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Journal of Biomedicine and Biotechnology
Volume 2011 (2011), Article ID 103924, 9 pages
http://dx.doi.org/10.1155/2011/103924
Review Article

Characterization of an Effective CTL Response against HIV and SIV Infections

Health Sciences Research Institute, Germans Trias i Pujol, 08916 Badalona, Spain

Received 1 July 2011; Accepted 1 August 2011

Academic Editor: Zhengguo Xiao

Copyright © 2011 Meritxell Genescà. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. P. Kiepiela, K. Ngumbela, C. Thobakgale et al., “CD8+ T-cell responses to different HIV proteins have discordant associations with viral load,” Nature Medicine, vol. 13, no. 1, pp. 46–53, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  2. Y. Riviere, M. B. McChesney, F. Porrot et al., “Gag-specific cytotoxic responses to HIV type 1 are associated with a decreased risk of progression to AIDS-related complex or AIDS,” AIDS Research and Human Retroviruses, vol. 11, no. 8, pp. 903–907, 1995. View at Scopus
  3. P. J. R. Goulder, C. Brander, Y. Tang et al., “Evolution and transmission of stable CTL escape mutations in HIV infection,” Nature, vol. 412, no. 6844, pp. 334–338, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  4. T. M. Allen, D. H. O'Connor, P. Jing et al., “Tat-specific cytotoxic T lymphocytes select for SIV escape variants during resolution of primary vimamia,” Nature, vol. 407, no. 6802, pp. 386–390, 2000. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  5. B. L. Shacklett and A. L. Ferre, “Mucosal immunity in HIV controllers: the right place at the right time,” Current Opinion in HIV and AIDS, vol. 6, no. 3, pp. 202–207, 2011. View at Publisher · View at Google Scholar · View at PubMed
  6. A. L. Ferre, P. W. Hunt, J. W. Critchfield et al., “Mucosal immune responses to HIV-1 in elite controllers: a potential correlate of immune control,” Blood, vol. 113, no. 17, pp. 3978–3989, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  7. A. R. Hersperger, J. N. Martin, L. Y. Shin et al., “Increased HIV-specific CD8+ T-cell cytotoxic potential in HIV elite controllers is associated with T-bet expression,” Blood, vol. 117, no. 14, pp. 3799–3808, 2011. View at Publisher · View at Google Scholar · View at PubMed
  8. A. Sáez-Cirión, C. Lacabaratz, O. Lambotte et al., “HIV controllers exhibit potent CD8 T cell capacity to suppress HIV infection ex vivo and peculiar cytotoxic T lymphocyte activation phenotype,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 16, pp. 6776–6781, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  9. J. E. Schmitz, M. J. Kuroda, S. Santra et al., “Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes,” Science, vol. 283, no. 5403, pp. 857–860, 1999. View at Publisher · View at Google Scholar · View at Scopus
  10. X. Jin, D. E. Bauer, S. E. Tuttleton et al., “Dramatic rise in plasma viremia after CD8+ T cell depletion in simian immunodeficiency virus-infected macaques,” Journal of Experimental Medicine, vol. 189, no. 6, pp. 991–998, 1999. View at Publisher · View at Google Scholar · View at Scopus
  11. T. Gaufin, R. M. Ribeiro, R. Gautam et al., “Experimental depletion of CD8+ cells in acutely SIVagm-Infected African Green Monkeys results in increased viral replication,” Retrovirology, vol. 7, article 42, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  12. M. Genescà, M. B. McChesney, and C. J. Miller, “Antiviral CD8+ T cells in the genital tract control viral replication and delay progression to AIDS after vaginal SIV challenge in rhesus macaques immunized with virulence attenuated SHIV 89.6,” Journal of Internal Medicine, vol. 265, no. 1, pp. 67–77, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  13. J. M. Greene, J. J. Lhost, B. J. Burwitz et al., “Extralymphoid CD8+ T cells resident in tissue from simian immunodeficiency virus SIVmac239△nef-vaccinated macaques suppress SIVmac239 replication ex vivo,” The Journal of Virology, vol. 84, no. 7, pp. 3362–3372, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  14. M. J. McElrath, S. C. De Rosa, Z. Moodie et al., “HIV-1 vaccine-induced immunity in the test-of-concept Step Study: a case-cohort analysis,” The Lancet, vol. 372, no. 9653, pp. 1894–1905, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. T. Demberg and M. Robert-Guroff, “Mucosal immunity and protection against HIV/SIV infection: strategies and challenges for vaccine design,” International Reviews of Immunology, vol. 28, no. 1-2, pp. 20–48, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  16. J. R. Almeida, D. Sauce, D. A. Price et al., “Antigen sensitivity is a major determinant of CD8+ T-cell polyfunctionality and HIV-suppressive activity,” Blood, vol. 113, no. 25, pp. 6351–6360, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  17. V. Appay, R. A. W. Van Lier, F. Sallusto, and M. Roederer, “Phenotype and function of human T lymphocyte subsets: consensus and issues,” Cytometry Part A, vol. 73, no. 11, pp. 975–983, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  18. M. C. Iglesias, J. R. Almeida, S. Fastenackels, et al., “Escape from highly effective public CD8+ T-cell clonotypes by HIV,” Blood, vol. 118, no. 8, pp. 2138–2149, 2011.
