Differences in HIV-specific T cell responses between HIV-exposed and -unexposed HIV-seronegative individuals

Journal of Virology

Volumn 85, Issue 7, 2011, Pages 3507-3516

  Ritchie, Adam J ^a   Campion, Suzanne L ^a   Kopycinski, Jakub ^a,g   Moodie, Zoe ^b   Wang, Z Maggie ^b   Pandya, Kruti ^b   Moore, Stephen ^a   Liu, Michael K P ^a   Brackenridge, Simon ^a   Kuldanek, Kristin ^c   Legg, Kenneth ^c   Cohen, Myron S ^d   Delwart, Eric L ^e   Haynes, Barton F ^f   Fidler, Sarah ^c   McMichael, Andrew J ^a   Goonetilleke, Nilu ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b Fred Hutchinson Cancer Research Center   (United States)

^c ST MARY S HOSPITAL   (United Kingdom)

^d UNIVERSITY OF NORTH CAROLINA   (United States)

^e BLOOD SYSTEMS RESEARCH INSTITUTE   (United States)

^f DUKE UNIVERSITY MEDICAL CENTER   (United States)

^g IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR5; EPITOPE; HLA DR ANTIGEN;

ARTICLE; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CLINICAL ARTICLE; CONTROLLED STUDY; CROSS REACTION; FEMALE; GENE EXPRESSION; HOMOZYGOSITY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; MALE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL;

CD4-POSITIVE T-LYMPHOCYTES; CROSS REACTIONS; EPITOPES, T-LYMPHOCYTE; FEMALE; HIV ANTIBODIES; HIV INFECTIONS; HIV-1; HLA-DR ANTIGENS; HUMANS; MALE;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 79952604140     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02444-10     Document Type: Article

References (82)

