DNA Prime-adenovirus boost immunization induces a vigorous and multifunctional T-cell response against hepadnaviral proteins in the mouse and woodchuck model

Journal of Virology

Volumn 86, Issue 17, 2012, Pages 9297-9310

  Kosinska, Anna D ^a   Johrden, Lena ^b   Zhang, Ejuan ^a,c   Fiedler, Melanie ^a   Mayer, Anja ^a   Wildner, Oliver ^b,d   Lu, Mengji ^a   Roggendorf, Michael ^a  

^a UNIVERSITY HOSPITAL ESSEN   (Germany)

^b RUHR UNIVERSITY BOCHUM   (Germany)

^c WUHAN INSTITUTE OF VIROLOGY   (China)

^d PAUL EHRLICH INSTITUT   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS SEROTYPE 5 VECTOR; ADENOVIRUS VECTOR; CD3 ANTIGEN; DNA VACCINE; EPITOPE; GAMMA INTERFERON; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A ANTIBODY; INTERLEUKIN 2; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PLASMID DNA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; WOODCHUCK HEPATITIS B CORE ANTIGEN VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIGEN EXPRESSION; ANTIVIRAL ACTIVITY; ARTICLE; BOOST IMMUNIZATION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL PROLIFERATION; CELLULAR IMMUNITY; CHRONIC HEPATITIS; COMPUTER MODEL; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY TEST; DEGRANULATION; DNA IMMUNIZATION; DRUG CYTOTOXICITY; DRUG DOSAGE FORM COMPARISON; EMBRYO; FLOW CYTOMETRY; HEPATITIS B; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNIZATION; IN VITRO STUDY; IN VIVO STUDY; INFECTION CONTROL; INTRON; MALE; MOUSE; MULTICOLOR FLOW CYTOMETRY; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROCESS OPTIMIZATION; T LYMPHOCYTE; VIRUS LOAD; VIRUS REPLICATION; WOODCHUCK;

ADENOVIRIDAE; ANIMALS; CELLS, CULTURED; DISEASE MODELS, ANIMAL; FEMALE; HEPATITIS B; HEPATITIS B CORE ANTIGENS; HEPATITIS B VACCINES; HEPATITIS B VIRUS; HUMANS; IMMUNIZATION, SECONDARY; MARMOTA; MICE; MICE, INBRED C57BL; T-LYMPHOCYTES; VACCINES, DNA;

ADENOVIRIDAE; ANIMALIA; HEPATITIS B VIRUS; MARMOTA MONAX; MUS; WOODCHUCK HEPATITIS VIRUS;

EID: 84866169967     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00506-12     Document Type: Article

References (83)

