Vaccine-induced cellular immune responses reduce plasma viral concentrations after repeated low-dose challenge with pathogenic simian immunodeficiency virus SIVmac239

Journal of Virology

Volumn 80, Issue 12, 2006, Pages 5875-5885

  Wilson, Nancy A ^a,g   Reed, Jason ^a   Napoe, Gnankang S ^a   Piaskowski, Shari ^b   Szymanski, Andy ^b   Furlott, Jessica ^a   Gonzalez, Edna J ^b   Yant, Levi J ^a   Maness, Nicholas J ^a   May, Gemma E ^a   Soma, Taeko ^a   Reynolds, Matthew R ^a   Rakasz, Eva ^a   Rudersdorf, Richard ^a   McDermott, Adrian B ^b,h   O'Connor, David H ^b   Friedrich, Thomas C ^a   Allison, David B ^c   Patki, Amit ^c   Picker, Louis J ^d   Burton, Dennis R ^e   Lin, Jing ^f   Huang, Lingyi ^f   Patel, Deepa ^f   Heindecker, Gwendolyn ^f   Fan, Jiang ^f   Citron, Michael ^f   Horton, Melanie ^f   Wang, Fubao ^f   Liang, Xiaoping ^f   Shiver, John W ^f   Casimiro, Danilo R ^f   Watkins, David I ^a,b,g   more..

^a UNIVERSITY OF WISCONSIN   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^d OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^e SCRIPPS RESEARCH INSTITUTE   (United States)

^f MERCK RESEARCH LABORATORIES   (United States)

^g UNIVERSITY OF WISCONSIN MADISON   (United States)

^h INTERNATIONAL AIDS VACCINE INITIATIVE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAG PROTEIN; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; NEF PROTEIN; NEUTRALIZING ANTIBODY; REV PROTEIN; TRANSACTIVATOR PROTEIN; VIRUS ENVELOPE PROTEIN;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ADENOVIRUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY PRODUCTION; ARTICLE; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; HUMAN; HUMAN CELL; LYMPHOCYTE; NONHUMAN; PRIORITY JOURNAL; RHESUS MONKEY; SIMIAN IMMUNODEFICIENCY VIRUS; VACCINATION; VIREMIA; VIRUS LOAD; VIRUS REPLICATION;

ANIMALS; ANTIBODIES, VIRAL; CD4 LYMPHOCYTE COUNT; CD4-POSITIVE T-LYMPHOCYTES; GENE PRODUCTS, ENV; IMMUNITY, CELLULAR; IMMUNIZATION; MACACA MULATTA; SAIDS VACCINES; SIMIAN IMMUNODEFICIENCY VIRUS; VIRAL LOAD; VIRUS REPLICATION;

ADENOVIRIDAE; AIDS VIRUS; ANIMALIA; MACACA MULATTA; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 33744902339     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00171-06     Document Type: Article

References (68)

