IL-12-based vaccination therapy reverses liver-induced systemic tolerance in a mouse model of hepatitis B virus carrier

Journal of Immunology

Volumn 191, Issue 8, 2013, Pages 4184-4193

  Zeng, Zhutian ^a   Kong, Xiaohui ^a   Li, Fenglei ^a   Wei, Haiming ^a,b   Sun, Rui ^a,b   Tian, Zhigang ^a,b  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIBODY; GAMMA INTERFERON; HEPATITIS B CORE ANTIGEN; HEPATITIS B SURFACE ANTIBODY; HEPATITIS B VACCINE; INTERLEUKIN 12; RECOMBINANT HEPATITIS B SURFACE ANTIGEN VACCINE; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIGEN SPECIFICITY; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG EFFECT; DRUG POTENTIATION; DRUG RESPONSE; GERMINAL CENTER; HEPATITIS B; HUMORAL IMMUNITY; IMMUNOLOGICAL TOLERANCE; INFECTION PREVENTION; LIVER CELL; LYMPHOCYTE PROLIFERATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; TREATMENT DURATION; VACCINATION; VIRAL CLEARANCE;

ANIMALS; ASYMPTOMATIC DISEASES; CARRIER STATE; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; FORKHEAD TRANSCRIPTION FACTORS; HEPATITIS B; HEPATITIS B ANTIBODIES; HEPATITIS B CORE ANTIGENS; HEPATITIS B SURFACE ANTIGENS; HEPATITIS B VACCINES; HEPATITIS B VIRUS; HEPATOCYTES; IMMUNE TOLERANCE; IMMUNOTHERAPY; INTERFERON-GAMMA; INTERLEUKIN-12; LIVER; MALE; MICE; MICE, INBRED C57BL; VIRAL LOAD;

EID: 84885445313     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1203449     Document Type: Article

References (40)

