Differential selection pressure exerted on HIV by CTL targeting identical epitopes but restricted by distinct HLA alleles from the same HLA supertype

Journal of Immunology

Volumn 177, Issue 7, 2006, Pages 4699-4708

  Leslie, Alasdair ^a,j   Price, David A ^b   Mkhize, Pamela ^c   Bishop, Karen ^c   Rathod, Almas ^c   Day, Cheryl ^c   Crawford, Hayley ^a   Honeyborne, Isobella ^a   Asher, Tedi E ^b   Luzzi, Graz ^e   Edwards, Anne ^f   Rosseau, Christine M ^g   Mullins, James I ^g   Tudor Williams, Gareth ^h   Novelli, Vas ⁱ   Brander, Christian ^d   Douek, Daniel C ^b   Kiepiela, Photini ^c   Walker, Bruce D ^d   Goulder, Philip J R ^a,c  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c UNIVERSITY OF KWAZULU NATAL   (South Africa)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

^e WYCOMBE HOSPITAL   (United Kingdom)

^f RADCLIFFE INFIRMARY   (United Kingdom)

^g UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^h ST MARY S HOSPITAL   (United Kingdom)

ⁱ GREAT ORMOND STREET HOSPITAL   (United Kingdom)

^j UNIVERSITY OF OXFORD   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; HLA ANTIGEN; T LYMPHOCYTE RECEPTOR;

ALLELE; ANTIGEN PRESENTATION; ARTICLE; CYTOTOXIC T LYMPHOCYTE; HLA SYSTEM; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MAJOR CLINICAL STUDY; MAJOR HISTOCOMPATIBILITY COMPLEX; PRIORITY JOURNAL; T LYMPHOCYTE SUBPOPULATION;

EID: 33749137810     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.177.7.4699     Document Type: Article

References (49)

