1887

Abstract

The X4-tropic simian/human immunodeficiency virus (SHIV) 89.6P (or 89.6PD) causes rapid CD4 T-cell depletion leading to an acute crash of the host immune system, whereas pathogenic R5-tropic simian immunodeficiency virus (SIV) infection, like HIV-1 infection in humans, results in chronic disease progression in macaques. Recent pre-clinical vaccine trials inducing cytotoxic T lymphocyte (CTL) responses have succeeded in controlling replication of the former but shown difficulty in control of the latter. Analysis of the immune responses involved in consistent control of SHIV would contribute to elucidation of the mechanism for consistent control of SIV replication. This study followed up rhesus macaques that showed vaccine-based control of primary SHIV89.6PD replication and found that all of these controllers maintained viraemia control for more than 2 years. SHIV89.6PD control was observed in vaccinees of diverse major histocompatibility complex (MHC) haplotypes and was maintained without rapid selection of CTL escape mutations, a sign of particular CTL pressure. Despite the vaccine regimen not targeting Env, all of the SHIV controllers showed efficient elicitation of neutralizing antibodies by 6 weeks post-challenge. These results contrast with our previous observation of particular MHC-associated control of SIV replication without involvement of neutralizing antibodies and suggest that vaccine-based control of SHIV89.6PD replication can be stably maintained in the presence of multiple functional immune effectors.

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2007-02-01
2024-03-29
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References

  1. Albritton L. M., Tseng L., Scadden D., Cunningham J. M. 1989; A putative murine ecotropic retrovirus receptor gene encodes a multiple membrane-spanning protein and confers susceptibility to virus infection. Cell 57:659–666 [CrossRef]
    [Google Scholar]
  2. Amara R. R., Villinger F., Altman J. D., Lydy S. L., O'Neil S. P., Staprans S. I., Montefiori D. C., Xu Y., Herndon J. G. other authors 2001; Control of a mucosal challenge and prevention of AIDS by a multiprotein DNA/MVA vaccine. Science 292:69–74 [CrossRef]
    [Google Scholar]
  3. Amara R. R., Smith J. M., Staprans S. I., Montefiori D. C., Villinger F., Altman J. D., O'Neil S. P., Kozyr N. L., Xu Y. other authors 2002; Critical role for Env as well as Gag-Pol in control of a simian-human immunodeficiency virus 89.6P challenge by a DNA prime/recombinant modified vaccinia virus Ankara vaccine. J Virol 76:6138–6146 [CrossRef]
    [Google Scholar]
  4. Arguello J. R., Little A. M., Pay A. L., Gallardo D., Rojas I., Marsh S. G., Goldman J. M., Madrigal J. A. 1998; Mutation detection and typing of polymorphic loci through double-strand conformation analysis. Nat Genet 18:192–194 [CrossRef]
    [Google Scholar]
  5. Barouch D. H., Santra S., Schmitz J. E., Kuroda M. J., Fu T. M., Wagner W., Bilska M., Craiu A., Zheng X. X. other authors 2000; Control of viremia and prevention of clinical AIDS in rhesus monkeys by cytokine-augmented DNA vaccination. Science 290:486–492 [CrossRef]
    [Google Scholar]
  6. Borrow P., Lewicki H., Hahn B. H., Shaw G. M., Oldstone M. B. 1994; Virus-specific CD8+ cytotoxic T-lymphocyte activity associated with control of viremia in primary human immunodeficiency virus type 1 infection. J Virol 68:6103–6110
    [Google Scholar]
  7. Borrow P., Lewicki H., Wei X., Horwitz M. S., Peffer N., Meyers H., Nelson J. A., Gairin J. E., Hahn B. H. other authors 1997; Antiviral pressure exerted by HIV-1-specific cytotoxic T lymphocytes (CTL) during primary infection demonstrated by rapid selection of CTL escape virus. Nat Med 3:205–211 [CrossRef]