1. Adams, S. L., R. A. Biti, and G. J. Stewart. 1997. T-cell response to HIV in natural infection: optimized culture conditions for detecting responses to gag peptides. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 15:257-263.
2. Alimonti, J. B., et al. 2006. Characterization of CD8 T-cell responses in HIV-1-exposed seronegative commercial sex workers from Nairobi, Kenya. Immunol. Cell Biol. 84:482-485.
3. Appay, V., et al. 2002. Persistent HIV-1-specific cellular responses despite prolonged therapeutic viral suppression. AIDS 16:161-170. (Pubitemid 34118562)
4. Barretina, J., et al. 2000. Evaluation of the putative role of C-C chemokines as protective factors of HIV-1 infection in seronegative hemophiliacs exposed to contaminated hemoderivatives. Transfusion 40:461-467. (Pubitemid 30230512)
5. Begaud, E., et al. 2006. Reduced CD4 T cell activation and in vitro susceptibility to HIV-1 infection in exposed uninfected Central Africans. Retrovirology 3:35.
6. Beretta, A., et al. 1996. HIV-1-specific immunity in persistently seronegative individuals at high risk for HIV infection. Immunol. Lett. 51:39-43.
7. Bernard, N. F., C. M. Yannakis, J. S. Lee, and C. M. Tsoukas. 1999. Human immunodeficiency virus (HIV)-specific cytotoxic T lymphocyte activity in HIV-exposed seronegative persons. J. Infect. Dis. 179:538-547.
8. Berzofsky, J. A., et al. 1991. Construction of peptides encompassing multi-determinant clusters of human immunodeficiency virus envelope to induce in vitro T cell responses in mice and humans of multiple MHC types. J. Clin. Invest. 88:876-884.
9. Boritz, E., E. L. Rapaport, T. B. Campbell, J. R. Koeppe, and C. C. Wilson. 2007. CD4+ T cell targeting of human immunodeficiency virus type 1 (HIV-1) peptide sequences present in vivo during chronic, progressive HIV-1 disease. Virology 361:34-44.
10. Campion, S., M. S. Cohen, A. J. McMichael, S. Galvin, and N. Goonetilleke. 2010. Improved detection of latent Mtb infection in HIV-1 seropositive individuals using cultured cellular assays. Eur. J. Immunol. doi:10.1002/eji.201040296.
11. Card, C. M., et al. 2009. Decreased immune activation in resistance to HIV-1 infection is associated with an elevated frequency of CD4(+)CD25 (+)FOXP3(+) regulatory T cells. J. Infect. Dis. 199:1318-1322.
12. Castelli, F. A., et al. 2008. Immunoprevalence of the CD4+ T-cell response to HIV Tat and Vpr proteins is provided by clustered and disperse epitopes, respectively. Eur. J. Immunol. 38:2821-2831.
13. Clerici, M., et al. 1992. Cell-mediated immune response to human immunodeficiency virus (HIV) type 1 in seronegative homosexual men with recent sexual exposure to HIV-1. J. Infect. Dis. 165:1012-1019.
14. Clerici, M., et al. 1989. Interleukin-2 production used to detect antigenic peptide recognition by T-helper lymphocytes from asymptomatic HIV-seropositive individuals. Nature 339:383-385. (Pubitemid 19144227)
15. Colf, L. A., et al. 2007. How a single T cell receptor recognizes both self and foreign MHC. Cell 129:135-146. (Pubitemid 46507586)
16. Corbet, S., et al. 2003. Optimization and immune recognition of multiple novel conserved HLA-A2, human immunodeficiency virus type 1-specific CTL epitopes. J. Gen. Virol. 84:2409-2421.
17. Currier, J. R., et al. 2002. A panel of MHC class I restricted viral peptides for use as a quality control for vaccine trial ELISPOT assays. J. Immunol. Methods 260:157-172. (Pubitemid 34132882)
18. Dean, M., et al. 1996. Genetic restriction of HIV-1 infection and progression to AIDS by a deletion allele of the CKR5 structural gene. Hemophilia Growth and Development Study, Multicenter AIDS Cohort Study, Multicenter Hemophilia Cohort Study, San Francisco City Cohort, ALIVE Study. Science 273:1856-1862. (Pubitemid 26322495)
19. De Groot, A. S., et al. 1991. Human immunodeficiency virus reverse transcriptase T helper epitopes identified in mice and humans: correlation with a cytotoxic T cell epitope. J. Infect. Dis. 164:1058-1065.
