Immune-based therapy for chronic hepatitis C

Journal of Leukocyte Biology

Volumn 86, Issue 1, 2009, Pages 33-39

  Chang, Dong Yeop ^a   Shin, Eui Cheol ^a  

^a Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

Author keywords

Cytokine; HCV; Immunotherapy; T cell

Indexed keywords

ANTIVIRUS AGENT; CPG 10101; ETANERCEPT; GAMMA INTERFERON; HEPATITIS C VIRUS AB68 ANTIBODY; HEPATITIS C VIRUS ANTIGEN; HLA A2 EPITOPE PEPTIDE; HLA A24 EPITOPE PEPTIDE; INTERLEUKIN 10; INTERLEUKIN 10 ANTIBODY; INTERLEUKIN 12; ISATORIBINE; PD 1 ANTIBODY; PEGINTERFERON ALPHA; PEPTIDE VACCINE; RECOMBINANT GAMMA INTERFERON; RECOMBINANT INTERLEUKIN 12; RESIQUIMOD; RIBAVIRIN; UNCLASSIFIED DRUG; VIRUS VACCINE;

ANTIINFLAMMATORY ACTIVITY; ANTIVIRAL ACTIVITY; CLINICAL FEATURE; DRUG EFFICACY; DRUG MECHANISM; GENOTYPE; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOTHERAPY; INTERVENTION STUDY; MONOTHERAPY; PRIORITY JOURNAL; REVIEW; VACCINATION; VIROLOGY; ARTICLE; CHRONIC DISEASE; METHODOLOGY;

HEPATITIS C VIRUS;

CHRONIC DISEASE; HEPATITIS C; HUMANS; IMMUNOTHERAPY;

EID: 68849127031     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.1208772     Document Type: Review

References (61)

