HIV-specific cytotoxic T cells from long-term survivors select a unique T cell receptor

Journal of Experimental Medicine

Volumn 200, Issue 12, 2004, Pages 1547-1557

  Dong, Tao ^a   Stewart Jones, Guillaume ^b   Chen, Nan ^a   Easterbrook, Philippa ^c   Xu, Xiaoning ^a   Papagno, Laura ^a   Appay, Victor ^a   Weekes, Michael ^a   Conlon, Chris ^a   Spina, Celsa ^e   Little, Susan ^e   Screaton, Gavin ^a   Van Der Merwe, Anton ^d   Richman, Douglas D ^e   McMichael, Andrew J ^a   Jones, E Yvonne ^b   Rowland Jones, Sarah L ^a  

^a JOHN RADCLIFFE HOSPITAL   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Apoptosis; Cross reactivity; Cytotoxic T lymphocytes (CTL); HIV; T cell receptor

Indexed keywords

EPITOPE; NEF PROTEIN; T LYMPHOCYTE RECEPTOR; TOLL LIKE RECEPTOR;

APOPTOSIS; ARTICLE; BETA CHAIN; COMPLEMENTARITY DETERMINING REGION; CYTOTOXIC T LYMPHOCYTE; DISEASE COURSE; HLA SYSTEM; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; IN VITRO STUDY; LONG TERM CARE; PATIENT; PRIORITY JOURNAL; VIRUS REPLICATION;

APOPTOSIS; EPITOPES, T-LYMPHOCYTE; FEMALE; GENE PRODUCTS, NEF; HIV INFECTIONS; HIV-1; HLA-B8 ANTIGEN; HUMANS; MALE; OLIGOPEPTIDES; PROGNOSIS; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; T-LYMPHOCYTES, CYTOTOXIC; VIRUS REPLICATION;

EID: 19944427950     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20032044     Document Type: Article

References (44)

