Removal of vaccinia virus genes that block interferon type I and II pathways improves adaptive and memory responses of the HIV/AIDS vaccine candidate NYVAC-C in mice

Journal of Virology

Volumn 86, Issue 9, 2012, Pages 5026-5038

  Gómez, Carmen Elena ^a   Perdiguero, Beatriz ^a   Nájera, Jose Luis ^a   Sorzano, Carlos Oscar S ^a   Jiménez, Victoria ^a   González Sanz, Rubén ^a   Esteban, Mariano ^a  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

GAG PROTEIN; GAMMA INTERFERON; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; HUMAN IMMUNODEFICIENCY VIRUS ANTIGEN; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; INTERFERON; NEF PROTEIN; POL PROTEIN; VIRUS ENVELOPE PROTEIN;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B19 GENE; B8 GENE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; GENE DELETION; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMORAL IMMUNITY; IMMUNOGENICITY; IMMUNOLOGICAL MEMORY; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; VACCINIA VIRUS; VIRUS GENE;

ADAPTIVE IMMUNITY; AIDS VACCINES; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CHICK EMBRYO; GENE DELETION; GENETIC VECTORS; HAPLORHINI; HIV ENVELOPE PROTEIN GP120; HIV INFECTIONS; HIV-1; IMMUNOLOGIC MEMORY; INTERFERON TYPE I; INTERFERON-GAMMA; MICE; MICE, INBRED BALB C; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; VACCINIA VIRUS;

HUMAN IMMUNODEFICIENCY VIRUS 1; MUS; POXVIRIDAE; VACCINIA VIRUS;

EID: 84861304314     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.06684-11     Document Type: Article

References (56)