1. World Health Organization (1997) HCV: global prevention. Wkly. Epidemiol. Rec. 72, 341-348.
2. Alter, H. J., Seeff, L. B. (2000) Recovery, persistence, and sequelae in hepatitis C virus infection: a perspective on long-term outcome. Semin. Liver Dis. 20, 17-35.
3. Fried, M. W., Shiffman, M. L., Reddy, K. R., Smith, C., Marinos, G., Gonçales Jr., F. L., Häussinger, D., Diago, M., Carosi, G., Dhumeaux, D., Craxi, A., Lin, A., Hoffman, J., Yu, J. (2002) Peginterferon α-2a plus ribavirin for chronic hepatitis C virus infection. N. Engl. J. Med. 347, 975-982.
4. Manns, M. P., McHutchison, J. G., Gordon, S. C., Rustgi, V. K., Shiffman, M., Reindollar, R., Goodman, Z. D., Koury, K., Ling, M., Albrecht, J. K. (2001) Peginterferon α-2b plus ribavirin compared with interferon α-2b plus ribavirin for initial treatment of chronic hepatitis C: a randomized trial. Lancet 358, 958-965. (Pubitemid 32913521)
5. Seeff, L. B. (2002) Natural history of chronic hepatitis C. Hepatology 36, S35-S46.
6. Rehermann, B., Nascimbeni, M. (2005) Immunology of hepatitis B virus and hepatitis C virus infection. Nat. Rev. Immunol. 5, 215-229.
7. Dustin, L. B., Rice, C. M. (2007) Flying under the radar: the immunobiology of hepatitis C. Annu. Rev. Immunol. 25, 71-99.
8. Shin, E. C., Seifert, U., Kato, T., Rice, C. M., Feinstone, S. M., Kloetzel, P. M., Rehermann, B. (2006) Virus-induced type I IFN stimulates generation of immunoproteasomes at the site of infection. J. Clin. Invest. 116, 3006-3014. (Pubitemid 44684485)
9. Shin, E. C., Capone, S., Cortese, R., Colloca, S., Nicosia, A., Folgori, A., Rehermann, B. (2008) The kinetics of hepatitis C virus-specific CD8 T-cell responses in the blood mirror those in the liver in acute hepatitis C virus infection. J. Virol. 82, 9782-9788.
10. Folgori, A., Capone, S., Ruggeri, L., Meola, A., Sporeno, E., Ercole, B. B., Pezzanera, M., Tafi, R., Arcuri, M., Fattori, E., Lahm, A., Luzzago, A., Vitelli, A., Colloca, S., Cortese, R., Nicosia, A. (2006) A T-cell HCV vaccine eliciting effective immunity against heterologous virus challenge in chimpanzees. Nat. Med. 12, 190-197. (Pubitemid 43214745)
11. Klade, C. S., Wedemeyer, H., Berg, T., Hinrichsen, H., Cholewinska, G., Zeuzem, S., Blum, H., Buschle, M., Jelovcan, S., Buerger, V., Tauber, E., Frisch, J., Manns, M. P. (2008) Therapeutic vaccination of chronic hepatitis C nonresponder patients with the peptide vaccine IC41. Gastroenterology 134, 1385-1395.
12. Schlaphoff, V., Klade, C. S., Jilma, B., Jelovcan, S. B., Cornberg, M., Tauber, E., Manns, M. P., Wedemeyer, H., The IC41 Study Group. (2007) Functional and phenotypic characterization of peptide-vaccine-induced HCV-specific CD8+ T cells in healthy individuals and chronic hepatitis C patients. Vaccine 25, 6793-6806.
13. Yutani, S., Yamada, A., Yoshida, K., Takao, Y., Tamura, M., Komatsu, N., Ide, T., Tanaka, M., Sata, M., Itoh, K. (2007) Phase I clinical study of a personalized peptide vaccination for patients infected with hepatitis C virus (HCV) 1b who failed to respond to interferon-based therapy. Vaccine 25, 7429-7435. (Pubitemid 47484009)
14. Nevens, F., Roskams, T., Van Vlierberghe, H., Horsmans, Y., Sprengers, D., Elewaut, A., Desmet, V., Leroux-Roels, G., Quinaux, E., Depla, E., Dincq, S., Vander Stichele, C., Maertens, G., Hulstaert, F. (2003) A pilot study of therapeutic vaccination with envelope protein E1 in 35 patients with chronic hepatitis C. Hepatology 38, 1289-1296. (Pubitemid 37314839)
15. Godfrey, D. I., MacDonald, H. R., Kronenberg, M., Smyth, M. J., Van Kaer, L. (2004) NKT cells: what's in a name? Nat. Rev. Immunol. 4, 231-237. (Pubitemid 38339089)
16. Veldt, B. J., van der Vliet, H. J., von Blomberg, B. M., van Vlierberghe, H., Gerken, G., Nishi, N., Hayashi, K., Scheper, R. J., de Knegt, R. J., van den Eertwegh, A. J., Janssen, H. L., van Nieuwkerk, C. M. (2007) Randomized placebo controlled phase I/II trial of α-galactosylceramide for the treatment of chronic hepatitis C. J. Hepatol. 47, 356-365. (Pubitemid 47176162)
