Evaluation of recombinant influenza virus-simian immunodeficiency virus vaccines in macaques

Journal of Virology

Volumn 83, Issue 15, 2009, Pages 7619-7628

  Sexton, Amy ^a   De Rose, Robert ^a   Reece, Jeanette C ^a   Alcantara, Sheilajen ^a   Loh, Liyen ^a   Moffat, Jessica M ^a   Laurie, Karen ^b   Hurt, Aeron ^b   Doherty, Peter C ^a   Turner, Stephen J ^a   Kent, Stephen J ^a   Stambas, John ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b VICTORIAN INFECTIOUS DISEASES REFERENCE LABORATORY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BETA7 INTEGRIN; INFLUENZA VIRUS VECTOR; SIMIAN IMMUNODEFICIENCY VIRUS VACCINE; UNCLASSIFIED DRUG; VIRUS VECTOR;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H3N2; MACACA; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; SEROCONVERSION; SIMIAN IMMUNODEFICIENCY VIRUS; VACCINATION; VIREMIA; VIRUS EXPRESSION; VIRUS INFECTION;

AIDS VACCINES; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE; GENETIC ENGINEERING; HIV; HIV INFECTIONS; HUMANS; INFLUENZA A VIRUS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H3N2 SUBTYPE; MACACA NEMESTRINA; MODELS, ANIMAL; SAIDS VACCINES; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VACCINATION;

ANIMALIA; HUMAN IMMUNODEFICIENCY VIRUS; INFLUENZA A VIRUS; MACACA; MACACA NEMESTRINA; ORTHOMYXOVIRIDAE; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 67650917877     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00470-09     Document Type: Article

References (60)

1. Allen, T. M., P. Jing, B. Calore, H. Horton, D. H. O'Connor, T. Hanke, M. Piekarczyk, R. Ruddersdorf, B. R. Mothe, C. Emerson, N. Wilson, J. D. Lifson, I. M. Belyakov, J. A. Berzofsky, C. Wang, D. B. Allison, D. C. Montefiori, R. C. Desrosiers, S. Wolinsky, K. J. Kunstman, J. D. Altman, A. Sette, A. J. McMichael, and D. I. Watkins. 2002. Effects of cytotoxic T lymphocytes (CTL) directed against a single simian immunodeficiency virus (SIV) Gag CTL epitope on the course of SIVmac239 infection. J. Virol. 76:10507-10511.
2. Allen, T. M., L. Mortara, B. R. Mothe, M. Liebl, P. Jing, B. Calore, M. Piekarczyk, R. Ruddersdorf, D. H. O'Connor, X. Wang, C. Wang, D. B. Allison, J. D. Altman, A. Sette, R. C. Desrosiers, G. Sutter, and D. I. Watkins. 2002. Tat-vaccinated macaques do not control simian immunode-ficiency virus SIVmac239 replication. J. Virol. 76:4108-4112.
3. Allen, T. M., D. H. O'Connor, P. Jing, J. L. Dzuris, B. R. Mothe, T. U. Vogel, E. Dunphy, M. E. Liebl, C. Emerson, N. Wilson, K. J. Kunstman, X. Wang, D. B. Allison, A. L. Hughes, R. C. Desrosiers, J. D. Altman, S. M. Wolinsky, A. Sette, and D. I. Watkins. 2000. Tat-specific cytotoxic T lymphocytes select for SIV escape variants during resolution of primary viraemia. Nature 407: 386-390.
4. +-T-cell responses. J. Virol. 79:4329-4339.
5. Arthos, J., C. Cicala, E. Martinelli, K. Macleod, D. Van Ryk, D. Wei, Z. Xiao, T. D. Veenstra, T. P. Conrad, R. A. Lempicki, S. McLaughlin, M. Pascuccio, R. Gopaul, J. McNally, C. C. Cruz, N. Censoplano, E. Chung, K. N. Reitano, S. Kottilil, D. J. Goode, and A. S. Fauci. 2008. HIV-1 envelope protein binds to and signals through integrin alpha4beta7, the gut mucosal homing receptor for peripheral T cells. Nat. Immunol. 9:301-309.
6. Barouch, D. H., J. Kunstman, M. J. Kuroda, J. E. Schmitz, S. Santra, F. W. Peyerl, G. R. Krivulka, K. Beaudry, M. A. Lifton, D. A. Gorgone, D. C. Montefiori, M. G. Lewis, S. M. Wolinsky, and N. L. Letvin. 2002. Eventual AIDS vaccine failure in a rhesus monkey by viral escape from cytotoxic T lymphocytes. Nature 415:335-339.
