Cellular immune selection with hepatitis C virus persistence in humans

Journal of Experimental Medicine

Volumn 201, Issue 11, 2005, Pages 1741-1752

  Cox, Andrea L ^a   Mosbruger, Timothy ^a   Mao, Qing ^a   Liu, Zhi ^a   Wang, Xiao Hong ^a   Yang, Hung Chih ^a   Sidney, John ^b   Sette, Alessandro ^b   Pardoll, Drew ^a   Thomas, David L ^a   Ray, Stuart C ^a  

^a DEPARTMENT OF PATHOLOGY   (United States)

^b LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; EPITOPE; PEPTIDE; POLYPROTEIN;

AMINO ACID SUBSTITUTION; ANTIGEN RECOGNITION; ARTICLE; CELL SELECTION; CELLULAR IMMUNITY; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE DURATION; EXTRACELLULAR SPACE; FOLLOW UP; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; INTRACELLULAR SPACE; LYMPHOCYTE FUNCTION; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PERSISTENT VIRUS INFECTION; PRIORITY JOURNAL; PROSPECTIVE STUDY; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; VIREMIA; VIRUS CELL INTERACTION; VIRUS ENVELOPE; VIRUS IMMUNITY; VIRUS MUTANT; VIRUS REPLICATION; VIRUS RESISTANCE;

AMINO ACID SUBSTITUTION; CD8-POSITIVE T-LYMPHOCYTES; CONSENSUS SEQUENCE; EPITOPES, T-LYMPHOCYTE; HEPACIVIRUS; HEPATITIS C; HUMANS; PEPTIDES; POLYMORPHISM, GENETIC; SELECTION (GENETICS); T-LYMPHOCYTE SUBSETS; VIRAL STRUCTURAL PROTEINS; VIREMIA; VIRUS REPLICATION;

EID: 21344442507     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20050121     Document Type: Article

References (61)

