Analysis of successful immune responses in persons infected with hepatitis C virus

Journal of Experimental Medicine

Volumn 191, Issue 9, 2000, Pages 1499-1512

  Lechner, Franziska ^a   Wong, David K H ^c   Dunbar, P Rod ^b   Chapman, Roger ^a   Chung, Raymond T ^c   Dohrenwend, Paul ^c   Robbins, Gregory ^c   Phillips, Rodney ^a   Klenerman, Paul ^a   Walker, Bruce D ^c  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Acute infection; Cytotoxic T lymphocytes; Interferon ; T helper cells; Tetramer staining

Indexed keywords

GAMMA INTERFERON; HLA ANTIGEN;

ACUTE HEPATITIS; ADULT; AGED; ARTICLE; CASE REPORT; CELLULAR IMMUNITY; CYTOTOXIC LYMPHOCYTE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HELPER CELL; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; IMMUNE RESPONSE; MALE; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; VIREMIA;

ACUTE DISEASE; ADULT; AGED; CYTOTOXICITY, IMMUNOLOGIC; EPITOPES; FEMALE; HEPATITIS C; HEPATITIS C ANTIBODIES; HEPATITIS C ANTIGENS; HEPATITIS C, CHRONIC; HUMANS; INTERFERON TYPE II; LYMPHOCYTE ACTIVATION; MALE; MIDDLE AGED; OLIGOPEPTIDES; T-LYMPHOCYTES, CYTOTOXIC; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 17644444485     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.191.9.1499     Document Type: Article

References (63)