1. + lymphocytes from simian immunodeficiency virus-infected rhesus macaques recognize 14 different epitopes bound by the major histocompatibility complex class I molecule mamu-A*01: implications for vaccine design and testing. J. Virol. 75:738-749.
2. Allen, T. M., D. H. O'Connor, P. Jing, et al. 2000. Tat-specific cytotoxic T lymphocytes select for SIV escape variants during resolution of primary viraemia. Nature 407:386-390.
3. Amara, R. R., F. Villinger, J. D. Altman, et al. 2001. Control of a mucosal challenge and prevention of AIDS by a multiprotein DNA/MVA vaccine. Science 292:69-74.
4. Barouch, D. H., S. Santra, M. J. Kuroda, et al. 2001. Reduction of simian-human immunodeficiency virus 89.6P viremia in rhesus monkeys by recombinant modified vaccinia virus Ankara vaccination. J. Virol. 75:5151-5158.
5. Barouch, D. H., S. Santra, J. E. Schmitz, et al. 2000. Control of viremia and prevention of clinical AIDS in rhesus monkeys by cytokine-augmented DNA vaccination. Science 290:486-492.
6. mac251: dependence on route of challenge exposure. J. Virol. 72:4170-4182.
7. Box, G. E. P., and D. R. Cox. 1964. An analysis of transformations. J. R. Stat. Soc. B 26:211-252.
8. Buge, S. L., L. Murty, K. Arora, et al. 1999. Factors associated with slow disease progression in macaques immunized with an adenovirus-simian immunodeficiency virus (SIV) envelope priming-gp120 boosting regimen and challenged vaginally with SIVmac251. J. Virol. 73:7430-7440.
9. Buge, S. L., E. Richardson, S. Alipanah, et al. 1997. An adenovirus-simian immunodeficiency virus env vaccine elicits humoral, cellular, and mucosal immune responses in rhesus macaques and decreases viral burden following vaginal challenge. J. Virol. 71:8531-8541.
10. Burton, D. R., R. C. Desrosiers, R. W. Doms, et al. 2004. HIV vaccine design and the neutralizing antibody problem. Nat. Immunol. 5:233-236.
11. Casimiro, D. R., F. Wang, W. A. Schleif, 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. Chakraborty, H., P. K. Sen, R. W. Helms, et al. 2001. Viral burden in genital secretions determines male-to-female sexual transmission of HIV-1: a probabilistic empiric model. AIDS 15:621-627.
13. Chakraborty, R., A. S. Morel, J. K. Sutton, et al. 2005. Correlates of delayed disease progression in HIV-1-infected Kenyan children. J. Immunol. 174: 8191-8199.
14. Chen, X., G. Scala, I. Quinto, et al. 2001. Protection of rhesus macaques against disease progression from pathogenic SHIV-89.6PD by vaccination with phage-displayed HIV-1 epitopes. Nat. Med. 7:1225-1231.
15. Cohen, M. S., and C. D. Pilcher. 2005. Amplified HIV transmission and new approaches to HIV prevention. J. Infect. Dis. 191:1391-1393.
16. Collins, K. L., B. K. Chen, S. A. Kalams, B. D. Walker, and D. Baltimore. 1998. HIV-1 Nef protein protects infected primary cells against killing by cytotoxic T lymphocytes. Nature 391:397-401.
17. Crotty, S., C. J. Miller, B. L. Lohman, et al. 2001. Protection against simian immunodeficiency virus vaginal challenge by using Sabin poliovirus vectors. J. Virol. 75:7435-7452.
18. Davis, N. L., I. J. Caley, K. W. Brown, et al. 2000. Vaccination of macaques against pathogenic simian immunodeficiency virus with Venezuelan equine encephalitis virus replicon particles. J. Virol. 74:371-378.
19. Egan, M. A., W. A. Charini, M. J. Kuroda, et al. 2000. Simian immunodeficiency virus (SIV) gag DNA-vaccinated rhesus monkeys develop secondary cytotoxic T-lymphocyte responses and control viral replication after pathogenic SIV infection. J. Virol. 74:7485-7495.
20. Feinberg, M. B., and J. P. Moore. 2002. AIDS vaccine models: challenging challenge viruses. Nat. Med. 8:207-210.
21. Fuller, D. H., P. A. Rajakumar, L. A. Wilson, et al. 2002. Induction of mucosal protection against primary, heterologous simian immunodeficiency virus by a DNA vaccine. J. Virol. 76:3309-3317.
22. Gallimore, A., M. Cranage, N. Cook, et al. 1995. Early suppression of SIV replication by CD8+ nef-specific cytotoxic T cells in vaccinated macaques. Nat. Med. 1:1167-1173.
23. Garcia, P. M., L. A. Kalish, J. Pitt, et al. 1999. Maternal levels of plasma human immunodeficiency virus type 1 RNA and the risk of perinatal transmission. N. Engl. J. Med. 341:394-402.
24. Gaschen, B., J. Taylor, K. Yusim, et al. 2002. Diversity considerations in HIV-1 vaccine selection. Science 296:2354-2360.
25. Gilbert, P. B., M. L. Peterson, D. Follmann, et al. 2005. Correlation between immunologic responses to a recombinant glycoprotein 120 vaccine and incidence of HIV-1 infection in a phase 3 HIV-1 preventive vaccine trial. J. Infect. Dis. 191:666-677.