17. Shin, E. C., Rehermann, B. (2006) Taking the brake off T cells in chronic viral infection. Nat. Med. 12, 276-277. (Pubitemid 43355069)
18. Barber, D. L., Wherry, E. J., Masopust, D., Zhu, B., Allison, J. P., Sharpe, A. H., Freeman, G. J., Ahmed, R. (2006) Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439, 682-687. (Pubitemid 43237609)
19. Sharpe, A. H., Wherry, E. J., Ahmed, R., Freeman, G. J. (2007) The function of programmed cell death 1 and its ligands in regulating autoimmunity and infection. Nat. Immunol. 8, 239-245. (Pubitemid 46745373)
20. Velu, V., Titanji, K., Zhu, B., Husain, S., Pladevega, A., Lai, L., Vanderford, T. H., Chennareddi, L., Silvestri, G., Freeman, G. J., Ahmed, R., Amara, R. R. (2009) Enhancing SIV-specific immunity in vivo by PD-1 blockade. Nature 458, 206-210.
21. Urbani, S., Amadei, B., Tola, D., Massari, M., Schivazappa, S., Missale, G., Ferrari, C. (2006) PD-1 expression in acute hepatitis C virus (HCV) infection is associated with HCV-specific CD8 exhaustion. J. Virol. 80, 11398-11403. (Pubitemid 44706581)
22. Radziewicz, H., Ibegbu, C. C., Fernandez, M. L., Workowski, K. A., Obideen, K., Wehbi, M., Hanson, H. L., Steinberg, J. P., Masopust, D., Wherry, E. J., Altman, J. D., Rouse, B. T., Freeman, G. J., Ahmed, R., Grakoui, A. (2007) Liver-infiltrating lymphocytes in chronic human hepatitis C virus infection display an exhausted phenotype with high levels of PD-1 and low levels of CD127 expression. J. Virol. 81, 2545-2553. (Pubitemid 46447020)
23. Golden-Mason, L., Palmer, B., Klarquist, J., Mengshol, J. A., Castelblanco, N., Rosen, H. R. (2007) Upregulation of PD-1 expression on circulating and intrahepatic hepatitis C virus-specific CD8+ T cells associated with reversible immune dysfunction. J. Virol. 81, 9249-9258. (Pubitemid 47311467)
24. Nakamoto, N., Kaplan, D. E., Coleclough, J., Li, Y., Valiga, M. E., Kaminski, M., Shaked, A., Olthoff, K., Gostick, E., Price, D. A., Freeman, G. J., Wherry, E. J., Chang, K. M. (2008) Functional restoration of HCV-specific CD8 T cells by PD-1 blockade is defined by PD-1 expression and compartmentalization. Gastroenterology 134, 1927-1937.
25. Rutebemberwa, A., Ray, S. C., Astemborski, J., Levine, J., Liu, L., Dowd, K. A., Clute, S., Wang, C., Korman, A., Sette, A., Sidney, J., Pardoll, D. M., Cox, A. L. (2008) High-programmed death-1 levels on hepatitis C virus-specific T cells during acute infection are associated with viral persistence and require preservation of cognate antigen during chronic infection. J. Immunol. 181, 8215-8225.
26. Ejrnaes, M., Filippi, C. M., Martinic, M. M., Ling, E. M., Togher, L. M., Crotty, S., von Herrath, M. G. (2006) Resolution of a chronic viral infection after interleukin-10 receptor blockade. J. Exp. Med. 203, 2461-2472. (Pubitemid 44664616)
27. Brooks, D. G., Trifilo, M. J., Edelmann, K. H., Teyton, L., McGavern, D. B., Oldstone, M. B. (2006) Interleukin-10 determines viral clearance or persistence in vivo. Nat. Med. 12, 1301-1309. (Pubitemid 44706933)
28. Ferrari, C. (2008) Therapeutic vaccination for hepatitis C: can protective T-cell responses be restored after prolonged antigen exposure? Gastroenterology 134, 1601-1604.
29. Ha, S. J., Mueller, S. N., Wherry, E. J., Barber, D. L., Aubert, R. D., Sharpe, A. H., Freeman, G. J., Ahmed, R. (2008) Enhancing therapeutic vaccination by blocking PD-1-mediated inhibitory signals during chronic infection. J. Exp. Med. 205, 543-555.
30. Brooks, D. G., Lee, A. M., Elsaesser, H., McGavern, D. B., Oldstone, M. B. (2008) IL-10 blockade facilitates DNA vaccine-induced T cell responses and enhances clearance of persistent virus infection. J. Exp. Med. 205, 533-541.
31. Law, M., Maruyama, T., Lewis, J., Giang, E., Tarr, A. W., Stamataki, Z., Gastaminza, P., Chisari, F. V., Jones, I. M., Fox, R. I., Ball, J. K., McKeating, J. A., Kneteman, N. M., Burton, D. R. (2008) Broadly neutralizing antibodies protect against hepatitis C virus quasispecies challenge. Nat. Med. 14, 25-27.
