Efficacious early antiviral activity of HIV Gag- and Pol-specific HLA-B*2705-restricted CD8+ T cells

Journal of Virology

Volumn 84, Issue 20, 2010, Pages 10543-10557

  Payne, Rebecca P ^a   Kløverpris, Henrik ^a   Sacha, Jonah B ^b   Brumme, Zabrina ^c,d   Brumme, Chanson ^d   Buus, Søren ^e   Sims, Stuart ^a   Hickling, Stephen ^a,f   Riddell, Lynn ^g   Chen, Fabian ^h   Luzzi, Graz ⁱ   Edwards, Anne ^j   Phillips, Rodney ^a   Prado, Julia G ^a,m   Goulder, Philip J R ^a,k,l  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c SIMON FRASER UNIVERSITY   (Canada)

^d BRITISH COLUMBIA CENTRE FOR EXCELLENCE IN HIV AIDS   (Canada)

^e UNIVERSITY OF COPENHAGEN   (Denmark)

^f UNIVERSITY OF OXFORD   (United Kingdom)

^g CAMHS   (United Kingdom)

^h ROYAL BERKSHIRE NHS FOUNDATION TRUST   (United Kingdom)

ⁱ WYCOMBE HOSPITAL   (United Kingdom)

^j CHURCHILL HOSPITAL   (United Kingdom)

^k MASSACHUSETTS GENERAL HOSPITAL   (United States)

^l UNIVERSITY OF KWAZULU NATAL   (South Africa)

^m HOSPITAL UNIVERSITARI GERMANS TRIAS I PUJOL   (Spain)

more..

Author keywords

[No Author keywords available]

Indexed keywords

GAG PROTEIN; GLYCYLARGINYLARGINYLGLYCYLTRYPTOPHANYLGLUTAMYLALANYLLEUCYLLYSYLTYROSINE; GRANZYME; HLA B ANTIGEN; ISOLEUCYLARGINYLLEUCYLARGINYLPROLYLGLYCYLGLYCYLLYSYLLYSYL; LYSYLARGINYLGLUTAMINYLASPARTYLISOLEUCYLASPARTYLLEUCYLASPARTYLLEUCYLTRYPTOPHANYLVALINE; LYSYLARGINYLLYSYLGLYCYLGLYCYLISOLEUCYLGLYCYLGLYCYLTYROSYL; LYSYLARGINYLTRYPTOPHANYLISOLEUCYLISOLEUCYLLEUCYLGLYCYLLEUCYLASPARAGINYLLYSINE; POL PROTEIN; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG; VALYLARGINYLHISTIDYLPHENYLALANYLPROLYLARGINYLISOLEUCYLTRYPTOPHANYLLEUCINE;

ANTIGEN SPECIFICITY; ANTIVIRAL ACTIVITY; ARTICLE; CD8+ T LYMPHOCYTE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOTOXICITY; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNE RESPONSE; MAJOR CLINICAL STUDY; MUTATIONAL ANALYSIS; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN SYNTHESIS; VIRUS INHIBITION; VIRUS REPLICATION;

AIDS VACCINES; AMINO ACID SEQUENCE; CD8-POSITIVE T-LYMPHOCYTES; CYTOTOXICITY, IMMUNOLOGIC; EPITOPES, T-LYMPHOCYTE; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HIV ANTIGENS; HIV INFECTIONS; HIV LONG-TERM SURVIVORS; HIV-1; HLA-B27 ANTIGEN; HUMANS; IMMUNODOMINANT EPITOPES; MOLECULAR SEQUENCE DATA; MUTATION; PEPTIDE FRAGMENTS; POL GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; VPR GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 77957195721     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00793-10     Document Type: Article

References (37)

