Burg, J. ter Schegget, C. J. Melief, and W. M. Kast. 1995. Cytotoxic T lymphocytes raised against a subdominant epitope offered as a synthetic peptide eradicate human papillomavirus type 16-induced tumors. Eur. J. Immunol. 25:2638-2642.
13. Ferrara, A., M. Nonn, P. Sehr, C. Schreckenberger, M. Pawlita, M. Durst, A. Schneider, and A. M. Kaufmann. 2003. Dendritic cell-based tumor vaccine for cervical cancer II: results of a clinical pilot study in 15 individual patients. J. Cancer Res. Clin. Oncol. 129:521-530.
14. Frahm, N., P. Goulder, and C. Brander. 2003. Broad HIV-1 specific CTL responses reveal extensive HLA class I binding promiscuity of HIV-derived, optimally denned CTL epitopes, p. 3-24. In B. Korber, C. Brander, B. Haynes, R. Koup, J. Moore, B. Walker, and D. Watkins (ed.), HIV immunology and HIV/SIV vaccine databases 2003. Los Alamos National Laboratory, Los Alamos, NM.
15. Frazer, I. H., M. Quinn, J. L. Nicklin, J. Tan, L. C. Perrin, P. Ng, V. M. O'Connor, O. White, N. Wendt, J. Martin, J. M. Crowley, S. J. Edwards, A. W. McKenzie, S. V. Mitchell, D. W. Maher, M. J. Pearse, and R. L. Basser. 2004. Phase 1 study of HPV16-specific immunotherapy with E6E7 fusion protein and ISCOMATRIX adjuvant in women with cervical intraepithelial neoplasia. Vaccine 23:172-181.
16. Gallimore, A., H. Hengartner, and R. Zinkernagel. 1998. Hierarchies of antigen-specific cytotoxic T-cell responses. Immunol. Rev. 164:29-36.
17. Garcia-Hernandez, E., J. L. Gonzalez-Sanchez, A. Andrade-Manzano, M. L. Contreras, S. Padilla, C. C. Guzman, R. Jimenez, L. Reyes, G. Morosoli, M. L. Verde, and R. Rosales. 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.
18. Heck, D. V., C. L. Yee, P. M. Howley, and K. Munger. 1992. Efficiency of binding the retinoblastoma protein correlates with the transforming capacity of the E7 oncoproteins of the human papillomaviruses. Proc. Natl. Acad. Sci. USA 89:4442-4446.
19. Kast, W. M., R. M. Brandt, J. Sidney, J. W. Drijfhout, R. T. Kubo, H. M. Grey, C. J. Melief, and A. Sette. 1994. Role of HLA-A motifs in identification of potential CTL epitopes in human papillomavirus type 16 E6 and E7 proteins. J. Immunol. 152:3904-3912.
20. Kaufmann, A. M., P. L. Stern, E. M. Rankin, H. Sommer, V. Nuessler, A. Schneider, M. Adams, T. S. Onon, T. Bauknecht, U. Wagner, K. Kroon, J. Hickling, C. M. Boswell, S. N. Stacey, H. C. Kitchener, J. Gillard, J. Wanders, J. S. Roberts, and H. Zwierzina. 2002. Safety and immunogenicity of TA-HPV, a recombinant vaccinia virus expressing modified human papillomavirus (HPV)-16 and HPV-18 E6 and E7 genes, in women with progressive cervical cancer. Clin. Cancer Res. 8:3676-3685.
21. Kim, K. H., R. Dishongh, A. D. Santin, M. J. Cannon, S. Bellone, and M. Nakagawa. 2006. Recognition of a cervical cancer derived tumor cell line by a human papillomavirus type 16 E6 52-61-specific CD8 T cell clone. Cancer Immun. 6:9.
22. Larsen, M. V., C. Lundegaard, K. Lamberth, S. Buus, S. Brunak, O. Lund, and M. Nielsen. 2005. An integrative approach to CTL epitope prediction: a combined algorithm integrating MHC class I binding, TAP transport efficiency, and proteasomal cleavage predictions. Eur. J. Immunol. 35:2295-2303.
23. Larsson, M., D. T. Wilkens, J. F. Fonteneau, T. J. Beadle, M. J. Merritt, R. G. Kost, P. A. Haslett, S. Cu-Uvin, N. Bhardwaj, D. F. Nixon, and B. L. Shacklett. 2002. Amplification of low-frequency antiviral CD8 T cell responses using autologous dendritic cells. AIDS 16:171-180.
24. Masemola, A. M., T. N. Mashishi, G. Khoury, H. Bredell, M. Paximadis, T. Mathebula, D. Barkhan, A. Puren, E. Vardas, M. Colvin, L. Zijenah, D. Katzenstein, R. Musonda, S. Allen, N. Kumwenda, T. Taha, G. Gray, J. McIntyre, S. A. Karim, H. W. Sheppard, and C. M. Gray. 2004. Novel and promiscuous CTL epitopes in conserved regions of Gag targeted by individuals with early subtype C HIV type 1 infection from southern Africa. J. Immunol. 173:4607-4617.
25. Muderspach, L., S. Wilczynski, L. Roman, L. Bade, J. Felix, L. A. Small, W. M. Kast, G. Fascio, V. Marty, and J. Weber. 2000. A phase I trial of a human papillomavirus (HPV) peptide vaccine for women with high-grade cervical and vulvar intraepithelial neoplasia who are HPV 16 positive. Clin. Cancer Res. 6:3406-3416.
26. Nakagawa, M., K. Kim, and A.-B. Moscicki. 2004. Different methods of identifying new antigenic epitopes of human papillomavirus type 16 E6 and E7 proteins. Clin. Diagn. Lab. Immunol. 11:889-896.
27. Nakagawa, M., K. H. Kim, and A. B. Moscicki. 2005. Patterns of CD8 T-cell epitopes within the human papillomavirus type 16 (HPV 16) E6 protein among young women whose HPV 16 infection has become undetectable. Clin. Diagn. Lab. Immunol. 12:1003-1005.
28. Nakagawa, M., D. P. Stites, S. Farhat, J. R. Sisler, B. Moss, F. Kong, A. B. Moscicki, and J. M. Palefsky. 1997. Cytotoxic T lymphocyte responses to E6 and E7 proteins of human papillomavirus type 16: relationship to cervical intraepithelial neoplasia. J. Infect. Dis. 175:927-931.
29. Nakagawa, M., D. P. Stites, S. Patel, S. Farhat, M. Scott, N. K. Hills, J. M. Palefsky, and A. B. Moscicki. 2000. Persistence of human papillomavirus type 16 infection is associated with lack of cytotoxic T lymphocyte response to the E6 antigens. J. Infect. Dis. 182:595-598.
30. Nielsen, M., C. Lundegaard, O. Lund, and C. Kesmir. 2005. The role of the proteasome in generating cytotoxic T-cell epitopes: insights obtained from improved predictions of proteasomal cleavage. Immunogenetics 57:33-41.
31. Oerke, S., H. Hohn, I. Zehbe, H. Pilch, K. H. Schicketanz, W. E. Hitzler, C. Neukirch, K. Freitag, and M. J. Maeurer. 2005. Naturally processed and HLA-B8-presented HPV16 E7 epitope recognized by T cells from patients with cervical cancer. Int. J. Cancer 114:766-778.
32. Pirisi, L., S. Yasumoto, M. Feller, J. Doniger, and J. DiPaolo. 1987. Transformation of human fibroblasts and keratinocytes with human papillomavirus type 16 DNA. J. Virol. 61:1061-1066.
33. Ressing, M. E., A. Sette, R. M. Brandt, J. Ruppert, P. A. Wentworth, M. Hartman, C. Oseroff, H. M. Grey, C. J. Melief, and W. M. Kast. 1995. Human CTL epitopes encoded by human papillomavirus type 16 E6 and E7 identified through in vivo and in vitro immunogenicity studies of HLA-A*0201-binding peptides. J. Immunol. 154:5934-5943.
34. Sadovnikova, E., X. Zhu, S. M. Collins, J. Zhou, K. Vousden, L. Crawford, P. Beverley, and H. J. Stauss. 1994. Limitations of predictive motifs revealed by cytotoxic T lymphocyte epitope mapping of the human papilloma virus E7 protein. Int. Immunol. 6:289-296.
35. Sarkar, A. K., G. Tortolero-Luna, P. N. Nehete, R. B. Arlinghaus, M. F. Mitchell, and K. J. Sastry. 1995. Studies on in vivo induction of cytotoxic T lymphocyte responses by synthetic peptides from E6 and E7 oncoproteins of human papillomavirus type 16. Viral Immunol. 8:165-174.
36. 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.
37. Schlegel, R., W. C. Phelps, Y. L. Zhang, and M. Barbosa. 1988. Quantitative keratinocyte assay detects two biological activities of human papillomavirus DNA and identifies viral types associated with cervical carcinoma. EMBO J. 7:3181-3187.
38. Seedorf, K., G. Krammer, M. Durst, S. Suhai, and W. G. Rowekamp. 1985. Human papillomavirus type 16 DNA sequence. Virology 145:181-185.
39. Serjeantson, S. W. 1989. The reasons for MHC polymorphism in man. Transplant Proc. 21:598-601.
40. Stevanovic, S. 2005. Antigen processing is predictable: from genes to T cell epitopes. Transpl. Immunol. 14:171-174.
41. Storey, A., D. Pim, A., Murray, K. Osborn, L. Banks, and L. Crawford. 1988. Comparison of the in vitro transforming activities of human papillomavirus types. EMBO J. 7:1815-1820.
42. Trimble, C. L. 2005. Prospects for therapeutic HPV vaccines. Gynecol. Oncol. 99:8249-8250.
43. Villa, L. L., R. L. Costa, C. A. Petta, R. P. Andrade, K. A. Ault, A. R. Giuliano, C. M. Wheeler, L. A. Koutsky, C. Malm, M. Lehtinen, F. E. Skjeldestad, S. E. Olsson, M. Steinwall, D. R. Brown, R. J. Kurman, B. M. Ronnett, M. H. Stoler, A. Ferenczy, D. M. Harper, G. M. Tamms, J. Yu, L. Lupinacci, R. Railkar, F. J. Taddeo, K. U. Jansen, M. T. Esser, H. L. Sings, A. J. Saah, and E. Barr. 2005. Prophylactic quadrivalent human papillomavirus (types 6, 11, 16, and 18) L1 virus-like particle vaccine in young women: a randomised double-blind placebo-controlled multicentre phase II efficacy trial. Lancet Oncol. 6:271-278.
44. Walker, B. D., and B. T. Korber. 2001. Immune control of HIV: the obstacles of HLA and viral diversity. Nat. Immunol. 2:473-475.
45. Youde, S. J., P. R. Dunbar, E. M. Evans, A. N. Fiander, L. K. Borysiewicz, V. Cerundolo, and S. Man. 2000. Use of fluorogenic histocompatibility leukocyte antigen-A*0201/HPV 16 E7 peptide complexes to isolate rare human cytotoxic T-lymphocyte-recognizing endogenous human papillomavirus antigens. Cancer Res. 60:365-371.
46. zur Hausen, H. 1996. Papillomavirus infections-a major cause of human cancers. Biochim. Biophys. Acta 1288:F55-F78.