Patients with chronic hepatitis C have circulating cytotoxic T cells which recognize hepatitis C virus-encoded peptides binding to HLA-A2.1 molecules

Journal of Virology

Volumn 69, Issue 4, 1995, Pages 2462-2470

  Battegay, Manuel ^a,g   Fikes, John ^b   Di Bisceglie, Adrian M ^a   Wentworth, Peggy A ^b   Sette, Alessandro ^b   Celis, Esteban ^b   Ching, Wei Mei ^c   Grakoui, Arash ^d   Rice, Charles M ^d   Kurokohchi, Kazutaka ^e   Berzofsky, Jay A ^e   Hoofnagle, Jay H ^a   Feinstone, Stephen M ^f   Akatsuka, Toshitaka ^f  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b CYTEL CORPORATION   (United States)

^c NAVAL MEDICAL RESEARCH INSTITUTE   (United States)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e NATIONAL CANCER INSTITUTE   (United States)

^f CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^g UNIVERSITY HOSPITAL BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; HEPATITIS VACCINE; HLA A2 ANTIGEN; MONOCLONAL ANTIBODY; VIRUS ANTIGEN;

ANTIGEN BINDING; ANTIGEN RECOGNITION; ARTICLE; CELLULAR IMMUNITY; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOPATHOGENESIS; LIVER CELL DAMAGE; MONONUCLEAR CELL; NONHUMAN; PRIORITY JOURNAL; VACCINATION;

EID: 0028962927     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.69.4.2462-2470.1995     Document Type: Article

References (68)

