Persistent Recognition of Autologous Virus by High-Avidity CD8 T Cells in Chronic, Progressive Human Immunodeficiency Virus Type 1 Infection

Journal of Virology

Volumn 78, Issue 2, 2004, Pages 630-641

  Draenert, R ^a   Verrill, C L ^a   Tang, Y ^a   Allen, T M ^a   Wurcel, A G ^a,b   Boczanowski, M ^a   Lechner, A ^a   Kim, A Y ^a   Suscovich, T ^a   Brown, N V ^a   Addo, M M ^a   Walker, B D ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b LEMUEL SHATTUCK HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIRETROVIRUS AGENT; CD4 ANTIGEN; CD8 ANTIGEN; EPITOPE; GAG PROTEIN; GAMMA INTERFERON; NEF PROTEIN; POL PROTEIN; REV PROTEIN; TRANSACTIVATOR PROTEIN; VIF PROTEIN; VIRUS ENVELOPE PROTEIN; VIRUS PROTEIN; VPR PROTEIN; VPU PROTEIN;

ANTIGEN PRESENTING CELL; ANTIGEN RECOGNITION; ARTICLE; CELL SPECIFICITY; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE COURSE; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITOPE MAPPING; GENETIC SCREENING; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IN VIVO STUDY; INTERFERON PRODUCTION; LYMPHOCYTE COUNT; LYMPHOCYTE FUNCTION; MONONUCLEAR CELL; NONHUMAN; PERIPHERAL CIRCULATION; PREDICTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEQUENCE ANALYSIS; STATISTICAL SIGNIFICANCE; T LYMPHOCYTE ACTIVATION; VIREMIA; VIRUS DIAGNOSIS; VIRUS INHIBITION; VIRUS LOAD; VIRUS MUTATION;

AMINO ACID SEQUENCE; CD8-POSITIVE T-LYMPHOCYTES; CHRONIC DISEASE; DISEASE PROGRESSION; EPITOPES, T-LYMPHOCYTE; GENE PRODUCTS, GAG; HIV INFECTIONS; HIV-1; HUMANS; INTERFERON TYPE II; MOLECULAR SEQUENCE DATA; PEPTIDES; VIRAL PROTEINS;

EID: 9144266646     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.2.630-641.2004     Document Type: Article

References (58)