1. Cohen, J. 1999. The scientific challenge of hepatitis C virus. Science. 285:26-30.
2. Koziel, M.J., D. Dudley, N. Afdhal, A. Grakoui, C.M. Rice, Q.L. Choo, M. Houghton, and B.D. Walker. 1995. HLA class I-restricted cytotoxic T lymphocytes specific for hepatitis C virus. Identification of multiple epitopes and characterization of patterns of cytokine release. J. Clin. Invest. 96: 2311-2321.
3. Rehermann, B., K. Chang, J. McHutchinson, R. Kokka, M. Houghton, C. Rice, and F. Chisan. 1996. Differential CTL responsiveness to hepatitis B and C viruses in chronically infected patients. J. Virol. 70:7092-7102.
4. Rehermann, B., K. Chang, J. McHutchinson, R. Kokka, M. Houghton, and F. Chisari. 1996. Quantitative analysis of the peripheral blood CTL response in patients with chronic HCV infection. J. Clin. Invest. 98:1432-1440.
5. Cerny, A., J. McHutchinson, C. Pasquellini, M. Brown, M. Brothers, B. Grabschied, P. Fowler, M. Houghton, and F. Chisari. 1995. CTL response to HCV-derived peptides containing the HLA-A2.1 binding motif. J. Clin. Invest. 95:521-530.
6. Cerny, A., P. Fowler, M. Brothers, M. Houghton, H. Schlicht, and F. Chisari. 1995. Induction in vitro of a primary human antiviral cytotoxic T cell response. Eur. J. Immunol. 25:627-630.
7. Hiroishi, K., H. Kita, M. Kojima, H. Okamoto, T. Moriyama, T. Kaneko, T. Ishikawa, S. Ohnishi, T. Aikawa, N. Tanaka, et al. 1997. Cytotoxic T lymphocyte response and viral load in hepatitis C virus infection. Hepatelogy. 25: 705-712.
8. Wong, D.K., D.D. Dudley, N.H. Afdhal, J. Dienstag, C.M. Rice, L. Wang, M. Houghton, B.D. Walker, and M.J. Koziel. 1998. Liver-derived CTL in hepatitis C virus infection: breadth and specificity of responses in a cohort of persons with chronic infection. J. Immunol. 160:1479-1488.
9. Giuggio, V., H. Bonkovsky, J. Smith, and A. Rothman. 1998. Inefficient recognition of antologous viral sequences by intrahepatic HCV-specific CTL in chronically infected subjects. Virology. 251:132-140.
10. He, X.-S., B. Rehermann, F. Lopez-Labrador, J. Boisvert, R. Cheung, J. Mumm, H. Wedermeyer, M. Berenguer, T. Wright, and M. Davis. 1999. Quantitative analysis of HCV-specific CD8+ T cells in peripheral blood and liver using peptide-MHC tetramers. Proc. Natl. Acad. Sci. USA. 96: 5692-5697.
11. Koup, R.A., J.T. Safrit, Y. Cao, C.A. Andrews, G. McLeod, W. Borkowsky, C. Farthing, and D.D. Ho. 1994. Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J. Virol. 68:4650-4655.
12. Watson, A., J. McClure, J. Ranchalis, M. Scheibel, A. Schmidt, B. Kennedy, W.R. Morton, N.L. Haigwood, and S.L. Hu. 1997. Early postinfection antiviral treatment reduces viral load and prevents CD4+ cell decline in HIV type 2-infected macaques. AIDS Res. Hum. Retroviruses. 13:1375-1381.
13. + T cells associated with the control of infection. Gastroenterology. 117:1386-1396.
14. Lisziewicz, J., E. Rosenberg, J. Lieberman, H. Jessen, L. Lopalco, R. Siliciano, B. Walker, and F. Lori. 1999. Control of HIV despite the discontinuation of antiretroviral therapy. N. Engl. J. Med. 340:1683-1684.
15. Pantaleo, G., J. Demarest, T. Schacker, M. Vaccarezza, O. Cohen, M. Daucher, C. Graziosi, S. Schnittman, T. Quinn, G. Shaw, et al. 1997. The qualitative nature of the primary immune response to HIV infection is a prognosticator of disease progression independent of the initial level of plasma viraemia. Proc. Natl. Acad. Sci. USA. 94:254-259.
16. Hay, C.M., D.J. Ruhl, N.O. Basgoz. C.C. Wilson, J.M. Billingsley, M.P. DePasquale, R.T. D'Aquila, S.M. Wolinsky, J.M. Crawford, D.C. Montefiori, and B.D. Walker. 1999. Lack of viral escape and defective in vivo activation of human immunodeficiency virus type 1-specific cytotoxic T lymphocytes in rapidly progressive infection. J. Virol. 73: 5509-5519.
17. Guidotti, L.G., T. Ishikawa, M.V. Hobbs, B. Matzke, R. Schreiber, and F.V. Chisari. 1996. Intracellular inactivation of the hepatitis B virus by cytotoxic T lymphocytes. Immunity. 4:25-36.
18. Yang, O.O., S.A. Kalams, A. Trocha, H. Cao, A. Luster, R.P. Johnson, and B.D. Walker. 1997. Suppression of human immunodeficiency virus type 1 replication by CD8+ cells: evidence for HLA class I-restricted triggering of cytolytic and noncytolytic mechanisms. J. Virol. 71:3120-3128.
19. Guidotti, L., R. Rochford, J. Chung, M. Shapiro, R. Purcell, and F. Chisari. 1999. Viral clearance without destruction of infected cells during acute HBV infection. Science. 284: 825-829.
20. Koziel, M. 1999. Cytokines in viral hepatitis. Semin. Liver Dis. 19:157-169.