20. De Groot, A. S., et al. 2005. HIV vaccine development by computer assisted design: the GAIA vaccine. Vaccine 23:2136-2148. (Pubitemid 40341440)
21. Division of AIDS, National Institute of Allergy and Infectious Diseases. 20 November 2006, posting date. HPTN 052. A randomized trial to evaluate the effectiveness of antiretroviral therapy plus HIV primary care versus HIV primary care alone to prevent the sexual transmission of HIV-1 in serodiscordant couples. HIV Prevention Trials Network. http://www.hptn.org /research-studies/ hptn052.asp.
22. Dyer, W. B., et al. 2008. Mechanisms of HIV non-progression; robust and sustained CD4+ T-cell proliferative responses to p24 antigen correlate with control of viraemia and lack of disease progression after long-term transfusion-acquired HIV-1 infection. Retrovirology 5:112.
23. Erickson, A. L., et al. 2008. Potentially exposed but uninfected individuals produce cytotoxic and polyfunctional human immunodeficiency virus type 1-specific CD8(+) T-cell responses which can be defined to the epitope level. Clin. Vaccine Immunol. 15:1745-1748.
24. Fabio, G., et al. 1990. Susceptibility to HIV infection and AIDS in Italian haemophiliacs is HLA associated. Br. J. Haematol. 75:531-536.
25. Fonseca, S. G., et al. 2006. Identification of novel consensus CD4 T-cell epitopes from clade B HIV-1 whole genome that are frequently recognized by HIV-1 infected patients. AIDS 20:2263-2273. (Pubitemid 44789528)
26. Fowke, K. R., et al. 1996. Resistance to HIV-1 infection among persistently seronegative prostitutes in Nairobi, Kenya. Lancet 348:1347-1351. (Pubitemid 26383775)
27. Fox, J., and S. Fidler. 2010. Sexual transmission of HIV-1. Antiviral Res. 85:276-285.
28. Frahm, N., et al. 2004. Consistent cytotoxic-T-lymphocyte targeting of immunodominant regions in human immunodeficiency virus across multiple ethnicities. J. Virol. 78:2187-2200. (Pubitemid 38228912)
29. Gahery-Segard, H., et al. 2000. Multiepitopic B- and T-cell responses induced in humans by a human immunodeficiency virus type 1 lipopeptide vaccine. J. Virol. 74:1694-1703. (Pubitemid 30434025)
30. Geretti, A. M., C. A. Van Baalen, J. C. Borleffs, C. A. Van Els, and A. D. Osterhaus. 1994. Kinetics and specificities of the T helper-cell response to gp120 in the asymptomatic stage of HIV-1 infection. Scand. J. Immunol. 39:355-362.
31. Goh, W. C., et al. 1999. Protection against human immunodeficiency virus type 1 infection in persons with repeated exposure: evidence for T cell immunity in the absence of inherited CCR5 coreceptor defects. J. Infect. Dis. 179:548-557.
32. Goonetilleke, N., et al. 2006. Induction of multifunctional human immunodeficiency virus type 1 (HIV-1)-specific T cells capable of proliferation in healthy subjects by using a prime-boost regimen of DNA- and modified vaccinia virus Ankara-vectored vaccines expressing HIV-1 Gag coupled to CD8+ T-cell epitopes. J. Virol. 80:4717-4728.
33. Hale, P. M., et al. 1989. T cell multideterminant regions in the human immunodeficiency virus envelope: toward overcoming the problem of major histocompatibility complex restriction. Int. Immunol. 1:409-415.
34. Hasselrot, K., et al. 2009. Oral HIV-exposure elicits mucosal HIV-neutralizing antibodies in uninfected men who have sex with men. AIDS 23:329-333.
35. Hatano, H., et al. 2009. Evidence for persistent low-level viremia in individuals who control human immunodeficiency virus in the absence of antiretroviral therapy. J. Virol. 83:329-335.
36. Hladik, F., et al. 2003. Most highly exposed seronegative men lack HIV-1-specific, IFN-gamma-secreting T cells. J. Immunol. 171:2671-2683. (Pubitemid 37025581)
37. Hudgens, M. G. 2003. Estimating cumulative probabilities from incomplete longitudinal binary responses with application to HIV vaccine trials. Stat. Med. 22:463-479.