1. World Health Organization. 1997. Hepatitis C: global prevalence. Weekly Epidemiological Record. 72:341-348.
2. Alter, M.J. 1997. Epidemiology of hepatitis C. Hepatology. 26:62S-65S.
3. Alter, M.J. 1995. Epidemiology of hepatitis C in the West. Semin. Liver Dis. 15:5-14.
4. Centers for Disease Control and Prevention. 1998. Recommendations for prevention and control of hepatitis C virus (HCV) infection and HCV-related chronic disease. MMWR 47(No. RR-19):1-39.
5. Villano, S.A., D. Vlahov, K.E. Nelson, S. Cohn, and D.L. Thomas. 1999. Persistence of viremia and the importance of long-term follow-up after acute hepatitis C infection. Hepatology. 29:908-914.
6. Cao, J., N. Sullivan, E. Desjardin, C. Parolin, J. Robinson, R. Wyatt, and J. Sodroski. 1997. Replication and neutralization of human immunodeficiency virus type 1 lacking the V1 and V2 variable loops of the gp120 envelope glycoprotein. J. Virol. 71:9808-9812.
7. Tong, M.J., N.S. El-Farra, A.R. Reikes, and R.L. Co. 1995. Clinical outcomes after transfusion-associated hepatitis C. N. Engl. J. Med. 332: 1463-1466.
8. Gerlach, J.T., H.M. Diepolder, R. Zachoval, N.H. Gruener, M.C. Jung, A. Ulsenheimer, W.W. Schraut, C.A. Schirren, M. Waechlter, M. Backmund, and G.R. Pape. 2003. Acute hepatitis C: high rate of both spontaneous and treatment-induced viral clearance. Gastroenterology. 125:80-88.
9. Jaeckel, E., M. Cornberg, H. Wedemeyer, T. Santantonio, J. Mayer, M. Zankel, G. Pastore, M. Dietrich, C. Trautwein, and M.P. Manns. 2001. Treatment of acute hepatitis C with interferon alfa-2b. N. Engl. J. Med. 345:1452-1457.
10. Nomura, H., S. Sou, H. Tanimoto, T. Nagahama, Y. Kimura, J. Hayashi, H. Ishibashi, and S. Kashiwagi. 2004. Short-term interferon-alfa therapy for acute hepatitis C: a randomized controlled trial. Hepatology. 39:1213-1219.
11. Cooper, S., A.L. Erickson, E.J. Adams, J. Kansopon, A.J. Weiner, D.Y. Chien, M. Houghton, P. Parham, and C.M. Walker. 1999. Analysis of a successful immune response against hepatitis C virus. Immunity. 10:439-449.
12. + T cells with viral clearance in acute hepatitis C. J. Infect. Dis. 181:1528-1536.
13. Lechner, F., D.K. Wong, P.R. Dunbar, R. Chapman, R.T. Chung, P. Dohrenwend, G. Robbins, R. Phillips, P. Klenerman, and B.D. Walker. 2000. Analysis of successful immune responses in persons infected with hepatitis C virus. J. Exp. Med. 191:1499-1512.
14. Takaki, A., M. Wiese, G. Maertens, E. Depla, U. Seifert, A. Liebetrau, J.L. Miller, M.P. Manns, and B. Rehermann. 2000. Cellular immune responses persist and humoral responses decrease two decades after recovery from a single-source outbreak of hepatitis C. Nat. Med. 6:578-582.
15. + T lymphocytes after infection with hepatitis C virus. J. Virol. 75:5550-5558.
16. Thimme, R., D. Oldach, K.M. Chang, C. Steiger, S.C. Ray, and F.V. Chisari. 2001. Determinants of viral clearance and persistence during acute hepatitis C virus infection. J. Exp. Med. 194:1395-1406.
17. 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.
18. 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. Hepatology. 25:705-712.
19. 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.
20. Rehermann, B., K.M. Chang, J.G. McHutchison, R. Kokka, M. Houghton, and F.V. Chisari. 1996. Quantitative analysis of the peripheral blood cytotoxic T lymphocyte response in patients with chronic hepatitis C virus infection. J. Clin. Invest. 98:1432-1440.
21. Crispe, I.N. 2003. Hepatic T cells and liver tolerance. Nat. Rev. Immunol. 3:51-62.
22. 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.
23. 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.
24. Wong, D.K., D.D. Dudley, N.H. Afdhal, J. Dienstag, C.M. Rice, L.P. 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.
25. + T cells in chronic hepatitis C virus infection. J. Immunol. 169:3447-3458.