1. Deacon, N.J., A. Tsykin, S.K. Smith, M. Ludford-Menting, D.J. Hooker, D.A. McPhee, A.L. Greenway, A. Ellett, C. Chatfield, V.A. Lawson, et al. 1995. Genomic structure of an attenuated quasi species of HIV-1 from a blood transfusion donor and recipients. Science. 270:988-991.
2. O'Brien, S.J., G.W. Nelson, C.A. Winkler, and M.W. Smith. 2000. Polygenic and multifactorial disease gene association in man: lessons from AIDS. Annu. Rev. Genet. 34:563-591.
3. Easterbrook, P.J. 1999. Long-term non-progression in HIV infection: definitions and epidemiological issues. J. Infect. 38:71-73.
4. Rosenberg, E.S., J.M. Billingsley, A. Caliendo, S.L. Boswell, P.E. Sax, S.A. Kalams, and B.D. Walker. 1997. Vigorous HIV-1-specific CD4+ T-cell responses associated with control of viraemia. Science. 278:1447-1450.
5. Pantaleo, G., S. Menzo, M. Vaccarezza, C. Graziosi, O. Cohen, J. Demarest, D. Montefiori, J. Orenstein, C. Fox, L. Schrager, et al. 1995. Studies in subjects with long-term non-progressive HIV infection. N. Engl. J. Med. 332:209-216.
6. Rinaldo, C., X.-L. Huang, Z. Fan, M. Ding, L. Beltz, A. Logar, D. Panicali, G. Mazzara, J. Liebmann, M. Cottrill, and P. Gupta. 1995. High levels of anti-HIV-1 memory CTL activity and low viral load are associated with lack of disease in HIV-1-infected long-term non-progressors. J. Virol. 69:5838-5842.
7. Papagno, L., V. Appay, J. Sutton, T. Rostron, G.M. Gillespie, G.S. Ogg, A. King, A.T. Makadzanhge, A. Waters, C. Balotta, et al. 2002. Comparison between HIV- and CMV-specific T cell responses in long-term HIV infected donors. Clin. Exp. Immunol. 130:509-517.
8. Addo, M.M., X.G. Yu, A. Rathod, D. Cohen, R.L. Eldridge, D. Strick, M.N. Johnston, C. Corcoran, A.G. Wurcel, C.A. Fitzpatrick, et al. 2003. Comprehensive epitope analysis of human immunodeficiency virus type 1 (HIV-1)-specific T-cell responses directed against the entire expressed HIV-1 genome demonstrate broadly directed responses, but no correlation to viral load. J. Virol. 77:2081-2092.
9. McMichael, A.J., and S.L. Rowland-Jones. 2001. Cellular immune responses to HIV. Nature. 410:980-987.
10. Appay, V., D.F. Nixon, S.M. Donahoe, G.M. Gillespie, T. Dong, A. King, G.S. Ogg, H.M. Spiegel, C. Conlon, C.A. Spina, et al. 2000. HIV-specific CD8(+) T cells produce antiviral cytokines but are impaired in cytolytic function. J. Exp. Med. 192:63-75.
11. Kostense, S., G.S. Ogg, E.H. Manting, G. Gillespie, J. Joling, K. Vandenberghe, E.Z. Veenhof, D. Baarle Dv, S. Jurriaans, M.R. Klein, and F. Miedema. 2001. High viral burden in the presence of major HIV-specific CD8(+) T cell expansions: evidence for impaired CTL effector function. Eur. J. Immunol. 31:677-686.
12. Appay, V., P.R. Dunbar, M. Callan, P. Klenerman, G.M. Gillespie, L. Papagno, G.S. Ogg, A. King, F. Lechner, C.A. Spina, et al. 2002. Memory CD8+ T cells vary in differentiation phenotype in different persistent virus infections. Nat. Med. 8:379-385.
13. Lieberman, J., P. Shankar, N. Manjunath, and J. Andersson. 2001. Dressed to kill? A review of why antiviral CD8 T lymphocytes fail to prevent progressive immunodeficiency in HIV-1 infection. Blood. 98:1667-1677.
14. Moss, P.A.H., R.J. Moots, W.M.C. Rosenberg, S.J. Rowland-Jones, A.J. McMichael, and J.I. Bell. 1991. Extensive conservation of alpha and beta chains of the human T cell antigen receptor recognizing HLA-A2 and influenza matrix peptide. Proc. Natl. Acad. Sci. USA. 88:8987-8991.
15. Stewart-Jones, G.B., A.J. McMichael, J.I. Bell, D.I. Stuart, and E.Y. Jones. 2003. A structural basis for immunodomimnt human T cell receptor recognition. Nat. Immunol. 4:657-663.