7. Batten, C. J., R. D. Rose, K. M. Wilson, M. B. Agy, S. Chea, I. Stratov, D. C. Montefiori, and S. J. Kent. 2006. Comparative evaluation of simian, simianhuman, and human immunodeficiency virus infections in the pigtail macaque (Macaca nemestrina) model. AIDS Res. Hum. Retroviruses 22:580-588.
8. Bello, G., C. Casado, V. Sandonis, M. Alonso-Nieto, J. L. Vicario, S. Garcia, V. Hernando, C. Rodriguez, J. del Romero, and C. Lopez-Galindez. 2005. A subset of human immunodeficiency virus type 1 long-term non-progressors is characterized by the unique presence of ancestral sequences in the viral population. J. Gen. Virol. 86:355-364.
9. Belshe, R. B., K. M. Edwards, T. Vesikari, S. V. Black, R. E. Walker, M. Hultquist, G. Kemble, and E. M. Connor. 2007. Live attenuated versus inactivated influenza vaccine in infants and young children. N. Engl. J. Med. 356:685-696.
10. Berendt, R. F. 1974. Simian model for the evaluation of immunity to influenza. Infect. Immun. 9:101-105.
11. Buchbinder, S. P., D. V. Mehrotra, A. Duerr, D. W. Fitzgerald, R. Mogg, D. Li, P. B. Gilbert, J. R. Lama, M. Marmor, C. Del Rio, M. J. McElrath, D. R. Casimiro, K. M. Gottesdiener, J. A. Chodakewitz, L. Corey, and M. N. Robertson. 2008. Efficacy assessment of a cell-mediated immunity HIV-1 vaccine (the Step Study): a double-blind, randomised, placebo-controlled, test-of-concept trial. Lancet 372:1881-1893.
12. Carroll, T. D., S. R. Matzinger, M. Genesca, L. Fritts, R. Colon, M. B. McChesney, and C. J. Miller. 2008. Interferon-induced expression of MxA in the respiratory tract of rhesus macaques is suppressed by influenza virus replication. J. Immunol. 180:2385-2395.
13. + T lymphocytes by attenuated simian immunodeficiency virus. J. Virol. 74:8762-8766.
14. Crotty, S., B. L. Lohman, F. X. Lu, S. Tang, C. J. Miller, and R. Andino. 1999. Mucosal immunization of cynomolgus macaques with two serotypes of live poliovirus vectors expressing simian immunodeficiency virus antigens: stimulation of humoral, mucosal, and cellular immunity. J. Virol. 73:9485-9495.
15. Daniel, M. D., F. Kirchhoff, S. C. Czajak, P. K. Sehgal, and R. C. Desrosiers. 1992. Protective effects of a live attenuated SIV vaccine with a deletion in the nef gene. Science 258:1938-1941.
16. Davenport, M. P., L. Loh, J. Petravic, and S. J. Kent. 2008. Rates of HIV immune escape and reversion: implications for vaccination. Trends Microbiol. 16:561-566.
17. Demberg, T., J. D. Boyer, N. Malkevich, L. J. Patterson, D. Venzon, E. L. Summers, I. Kalisz, V. S. Kalyanaraman, E. M. Lee, D. B. Weiner, and M. Robert-Guroff. 2008. Sequential priming with simian immunodeficiency virus (SIV) DNA vaccines, with or without encoded cytokines, and a replicating adenovirus-SIV recombinant followed by protein boosting does not control a pathogenic SIVmac251 mucosal challenge. J. Virol. 82:10911-10921.
18. De Rose, R., C. J. Batten, M. Z. Smith, C. S. Fernandez, V. Peut, S. Thomson, I. A. Ramshaw, B. E. Coupar, D. B. Boyle, V. Venturi, M. P. Davenport, and S. J. Kent. 2007. Comparative efficacy of subtype AE simian-human immunodeficiency virus priming and boosting vaccines in pigtail macaques. J. Virol. 81:292-300.
19. De Rose, R., C. S. Fernandez, M. Z. Smith, C. J. Batten, S. Alcantara, V. Peut, E. Rollman, L. Loh, R. D. Mason, C. M. Wilson, M. G. Law, A. J. Handley, and S. J. Kent. 2008. Control of viremia following immunotherapy of SIV-infected macaques with peptide pulsed blood. PLoS Pathog. 4:e1000055.
20. Evans, D. T., L. M. Chen, J. Gillis, K. C. Lin, B. Harty, G. P. Mazzara, R. O. Donis, K. G. Mansfield, J. D. Lifson, R. C. Desrosiers, J. E. Galan, and R. P. Johnson. 2003. Mucosal priming of simian immunodeficiency virus-specific cytotoxic T-lymphocyte responses in rhesus macaques by the Salmonella type III secretion antigen delivery system. J. Virol. 77:2400-2409.