38. Kaufmann, D. E., et al. 2004. Comprehensive analysis of human immunodeficiency virus type 1-specific CD4 responses reveals marked immunodominance of gag and nef and the presence of broadly recognized peptides. J. Virol. 78:4463-4477. (Pubitemid 38501066)
39. Kaul, R., et al. 2001. CD8(+) lymphocytes respond to different HIV epitopes in seronegative and infected subjects. J. Clin. Invest. 107:1303-1310.
40. Kaul, R., et al. 2000. HIV-1-specific mucosal CD8+ lymphocyte responses in the cervix of HIV-1-resistant prostitutes in Nairobi. J. Immunol. 164:1602-1611. (Pubitemid 30067280)
41. Kebba, A., et al. 2004. HIV type 1 antigen-responsive CD4+ T-lymphocytes in exposed yet HIV type 1 seronegative Ugandans. AIDS Res. Hum. Retroviruses 20:67-75.
42. Koning, F. A., et al. 2004. Correlates of resistance to HIV-1 infection in homosexual men with high-risk sexual behaviour. AIDS 18:1117-1126. (Pubitemid 38738511)
43. Koning, F. A., et al. 2005. Low-level CD4+ T cell activation is associated with low susceptibility to HIV-1 infection. J. Immunol. 175:6117-6122. (Pubitemid 41508099)
44. Leitner, T., et al. 2005. HIV sequence compendium. Theoretical Biology and Biophysics Group, Los Alamos National Laboratory, Los Alamos, NM.
45. Liang, K.-Y., and S. L. Zeger. 1986. Longitudinal data analysis using generalized linear models. Biometrika 73:13-22.
46. Liu, R., et al. 1996. Homozygous defect in HIV-1 coreceptor accounts for resistance of some multiply-exposed individuals to HIV-1 infection. Cell 86:367-377. (Pubitemid 26272077)
47. Lo, W. L., et al. 2009. An endogenous peptide positively selects and augments the activation and survival of peripheral CD4+ T cells. Nat. Immunol. 10:1155-1161.
48. Lo Caputo, S., et al. 2003. Mucosal and systemic HIV-1-specific immunity in HIV-1-exposed but uninfected heterosexual men. AIDS 17:531-539. (Pubitemid 36293106)
49. Lubong Sabado, R., et al. 2009. In vitro priming recapitulates in vivo HIV-1 specific T cell responses, revealing rapid loss of virus reactive CD4 T cells in acute HIV-1 infection. PLoS One 4:e4256.
50. Makedonas, G., et al. 2002. HIV-specific CD8 T-cell activity in uninfected injection drug users is associated with maintenance of seronegativity. AIDS 16:1595-1602. (Pubitemid 34921104)
51. Mason, D. 1998. A very high level of crossreactivity is an essential feature of the T-cell receptor. Immunol. Today 19:395-404. (Pubitemid 28392279)
52. Mason, R. D., M. I. Bowmer, C. M. Howley, and M. D. Grant. 2005. Cross-reactive cytotoxic T lymphocytes against human immunodeficiency virus type 1 protease and gamma interferon-inducible protein 30. J. Virol. 79:5529-5536.
53. McElrath, M. J., et al. 2008. HIV-1 vaccine-induced immunity in the test-of-concept step study: a case-cohort analysis. Lancet 372:1894-1905.
54. Michael, N. 2010. Correlates of immunity: RV144 - lessons learned. Presented at the AIDS Vaccine Conference, Atlanta, GA. http://www .hivvaccineenterprise.org/conference-archive/2010/pdf-presentations/Friday/ Plenary-03/MichaelN.pdf.
55. Missale, G., et al. 2004. Parenteral exposure to high HIV viremia leads to virus-specific T cell priming without evidence of infection. Eur. J. Immunol. 34:3208-3215.
56. Moodie, Z., et al. 2010. Response definition criteria for ELISPOT assays revisited. Cancer Immunol. Immunother. 59:1489-1501.
57. Moser, J. M., et al. 2010. Optimization of a dendritic cell-based assay for the in vitro priming of naive human CD4+ T cells. J. Immunol. Methods 353:8-19.
58. Nicastri, E., et al. 1999. Reduction of IFN-gamma and IL-2 production by peripheral lymphocytes of HIV-exposed seronegative subjects. AIDS 13:1333-1336. (Pubitemid 29408447)
59. Pancre, V., et al. 2007. Presence of HIV-1 Nef specific CD4 T cell response is associated with non-progression in HIV-1 infection. Vaccine 25:5927-5937. (Pubitemid 47043215)
60. Perez, C. L., K. Hasselrot, G. Bratt, K. Broliden, and A. C. Karlsson. 2010. Induction of systemic HIV-1-specific cellular immune responses by oral exposure in the uninfected partner of discordant couples. AIDS 24:969-974.