1. + T-cell-deficient mice. J. Virol. 68:4700-4704.
2. Bhardwaj, N., A. Bender, N. Gonzales. L. Kim Bui, M. C. Garrett, and R. M. Steinman. 1994. Influenza virus-infected dendritic cells stimulate strong proliferative and cytolytic responses from human CD8+ T cells. J. Clin. Invest. 94:797-807.
3. Botarelli, P., M. R. Brunetto, M. A. Minutello, P. Calvo, D. Unutmaz, A. J. Weiner, Q.-L. Choo, J. R. Shuster, G. Kuo. F. Bonino, M. Houghton, and S. Abrignani. 1993. T-lymphocyte response to hepatitis C virus in different clinical courses of infection. Gastroenterology 104:580-587.
4. Buus, S., A. Sette, S. M. Colon, C. Miles, and H. M. Grey. 1987. The relation between major histocompatibility complex (MHC) restriction and the capacity of Ia to bind immunogenic peptides. Science 235:1353-1358.
5. Carmichael, A., X. Jin, P. Sissons, and L. Borysiewicz. 1993. Quantitative analysis of the human immunodeficiency virus type 1 (HIV-1)-specific cytotoxic T lymphocyte (CTL) response at different stages of HIV-1 infection: differential CTL responses to HIV-1 and Epstein-Barr virus in late disease. J. Exp. Med. 177:249-256.
6. Celis, E., V. Tsai, C. Crimi, R. DeMars, P. A. Wentworth, R. W. Chesnut, H. M. Grey, A. Sette, and H. M. Serre. 1994. Induction of anti-tumor cytotoxic T lymphocytes in normal humans using primary cultures and synthetic peptide epitopes. Proc. Natl. Acad. Sci. USA 91:2105-2109.
7. Cerny, A., C. Ferrari, and F. V. Chisari. 1994. The class I-restricted cytotoxic T lymphocyte response to predetermined epitopes in the hepatitis B and C viruses. Curr. Top. Microbiol. Immunol. 189:169-186.
8. Chen, P.-J., M.-H. Lin, K.-F. Tai, P.-C. Liu, C.-J. Lin, and D. S. Chen. 1992. The Taiwanese hepatitis C genome: sequence determination and mapping the 5′ termini of viral genomic and antigenomic RNA. Virology 188:102-113.
9. Choo, Q.-L., G. Kuo, A. J. Weiner, L. R. Overby, D. W. Bradley, and M. Houghton. 1989. Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome. Science 244:359-362.
10. Choo, Q.-L., K. H. Richman, J. H. Han, K. Berger, C. Lee, C. Dong, C. Gallegos, D. Coit, A. Medina-Selby, P. J. Barr, A. J. Weiner, D. W. Bradley, G. Kuo, and M. Houghton. 1991. Genetic organization and diversity of the hepatitis C virus. Proc. Natl. Acad. Sci. USA 88:2451-2455.
11. Croft, M. 1994. Activation of naive, memory and effector T cells. Curr. Opin. Immunol. 6:431-437.
12. Daemer, R., C. Wychowski, A. Grakoui, C. M. Rice, and S. M. Feinstone. Unpublished data.
13. DeBruijn, M. L. H., J. D. Nieland, T. N. M. Schumacher, H. L. Ploegh, W. M. Kast, and C. J. M. Melief. 1992. Mechanisms of induction of primary virus-specific cytotoxic T lymphocyte responses. Eur. J. Immunol. 22:3013-3020.
14. Delisi, C., and J. A. Berzofsky. 1985. T-cell antigenic sites tend to be amphipathic structures. Proc. Natl. Acad. Sci. USA 82:7048-7052.
15. Di Bisceglie, A. M., P. Martin, C. Kassianides, M. Lisker-Melman, L. Murray, J. Waggoner, Z. Goodman, S. M. Banks, and J. H. Hoofnagle. 1989. Recombinant interferon alpha therapy for chronic hepatitis C: a randomized, double-blind, placebo-controlled trial. N. Engl. J. Med. 321:1506-1510.
16. Engelhard, V. H. 1994. Structure of peptides associated with MHC class I molecules. Curr. Opin. Immunol. 6:13-23.
17. Erickson, A. L., M. Houghton, Q. L. Choo, A. J. Weiner, R. Ralston, E. Muchmore, and C. M. Walker. 1993. Hepatitis C virus specific CTL responses in the liver of chimpanzees with acute and chronic hepatitis C. J. Immunol. 151:4189-4199.
18. Falk, K., O. Rötzschke, S. Stevanovic, G. Jung, and H.-G. Rammensee. 1991. Allele-specific motifs revealed by sequencing of self-peptides eluted from MHC molecules. Nature (London) 351:290-296.
19. Farci, P., H. J. Alter, S. Govindarajan, D. C. Wong, R. Engle, R. R. Lesniewsky, I. K. Mushahwar, S. M. Desai, R. H. Miller, N. Ogata, and R. H. Purcell. 1992. Lack of protective immunity against reinfection with hepatitis C virus. Science 258:135-140.
