High-capacity adenoviral vectors circumvent the limitations of ΔE1 and ΔE1/ΔE3 adenovirus vectors to induce multispecific transgene product-directed CD8 T-cell responses

Journal of Gene Medicine

Volumn 13, Issue 12, 2011, Pages 648-657

  Kron, Matthias W ^a   Engler, Tatjana ^a   Schmidt, Erika ^a   Schirmbeck, Reinhold ^b   Kochanek, Stefan ^a   Kreppel, Florian ^a  

^a UNIVERSITY OF ULM   (Germany)

^b UNIVERSITY HOSPITAL ULM   (Germany)

Author keywords

Adenovirus; Genetic vaccination; Hepatitis B; High capacity; Multispecificity

Indexed keywords

ADENOVIRUS VECTOR; EPITOPE; GAMMA INTERFERON; GENE PRODUCT; HEPATITIS B SURFACE ANTIGEN; HEPATITIS B VACCINE;

ANIMAL CELL; ANTIBODY RESPONSE; ANTIBODY TITER; ANTIGEN EXPRESSION; ARTICLE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; GENE DELETION; GENETIC IMMUNIZATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRANSGENE;

ANIMALS; ANTIBODY SPECIFICITY; CD8-POSITIVE T-LYMPHOCYTES; GENE DELETION; GENETIC VECTORS; HEPATITIS B; HEPATITIS B SURFACE ANTIGENS; HEPATITIS B VACCINES; HEPATITIS B VIRUS; HUMANS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; T-LYMPHOCYTES, CYTOTOXIC; TRANSGENES; VACCINES, ADENOVIRUS;

EID: 84255178519     PISSN: 1099498X     EISSN: 15212254     Source Type: Journal    
DOI: 10.1002/jgm.1629     Document Type: Article

References (45)