1. Crispe, I. N. 2009. The liver as a lymphoid organ. Annu. Rev. Immunol. 27: 147-163.
2. Ganem, D., and A. M. Prince. 2004. Hepatitis B virus infection-natural history and clinical consequences. N. Engl. J. Med. 350: 1118-1129.
3. Chisari, F. V., M. Isogawa, and S. F. Wieland. 2010. Pathogenesis of hepatitis B virus infection. Pathol. Biol. (Paris) 58: 258-266.
4. Rehermann, B., and M. Nascimbeni. 2005. Immunology of hepatitis B virus and hepatitis C virus infection. Nat. Rev. Immunol. 5: 215-229.
5. Pol, S., and M. L. Michel. 2006. Therapeutic vaccination in chronic hepatitis B virus carriers. Expert Rev. Vaccines 5: 707-716.
6. Michel, M. L., and P. Tiollais. 2010. Hepatitis B vaccines: protective efficacy and therapeutic potential. Pathol. Biol. (Paris) 58: 288-295.
7. Dény, P., and F. Zoulim. 2010. Hepatitis B virus: from diagnosis to treatment. Pathol. Biol. (Paris) 58: 245-253.
8. Mancini, M., M. Hadchouel, P. Tiollais, C. Pourcel, and M. L. Michel. 1993. Induction of anti-hepatitis B surface antigen (HBsAg) antibodies in HBsAg producing transgenic mice: a possible way of circumventing " nonresponse" to HBsAg. J. Med. Virol. 39: 67-74.
9. Akbar, S. M., K. Kajino, K. Tanimoto, K. Kurose, T. Masumoto, K. Michitaka, N. Horiike, and M. Onji. 1997. Placebo-controlled trial of vaccination with hepatitis B virus surface antigen in hepatitis B virus transgenic mice. J. Hepatol. 26: 131-137.
10. Pol, S., B. Nalpas, F. Driss, M. L. Michel, P. Tiollais, J. Denis, and C. Brécho; Multicenter study group. 2001. Efficacy and limitations of a specific immunotherapy in chronic hepatitis B. J. Hepatol. 34: 917-921.
11. Dikici, B., M. Bosnak, H. Ucmak, A. Dagli, A. Ece, and K. Haspolat. 2003. Failure of therapeutic vaccination using hepatitis B surface antigen vaccine in the immunotolerant phase of children with chronic hepatitis B infection. J. Gastroenterol. Hepatol. 18: 218-222.
12. Huang, L. R., H. L. Wu, P. J. Chen, and D. S. Chen. 2006. An immunocompetent mouse model for the tolerance of human chronic hepatitis B virus infection. Proc. Natl. Acad. Sci. USA 103: 17862-17867.
13. Takehara, T., T. Suzuki, K. Ohkawa, A. Hosui, M. Jinushi, T. Miyagi, T. Tatsumi, Y. Kanazawa, and N. Hayashi. 2006. Viral covalently closed circular DNA in a non-transgenic mouse model for chronic hepatitis B virus replication. J. Hepatol. 44: 267-274.
14. Malanchère-Brès, E., P. J. Payette, M. Mancini, P. Tiollais, H. L. Davis, and M. L. Michel. 2001. CpG oligodeoxynucleotides with hepatitis B surface antigen (HBsAg) for vaccination in HBsAg-transgenic mice. J. Virol. 75: 6482-6491.
15. Vandepapelière, P., G. K. Lau, G. Leroux-Roels, Y. Horsmans, E. Gane, T. Tawandee, M. I. Merican, K. M. Win, C. Trepo, G. Cooksley, et al; Therapeutic HBV Vaccine Group of Investigators. 2007. Therapeutic vaccination of chronic hepatitis B patients with virus suppression by antiviral therapy: a randomized, controlled study of co-Administration of HBsAg/AS02 candidate vaccine and lamivudine. Vaccine 25: 8585-8597.
16. Trinchieri, G. 2003. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat. Rev. Immunol. 3: 133-146.
17. Beckebaum, S., V. R. Cicinnati, X. Zhang, S. Ferencik, A. Frilling, H. Grosse-Wilde, C. E. Broelsch, and G. Gerken. 2003. Hepatitis B virus-induced defect of monocyte-derived dendritic cells leads to impaired T helper type 1 response in vitro: mechanisms for viral immune escape. Immunology 109: 487-495.
18. Cavanaugh, V. J., L. G. Guidotti, and F. V. Chisari. 1997. Interleukin-12 inhibits hepatitis B virus replication in transgenic mice. J. Virol. 71: 3236-3243.
19. Carreño, V., S. Zeuzem, U. Hopf, P. Marcellin,W. G. Cooksley, J. Fevery,M. Diago, R. Reddy, M. Peters, K. Rittweger, et al. 2000. A phase I/II study of recombinant human interleukin-12 in patients with chronic hepatitis B. J. Hepatol. 32: 317-324.
20. Dong, Z., H. Wei, R. Sun, Z. Hu, B. Gao, and Z. Tian. 2004. Involvement of natural killer cells in PolyI:C-induced liver injury. J. Hepatol. 41: 966-973.
21. Nutt, S. L., and D. M. Tarlinton. 2011. Germinal center B and follicular helper T cells: siblings, cousins or just good friends? Nat. Immunol. 12: 472-477.
22. McDermott, D. S., and S. M. Varga. 2011. Quantifying antigen-specific CD4 T cells during a viral infection: CD4 T cell responses are larger than we think. J. Immunol. 187: 5568-5576.