20. Germain, R. N., and D. H. Margulies. 1994. The biochemistry and cell biology of antigen processing and presentation. Annu. Rev. Immunol. 11: 403-450.
21. Grakoui, A., and C. M. Rice. Unpublished data.
22. Grakoui, A., C. Wychowski, C. Lin, S. M. Feinstone, and C. M. Rice. 1993. Expression and identification of hepatitis C virus polyprotein cleavage products. J. Virol. 67:1385-1395.
23. Hayashi, N., H. Higashi, K. Kaminaka, H. Sugimoto, M. Esumi, K. Komatsu, K. Hayashi, M. Sugitani, K. Suzuki, O. Tadao, C. Nozaki, K. Mizuno, and T. Shikata. 1993. Molecular cloning and heterogeneity of the human hepatitis C virus (HCV) genome. J. Hepatol. 17(Suppl. 3):S94-S107.
24. Hou, S., L. Hyland, K. W. Ryan, A. Portner, and P. C. Doherty. 1994. Virus-specific CD8+ T-cell memory determined by clonal burst size. Nature (London) 369:352-354.
25. Houbiers, J. G. A., H. W. Nijman, S. H. van der Burg, J. W. Drijfhout, P. Kenemans, C. J. H. van de Velde, A. Brand, F. Momburg, W. M. Kast, and C. J. M. Melief. 1993. In vitro induction of human cytotoxic T lymphocyte responses against peptides of mutant and wild-type p53. Eur. J. Immunol. 23:2072-2077.
26. Hunt, D. F., R. A. Henderson, J. Shabanowitz, K. Sakaguchi, H. Michel, N. Sevilir, A. L. Cox, E. Appella, and V. H. Engelhard. 1992. Characterization of peptides bound to the class I MHC molecule HLA-A2.1 by mass spectrometry. Science 255:1261-1263.
27. Inchauspe, G., S. Zebedee, D. H. Lee, M. Sugitani, M. Nasoff, and A. M. Prince. 1991. Genomic structure of the human prototype strain H of hepatitis C virus: comparison with American and Japanese isolates. Proc. Natl. Acad. Sci. USA 88:10292-10296.
28. Kast, M. W., R. M. P. Brandt, J. Sidney, J. W. Drijfhout, R. T. Kubo, H. M. Grey, C. J. M. 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.
29. Kato, N., M. Hijikata, Y. Ootsuyama, K. Muraiso, S. Ohkoshi, and K. Shimotohno. 1991. Molecular structure of the Japanese hepatitis C viral genome. FEBS Lett. 280:325-328.
30. Kita, H., T. Moriyama, T. Kaneko, I. Harase, M. Nomura, H. Miura, I. Nakamura, Y. Yazaki, and M. Imawari. 1993. HLA B44-restricted cytotoxic T lymphocytes recognizing an epitope on hepatitis C virus nucleocapsid protein. Hepatology 18:1039-1044.
31. Koziel, M. J., D. Dudley, N. Afdhal, Q. L. Choo, M. Houghton, R. Ralston, and B. D. Walker. 1993. Hepatitis C virus (HCV)-specific cytotoxic T lymphocytes recognize epitopes in the core and envelope proteins of HCV. J. Virol. 67:7522-7532.
32. Koziel, M. J., D. Dudley, J. T. Wong, J. Dienstag, M. Houghton, R. Ralston, and B. D. Walker. 1992. Intrahepatic cytotoxic T lymphocytes specific for hepatitis C virus in persons with chronic hepatitis. J. Immunol. 149:3339-3344.
33. Kuo, G., Q. L. Choo, H. J. Alter, G. L. Gitnick, A. G. Redeker, R. H. Purcell, T. Miyamura, J. L. Dienstag, M. J. Alter, C. E. Stevens, G. E. Tegtmeier, F. Bonino, M. Colombo, W.-S. Lee, C. Kuo, K. Berger, J. R. Shuster, L. R. Overby, D. W. Bradley, and M. Houghton. 1989. An assay for circulating antibodies to a major etiologic virus of human non-A, non-B hepatitis. Science 244:362-364.
34. Lai, M. E., A. P. Mazzoleni, F. Argiolu, S. De Virgilis, A. Balestrieri, R. H. Purcell, A. Cao, and P. Farci. 1994. Hepatitis C virus in multiple episodes of acute hepatitis in polytransfused thalassaemic children. Lancet 343:388-390.
35. Lau, J. Y. N., M. Mizokami, T. Ohno, D. A. Diamond, J. Kniffen, and G. L. Davis. 1993. Discrepancy between biochemical and virological responses to interferon-α in chronic hepatitis C. Lancet 342:1208-1209.
36. Lau, L. L., B. D. Jamleson, T. Somasundaram, and R. Ahmed. 1994. Cytotoxic T-cell memory without antigen. Nature (London) 369:648-652.
37. Lin, C., B. D. Lindenbach, B. M. Pragai, D. W. McCourt, and C. M. Rice. 1994. Processing in the hepatitis C virus E2-NS2 region: identification of p7 and two distinct E2-specific products with different C termini. J. Virol. 68:5063-5073.