1. Tatsis N, Ertl HC. Adenoviruses as vaccine vectors. Mol Ther 2004; 10: 616-629.
2. Lasaro MO, Ertl HC. New insights on adenovirus as vaccine vectors. Mol Ther 2009; 17: 1333-1339.
3. Jooss K, Yang Y, Fisher KJ, Wilson JM. Transduction of dendritic cells by DNA viral vectors directs the immune response to transgene products in muscle fibers. J Virol 1998; 72: 4212-4223.
4. De Geest BR, Van Linthout SA, Collen D. Humoral immune response in mice against a circulating antigen induced by adenoviral transfer is strictly dependent on expression in antigen-presenting cells. Blood 2003; 101: 2551-2556.
5. McKelvey T, Tang A, Bett AJ, Casimiro DR, Chastain M. T-cell response to adenovirus hexon and DNA-binding protein in mice. Gene Ther 2004; 11: 791-796.
6. Schirmbeck R, Reimann J, Kochanek S, Kreppel F. The immunogenicity of adenovirus vectors limits the multispecificity of CD8 T-cell responses to vector-encoded transgenic antigens. Mol Ther 2008; 16: 1609-1616.
7. Price DA, Goulder PJ, Klenerman P, et al. Positive selection of HIV-1 cytotoxic T lymphocyte escape variants during primary infection. Proc Natl Acad Sci USA 1997; 94: 1890-1895.
8. Locarnini SA, Yuen L. Molecular genesis of drug-resistant and vaccine-escape HBV mutants. Antivir Ther (Lond) 2010; 15: 451-461.
9. Riedl P, Wieland A, Lamberth K, et al. Elimination of immunodominant epitopes from multispecific DNA-based vaccines allows induction of CD8 T cells that have a striking antiviral potential. J Immunol 2009; 183: 370-380.
10. Ellis RW (ed). Hepatitis B Vaccines in Clinical Practice. Marcel-Dekker: New York, 1993.
11. Schirmbeck R, Wild J, Reimann J. Similar as well as distinct MHC class I-binding peptides are generated by exogenous and endogenous processing of hepatitis B virus surface antigen. Eur J Immunol 1998; 28: 4149-4161.
12. Schirmbeck R, Stober D, El Kholy S, Riedl P, Reimann J. The immunodominant, Ld-restricted T cell response to hepatitis B surface antigen (HBsAg) efficiently suppresses T cell priming to multiple Dd-, Kd-, and Kb-restricted HBsAg epitopes. J Immunol 2002; 168: 6253-6262.
13. Yewdell JW, Bennink JR. Immunodominance in major histocompatibility complex class I-restricted T lymphocyte responses. Annu Rev Immunol 1999; 17: 51-88.
14. Chen W, Antón LC, Bennink JR. Yewdell JW Dissecting the multifactorial causes of immunodominance in class I-restricted T cell responses to viruses. Immunity 2000; 12: 83-93.
15. Schiedner G, Morral N, Parks RJ, et al. Genomic DNA transfer with a high-capacity adenovirus vector results in improved in vivo gene expression and decreased toxicity. Nat Genet 1998; 18: 180-183.
16. Cerullo V, McCormack W, Seiler M, et al. Antigen-specific tolerance of human alpha1-antitrypsin induced by helper-dependent adenovirus. Hum Gene Ther 2007; 18: 1215-1224.
17. Jiang Z, Schiedner G, van Rooijen N, et al. Sustained muscle expression of dystrophin from a high-capacity adenoviral vector with systemic gene transfer of T cell costimulatory blockade. Mol Ther 2004; 10: 688-696.
18. Pastore L, Morral N, Zhou H, et al. Use of a liver-specific promoter reduces immune response to the transgene in adenoviral vectors. Hum Gene Ther 1999; 10: 1773-1781.
19. Schirmbeck R, Wild J, Stober D, et al. Ongoing murine T1 or T2 immune responses to the hepatitis B surface antigen are excluded from the liver that expresses transgene-encoded hepatitis B surface antigen. J Immunol 2000; 164: 4235-4243.
20. Schiedner G, Hertel S, Kochanek S. Efficient transformation of primary human amniocytes by E1 functions of Ad5: generation of new cell lines for adenoviral vector production. Hum Gene Ther 2000; 11: 2105-2116.
21. Palmer D, Ng P. Improved system for helper-dependent adenoviral vector production. Mol Ther 2003; 8: 846-852.
22. Dinser R, Kreppel F, Zaucke F, et al. Comparison of long-term transgene expression after non-viral and adenoviral gene transfer into primary articular chondrocytes. Histochem Cell Biol 2001; 116: 69-77.
23. Kreppel F, Kochanek S. Long-term transgene expression in proliferating cells mediated by episomally maintained high-capacity adenovirus vectors. J Virol 2004; 78: 9-22.
24. Kreppel F, Biermann V, Kochanek S, Schiedner GA. DNA-based method to assay total and infectious particle contents and helper virus contamination in high-capacity adenoviral vector preparations. Hum Gene Ther 2002; 13: 1151-1156.
