Immune responses in hepatitis C virus infection and mechanisms of hepatitis C virus persistence

Journal of Gastroenterology and Hepatology (Australia)

Volumn 23, Issue 10, 2008, Pages 1473-1482

  Hiroishi, Kazumasa ^a   Ito, Takayoshi ^a   Imawari, Michio ^a  

^a SHOWA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Cytotoxic T lymphocyte; Dendritic cell; Helper T cell; Natural killer cell; Regulatory T cell

Indexed keywords

ALPHA INTERFERON; AMINO ACID; RIBAVIRIN; VIRUS PROTEIN;

ADOPTIVE TRANSFER; ANTIVIRAL THERAPY; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOPATHOGENESIS; IMMUNOSUPPRESSIVE TREATMENT; LIVER CELL; LIVER CIRRHOSIS; MUTATION; NATURAL KILLER CELL; NATURAL KILLER T CELL; NONHUMAN; PATHOGENESIS; PERSISTENT VIRUS INFECTION; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

EID: 53349099559     PISSN: 08159319     EISSN: 14401746     Source Type: Journal    
DOI: 10.1111/j.1440-1746.2008.05475.x     Document Type: Review

References (69)

1. Choo QL, Kuo G, Weiner AJ, Overby LR, Bradley DW, Houghton M. Isolation of a cDNA clone derived from a blood-borne non-a, non-b viral hepatitis genome. Science 1989 244 : 359 62.
2. Imawari M, Nomura M, Kaieda T et al. Establishment of a human T-cell clone cytotoxic for both autologous and allogeneic hepatocytes from chronic hepatitis patients with type non-A, non-B virus. Proc. Natl. Acad. Sci. USA 1989 86 : 2883 7.
3. Kita H, Moriyama T, Kaneko T et al. HLA B44-restricted cytotoxic T lymphocytes recognizing an epitope on hepatitis C virus nucleocapsid protein. Hepatology. 1993 18 : 1039 44.
4. Yap KL, Ada GL, McKenzie IF. Transfer of specific cytotoxic T lymphocytes protects mice inoculated with influenza virus. Nature 1978 273 : 238 9.
5. Kita H, Hiroishi K, Moriyama T et al. A minimal and optimal cytotoxic T cell epitope within hepatitis C virus nucleoprotein. J. Gen. Virol. 1995 76 (Pt 12 3189 93.
6. Kaneko T, Nakamura I, Kita H, Hiroishi K, Moriyama T, Imawari M. Three new cytotoxic T cell epitopes identified within the hepatitis C virus nucleoprotein. J. Gen. Virol. 1996 77 (Pt 6 1305 9.
7. Hakamada T, Funatsuki K, Morita H et al. Identification of novel hepatitis C virus-specific cytotoxic T lymphocyte epitopes by ELISpot assay using peptides with human leukocyte antigen-A*2402-binding motifs. J. Gen. Virol. 2004 85 : 1521 31.
8. Wertheimer AM, Miner C, Lewinsohn DM, Sasaki AW, Kaufman E, Rosen HR. Novel CD4+ and CD8+ T-cell determinants within the NS3 protein in subjects with spontaneously resolved HCV infection. Hepatology 2003 37 : 577 89.
9. Hiroishi K, Kita H, Kojima M et al. Cytotoxic T lymphocyte response and viral load in hepatitis C virus infection. Hepatology 1997 25 : 705 12.
10. Rothman AL, Morishima C, Bonkovsky HL et al. Associations among clinical, immunological, and viral quasispecies measurements in advanced chronic hepatitis C. Hepatology 2005 41 : 617 25.
11. Urbani S, Amadei B, Fisicaro P et al. Heterologous T cell immunity in severe hepatitis C virus infection. J. Exp. Med. 2005 201 : 675 80.
12. Soderholm J, Ahlen G, Kaul A et al. Relation between viral fitness and immune escape within the hepatitis C virus protease. Gut 2006 55 : 266 74.
13. Ando K, Hiroishi K, Kaneko T et al. Perforin, Fas/Fas ligand, and TNF-alpha pathways as specific and bystander killing mechanisms of hepatitis C virus-specific human CTL. J. Immunol. 1997 158 : 5283 91.
14. Kaneko T, Moriyama T, Udaka K et al. Impaired induction of cytotoxic T lymphocytes by antagonism of a weak agonist borne by a variant hepatitis C virus epitope. Eur. J. Immunol. 1997 27 : 1782 7.