    [Google Scholar]
  8. Casimiro D. R., Wang F., Schleif W. A., Liang X., Zhang Z. Q., Tobery T. W., Davies M. E., McDermott A. B., O'Connor D. H. other authors 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 [CrossRef]
    [Google Scholar]
  9. Feinberg M. B., Moore J. P. 2002; AIDS vaccine models: challenging challenge viruses. Nat Med 8:207–210 [CrossRef]
    [Google Scholar]
  10. Goulder P. J., Watkins D. I. 2004; HIV and SIV CTL escape: implications for vaccine design. Nat Rev Immunol 4:630–640 [CrossRef]
    [Google Scholar]
  11. Goulder P. J., Phillips R. E., Colbert R. A., McAdam S., Ogg G., Nowak M. A., Giangrande P., Luzzi G., Morgan B. other authors 1997; Late escape from an immunodominant cytotoxic T-lymphocyte response associated with progression to AIDS. Nat Med 3:212–217 [CrossRef]
    [Google Scholar]
  12. Horton H., Vogel T. U., Carter D. K., Vielhuber K., Fuller D. H., Shipley T., Fuller J. T., Kunstman K. J., Sutter G. other authors 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 [CrossRef]
    [Google Scholar]
  13. Jin X., Bauer D. E., Tuttleton S. E., Lewin S., Gettie A., Blanchard J., Irwin C. E., Safrit J. T., Mittler J. other authors 1999; Dramatic rise in plasma viremia after CD8+ T cell depletion in simian immunodeficiency virus-infected macaques. J Exp Med 189:991–998 [CrossRef]
    [Google Scholar]
  14. Kano M., Matano T., Kato A., Nakamura H., Takeda A., Suzaki Y., Ami Y., Terao K., Nagai Y. 2002; Primary replication of a recombinant Sendai virus vector in macaques. J Gen Virol 83:1377–1386
    [Google Scholar]
  15. Kato A., Sakai Y., Shioda T., Kondo T., Nakanishi M., Nagai Y. 1996; Initiation of Sendai virus multiplication from transfected cDNA or RNA with negative or positive sense. Genes Cells 1:569–579 [CrossRef]
    [Google Scholar]
  16. Kawada M., Igarashi H., Takeda A., Tsukamoto T., Yamamoto H., Dohki S., Takiguchi M., Matano T. 2006; Involvement of multiple epitope-specific cytotoxic T-lymphocyte responses in vaccine-based control of simian immunodeficiency virus replication in rhesus macaques. J Virol 80:1949–1958 [CrossRef]
    [Google Scholar]
  17. Koup R. A., Safrit J. T., Cao Y., Andrews C. A., McLeod G., Borkowsky W., Farthing C., Ho D. D. 1994; Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J Virol 68:4650–4655
    [Google Scholar]
  18. Letvin N. L., Mascola J. R., Sun Y., Gorgone D. A., Buzby A. P., Xu L., Yang Z. Y., Chakrabarti B., Rao S. S. other authors 2006; Preserved CD4+ central memory T cells and survival in vaccinated SIV-challenged monkeys. Science 312:1530–1533 [CrossRef]
    [Google Scholar]
  19. Li H. O., Zhu Y. F., Asakawa M., Kuma H., Hirata T., Ueda Y., Lee Y. S., Fukumura M., Iida A. other authors 2000; A cytoplasmic RNA vector derived from nontransmissible Sendai virus with efficient gene transfer and expression. J Virol 74:6564–6569 [CrossRef]
    [Google Scholar]
  20. Li Q., Duan L., Estes J. D., Ma Z. M., Rourke T., Wang Y., Reilly C., Carlis J., Miller C. J., Haase A. T. 2005; Peak SIV replication in resting memory CD4+ T cells depletes gut lamina propria CD4+ T cells. Nature 434:1148–1152
    [Google Scholar]
  21. Lu Y., Pauza C. D., Lu X., Montefiori D. C., Miller C. J. 1998; Rhesus macaques that become systemically infected with pathogenic SHIV 89.6-PD after intravenous, rectal, or vaginal inoculation and fail to make an antiviral antibody response rapidly develop AIDS. J Acquir Immune Defic Syndr Hum Retrovirol 19:6–18 [CrossRef]