25. Wortmann A, Vohringer S, Engler T, et al. Fully detargeted polyethylene glycol-coated adenovirus vectors are potent genetic vaccines and escape from pre-existing anti-adenovirus antibodies. Mol Ther 2008; 16: 154-162.
26. Casimiro DR, Chen L, Fu T-M, et al. Comparative immunogenicity in rhesus monkeys of DNA plasmid, recombinant vaccinia virus, and replication-defective adenovirus vectors expressing a human immunodeficiency virus type 1 gag gene. J Virol 2003; 77: 6305-6313.
27. Kaufman DR, Liu J, Carville A, et al. Trafficking of antigen-specific CD8+ T lymphocytes to mucosal surfaces following intramuscular vaccination. J Immunol 2008; 181: 4188-4198.
28. Santra S, Seaman MS, Xu L, et al. Replication-defective adenovirus serotype 5 vectors elicit durable cellular and humoral immune responses in nonhuman primates. J Virol 2005; 79: 6516-6522.
29. Reyes-Sandoval A, Sridhar S, Berthoud T, et al. Single-dose immunogenicity and protective efficacy of simian adenoviral vectors against Plasmodium berghei. Eur J Immunol 2008; 38: 732-741.
30. Wieland A, Riedl P, Reimann J, Schirmbeck R. Silencing an immunodominant epitope of hepatitis B surface antigen reveals an alternative repertoire of CD8 T cell epitopes of this viral antigen. Vaccine 2009; 28: 114-119.
31. Lichtenstein DL, Toth K, Doronin K, Tollefson AE, Wold WSM. Functions and mechanisms of action of the adenovirus E3 proteins. Int Rev Immunol 2004; 23: 75-111.
32. Rawle FC, Tollefson AE, Wold WS, Gooding LR. Mouse anti-adenovirus cytotoxic T lymphocytes. Inhibition of lysis by E3 gp19K but not E3 14.7K. J Immunol 1989; 143: 2031-2037.
33. Bergthaler A, Flatz L, Verschoor A, et al. Impaired antibody response causes persistence of prototypic T cell-contained virus. PLoS Biol 2009; 7: E1000080.
34. Weaver EA, Nehete PN, Buchl SS, et al. Comparison of replication-competent, first generation, and helper-dependent adenoviral vaccines. PLoS One 2009; 4: E5059, 2009.
35. Harui A, Roth MD, Kiertscher SM, Mitani K, Basak SK. Vaccination with helper-dependent adenovirus enhances the generation of transgene-specific CTL. Gene Ther 2004; 11: 1617-1626.
36. Y-hui F, J-sheng H, X-xian Z, et al. Intranasal vaccination with a helper-dependent adenoviral vector enhances transgene-specific immune responses in BALB/c mice. Biochem Biophys Res Commun 2010; 391: 857-861.
37. Weaver EA, Nehete PN, Nehete BP, et al. Protection against mucosal SHIV challenge by peptide and helper-dependent adenovirus vaccines. Viruses 2009; 1: 920.
38. Schweighardt B, Wrin T, Meiklejohn DA, et al. Immune escape mutations detected within HIV-1 epitopes associated with viral control during treatment interruption. J Acquir Immune Defic Syndr 2010; 53: 36-46.
39. Barouch DH, Kunstman J, Kuroda MJ, et al. Eventual AIDS vaccine failure in a rhesus monkey by viral escape from cytotoxic T lymphocytes. Nature 2002; 415: 335-339.
40. Prieur E, Gilbert SC, Schneider J, et al. A Plasmodium falciparum candidate vaccine based on a six-antigen polyprotein encoded by recombinant poxviruses. Proc Natl Acad Sci USA 2004; 101: 290-295.
41. Lin Y, Kwon T, Polo J, et al. Induction of broad CD4+ and CD8+ T-cell responses and cross-neutralizing antibodies against hepatitis C virus by vaccination with Th1-adjuvanted polypeptides followed by defective alphaviral particles expressing envelope glycoproteins gpE1 and gpE2 and nonstructural proteins 3, 4 and 5. J Virol 2008; 82: 7492-7503.
42. Vogel TU, Reynolds MR, Fuller DH, et al. Multispecific vaccine-induced mucosal cytotoxic T lymphocytes reduce acute-phase viral replication but fail in long-term control of simian immunodeficiency virus SIVmac239. J Virol 2003; 77: 13348-13360, 2003.
43. Casimiro DR, Cox K, Tang A, et al. Efficacy of multivalent adenovirus-based vaccine against simian immunodeficiency virus challenge. J Virol 2010; 84: 2996-3003.
44. Pal R, Venzon D, Letvin NL, et al. ALVAC-SIV-gag-pol-env-based vaccination and macaque major histocompatibility complex class I (A*01) delay simian immunodeficiency virus SIVmac-induced immunodeficiency. J Virol 2002; 76: 292-302.
45. Smith CL, Mirza F, Pasquetto V, et al. Immunodominance of poxviral-specific CTL in a human trial of recombinant-modified vaccinia Ankara. J Immunol 2005; 175: 8431-8437.