Functional aspects of intrahepatic hepatitis B virus-specific T cells induced by therapeutic DNA vaccination

Molecular Therapy

Volumn 23, Issue 3, 2015, Pages 578-590

  Brass, Anette ^a   Frelin, Lars ^a   Milich, David R ^b   Sällberg, Matti ^a   Ahlén, Gustaf ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b Vaccine Research Institute of San Diego   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA VACCINE; HEPATITIS B CORE ANTIGEN; HEPATITIS B(E) ANTIGEN; INTERLEUKIN 12; HEPATITIS B ANTIBODY; HEPATITIS B VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY BLOOD LEVEL; ANTIGEN SPECIFICITY; ARTICLE; B LYMPHOCYTE; CELL EXPANSION; CODON; CONTROLLED STUDY; DNA IMMUNIZATION; DRUG DELIVERY SYSTEM; HBCAG GENE; HEPATITIS B VIRUS; IMMUNE RESPONSE; IMMUNOGENICITY; IN VIVO ELECTROPORATION; IN VIVO INTRACELLULAR INJECTION; LIVER; LIVER CELL; LONGEVITY; LYMPHOCYTE FUNCTION; MOUSE; NONHUMAN; PLASMID; T LYMPHOCYTE; TH1 TH2 BALANCE; TRANSGENIC MOUSE; ANIMAL; BIOSYNTHESIS; CELL PROLIFERATION; CHEMISTRY; ELECTROPORATION; GENE EXPRESSION; GENETICS; HEPATITIS B, CHRONIC; HUMAN; IMMUNOLOGY; METABOLISM; VACCINATION; VIROLOGY;

HEPATITIS B VIRUS; MUS MUSCULUS;

ANIMALS; CELL PROLIFERATION; ELECTROPORATION; GENE EXPRESSION; HEPATITIS B ANTIBODIES; HEPATITIS B CORE ANTIGENS; HEPATITIS B E ANTIGENS; HEPATITIS B VACCINES; HEPATITIS B VIRUS; HEPATITIS B, CHRONIC; HEPATOCYTES; HUMANS; INTERLEUKIN-12; LIVER; MICE; MICE, TRANSGENIC; PLASMIDS; T-LYMPHOCYTES; VACCINATION; VACCINES, DNA;

EID: 84924062740     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2014.233     Document Type: Article

References (46)