1. Almeida, J. R., D. A. Price, L. Papagno, Z. A. Arkoub, D. Sauce, E. Bornstein, T. E. Asher, A. Samri, A. Schnuriger, I. Theodorou, D. Costagliola, C. Rouzioux, H. Agut, A. G. Marcelin, D. Douek, B. Autran, and V. Appay. 2007. Superior control of HIV-1 replication by CD8+ T cells is reflected by their avidity, polyfunctionality, and clonal turnover. J. Exp. Med. 204:2473-2485.
2. Almeida, J. R., D. Sauce, D. A. Price, L. Papagno, S. Y. Shin, A. Moris, M. Larsen, G. Pancino, D. C. Douek, B. Autran, A. Saez-Cirion, and V. Appay. 2009. Antigen sensitivity is a major determinant of CD8+ T-cell polyfunctionality and HIV-suppressive activity. Blood 113:6351-6360.
3. Altfeld, M. A., A. Trocha, R. L. Eldridge, E. S. Rosenberg, M. N. Phillips, M. M. Addo, R. P. Sekaly, S. A. Kalams, S. A. Burchett, K. McIntosh, B. D. Walker, and P. J. Goulder. 2000. Identification of dominant optimal HLA-B60- and HLA-B61-restricted cytotoxic T-lymphocyte (CTL) epitopes: rapid characterization of CTL responses by enzyme-linked immunospot assay. J. Virol. 74:8541-8549.
4. Appay, V., P. R. Dunbar, M. Callan, P. Klenerman, G. M. Gillespie, L. Papagno, G. S. Ogg, A. King, F. Lechner, C. A. Spina, S. Little, D. V. Havlir, D. D. Richman, N. Gruener, G. Pape, A. Waters, P. Easterbrook, M. Salio, V. Cerundolo, A. J. McMichael, and S. L. Rowland-Jones. 2002. Memory CD8+ T cells vary in differentiation phenotype in different persistent virus infections. Nat. Med. 8:379-385.
5. Betts, M. R., B. Exley, D. A. Price, A. Bansal, Z. T. Camacho, V. Teaberry, S. M. West, D. R. Ambrozak, G. Tomaras, M. Roederer, J. M. Kilby, J. Tartaglia, R. Belshe, F. Gao, D. C. Douek, K. J. Weinhold, R. A. Koup, P. Goepfert, and G. Ferrari. 2005. Characterization of functional and phenotypic changes in anti-Gag vaccine-induced T cell responses and their role in protection after HIV-1 infection. Proc. Natl. Acad. Sci. U. S. A. 102:4512-4517.
6. Betts, M. R., M. C. Nason, S. M. West, S. C. De Rosa, S. A. Migueles, J. Abraham, M. M. Lederman, J. M. Benito, P. A. Goepfert, M. Connors, M. Roederer, and R. A. Koup. 2006. HIV nonprogressors preferentially maintain highly functional HIV-specific CD8+ T cells. Blood 107:4781-4789.
7. Brockman, M. A., A. Schneidewind, M. Lahaie, A. Schmidt, T. Miura, I. Desouza, F. Ryvkin, C. A. Derdeyn, S. Allen, E. Hunter, J. Mulenga, P. A. Goepfert, B. D. Walker, and T. M. Allen. 2007. Escape and compensation from early HLA-B57-mediated cytotoxic T-lymphocyte pressure on human immunodeficiency virus type 1 Gag alter capsid interactions with cyclophilin A. J. Virol. 81:12608-12618.
8. Brumme, Z. L., C. J. Brumme, J. Carlson, H. Streeck, M. John, Q. Eichbaum, B. L. Block, B. Baker, C. Kadie, M. Markowitz, H. Jessen, A. D. Kelleher, E. Rosenberg, J. Kaldor, Y. Yuki, M. Carrington, T. M. Allen, S. Mallal, M. Altfeld, D. Heckerman, and B. D. Walker. 2008. Marked epitope- and allele-specific differences in rates of mutation in human immunodeficiency type 1 (HIV-1) Gag, Pol, and Nef cytotoxic T-lymphocyte epitopes in acute/early HIV-1 infection. J. Virol. 82:9216-9227.