61. Pettersson, F. E., and K. O. Gronvik. 2003. Long-term CD4+ and CD8+ memory T cells developed in severe combined immunodeficiency mice during homoeostasis exhibit differences in sensitivity to antigen. Scand. J. Immunol. 57:311-318.
62. Rosenberg, E. S., et al. 1997. Vigorous HIV-1-specific CD4+ T cell responses associated with control of viremia. Science 278:1447-1450. (Pubitemid 27509814)
63. Rowland-Jones, S., et al. 1995. HIV-specific cytotoxic T-cells in HIV-exposed but uninfected Gambian women. Nat. Med. 1:59-64.
64. Rowland-Jones, S. L., et al. 1998. Cytotoxic T cell responses to multiple conserved HIV epitopes in HIV-resistant prostitutes in Nairobi. J. Clin. Invest. 102:1758-1765.
65. Rowland-Jones, S. L., et al. 1993. HIV-specific cytotoxic T-cell activity in an HIV-exposed but uninfected infant. Lancet 341:860-861. (Pubitemid 23094512)
66. Rychert, J., S. Saindon, S. Placek, D. Daskalakis, and E. Rosenberg. 2007. Sequence variation occurs in CD4 epitopes during early HIV infection. J. Acquir. Immune Defic. Syndr. 46:261-267.
67. Saez-Cirion, A., et al. 2006. Persistent resistance to HIV-1 infection in CD4 T cells from exposed uninfected Vietnamese individuals is mediated by entry and post-entry blocks. Retrovirology 3:81.
68. Sallusto, F., and A. Lanzavecchia. 2009. Heterogeneity of CD4+ memory T cells: functional modules for tailored immunity. Eur. J. Immunol. 39:2076-2082.
69. Schenal, M., et al. 2005. Distinct patterns of HIV-specific memory T lymphocytes in HIV-exposed uninfected individuals and in HIV-infected patients. AIDS 19:653-661. (Pubitemid 40593070)
70. Schmechel, S. C., et al. 2001. Immune defence against HIV-1 infection in HIV-1-exposed seronegative persons. Immunol. Lett. 79:21-27.
71. Shacklett, B. L., et al. 2002. Dendritic cell amplification of HIV type 1-specific CD8+ T cell responses in exposed, seronegative heterosexual women. AIDS Res. Hum. Retroviruses 18:805-815.
72. Simonsen, J. N., et al. 1990. HIV infection among lower socioeconomic strata prostitutes in Nairobi. AIDS 4:139-144. (Pubitemid 20108772)
73. Stockinger, B., C. Bourgeois, and G. Kassiotis. 2006. CD4+ memory T cells: functional differentiation and homeostasis. Immunol. Rev. 211:39-48.
74. Suy, A., et al. 2007. Immunological profile of heterosexual highly HIV-exposed uninfected individuals: predominant role of CD4 and CD8 T-cell activation. J. Infect. Dis. 196:1191-1201.
75. Tenenbaum, S. A., et al. 2005. Evidence of HIV exposure and transient serore-activity in archived HIV-negative severe hemophiliac sera. Virol. J. 2:65.
76. Tomescu, C., et al. 2010. Increased plasmacytoid dendritic cell maturation and natural killer cell activation in HIV-1 exposed, uninfected intra-venous drug users. AIDS 24:2151-2160.
77. Truong, L. X., et al. 2003. CD4 cell and CD8 cell-mediated resistance to HIV-1 infection in exposed uninfected intravascular drug users in Vietnam. AIDS 17:1425-1434. (Pubitemid 36900542)
78. Wahren, B., et al. 1989. HIV-1 peptides induce a proliferative response in lymphocytes from infected persons. J. Acquir. Immune Defic. Syndr. 2:448-456.
79. Wang, S., et al. 2007. Identification of HLA-A11-restricted HIV-1-specific cytotoxic T-lymphocyte epitopes in China. Curr. HIV Res. 5:119-128.
80. Wilson, C. C., et al. 2001. Identification and antigenicity of broadly cross-reactive and conserved human immunodeficiency virus type 1-derived helper T-lymphocyte epitopes. J. Virol. 75:4195-4207. (Pubitemid 32410132)
81. Wu, L., et al. 1997. CCR5 levels and expression pattern correlate with infectability by macrophage-tropic HIV-1, in vitro. J. Exp. Med. 185:1681-1691.
82. Yu, X. G., et al. 2002. Consistent patterns in the development and immunodominance of human immunodeficiency virus type 1 (HIV-1)-specific CD8+ T-cell responses following acute HIV-1 infection. J. Virol. 76:8690-8701. (Pubitemid 34864064)