Subversion of immune responses by hepatitis C virus: Immunomodulatory strategies beyond evasion?

Current Opinion in Immunology

Volumn 15, Issue 4, 2003, Pages 443-449

  Hahn, Young S ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD81 ANTIGEN; COMPLEMENT RECEPTOR; CORE PROTEIN; EPITOPE; GLYCOPROTEIN E; ISOPROTEIN;

CELL ACTIVITY; CELL FUNCTION; CHRONIC DISEASE; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; IMMUNE RESPONSE; IMMUNOMODULATION; MOLECULAR INTERACTION; NATURAL KILLER CELL; PERSISTENT VIRUS INFECTION; PROTEIN INTERACTION; REGULATORY MECHANISM; REVIEW; T LYMPHOCYTE; VIRUS ENVELOPE; VIRUS MUTATION;

EID: 0042905866     PISSN: 09527915     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0952-7915(03)00076-1     Document Type: Review

References (75)

1. Alter M.J. Epidemiology of hepatitis C. Hepatology. 26:1997;62S-65S.
2. Choo Q.L., Kuo G., Weiner A., Wang K.S., Overby L., Bradley D., Houghton M. Identification of the major, parenteral non-A, non-B hepatitis agent (hepatitis C virus) using a recombinant cDNA approach. Semin Liver Dis. 12:1992;279-288.
3. Tanaka Y., Hanada K., Mizokami M., Yeo A.E., Shih J.W., Gojobori T., Alter H.J. A comparison of the molecular clock of hepatitis C virus in the United States and Japan predicts that hepatocellular carcinoma incidence in the United States will increase over the next two decades. Proc Natl Acad Sci USA. 99:2002;15584-15589.
4. El-Serag H.B., Hampel H., Yeh C., Rabeneck L. Extrahepatic manifestations of hepatitis C among United States male veterans. Hepatology. 36:2002;1439-1445.
5. Houghton M: Hepatitis C viruses. In Fields Virology, edn 3. Edited by Fields BN, Knipe DM, Howley PM et al. Philadelphia: Lippincott-Raven Publishers; 1996.
6. Houghton M., Weiner A., Han J., Kuo G., Choo Q.L. Molecular biology of the hepatitis C viruses: implications for diagnosis, development and control of viral disease. Hepatology. 14:1991;381-388.
7. Hamaia S., Li C., Allain J.P. The dynamics of hepatitis C virus binding to platelets and 2 mononuclear cell lines. Blood. 98:2001;2293-2300.
8. Sung V.M., Shimodaira S., Doughty A.L., Picchio G.R., Can H., Yen T.S., Lindsay K.L., Levine A.M., Lai M.M. 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. 77:2003;2134-2146.
9. Jardi R., Rodriguez F., Buti M., Costa X., Cotrina M., Galimany R., Esteban R., Guardia J. Role of hepatitis B, C, and D viruses in dual and triple infection: influence of viral genotypes and hepatitis B precore and basal core promoter mutations on viral replicative interference. Hepatology. 34:2001;404-410.
10. Spinzi G., Pellicano R., Minoli G., Terreni N., Cutufia M.A., Fagoonee S., Rizzetto M., Ponzetto A. Helicobacter pyloris prevalence in hepatitis C virus positive patients with cirrhosis. The Como cross-sectional study. Panminerva Med. 43:2001;85-87.
11. Mohamed A., Elsheikh A., Ghandour Z., Al Karawi M. Impact of hepatitis C virus infection on schistosomal liver disease. Hepatogastroenterology. 45:1998;1492-1496.
12. Blanton R.E., Salam E.A., Kariuki H.C., Magak P., Silva L.K., Muchiri E.M., Thiongo F., Abdel-Meghid I.E., Butterworth A.E., Reis M.G.et al. Population-based differences in Schistosoma mansoni- and hepatitis C-induced disease. J Infect Dis. 185:2002;1644-1649.
13. Chen M., Sallberg M., Sonnerborg A., Weiland O., Mattsson L., Jin L., Birkett A., Peterson D., Milich D.R. Limited humoral immunity in hepatitis C virus infection. Gastroenterology. 116:1999;135-143.
14. Cerny A., Chisari F.V. Pathogenesis of chronic hepatitis C: immunological features of hepatic injury and viral persistence. Hepatology. 30:1999;595-601.