9. Brumme, Z. L., M. John, J. M. Carlson, C. J. Brumme, D. Chan, M. A. Brockman, L. C. Swenson, I. Tao, S. Szeto, P. Rosato, J. Sela, C. M. Kadie, N. Frahm, C. Brander, D. W. Haas, S. A. Riddler, R. Haubrich, B. D. Walker, P. R. Harrigan, D. Heckerman, and S. Mallal. 2009. HLA-associated immune escape pathways in HIV-1 subtype B Gag, Pol and Nef proteins. PLoS One 4:e6687.
10. Chen, H., A. Piechocka-Trocha, T. Miura, M. A. Brockman, B. D. Julg, B. M. Baker, A. C. Rothchild, B. L. Block, A. Schneidewind, T. Koibuchi, F. Pereyra, T. M. Allen, and B. D. Walker. 2009. Differential neutralization of human immunodeficiency virus (HIV) replication in autologous CD4 T cells by HIV-specific cytotoxic T lymphocytes. J. Virol. 83:3138-3149.
11. Crawford, H., J. G. Prado, A. Leslie, S. Hue, I. Honeyborne, S. Reddy, M. van der Stok, Z. Mncube, C. Brander, C. Rousseau, J. I. Mullins, R. Kaslow, P. Goepfert, S. Allen, E. Hunter, J. Mulenga, P. Kiepiela, B. D. Walker, and P. J. Goulder. 2007. Compensatory mutation partially restores fitness and delays reversion of escape mutation within the immunodominant HLA-B* 5703-restricted Gag epitope in chronic human immunodeficiency virus type 1 infection. J. Virol. 81:8346-8351.
12. Day, C. L., P. Kiepiela, A. J. Leslie, M. van der Stok, K. Nair, N. Ismail, I. Honeyborne, H. Crawford, H. M. Coovadia, P. J. Goulder, B. D. Walker, and P. Klenerman. 2007. Proliferative capacity of epitope-specific CD8 T-cell responses is inversely related to viral load in chronic human immunodeficiency virus type 1 infection. J. Virol. 81:434-438.
13. Dinges, W. L., J. Richardt, D. Friedrich, E. Jalbert, Y. Liu, C. E. Stevens, J. Maenza, A. C. Collier, D. E. Geraghty, J. Smith, Z. Moodie, J. I. Mullins, M. J. McElrath, and H. Horton. 2010. Virus-specific CD8+ T-cell responses better define HIV disease progression than HLA genotype. J. Virol. 84: 4461-4468.
14. Feeney, M. E., Y. Tang, K. A. Roosevelt, A. J. Leslie, K. McIntosh, N. Karthas, B. D. Walker, and P. J. Goulder. 2004. Immune escape precedes breakthrough human immunodeficiency virus type 1 viremia and broadening of the cytotoxic T-lymphocyte response in an HLA-B27-positive long-term-nonprogressing child. J. Virol. 78:8927-8930.
15. Geldmacher, C., J. R. Currier, E. Herrmann, A. Haule, E. Kuta, F. McCutchan, L. Njovu, S. Geis, O. Hoffmann, L. Maboko, C. Williamson, D. Birx, A. Meyerhans, J. Cox, and M. Hoelscher. 2007. CD8 T-cell recognition of multiple epitopes within specific Gag regions is associated with maintenance of a low steady-state viremia in human immunodeficiency virus type 1-seropositive patients. J. Virol. 81:2440-2448.
16. Goulder, P. J., R. E. Phillips, R. A. Colbert, S. McAdam, G. Ogg, M. A. Nowak, P. Giangrande, G. Luzzi, B. Morgan, A. Edwards, A. J. McMichael, and S. Rowland-Jones. 1997. Late escape from an immunodominant cytotoxic T-lymphocyte response associated with progression to AIDS. Nat. Med. 3:212-217.
17. Harndahl, M., S. Justesen, K. Lamberth, G. Roder, M. Nielsen, and S. Buus. 2009. Peptide binding to HLA class I molecules: homogenous, high-throughput screening, and affinity assays. J. Biomol. Screen. 14:173-180.
18. Honeyborne, I., A. Rathod, R. Buchli, D. Ramduth, E. Moodley, P. Rathnavalu, S. Chetty, C. Day, C. Brander, W. Hildebrand, B. D. Walker, P. Kiepiela, and P. J. Goulder. 2006. Motif inference reveals optimal CTL epitopes presented by HLA class I alleles highly prevalent in southern Africa. J. Immunol. 176:4699-4705.