16. Argaet, V.P., C.W. Schmidt, S.R. Burrows, S.L. Silins, M.G. Kurilla, D.L. Doolan, A. Suhrbier, D.J. Moss, E. Kieff, T.B. Suclley, et al. 1994. Dominant selection of an invariant T cell antigen receptor in response to persistent infection by Epstein-Barr virus. J. Exp. Med. 180:2335-2340.
17. Kjer-Nielsen, L., C.S. Clements, A.W. Purcell, A.G. Brooks, J.C. Whisstock, S.R. Burrows, J. McCluskey, and J. Rossjohn. 2003. A structural basis for the selection of dominant alphabeta T cell receptors in antiviral immunity. Immunity. 18:53-64.
18. Pantaleo, G., J.F. Demarest, H. Soudeyns, C. Graziosi, F. Denis, J.W. Adelsberger, P. Borrow, M.S. Saag, G.M. Shaw, R.P. Sekaly, and A.S. Fauci. 1994. Major expansion of CD8+ T cells with a predominant Vb usage during the primary immune response to HIV. Nature. 370:463-467.
19. Wilson, J.D.K., G.S. Ogg, R.L. Allen, P.J.R. Goulder, A. Kelleher, A.K. Sewell, C.A. O'Callaghan, S.L. Rowland-Jones, M.F.C. Callan, and A.J. McMichael. 1998. Oligoclonal expansions of CD8(+) T cells in chronic HIV infection are antigen specific. J. Exp. Med. 188:785-790.
20. Douek, D.C., M.R. Betts, J.M. Brenchley, B.J. Hill, D.R. Ambrozak, K.L. Ngai, N.J. Karandikar, J.P. Casazza, and R.A. Koup. 2002. A novel approach to the analysis of specificity, clonality, and frequency of HIV-specific T cell responses reveals a potential mechanism for control of viral escape. J. Immunol. 168:3099-3104.
21. Price, D.A., P.J. Goulder, P. Klenerman, A.K. Sewell, P.J. Easterbrook, M. Troop, C.R. Bangham, and R.E. Phillips. 1997. Positive selection of HIV-1 cytotoxic T lymphocyte escape variants during primary infection. Proc. Natl. Acad. Sci. USA. 94:1890-1895.
22. Easterbrook, P.J., and L.K. Schrager. 1998. Long-term non-progression in HIV infection: methodological issues and scientific priorities. Report of an international European community-National Institutes of Health Workshop, The Royal Society, London, England, November 27-29, 1995. Scientific Coordinating Committee. AIDS Res. Hum. Retroviruses. 14:1211-1228.
23. Bunce, M., C.M. O'Neill, M.C. Barnardo, P. Krausa, M.J. Browning, P.J. Morris, and K.I. Welsh. 1995. Phototyping: comprehensive DNA typing for HLA-A, B, C, DRB1, DRB3, DRB4, DRB5 & DQB1 by PCR with 144 primer mixes utilizing sequence-specific primers. Tissue Antigens. 46:355-367.
24. Altman, J., P.A.H. Moss, P. Goulder, D. Barouch, M. McHeyzer-Williams, J.I. Bell, A.J. McMichael, and M.M. Davis. 1996. Direct visualization and phenotypic analysis of virus-specific T lymphocytes in HIV-infected individuals. Science. 274:94-96.
25. Lalvani, A., R. Brookes, S. Hambleton, W.J. Britton, A.V. Hill, and A.J. McMichael. 1997. Rapid effector function in CD8+ memory T cells. J. Exp. Med. 186:859-865.
26. Gorczyca, W., J. Gong, and Z. Darzynkiewicz. 1993. Detection of DNA strand breaks in individual apoptotic cells by the in situ terminal deoxynucleotidyl transferase and nick translation assays. Cancer Res. 53:1945-1951.
27. Dong, T., D. Boyd, W. Rosenberg, N. Alp, M. Takiguchi, A.J. McMichael, and S.L. Rowland-Jones. 1996. Increased affinity for HLA-B35 of an influenza A epitope modified at an "anchor" residue results in an antagonist peptide. Eur. J. Immunol. 26:335-339.
28. Zhu, Y.Y., E.M. Machleder, A. Chenchik, R. Li, and P.D. Siebert. 2001. Reverse transcriptase template switching: a SMART approach for full-length cDNA library construction. Biotechniques. 30:892-897.