26. Gomez-Roman, V. R., L. J. Patterson, D. Venzon, et al. 2005. Vaccine-elicited antibodies mediate antibody-dependent cellular cytotoxicity correlated with significantly reduced acute viremia in rhesus macaques challenged with SIVmac251. J. Immunol. 174:2185-2189.
27. Gray, R. H., X. Li, M. J. Wawer, et al. 2003. Stochastic simulation of the impact of antiretroviral therapy and HIV vaccines on HIV transmission; Rakai, Uganda. AIDS 17:1941-1951.
28. Gray, R. H., M. J. Wawer, R. Brookmeyer, et al. 2001. Probability of HIV-1 transmission per coital act in monogamous, heterosexual, HIV-1-discordant couples in Rakai, Uganda. Lancet 357:1149-1153.
29. Gruters, R. A., C. A. van Baalen, and A. D. Osterhaus. 2002. The advantage of early recognition of HIV-infected cells by cytotoxic T-lymphocytes. Vaccine 20:2011-2015.
30. Hel, Z., J. Nacsa, E. Tryniszewska, et al. 2002. Containment of simian immunodeficiency virus infection in vaccinated macaques: correlation with the magnitude of virus-specific pre- and postchallenge CD4+ and CD8+ T cell responses. J. Immunol. 169:4778-4787.
31. Hel, Z., W. P. Tsai, E. Tryniszewska, et al. 2006. Improved vaccine protection from simian AIDS by the addition of nonstructural simian immunodeficiency virus genes. J. Immunol. 176:85-96.
32. Hirsch, V. M., T. R. Fuerst, G. Sutter, et al. 1996. Patterns of viral replication correlate with outcome in simian immunodeficiency virus (SIV)-infected macaques: effect of prior immunization with a trivalent SIV vaccine in modified vaccinia virus Ankara. J. Virol. 70:3741-3752.
33. Johnson, P. R., B. C. Schnepp, M. J. Connell, et al. 2005. Novel adeno-associated virus vector vaccine restricts replication of simian immunodeficiency virus in macaques. J. Virol. 79:955-965.
34. Knapp, L. A., E. Lehmann, L. Hennes, M. E. Eberle, and D. I. Watkins. 1997. High-resolution HLA-DRB typing using denaturing gradient gel electrophoresis and direct sequencing. Tissue Antigens 50:170-177.
35. Li, Q., L. Duan, J. D. Estes, et al. 2005. Peak SIV replication in resting memory CD4+ T cells depletes gut lamina propria CD4+ T cells. Nature 434:1148-1152.
36. Lifson, J. D., J. L. Rossio, R. Arnaout, et al. 2000. Containment of simian immunodeficiency virus infection: cellular immune responses and protection from rechallenge following transient postinoculation antiretroviral treatment. J. Virol. 74:2584-2593.
37. + lymphocytes in control of simian immunodeficiency virus infection and resistance to rechallenge after transient early antiretroviral treatment. J. Virol. 75:10187-10199.
38. Loffredo, J. T., J. Sidney, C. Wojewoda, et al. 2004. Identification of seventeen new simian immunodeficiency virus-derived CD8+ T cell epitopes restricted by the high frequency molecule, Mamu-A*02, and potential escape from CTL recognition. J. Immunol. 173:5064-5076.
39. Matano, T., M. Kano, H. Nakamura, A. Takeda, and Y. Nagai. 2001. Rapid appearance of secondary immune responses and protection from acute CD4 depletion after a highly pathogenic immunodeficiency virus challenge in macaques vaccinated with a DNA prime/Sendai virus vector boost regimen. J. Virol. 75:11891-11896.
40. Matano, T., M. Kobayashi, H. Igarashi, et al. 2004. Cytotoxic T lymphocyte-based control of simian immunodeficiency virus replication in a preclinical AIDS vaccine trial. J. Exp. Med. 199:1709-1718.
41. Mattapallil, J. J., D. C. Douek, B. Hill, et al. 2005. Massive infection and loss of memory CD4+ T cells in multiple tissues during acute SIV infection. Nature 434:1093-1097.
42. McDermott, A. B., J. Mitchen, S. Piaskowski, et al. 2004. Repeated low-dose mucosal simian immunodeficiency virus SIVmac239 challenge results in the same viral and immunological kinetics as high-dose challenge: a model for the evaluation of vaccine efficacy in nonhuman primates. J. Virol. 78:3140-3144.
43. Mellors, J. W., A. Munoz, J. V. Giorgi, et al. 1997. Plasma viral load and CD4+ lymphocytes as prognostic markers of HIV-1 infection. Ann. Intern. Med. 126:946-954.
44. Mellors, J. W., C. R. J. Rinaldo, P. Gupta, et al. 1996. Prognosis in HIV-1 infection predicted by the quantity of virus in plasma. Science 272:1167-1170.
45. Murphy, C. G., W. T. Lucas, R. E. Means, et al. 2000. Vaccine protection against simian immunodeficiency virus by recombinant strains of herpes simplex virus. J. Virol. 74:7745-7754.