1. 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, M. E. Feeney, W. R. Rodriguez, N. Basgoz, R. Draenert, D. R. Stone, C. Brander, P. J. Goulder, E. S. Rosenberg, M. Altfeld, and B. D. Walker. 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.
2. Alexander-Miller, M. A., G. R. Leggatt, and J. A. Berzofsky. 1996. Selective expansion of high- or low-avidity cytotoxic T lymphocytes and efficacy for adoptive immunotherapy. Proc. Natl. Acad. Sci. USA 93:4102-4107.
3. 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, K. J. Kunstman, X. Wang, D. B. Allison, A. L. Hughes, R. C. Desrosiers, J. D. Altman, S. M. Wolinsky, A. Sette, and D. I. Watkins. 2000. Tat-specific cytotoxic T lymphocytes select for SIV escape variants during resolution of primary viraemia. Nature 407:386-390.
4. Altfeld, M., M. M. Addo, R. L. Eldridge, X. G. Yu, S. Thomas, A. Khatri, D. Strick, M. N. Phillips, G. B. Cohen, S. A. Islam, S. A. Kalams, C. Brander, P. J. Goulder, E. S. Rosenberg, and B. D. Walker. 2001. Vpr is preferentially targeted by CTL during HIV-1 infection. J. Immunol. 167:2743-2752.
5. Altfeld, M., et al. 2003. Enhanced detection of human immunodeficiency virus type 1-specific T-cell responses to highly variable regions by using peptides based on autologous virus sequences. J. Virol. 77:7330-7340.
6. Altfeld, M., T. M. Allen, X. G. Yu, M. N. Johnston, D. Agrawal, B. T. Korber, D. C. Montefiori, D. H. O'Connor, B. T. Davis, P. K. Lee, E. L. Maier, J. Harlow, P. J. Goulder, C. Brander, E. S. Rosenberg, and B. D. Walker. 2002. HIV-1 superinfection despite broad CD8+ T-cell responses containing replication of the primary virus. Nature 420:434-439.
7. Altfeld, M., E. S. Rosenberg, R. Shankarappa, J. S. Mukherjee, F. M. Hecht, R. L. Eldridge, M. M. Addo, S. H. Poon, M. N. Phillips, G. K. Robbins, P. E. Sax, S. Boswell, J. O. Kahn, C. Brander, P. J. Goulder, J. A. Levy, J. I. Mullins, and B. D. Walker. 2001. Cellular immune responses and viral diversity in individuals treated during acute and early HIV-1 infection. J. Exp. Med. 193:169-180.
8. 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.
9. Altfeld, M. A., et al. Influence of HLA-B57 on clinical presentation and viral control during acute HIV-1 infection. AIDS, in press.
10. 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.
11. Barouch, D. H., S. Santra, J. E. Schmitz, M. J. Kuroda, T. M. Fu, W. Wagner, M. Bilska, A. Craiu, X. X. Zheng, G. R. Krivulka, K. Beaudry, M. A. Lifton, C. E. Nickerson, W. L. Trigona, K. Punt, D. C. Freed, L. Guan, S. Dubey, D. Casimiro, A. Simon, M. E. Davies, M. Chastain, T. B. Strom, R. S. Gelman, D. C. Montefiori, M. G. Lewis, E. A. Emini, J. W. Shiver, and N. L. Letvin. 2000. Control of viremia and prevention of clinical AIDS in rhesus monkeys by cytokine-augmented DNA vaccination. Science 290:486-492.
12. + T-cell responses: relationship to viral load in untreated HIV infection. J. Virol. 75:11983-11991.
13. Betts, M. R., J. P. Casazza, and R. A. Koup. 2001. Monitoring HIV-specific CD8+ T cell responses by intracellular cytokine production. Immunol. Lett. 79:117-125.
14. + cytotoxic T-lymphocyte activity associated with control of viremia in primary human immunodeficiency virus type 1 infection. J. Virol. 68:6103-6110.
15. Borrow, P., H. Lewicki, X. Wei, M. S. Horwitz, N. Peffer, H. Meyers, J. A. Nelson, J. E. Gairin, B. H. Hahn, M. B. Oldstone, and G. M. Shaw. 1997. Antiviral pressure exerted by HIV-1-specific cytotoxic T lymphocytes (CTLs) during primary infection demonstrated by rapid selection of CTL escape virus. Nat. Med. 3:205-211.
16. Brander, C., and B. D. Walker. 1999. T lymphocyte responses in HIV-1 infection: implications for vaccine development. Curr. Opin. Immunol. 11:451-459.
