Modulation of the peripheral T-cell response by CD4 mutants of hepatitis C virus: Transition from a Th1 to a Th2 response

Human Immunology

Volumn 64, Issue 7, 2003, Pages 662-673

  Wang, Jane H ^a   Layden, Thomas J ^a   Eckels, David D ^b,c  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b CHILDREN S HOSPITAL OF WISCONSIN   (United States)

^c MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

Cytokines; HCV; Helper T cells; Peptides

Indexed keywords

HLA DR ANTIGEN; INTERLEUKIN 4;

AMINO ACID SUBSTITUTION; ARTICLE; CASE REPORT; CELL PROLIFERATION; CELLULAR IMMUNITY; CYTOKINE RELEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; MONONUCLEAR CELL; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN BINDING; QUANTITATIVE ANALYSIS; T LYMPHOCYTE; TH1 CELL; TH2 CELL;

EID: 0038345165     PISSN: 01988859     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0198-8859(03)00070-3     Document Type: Article

References (77)

1. Brodsky FM: Stealth, sabotage and exploitation. Immunol Rev 168:5, 1999.
2. Meier UC, Klenerman P, Griffin P, James W, Koppe B, Larder B, McMichael A, Phillips R: Cytotoxic T lymphocyte lysis inhibited by viable HIV mutants. Science 270:1360, 1995.
3. Goulder PJ, Walker BD: The great escape-AIDS viruses and immune control. Nat Med 5:1233, 1999.
4. Price DA, Meier UC, Klenerman P, Purbhoo MA, Phillips RE, Sewell AK: The influence of antigenic variation on cytotoxic T lymphocyte responses in HIV-1 infection. J Mol Med 76:699, 1998.
5. Nowak MA, May RM, Phillips RE, Rowland-Jones S, Lalloo DG, McAdam S, Klenerman P, Koppe B, Sigmund K, Bangham CR: Antigenic oscillations and shifting im munodominance in HIV-1 infections. Nature 375:606, 1995.
6. Chang KM, Rehermann B, McHutchison JG, Pasquinelli C, Southwood S, Sette A, Chisari FV: Immunological significance of cytotoxic T lymphocyte epitope variants in patients chronically infected by the hepatitis C virus. J Clin Invest 100:2376, 1997.
7. Diepolder HM, Hoffmann RM, Gerlach JT, Zachoval R, Jung MC, Pape GR: Immunopathogenesis of HCV infection. Curr Stud Hematol Blood Transfus 62:135, 1998.
8. McMichael A: T-cell responses and viral escape. Cell 93:673, 1998.
9. Wagner R, Leschonsky B, Harrer E, Paulus C, Weber C, Walker BD, Buchbinder S, Wolf H, Kalden JR, Harrer T: Molecular and functional analysis of a conserved CTL epitope in HIV-1 p24 recognized from a long-term nonprogressor: constraints on immune escape associated with targeting a sequence essential for viral replication. J Immunol 162:3727, 1999.
10. Yang OO, Nguyen PT, Kalams SA, Dorfman T, Gottlinger HG, Stewart S, Chen IS, Threlkeld S, Walker BD: Nef-mediated resistance of human immunodeficiency virus type 1 to antiviral cytotoxic T lymphocytes. J Virol 76:1626, 2002.
11. Klenerman P, Rowland-Jones S, McAdam S, Edwards J, Daenke S, Lalloo D, Koppe B, Rosenberg W, Boyd D, Edwards A, et al: Cytotoxic T-cell activity antagonized by naturally occurring HIV-1 Gag variants. Nature 369:403, 1994.
12. Klenerman P, Meier UC, Phillips RE, McMichael AJ: The effects of natural altered peptide ligands on the whole blood cytotoxic T lymphocyte response to human immunodeficiency virus. Eur J Immunol 25:1927, 1995.
13. Montefiori DC, Hill TS, Vo HT, Walker BD, Rosenberg ES: Neutralizing antibodies associated with viremia control in a subset of individuals after treatment of acute human immunodeficiency virus type 1 infection. J Virol 75:10200, 2001.
14. Price DA, Goulder PJ, Klenerman P, Sewell AK, Easterbrook PJ, Troop M, Bangham CR, Phillips RE: Positive selection of HIV-1 cytotoxic T lymphocyte escape variants during primary infection. Proc Natl Acad Sci USA 94:1890, 1997.
15. Wilson CC, Kalams SA, Wilkes BM, Ruhl DJ, Gao F, Hahn BH, Hanson IC, Luzuriaga K, Wolinsky S, Koup R, Buchbinder SP, Johnson RP, Walker BD: Overlapping epitopes in human immunodeficiency virus type 1 gp120 presented by HLA A, B, and C molecules: effects of viral variation on cytotoxic T-lymphocyte recognition. J Virol 71:1256, 1997.