1. Aguet M, Dembic Z, Merlin G. 1988. Molecular cloning and expression of the human interferon-gamma receptor. Cell 55:273-280.
2. Alcami A, Smith GL. 2002. The vaccinia virus soluble interferon-gamma receptor is a homodimer. J. Gen. Virol. 83:545-549.
3. Alcami A, Smith GL. 1995. Vaccinia, cowpox, and camelpox viruses encode soluble gamma interferon receptors with novel broad species specificity. J. Virol. 69:4633-4639.
4. Alcami A, Symons JA, Smith GL. 2000. The vaccinia virus soluble alpha/beta interferon (IFN) receptor binds to the cell surface and protects cells from the antiviral effects of IFN. J. Virol. 74:11230-11239.
5. Antoine G, Scheiflinger F, Dorner F, Falkner FG. 1998. The complete genomic sequence of the modified vaccinia Ankara strain: comparison with other orthopoxviruses. Virology 244:365-396.
6. Bart PA, et al. 2008. EV01: a phase I trial in healthy HIV negative volunteers to evaluate a clade C HIV vaccine, NYVAC-C undertaken by the EuroVacc Consortium. Vaccine 26:3153-3161.
7. Blanchard TJ, Alcami A, Andrea P, Smith GL. 1998. Modified vaccinia virus Ankara undergoes limited replication in human cells and lacks several immunomodulatory proteins: implications for use as a human vaccine. J. Gen. Virol. 79:1159-1167.
8. Clark RH, Kenyon JC, Bartlett NW, Tscharke DC, Smith GL. 2006. Deletion of gene A41L enhances vaccinia virus immunogenicity and vaccine efficacy. J. Gen. Virol. 87:29-38.
9. Colamonici OR, Domanski P, Sweitzer SM, Larner A, Buller RM. 1995. Vaccinia virus B18R gene encodes a type I interferon-binding protein that blocks interferon alpha transmembrane signaling. J. Biol. Chem. 270: 15974-15978.
10. Cottingham MG, et al. 2008. Recombination-mediated genetic engineering of a bacterial artificial chromosome clone of modified vaccinia virus Ankara (MVA). PLoS One 3:e1638.
11. Curtsinger JM, Valenzuela JO, Agarwal P, Lins D, Mescher MF. 2005. Type I IFNs provide a third signal to CD8 T cells to stimulate clonal expansion and differentiation. J. Immunol. 174:4465-4469.
12. Denes B, et al. 2006. Attenuation of a vaccine strain of vaccinia virus via inactivation of interferon viroceptor. J. Gene Med. 8:814-823.
13. Deonarain R, et al. 2000. Impaired antiviral response and alpha/beta interferon induction in mice lacking beta interferon. J. Virol. 74:3404-3409.
14. Flynn BJ, et al. 2011. Immunization with HIV Gag targeted to dendritic cells followed by recombinant New York vaccinia virus induces robust T-cell immunity in nonhuman primates. Proc. Natl. Acad. Sci. U. S. A. 108:7131-7136.
15. Garcia-Arriaza J, Najera JL, Gomez CE, Sorzano CO, Esteban M. 2010. Immunogenic profiling in mice of a HIV/AIDS vaccine candidate (MVA-B) expressing four HIV-1 antigens and potentiation by specific gene deletions. PLoS One 5:e12395.
16. Garcia-Arriaza J, et al. 2011. A candidate HIV/AIDS vaccine (MVA-B) lacking vaccinia virus gene C6L enhances memory HIV-1-specific T-cell responses. PLoS One 6:e24244.
17. Gomez CE, et al. 2007. Generation and immunogenicity of novel HIV/AIDS vaccine candidates targeting HIV-1 Env/Gag-Pol-Nef antigens of clade C. Vaccine 25:1969-1992.
18. Gomez CE, Najera JL, Krupa M, Perdiguero B, Esteban M. 2011. MVA and NYVAC as vaccines against emergent infectious diseases and cancer. Curr. Gene Ther. 11:189-217.
19. Hansen SG, et al. 2011. Profound early control of highly pathogenic SIV by an effector memory T-cell vaccine. Nature 473:523-527.
20. 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.
21. Havenar-Daughton C, Kolumam GA, Murali-Krishna K. 2006. Cutting edge: the direct action of type I IFN on CD4 T cells is critical for sustaining clonal expansion in response to a viral but not a bacterial infection. J. Immunol. 176:3315-3319.
22. Jackson SS, et al. 2005. Role of genes that modulate host immune responses in the immunogenicity and pathogenicity of vaccinia virus. J. Virol. 79:6554-6559.
23. Kastenmuller W, et al. 2007. Cross-competition of CD8+ T cells shapes the immunodominance hierarchy during boost vaccination. J. Exp. Med. 204:2187-2198.
24. Kibler KV, et al. 2011. Improved NYVAC-based vaccine vectors. PLoS One 6:e25674.
25. Kolumam GA, Thomas S, Thompson LJ, Sprent J, Murali-Krishna K. 2005. Type I interferons act directly on CD8 T cells to allow clonal expansion and memory formation in response to viral infection. J. Exp. Med. 202:637-650.
26. Kotenko SV, et al. 2003. IFN-lambdas mediate antiviral protection through a distinct class II cytokine receptor complex. Nat. Immunol. 4:69-77.
27. McCormack S, et al. 2008. EV02: a phase I trial to compare the safety and immunogenicity of HIV DNA-C prime-NYVAC-C boost to NYVAC-C alone. Vaccine 26:3162-3174.
28. Miyahira Y, et al. 1995. Quantification of antigen specific CD8+ T cells using an ELISPOT assay. J. Immunol. Methods 181:45-54.