1. +T cells is reflected by their avidity, polyfunctionality, and clonal turnover. J. Exp. Med. 204:2473-2485.
2. Barber DL, Wherry EJ, Ahmed R. 2003. Cutting edge: rapid in vivo killing by memory CD8 T cells. J. Immunol. 171:27-31.
3. Barouch DH, et al. 2001. Elicitation of high-frequency cytotoxic T-lymphocyte responses against both dominant and subdominant simianhuman immunodeficiency virus epitopes by DNA vaccination of rhesus monkeys. J. Virol. 75:2462-2467.
4. Bayer W, Schimmer S, Hoffmann D, Dittmer U, Wildner O. 2008. Evaluation of the Friend virus model for the development of improved adenovirus-vectored anti-retroviral vaccination strategies. Vaccine 26:716-726.
5. Bergelson JM. 1999. Receptors mediating adenovirus attachment and internalization. Biochem. Pharmacol. 57:975-979.
6. + T cells by a flow cytometric assay for degranulation. J. Immunol. Methods 281:65-78.
7. Betts MR, et al. 2005. Characterization of functional and phenotypic changes in anti-Gag vaccine-induced T cell responses and their role in protection after HIV-1 infection. Proc. Natl. Acad. Sci. U. S. A. 102:4512-4517.
8. + T cells. Blood 107:4781-4789.
9. Busch DH, Pamer EG. 1999. T cell affinity maturation by selective expansion during infection. J. Exp. Med. 189:701-710.
10. Casimiro DR, et al. 2003. Comparative immunogenicity in rhesus monkeys of DNA plasmid, recombinant vaccinia virus, and replicationdefective adenovirus vectors expressing a human immunodeficiency virus type 1 gag gene. J. Virol. 77:6305-6313.
11. Casimiro DR, et al. 2005. Attenuation of simian immunodeficiency virus SIVmac239 infection by prophylactic immunization with DNA and recombinant adenoviral vaccine vectors expressing Gag. J. Virol. 79:15547-15555.
12. Chisari FV, Ferrari C. 1995. Hepatitis B virus immunopathogenesis. Annu. Rev. Immunol. 13:29-60.
13. Cho HI, Celis E. 2012. Design of immunogenic and effective multiepitope DNA vaccines for melanoma. Cancer Immunol. Immunother. 61:343-351.
14. Cote PJ, et al. 1986. Protection of chimpanzees from type B hepatitis by immunization with woodchuck hepatitis virus surface antigen. J. Virol. 60:895-901.
15. Couillin I, et al. 1999. Specific vaccine therapy in chronic hepatitis B: induction of T cell proliferative responses specific for envelope antigens. J. Infect. Dis. 180:15-26.
16. Dahmen A, Herzog-Hauff S, Bocher WO, Galle PR, Lohr HF. 2002. Clinical and immunological efficacy of intradermal vaccine plus lamivudine with or without interleukin-2 in patients with chronic hepatitis B. J. Med. Virol. 66:452-460.
17. Darrah PA, et al. 2007. Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat. Med. 13:843-850.
18. Das A, et al. 2008. Functional skewing of the global CD8 T cell population in chronic hepatitis B virus infection. J. Exp. Med. 205:2111-2124.
19. + T cells and reduces chronic retroviral set points. Proc. Natl. Acad. Sci. U. S. A. 108:2420-2425.
20. Dikici B, et al. 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.
21. Falk K, Rotzschke O, Stevanovic S, Jung G, Rammensee HG. 1991. Allele-specific motifs revealed by sequencing of self-peptides eluted from MHC molecules. Nature 351:290-296.
22. Ferrari C, et al. 1990. Cellular immune response to hepatitis B virusencoded antigens in acute and chronic hepatitis B virus infection. J. Immunol. 145:3442-3449.
23. Fiedler M, Lu M, Siegel F, Whipple J, Roggendorf M. 2001. Immunization of woodchucks (Marmota monax) with hepatitis delta virus DNA vaccine. Vaccine 19:4618-4626.
24. Fitzgerald JC, et al. 2003. A simian replication-defective adenoviral recombinant vaccine to HIV-1 Gag. J. Immunol. 170:1416-1422.
25. Flatz L, et al. 2011. Single-cell gene-expression profiling reveals qualitatively distinct CD8 T cells elicited by different gene-based vaccines. Proc. Natl. Acad. Sci. U. S. A. 108:5724-5729.
26. Frank I, et al. 2007. Acute resolving woodchuck hepatitis virus (WHV) infection is associated with a strong cytotoxic T-lymphocyte response to a single WHV core peptide. J. Virol. 81:7156-7163.
27. Fujiwara T. 2011. A novel molecular therapy using bioengineered adenovirus for human gastrointestinal cancer. Acta Med. Okayama 65:151-162.
28. a T-cell epitopes. J. Virol. 80:4717-4728.
29. Guidotti LG, et al. 1999. Viral clearance without destruction of infected cells during acute HBV infection. Science 284:825-829.
30. Guzelbulut F, et al. 2012. Comparison of the efficacy of entecavir and tenofovir in chronic hepatitis B. Hepatogastroenterology 59:477-480.