16. Mehrotra PT, Wu D, Crim JA, Mostowski HS, Siegel JP: Effects of IL-12 on the generation of cytotoxic activity in human CD8+ T lymphocytes. J Immunol 151:2444, 1993.
17. Ciurea A, Klenerman P, Hunziker L, Horvath E, Senn BM, Ochsenbein AF, Hengartner H, Zinkernagel RM: Viral persistence in vivo through selection of neutralizing antibody-escape variants. Proc Natl Acad Sci USA 97:2749, 2000.
18. Isaguliants MG, Widell A, Zhang SM, Sidorchuk A, Levi M, Smirnov VD, Santantonio T, Diepolder HM, Pape GR, Nordenfelt E: Antibody responses against B-cell epitopes of the hypervariable region 1 of hepatitis C virus in self-limiting and chronic human hepatitis C followed-up using consensus peptides. J Med Virol 66:204, 2002.
19. Eckels DD, Wang H, Bian T-H, Tabatabai N, Gill JC: Immunobiology of hepatitis C virus infection: the role of CD4 T-cells in HCV infection. Immunol Rev 174:90, 2000.
20. Frasca L, Porto PD, Tuosto L, Marinari B, Scotta C, Carbonari M, Nicosia A, Piccolella E: Hypervariable region 1 variants act as TCR antagonists for hepatitis C virus-specific CD4+ T cells. J Immunol 163:650, 1999.
21. Gandhi RT, Walker BD: Immunologic control of HIV-1. Annu Rev Med 53:149, 2002.
22. Diepolder HM, Zachoval R, Hoffmann RM, Jung MC, Gerlach T, Pape GR: The role of hepatitis C virus specific CD4+ T lymphocytes in acute and chronic hepatitis C. J Mol Med 74:583, 1996.
23. Cohen DE, Walker BD: Human immunodeficiency virus pathogenesis and prospects for immune control in patients with established infection. Clin Infect Dis 32:1756, 2001.
24. Kalams SA, Buchbinder SP, Rosenberg ES, Billingsley JM, Colbert DS, Jones NG, Shea AK, Trocha AK, Walker BD: Association between virus-specific cytotoxic T-lymphocyte and helper responses in human immunodeficiency virus type 1 infection. J Virol 73:6715, 1999.
25. Norris PJ, Sumaroka M, Brander C, Moffett HF, Boswell SL, Nguyen T, Sykulev Y, Walker BD, Rosenberg ES: Multiple effector functions mediated by human immunodeficiency virus-specific CD4(+) T-cell clones. J Virol 75:9771, 2001.
26. Rosenberg ES, Billingsley JM, Caliendo AM, Boswell SL, Sax PE, Kalams SA, Walker BD: Vigorous HIV-1-specific CD4+ T cell responses associated with control of viremia. Science 278:1447, 1997.
27. Plebanski M, Flanagan KL, Lee EA, Reece WH, Hart K, Gelder C, Gillespie G, Pinder M, Hill AV: Interleukin 10-mediated immunosuppression by a variant CD4 T cell epitope of Plasmodium falciparum. Immunity 10:651, 1999.
28. Bertoletti A, Sette A, Chisari FV, Penna A, Levrero M, De Carli M, Fiaccadori F, Ferrari C: Natural variants of cytotoxic epitopes are T-cell receptor antagonists for antiviral cytotoxic T cells. Nature 369:407, 1994.
29. Koziel MJ: Immunology of viral hepatitis. Am J Med 100:98, 1996.
30. Rehermann B, Chang KM, McHutchison JG, Kokka R, Houghton M, Chisari FV: Quantitative analysis of the peripheral blood cytotoxic T lymphocyte response in patients with chronic hepatitis C virus infection. J Clin Invest 98:1432, 1996.
31. Chisari FV: Cytotoxic T cells and viral hepatitis. J Clin Invest 99:1472, 1997.
32. Chang KM, Thimme R, Melpolder JJ, Oldach D, Pemberton J, Moorhead-Loudis J, McHutchison JG, Alter HJ, Chisari FV: Differential CD4(+) and CD8(+) T-cell responsiveness in hepatitis C virus infection. Hepatology 33:267, 2001.
33. Koziel MJ, Walker BD: Characteristics of the intrahepatic cytotoxic T lymphocyte response in chronic hepatitis C virus infection. Springer Semin Immunopathol 19:69, 1997.
34. Koziel MJ, Wong DK, Dudley D, Houghton M, Walker BD: Hepatitis C virus-specific cytolytic T lymphocyte and T helper cell responses in seronegative persons. J Infect Dis 176:859, 1997.
35. Mizukoshi E, Rehermann B: Immune responses and immunity in hepatitis C virus infection. J Gastroenterol 36:799, 2001.
36. Rehermann B, Chisari FV: Cell mediated immune response to the hepatitis C virus. Curr Top Microbiol Immunol 242:299, 2000.