1. Goulder, P. J., and D. I. Watkins. 2004. HIV and SIV CTL escape: implications for vaccine design. Nat. Rev. Immunol. 4: 630-640.
2. McMichael, A. J., and T. Hanke. 2003. HIV vaccines 1983-2003. Nat. Med. 9: 874-880.
3. Vogel, T. U., M. R. Reynolds, D. H. Fuller, K. Vielhuber, T. Shipley, J. T. Fuller, K. J. Kunstman, G. Sutter, M. L. Marthas, V. Erfle, et al. 2003. Multispecific vaccine-induced mucosal cytotoxic T lymphocytes reduce acute-phase viral replication but fail in long-term control of simian immunodeficiency virus SIV-mac239. J. Virol. 77: 13348-13360.
4. Ishioka, G. Y., J. Fikes, G. Hermanson, B. Livingston, C. Crimi, M. Qin, M. F. del Guercio, C. Oseroff, C. Dahlberg, J. Alexander, et al. 1999. Utilization of MHC class I transgenic mice for development of minigene DNA vaccines encoding multiple HLA-restricted CTL epitopes. J. Immunol. 162: 3915-3925.
5. Wilson, C. C., D. McKinney, M. Anders, S. MaWhinney, J. Forster, C. Crimi, S. Southwood, A. Sette, R. Chesnut, M. J. Newman, and B. D. Livingston. 2003. Development of a DNA vaccine designed to induce cytotoxic T lymphocyte responses to multiple conserved epitopes in HIV-1. J. Immunol. 171: 5611-5623.
6. + T-cell responses is dramatically modified by DNA immunization and is regulated by γ interferon. J. Virol. 76: 4251-4259.
7. McMichael, A., and P. Klenerman. 2002. HIV/AIDS: HLA leaves its footprints on HIV. Science 296: 1410-1411.
8. Sette, A., and J. Sidney. 1999. Nine major HLA class I supertypes account for the vast preponderance of HLA-A and -B polymorphism. Immunogenetics 50: 201-212.
9. Sidney, J., M. F. del Guercio, S. Southwood, V. H. Engelhard, E. Appella, H. G. Rammensee, K. Falk, O. Rotzschke, M. Takiguchi, R. T. Kubo, et al. 1995. Several HLA alleles share overlapping peptide specificities. J. Immunol. 154: 247-259.
10. Barber, L. D., B. Gillece-Castro, L. Percival, X. Li, C. Clayberger, and P. Parham. 1995. Overlap in the repertoires of peptides bound in vivo by a group of related class I HLA-B allotypes. Curr. Biol. 5: 179-190.
11. Barber, L. D., L. Percival, K. L. Arnett, J. E. Gumperz, L. Chen, and P. Parham. 1997. Polymorphism in the α 1 helix of the HLA-B heavy chain can have an overriding influence on peptide-binding specificity. J. Immunol. 158: 1660-1669.
12. Honeyborne, I., A. Rathod, R. Buchli, D. Ramduth, E. Moodley, P. Rathnavalu, S. Chetty, C. Day, C. Brander, W. Hildebrand, et al. 2006. Motif inference reveals optimal CTL epitopes presented by HLA class I alleles highly prevalent in southern Africa. J. Immunol. 176: 4699-4705.
13. Lund, O., M. Nielsen, C. Kesmir, A. G. Petersen, C. Lundegaard, P. Worning, C. Sylvester-Hvid, K. Lamberth, G. Roder, S. Justesen, et al. 2004. Definition of supertypes for HLA molecules using clustering of specificity matrices. Immunogenetics 55: 797-810.
14. Doytchinova, I. A., P. Guan, and D. R. Flower. 2004. Identifying human MHC supertypes using bioinformatic methods. J. Immunol. 172: 4314-4323.
15. Sidney, J., S. Southwood, and A. Sette. 2005. Classification of A1- and A24-supertype molecules by analysis of their MHC-peptide binding repertoires. Immunogenetics 57: 393-408.
16. Burrows, S. R., R. A. Elkington, J. J. Miles, K. J. Green, S. Walker, S. M. Haryana, D. J. Moss, H. Dunckley, J. M. Burrows, and R. Khanna. 2003. Promiscuous CTL recognition of viral epitopes on multiple human leukocyte antigens: biological validation of the proposed HLA A24 supertype. J. Immunol. 171: 1407-1412.
17. Wang, R. F., S. L. Johnston, S. Southwood, A. Sette, and S. A. Rosenberg. 1998. Recognition of an antigenic peptide derived from tyrosinase-related protein-2 by CTL in the context of HLA-A31 and -A33. J. Immunol. 160: 890-897.