21. Ferko, B., C. Kittel, J. Romanova, S. Sereinig, H. Katinger, and A. Egorov. 2006. Live attenuated influenza virus expressing human interleukin-2 reveals increased immunogenic potential in young and aged hosts. J. Virol. 80: 11621-11627.
22. Fernandez, C. S., M. Z. Smith, C. J. Batten, R. De Rose, J. C. Reece, E. Rollman, V. Venturi, M. P. Davenport, and S. J. Kent. 2007. Vaccineinduced T cells control reversion of AIDS virus immune escape mutants. J. Virol. 81:4137-4144.
23. Fernandez, C. S., I. Stratov, R. De Rose, K. Walsh, C. J. Dale, M. Z. Smith, M. B. Agy, S. L. Hu, K. Krebs, D. I. Watkins, H. O'Connor, D. M. P. Davenport, and S. J. Kent. 2005. Rapid viral escape at an immunodominant simian-human immunodeficiency virus cytotoxic T-lymphocyte epitope exacts a dramatic fitness cost. J. Virol. 79:5721-5731.
24. Franchini, G., M. Robert-Guroff, J. Tartaglia, A. Aggarwal, A. Abimiku, J. Benson, P. Markham, K. Limbach, G. Hurteau, J. Fullen, et al. 1995. Highly attenuated HIV type 2 recombinant poxviruses, but not HIV-2 recombinant Salmonella vaccines, induce long-lasting protection in rhesus macaques. AIDS Res. Hum. Retroviruses 11:909-920.
25. Genesca, M., T. Rourke, J. Li, K. Bost, B. Chohan, M. B. McChesney, and C. J. Miller. 2007. Live attenuated lentivirus infection elicits polyfunctional simian immunodeficiency virus Gag-specific CD8+ T cells with reduced apoptotic susceptibility in rhesus macaques that control virus replication after challenge with pathogenic SIVmac239. J. Immunol. 179:4732-4740.
26. Genesca, M., P. J. Skinner, K. M. Bost, D. Lu, Y. Wang, T. L. Rourke, A. T. Haase, M. B. McChesney, and C. J. Miller. 2008. Protective attenuated lentivirus immunization induces SIV-specific T cells in the genital tract of rhesus monkeys. Mucosal Immunol. 1:219-228.
27. Gherardi, M. M., J. L. Najera, E. Perez-Jimenez, S. Guerra, A. Garcia-Sastre, and M. Esteban. 2003. Prime-boost immunization schedules based on influenza virus and vaccinia virus vectors potentiate cellular immune responses against human immunodeficiency virus Env protein systemically and in the genitorectal draining lymph nodes. J. Virol. 77:7048-7057.
28. Gonzalo, R. M., D. Rodriguez, A. Garcia-Sastre, J. R. Rodriguez, P. Palese, and M. Esteban. 1999. Enhanced CD8+ T cell response to HIV-1 env by combined immunization with influenza and vaccinia virus recombinants. Vaccine 17:887-892.
29. Goulder, P. J., and D. I. Watkins. 2004. HIV and SIV CTL escape: implications for vaccine design. Nat. Rev. Immunol. 4:630-640.
30. Hansen, S. G., C. Vieville, N. Whizin, L. Coyne-Johnson, D. C. Siess, D. D. Drummond, A. W. Legasse, M. K. Axthelm, K. Oswald, C. M. Trubey, M. Piatak, Jr., J. D. Lifson, J. A. Nelson, M. A. Jarvis, and L. J. Picker. 2009. Effector memory T cell responses are associated with protection of rhesus monkeys from mucosal simian immunodeficiency virus challenge. Nat. Med. 15:293-299.
31. Hoffmann, E., G. Neumann, Y. Kawaoka, G. Hobom, and R. G. Webster. 2000. A DNA transfection system for generation of influenza A virus from eight plasmids. Proc. Natl. Acad. Sci. USA 97:6108-6113.
32. Horton, H., T. U. Vogel, D. K. Carter, K. Vielhuber, D. H. Fuller, T. Shipley, J. T. Fuller, K. J. Kunstman, G. Sutter, D. C. Montefiori, V. Erfle, R. C. Desrosiers, N. Wilson, L. J. Picker, S. M. Wolinsky, C. Wang, D. B. Allison, and D. I. Watkins. 2002. Immunization of rhesus macaques with a DNA prime/modified vaccinia virus Ankara boost regimen induces broad simian immunodeficiency virus (SIV)-specific T-cell responses and reduces initial viral replication but does not prevent disease progression following challenge with pathogenic SIVmac239. J. Virol. 76:7187-7202.