21. Planz, O., S. Ehl, E. Furrer, E. Horvath, M. Brundler, H. Hengartner, and R. Zinkernagel. 1997. A critical role for neutralizing antibody-producing B cells, CD4+ cells and interferons in persistent infections of mice with LCMV: implications for adoptive immunotherapy of virus carriers. Proc. Natl. Acad. Sci. USA. 94:6874-6879.
22. Zajac, A.J., J.N. Blattman, K. Murali-Krishna, D.J. Sourdive, M. Suresh, J.D. Altman, and R. Ahmed. 1998. Viral immune evasion due to persistence of activated T cells without effector function. J. Exp. Med. 188:2205-2213.
23. Diepolder, H., R. Zachoval, R. Hoffman, E. Wierenga, T. Santorino, M. Jung, D. Eichenlaub, and G. Pape. 1995. Possible mechanism involving T lymphocyte response to NS3 in viral clearance in acute HCV infection. Lancet. 346:1006-1007.
24. Missale, G., R. Bertoni, V. Limonaca, A. Valli, M. Massari, C. Mori, M. Rumi, M. Houghton, F. Fiaccadori, and C. Ferrari. 1996. Different clinical behaviors of acute HCV infection are associated with different vigor of the anti-viral T cell response. J. Clin. Invest. 98:706-714.
25. Cooper, S., A. Erickson, E. Adams, J. Kansopon, A. Weiner, D. Chien, M. Houghton, P. Parham, and C. Walker. 1999. Analysis of a successful immune response against HCV. Immunity. 10:439-449.
26. Gallimore, A., A. Glithero, A. Godkin, A.C. Tissot, A. Pluckthun, T. Elliott, H. Hengartner, and R. Zinkernagel. 1998. Induction and exhaustion of lymphocytic choriomeningitis virus-specific cytotoxic T lymphocytes visualized using soluble tetrameric major histocompatibility complex class I-peptide complexes. J. Exp. Med. 187:1383-1393.
27. Murali-Krishna, K., J.D. Altman, M. Suresh, D.J. Sourdive, A.J. Zajac, J.D. Miller, J. Slansky, and R. Ahmed. 1998. Counting antigen-specific CD8 T cells: a reevaluation of bystander activation during viral infection. Immunity. 8:177-187.
28. Lee, P.P., C. Yee, P.A. Savage, L. Fong, D. Brockstedt, J.S. Weber, D. Johnson, S. Swetter, J. Thompson, P.D. Greenberg, et al. 1999. Characterization of circulating T cells specific for tumor-associated antigens in melanoma patients. Nat. Med. 5:677-685.
29. Lubaki, M.N., M.A. Egan, R.F. Siliciano, K.J. Weinhold, and R.C. Bollinger. 1994. A novel method for detection and ex vivo expansion of HIV type 1-specific cytolytic T lymphocytes. AIDS Res. Hum. Retroviruses. 10:1427-1431.
30. 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.
31. Altman, J., P.A.H. Moss, P. Goulder, D. Barouch, M. McHeyzer-Williams, J.I. Bell, A.J. McMichael, and M.M. Davis. 1996. Direct visualization and phenotypic analysis of virus-specitic T lymphocytes in HIV-infected individuals. Science. 274:94-96.
32. Battegay, M., J. Fikes, A.M. Di Bisceglie, P.A. Wentworth, A. Sette, E. Celis, W.M. Ching, A. Grakoui, C.M. Rice, K. Kurokohchi, et al. 1995. Patients with chronic hepatitis C have circulating cytotoxic T cells which recognize hepatitis C virus-encoded peptides binding to HLA-A2.1 molecules. J. Virol. 69:2462-2470.
33. + T cells during the primary immune response to EBV in vivo. J. Exp. Med. 187:1395-1402.
34. Dunbar, P.R., G.S. Ogg, J. Chen, N. Rust, P. van der Bruggen, and V. Cerundolo. 1998. Direct isolation, phenotyping and cloning of low-frequency antigen-specific cytotoxic T lymphocytes from peripheral blood. Curr. Biol. 8:413-416.
35. Rammensee, H.G., K. Falk, and O. Rotzschke. 1993. Peptides naturally presented by MHC class 1 molecules. Annu. Rev. Immunol. 11:213-244.
36. Klenerman, P., G. Luzzi, K. McIntyre, R. Phillips, and A. McMichael. 1996. Identification of a novel A-25 restricted epitope in a conserved region of p24 gag (positions 71-80). AIDS. 10:348-350.
37. Cerwenka, A., T.M. Morgan, A.G. Harmsen, and R.W. Dutton. 1999. Migration kinetics and final destination of type 1 and type 2 CD8 effector cells predict protection against pulmonary virus infection. J. Exp. Med. 189:423-434.
38. Moskophidis, D., F. Lechner, H. Pircher, and R.M. Zinkernagel. 1993. Virus persistence in acutely infected immunocompetent mice by exhaustion of antiviral cytotoxic effector T cells. Nature. 362:758-761.
39. Valitutti, S., S. Miller, M. Cella, E. Padovan, and A. Lanzavecchia. 1995. Serial triggering of many T cell receptors by a few peptide-MHC complexes. Nature. 375:148-151.
40. Viola, A., and A. Lanzavecchia. 1996. T cell activation determined by TCR number and tunable thresholds. Science. 273: 104-106.
41. Viola, A., M. Salio, L. Tuosto, S. Linkert, O. Acuto, and A. Lanzavecchia. 1997. Quantitative contribution of CD4 and CD8 to T cell antigen receptor serial triggering. J. Exp. Med. 186:1775-1779.
42. Busch, D.H., I.M. Pilip, S. Vijh, and E.G. Panier. 1998. Coordinate regulation of complex T cell populations responding to bacterial infection. Immunity. 8:353-362.