18. Threlkeld, S. C., P. A. Wentworth, S. A. Kalams, B. M. Wilkes, D. J. Ruhl, E. Keogh, J. Sidney, S. Southwood, B. D. Walker, and A. Sette. 1997. Degenerate and promiscuous recognition by CTL of peptides presented by the MHC class I A3-like superfamily: implications for vaccine development. J. Immunol. 159: 1648-1657.
19. Bertoni, R., J. Sidney, P. Fowler, R. W. Chesnut, F. V. Chisari, and A. Sette, 1997. Human histocompatibility leukocyte antigen-binding supermotifs predict broadly cross-reactive cytotoxic T lymphocyte responses in patients with acute hepatitis. J. Clin. Invest. 100: 503-513.
20. Brehm, M. A., A. K. Pinto, K. A. Daniels, J. P. Schneck, R. M. Welsh, and L. K. Selin. 2002. T cell immunodominance and maintenance of memory regulated by unexpectedly cross-reactive pathogens. Nat. Immunol. 3: 627-634.
21. Kiepiela, P., A. J. Leslie, I. Honeyborne, D. Ramduth, C. Thobakgale, S. Chetty, P. Rathnavalu, C. Moore, K. J. Pfafferott, L. Hilton, et al. 2004. Dominant influence of HLA-B in mediating the potential co-evolution of HIV and HLA. Nature 432: 769-775.
22. Prugnolle, F., A. Manica, M. Charpentier, J. F. Guegan, V. Guernier, and F. Balloux. 2005. Pathogen-driven selection and worldwide HLA class I diversity. Curr. Biol. 15: 1022-1027.
23. Leslie, A. J., K. J. Pfafferott, P. Chetty, R. Draenert, M. M. Addo, M. Feeney, Y. Tang, E. C. Holmes, T. Allen, J. G. Prado, et al. 2004. HIV evolution: CTL escape mutation and reversion after transmission. Nat. Med. 10: 282-289.
24. Leslie, A., D. Kavanagh, I. Honeyborne, K. Pfafferott, C. Edwards, T. Pillay, L. Hilton, C. Thobakgale, D. Ramduth, R. Draenert, et al. 2005. Transmission and accumulation of CTL escape variants drive negative associations between HIV polymorphisms and HLA. J. Exp. Med. 201: 891-902.
25. Rousseau, C. M., B. A. Birditt, A. R. McKay, J. N. Stoddard, T. C. Lee, S. McLaughlin, S. W. Moore, N. Shindo, G. H. Learn, B. T. Korber, et al. 2006. Method for high-throughput amplification, cloning and sequencing of full-length HIV-1 subtype C genomes. J. Virol. Methods 136: 118-125.
26. Altman, J. D., P. A. Moss, P. J. Goulder, D. H. Barouch, M. G. McHeyzer-Williams, J. I. Bell, A. J. McMichael, and M. M. Davis. 1996. Phenotypic analysis of antigen-specific T lymphocytes. Science 274: 94-96.
27. 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.
28. + T cell populations specific for persistent DNA viruses. J. Exp. Med. 202: 1349-1361.
29. 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.
30. + T-cell responses represents a major driving force of human immunodeficiency virus type 1 (HIV-1) sequence diversity and reveals constraints on HIV-1 evolution. J. Virol. 79: 13239-13249.
31. Brander, C., K. E. Hartman, A. K. Trocha, N. G. Jones, R. P. Johnson, B. Korber, P. Wentworth, S. P. Buchbinder, S. Wolinsky, B. D. Walker, and S. A. Kalams. 1998. Lack of strong immune selection pressure by the immunodominant. HLA-A*0201-restricted cytotoxic T lymphocyte response in chronic human immunodeficiency virus-1 infection. J. Clin. Invest. 101: 2559-2566.
32. Price, D. A., S. M. West, M. R. Betts, L. E. Ruff, J. M. Brenchley, D. R. Ambrozak, Y. Edghill-Smith, M. J. Kuroda, D. Bogdan, K. Kunstman, et al. 2004. T cell receptor recognition motifs govern immune escape patterns in acute SIV infection. Immunity 21: 793-803.
33. Cibotti, R., J. P. Cabaniols, C. Pannetier, C. Delarbre, I. Vergnon, J. M. Kanellopoulos, and P. Kourilsky. 1994. Public and private Vβ T cell receptor repertoires against hen egg white lysozyme (HEL) in nontransgenic versus HEL transgenic mice. J. Exp. Med. 180: 861-872.
34. Dong, T., G. Stewart-Jones, N. Chen, P. Easterbrook, X. Xu, L. Papagno, V. Appay, M. Weekes, C. Conlon, C. Spina, et al. 2004. HIV-specific cytotoxic T cells from long-term survivors select a unique T cell receptor. J. Exp. Med. 200: 1547-1557.