15. Hiroishi K, Eguchi J, Ishii S, Okamoto H, Mitamura K, Imawari M. Differential effect of cytotoxic T lymphocyte variant epitopes on generation and cytotoxicity in chronic hepatitis C virus infection. Hepatol. Res. 2002 24 : 91 4.
16. Zhou YH, Sugitani M, Esumi M. Sequences in the hypervariable region 1 of hepatitis C virus show only minimal variability in the presence of antibodies against hypervariable region 1 during acute infection in chimpanzees. Arch. Virol. 2002 147 : 1955 62.
17. von Hahn T, Yoon JC, Alter H et al. Hepatitis C virus continuously escapes from neutralizing antibody and T-cell responses during chronic infection in vivo. Gastroenterology 2007 132 : 667 78.
18. Wang JH, Layden TJ, Eckels DD. Modulation of the peripheral T-Cell response by CD4 mutants of hepatitis C virus: transition from a Th1 to a Th2 response. Hum. Immunol. 2003 64 : 662 73.
19. Urbani S, Amadei B, Cariani E et al. The impairment of CD8 responses limits the selection of escape mutations in acute hepatitis C virus infection. J. Immunol. 2005 175 : 7519 29.
20. Tseng CT, Klimpel GR. Binding of the hepatitis C virus envelope protein E2 to CD81 inhibits natural killer cell functions. J. Exp. Med. 2002 195 : 43 9.
21. Herzer K, Falk CS, Encke J et al. Upregulation of major histocompatibility complex class I on liver cells by hepatitis C virus core protein via p53 and TAP1 impairs natural killer cell cytotoxicity. J. Virol. 2003 77 : 8299 309.
22. Jinushi M, Takehara T, Tatsumi T et al. Negative regulation of NK cell activities by inhibitory receptor CD94/NKG2A leads to altered NK cell-induced modulation of dendritic cell functions in chronic hepatitis C virus infection. J. Immunol. 2004 173 : 6072 81.
23. Nattermann J, Nischalke HD, Hofmeister V et al. The HLA-A2 restricted T cell epitope HCV core 35-44 stabilizes HLA-E expression and inhibits cytolysis mediated by natural killer cells. Am. J. Pathol. 2005 166 : 443 53.
24. Ahlenstiel G, Rehermann B. Hepatitis C virus and the threshold of natural killer cell inhibition. Hepatology 2005 41 : 675 7.
25. Zuckerman E, Slobodin G, Kessel A et al. Peripheral B-cell CD5 expansion and CD81 overexpression and their association with disease severity and autoimmune markers in chronic hepatitis C virus infection. Clin. Exp. Immunol. 2002 128 : 353 8.
26. Maki A, Matsuda M, Asakawa M, Kono H, Fujii H, Matsumoto Y. Decreased CD3 zeta molecules of T lymphocytes from patients with hepatocellular carcinoma associated with hepatitis C virus. Hepatol. Res. 2003 27 : 272 8.
27. Missale G, Cariani E, Ferrari C. Role of viral and host factors in HCV persistence: which lesson for therapeutic and preventive strategies? Dig. Liver Dis. 2004 36 : 703 11.
28. Kittlesen DJ, Chianese-Bullock KA, Yao ZQ, Braciale TJ, Hahn YS. Interaction between complement receptor gC1qR and hepatitis C virus core protein inhibits T-lymphocyte proliferation. J. Clin. Invest. 2000 106 : 1239 49.
29. Yao ZQ, Eisen-Vandervelde A, Ray S, Hahn YS. HCV core/gC1qR interaction arrests T cell cycle progression through stabilization of the cell cycle inhibitor p27Kip1. Virology 2003 314 : 271 82.
30. Konan KV, Giddings TH Jr., Ikeda M, Li K, Lemon SM, Kirkegaard K. Nonstructural protein precursor NS4A/B from hepatitis C virus alters function and ultrastructure of host secretory apparatus. J. Virol. 2003 77 : 7843 55.
31. Francavilla V, Accapezzato D, De Salvo M et al. Subversion of effector CD8+ T cell differentiation in acute hepatitis C virus infection: exploring the immunological mechanisms. Eur. J. Immunol. 2004 34 : 427 37.
32. Yao ZQ, Nguyen DT, Hiotellis AI, Hahn YS. Hepatitis C virus core protein inhibits human T lymphocyte responses by a complement-dependent regulatory pathway. J. Immunol. 2001 167 : 5264 72.