    [Google Scholar]
  22. Matano T., Shibata R., Siemon C., Connors M., Lane H. C., Martin M. A. 1998; Administration of an anti-CD8 monoclonal antibody interferes with the clearance of chimeric simian/human immunodeficiency virus during primary infections of rhesus macaques. J Virol 72:164–169
    [Google Scholar]
  23. Matano T., Kano M., Odawara T., Nakamura H., Takeda A., Mori K., Sato T., Nagai Y. 2000; Induction of protective immunity against pathogenic simian immunodeficiency virus by a foreign receptor-dependent replication of an engineered avirulent virus. Vaccine 18:3310–3318 [CrossRef]
    [Google Scholar]
  24. Matano T., Kano M., Nakamura H., Takeda A., Nagai Y. 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 [CrossRef]
    [Google Scholar]
  25. Matano T., Kobayashi M., Igarashi H., Takeda A., Nakamura H., Kano M., Sugimoto C., Mori K., Iida A. other authors 2004; Cytotoxic T lymphocyte-based control of simian immunodeficiency virus replication in a preclinical AIDS vaccine trial. J Exp Med 199:1709–1718 [CrossRef]
    [Google Scholar]
  26. Mattapallil J. J., Douek D. C., Hill B., Nishimura Y., Martin M. A., Roederer M. 2005; Massive infection and loss of memory CD4+ T cells in multiple tissues during acute SIV infection. Nature 434:1093–1097 [CrossRef]
    [Google Scholar]
  27. Mattapallil J. J., Douek D. C., Buckler-White A., Montefiori D. C., Letvin N. L., Nabel G. J., Roederer M. 2006; Vaccination preserves CD4 memory T cells during acute simian immunodeficiency virus challenge. J Exp Med 203:1533–1541 [CrossRef]
    [Google Scholar]
  28. McMichael A. J., Hanke T. 2003; HIV vaccines 1983–2003. Nat Med 9:874–880 [CrossRef]
    [Google Scholar]
  29. Nishimura Y., Igarashi T., Donau O. K., Buckler-White A., Buckler C., Lafont B. A., Goeken R. M., Goldstein S., Hirsch V. M., Martin M. A. 2004; Highly pathogenic SHIVs and SIVs target different CD4+ T cell subsets in rhesus monkeys, explaining their divergent clinical courses. Proc Natl Acad Sci U S A 101:12324–12329 [CrossRef]
    [Google Scholar]
  30. Nishimura Y., Brown C. R., Mattapallil J. J., Igarashi T., Buckler-White A., Lafont B. A., Hirsch V. M., Roederer M., Martin M. A. 2005; Resting naive CD4+ T cells are massively infected and eliminated by X4-tropic simian-human immunodeficiency viruses in macaques. Proc Natl Acad Sci U S A 102:8000–8005 [CrossRef]
    [Google Scholar]
  31. Ogg G. S., Jin X., Bonhoeffer S., Dunbar P. R., Nowak M. A., Monard S., Segal J. P., Cao Y., Rowland-Jones S. L. other authors 1998; Quantitation of HIV-1-specific cytotoxic T lymphocytes and plasma load of viral RNA. Science 279:2103–2106 [CrossRef]
    [Google Scholar]
  32. Picker L. J., Watkins D. I. 2005; HIV pathogenesis: the first cut is the deepest. Nat Immunol 6:430–432 [CrossRef]
    [Google Scholar]
  33. Picker L. J., Hagen S. I., Lum R., Reed-Inderbitzin E. F., Daly L. M., Sylwester A. W., Walker J. M., Siess D. C., Piatak M. Jr other authors 2004; Insufficient production and tissue delivery of CD4+ memory T cells in rapidly progressive simian immunodeficiency virus infection. J Exp Med 200:1299–1314 [CrossRef]
    [Google Scholar]
  34. Price D. A., Goulder P. J., Klenerman P., Sewell A. K., Easterbrook P. J., Troop M., Bangham C. R., Phillips R. E. 1997; Positive selection of HIV-1 cytotoxic T lymphocyte escape variants during primary infection. Proc Natl Acad Sci U S A 94:1890–1895 [CrossRef]
    [Google Scholar]