35. O'Connor, D. H., T. M. Allen, T. U. Vogel, P. Jing, I. P. DeSouza, E. Dodds, E. J. Dunphy, C. Melsaether, B. Mothe, H. Yamamoto, et al. 2002. Acute phase cytotoxic T lymphocyte escape is a hallmark of simian immunodeficiency virus infection. Nat. Med. 8: 493-499.
36. Vogel, T. U., T. C. Friedrich, D. H. O'Connor, W. Rehrauer, E. J. Dodds, H. Hickman, W. Hildebrand, J. Sidney, A. Sette, A. Hughes, et al. 2002. Escape in one of two cytotoxic T-lymphocyte epitopes bound by a high-frequency major histocompattbility complex class I molecule, Mamu-A*02: a paradigm for virus evolution and persistence? J. Virol. 76: 11623-11636.
37. Klenerman, P., Y. Wu, and R. Phillips. 2002. HIV: current opinion in escapology. Curr. Opin. Microbiol. 5: 408-413.
38. Iversen, A. K., G. Stewart-Jones, G. H. Learn, N. Christie, C. Sylvester-Hviid, A. E. Armitage, R. Kaul, T. Beattie, J. K. Lee, Y. Li, et al. 2006. Conflicting selective forces affect T cell receptor contacts in an immunodominant human immunodeficiency virus epitope. Nat. Immunol. 7: 121-122.
39. Marsh, S. G. E., P. Parham, and L. D. Barber. 2000. The HLA Facts Book. Academic Press, London.
40. Bihl, F., N. Frahm, L. Di Giammarino, J. Sidney, M. John, K. Yusim, T. Woodberry, K. Sango, H. S. Hewitt, L. Henry, et al. 2006. Impact of HLA-B alleles, epitope binding affinity, functional avidity, and viral coinfection on the immunodominance of virus-specific CTL responses. J. Immunol. 176: 4094-4101.
41. Altfeld, M., M. M. Addo, E. S. Rosenberg, F. M. Hecht, P. K. Lee, M. Vogel, X. G. Yu, R. Draenert, M. N. Johnston, D. Strick, et al. 2003. Influence of HLA-B57 on clinical presentation and viral control during acute HIV-1 infection. AIDS 17: 2581-2591.
42. Martinez-Picado, J., J. Prado, E. Fry, K. Pfafferott, A. Leslie, S. Chetty, C. Thobakgale, I. Honeyborne, H. Crawford, P. Matthews, et al. 2006. Fitness cost of escape mutation in p24 Gag in association with control of HIV-1. J. Virol. 80: 3617-3623.
43. + long-term nonprogressors and progressors to restrict human immunodeficiency virus replication is not caused by loss of recognition of autologous viral gag sequences. J. Virol. 77: 6889-6898.
44. Burrows, S. R., S. L. Silins, S. M. Cross, C. A. Peh, M. Rischmueller, J. M. Burrows, S. L. Elliott, and J. McCluskey. 1997. Human leukocyte antigen phenotype imposes complex constraints on the antigen-specific cytotoxic T lymphocyte repertoire. Eur. J. Immunol. 27: 178-182.
45. Gao, X., G. W. Nelson, P. Karacki, M. P. Martin, J. Phair, R. Kaslow, J. J. Goedert, S. Buchbinder, K. Hoots, D. Vlahov, et al. 2001. Effect of a single amino acid change in MHC class I molecules on the rate of progression to AIDS. N. Engl. J. Med. 344: 1668-1675.
46. Tynan, F. E., D. Elhassen, A. W. Purcell, J. M. Burrows, N. A. Borg, J. J. Miles, N. A. Williamson, K. J. Green, J. Tellam, L. Kjer-Nielsen, et al. 2005. The immunogenicity of a viral cytotoxic T cell epitope is controlled by its MHC-bound conformation. J. Exp. Med. 202: 1249-1260.
47. Zernich, D., A. W. Purcell, W. A. Macdonald, L. Kjer-Nielsen, L. K. Ely, N. Laham, T. Crockford, N. A. Mifsud, M. Bharadwaj, L. Chang, et al. 2004. Natural HLA class I polymorphism controls the pathway of antigen presentation and susceptibility to viral evasion. J. Exp. Med. 200: 13-24.
48. Mwau, M., A. J. McMichael, and T. Hanke. 2002. Design and validation of an enzyme-linked immunospot assay for use in clinical trials of candidate HIV vaccines. AIDS Res. Hum. Retroviruses 18: 611-618.
49. Yewdell, J. W., and J. R. Bennink. 1999. Immunodominance in major histocompatibility complex class I-restricted T lymphocyte-responses. Annu. Rev. Immunol. 17: 51-88.