15. Koziel M.J., Dudley D., Afdhal N., Choo Q.L., Houghton M., Ralston R., Walker B.D. Hepatitis C virus (HCV)-specific cytotoxic T lymphocytes recognize epitopes in the core and envelope proteins of HCV. J Virol. 67:1993;7522-7532.
16. Nelson D.R., Marousis C.G., Davis G.L., Rice C.M., Wong J., Houghton M., Lau J.Y. The role of hepatitis C virus-specific cytotoxic T lymphocytes in chronic hepatitis C. J Immunol. 158:1997;1473-1481.
17. Gerlach J.T., Diepolder H.M., Jung M.C., Gruener N.H., Schraut W.W., Zachoval R., Hoffmann R., Schirren C.A., Santantonio T., Pape G.R. Recurrence of hepatitis C virus after loss of virus-specific CD4(+) T-cell response in acute hepatitis C. Gastroenterology. 117:1999;933-941.
18. Cooper S., Erickson A.L., Adams E.J., Kansopon J., Weiner A.J., Chien D.Y., Houghton M., Parham P., Walker C.M. Analysis of a successful immune response against hepatitis C virus. Immunity. 10:1999;439-449.
19. Lechner F., Gruener N.H., Urbani S., Uggeri J., Santantonio T., Kammer A.R., Cerny A., Phillips R., Ferrari C., Pape G.R.et al. CD8+ T lymphocyte responses are induced during acute hepatitis C virus infection but are not sustained. Eur J Immunol. 30:2000;2479-2487.
20. Chisari F.V. Cytotoxic T cells and viral hepatitis. J Clin Invest. 99:1997;1472-1477.
21. Takaki A., Wiese M., Maertens G., Depla E., Seifert U., Liebetrau A., Miller J.L., Manns M.P., Rehermann B. Cellular immune responses persist and humoral responses decrease two decades after recovery from a single-source outbreak of hepatitis C. Nat Med. 6:2000;578-582.
22. He X.S., Rehermann B., Lopez-Labrador F.X., Boisvert J., Cheung R., Mumm J., Wedemeyer H., Berenguer M., Wright T.L., Davis M.M.et al. Quantitative analysis of hepatitis C virus-specific CD8+ T cells in peripheral blood and liver using peptide-MHC tetramers. Proc Natl Acad Sci USA. 96:1999;5692-5697.
23. Grabowska A.M., Lechner F., Klenerman P., Tighe P.J., Ryder S., Ball J.K., Thomson B.J., Irving W.L., Robins R.A. Direct ex vivo comparison of the breadth and specificity of the T cells in the liver and peripheral blood of patients with chronic HCV infection. Eur J Immunol. 31:2001;2388-2394.
24. Wong D.K., Dudley D.D., Afdhal N.H., Dienstag J., Rice C.M., Wang L., Houghton M., Walker B.D., Koziel M.J. Liver-derived CTL in hepatitis C virus infection: breadth and specificity of responses in a cohort of persons with chronic infection. J Immunol. 160:1998;1479-1488.
25. Thimme R., Oldach D., Chang K.M., Steiger C., Ray S.C., Chisari F.V. Determinants of viral clearance and persistence during acute hepatitis C virus infection. J Exp Med. 194:2001;1395-1406.
26. Thimme R., Bukh J., Spangenberg H.C., Wieland S., Pemberton J., Steiger C., Govindarajan S., Purcell R.H., Chisari F.V. Viral and immunological determinants of hepatitis C virus clearance, persistence, and disease. Proc Natl Acad Sci USA. 99:2002;15661-15668.
27. Su A.I., Pezacki J.P., Wodicka L., Brideau A.D., Supekova L., Thimme R., Wieland S., Bukh J., Purcell R.H., Schultz P.G.et al. Genomic analysis of the host response to hepatitis C virus infection. Proc Natl Acad Sci USA. 99:2002;15669-15674 The progression of HCV infection was examined by gene analysis of liver biopsies in acutely infected chimpanzees that developed persistent infection, transient viral clearance or sustained clearance. Genes related to the induction of IFN-γ, antigen processing and presentation, and T-cell recruitment correlate with viral clearance. Interestingly, HCV-infected cells successfully induce the expression of antiviral IFN-α-stimulated genes, but these genes have no effect on viral clearance.