  19. Q. Li, P. J. Skinner, S. J. Ha et al., “Visualizing antigen-specific and infected cells in situ predicts outcomes in early viral infection,” Science, vol. 323, no. 5922, pp. 1726–1729, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  20. H. Streeck, Z. L. Brumme, M. Anastario et al., “Antigen load and viral sequence diversification determine the functional profile of HIV-1-specific CD8+ T cells,” PLoS Medicine, vol. 5, no. 5, article e100, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  21. S. G. Hansen, J. C. Ford, M. S. Lewis et al., “Profound early control of highly pathogenic SIV by an effector memory T-cell vaccine,” Nature, vol. 473, no. 7348, pp. 523–527, 2011. View at Publisher · View at Google Scholar · View at PubMed
  22. S. A. Migueles, C. M. Osborne, C. Royce et al., “Lytic granule loading of CD8+ T cells is required for HIV-infected cell elimination associated with immune control,” Immunity, vol. 29, no. 6, pp. 1009–1021, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  23. B. Poonia, C. D. Pauza, and M. S. Salvato, “Role of the Fas/FasL pathway in HIV or SIV disease,” Retrovirology, vol. 6, article 91, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  24. M. Genescà, P. J. Skinner, J. H. Jung et al., “With minimal systemic T-cell expansion, CD8+ T cells mediate protection of rhesus macaques immunized with attenuated simian-human immunodeficiency virus SHIV89.6 from vaginal challenge with simian immunodeficiency virus,” The Journal of Virology, vol. 82, no. 22, pp. 11181–11196, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  25. E. Rollman, M. Z. Smith, A. G. Brooks et al., “Killing kinetics of simian immunodeficiency virus-specific CD8+ T cells: implications for HIV vaccine strategies,” Journal of Immunology, vol. 179, no. 7, pp. 4571–4579, 2007. View at Scopus
  26. B. L. Shacklett, J. W. Critchfield, A. L. Ferre, and T. L. Hayes, “Mucosal T-cell responses to HIV: responding at the front lines,” Journal of Internal Medicine, vol. 265, no. 1, pp. 58–66, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  27. P. Wolint, M. R. Betts, R. A. Koup, and A. Oxenius, “Immediate cytotoxicity but not degranulation distinguishes effector and memory subsets of CD8+ T cells,” Journal of Experimental Medicine, vol. 199, no. 7, pp. 925–936, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  28. M. R. Betts and R. A. Koup, “Detection of T-cell degranulation: CD107a and b,” Methods in Cell Biology, vol. 2004, no. 75, pp. 497–512, 2004. View at Scopus
  29. M. R. Betts, M. C. Nason, S. M. West et al., “HIV nonprogressors preferentially maintain highly functional HIV-specific CD8+ T cells,” Blood, vol. 107, no. 12, pp. 4781–4789, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  30. M. Genescà, T. Rourke, J. Li et al., “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,” Journal of Immunology, vol. 179, no. 7, pp. 4732–4740, 2007. View at Scopus
  31. M. R. Betts and A. Harari, “Phenotype and function of protective T cell immune responses in HIV,” Current Opinion in HIV and AIDS, vol. 3, no. 3, pp. 349–355, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  32. D. A. Price, T. E. Asher, N. A. Wilson et al., “Public clonotype usage identifies protective gag-specific CD8+ t cell responses in SIV infection,” Journal of Experimental Medicine, vol. 206, no. 4, pp. 923–936, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  33. C. L. Althaus and R. J. De Boer, “Dynamics of immune escape during HIV/SIV infection,” PLoS Computational Biology, vol. 4, no. 7, Article ID e1000103, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  34. M. R. Betts, D. A. Price, J. M. Brenchley et al., “The functional profile of primary human antiviral CD8+ T cell effector activity is dictated by cognate peptide concentration,” Journal of Immunology, vol. 172, no. 10, pp. 6407–6417, 2004. View at Scopus
  35. I. M. Belyakov, D. Isakov, Q. Zhu, A. Dzutsev, and J. A. Berzofsky, “A novel functional CTL avidity/activity compartmentalization to the site of mucosal immunization contributes to protection of macaques against simian/human immunodeficiency viral depletion of mucosal CD4+ T cells,” Journal of Immunology, vol. 178, no. 11, pp. 7211–7221, 2007. View at Scopus
  36. C. T. Berger, N. Frahm, D. A. Price et al., “High-functional-avidity cytotoxic T lymphocyte responses to HLA-B-restricted Gag-derived epitopes associated with relative HIV control,” Journal of Virology, vol. 85, no. 18, pp. 9334–9345, 2011. View at Publisher · View at Google Scholar · View at PubMed
  37. H. T. Jin, R. Ahmed, and T. Okazaki, “Role of PD-1 in regulating T-cell immunity,” Current Topics in Microbiology and Immunology, vol. 350, pp. 17–37, 2011.