19. Kelleher, A. D., C. Long, E. C. Holmes, R. L. Allen, J. Wilson, C. Conlon, C. Workman, S. Shaunak, K. Olson, P. Goulder, C. Brander, G. Ogg, J. S. Sullivan, W. Dyer, I. Jones, A. J. McMichael, S. Rowland-Jones, and R. E. Phillips. 2001. Clustered mutations in HIV-1 gag are consistently required for escape from HLA-B27-restricted cytotoxic T lymphocyte responses. J. Exp. Med. 193:375-386.
20. Kiepiela, P., K. Ngumbela, C. Thobakgale, D. Ramduth, I. Honeyborne, E. Moodley, S. Reddy, C. de Pierres, Z. Mncube, N. Mkhwanazi, K. Bishop, M. van der Stok, K. Nair, N. Khan, H. Crawford, R. Payne, A. Leslie, J. Prado, A. Prendergast, J. Frater, N. McCarthy, C. Brander, G. H. Learn, D. Nickle, C. Rousseau, H. Coovadia, J. I. Mullins, D. Heckerman, B. D. Walker, and P. Goulder. 2007. CD8+ T-cell responses to different HIV proteins have discordant associations with viral load. Nat. Med. 13:46-53.
21. Martinez-Picado, J., J. G. Prado, E. E. Fry, K. Pfafferott, A. Leslie, S. Chetty, C. Thobakgale, I. Honeyborne, H. Crawford, P. Matthews, T. Pillay, C. Rousseau, J. I. Mullins, C. Brander, B. D. Walker, D. I. Stuart, P. Kiepiela, and P. Goulder. 2006. Fitness cost of escape mutations in p24 Gag in association with control of human immunodeficiency virus type 1. J. Virol. 80:3617-3623.
22. Migueles, S. A., C. M. Osborne, C. Royce, A. A. Compton, R. P. Joshi, K. A. Weeks, J. E. Rood, A. M. Berkley, J. B. Sacha, N. A. Cogliano-Shutta, M. Lloyd, G. Roby, R. Kwan, M. McLaughlin, S. Stallings, C. Rehm, M. A. O'Shea, J. Mican, B. Z. Packard, A. Komoriya, S. Palmer, A. P. Wiegand, F. Maldarelli, J. M. Coffin, J. W. Mellors, C. W. Hallahan, D. A. Follman, and M. Connors. 2008. Lytic granule loading of CD8+ T cells is required for HIV-infected cell elimination associated with immune control. Immunity 29:1009-1021.
23. Moskophidis, D., and R. M. Zinkernagel. 1995. Immunobiology of cytotoxic T-cell escape mutants of lymphocytic choriomeningitis virus. J. Virol. 69: 2187-2193.
24. Pircher, H., D. Moskophidis, U. Rohrer, K. Burki, H. Hengartner, and R. M. Zinkernagel. 1990. Viral escape by selection of cytotoxic T cell-resistant virus variants in vivo. Nature 346:629-633.
25. Prado, J. G., I. Honeyborne, I. Brierley, M. C. Puertas, J. Martinez-Picado, and P. J. Goulder. 2009. Functional consequences of human immunodeficiency virus escape from an HLA-B*13-restricted CD8+ T-cell epitope in p1 Gag protein. J. Virol. 83:1018-1025.
26. Sacha, J. B., C. Chung, E. G. Rakasz, S. P. Spencer, A. K. Jonas, A. T. Bean, W. Lee, B. J. Burwitz, J. J. Stephany, J. T. Loffredo, D. B. Allison, S. Adnan, A. Hoji, N. A. Wilson, T. C. Friedrich, J. D. Lifson, O. O. Yang, and D. I. Watkins. 2007. Gag-specific CD8+ T lymphocytes recognize infected cells before AIDS-virus integration and viral protein expression. J. Immunol. 178:2746-2754.
27. Sacha, J. B., C. Chung, J. Reed, A. K. Jonas, A. T. Bean, S. P. Spencer, W. Lee, L. Vojnov, R. Rudersdorf, T. C. Friedrich, N. A. Wilson, J. D. Lifson, and D. I. Watkins. 2007. Pol-specific CD8+ T cells recognize simian immunodeficiency virus-infected cells prior to Nef-mediated major histocompatibility complex class I downregulation. J. Virol. 81:11703-11712.