26. Bain, C., A. Fatmi, F. Zoulim, J.P. Zarski, C. Trepo, and G. Inchauspe. 2001. Impaired allostimulatory function of dendritic cells in chronic hepatitis C infection. Gastroenterology. 120:512-524.
27. Kanto, T., N. Hayashi, T. Takehara, T. Tatsumi, N. Kuzushita, A. Ito, Y. Sasaki, A. Kasahara, and M. Hori. 1999. Impaired allostimulatory capacity of peripheral blood dendritic cells recovered from hepatitis C virus-infected individuals. J. Immunol. 162:5584-5591.
28. + cytotoxic T lymphocyte response. J. Exp. Med. 200:1243-1256.
29. Neumann, A.U., N.P. Lam, H. Dahari, D.R. Gretch, T.E. Wiley, T.J. Layden, and A.S. Perelson. 1998. Hepatitis C viral dynamics in vivo and the antiviral efficacy of interferon-alpha therapy. Science. 282:103-107.
30. Eckels, D.D., H. Wang, T.H. Bian, N. Tabatabai, and J.C. Gill. 2000. Immunobiology of hepatitis C virus (HCV) infection: the role of CD4 T cells in HCV infection. Immunol. Rev. 174:90-97.
31. Erickson, A.L., Y. Kimura, S. Igarashi, J. Eichelberger, M. Houghton, J. Sidney, D. McKinney, A. Sette, A.L. Hughes, and C.M. Walker. 2001. The outcome of hepatitis C virus infection is predicted by escape mutations in epitopes targeted by cytotoxic T lymphocytes. Immunity. 15:883-895.
32. Timm, J., G.M. Lauer, D.G. Kavanagh, I. Sheridan, A.Y. Kim, M. Lucas, T. Pillay, K. Ouchi, L.L. Reyor, J.S. Zur Wiesch, et al. 2004. CD8 epitope escape and reversion in acute HCV infection. J. Exp. Med. 200:1593-1604.
33. 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.
34. Kaneko, T., I. Nakamura, H. Kita, K. Hiroishi, T. Moriyama, and M. Imawari. 1996. Three new cytotoxic T cell epitopes identified within the hepatitis C virus nucleoprotein. J. Gen. Virol. 77:1305-1309.
35. 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. 115:954-966.
36. Mizukoshi, E., C. Eisenbach, B. Edlin, C. Weiler, M. Carrington, T. O'Brien, and B. Rehermann. 2003. HCV-specific cellular immune responses in subjects who are anti-HCV-negative, HCV RNA-negative despite long term (>15 years) injection drug use. Hepatology 38:210A (Abstr.).
37. + lymphocytes can control HIV infection in vitro by suppressing virus replication. Science. 234:1563-1566.
38. Seifert, U., H. Liermann, V. Racanelli, A. Halenius, M. Wiese, H. Wedemeyer, T. Ruppert, K. Rispeter, P. Henklein, A. Sijts, et al. 2004. Hepatitis C virus mutation affects proteasomal epitope processing. J. Clin. Invest. 114:250-259.
39. Ray, S.C., L. Fanning, X.-H. Wang, D.M. Netski, E. Kenny-Walsh, and D.L. Thomas. 2005. Divergent and convergent evolution following a common-source outbreak of hepatitis C virus. J. Exp. Med. 201:1753-1759.
40. He, X.S., B. Rehermann, F.X. Lopez-Labrador, J. Boisvert, R. Cheung, J. Mumm, H. Wedemeyer, M. Berenguer, T.L. Wright, M.M. Davis, and H.B. Greenberg. 1999. Quantitative analysis of hepatitis C virus-specific CD8(+) T cells in peripheral blood and liver using peptide-MHC tetramers. Proc. Natl. Acad. Sci. USA. 96:5692-5697.
41. Wong, D.K., D.D. Dudley, P.B. Dohrenwend, G.M. Lauer, R.T. Chung, D.L. Thomas, and B.D. Walker. 2001. Detection of diverse hepatitis C virus (HCV)-specific cytotoxic T lymphocytes in peripheral blood of infected persons by screening for responses to all translated proteins of HCV. J. Virol. 75:1229-1235.
42. Farci, P., A. Shimoda, A. Coiana, G. Diaz, G. Peddis, J.C. Melpolder, A. Strazzera, D.Y. Chien, S.J. Munoz, A. Balestrieri, et al. 2000. The outcome of acute hepatitis C predicted by the evolution of the viral quasispecies. Science. 288:339-344.
43. Friedrich, T.C., E.J. Dodds, L.J. Yant, L. Vojnov, R. Rudersdorf, C. Cullen, D.T. Evans, R.C. Desrosiers, B.R. Mothe, J. Sidney, et al. 2004. Reversion of CTL escape-variant immunodeficiency viruses in vivo. Nat. Med. 10:275-281.