  38. S. D. Blackburn, H. Shin, W. N. Haining et al., “Coregulation of CD8+ T cell exhaustion by multiple inhibitory receptors during chronic viral infection,” Nature Immunology, vol. 10, no. 1, pp. 29–37, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  39. M. Quigley, F. Pereyra, B. Nilsson et al., “Transcriptional analysis of HIV-specific CD8+ T cells shows that PD-1 inhibits T cell function by upregulating BATF,” Nature Medicine, vol. 16, no. 10, pp. 1147–1151, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  40. V. Velu, K. Titanji, B. Zhu et al., “Enhancing SIV-specific immunity in vivo by PD-1 blockade,” Nature, vol. 458, no. 7235, pp. 206–210, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  41. S. M. Henson, O. Franzese, R. Macaulay et al., “KLRG1 signaling induces defective Akt (ser473) phosphorylation and proliferative dysfunction of highly differentiated CD8+ T cells,” Blood, vol. 113, no. 26, pp. 6619–6628, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  42. S. Koch, A. Larbi, E. Derhovanessian, D. Özcelik, E. Naumova, and G. Pawelec, “Multiparameter flow cytometric analysis of CD4 and CD8 T cell subsets in young and old people,” Immunity and Ageing, vol. 5, article 6, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  43. J. M. Brenchley, N. J. Karandikar, M. R. Betts et al., “Expression of CD57 defines replicative senescence and antigen-induced apoptotic death of CD8+ T cells,” Blood, vol. 101, no. 7, pp. 2711–2720, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  44. P. K. Chattopadhyay, M. R. Betts, D. A. Price et al., “The cytolytic enzymes granyzme A, granzyme B, and perforin: expression patterns, cell distribution, and their relationship to cell maturity and bright CD57 expression,” Journal of Leukocyte Biology, vol. 85, no. 1, pp. 88–97, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  45. Y. Le Priol, D. Puthier, C. Lécureuil et al., “High cytotoxic and specific migratory potencies of senescent CD8+CD57+ cells in HIV-infected and uninfected individuals,” Journal of Immunology, vol. 177, no. 8, pp. 5145–5154, 2006.
  46. H. Streeck, D. S. Kwon, A. Pyo et al., “Epithelial adhesion molecules can inhibit HIV-1-specific CD8+ T-cell functions,” Blood, vol. 117, no. 19, pp. 5112–5122, 2011. View at Publisher · View at Google Scholar · View at PubMed
  47. C. Petrovas, B. Chaon, D. R. Ambrozak et al., “Differential association of programmed death-1 and CD57 with ex vivo survival of CD8+ T cells in HIV infection,” Journal of Immunology, vol. 183, no. 2, pp. 1120–1132, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  48. G. Breton, B. Yassine-Diab, L. Cohn et al., “SiRNA knockdown of PD-L1 and PD-L2 in monocyte-derived dendritic cells only modestly improves proliferative responses to gag by CD8+ T cells from HIV-1-infected individuals,” Journal of Clinical Immunology, vol. 29, no. 5, pp. 637–645, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  49. K. Newton and A. Strasser, “Cell death control in lymphocytes,” Advances in Immunology, vol. 76, pp. 179–226, 2000. View at Scopus
  50. A. V. Gett, F. Sallusto, A. Lanzavecchia, and J. Geginat, “T cell fitness determined by signal strength,” Nature Immunology, vol. 4, no. 4, pp. 355–360, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  51. J. V. Giorgi, H.-N. Ho, K. Hirji et al., “CD8+ lymphocyte activation at human immunodeficiency virus type 1 seroconversion: development of HLA-DR+ CD38- CD8+ cells is associated with subsequent stable CD4+ cell levels,” Journal of Infectious Diseases, vol. 170, no. 4, pp. 775–781, 1994.