33. Ibraghimov, A. R., and R. G. Lynch. 1994. T cell specialization at environmental interfaces: T cells from the lung and the female genital tract of lpr and gld mice differ from their splenic and lymph node counterparts. Eur. J. Immunol. 24:1848-1852.
34. Jenkins, M. R., R. Webby, P. C. Doherty, and S. J. Turner. 2006. Addition of a prominent epitope affects influenza A virus-specific CD8+ T cell immunodominance hierarchies when antigen is limiting. J. Immunol. 177:2917-2925.
35. Kaufman, D. R., J. Liu, A. Carville, K. G. Mansfield, M. J. Havenga, J. Goudsmit, and D. H. Barouch. 2008. Trafficking of antigen-specific CD8+ T lymphocytes to mucosal surfaces following intramuscular vaccination. J. Immunol. 181:4188-4198.
36. Kent, S. J., R. De Rose, V. V. Mokhonov, E. A. Mohkonova, C. S. Fernandez, S. Alcantara, E. Rollman, R. D. Mason, L. Loh, V. Peut, J. Reece, X. J. Wang, K. M. Wilson, A. Suhrbier, and A. A. Khromykh. 2008. Evaluation of recombinant Kunjin replicon SIV vaccines for protective efficacy in macaques. Virology 374:528-534.
37. Kittel, C., S. Sereinig, B. Ferko, J. Stasakova, J. Romanova, A. Wolkerstorfer, H. Katinger, and A. Egorov. 2004. Rescue of influenza virus expressing GFP from the NS1 reading frame. Virology 324:67-73.
38. Klavinskis, L. S., C. Barnfield, L. Gao, and S. Parker. 1999. Intranasal immunization with plasmid DNA-lipid complexes elicits mucosal immunity in the female genital and rectal tracts. J. Immunol. 162:254-262.
39. La Gruta, N. L., K. Kedzierska, K. Pang, R. Webby, M. Davenport, W. Chen, S. J. Turner, and P. C. Doherty. 2006. A virus-specific CD8+ T cell immunodominance hierarchy determined by antigen dose and precursor frequencies. Proc. Natl. Acad. Sci. USA 103:994-999.
40. Liu, J., K. L. O'Brien, D. M. Lynch, N. L. Simmons, A. La Porte, A. M. Riggs, P. Abbink, R. T. Coffey, L. E. Grandpre, M. S. Seaman, G. Landucci, D. N. Forthal, D. C. Montefiori, A. Carville, K. G. Mansfield, M. J. Havenga, M. G. Pau, J. Goudsmit, and D. H. Barouch. 2009. Immune control of an SIV challenge by a T-cell-based vaccine in rhesus monkeys. Nature 457:87-91.
41. Loh, L., J. Petravic, C. J. Batten, M. P. Davenport, and S. J. Kent. 2008. Vaccination and timing influence SIV immune escape viral dynamics in vivo. PLoS Pathog. 4:e12.
42. Lohmeyer, J., J. Friedrich, F. Grimminger, U. Maus, R. Tenter, H. Morr, H. G. Velcovsky, W. Seeger, and S. Rosseau. 1999. Expression of mucosarelated integrin alphaEbeta7 on alveolar T cells in interstitial lung diseases. Clin. Exp. Immunol. 116:340-346.
43. McElrath, M. J., S. C. De Rosa, Z. Moodie, S. Dubey, L. Kierstead, H. Janes, O. D. Defawe, D. K. Carter, J. Hural, R. Akondy, S. P. Buchbinder, M. N. Robertson, D. V. Mehrotra, S. G. Self, L. Corey, J. W. Shiver, and D. R. Casimiro. 2008. HIV-1 vaccine-induced immunity in the test-of-concept Step Study: a case-cohort analysis. Lancet 372:1894-1905.
44. Nakaya, Y., T. Nakaya, M. S. Park, J. Cros, J. Imanishi, P. Palese, and A. Garcia-Sastre. 2004. Induction of cellular immune responses to simian immunodeficiency virus Gag by two recombinant negative-strand RNA virus vectors. J. Virol. 78:9366-9375.
45. Nakaya, Y., H. Zheng, and A. Garcia-Sastre. 2003. Enhanced cellular immune responses to SIV Gag by immunization with influenza and vaccinia virus recombinants. Vaccine 21:2097-2106.