1. Lok, AS (2013). Hepatitis: Long-term therapy of chronic hepatitis B reverses cirrhosis. Nat Rev Gastroenterol Hepatol 10: 199-200.
2. Hosaka, T, Suzuki, F, Kobayashi, M, Seko, Y, Kawamura, Y, Sezaki, H et al. (2013). Long-term entecavir treatment reduces hepatocellular carcinoma incidence in patients with hepatitis B virus infection. Hepatology 58: 98-107.
3. Zoulim, F and Locarnini, S (2009). Hepatitis B virus resistance to nucleos(t)ide analogues. Gastroenterology 137: 1593-608.e1.
4. Whalley, SA, Murray, JM, Brown, D, Webster, GJ, Emery, VC, Dusheiko, GM et al. (2001). Kinetics of acute hepatitis B virus infection in humans. J Exp Med 193: 847-854.
5. Webster, GJ, Reignat, S, Maini, MK, Whalley, SA, Ogg, GS, King, A et al. (2000). Incubation phase of acute hepatitis B in man: dynamic of cellular immune mechanisms. Hepatology 32: 1117-1124.
6. Maini, MK, Boni, C, Lee, CK, Larrubia, JR, Reignat, S, Ogg, GS et al. (2000). The role of virus-specific CD8(+) cells in liver damage and viral control during persistent hepatitis B virus infection. J Exp Med 191: 1269-1280.
7. Marinos, G, Torre, F, Chokshi, S, Hussain, M, Clarke, BE, Rowlands, DJ et al. (1995). Induction of T-helper cell response to hepatitis B core antigen in chronic hepatitis B: a major factor in activation of the host immune response to the hepatitis B virus. Hepatology 22(4 Pt 1): 1040-1049.
8. Löhr, HF, Weber, W, Schlaak, J, Goergen, B, Meyer zum Buschenfelde, KH and Gerken, G (1995). Proliferative response of CD4+ T cells and hepatitis B virus clearance in chronic hepatitis with or without hepatitis B e-minus hepatitis B virus mutants. Hepatology 22: 61-68.
9. Penna, A, Chisari, FV, Bertoletti, A, Missale, G, Fowler, P, Giuberti, T et al. (1991). Cytotoxic T lymphocytes recognize an HLA-A2-restricted epitope within the hepatitis B virus nucleocapsid antigen. J Exp Med 174: 1565-1570.
10. Boni, C, Bertoletti, A, Penna, A, Cavalli, A, Pilli, M, Urbani, S et al. (1998). Lamivudine treatment can restore T cell responsiveness in chronic hepatitis B. J Clin Invest 102: 968-975.
11. Boni, C, Laccabue, D, Lampertico, P, Giuberti, T, Viganò, M, Schivazappa, S et al. (2012). Restored function of HBV-specific T cells after long-term effective therapy with nucleos(t)ide analogues. Gastroenterology 143: 963-73.e9.
12. Gish, R, Jia, JD, Locarnini, S and Zoulim, F (2012). Selection of chronic hepatitis B therapy with high barrier to resistance. Lancet Infect Dis 12: 341-353.
13. Tavis, JE, Gehring, AJ and Hu, Y (2013). How further suppression of virus replication could improve current HBV treatment. Expert Rev Anti Infect Ther 11: 755-757.
14. Mancini-Bourgine, M, Fontaine, H, Scott-Algara, D, Pol, S, Bréchot, C and Michel, ML (2004). Induction or expansion of T-cell responses by a hepatitis B DNA vaccine administered to chronic HBV carriers. Hepatology 40: 874-882.
15. Scott-Algara, D, Mancini-Bourgine, M, Fontaine, H, Pol, S and Michel, ML (2010). Changes to the natural killer cell repertoire after therapeutic hepatitis B DNA vaccination. PLoS One 5: e8761.
16. Habersetzer, F, Honnet, G, Bain, C, Maynard-Muet, M, Leroy, V, Zarski, JP et al. (2011). A poxvirus vaccine is safe, induces T-cell responses, and decreases viral load in patients with chronic hepatitis C. Gastroenterology 141: 890-899.e1.
17. Weiland, O, Ahlén, G, Diepolder, H, Jung, MC, Levander, S, Fons, M et al. (2013). Therapeutic DNA vaccination using in vivo electroporation followed by standard of care therapy in patients with genotype 1 chronic hepatitis C. Mol Ther 21: 1796-1805.
18. Godon, O, Fontaine, H, Kahi, S, Meritet, J, Scott-Algara, D, Pol, S et al. (2014). Immunological and antiviral responses after therapeutic DNA immunization in chronic hepatitis B patients efficiently treated by analogues. Mol Ther 22: 675-684.
19. Boni, C, Fisicaro, P, Valdatta, C, Amadei, B, Di Vincenzo, P, Giuberti, T et al. (2007). Characterization of hepatitis B virus (HBV)-specific T-cell dysfunction in chronic HBV infection. J Virol 81: 4215-4225.
20. Thimme, R, Wieland, S, Steiger, C, Ghrayeb, J, Reimann, KA, Purcell, RH et al. (2003). CD8(+) T cells mediate viral clearance and disease pathogenesis during acute hepatitis B virus infection. J Virol 77: 68-76.
21. Webster, GJ, Reignat, S, Brown, D, Ogg, GS, Jones, L, Seneviratne, SL et al. (2004). Longitudinal analysis of CD8+ T cells specific for structural and nonstructural hepatitis B virus proteins in patients with chronic hepatitis B: implications for immunotherapy. J Virol 78: 5707-5719.
22. Seder, RA, Darrah, PA and Roederer, M (2008). T-cell quality in memory and protection: implications for vaccine design. Nat Rev Immunol 8: 247-258.
23. Badr, G, Bédard, N, Abdel-Hakeem, MS, Trautmann, L, Willems, B, Villeneuve, JP et al. (2008). Early interferon therapy for hepatitis C virus infection rescues polyfunctional, long-lived CD8+ memory T cells. J Virol 82: 10017-10031.
24. Nyström, J, Chen, A, Frelin, L, Ahlén, G, Koh, S, Brass, A et al. (2010). Improving on the ability of endogenous hepatitis B core antigen to prime cytotoxic T lymphocytes. J Infect Dis 201: 1867-1879.