43. Gerlach, J., H. Diepolder, M.-C. Jung, N. Gruener, W. Schraut, R. Zachoval, R. Hoffman, C. Schirren, T. Santantonio, and G. Pape. 1999. Recurrence of HCV after loss of virus specific CD4+ T cell response in acute hepatitis C. Gastroenterology. 117:933-941.
44. Minutello, M., P. Pileri, D. Unutmaz, S. Censini, G. Kuo, M. Houghton, M. Brunetto, F. Bonino, and S. Abrignani. 1993. Compartmentalization of T lymphocytes to the site of disease: intrahepatic T cells specific for the NS4 protein of hepatitis C virus in patients with chronic hepatitis C. J. Exp. Med. 178:17-25.
45. Zinkernagel, R.M., D. Moskophidis, T. Kundig, S. Oehen, H. Pircher, and H. Hengartner. 1993. Effector T-cell induction and T-cell memory versus peripheral deletion of T cells. Immunol. Rev. 133:199-223.
46. Borrow, P., H. Lewicki, X. Wei, M. Horowitz, N. Peffer, H. Meyers, J. Nelson, J. Gairin, B. Hahn, M. Oldstone, and G. Shaw. 1997. Antiviral pressure exerted by HIV-1 specific CTL during primary infection demonstrated by rapid selection of CTL escape virus. Nat. Med. 3:205-211.
47. Ogg, G., X. Jin, S. Bonhoeffer, P. Dunbar, M. Nowak, S. Monard, J. Segal, Y. Cao, S. Rowland-Jones, V. Cerundolo, et al. 1998. Quantitation of HIV-1 specific CTL and plasma load of HIV-1. Science. 279:2103-2106.
48. Sallusto, F., D. Lenig, R. Forster, M. Lipp, and A. Lanzavecchia. 1999. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature. 401: 708-712.
49. Evavold, B., and P. Allen. 1991. Separation of IL-4 production from proliferation by an altered peptide ligand. Science. 252:1308-1310.
50. Moskophidis, D., F. Lechner, H. Hengartner, and R.M. Zinkernagel. 1994. MHC class I and non-MHC-linked capacity for generating an anti-viral CTL response determines susceptibility to CTL exhaustion and establishment of virus persistence in mice. J. Immunol. 152:4976-1983.
51. Mehal, W.Z., A.E. Juedes, and I.N. Crispe. 1999. Selective retention of activated CD8+ T cells by the normal liver. J. Immunol. 163:3202-3210.
52. Naoumov, N. 1999. HCV specific CD4+ T cells: do they help or damage? Gastroenterology. 117:1012-1014.
53. Weiland, O. 1998. Can HCV infection be cleared? Lancet. 352:668-670.
54. Dries, V., I. von Both, M. Muller, G. Gerken, P. Schirmacher, M. Odenthal, R. Bartenschlager, U. Drebber, K.H. Meyer zum Buschenfeld, and H.P. Dienes. 1999. Detection of hepatitis C virus in paraffin-embedded liver biopsies of patients negative for viral RNA in serum. Hepatology. 29:223-229.
55. Kaufmann, G., J. Zaunders, P. Cunningham, and D. Cooper. 1999. Phenotypic analysis of CD8+ T lymphocytes in a cohort of HIV-1 infected patients treated with saquinavir, ritonavir and two nucleoside analogues for 1 year and association with plasma HIV-1 RNA. AIDS Res. Hum. Retroviruses. 15:963-972.
56. Kalams, S.A., P.J. Goulder, A.K. Shea, N.G. Jones, A.K. Trocha, G.S. Ogg, and B.D. Walker. 1999. Levels of human immunodeficiency virus type 1-specific cytotoxic T-lymphocyte effector and memory responses decline after suppression of viremia with highly active antiretroviral therapy. J. Virol. 73:6721-6728.
57. Giorgi, J.V., Z. Liu, L.E. Hultin, W.G. Cumberland, K. Hennessey, and R. Detels. 1993. Elevated levels of CD38+ CD8+ T cells in HIV infection add to the prognostic value of low CD4+ T cell levels: results of 6 years of follow-up. The Los Angeles Center, Multicenter AIDS Cohort Study. J. Acquir. Immune Defic. Syndr. 6:904-912.
58. Valiante, N., A. D. Andrea, S. Crotta, S. Nuti, A. Wack, and S. Abrignani. 2000. Life, activation and death of intra-hepatic lymphocytes in chronic viral hepatitis. Immunol. Rev. In press.
59. Chang, K.M., B. Rehermann, J.G. McHutchison, C. Pasquinelli, S. Southwood, A. Sette, and F.V. Chisari. 1997. Immunological significance of cytotoxic T lymphocyte epitope variants in patients chronically infected by the hepatitis C virus. J. Clin. Invest. 100:2376-2385.
60. Klenerman, P., R. Phillips, and A. McMichael. 1996. Cytotoxic T cell antagonism in HIV. Semin. Virol. 7:31-39.
61. Tsai, S.L., Y.M. Chen, M.H. Chen, C.Y. Huang, I.S. Sheen, C.T. Yeh, J.H. Huang, G.C. Kuo, and Y.F. Liaw. 1998. Hepatitis C virus variants circumventing cytotoxic T lymphocyte activity as a mechanism of chronicity. Gastroenterology. 115:954-965.
62. Moskophidis, D., and R.M. Zinkernagel. 1995. Immunobiology of cytotoxic T-cell escape mutants of lymphocytic choriomeningitis virus. J. Virol. 69:2187-2193.
63. Weiner, A., A.L. Erickson, J. Kansopon, K. Crawford, E. Muchmore, A.L. Hughes, M. Houghton, and C.M. Walker. 1995. Persistent hepatitis C virus infection in a chimpanzee is associated with emergence of a cytotoxic T lymphocyte escape variant. Proc. Natl. Acad. Sci. USA. 92:2755-2759.