32. Galun, E., Terrault, N. A., Eren, R., Zauberman, A., Nussbaum, O., Terkieltaub, D., Zohar, M., Buchnik, R., Ackerman, Z., Safadi, R., Ashur, Y., Misrachi, S., Liberman, Y., Rivkin, L., Dagan, S. (2007) Clinical evaluation (phase I) of a human monoclonal antibody against hepatitis C virus: safety and antiviral activity. J. Hepatol. 46, 37-44. (Pubitemid 44827422)
33. Schiano, T. D., Charlton, M., Younossi, Z., Galun, E., Pruett, T., Tur-Kaspa, R., Eren, R., Dagan, S., Graham, N., Williams, P. V., Andrews, J. (2006) Monoclonal antibody HCV-AbXTL68 in patients undergoing liver transplantation for HCV: results of a phase 2 randomized study. Liver Transpl. 12, 1381-1389. (Pubitemid 44405128)
34. Davis, G. L., Nelson, D. R., Terrault, N., Pruett, T. L., Schiano, T. D., Fletcher, C. V., Sapan, C. V., Riser, L. N., Li, Y., Whitley, R. J., Gnann Jr., J. W., Collaborative Antiviral Study Group (2005) A randomized, open-label study to evaluate the safety and pharmacokinetics of human hepatitis C immune globulin (Civacir) in liver transplant recipients. Liver Transpl. 11, 941-949.
35. Abu Dayyeh, B. K., Chung, R. T. (2008) Broadly neutralizing antibodies against hepatitis C virus: new hope for immunization? Gastroenterology 134, 2184-2186.
36. Feld, J. J., Hoofnagle, J. H. (2005) Mechanism of action of interferon and ribavirin in treatment of hepatitis C. Nature 436, 967-972. (Pubitemid 41191673)
37. Frese, M., Schwärzle, V., Barth, K., Krieger, N., Lohmann, V., Mihm, S., Haller, O., Bartenschlager, R. (2002) Interferon-γ inhibits replication of subgenomic and genomic hepatitis C virus RNAs. Hepatology 35, 694-703. (Pubitemid 34183976)
38. Cheney, I. W., Lai, V. C., Zhong, W., Brodhag, T., Dempsey, S., Lim, C., Hong, Z., Lau, J. Y., Tam, R. C. (2002) Comparative analysis of anti-hepatitis C virus activity and gene expression mediated by α, β, and γ interferons. J. Virol. 76, 11148-11154. (Pubitemid 35176233)
39. Soza, A., Heller, T., Ghany, M., Lutchman, G., Liang, T. J., Germain, J., Hsu, H. H., Park, Y., Hoofnagle, J. H. (2005) Pilot study of interferon γ for chronic hepatitis C. J. Hepatol. 43, 67-71. (Pubitemid 40805274)
40. Shin, E. C., Protzer, U., Untergasser, A., Feinstone, S. M., Rice, C. M., Hasselschwert, D., Rehermann, B. (2005) Liver-directed γ interferon gene delivery in chronic hepatitis C. J. Virol. 79, 13412-13420. (Pubitemid 41508154)
41. Zeuzem, S., Hopf, U., Carreno, V., Diago, M., Shiffman, M., Grüne, S., Dudley, F. J., Rakhit, A., Rittweger, K., Yap, S. H., Koff, R. S., Thomas, H. C. (1999) A phase I/II study of recombinant human interleukin-12 in patients with chronic hepatitis C. Hepatology 29, 1280-1287. (Pubitemid 29168766)
42. O'Brien, C. B., Moonka, D. K., Henzel, B. S., Caufield, M., DeBruin, M. F. (2001) A pilot trial of recombinant interleukin-12 in patients with chronic hepatitis C who previously failed treatment with interferon-α. Am. J. Gastroenterol. 96, 2473-2479. (Pubitemid 32769214)
43. Pockros, P. J., Patel, K., O'Brien, C., Tong, M., Smith, C., Rustgi, V., Carithers, R. L., McHutchison, J. G., Olek, E., Debruin, M. F. (2003) A multicenter study of recombinant human interleukin 12 for the treatment of chronic hepatitis C virus infection in patients nonresponsive to previous therapy. Hepatology 37, 1368-1374. (Pubitemid 36667317)
44. Kawai, T., Akira, S. (2006) Innate immune recognition of viral infection. Nat. Immunol. 7, 131-137. (Pubitemid 43135878)
45. Horsmans, Y., Berg, T., Desager, J. P., Mueller, T., Schott, E., Fletcher, S. P., Steffy, K. R., Bauman, L. A., Kerr, B. M., Averett, D. R. (2005) Isatoribine, an agonist of TLR7, reduces plasma virus concentration in chronic hepatitis C infection. Hepatology 42, 724-731. (Pubitemid 41233667)
46. Pockros, P. J., Guyader, D., Patton, H., Tong, M. J., Wright, T., McHutchison, J. G., Meng, T. C. (2007) Oral resiquimod in chronic HCV infection: safety and efficacy in 2 placebo-controlled, double-blind phase IIa studies. J. Hepatol. 47, 174-182. (Pubitemid 47021257)