31. Harari A, et al. 2008. An HIV-1 clade C DNA prime, NYVAC boost vaccine regimen induces reliable, polyfunctional, and long-lasting T cell responses. J. Exp. Med. 205:63-77.
32. Hermening S, Kugler S, Bahr M, Isenmann S. 2004. Increased protein expression from adenoviral shuttle plasmids and vectors by insertion of a small chimeric intron sequence. J. Virol. Methods 122:73-77.
33. Hervas-Stubbs S, et al. 1997. Therapeutic vaccination of woodchucks against chronic woodchuck hepatitis virus infection. J. Hepatol. 27:726-737.
34. Hervas-Stubbs S, et al. 2001. T-helper cell response to woodchuck hepatitis virus antigens after therapeutic vaccination of chronically-infected animals treated with lamivudine. J. Hepatol. 35:105-111.
35. Hoofnagle JH. 1981. Serologic markers of hepatitis B virus infection. Annu. Rev. Med. 32:1-11.
36. Horiike N, et al. 2005. In vivo immunization by vaccine therapy following virus suppression by lamivudine: a novel approach for treating patients with chronic hepatitis B. J. Clin. Virol. 32:156-161.
37. + T-cell proliferative response in chronic hepatitis B carriers. Vaccine 20:3598-3612.
38. Jung MC, et al. 1991. Hepatitis B virus antigen-specific T-cell activation in patients with acute and chronic hepatitis B. J. Hepatol. 13:310-317.
39. Kwak MS, et al. 2011. Long-term efficacy of entecavir therapy in chronic hepatitis B patients with antiviral resistance to lamivudine and adefovir. J. Viral Hepat. 18:e432-e438. doi:10.1111/j.1365-2893.2011.01461.x.
40. Li HW, Gao YX, Raizada MK, Sumners C. 2005. Intronic enhancement of angiotensin II type 2 receptor transgene expression in vitro and in vivo. Biochem. Biophys. Res. Commun. 336:29-35.
41. Lu M, et al. 1999. Immunization of woodchucks with plasmids expressing woodchuck hepatitis virus (WHV) core antigen and surface antigen suppresses WHV infection. J. Virol. 73:281-289.
42. Lu M, Isogawa M, Xu Y, Hilken G. 2005. Immunization with the gene expressing woodchuck hepatitis virus nucleocapsid protein fused to cytotoxic-T-lymphocyte-associated antigen 4 leads to enhanced specific immune responses in mice and woodchucks. J. Virol. 79:6368-6376.
43. Lu M, et al. 2003. Induction of antibodies to the PreS region of surface antigens of woodchuck hepatitis virus (WHV) in chronic carrier woodchucks by immunizations withWHVsurface antigens. J. Hepatol. 39:405-413.
44. Lu M, et al. 2008. Combination of an antiviral drug and immunomodulation against hepadnaviral infection in the woodchuck model. J. Virol. 82:2598-2603.
45. + cells in liver damage and viral control during persistent hepatitis B virus infection. J. Exp. Med. 191:1269-1280.
46. Mancini-Bourgine M, et al. 2004. Induction or expansion of T-cell responses by a hepatitis B DNA vaccine administered to chronic HBV carriers. Hepatology 40:874-882.
47. Menne S, et al. 2002. Immunogenic effects of woodchuck hepatitis virus surface antigen vaccine in combination with antiviral therapy: breaking of humoral and cellular immune tolerance in chronic woodchuck hepatitis virus infection. Intervirology 45:237-250.
48. Milich DR, McLachlan A, Thornton GB, Hughes JL. 1987. Antibody production to the nucleocapsid and envelope of the hepatitis B virus primed by a single synthetic T cell site. Nature 329:547-549.
49. Parker KC, Bednarek MA, Coligan JE. 1994. Scheme for ranking potential HLA-A2 binding peptides based on independent binding of individual peptide side-chains. J. Immunol. 152:163-175.
50. Penna A, et al. 1996. Long-lasting memory T cell responses following self-limited acute hepatitis B. J. Clin. Invest. 98:1185-1194.
51. Penna A, 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.
52. Penna A, et al. 1997. Predominant T-helper 1 cytokine profile of hepatitis B virus nucleocapsid-specific T cells in acute self-limited hepatitis B. Hepatology 25:1022-1027.
53. Pesonen S, Kangasniemi L, Hemminki A. 2011. Oncolytic adenoviruses for the treatment of human cancer: focus on translational and clinical data. Mol. Pharm. 8:12-28.
54. Petersen J, et al. 2012. Entecavir plus tenofovir combination as rescue therapy in pre-treated chronic hepatitis B patients: an international multicenter cohort study. J. Hepatol. 56:520-526.
55. Piccolo P, et al. 2009. A randomized controlled trial of pegylated interferon-alpha2a plus adefovir dipivoxil for hepatitis B e antigen-negative chronic hepatitis B. Antivir. Ther. 14:1165-1174.
56. Pol S, et al. 1994. Specific vaccine therapy in chronic hepatitis B infection. Lancet 344:342.