37. Rehermann B: Interaction between the hepatitis C virus and the immune system. Semin Liver Dis 20:127, 2000.
38. Takaki A, Wiese M, Maertens G, Depla E, Seifert U, Liebetrau A, Miller JL, Manns MP, Rehermann B: Cellular immune responses persist and humoral responses decrease two decades after recovery from a single-source outbreak of hepatitis C. Nat Med 6:578, 2000.
39. Wong DK, Dudley DD, Dohrenwend PB, Lauer GM, Chung RT, Thomas DL, Walker BD: 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, 2001.
40. Wong DK, Dudley DD, Afdhal NH, Dienstag J, Rice CM, Wang L, Houghton M, Walker BD, Koziel MJ: 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, 1998.
41. Cerny A, Chisari FV: Pathogenesis of chronic hepatitis C: immunological features of hepatic injury and viral persistence. Hepatology 30:595, 1999.
42. Gruener NH, Lechner F, Jung MC, Diepolder H, Gerlach T, Lauer G, Walker B, Sullivan J, Phillips R, Pape GR, Klenerman P: Sustained dysfunction of antiviral CD8+ T lymphocytes after infection with hepatitis C virus. J Virol 75:5550, 2001.
43. Klenerman P, Lucas M, Barnes E, Harcourt G: Immunity to hepatitis C virus: stunned but not defeated. Microbes Infect 4:57, 2002.
44. Klenerman P, Lechner F, Kantzanou M, Ciurea A, Hengartner H, Zinkernagel R: Viral escape and the failure of cellular immune responses. Science 289:2003, 2000.
45. Martell M, Esteban JI, Quer J, Genesca J, Weiner A, Esteban R, Guardia J, Gomez J: Hepatitis C virus (HCV) circulates as a population of different but closely related genomes: quasispecies nature of HCV genome distribution. J Virol 66:3225, 1992.
46. Bouffard P, Hayashi PH, Acevedo R, Levy N, Zeldis JB: Hepatitis C virus is detected in a monocyte/macrophage subpopulation of peripheral blood mononuclear cells of infected patients. J Infect Dis 166:1276, 1992.
47. Sung VM, Shimodaira S, Doughty AL, Picchio GR, Can H, Yen TS, Lindsay KL, Levine AM, Lai MM: Establishment of B-cell lymphoma cell lines persistently infected with hepatitis C virus in vivo and in vitro: the apoptotic effects of virus infection. J Virol 77:2134, 2003.
48. Cooper S, Erickson AL, Adams EJ, Kansopon J, Weiner AJ, Chien DY, Houghton M, Parham P, Walker CM: Analysis of a successful immune response against hepatitis C virus. Immunity 10:439, 1999.
49. Napoli J, Bishop GA, McGuinness PH, Painter DM, McCaughan GW: Progressive liver injury in chronic hepatitis C infection correlates with increased intrahepatic expression of Th1-associated cytokines. Hepatology 24:759, 1996.
50. Eckels DD, Tabatabai N, Bian T-H, Wang H, Muheisen SS, Rice CM, Yoshizawa K, Gill J: In vitro human Th-cell responses to a recombinant hepatitis C virus antigen: failure in IL-2 production despite proliferation. Hum Immunol 60:187, 1999.
51. Tabatabai N, Bian TH, Rice CM, Yoshizawa K, Gill J, Eckels DD: Functionally distinct T-cell epitopes within the hepatitis C virus non-structural 3 protein. Hum Immunol 60:105, 1999.
52. Diepolder HM, Gerlach JT, Zachoval R, Hoffmann RM, Jung MC, Wierenga EA, Scholz S, Santantonio T, Houghton M, Southwood S, Sette A, Pape GR: Immunodominant CD4+ T-cell epitope within nonstructural protein 3 in acute hepatitis C virus infection. J Virol 71:6011, 1997.
53. Wang H, Eckels DD: Mutations in immunodominant T cell epitopes derived from the non-structural 3 protein of hepatitis C virus have the potential for generating escape variants that may have important consequences for T cell recognition. J Immunol 162:4177, 1999.
54. Eckels DD, Zhou H, Bian TH, Wang H: Identification of antigenic escape variants in an immunodominant epitope of Hepatitis C Virus. Int Immunol 11:577, 1999.
55. Wang H, Bian T, Merrill SJ, Eckels DD: Sequence variation in the gene encoding the nonstructural 3 protein of hepatitis C virus: evidence for immune selection. J Mol Evol 54:465, 2002.
56. Grakoui A, McCourt DW, Wychowski C, Feinstone SM, Rice CM: Characterization of the hepatitis C virus-encoded serine proteinase: Determination of proteinase-de pendent polyprotein cleavage sites. J Virol 67:2832, 1993.