47. Lee, J., Wu, C. C., Lee, K. J., Chuang, T. H., Katakura, K., Liu, Y. T., Chan, M., Tawatao, R., Chung, M., Shen, C., Cottam, H. B., Lai, M. M., Raz, E., Carson, D. A. (2006) Activation of anti-hepatitis C virus responses via Toll-like receptor 7. Proc. Natl. Acad. Sci. USA 103, 1828-1833. (Pubitemid 43228778)
48. McHutchison, J. G., Bacon, B. R., Gordon, S. C., Lawitz, E., Shiffman, M., Afdhal, N. H., Jacobson, I. M., Muir, A., Al-Adhami, M., Morris, M. L., Lekstrom-Himes, J. A., Efler, S. M., Davis, H. L. (2007) Phase 1B, randomized, double-blind, dose-escalation trial of CPG 10101
49. Kanzler, H., Barrat, F. J., Hessel, E. M., Coffman, R. L. (2007) Therapeutic targeting of innate immunity with Toll-like receptor agonists and antagonists. Nat. Med. 13, 552-559. (Pubitemid 46830615)
50. Chuang, E., Del Vecchio, A., Smolinski, S., Song, X. Y., Sarisky, R. T. (2004) Biomedicines to reduce inflammation but not viral load in chronic HCV - what's the sense? Trends Biotechnol. 22, 517-523. (Pubitemid 39265183)
51. Batdelger, D., Dandii, D., Jirathitikal, V., Bourinbaiar, A. S. (2008) Open-label trial of therapeutic immunization with oral V-5 Immunitor (V5) vaccine in patients with chronic hepatitis C. Vaccine 26, 2733-2737.
52. Hong, F., Nguyen, V. A., Gao, B. (2001) Tumor necrosis factor α attenuates interferon α signaling in the liver: involvement of SOCS3 and SHP2 and implication in resistance to interferon therapy. FASEB J. 15, 1595-1597.
53. Frese, M., Barth, K., Kaul, A., Lohmann, V., Schwärzle, V., Bartenschlager, R. (2003) Hepatitis C virus RNA replication is resistant to tumor necrosis factor-α. J. Gen. Virol. 84, 1253-1259. (Pubitemid 36592618)
54. Zein, N. N., Etanercept Study Group. (2005) Etanercept as an adjuvant to interferon and ribavirin in treatment-naive patients with chronic hepatitis C virus infection: a phase 2 randomized, double-blind, placebo-controlled study. J. Hepatol. 42, 315-322.
55. Nelson, D. R., Lauwers, G. Y., Lau, J. Y., Davis, G. L. (2000) Interleukin 10 treatment reduces fibrosis in patients with chronic hepatitis C: a pilot trial of interferon nonresponders. Gastroenterology 118, 655-660. (Pubitemid 30171614)
56. Nelson, D. R., Tu, Z., Soldevila-Pico, C., Abdelmalek, M., Zhu, H., Xu, Y. L., Cabrera, R., Liu, C., Davis, G. L. (2003) Long-term interleukin 10 therapy in chronic hepatitis C patients has a proviral and anti-inflammatory effect. Hepatology 38, 859-868. (Pubitemid 37221669)
57. Ulloa, L., Doody, J., Massagué, J. (1999) Inhibition of transforming growth factor-β/SMAD signaling by the interferon-γ/STAT pathway. Nature 397, 710-713. (Pubitemid 29108392)
58. Pockros, P. J., Jeffers, L., Afdhal, N., Goodman, Z. D., Nelson, D., Gish, R. G., Reddy, K. R., Reindollar, R., Rodriguez-Torres, M., Sullivan, S., Blatt, L. M., Faris-Young, S. (2007) Final results of a double-blind, placebo-controlled trial of the antifibrotic efficacy of interferon-γ1b in chronic hepatitis C patients with advanced fibrosis or cirrhosis. Hepatology 45, 569-578. (Pubitemid 46450609)
59. Sáez-Royuela, F., Porres, J. C., Moreno, A., Castillo, I., Martinez, G., Galiana, F., Carreño, V. (1991) High doses of recombinant α-interferon or γ-interferon for chronic hepatitis C: a randomized, controlled trial. Hepatology 13, 327-331.
60. Di Bisceglie, A. M., Shiffman, M. L., Everson, G. T., Lindsay, K. L., Everhart, J. E., Wright, E. C., Lee, W. M., Lok, A. S., Bonkovsky, H. L., Morgan, T. R., Ghany, M. G., Morishima, C., Snow, K. K., Dienstag, J. L., HALT-C Trial Investigators. (2008) Prolonged therapy of advanced chronic hepatitis C with low-dose peginterferon. N. Engl. J. Med. 359, 2429-2441.
61. Lok, A. S., Seeff, L. B., Morgan, T. R., Di Bisceglie, A. M., Sterling, R. K., Curto, T. M., Everson, G. T., Lindsay, K. L., Lee, W. M., Bonkovsky, H. L., Dienstag, J. L., Ghany, M. G., Morishima, C., Goodman, Z. D., HALT-C Trial Group. (2009) Incidence of hepatocellular carcinoma and associated risk factors in hepatitis C-related advanced liver disease. Gastroenterology 136, 138-148.