57. Pol S, et al. 2001. Efficacy and limitations of a specific immunotherapy in chronic hepatitis B. J. Hepatol. 34:917-921.
58. + T cell responses. J. Exp. Med. 204:1405-1416.
59. Prud'homme GJ. 2005. DNA vaccination against tumors. J. Gene Med. 7:3-17.
60. Rammensee H, Bachmann J, Emmerich NP, Bachor OA, Stevanovic S. 1999. SYFPEITHI: database for MHC ligands and peptide motifs. Immunogenetics 50:213-219.
61. Ratnam D, et al. 2011. The efficacy and tolerability of pegylated interferon-alpha-2a in chronic hepatitis B: a multicenter clinical experience. J. Gastroenterol. Hepatol. [Epub ahead of print.] doi: 10.1111/j.1440-1746.2011.07051.x.
62. Rehermann B, Nascimbeni M. 2005. Immunology of hepatitis B virus and hepatitis C virus infection. Nat. Rev. Immunol. 5:215-229.
63. Ren F, et al. 2003. Cytokine-dependent anti-viral role of CD4-positive T cells in therapeutic vaccination against chronic hepatitis B viral infection. J. Med. Virol. 71:376-384.
64. Richardson JS, et al. 2009. Enhanced protection against Ebola virus mediated by an improved adenovirus-based vaccine. PLoS One 4:e5308. doi: 10.1371/journal.pone.0005308.
65. Roggendorf M, Tolle TK. 1995. The woodchuck: an animal model for hepatitis B virus infection in man. Intervirology 38:100-112.
66. Rubio V, et al. 2003. Ex vivo identification, isolation and analysis of tumor-cytolytic T cells. Nat. Med. 9:1377-1382.
67. Safadi R, et al. 2003. Treatment of chronic hepatitis B virus infection via oral immune regulation toward hepatitis B virus proteins. Am. J. Gastroenterol. 98:2505-2515.
68. Sakurai F, Kawabata K, Yamaguchi T, Hayakawa T, Mizuguchi H. 2005. Optimization of adenovirus serotype 35 vectors for efficient transduction in human hematopoietic progenitors: comparison of promoter activities. Gene Ther. 12:1424-1433.
69. Schlereth B, Germann PG, ter Meulen V, Niewiesk S. 2000. DNA vaccination with both the haemagglutinin and fusion proteins but not the nucleocapsid protein protects against experimental measles virus infection. J. Gen. Virol. 81:1321-1325.
70. Shiver JW, et al. 2002. Replication-incompetent adenoviral vaccine vector elicits effective anti-immunodeficiency virus immunity. Nature 415: 331-335.
71. Siegel F, Lu M, Roggendorf M. 2001. Coadministration of gamma interferon with DNA vaccine expressing woodchuck hepatitis virus (WHV) core antigen enhances the specific immune response and protects against WHV infection. J. Virol. 75:5036-5042.
72. Sullivan NJ, et al. 2006. Immune protection of nonhuman primates against Ebola virus with single low-dose adenovirus vectors encoding modified GPs. PLoS Med. 3:e177. doi:10.1371/journal.pmed.0030177.
73. Sullivan NJ, Sanchez A, Rollin PE, Yang ZY, Nabel GJ. 2000. Development of a preventive vaccine for Ebola virus infection in primates. Nature 408:605-609.
74. + T cells mediate viral clearance and disease pathogenesis during acute hepatitis B virus infection. J. Virol. 77:68-76.
75. Vandepapeliere P, et al. 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.
76. Wang J, Gujar SA, Cova L, Michalak TI. 2007. Bicistronic woodchuck hepatitis virus core and gamma interferon DNA vaccine can protect from hepatitis but does not elicit sterilizing antiviral immunity. J. Virol. 81:903-916.
77. Wu L, Kong WP, Nabel GJ. 2005. Enhanced breadth of CD4 T-cell immunity by DNA prime and adenovirus boost immunization to human immunodeficiency virus Env and Gag immunogens. J. Virol. 79:8024-8031.
78. Yalcin K, Acar M, Degertekin H. 2003. Specific hepatitis B vaccine therapy in inactive HBsAg carriers: a randomized controlled trial. Infection 31:221-225.
79. Yang PL, et al. 2010. Immune effectors required for hepatitis B virus clearance. Proc. Natl. Acad. Sci. U. S. A. 107:798-802.
80. Yang ZY, et al. 2003. Overcoming immunity to a viral vaccine by DNA priming before vector boosting. J. Virol. 77:799-803.
81. Zakhartchouk AN, Viswanathan S, Mahony JB, Gauldie J, Babiuk LA. 2005. Severe acute respiratory syndrome coronavirus nucleocapsid protein expressed by an adenovirus vector is phosphorylated and immunogenic in mice. J. Gen. Virol. 86:211-215.
82. Zelinskyy G, Dietze K, Sparwasser T, Dittmer U. 2009. Regulatory T cells suppress antiviral immune responses and increase viral loads during acute infection with a lymphotropic retrovirus. PLoS Pathog. 5:e1000406. doi:10.1371/journal.ppat.1000406.
83. Zimmerli SC, et al. 2005. HIV-1-specific IFN-gamma/IL-2-secreting CD8 T cells support CD4-independent proliferation of HIV-1-specific CD8 T cells. Proc. Natl. Acad. Sci. U. S. A. 102:7239-7244.