33. Urbani S, Amadei B, Tola D et al. PD-1 expression in acute hepatitis C virus (HCV) infection is associated with HCV-specific CD8 exhaustion. J. Virol. 2006 80 : 11398 403.
34. Mehal WZ, Azzaroli F, Crispe IN. Immunology of the healthy liver: old questions and new insights. Gastroenterology 2001 120 : 250 60.
35. Sarobe P, Lasarte JJ, Zabaleta A et al. Hepatitis C virus structural proteins impair dendritic cell maturation and inhibit in vivo induction of cellular immune responses. J. Virol. 2003 77 : 10862 71.
36. Szabo G, Dolganiuc A. Subversion of plasmacytoid and myeloid dendritic cell functions in chronic HCV infection. Immunobiology 2005 210 : 237 47.
37. Wilson NS, Behrens GM, Lundie RJ et al. Systemic activation of dendritic cells by Toll-like receptor ligands or malaria infection impairs cross-presentation and antiviral immunity. Nat. Immunol. 2006 7 : 165 72.
38. Yakushijin T, Kanto T, Inoue M et al. Reduced expression and functional impairment of Toll-like receptor 2 on dendritic cells in chronic hepatitis C virus infection. Hepatol. Res. 2006 34 : 156 62.
39. Ulsenheimer A, Gerlach JT, Jung MC et al. Plasmacytoid dendritic cells in acute and chronic hepatitis C virus infection. Hepatology 2005 41 : 643 51.
40. Jinushi M, Takehara T, Tatsumi T et al. Autocrine/paracrine IL-15 that is required for type I IFN-mediated dendritic cell expression of MHC class I-related chain A and B is impaired in hepatitis C virus infection. J. Immunol. 2003 171 : 5423 9.
41. Lozach PY, Lortat-Jacob H, de Lavalette A et al. DC-SIGN and L-SIGN are high affinity binding receptors for hepatitis C virus glycoprotein E2. J. Biol. Chem. 2003 278 : 20358 66.
42. Pohlmann S, Zhang J, Baribaud F et al. Hepatitis C virus glycoproteins interact with DC-SIGN and DC-SIGNR. J. Virol. 2003 77 : 4070 80.
43. Siavoshian S, Abraham JD, Thumann C, Kieny MP, Schuster C. Hepatitis C virus core, NS3, NS5A, NS5B proteins induce apoptosis in mature dendritic cells. J. Med. Virol. 2005 75 : 402 11.
44. Rollier C, Drexhage JA, Verstrepen BE et al. Chronic hepatitis C virus infection established and maintained in chimpanzees independent of dendritic cell impairment. Hepatology 2003 38 : 851 8.
45. Piccioli D, Tavarini S, Nuti S et al. Comparable functions of plasmacytoid and monocyte-derived dendritic cells in chronic hepatitis C patients and healthy donors. J. Hepatol. 2005 42 : 61 7.
46. Li W, Li J, Tyrrell DL, Agrawal B. Expression of hepatitis C virus-derived core or NS3 antigens in human dendritic cells leads to induction of pro-inflammatory cytokines and normal T-cell stimulation capabilities. J. Gen. Virol. 2006 87 : 61 72.
47. Longman RS, Talal AH, Jacobson IM, Rice CM, Albert ML. Normal functional capacity in circulating myeloid and plasmacytoid dendritic cells in patients with chronic hepatitis C. J. Infect. Dis. 2005 192 : 497 503.
48. Blindenbacher A, Duong FH, Hunziker L et al. Expression of hepatitis c virus proteins inhibits interferon alpha signaling in the liver of transgenic mice. Gastroenterology 2003 124 : 1465 75.
49. Moorman JP, Prayther D, McVay D, Hahn YS, Hahn CS. The C-terminal region of hepatitis C core protein is required for Fas-ligand independent apoptosis in Jurkat cells by facilitating Fas oligomerization. Virology 2003 312 : 320 9.
50. Hahn YS. Subversion of immune responses by hepatitis C virus: immunomodulatory strategies beyond evasion?. Curr. Opin. Immunol. 2003 15 : 443 9.
51. Soguero C, Joo M, Chianese-Bullock KA, Nguyen DT, Tung K, Hahn YS. Hepatitis C virus core protein leads to immune suppression and liver damage in a transgenic murine model. J. Virol. 2002 76 : 9345 54.