38. Madden, D. R., D. N. Garboczi, and D. C. Wiley. 1993. The antigenic identity to peptide-MHC complexes: a comparison of the conformations of five viral peptides presented by HLA-A2. Cell 75:693-708.
39. Margalit, H., J. L. Spouge, J. L. Cornette, K. B. Cease, C. Delisi, and J. A. Berzofsky. 1987. Prediction of immunodominant helper T cell antigenic sites from the primary sequence. J. Immunol. 138:2213-2229.
40. Mehta-Damani, A., S. Markowicz, and E. G. Engleman. 1994. Generation of antigen-specific CD8+ CTL from naive precursors. J. Immunol. 153:996-1003.
41. Minutello, M. A., P. Pileri, D. Unutmaz, S. Censini, G. Kuo, M. Houghton, M. R. Brunetto, F. Bonino, and S. Abrignani. 1993. Compartmentalization of T lymphocytes to the site of disease: intrahepatic CD4+ T cells specific for the protein NS4 of hepatitis C virus in patients with chronic hepatitis C. J. Exp. Med. 178:17-25.
42. Moskophidis, D., F. Lechner, H. P. Pircher, and R. M. Zinkernagel. 1993. Virus persistence in acutely infected immunocompetent mice by exhaustion of antiviral cytotoxic effector T cells. Nature (London) 362:758-761.
43. Oehen, S., H. P. Waldner, T. Kündig, H. Hengartner, and R. M. Zinkernagel. 1992. Antivirally protective cytotoxic T cell memory to lymphocytic choriomeningitis virus is governed by persisting antigen. J. Exp. Med. 176:1273-1281.
44. Ohashi, P. S., H. Hengartner, M. Battegay, R. M. Zinkernagel, and H. P. Pircher. 1994. Thymocyte selection and peripheral tolerance using the lymphocytic choriomeningitis virus as a model, p. 113-133. In H. Bluethmann and P. S. Ohashi (ed.), Transgenesis and targeted mutagenesis in immunology. Academic Press, San Diego, Calif.
45. Okamoto, H., M. Kojima, S.-I. Okada, H. Yoshizawa, H. Iizuka, T. Tanaka, E. E. Muchmore, D. A. Peterson, Y. Ito, and S. Mishiro. 1992. Genetic drift of hepatitis C virus during an 8.2 year infection in a chimpanzee: variability and stability. Virology 190:894-899.
46. Okamoto, H., K. Kurai, S.-I. Okada, K. Yamamoto, H. Iizuka, T. Tanaka, S. Fukuda, F. Tsuda, and S. Mishiro. 1992. Full-length sequence of a hepatitis virus genome having poor homology to reported isolates: comparative study of four distinct genotypes. Virology 188:331-341.
47. Okamoto, H., S. Okada, Y. Sugiyama, K. Kurai, H. Iizuka, A. Machida, Y. Miyakawa, and M. Mayumi. 1991. Nucleotide sequence of the genomic RNA of hepatitis C virus isolated from a human carrier: comparison with reported isolates for conserved and divergent regions. J. Gen. Virol. 72: 2697-2704.
48. Parham, P., and F. M. Brodsky. 1981. Partial purification and some properties of BB7.2: a cytotoxic monoclonal antibody with specificity for HLA-A2 and a variant of HLA-A28. Hum. Immunol. 3:277-299.
49. Phillips, R. E., S. Rowland-Jones, D. F. Nixon, F. M. Gotch, J. P. Edwards, A. O. Ogunlesi, J. G. Elvin, J. A. Rothbard, C. R. M. Bangham, C. R. Rizza, and A. J. McMichael. 1991. Human immunodeficiency virus genetic variation that can escape cytotoxic T cell recognition. Nature (London) 354:453-459.
50. Pircher, H. P., D. Moskophidis, U. Rohrer, K. Bürki, H. Hengartner, and R. M. Zinkernagel. 1990. Viral escape by selection of cytotoxic T cell-resistant virus variants in vivo. Nature (London) 346:629-633.
51. Ruppert, J., J. Sidney, E. Celis, R. T. Kubo, H. M. Grey, and A. Sette. 1993. Prominent role of secondary anchor residues in peptide binding to HLA-A2.1 molecules. Cell 74:929-937.
52. Saito, I., T. Miyamura, A. Ohbayashi, H. Harada, T. Katayama, S. Kikuchi, T. Y. Watanabe, S. Koi, M. Onji, Y. Ohta, Q.-L. Choo, M. Houghton, and G. Kuo. 1990. Hepatitis C virus infection is associated with the development of hepatocellular carcinoma. Proc. Natl. Acad. Sci. USA 87:6547-6549.