23. Rai, D., N. L. Pham, J. T. Harty, and V. P. Badovinac. 2009. Tracking the total CD8 T cell response to infection reveals substantial discordance in magnitude and kinetics between inbred and outbred hosts. J. Immunol. 183: 7672-7681.
24. Kaech, S. M., E. J. Wherry, and R. Ahmed. 2002. Effector and memory T-cell differentiation: implications for vaccine development. Nat. Rev. Immunol. 2: 251-262.
25. Zhang, N., and M. J. Bevan. 2012. TGF-b signaling to T cells inhibits autoimmunity during lymphopenia-driven proliferation. Nat. Immunol. 13: 667-673.
26. Thornton, A. M., P. E. Korty, D. Q. Tran, E. A. Wohlfert, P. E. Murray, Y. Belkaid, and E. M. Shevach. 2010. Expression of Helios, an Ikaros transcription factor family member, differentiates thymic-derived from peripherally induced Foxp3+ T regulatory cells. J. Immunol. 184: 3433-3441.
27. Gottschalk, R. A., E. Corse, and J. P. Allison. 2012. Expression of Helios in peripherally induced Foxp3+ regulatory T cells. J. Immunol. 188: 976-980.
28. Guidotti, L. G., R. Rochford, J. Chung, M. Shapiro, R. Purcell, and F. V. Chisari. 1999. Viral clearance without destruction of infected cells during acute HBV infection. Science 284: 825-829.
29. Thimme, R., S. Wieland, C. Steiger, J. Ghrayeb, K. A. Reimann, R. H. Purcell, and F. V. Chisari. 2003. CD8(+) T cells mediate viral clearance and disease pathogenesis during acute hepatitis B virus infection. J. Virol. 77: 68-76.
30. Sette, A. D., C. Oseroff, J. Sidney, J. Alexander, R. W. Chesnut, K. Kakimi, L. G. Guidotti, and F. V. Chisari. 2001. Overcoming T cell tolerance to the hepatitis B virus surface antigen in hepatitis B virus-transgenic mice. J. Immunol. 166: 1389-1397.
31. Schirmbeck, R., N. Dikopoulos, M. Kwissa, F. Leithäuser, K. Lamberth, S. Buus, K. Melber, and J. Reimann. 2003. Breaking tolerance in hepatitis B surface antigen (HBsAg) transgenic mice by vaccination with cross-reactive, natural HBsAg variants. Eur. J. Immunol. 33: 3342-3352.
32. Tiegs, G., and A. W. Lohse. 2010. Immune tolerance: what is unique about the liver. J. Autoimmun. 34: 1-6.
33. Yang, S. H., C. G. Lee, S. H. Park, S. J. Im, Y. M. Kim, J. M. Son, J. S. Wang, S. K. Yoon, M. K. Song, A. Ambrozaitis, et al. 2006. Correlation of antiviral Tcell responses with suppression of viral rebound in chronic hepatitis B carriers: a proof-of-concept study. Gene Ther. 13: 1110-1117.
34. Crettaz, J., I. Otano, L. Ochoa-Callejero, A. Benito, A. Paneda, I. Aurrekoetxea, P. Berraondo, J. R. Rodríguez-Madoz, A. Astudillo, F. Kreppel, et al. 2009. Treatment of chronic viral hepatitis in woodchucks by prolonged intrahepatic expression of interleukin-12. [Published erratum appears in 2011 J Virol. 85: 13475.] J. Virol. 83: 2663-2674.
35. Stoop, J. N., R. G. van der Molen, C. C. Baan, L. J. van der Laan, E. J. Kuipers, J. G. Kusters, and H. L. Janssen. 2005. Regulatory T cells contribute to the impaired immune response in patients with chronic hepatitis B virus infection. Hepatology 41: 771-778.
36. Xu, D., J. Fu, L. Jin, H. Zhang, C. Zhou, Z. Zou, J. M. Zhao, B. Zhang, M. Shi, X. Ding, et al. 2006. Circulating and liver resident CD4+CD25+ regulatory T cells actively influence the antiviral immune response and disease progression in patients with hepatitis B. J. Immunol. 177: 739-747.
37. King, I. L., and B. M. Segal. 2005. Cutting edge: IL-12 induces CD4+CD25-T cell activation in the presence of T regulatory cells. J. Immunol. 175: 641-645.
38. Eto, D., C. Lao, D. DiToro, B. Barnett, T. C. Escobar, R. Kageyama, I. Yusuf, and S. Crotty. 2011. IL-21 and IL-6 are critical for different aspects of B cell immunity and redundantly induce optimal follicular helper CD4 T cell (Tfh) differentiation. PLoS ONE 6: e17739.
39. Harker, J. A., G. M. Lewis, L. Mack, and E. I. Zuniga. 2011. Late interleukin-6 escalates T follicular helper cell responses and controls a chronic viral infection. Science 334: 825-829.
40. Yang, Z. Z., D. M. Grote, S. C. Ziesmer, T. Niki, M. Hirashima, A. J. Novak, T. E. Witzig, and S. M. Ansell. 2012. IL-12 upregulates TIM-3 expression and induces T cell exhaustion in patients with follicular B cell non-Hodgkin lymphoma. J. Clin. Invest. 122: 1271-1282.