  52. J. V. Giorgi, “Phenotype and function of T cells in HIV disease,” in Immunology of HIV Infection, S. Gupta, Ed., pp. 181–199, Plenum Press, New York, NY, USA, 1996.
  53. M. Genescà, J. Li, L. Fritts et al., “Depo-Provera abrogates attenuated lentivirus-induced protection in male rhesus macaques challenged intravenously with pathogenic SIVmac239,” Journal of Medical Primatology, vol. 36, no. 4-5, pp. 266–275, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  54. J. D. Miller, R. G. van der Most, R. S. Akondy et al., “Human effector and memory CD8+ T cell responses to smallpox and yellow fever vaccines,” Immunity, vol. 28, no. 5, pp. 710–722, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  55. F. Hladik and M. J. McElrath, “Setting the stage: host invasion by HIV,” Nature Reviews Immunology, vol. 8, no. 6, pp. 447–457, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  56. B. F. Keele, H. Li, G. H. Learn et al., “Low-dose rectal inoculation of rhesus macaques by SIVsmE660 or SIVmac251 recapitulates human mucosal infection by HIV-1,” Journal of Experimental Medicine, vol. 206, no. 5, pp. 1117–1134, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  57. C. J. Miller, Q. Li, K. Abel et al., “Propagation and dissemination of infection after vaginal transmission of simian immunodeficiency virus,” The Journal of Virology, vol. 79, no. 14, pp. 9217–9227, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  58. F. Sallusto, J. Geginat, and A. Lanzavecchia, “Central memory and effector memory T cell subsets: function, generation, and maintenance,” Annual Review of Immunology, vol. 22, pp. 745–763, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  59. S. G. Hansen, C. Vieville, N. Whizin et al., “Effector memory T cell responses are associated with protection of rhesus monkeys from mucosal simian immunodeficiency virus challenge,” Nature Medicine, vol. 15, no. 3, pp. 293–299, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  60. M. Genescà and C. J. Miller, “Use of nonhuman primate models to develop mucosal AIDS vaccines,” Current HIV/AIDS Reports, vol. 7, no. 1, pp. 19–27, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  61. R. M. Zinkernagel, “On natural and artificial vaccinations,” Annual Review of Immunology, vol. 21, pp. 515–546, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  62. M. Jeyanathan, J. Mu, S. McCormick et al., “Murine airway luminal antituberculosis memory CD8 T cells by mucosal immunization are maintained via antigen-driven in situ proliferation, independent of peripheral T cell recruitment,” American Journal of Respiratory and Critical Care Medicine, vol. 181, no. 8, pp. 862–872, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  63. B. F. Haynes and R. J. Shattock, “Critical issues in mucosal immunity for HIV-1 vaccine development,” Journal of Allergy and Clinical Immunology, vol. 122, no. 1, pp. 3–9, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  64. B. D. Walker and D. R. Burton, “Toward an AIDS vaccine,” Science, vol. 320, no. 5877, pp. 760–764, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  65. S. Rerks-Ngarm, P. Pitisuttithum, S. Nitayaphan et al., “Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand,” The New England Journal of Medicine, vol. 361, no. 23, pp. 2209–2220, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  66. K. Abel, L. Compton, T. Rourke et al., “Simian-human immunodeficiency virus SHIV89.6-induced protection against intravaginal challenge with pathogenic SIVmac239 is independent of the route of immunization and is associated with a combination of cytotoxic T-lymphocyte and alpha interferon responses,” The Journal of Virology, vol. 77, no. 5, pp. 3099–3118, 2003. View at Publisher · View at Google Scholar · View at Scopus
  67. R. P. Johnson and R. C. Desrosiers, “Protective immunity induced by live attenuated simian immunodeficiency virus,” Current Opinion in Immunology, vol. 10, no. 4, pp. 436–443, 1998. View at Publisher · View at Google Scholar · View at Scopus
  68. B. L. Lohman, M. B. McChesney, C. J. Miller et al., “A partially attenuated simian immunodeficiency virus induces host immunity that correlates with resistance to pathogenic virus challenge,” The Journal of Virology, vol. 68, no. 11, pp. 7021–7029, 1994. View at Scopus