29. Easterbrook, P.J., T. Rostron, N. Ives, M. Troop, B.G. Gazzard, and S.L. Rowland-Jones. 1999. Chemokine receptor polymorphisms and human immunodeficiency virus disease progression. J. Infect. Dis. 180:1096-1105.
30. Kabat, E.A., and T.T. Wu. 1991. Identical V region amino acid sequences and segments of sequences in antibodies of different specificities. Relative contributions of VH and VL genes, minigenes, and complementarity-determining regions to binding of antibody-combining sites. J. Immunol. 147:1709-1719.
31. Moss, P.A., and J.I. Bell. 1996. Comparative sequence analysis of the human T cell receptor TCRA and TCRB CDR3 regions. Hum. Immunol. 48:32-38.
32. Xu, X.-N., G.R. Screaton, F.M. Gotch, T. Dong, R. Tan, N. Almond, B. Walker, R. Stebbings, K. Kent, S. Nagata, et al. 1997. Evasion of CTL responses by nef-dependent induction of Fas ligand expression on SIV-infected cells. J. Exp. Med. 186:7-16.
33. Wilson, S.E., S.L. Pedersen, J.C. Kunich, V.L. Wilkins, D.L. Mann, G.P. Mazzara, J. Tartaglia, C.L. Celum, and H.W. Sheppard. 1998. Cross-clade envelope glycoprotein 160-specific CD8+ cytotoxic T lymphocyte responses in early HIV type 1 clade B infection. AIDS Res. Hum. Retroviruses. 14:925-937.
34. van der Merwe, P.A., and S.J. Davis. 2003. Molecular interactions mediating T cell antigen recognition. Annu. Rev. Immunol. 21:659-684.
35. Phillips, R.E., S.L. Rowland-Jones, D.F. Nixon, F.M. Gotch, J.P. Edwards, A.O. Ogunlesi, J.G. Elvin, J.A. Rothbard, C.R. Bangham, C.R. Rizza, and A.J. McMichael. 1991. Human immunodeficiency virus genetic variation that can escape cytotoxic T cell recognition. Nature. 354:453-459.
36. 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, et al. 2000. Tat-specific cytotoxic T lymphocytes select for SIV escape variants during resolution of primary viraemia. Nature. 407:386-390.
37. 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, et al. 2002. Eventual AIDS vaccine failure in a rhesus monkey by viral escape from cytotoxic T lymphocytes. Nature. 415:335-339.
38. Moore, C.B., M. John, I.R. James, F.T. Christiansen, C.S. Witt, and S.A. Mallal. 2002. Evidence of HIV-1 adaptation to HLA-restricted immune responses at a population level. Science. 296:1439-1443.
39. Gillespie, G.M., R. Kaul, T. Dong, H.B. Yang, T. Rostron, J.J. Bwayo, P. Kiania, T. Peto, F.A. Plummer, A.J. McMichael, and S.L. Rowland-Jones. 2002. Cross-reactive cytotoxic T lymphocytes against a HIV-1 p24 epitope in slow processors with B*57. AIDS. 16:961-972.
40. Reid, S.W., S. McAdam, K.J. Smith, P. Klenerman, C.A. O'Callaghan, K. Harlos, B.K. Jakobsen, A.J. McMichael, J.I. Bell, D.I. Stuart, and E.Y. Jones. 1996. Antagonist HIV-1 Gag peptides induce structural changes in HLA B8. J. Exp. Med. 184:2279-2286.
41. Gett, A.V., F. Sallusto, A. Lanzavecchia, and J. Geginat. 2003. T cell fitness determined by signal strength. Nat. Immunol. 4:355-360.
42. Moss, P.A.H., S.L. Rowland-Jones, P.M. Frodsham, S. McAdam, P. Giangrande, A.J. McMichael, and J.I. Bell. 1995. Persistent high frequency of human immunodeficiency virus-specific cytotoxic T cells in peripheral blood of infected donors. Proc. Natl. Acad. Sci. USA. 92:5773-5777.
43. Chen, Z.W., L. Shen, J.D. Regan, Z. Kou, S.H. Ghim, and N.L. Letvin. 1996. The T cell receptor gene usage by simian immunodeficiency virus gag-specific cytotoxic T lymphocytes in rhesus monkeys. J. Immunol. 156:1469-1475.
44. Chen, Z.W., Y. Li, X. Zeng, M.J. Kuroda, J.E. Schmitz, Y. Shen, X. Lai, L. Shen, and N.L. Letvin. 2001. The TCR repertoire of an immunodominant CD8+ T lymphocyte population. J. Immunol. 166:4525-4533.