29. Montanuy I, Alejo A, Alcami A. 2011. Glycosaminoglycans mediate retention of the poxvirus type I interferon binding protein at the cell surface to locally block interferon antiviral responses. FASEB J. 25:1960-1971.
30. Mooij P, et al. 2008. Differential CD4+ versus CD8+ T-cell responses elicited by different poxvirus-based human immunodeficiency virus type 1 vaccine candidates provide comparable efficacies in primates. J. Virol. 82:2975-2988.
31. Mossman K, Upton C, Buller RM, McFadden G. 1995. Species specificity of ectromelia virus and vaccinia virus interferon-gamma binding proteins. Virology 208:762-769.
32. Mueller SN, Langley WA, Carnero E, Garcia-Sastre A, Ahmed R. 2010. Immunization with live attenuated influenza viruses that express altered NS1 proteins results in potent and protective memory CD8+ T-cell responses. J. Virol. 84:1847-1855.
33. Muller U, et al. 1994. Functional role of type I and type II interferons in antiviral defense. Science 264:1918-1921.
34. Najera JL, Gomez CE, Garcia-Arriaza J, Sorzano CO, Esteban M. 2010. Insertion of vaccinia virus C7L host range gene into NYVAC-B genome potentiates immune responses against HIV-1 antigens. PLoS One 5:e11406.
35. Pantaleo G, Esteban M, Jacobs B, Tartaglia J. 2010. Poxvirus vectorbased HIV vaccines. Curr. Opin. HIV AIDS 5:391-396.
36. Paoletti E. 1996. Applications of pox virus vectors to vaccination: an update. Proc. Natl. Acad. Sci. U. S. A. 93:11349-11353.
37. Perdiguero B, Esteban M. 2009. The interferon system and vaccinia virus evasion mechanisms. J. Interferon Cytokine Res. 29:581-598.
38. Perkus ME, Tartaglia J, Paoletti E. 1995. Poxvirus-based vaccine candidates for cancer, AIDS, and other infectious diseases. J. Leukoc. Biol. 58: 1-13.
39. Pestka S, Langer JA, Zoon KC, Samuel CE. 1987. Interferons and their actions. Annu. Rev. Biochem. 56:727-777.
40. Pillai VK, et al. 2011. Different patterns of expansion, contraction and memory differentiation of HIV-1 Gag-specific CD8 T cells elicited by adenovirus type 5 and modified vaccinia Ankara vaccines. Vaccine 29:5399-5406.
41. Prlic M, Williams MA, Bevan MJ. 2007. Requirements for CD8 T-cell priming, memory generation and maintenance. Curr. Opin. Immunol. 19:315-319.
42. Quakkelaar ED, et al. 2011. Improved innate and adaptive immunostimulation by genetically modified HIV-1 protein expressingNYVACvectors. PLoS One 6:e16819.
43. Ramirez JC, Gherardi MM, Esteban M. 2000. Biology of attenuated modified vaccinia virus Ankara recombinant vector in mice: virus fate and activation of B-and T-cell immune responses in comparison with the Western Reserve strain and advantages as a vaccine. J. Virol. 74:923-933.
44. Rerks-Ngarm S, et al. 2009. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N. Engl. J. Med. 361:2209-2220.
45. Rodriguez JR, Rodriguez D, Esteban M. 1991. Interferon treatment inhibits early events in vaccinia virus gene expression in infected mice. Virology 185:929-933.
46. Sercan O, Stoycheva D, Hammerling GJ, Arnold B, Schuler T. 2010. IFN-gamma receptor signaling regulates memory CD8+ T cell differentiation. J. Immunol. 184:2855-2862.
47. Staib C, Kisling S, Erfle V, Sutter G. 2005. Inactivation of the viral interleukin 1 β receptor improves CD8+ T-cell memory responses elicited upon immunization with modified vaccinia virus Ankara. J. Gen. Virol. 86:1997-2006.
48. Symons JA, Alcami A, Smith GL. 1995. Vaccinia virus encodes a soluble type I interferon receptor of novel structure and broad species specificity. Cell 81:551-560.
49. Tartaglia J, et al. 1992. Highly attenuated poxvirus vectors. AIDS Res. Hum. Retrovir. 8:1445-1447.
50. Tscharke DC, et al. 2006. Poxvirus CD8+ T-cell determinants and crossreactivity in BALB/c mice. J. Virol. 80:6318-6323.
51. Unsoeld H, Pircher H. 2005. Complex memory T-cell phenotypes revealed by coexpression of CD62L and CCR7. J. Virol. 79:4510-4513.
52. Unterholzner L, et al. 2011. Vaccinia virus protein C6 is a virulence factor that binds TBK-1 adaptor proteins and inhibits activation of IRF3 and IRF7. PLoS Pathog. 7:e1002247.
53. van den Broek MF, Muller U, Huang S, Aguet M, Zinkernagel RM. 1995. Antiviral defense in mice lacking both alpha/beta and gamma interferon receptors. J. Virol. 69:4792-4796.
54. Verardi PH, Jones LA, Aziz FH, Ahmad S, Yilma TD. 2001. Vaccinia virus vectors with an inactivated gamma interferon receptor homolog gene (B8R) are attenuated In vivo without a concomitant reduction in immunogenicity. J. Virol. 75:11-18.
55. Waibler Z, et al. 2009. Vaccinia virus-mediated inhibition of type I interferon responses is a multifactorial process involving the soluble type I interferon receptor B18 and intracellular components. J. Virol. 83:1563-1571.
56. Wild J, et al. 2009. Preclinical evaluation of the immunogenicity of C-type HIV-1-based DNA and NYVAC vaccines in the BALB/c mouse model. Viral Immunol. 22:309-319.