  35. Rasmussen R. A., Hofmann-Lehmann R., Li P. L., Vlasak J., Schmitz J. E., Reimann K. A., Kuroda M. J., Letvin N. L., Montefiori D. C. other authors 2002; Neutralizing antibodies as a potential secondary protective mechanism during chronic SHIV infection in CD8+ T-cell-depleted macaques. AIDS 16:829–838 [CrossRef]
    [Google Scholar]
  36. Reimann K. A., Li J. T., Veazey R., Halloran M., Park I. W., Karlsson G. B., Sodroski J., Letvin N. L. 1996; A chimeric simian/human immunodeficiency virus expressing a primary patient human immunodeficiency virus type 1 isolate env causes an AIDS-like disease after in vivo passage in rhesus monkeys. J Virol 70:6922–6928
    [Google Scholar]
  37. Rose N. F., Marx P. A., Luckay A., Nixon D. F., Moretto W. J., Donahoe S. M., Montefiori D., Roberts A., Buonocore L., Rose J. K. 2001; An effective AIDS vaccine based on live attenuated vesicular stomatitis virus recombinants. Cell 106:539–549 [CrossRef]
    [Google Scholar]
  38. Sadagopal S., Amara R. R., Montefiori D. C., Wyatt L. S., Staprans S. I., Kozyr N. L., McClure H. M., Moss B., Robinson H. L. 2005; Signature for long-term vaccine-mediated control of a simian and human immunodeficiency virus 89.6P challenge: stable low-breadth and low-frequency T-cell response capable of coproducing gamma interferon and interleukin-2. J Virol 79:3243–3253 [CrossRef]
    [Google Scholar]
  39. Schmitz J. E., Kuroda M. J., Santra S., Sasseville V. G., Simon M. A., Lifton M. A., Racz P., Tenner-Racz K., Dalesandro M. other authors 1999; Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes. Science 283:857–860 [CrossRef]
    [Google Scholar]
  40. Shibata R., Maldarelli F., Siemon C., Matano T., Parta M., Miller G., Fredrickson T., Martin M. A. 1997a; Infection and pathogenicity of chimeric simian-human immunodeficiency viruses in macaques: determinants of high virus loads and CD4 cell killing. J Infect Dis 176:362–373 [CrossRef]
    [Google Scholar]
  41. Shibata R., Siemon C., Czajak S. C., Desrosiers R. C., Martin M. A. 1997b; Live, attenuated simian immunodeficiency virus vaccines elicit potent resistance against a challenge with a human immunodeficiency virus type 1 chimeric virus. J Virol 71:8141–8148
    [Google Scholar]
  42. Shiver J. W., Fu T. M., Chen L., Casimiro D. R., Davies M. E., Evans R. K., Zhang Z. Q., Simon A. J., Trigona W. L. other authors 2002; Replication-incompetent adenoviral vaccine vector elicits effective anti-immunodeficiency-virus immunity. Nature 415:331–335 [CrossRef]
    [Google Scholar]
  43. Takeda A., Igarashi H., Nakamura H., Kano M., Iida A., Hirata T., Hasegawa M., Nagai Y., Matano T. 2003; Protective efficacy of an AIDS vaccine, a single DNA-priming followed by a single booster with a recombinant replication-defective Sendai virus vector, in a macaque AIDS model. J Virol 77:9710–9715 [CrossRef]
    [Google Scholar]
  44. Willey R. L., Byrum R., Piatak M., Kim Y. B., Cho M. W., Rossio J. L., Bess J., Jr, Igarashi T., Endo Y. other authors 2003; Control of viremia and prevention of simian-human immunodeficiency virus-induced disease in rhesus macaques immunized with recombinant vaccinia viruses plus inactivated simian immunodeficiency virus and human immunodeficiency virus type 1 particles. J Virol 77:1163–1174 [CrossRef]
    [Google Scholar]
  45. Wilson N. A., Reed J., Napoe G. S., Piaskowski S., Szymanski A., Furlott J., Gonzalez E. J., Yant L. J., Maness N. J. Jr other authors 2006; Vaccine-induced cellular immune responses reduce plasma viral concentrations after repeated low-dose challenge with pathogenic simian immunodeficiency virus SIVmac239. J Virol 80:5875–5885 [CrossRef]
    [Google Scholar]
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