57. Yoshioka K, Kakumu S, Wakita T, Ishikawa T, Itoh Y, Takayanagi M, Higashi Y, Shibata M, Morishima T: Detection of hepatitis C virus by polymerase chain reaction and response to interferon-alpha therapy: relationship to genotypes of hepatitis C virus. Hepatology 16:293, 1992.
58. Flint M, Maidens C, Loomis-Price LD, Shotton C, Dubuisson J, Monk P, Higginbottom A, Levy S, McKeating JA: Characterization of hepatitis C virus E2 glycoprotein interaction with a putative cellular receptor, CD81. J Virol 73:6235, 1999.
59. Gerlach JT, Diepolder HM, Jung MC, Gruener NH, Schraut WW, Zachoval R, Hoffmann R, Schirren CA, Santantonio T, Pape GR: Recurrence of hepatitis C virus after loss of virus-specific CD4(+) T-cell response in acute hepatitis C. Gastroenterol 117:933, 1999.
60. Pape GR, Gerlach TJ, Diepolder HM, Gruner N, Jung M, Santantonio T: Role of the specific T-cell response for clearance and control of hepatitis C virus. J Viral Hepat 6(Suppl 1):36, 1999.
61. Rico MA, Quiroga JA, Subira D, Garcia E, Castanon S, Sallberg M, Leroux-Roels G, Weiland O, Pardo M, Carreno V: Features of the CD4(+) T-cell response in liver and peripheral blood of hepatitis C virus-infected patients with persistently normal and abnormal alanine aminotransferase levels. J Hepatol 36:408, 2002.
62. Cerny A, Chisari FV: Pathogenesis of chronic hepatitis C: immunological features of hepatic injury and viral persistence. Hepatology 30:595, 1999.
63. Eckels DD, Flomenberg P, Gill JC: Hepatitis C virus: models of immunopathogenesis and prophylaxis. Transfusion 36:836, 1996.
64. Donnelly JJ, Ulmer JB, Shiver JW, Liu MA: DNA vaccines. Annu Rev Immunol 15:617, 1997.
65. Zhu F, Eckels DD: Functionally distinct helper T-cell epitopes of HCV and their role in modulation of NS3-specific, CD8+/tetramer positive CTL. Hum Immunol 63:710, 2002.
66. Guidotti LG, Rochford R, Chung J, Shapiro M, Purcell R, Chisari FV: Viral clearance without destruction of infected cells during acute HBV infection. Science 284:825, 1999.
67. Franco A, Guidotti LG, Hobbs MV, Pasquetto V, Chisari FV: Pathogenetic effector function of CD4-positive T helper 1 cells in hepatitis B virus transgenic mice. J Immunol 159:2001, 1997.
68. Guidotti LG, Ishikawa T, Hobbs MV, Matzke B, Schreiber R, Chisari FV: Intracellular inactivation of the hepatitis B virus by cytotoxic T lymphocytes. Immunity 4:25, 1996.
69. Novak EJ, Liu AW, Nepom GT, Kwok WW: MHC class II tetramers identify peptide-specific human CD4(+) T cells proliferating in response to influenza A antigen. J Clin Invest 104:R63, 1999.
70. Ciurea A, Hunziker L, Martinic MM, Oxenius A, Hengartner H, Zinkernagel RM: CD4+ T-cell-epitope escape mutant virus selected in vivo. Nat Med 7:795, 2001.
71. Murray JS, Madri J, Pasqualini T, Bottomly K: Functional CD4 T cell subset interplay in an intact immune system. J Immunol 150:4270, 1993.
72. Malherbe L, Filippi C, Julia V, Foucras G, Moro M, Appel H, Wucherpfennig K, Guery JC, Glaichenhaus N: Selective activation and expansion of high-affinity CD4+ T cells in resistant mice upon infection with Leishmania major. Immunity 13:771, 2000.
73. + T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature 389:737, 1997.
74. Sloan-Lancaster J, Evavold BD, Allen PM: Induction of T-cell anergy by altered T-cell-receptor ligand on live antigen-presenting cells. Nature 363:156, 1993.
75. Sloan-Lancaster J, Evavold BD, Allen PM: Th2 cell clonal anergy as a consequence of partial activation. J Exp Med 180:1195, 1994.
76. Plebanski M, Lee EA, Hannan CM, Flanagan KL, Gilbert SC, Gravenor MB, Hill AV: Altered peptide ligands narrow the repertoire of cellular immune responses by interfering with T-cell priming. Nat Med 5:565, 1999.
77. Pileri P, Uematsu Y, Campagnoli S, Galli G, Falugi F, Petracca R, Weiner AJ, Houghton M, Rosa D, Grandi G, Abrignani S: Binding of hepatitis C virus to CD81. Science 282:938, 1998.