46. Ourmanov, I., C. R. Brown, B. Moss, et al. 2000. Comparative efficacy of recombinant modified vaccinia virus Ankara expressing simian immunodeficiency virus (SIV) Gag-Pol and/or Env in macaques challenged with pathogenic SIV. J. Virol. 74:2740-2751.
47. Pal, R., D. Venzon, N. L. Letvin, et al. 2002. 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. 76:292-302.
48. Patterson, L. J., N. Malkevitch, D. Venzon, et al. 2004. Protection against mucosal simian immunodeficiency virus SIV(mac251) challenge by using replicating adenovirus-SIV multigene vaccine priming and subunit boosting. J. Virol. 78:2212-2221.
49. Picker, L. J., S. I. Hagen, R. Lum, et al. 2004. Insufficient production and tissue delivery of CD4+ memory T cells in rapidly progressive simian immunodeficiency virus infection. J. Exp. Med. 200:1299-1314.
50. Pilcher, C. D., H. C. Tien, J. J. J. Eron, et al. 2004. Brief but efficient: acute HIV infection and the sexual transmission of HIV. J. Infect. Dis. 189:1785-1792.
51. Pitcher, C. J., S. I. Hagen, J. M. Walker, et al. 2002. Development and homeostasis of T cell memory in rhesus macaque. J. Immunol. 168:29-43.
52. Quinn, T. C., M. J. Wawer, N. Sewankambo, et al. 2000. Viral load and heterosexual transmission of human immunodeficiency virus type 1. N. Engl. J. Med. 342:921-929.
53. Recher, M., K. S. Lang, L. Hunziker, et al. 2004. Deliberate removal of T cell help improves virus-neutralizing antibody production. Nat. Immunol. 5:934-942.
54. Rose, N. F., P. A. Marx, A. Luckay, et al. 2001. An effective AIDS vaccine based on live attenuated vesicular stomatitis virus recombinants. Cell 106: 539-549.
55. Rosenberg, E. S., J. M. Billingsley, A. M. Caliendo, et al. 1997. Vigorous HIV-1-specific CD4+ T cell responses associated with control of viremia. Science 278:1447-1450.
56. Schwartz, O., V. Marechal, S. Le Gall, F. Lemonnier, and J. M. Heard. 1996. Endocytosis of major histocompatibility complex class I molecules is induced by the HIV-1 Nef protein. Nat. Med. 2:338-342.
57. Shiver, J. W., T. M. Fu, L. Chen, et al. 2002. Replication-incompetent adenoviral vaccine vector elicits effective anti-immunodeficiency-virus immunity. Nature 415:331-335.
58. Stittelaar, K. J., R. A. Gruters, M. Schutten, et al. 2002. Comparison of the efficacy of early versus late viral proteins in vaccination against SIV. Vaccine 20:2921-2927.
59. Ten Haaft, P., B. Verstrepen, K. Uberla, B. Rosenwirth, and J. Heeney. 1998. A pathogenic threshold of virus load defined in simian immunodeficiency virus- or simian-human immunodeficiency virus-infected macaques. J. Virol. 72:10281-10285.
60. van Baalen, C. A., C. Guillon, M. van Baalen, et al. 2002. Impact of antigen expression kinetics on the effectiveness of HIV-specific cytotoxic T lymphocytes. Eur. J. Immunol. 32:2644-2652.
61. Van Baalen, C. A., M. Schutten, R. C. Huisman, et al. 1998. Kinetics of antiviral activity by human immunodeficiency virus type 1-specific cytotoxic T lymphocytes (CTL) and rapid selection of CTL escape virus in vitro. J. Virol. 72:6851-6857.
62. Vogel, T. U., T. C. Friedrich, D. H. O'Connor, et al. 2002. Escape in one of two cytotoxic T-lymphocyte epitopes bound by a high-frequency major histocompatibility complex class I molecule, Mamu-A*02: a paradigm for virus evolution and persistence? J. Virol. 76:11623-11636.
63. Wawer, M. J., R. H. Gray, N. K. Sewankambo, et al. 2005. Rates of HIV-1 transmission per coital act, by stage of HIV-1 infection, in Rakai, Uganda. J. Infect. Dis. 191:1403-1409.
64. Yang, O. O., P. T. Sarkis, A. Ali, et al. 2003. Determinant of HIV-1 mutational escape from cytotoxic T lymphocytes. J. Exp. Med. 197:1365-1375.
65. Yang, O. O., P. T. Sarkis, A. Trocha, et al. 2003. Impacts of avidity and specificity on the antiviral efficiency of HIV-1-specific CTL. J. Immunol. 171:3718-3724.
66. Yant, L. J., T. C. Friedrich, R. C. Johnson, et al. 2006. The high-frequency major histocompatibility complex class I allele Mamu-B*17 is associated with control of simian immunodeficiency virus SIVmac239 replication. J. Virol. 80:5074-5077.
67. Zhao, J., J. Pinczewski, V. R. Gomez-Roman, et al. 2003. Improved protection of rhesus macaques against intrarectal simian immunodeficiency virus SIV(mac251) challenge by a replication-competent Ad5hr-SIVenv/rev and Ad5hr-SIVgag recombinant priming/gp120 boosting regimen. J. Virol. 77: 8354-8365.
68. Zwick, M. B., R. Jensen, S. Church, et al. 2005. Anti-human immunodeficiency virus type 1 (HIV-1) antibodies 2F5 and 4E10 require surprisingly few crucial residues in the membrane-proximal external region of glycoprotein gp41 to neutralize HIV-1. J. Virol. 79:1252-1261.