53. Saracco, G., F. Rosina, M. L. Abate, L. Chiandussi, V. Gallo, E. Cerutti, A. Di Napoli, A. Solinas, A. Deplano, A. Tocco, P. Cossu, D. Chien, G. Kuo, A. Polito, A. J. Weiner, M. Houghton, G. Verme, F. Bonino, and M. Rizzetto. 1993. Long-term follow-up of patients with chronic hepatitis C treated with different doses of interferon-α2b. Hepatology 18:1300-1305.
54. Sette, A., J. Sidney, M. F. del Guercio, S. Southwood, J. Ruppert, C. Dahlberg, H. M. Grey, and R. T. Kubo. 1994. Peptide binding to the most frequent HLA-A class I alleles measured by quantitative molecular binding assays. Mol. Immunol. 31:813-822.
55. Shindo, M., A. M. Di Bisceglie, and J. H. Hoofnagle. 1992. Long term follow-up of patients with chronic hepatitis C treated with α-interferon. Hepatology 15:1013-1016.
56. Shirai, M., T. Akatsuka, C. D. Pendleton, R. Houghten, C. Wychowski, K. Mihalik, S. Feinstone, and J. A. Berzofsky. 1992. Induction of cytotoxic T cells to a cross-reactive epitope in the hepatitis C virus nonstructural RNA polymerase-like protein. J. Virol. 66:4098-4106.
57. Shirai, M., T. Arichi, M. Nishioka, T. Nomura, K. Ikeda, K. Kawanishi, V. H. Engelhard, S. M. Feinstone, and J. A. Berzofsky. Cytotoxic T lymphocyte (CTL) responses of HLA-A2.1-transgenic mice specific for hepatitis C viral peptides predict epitopes for CTL of humans carrying HLA-A2.1. J. Immunol., in press.
58. Shirai, M., H. Okada, M. Nishioka, T. Akatsuka, C. Wychowski, R. Houghten, C. D. Pendleton, S. M. Feinstone, and J. A. Berzofsky. 1994. An epitope in hepatitis C virus core region recognized by cytotoxic T cells in mice and humans. J. Virol. 68:3334-3342.
59. Simmonds, P., E. C. Holmes, T.-A. Cha, S.-W. Chan, F. McOmish, B. Irvine, E. Beall, P. L. Yap, J. Kolberg, and M. S. Urdea. 1993. Classification of hepatitis C virus into six major genotypes and a series of subtypes by phylogenetic analysis of the NS-5 region. J. Gen. Virol. 74:2391-2399.
60. Takamizawa, A., E. Mori, I. Fuke, S. Manabe, S. Murakami, J. Fujita, E. Onishi, T. Andoh, I. Yoshida, and H. Okayama. 1991. Structure and organization of the hepatitis C virus genome isolated from human carriers. J. Virol. 65:1105-1113.
61. Tanaka, T., N. Kato, M. Nakagawa, Y. Ootsuyama, M.-J. Cho, T. Nakazawa, M. Hijikata, Y. Ishimura, and K. Shimitohno. 1992. Molecular cloning of hepatitis C virus genome from a single Japanese carrier: sequence variation within the same individual and among infected individuals. Virus Res. 23: 39-53.
62. Taylor, P. M., and B. A. Askonas. 1986. Influenza nucleoprotein-specific cytotoxic T-cell clones are protective in vivo. Immunology 58:417-420.
63. Townsend, A., and H. Bodmer. 1989. Antigen recognition by class I-restricted T lymphocytes. Annu. Rev. Immunol. 7:601-624.
64. Tussey, L. G., M. Matsui, S. Rowland-Jones, R. Warburton, J. A. Frelinger, and A. McMichael. 1994. Analysis of mutant HLA-A2 molecules. Differential effects on peptide binding and CTL recognition. J. Immunol. 152:1213-1221.
65. Vitiello, A., G. Ishioka, H. M. Grey, R. Rose, P. Farness. R. LaFond, L. Yuan, F. V. Chisari, J. Furze, R. Bartholomeuz, and R. W. Chesnut. 1995. Development of a lipopeptide-based therapeutic vaccine to treat chronic HBV infection. I. Induction of a primary cytotoxic T lymphocyte response in humans. J. Clin. Invest. 95:341-349.
66. Wentworth, P. A., et al. Unpublished data.
67. Wentworth, P. A., E. Celis, C. Crimi, S. Stitely, L. Hale, V. Tsai, H. M. Serra, M-F. del Guercio, B. Livingston, D. Alazard, J. Fikes, R. T. Kubo, H. M. Grey, R. W. Chesnut, F. V. Chisari, and A. Sette. In vitro induction of primary, antigen specific CTL from human peripheral blood mononuclear cells stimulated with synthetic peptides. Mol. Immunol., in press.
68. Zinkernagel, R. M., D. Moskophidis. T. Kündig, S. Oehen, H. P. Pircher, and H. Hengartner. 1993. Effector T-cell induction and T-cell memory versus peripheral deletion of T cells. Immunol. Rev. 131:198-223.