28. Bukh J., Miller R.H., Purcell R.H. Genetic heterogeneity of hepatitis C virus: quasispecies and genotypes. Semin Liver Dis. 15:1995;41-63.
29. Neumann A.U., Lam N.P., Dahari H., Gretch D.R., Wiley T.E., Layden T.J., Perelson A.S. Hepatitis C viral dynamics in vivo and the antiviral efficacy of interferon-alpha therapy. Science. 282:1998;103-107.
30. Farci P., Shimoda A., Wong D., Cabezon T., De G.D., Strazzera A., Shimizu Y., Shapiro M., Alter H.J., Purcell R.H. Prevention of hepatitis C virus infection in chimpanzees by hyperimmune serum against the hypervariable region 1 of the envelope 2 protein. Proc Natl Acad Sci USA. 93:1996;15394-15399.
31. Farci P., Shimoda A., Coiana A., Diaz G., Peddis G., Melpolder J.C., Strazzera A., Chien D.Y., Munoz S.J., Balestrieri A.et al. The outcome of acute hepatitis C predicted by the evolution of the viral quasispecies. Science. 288:2000;339-344.
32. Ray S.C., Mao Q., Lanford R.E., Bassett S., Laeyendecker O., Wang Y.M., Thomas D.L. Hypervariable region 1 sequence stability during hepatitis C virus replication in chimpanzees. J Virol. 74:2000;3058-3066.
33. Farci P., Alter H.J., Govindarajan S., Wong D.C., Engle R., Lesniewski R.R., Mushahwar I.K., Desai S.M., Miller R.H., Ogata N.et al. Lack of protective immunity against reinfection with hepatitis C virus. Science. 258:1992;135-140.
34. Eckels D.D., Wang H., Bian T.H., Tabatabai N., Gill J.C. Immunobiology of hepatitis C virus (HCV) infection: the role of CD4 T cells in HCV infection. Immunol Rev. 174:2000;90-97.
35. Weiner A., Erickson A.L., Kansopon J., Crawford K., Muchmore E., Hughes A.L., Houghton M., Walker C.M. Persistent hepatitis C virus infection in a chimpanzee is associated with emergence of a cytotoxic T lymphocyte escape variant. Proc Natl Acad Sci USA. 92:1995;2755-2759.
36. Wang H., Eckels D.D. Mutations in immunodominant T cell epitopes derived from the nonstructural 3 protein of hepatitis C virus have the potential for generating escape variants that may have important consequences for T cell recognition. J Immunol. 162:1999;4177-4183.
37. Erickson A.L., Kimura Y., Igarashi S., Eichelberger J., Houghton M., Sidney J., McKinney D., Sette A., Hughes A.L., Walker C.M. The outcome of hepatitis C virus infection is predicted by escape mutations in epitopes targeted by cytotoxic T lymphocytes. Immunity. 15:2001;883-895.
38. Chang K.M., Rehermann B., McHutchison J.G., Pasquinelli C., Southwood S., Sette A., Chisari F.V. Immunological significance of cytotoxic T lymphocyte epitope variants in patients chronically infected by the hepatitis C virus. J Clin Invest. 100:1997;2376-2385.
39. Gruner N.H., Gerlach T.J., Jung M.C., Diepolder H.M., Schirren C.A., Schraut W.W., Hoffmann R., Zachoval R., Santantonio T., Cucchiarini M.et al. Association of hepatitis C virus-specific CD8+ T cells with viral clearance in acute hepatitis C. J Infect Dis. 181:2000;1528-1536.
40. Lechner F., Wong D.K., Dunbar P.R., Chapman R., Chung R.T., Dohrenwend P., Robbins G., Phillips R., Klenerman P., Walker B.D. Analysis of successful immune responses in persons infected with hepatitis C virus. J Exp Med. 191:2000;1499-1512.
41. + T cells might contribute to viral persistence.
42. + T-cell function remains dysfunctional in chronic patients.
43. Gruener N.H., Lechner F., Jung M., Diepolder H., Gerlach T., Lauer G., Walker B., Sullivan J., Phillips R., Pape D.et al. Sustained dysfunction of antiviral CD8+ T lymphocytes after infection with hepatitis C virus. J Virol. 75:2001;5550-5558.
44. Bain C., Fatmi A., Zoulim F., Zarski J.P., Trepo C., Inchauspe G. Impaired allostimulatory function of dendritic cells in chronic hepatitis C infection. Gastroenterology. 120:2001;512-524.