  69. T. H. Mogensen, J. Melchjorsen, C. S. Larsen, and S. R. Paludan, “Innate immune recognition and activation during HIV infection,” Retrovirology, vol. 7, article 54, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  70. I. Pandrea, T. Gaufin, J. M. Brenchley et al., “Cutting edge: experimentally induced immune activation in natural hosts of simian immunodeficiency virus induces significant increases in viral replication and CD4+ T cell depletion,” Journal of Immunology, vol. 181, no. 10, pp. 6687–6691, 2008. View at Scopus
  71. R. E. Owen, J. W. Heitman, D. F. Hirschkorn et al., “HIV+ elite controllers have low HIV-specific T-cell activation yet maintain strong, polyfunctional T-cell responses,” AIDS, vol. 24, no. 8, pp. 1095–1105, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  72. M. Stone, Z. M. Ma, M. Genescà et al., “Limited dissemination of pathogenic SIV after vaginal challenge of rhesus monkeys immunized with a live, attenuated lentivirus,” Virology, vol. 392, no. 2, pp. 260–270, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  73. M. Genescà, P. J. Skinner, K. M. Bost, D. Lu, et al., “Protective attenuated lentivirus immunization induces SIV-specific T cells in the genital tract of rhesus monkeys,” Mucosal Immunology, vol. 1, no. 3, pp. 219–228, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  74. A. L. Ferre, P. W. Hunt, D. H. McConnell et al., “HIV controllers with HLA-DRB113 and HLA-DQB106 alleles have strong, polyfunctional mucosal CD4+ T-cell responses,” The Journal of Virology, vol. 84, no. 21, pp. 11020–11029, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  75. S. A. Kalams and B. D. Walker, “The critical need for CD4 help in maintaining effective cytotoxic T lymphocyte responses,” Journal of Experimental Medicine, vol. 188, no. 12, pp. 2199–2204, 1998. View at Publisher · View at Google Scholar · View at Scopus
  76. J. Estaquier and J. J. Zaunders, “Cytokines and the pathogenesis of HIV infection,” European Cytokine Network, vol. 21, no. 3, pp. 195–196, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  77. A. Viola, B. Molon, and R. L. Contento, “Chemokines: coded messages for T-cell missions,” Frontiers in Bioscience, vol. 13, pp. 6341–6353, 2008. View at Scopus
  78. J. T. Harty and V. P. Badovinac, “Shaping and reshaping CD8+ T-cell memory,” Nature Reviews Immunology, vol. 8, no. 2, pp. 107–119, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  79. B. Jacquelin, V. Mayau, B. Targat et al., “Nonpathogenic SIV infection of African green monkeys induces a strong but rapidly controlled type I IFN response,” The Journal of Clinical Investigation, vol. 119, no. 12, pp. 3544–3555, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  80. G. Zelinskyy, K. K. Dietze, Y. P. Hüsecken et al., “The regulatory T-cell response during acute retroviral infection is locally defined and controls the magnitude and duration of the virus-specific cytotoxic T-cell response,” Blood, vol. 114, no. 15, pp. 3199–3207, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  81. C. M. Card, P. J. McLaren, C. Wachihi, J. Kimani, F. A. Plummer, and K. R. Fowke, “Decreased immune activation in resistance to HIV-1 infection is associated with an elevated frequency of CD8+CD25+FOXP3+ regulatory T rells,” Journal of Infectious Diseases, vol. 199, no. 9, pp. 1318–1322, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  82. S. N. Gordon, N. R. Klatt, S. E. Bosinger et al., “Severe depletion of mucosal CD4+ T cells in AIDS-free simian immunodeficiency virus-infected sooty mangabeys,” Journal of Immunology, vol. 179, no. 5, pp. 3026–3034, 2007. View at Scopus
  83. I. Pandrea, C. Apetrei, J. Dufour et al., “Simian immunodeficiency virus SIVagm.sab infection of Caribbean African green monkeys: a new model for the study of SIV pathogenesis in natural hosts,” The Journal of Virology, vol. 80, no. 10, pp. 4858–4867, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  84. I. V. Pandrea, R. Gautam, R. M. Ribeiro et al., “Acute loss of intestinal CD4+ T cells is not predictive of simian immunodeficiency virus virulence,” Journal of Immunology, vol. 179, no. 5, pp. 3035–3046, 2007. View at Scopus
  85. K. A. Kraynyak, M. A. Kutzler, N. J. Cisper et al., “Systemic immunization with CCL27/CTACK modulates immune responses at mucosal sites in mice and macaques,” Vaccine, vol. 28, no. 8, pp. 1942–1951, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus