Identification of an HLA-A24-restricted cytotoxic T lymphocyte epitope from human papillomavirus type-16 E6: The combined effects of bortezomib and interferon-γ on the presentation of a cryptic epitope

International Journal of Cancer

Volumn 120, Issue 3, 2007, Pages 594-604

  Morishima, Satoko ^a   Akatsuka, Yoshiki ^a   Nawa, Akihiro ^a   Kondo, Eisei ^a   Kiyono, Tohru ^b   Torikai, Hiroki ^a   Nakanishi, Toru ^a   Ito, Yoshinori ^a   Tsujimura, Kunio ^a   Iwata, Kosuke ^c   Ito, Koji ^d   Kodera, Yushihisa ^e   Morishima, Yasuo ^a   Kuzushima, Kiyotaka ^a   Takahashi, Toshitada ^a  

^a AICHI CANCER CENTER HOSPITAL   (Japan)

^b NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^c Iwata Hospital   (Japan)

^d Sakae Obstetrics and Gynecology Clinic   (Japan)

^e JAPANESE RED CROSS NAGOYA FIRST HOSPITAL   (Japan)

Author keywords

Bortezomib; Cytotoxic T lymphocyte; Epitope, cervical neoplasm; Tumor immunity

Indexed keywords

BORTEZOMIB; EPITOPE; GAMMA INTERFERON; HLA A24 ANTIGEN; PROTEINASE INHIBITOR; SYNTHETIC PEPTIDE; TETRAMER; VALYLTYROSYLASPARTYLPHENYLALANYLALANYLPHENYLALANYLARGINYLASPARTYLLEUCINE;

ALLELE; ARTICLE; CONTROLLED STUDY; CYTOLYSIS; CYTOTOXIC T LYMPHOCYTE; DRUG EFFECT; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 16; INTERFERON PRODUCTION; JAPAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TUMOR IMMUNITY; UTERINE CERVIX CANCER; UTERINE CERVIX CARCINOMA IN SITU;

ADULT; AMINO ACID SEQUENCE; ANIMALS; BORONIC ACIDS; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE; CELL LINE, TUMOR; DRUG SYNERGISM; EPITOPES, T-LYMPHOCYTE; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; HLA-A ANTIGENS; HUMANS; INTERFERON TYPE II; MICE; MIDDLE AGED; NIH 3T3 CELLS; ONCOGENE PROTEINS, VIRAL; PROTEASE INHIBITORS; PYRAZINES; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; T-LYMPHOCYTES, CYTOTOXIC; UTERINE CERVICAL NEOPLASMS;

EID: 33845691016     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.22312     Document Type: Article

References (49)

1. Frazer IH. Prevention of cervical cancer through papillomavirus vaccination. Nat Rev Immunol 2004;4:46-54.
2. 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.
3. Munoz N, Bosch FX, de Sanjose S, Herrero R, Castellsague X, Shah KV, Snijders PJ, Meijer CJ. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med 2003;348:518-27.
4. Asato T, Maehama T, Nagai Y, Kanazawa K, Uezato H, Kariya K. A large case-control study of cervical cancer risk associated with human papillomavirus infection in Japan, by nucleotide sequencing-based genotyping. J Infect Dis 2004;189:1829-32.
5. Schlecht NF, Platt RW, Duarte-Franco E, Costa MC, Sobrinho JP, Prado JC, Ferenczy A, Rohan TE, Villa LL, Franco EL. Human papillomavirus infection and time to progression and regression of cervical intraepithelial neoplasia. J Natl Cancer Inst 2003;95:1336-43.
6. Alloub MI, Barr BB, McLaren KM, Smith IW, Bunney MH, Smart GE. Human papillomavirus infection and cervical intraepithelial neoplasia in women with renal allografts. BMJ 1989;298:153-6.
7. Petry KU, Scheffel D, Bode U, Gabrysiak T, Kochel H, Kupsch E, Glaubitz, M. Niesert S, Kuhnle H, Schedel I. Cellular immunodeficiency enhances the progression of human papillomavirus-associated cervical lesions. Int J Cancer 1994;57:836-40.
8. Maiman M. Management of cervical neoplasia in human immunodeficiency virus-infected women. J Natl Cancer Inst Monogr 1998:43-9.
9. zur Hausen H. Papillomaviruses and cancer: from basic studies to clinical application. Nat Rev Cancer 2002;2:342-50.
10. Rajkumar SV, Richardson PG, Hideshima T, Anderson KC. Proteasome inhibition as a novel therapeutic target in human cancer. J Clin Oncol 2005;23:630-9.
11. Valmori D, Gileadi U, Servis C, Dunbar PR, Cerottini JC, Romero P, Cerundolo V, Levy F. Modulation of proteasomal activity required for the generation of a ctotoxic T lymphocyte-defined peptide derived from the tumor antigen MAGE-3. J Exp Med 1999;189:895-906.
12. Schwarz K, de Giuli R, Schmidtke G, Kostka S, van den Broek M, Kim KB, Crews CM, Kraft R, Groettrup M. The selective proteasome inhibitors lactacystin and epoxomicin can be used to either up- or down-regulate antigen presentation at nontoxic doses. J Immunol 2000;164:6147-57.
13. Anton LC, Snyder HL, Bennink JR, Vinitsky A, Orlowski M, Porgador A, Yewdell JW. Dissociation of proteasomal degradation of biosynthesized viral proteins from generation of MHC class I-associated antigenic peptides. J Immunol 1998;160:4859-68.
14. Richardson PG, Barlogie B, Berenson J, Singhal S, Jagannath S, Irwin D, Rajkumar SV, Srkalovic G, Alsina M, Alexanian R, Siegel D, Orlowski RZ, et al. A phase 2 study of bortezomib in relapsed, refractory myeloma. N Engl J Med 2003;348:2609-17.
15. Adams J, Palombella VJ, Sausville EA, Johnson J, Destree A, Lazarus DD, Maas J, Pien CS, Prakash S, Elliott PJ. Proteasome inhibitors: a novel class of potent and effective antitumor agents. Cancer Res 1999;59:2615-22.
16. Altun M, Galardy PJ, Shringarpure R, Hideshima T, LeBlanc R, Anderson KC, Ploegh HL, Kessler BM. Effects of PS-341 on the activity and composition of proteasomes in multiple myeloma cells. Cancer Res 2005;65:7896-901.
17. Berkers CR, Verdoes M, Lichtman E, Fiebiger E, Kessler BM, Anderson KC, Ploegh HL, Ovaa H, Galardy PJ. Activity probe for in vivo profiling of the specificity of proteasome inhibitor bortezomib. Nat Methods 2005;2:357-62.
18. Crawford LJ, Walker B, Ovaa H, Chauhan D, Anderson KC, Morris TC, Irvine AE. Comparative selectivity and specificity of the proteasome inhibitors BzLLLCOCHO, PS-341, and MG-132. Cancer Res 2006;66:6379-86.
19. Kondo E, Topp MS, Kiem HP, Obata Y, Morishima Y, Kuzushima K, Tanimoto M, Harada M, Takahashi T, Akatsuka Y. Efficient generation of antigen-specific cytotoxic T cells using retrovirally transduced CD40-activated B cells. J Immunol 2002;169:2164-71.
20. Schultze JL, Cardoso AA, Freeman GJ, Seamon MJ, Daley J, Pinkus GS, Gribben JG, Nadler LM. Follicular lymphomas can be induced to present alloantigen efficiently: a conceptual model to improve their tumor immunogenicity. Proc Natl Acad Sci USA 1995;92:8200-4.
21. Nozawa S, Udagawa Y, Ohta H, Kurihara S, Fishman WH. Newly established uterine cervical cancer cell line (SKG-III) with Regan isoenzyme, human chorionic gonadotropin β-subunit, and pregnancy-specific β 1-glycoprotein phenotypes. Cancer Res 1983;43:1748-60.
22. de Roda Husman AM, Walboomers JM, van den Brule AJ, Meijer CJ, Snijders PJ. The use of general primers GP5 and GP6 elongated at their 3′ ends with adjacent highly conserved sequences improves human papillomavirus detection by PCR. J Gen Virol 1995;76(Pt 4):1057-62.
23. Yoshikawa H, Kawana T, Kitagawa K, Mizuno M, Yoshikura H, Iwamoto A. Amplification and typing of multiple cervical cancer-associated human papillomavirus DNAs using a single pair of primers. Int J Cancer 1990;45:990-2.
24. Kinsella TM, Nolan GP. Episomal vectors rapidly and stably produce high-titer recombinant retrovirus. Hum Gene Ther 1996;7:1405-13.
25. Akatsuka Y, Goldberg TA, Kondo E, Martin EG, Obata Y, Morishima Y, Takahashi T, Hansen JA. Efficient cloning and expression of HLA class I cDNA in human B-lymphoblastoid cell lines. Tissue Antigens 2002;59:502-11.
26. Parker KC, Bednarck MA, Coligan JE. Scheme for ranking potential HLA-A2 binding peptides based on independent binding of individual peptide side-chains. J Immunol 1994;152:163-75.
27. Kuzushima K, Hayashi N, Kimura H, Tsurumi T. Efficient identification of HLA-A*2402-restricted cytomegalovirus-specific CD8(+) T-cell epitopes by a computer algorithm and an enzyme-linked immunospot assay. Blood 2001;98:1872-81.
28. Waldrop SL, Pitcher CJ, Peterson DM, Maino VC, Picker LJ. Determination of antigen-specific memory/effector CD4+ T cell frequencies by flow cytometry: evidence for a novel, antigen-specific homeostatic mechanism in HIV-associated immunodeficiency. J Clin Invest 1997;99:1739-50.
29. Altman JD, Moss PA, Goulder PJ, Barouch DH, McHeyzer-Williams MG, Bell JI, McMichael AJ, Davis MM. Phenotypic analysis of antigen-specific T lymphocytes. Science 1996;274:94-6.
30. Yee C, Savage PA, Lee PP, Davis MM, Greenberg PD. Isolation of high avidity melanoma-reactive CTL from heterogeneous populations using peptide-MHC tetramers. J Immunol 1999;162:2227-34.
31. Schneider-Gadicke A, Schwarz E. Different human cervical carcinoma cell lines show similar transcription patterns of human papillomavirus type 18 early genes. EMBO J 1986;5:2285-92.
32. Smotkin D, Prokoph H, Weltstein FO. Oncogenic and nononcogenic human genital papillomaviruses generate the E7 mRNA by different mechanisms. J Virol 1989;63:1441-7.
33. Kim KY, Blatt L, Taylor MW. The effects of interferon on the expression of human papillomavirus oncogenes. J Gen Virol 2000;81:695-700.
34. Ressing ME, Sette A, Brandt RM, Ruppert J, Wentworth PA, Hartman M, Oseroff C, Grey HM, Melief CJ, Kast WM. 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 1995;154:5934-43.
35. Muderspach L, Wilczynski S, Roman L, Bade L, Felix J, Small LA, Kast WM, Fascio G, Marty V, Weber J. 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 2000;6:3406-16.
36. Kast WM, Brandt RM, Sidney J, Drijfhout JW, Kubo RT, Grey HM, Melief CJ, Sette A. Role of HLA-A motifs in identification of potential CTL epitopes in human papillomavirus type 16 E6 and E7 proteins. J Immunol 1994;152:3904-12.
37. Hara M, Matsueda S, Tamura M, Takedatsu H, Tanaka M, Kawano K, Mochizuki K, Kamura T, Itoh K, Harada M. Identification of human papillomavirus 16-E6 protein-derived peptides with the potential to generate cytotoxic T-lymphocytes toward human leukocyte antigen-A24+ cervical cancer. Int J Oncol 2005;27:1371-9.
38. Rammensee H, Bachmann J, Emmerich NP, Bachor OA, Stevanovic S. SYFPEITHI: database for MHC ligands and peptide motifs. Immunogenetics 1999;50:213-9.
39. Evans M, Borysiewicz LK, Evans AS, Rowe M, Jones M, Gileadi U, Cerundolo V, Man S. Antigen processing defects in cervical carcinomas limit the presentation of a CTL epitope from human papillomavirus 16 E6. J Immunol 2001;167:5420-8.
40. Seedorf K, Oltersdorf T, Krammer G, Rowekamp W. Identification of early proteins of the human papilloma viruses type 16 (HPV 16) and type 18 (HPV 18) in cervical carcinoma cells. EMBO J 1987;6:139-44.
41. 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.
42. Chapiro J, Claverol S, Piette F, Ma W, Stroobant V, Guillaume B, Gairin JE, Morel S, Burlet-Schiltz O, Monsarrat B, Boon T, Van den Eynde BJ. Destructive cleavage of antigenic peptides either by the immunoproteasome or by the standard proteasome results in differential antigen presentation. J Immunol 2006;176:1053-61.
43. Sunwoo JB, Chen Z, Dong G, Yeh N, Crowl Bancroft C, Sausville E, Adams J, Elliott P, Van Waes C. Novel proteasome inhibitor PS-341 inhibits activation of nuclear factor-κ B, cell survival, tumor growth, and angiogenesis in squamous cell carcinoma. Clin Cancer Res 2001;7:1419-28.
44. Vinitsky A, Anton LC, Snyder HL, Orlowski M, Bennink JR, Yewdell JW. The generation of MHC class I-associated peptides is only partially inhibited by proteasome inhibitors: involvement of nonproteasomal cytosolic proteases in antigen processing? J Immunol 1997;159:554-64.
45. Lopez D, Del Val M. Selective involvement of proteasomes and cysteine proteases in MHC class I antigen presentation. J Immunol 1997;159:5769-72.
46. Youde SJ, Dunbar PR, Evans EM, Fiander AN, Borysiewicz LK, Cerundolo V, Man S. 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 2000;60:365-71.
47. Bontkes HJ, de Gruijl TD, van den Muysenberg AJ, Verheijen RH, Stukart MJ, Meijer CJ, Scheper RJ, Stacey SN, Duggan-Keen MF, Stern PL, Man S, Borysiewicz LK, et al. Human papillomavirus type 16 E6/E7-specific cytotoxic T lymphocytes in women with cervical neoplasia. Int J Cancer 2000;88:92-8.
48. Nakagawa M, Stites DP, Patel S, Farhat S, Scott M, Hills NK, Palefsky JM, Moscicki AB. Persistence of human papillomavirus type 16 infection is associated with lack of cytotoxic T lymphocyte response to the E6 antigens. J Infect Dis 2000;182:595-8.
49. Kim CJ, Jeong JK, Park M, Park TS, Park TC, Namkoong SE, Park JS. HPV oligonucleotide microarray-based detection of HPV genotypes in cervical neoplastic lesions. Gynecol Oncol 2003;89:210-7.