25. Chen, A, Ahlén, G, Brenndörfer, ED, Brass, A, Holmström, F, Chen, M et al. (2011). Heterologous T cells can help restore function in dysfunctional hepatitis C virus nonstructural 3/4A-specific T cells during therapeutic vaccination. J Immunol 186: 5107-5118.
26. Milich, DR, Jones, JE, Hughes, JL, Price, J, Raney, AK and McLachlan, A (1990). Is a function of the secreted hepatitis B e antigen to induce immunologic tolerance in utero? Proc Natl Acad Sci USA 87: 6599-6603.
27. Milich, DR, McLachlan, A, Raney, AK, Houghten, R, Thornton, GB, Maruyama, T et al. (1991). Autoantibody production in hepatitis B e antigen transgenic mice elicited with a self T-cell peptide and inhibited with nonself peptides. Proc Natl Acad Sci USA 88: 4348-4352.
28. Milich, DR, Schödel, F, Peterson, DL, Jones, JE and Hughes, JL (1995). Characterization of self-reactive T cells that evade tolerance in hepatitis B e antigen transgenic mice. Eur J Immunol 25: 1663-1672.
29. Rossol, S, Marinos, G, Carucci, P, Singer, MV, Williams, R and Naoumov, NV (1997). Interleukin-12 induction of Th1 cytokines is important for viral clearance in chronic hepatitis B. J Clin Invest 99: 3025-3033.
30. Kim, JJ, Ayyavoo, V, Bagarazzi, ML, Chattergoon, MA, Dang, K, Wang, B et al. (1997). In vivo engineering of a cellular immune response by coadministration of IL-12 expression vector with a DNA immunogen. J Immunol 158: 816-826.
31. Ahlen, G, Nystrom, J, Pult, I, Frelin, L, Hultgren, C and Sallberg, M (2005). In vivo clearance of hepatitis C virus nonstructural 3/4A-expressing hepatocytes by DNA vaccine-primed cytotoxic T lymphocytes. J Infect Dis 192: 2112-2116.
32. Lazdina, U, Alheim, M, Nyström, J, Hultgren, C, Borisova, G, Sominskaya, I et al. (2003). Priming of cytotoxic T cell responses to exogenous hepatitis B virus core antigen is B cell dependent. J Gen Virol 84(Pt 1): 139-146.
33. Kuhöber, A, Pudollek, HP, Reifenberg, K, Chisari, FV, Schlicht, HJ, Reimann, J et al. (1996). DNA immunization induces antibody and cytotoxic T cell responses to hepatitis B core antigen in H-2b mice. J Immunol 156: 3687-3695.
34. Milich, DR, Peterson, DL, Schödel, F, Jones, JE and Hughes, JL (1995). Preferential recognition of hepatitis B nucleocapsid antigens by Th1 or Th2 cells is epitope and major histocompatibility complex dependent. J Virol 69: 2776-2785.
35. Milich, DR, Schödel, F, Hughes, JL, Jones, JE and Peterson, DL (1997). The hepatitis B virus core and e antigens elicit different Th cell subsets: antigen structure can affect Th cell phenotype. J Virol 71: 2192-2201.
36. Frelin, L, Wahlström, T, Tucker, AE, Jones, J, Hughes, J, Lee, BO et al. (2009). A mechanism to explain the selection of the hepatitis e antigen-negative mutant during chronic hepatitis B virus infection. J Virol 83: 1379-1392.
37. Obeng-Adjei, N, Choo, DK, Saini, J, Yan, J, Pankhong, P, Parikh, A et al. (2012). Synthetic DNA immunogen encoding hepatitis B core antigen drives immune response in liver. Cancer Gene Ther 19: 779-787.
38. Chong, SY, Egan, MA, Kutzler, MA, Megati, S, Masood, A, Roopchard, V et al. (2007). Comparative ability of plasmid IL-12 and IL-15 to enhance cellular and humoral immune responses elicited by a SIVgag plasmid DNA vaccine and alter disease progression following SHIV(89.6P) challenge in rhesus macaques. Vaccine 25: 4967-4982.
39. Kalams, SA, Parker, S, Jin, X, Elizaga, M, Metch, B, Wang, M et al.; NIAID HIV Vaccine Trials Network. (2012). Safety and immunogenicity of an HIV-1 gag DNA vaccine with or without IL-12 and/or IL-15 plasmid cytokine adjuvant in healthy, HIV-1 uninfected adults. PLoS One 7: e29231.
40. Babiuk, S, Baca-Estrada, ME, Foldvari, M, Middleton, DM, Rabussay, D, Widera, G et al. (2004). Increased gene expression and inflammatory cell infiltration caused by electroporation are both important for improving the efficacy of DNA vaccines. J Biotechnol 110: 1-10.
41. Ahlén, G, Söderholm, J, Tjelle, T, Kjeken, R, Frelin, L, Höglund, U et al. (2007). In vivo electroporation enhances the immunogenicity of hepatitis C virus nonstructural 3/4A DNA by increased local DNA uptake, protein expression, inflammation, and infiltration of CD3+ T cells. J Immunol 179: 4741-4753.
42. Kosinska, AD, Zhang, E, Johrden, L, Liu, J, Seiz, PL, Zhang, X et al. (2013). Combination of DNA prime-adenovirus boost immunization with entecavir elicits sustained control of chronic hepatitis B in the woodchuck model. PLoS Pathog 9: e1003391.
43. Chen, H, Chuai, X, Deng, Y, Wen, B, Wang, W, Xiong, S et al. (2012). Optimisation of prime-boost immunization in mice using novel protein-based and recombinant vaccinia (Tiantan)-based HBV vaccine. PLoS One 7: e43730.
44. Milich, DR, Chen, M, Schödel, F, Peterson, DL, Jones, JE and Hughes, JL (1997). Role of B cells in antigen presentation of the hepatitis B core. Proc Natl Acad Sci USA 94: 14648-14653.
45. Sällberg, M, Rudén, U, Magnius, LO, Norrby, E and Wahren, B (1991). Rapid "tea-bag" peptide synthesis using 9-fluorenylmethoxycarbonyl (Fmoc) protected amino acids applied for antigenic mapping of viral proteins. Immunol Lett 30: 59-68.
46. Ahlén, G, Holmström, F, Gibbs, A, Alheim, M and Frelin, L (2014). Long-term functional duration of immune responses to HCV NS3/4A induced by DNA vaccination. Gene Ther 21: 739-750.