28. Schellens, I. M., C. Kesmir, F. Miedema, D. van Baarle, and J. A. Borghans. 2008. An unanticipated lack of consensus cytotoxic T lymphocyte epitopes in HIV-1 databases: the contribution of prediction programs. AIDS 22:33-37.
29. Schneidewind, A., M. A. Brockman, J. Sidney, Y. E. Wang, H. Chen, T. J. Suscovich, B. Li, R. I. Adam, R. L. Allgaier, B. R. Mothe, T. Kuntzen, C. Oniangue-Ndza, A. Trocha, X. G. Yu, C. Brander, A. Sette, B. D. Walker, and T. M. Allen. 2008. Structural and functional constraints limit options for cytotoxic T-lymphocyte escape in the immunodominant HLA-B27-restricted epitope in human immunodeficiency virus type 1 capsid. J. Virol. 82:5594-5605.
30. Schneidewind, A., M. A. Brockman, R. Yang, R. I. Adam, B. Li, S. Le Gall, C. R. Rinaldo, S. L. Craggs, R. L. Allgaier, K. A. Power, T. Kuntzen, C. S. Tung, M. X. LaBute, S. M. Mueller, T. Harrer, A. J. McMichael, P. J. Goulder, C. Aiken, C. Brander, A. D. Kelleher, and T. M. Allen. 2007. Escape from the dominant HLA-B27-restricted cytotoxic T-lymphocyte response in Gag is associated with a dramatic reduction in human immunodeficiency virus type 1 replication. J. Virol. 81:12382-12393.
31. Streeck, H., Z. L. Brumme, M. Anastario, K. W. Cohen, J. S. Jolin, A. Meier, C. J. Brumme, E. S. Rosenberg, G. Alter, T. M. Allen, B. D. Walker, and M. Altfeld. 2008. Antigen load and viral sequence diversification determine the functional profile of HIV-1-specific CD8+ T cells. PLoS Med. 5:e100.
32. Streeck, H., B. Li, A. F. Poon, A. Schneidewind, A. D. Gladden, K. A. Power, D. Daskalakis, S. Bazner, R. Zuniga, C. Brander, E. S. Rosenberg, S. D. Frost, M. Altfeld, and T. M. Allen. 2008. Immune-driven recombination and loss of control after HIV superinfection. J. Exp. Med. 205:1789-1796.
33. Weber, J., J. Weberova, M. Carobene, M. Mirza, J. Martinez-Picado, P. Kazanjian, and M. E. Quinones-Mateu. 2006. Use of a novel assay based on intact recombinant viruses expressing green (EGFP) or red (DsRed2) fluorescent proteins to examine the contribution of pol and env genes to overall HIV-1 replicative fitness. J. Virol. Methods 136:102-117.
34. Weston, S. A., and C. R. Parish. 1990. New fluorescent dyes for lymphocyte migration studies. Analysis by flow cytometry and fluorescence microscopy. J. Immunol. Methods 133:87-97.
35. Yang, O. O., S. A. Kalams, A. Trocha, H. Cao, A. Luster, R. P. Johnson, and B. D. Walker. 1997. Suppression of human immunodeficiency virus type 1 replication by CD8+ cells: evidence for HLA class I-restricted triggering of cytolytic and noncytolytic mechanisms. J. Virol. 71:3120-3128.
36. Yang, O. O., P. T. Sarkis, A. Trocha, S. A. Kalams, R. P. Johnson, and B. D. Walker. 2003. Impacts of avidity and specificity on the antiviral efficiency of HIV-1-specific CTL. J. Immunol. 171:3718-3724.
37. Zuniga, R., A. Lucchetti, P. Galvan, S. Sanchez, C. Sanchez, A. Hernandez, H. Sanchez, N. Frahm, C. H. Linde, H. S. Hewitt, W. Hildebrand, M. Altfeld, T. M. Allen, B. D. Walker, B. T. Korber, T. Leitner, J. Sanchez, and C. Brander. 2006. Relative dominance of Gag p24-specific cytotoxic T lymphocytes is associated with human immunodeficiency virus control. J. Virol. 80:3122-3125.