46. O'Connor, D. H., T. M. Allen, T. U. Vogel, P. Jing, I. P. DeSouza, E. Dodds, E. J. Dunphy, C. Melsaether, B. Mothe, H. Yamamoto, H. Horton, N. Wilson, A. L. Hughes, and D. I. Watkins. 2002. Acute phase cytotoxic T lymphocyte escape is a hallmark of simian immunodeficiency virus infection. Nat. Med. 8:493-499.
47. Oh, D. Y., I. G. Barr, J. A. Mosse, and K. L. Laurie. 2008. MDCK-SIAT1 cells show improved isolation rates for recent human influenza viruses compared to conventional MDCK cells. J. Clin. Microbiol. 46:2189-2194.
48. Palese, P., F. Zavala, T. Muster, R. S. Nussenzweig, and A. Garcia-Sastre. 1997. Development of novel influenza virus vaccines and vectors. J. Infect. Dis. 176(Suppl. 1):S45-S49.
49. Patterson, L. J., J. Beal, T. Demberg, R. H. Florese, N. Malkevich, D. Venzon, K. Aldrich, E. Richardson, V. S. Kalyanaraman, I. Kalisz, E. M. Lee, D. C. Montefiori, F. A. Robey, and M. Robert-Guroff. 2008. Replicating adenovirus HIV/SIV recombinant priming alone or in combination with a gp140 protein boost results in significant control of viremia following a SHIV89.6P challenge in Mamu-A*01 negative rhesus macaques. Virology 374:322-337.
50. Picker, L. J., and D. I. Watkins. 2005. HIV pathogenesis: the first cut is the deepest. Nat. Immunol. 6:430-432.
51. Pratt, B. F., D. H. O'Connor, B. A. Lafont, J. L. Mankowski, C. S. Fernandez, R. Triastuti, A. G. Brooks, S. J. Kent, and M. Z. Smith. 2006. MHC class I allele frequencies in pigtail macaques of diverse origin. Immunogenetics 58:995-1001.
52. Rimmelzwaan, G. F., T. Kuiken, G. van Amerongen, T. M. Bestebroer, R. A. Fouchier, and A. D. Osterhaus. 2001. Pathogenesis of influenza A (H5N1) virus infection in a primate model. J. Virol. 75:6687-6691.
53. Rollman, E., R. D. Mason, J. Lin, A. Brooks, and S. J. Kent. 2008. Protection afforded by live attenuated SIV is associated with rapid killing kinetics of CTLs. J. Med. Primatol. 37:24-32.
54. Rollman, E., M. Z. Smith, A. G. Brooks, D. F. Purcell, B. Zuber, I. A. Ramshaw, and S. J. Kent. 2007. Killing kinetics of simian immunodeficiency virus-specific CD8+ T cells: implications for HIV vaccine strategies. J. Immunol. 179:4571-4579.
55. Rose, N. F., P. A. Marx, A. Luckay, D. F. Nixon, W. J. Moretto, S. M. Donahoe, D. Montefiori, A. Roberts, L. Buonocore, and J. K. Rose. 2001. An effective AIDS vaccine based on live attenuated vesicular stomatitis virus recombinants. Cell 106:539-549.
56. Sereinig, S., M. Stukova, N. Zabolotnyh, B. Ferko, C. Kittel, J. Romanova, T. Vinogradova, H. Katinger, O. Kiselev, and A. Egorov. 2006. Influenza virus NS vectors expressing the Mycobacterium tuberculosis ESAT-6 protein induce CD4+ Th1 immune response and protect animals against tuberculosis challenge. Clin. Vaccine Immunol. 13:898-904.
57. Townsend, A. R., F. M. Gotch, and J. Davey. 1985. Cytotoxic T cells recognize fragments of the influenza nucleoprotein. Cell 42:457-467.
58. Wahl, A., F. Schafer, W. Bardet, R. Buchli, G. M. Air, and W. H. Hildebrand. 2009. HLA class I molecules consistently present internal influenza epitopes. Proc. Natl. Acad. Sci. USA 106:540-545.
59. Webby, R. J., S. Andreansky, J. Stambas, J. E. Rehg, R. G. Webster, P. C. Doherty, and S. J. Turner. 2003. Protection and compensation in the influenza virus-specific CD8+ T cell response. Proc. Natl. Acad. Sci. USA 100: 7235-7240.
60. Yun, N. E., N. S. Linde, M. A. Zacks, I. G. Barr, A. C. Hurt, J. N. Smith, N. Dziuba, M. R. Holbrook, L. Zhang, J. M. Kilpatrick, C. S. Arnold, and S. Paessler. 2008. Injectable peramivir mitigates disease and promotes survival in ferrets and mice infected with the highly virulent influenza virus, A/Vietnam/ 1203/04 (H5N1). Virology 374:198-209.