44. Allen, T.M., M. Altfeld, X.G. Yu, K.M. O'Sullivan, M. Lichterfeld, S. Le Gall, M. John, B.R. Mothe, P.K. Lee, E.T. Kalife, et al. 2004. Selection, transmission, and reversion of an antigen-processing cytotoxic T-lymphocyte escape mutation in human immunodeficiency virus type 1 infection. J. Virol. 78:7069-7078.
45. Grakoui, A., N.H. Shoukry, D.J. Woollard, J.H. Han, H.L. Hanson, J. Ghrayeb, K.K. Murthy, C.M. Rice, and C.M. Walker. 2003. HCV persistence and immune evasion in the absence of memory T cell help. Science. 302:659-662.
46. Foy, E., K. Li, C. Wang, R. Sumpter, Jr., M. Ikeda, S.M. Lemon, and M. Gale, Jr. 2003. Regulation of interferon regulatory factor-3 by the hepatitis C virus serine protease. Science. 300:1145-1148.
47. Gale, M.J., C.M. Blakely, B. Kwieciszewski, S.L. Tan, M. Dossett, N.M. Tang, M.J. Korth, S.J. Polyak, D.R. Gretch, and M.G. Katze. 1998. Control of PKR protein kinase by hepatitis C virus nonstructural 5A protein: molecular mechanisms of kinase regulation. Mol. Cell. Biol. 18:5208-5218.
48. Klenerman, P., and R.M. Zinkernagel. 1998. Original antigenic sin impairs cytotoxic T lymphocyte responses to viruses bearing variant epitopes. Nature. 394:482-485.
49. Garfein, R.S., M.C. Doherty, E.R. Monterroso, D.L. Thomas, K.E. Nelson, and D. Vlahov. 1998. Prevalence and incidence of hepatitis C virus infection among young adult injection drug users. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 18(Suppl. 1):S11-S19.
50. Liu, Z., D.M. Netski, Q. Mao, O. Laeyendecker, J.R. Ticehurst, X.H. Wang, D.L. Thomas, and S.C. Ray. 2004. Accurate representation of the hepatitis C virus quasispecies in 5.2-kilobase amplicons. J. Clin. Microbiol. 42:4223-4229.
51. Ray, S.C., R.R. Arthur, A. Carella, J. Bukh, and D.L. Thomas. 2000. Genetic epidemiology of hepatitis C virus throughout Egypt. J. Infect. Dis. 182:698-707.
52. Jeanmougin, F., J.D. Thompson, M. Gouy, D.G. Higgins, and T.J. Gibson. 1998. Multiple sequence alignment with Clustal X. Trends Biochem. Sci. 23:403-405.
53. Hall, T.A. 2001. BioEdit: Biological sequence alignment editor for Windows 95/98/NT version 5.0.9. software. http://www.mbio.ncsu.edu/ RNaseP/info/programs/BIOEDIT/bioedit.html.
54. Posada, D., and K.A. Crandall. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics. 14:817-818.
55. Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution. 39:783-791.
56. Cox, A.L., D.M. Netski, T. Mosbruger, S.G. Sherman, S. Strathdee, D.C. Ompad, D. Vlahov, D. Chien, V. Shyamala, S.C. Ray, and D.L. Thomas. 2004. Prospective evaluation of community-acquired acute hepatitis C virus infection. Clin. Infect. Dis. 40:951-958.
57. Wang, Y.M., S.C. Ray, O. Laeyendecker, J.R. Ticehurst, and D.L. Thomas. 1998. Assessment of hepatitis C virus sequence complexity by electrophoretic mobilities of both single- and double-stranded DNAs. J. Clin. Microbiol. 36:2982-2989.
58. Lauer, G.M., K. Ouchi, R.T. Chung, T.N. Nguyen, C.L. Day, D.R. Purkis, M. Reiser, A.Y. Kim, M. Lucas, P. Klenerman, and B.D. Walker. 2002. Comprehensive analysis of CD8(+)-T-cell responses against hepatitis C virus reveals multiple unpredicted specificities. J. Virol. 76:6104-6113.
59. Ward, S., G. Lauer, R. Isba, B. Walker, and P. Klenerman. 2002. Cellular immune responses against hepatitis C virus: the evidence base 2002. Clin. Exp. Immunol. 128:195-203.
60. Currier, J.R., E.G. Kuta, E. Turk, L.B. Earhart, L. Loomis-Price, S. Janetzki, G. Ferrari, D.L. Birx, and J.H. Cox. 2002. A panel of MHC class I restricted viral peptides for use as a quality control for vaccine trial ELISPOT assays. J. Immunol. Methods. 260:157-172.
61. Sidney, J., S. Southwood, C. Oseroff, J.F. Del Guercio, A. Sette, and H. Grey. 1998. Measurement of MHC/peptide interactions by gel filtration. In Current Protocols in Immunology. B. Bierer, J.E. Coligan, D.H. Margulies, E.M. Shevach, W. Strober, and A. Kruisbeek, editors. John Wiley & Sons, Inc., New York. 18.3.1-18.3.19.