45. Lee C.H., Choi Y.H., Yang S.H., Lee C.W., Ha S.J., Sung Y.C. Hepatitis C virus core protein inhibits interleukin 12 and nitric oxide production from activated macrophages. Virology. 279:2001;271-279.
46. Sarobe P., Lasarte J.J., Casares N., Lopez-Diaz De Cerio A., Baixeras E., Labarga P., Garcia N., Borras-Cuesta F., Prieto J. Abnormal priming of CD4(+) T cells by dendritic cells expressing hepatitis C virus core and E1 proteins. J Virol. 76:2002;5062-5070.
47. Lai M.M., Ware C.F. Hepatitis C virus core protein: possible roles in viral pathogenesis. Curr Top Microbiol Immunol. 242:2000;117-134.
48. Ray R.B., Ray R. Hepatitis C virus core protein: intriguing properties and functional relevance. FEMS Microbiol Lett. 202:2001;149-156.
49. Large M.K., Kittlesen D.J., Hahn Y.S. Suppression of host immune response by the core protein of hepatitis C virus: possible implications for hepatitis C virus persistence. J Immunol. 162:1999;931-938.
50. Soguero C., Joo M., Chianese-Bullock K.A., Nguyen D.T., Tung K., Hahn Y.S., Hepatitis C. virus core protein leads to immune suppression and liver damage in a transgenic murine model. J Virol. 76:2002;9345-9354.
51. Matsumoto M., Hsieh T., Zhu N., VanArsdale T., Hwang S.B., Jeng K., Gorbalenya A.E., Lo S., Ou J., Ware C.F., Lai M.M. Hepatitis C virus core protein interacts with the cytoplasmic tail of Lymphotoxin-B receptor. J Virol. 71:1997;1301-1309.
52. Kittlesen D.J., Chianese-Bullock K.A., Yao Z.Q., Braciale T.J., Hahn Y.S. Interaction between complement receptor gC1qR and hepatitis C virus core protein inhibits T-lymphocyte proliferation. J Clin Invest. 106:2000;1239-1249.
53. Zhu N., Ware C.F., Lai M.M. Hepatitis C virus core protein enhances FADD-mediated apoptosis and suppresses TRADD signaling of tumor necrosis factor receptor. Virology. 283:2001;178-187.
54. Hahn C.S., Cho Y., Kang B.S., Lester I.M., Hahn Y.S. The HCV core protein acts as a positive regulator of Fas-mediated apoptosis in a human lymphoblastoid T cell line: Possible implications for HCV pathogenesis. Virology. 276:2000;127-137.
55. Widell A., Molnegren V., Pieksma F., Calmann M., Peterson J., Lee S.R. Detection of hepatitis C core antigen in serum or plasma as a marker of hepatitis C viraemia in the serological window-phase. Transfus Med. 12:2002;107-113.
56. Maillard P., Krawczynski K., Nitkiewicz J., Bronnert C., Sidorkiewicz M., Gounon P., Dubuisson J., Faure G., Crainic R., Budkowska A. Nonenveloped nucleocapsids of hepatitis C virus in the serum of infected patients. J Virol. 75:2001;8240-8250.
57. Ishida S., Kaito M., Kohara M., Tsukiyama-Kohora K., Fujita N., Ikoma J., Adachi Y., Watanabe S. Hepatitis C virus core particle detected by immunoelectron microscopy and optical rotation technique. Hepatol Res. 20:2001;335-347.
58. Yao Z.Q., Nguyen D.T., Hiotellis A.I., Hahn Y.S. Hepatitis C virus core protein inhibits human T lymphocyte responses by a complement-dependent regulatory pathway. J Immunol. 167:2001;5264-5272.
59. Reid K.B., Colomb M.G., Loos M. Complement component C1 and the collectins: parallels between routes of acquired and innate immunity. Immunol Today. 19:1998;56-59.
60. Ghebrehiwet B., Lim B.L., Kumar R., Feng X., Peerschke E.I. gC1q-R/p33, a member of a new class of multifunctional and multicompartmental cellular proteins, is involved in inflammation and infection. Immunol Rev. 180:2001;65-77.
61. Feng X., Tonnesen M.G., Peerschke E.I., Ghebrehiwet B. Cooperation of C1q receptors and integrins in C1q-mediated endothelial cell adhesion and spreading. J Immunol. 168:2002;2441-2448.