52. Disson O, Haouzi D, Desagher S et al. Impaired clearance of virus-infected hepatocytes in transgenic mice expressing the hepatitis C virus polyprotein. Gastroenterology 2004 126 : 859 72.
53. Saito K, Meyer K, Warner R, Basu A, Ray RB, Ray R. Hepatitis C virus core protein inhibits tumor necrosis factor alpha-mediated apoptosis by a protective effect involving cellular FLICE inhibitory protein. J. Virol. 2006 80 : 4372 9.
54. van Driel IR, Ang DK. Role of regulatory T cells in gastrointestinal inflammatory disease. J. Gastroenterol. Hepatol. 2008 23 : 171 7.
55. Boettler T, Spangenberg HC, Neumann-Haefelin C et al. T cells with a CD4+CD25+ regulatory phenotype suppress in vitro proliferation of virus-specific CD8+ T cells during chronic hepatitis C virus infection. J. Virol. 2005 79 : 7860 7.
56. Sugimoto K, Ikeda F, Stadanlick J, Nunes FA, Alter HJ, Chang KM. Suppression of HCV-specific T cells without differential hierarchy demonstrated ex vivo in persistent HCV infection. Hepatology 2003 38 : 1437 48.
57. MacDonald AJ, Duffy M, Brady MT et al. CD4 T helper type 1 and regulatory T cells induced against the same epitopes on the core protein in hepatitis C virus-infected persons. J. Infect. Dis. 2002 185 : 720 7.
58. Accapezzato D, Francavilla V, Paroli M et al. Hepatic expansion of a virus-specific regulatory CD8(+) T cell population in chronic hepatitis C virus infection. J. Clin. Invest. 2004 113 : 963 72.
59. Sakaki M, Hiroishi K, Baba T et al. Intrahepatic status of regulatory T cells in autoimmune liver diseases and chronic viral hepatitis. Hepatol. Res. 2007.
60. Brady MT, MacDonald AJ, Rowan AG, Mills KH. Hepatitis C virus non-structural protein 4 suppresses Th1 responses by stimulating IL-10 production from monocytes. Eur. J. Immunol. 2003 33 : 3448 57.
61. Tajimi M, Ugajin T, Ota M, Hiroishi K, Nakamura I, Imawari M. Immune responses of liver-infiltrating lymphocytes and peripheral blood mononuclear cells to hepatitis C virus core and NS3 antigens. Hepatol. Res. 2006 35 : 250 5.
62. Gale MJ Jr., Korth MJ, Tang NM et al. Evidence that hepatitis C virus resistance to interferon is mediated through repression of the PKR protein kinase by the nonstructural 5A protein. Virology 1997 230 : 217 27.
63. Gale M Jr., Blakely CM, Kwieciszewski B et al. Control of PKR protein kinase by hepatitis C virus nonstructural 5A protein: molecular mechanisms of kinase regulation. Mol. Cell Biol. 1998 18 : 5208 18.
64. Foy E, Li K, Wang C et al. Regulation of interferon regulatory factor-3 by the hepatitis C virus serine protease. Science 2003 300 : 1145 8.
65. Meylan E, Curran J, Hofmann K et al. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 2005 437 : 1167 72.
66. Gehring S, Gregory SH, Kuzushita N, Wands JR. Type 1 interferon augments DNA-based vaccination against hepatitis C virus core protein. J. Med. Virol. 2005 75 : 249 57.
67. Fang SH, Hwang LH, Chen DS, Chiang BL. Ribavirin enhancement of hepatitis C virus core antigen-specific type 1 T helper cell response correlates with the increased IL-12 level. J. Hepatol. 2000 33 : 791 8.
68. Freeman AJ, Marinos G, Ffrench RA, Lloyd AR. Intrahepatic and peripheral blood virus-specific cytotoxic T lymphocyte activity is associated with a response to combination IFN-alpha and ribavirin treatment among patients with chronic hepatitis C virus infection. J. Viral. Hepat. 2005 12 : 125 9.
69. Yu H, Huang H, Xiang J, Babiuk LA, Hurk S. Dendritic cells pulsed with hepatitis C virus NS3 protein induce immune responses and protection from infection with recombinant vaccinia virus expressing NS3. J. Gen. Virol. 2006 87 : 1 10.