62. Karp C.L., Wahl L.M., Ahearn J.M., Cuomo P.J., Sherry B., Trinchieri G., Griffin D.E. Mechanism of suppression of cell-mediated immunity by measles virus. Science. 273:1996;228-231.
63. Fingeroth J.D., Weis J.J., Tedder T.F., Strominger J.L., Biro P.A., Fearon D.T. Epstein-Barr virus receptor of human B lymphocytes is the C3d receptor CR2. Proc Natl Acad Sci USA. 81:1984;4510-4514.
64. Viscidi R.P., Mayur K., Lederman H.M., Frankel A.D. Inhibition of antigen-induced lymphocyte proliferation by Tat protein from HIV-1. Science. 246:1989;1606-1608.
65. Chang K.M., Thimme R., Melpolder J.J., Oldach D., Pemberton J., Moorhead-Loudis J., McHutchison J.G., Alter H.J., Chisari F.V. Differential CD4(+) and CD8(+) T-cell responsiveness in hepatitis C virus infection. Hepatology. 33:2001;267-276.
66. Alvarez-Obregon J.C., Duenas-Carrera S., Valenzuela C., Grillo J.M. A truncated HCV core protein elicits a potent immune response with a strong participation of cellular immunity components in mice. Vaccine. 19:2001;3940-3946.
67. Duenas-Carrera S., Alvarez-Lajonchere L., Alvarez-Obregon J.C., Herrera A., Lorenzo L.J., Pichardo D., Morales J. A truncated variant of the hepatitis C virus core induces a slow but potent immune response in mice following DNA immunization. Vaccine. 19:2000;992-997.
68. Liu Z.X., Nishida H., He J.W., Lai M.M., Feng N., Dennert G. Hepatitis C virus genotype 1b core protein does not exert immunomodulatory effects on virus-induced cellular immunity. J Virol. 76:2002;990-997.
69. Poccia F., Agrati C., Ippolito G., Colizzi V., Malkovsky M. Natural T cell immunity to intracellular pathogens and nonpeptidic immunoregulatory drugs. Curr Mol Med. 1:2001;137-151.
70. Biron C.A., Brossay L. NK cells and NKT cells in innate defense against viral infections. Curr Opin Immunol. 13:2001;458-464.
71. Fiore G., Angarano I., Caccetta L., Serrone M., Jirillo E., Schiraldi O., Antonaci S. In-situ immunophenotyping study of hepatic-infiltrating cytotoxic cells in chronic active hepatitis C. Eur J Gastroenterol Hepatol. 9:1997;491-496.
72. Par G., Rukavina D., Podack E., Horanyi M., Szekeres-Bartho J., Hegedus G., Paal M., Szereday L., Mozsik G., Par A. Decrease in CD3-negative-CD8dim(+) and Vdelta2/Vgamma9 TcR+ peripheral blood lymphocyte counts, low perforin expression and the impairment of natural killer cell activity is associated with chronic hepatitis C virus infection. J Hepatol. 37:2002;514.
73. Pileri P., Uematsu Y., Campagnoli S., Galli G., Falugi F., Petracca R., Weiner A.J., Houghton M., Rosa D., Grandi G.et al. Binding of hepatitis C virus to CD81. Science. 282:1998;938-941.
74. Crotta S., Stilla A., Wack A., D'Andrea A., Nuti S., D'Oro U., Mosca M., Filliponi F., Brunetto R.M., Bonino F.et al. Inhibition of natural killer cells through engagement of CD81 by the major hepatitis C virus envelope protein. J Exp Med. 195:2002;35-41 HCV envelope protein E2 binds to CD81. Interestingly, the cross-linking of CD81 by immobilized E2 exerts the opposing effect on the function of NK cells and T cells. E2-CD81 engagement inhibits the cytolytic activity and IFN-γ production of NK cells, whereas it stimulates T-cell proliferation.
75. Tseng C.T., Klimpel G.R. Binding of the hepatitis C virus envelope protein E2 to CD81 inhibits natural killer cell functions. J Exp Med. 195:2002;43-49 The cross-linking of CD81 by HCV E2 protein or anti-CD81 antibodies blocks NK cell activation in terms of cytokine production, cytotoxic granule release and proliferation. By contrast, CD81 ligation delivered a co-stimulatory signal to NK-like T cells.