17. Brander, C., O. O. Yang, N. G. Jones, Y. Lee, P. Goulder, R. P. Johnson, A. Trocha, D. Colbert, C. Hay, S. Buchbinder, C. C. Bergmann, H. J. Zweerink, S. Wolinsky, W. A. Blattner, S. A. Kalams, and B. D. Walker. 1999. Efficient processing of the immunodominant, HLA-A*0201-restricted human immunodeficiency virus type 1 cytotoxic T-lymphocyte epitope despite multiple variations in the epitope flanking sequences. J. Virol. 73:10191-10198.
18. Cao, H., P. Kaleebu, D. Hom, J. Flores, D. Agrawal, N. Jones, J. Serwanga, M. Okello, C. Walker, H. Sheppard, R. El-Habib, M. Klein, E. Mbidde, P. Mugyenyi, B. Walker, J. Ellner, and R. Mugerwa. 2003. Immunogenicity of a recombinant human immunodeficiency virus (HIV)-canarypox vaccine in HIV-seronegative Ugandan volunteers: results of the HIV Network for Prevention Trials 007 Vaccine Study. J. Infect. Dis. 187:887-895.
19. + T cells in primary HIV-1 infection. J. Virol. 77:6867-6878.
20. Champagne, P., G. S. Ogg, A. S. King, C. Knabenhans, K. Ellefsen, M. Nobile, V. Appay, G. P. Rizzardi, S. Fleury, M. Lipp, R. Forster, S. Rowland-Jones, R. P. Sekaly, A. J. McMichael, and G. Pantaleo. 2001. Skewed maturation of memory HIV-specific CD8 T lymphocytes. Nature 410:106-111.
21. Collins, K. L., B. K. Chen, S. A. Kalams, B. D. Walker, and D. Baltimore. 1998. HIV-1 Nef protein protects infected primary cells against killing by cytotoxic T lymphocytes. Nature 391:397-401.
22. Connick, E., R. L. Schlichtemeier, M. B. Purner, K. M. Schneider, D. M. Anderson, S. MaWhinney, T. B. Campbell, D. R. Kuritzkes, J. M. Douglas, Jr., F. N. Judson, and R. T. Schooley. 2001. Relationship between human immunodeficiency virus type 1 (HIV-1)-specific memory cytotoxic T lymphocytes and virus load after recent HIV-1 seroconversion. J. Infect. Dis. 184:1465-1469.
23. Couillin, I., F. Letourneur, P. Lefebvre, J. G. Guillet, and F. Martinon. 2001. DNA vaccination of macaques with several different Nef sequences induces multispecific T cell responses. Virology 279:136-145.
24. Derby, M., M. Alexander-Miller, R. Tse, and J. Berzofsky. 2001. High-avidity CTL exploit two complementary mechanisms to provide better protection against viral infection than low-avidity CTL. J. Immunol. 166:1690-1697.
25. Draenert, R., M. Altfeld, C. Brander, N. Basgoz, C. Corcoran, A. G. Wurcel, D. R. Stone, S. A. Kalams, A. Trocha, M. M. Addo, P. J. Goulder, and B. D. Walker. 2003. Comparison of overlapping peptide sets for detection of antiviral CD8 and CD4 T cell responses. J. Immunol. Methods 275:19-29.
26. + T-cell responses to the Gag protein of human immunodeficiency virus type 1 correlates inversely with viral load in plasma. J. Virol. 76:2298-2305.
27. Goulder, P. J., M. A. Altfeld, E. S. Rosenberg, T. Nguyen, Y. Tang, R. L. Eldridge, M. M. Addo, S. He, J. S. Mukherjee, M. N. Phillips, M. Bunce, S. A. Kalams, R. P. Sekaly, B. D. Walker, and C. Brander. 2001. Substantial differences in specificity of HIV-specific cytotoxic T cells in acute and chronic HIV infection. J. Exp. Med. 193:181-194.
28. 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.
29. Goulder, P. J., Y. Tang, S. I. Pelton, and B. D. Walker. 2000. HLA-B57-restricted cytotoxic T-lymphocyte activity in a single infected subject toward two optimal epitopes, one of which is entirely contained within the other. J. Virol. 74:5291-5299.
30. Hay, C. M., D. J. Ruhl, N. O. Basgoz, C. C. Wilson, J. M. Billingsley, M. P. DePasquale, R. T. D'Aquila, S. M. Wolinsky, J. M. Crawford, D. C. Montefiori, and B. D. Walker. 1999. Lack of viral escape and defective in vivo activation of human immunodeficiency virus type 1-specific cytotoxic T lymphocytes in rapidly progressive infection. J. Virol. 73:5509-5519.
31. Horton, H., T. U. Vogel, D. K. Carter, K. Vielhuber, D. H. Fuller, T. Shipley, J. T. Fuller, K. J. Kunstman, G. Sutter, D. C. Montefiori, V. Erfle, R. C. Desrosiers, N. Wilson, L. J. Picker, S. M. Wolinsky, C. Wang, D. B. Allison, and D. I. Watkins. 2002. Immunization of rhesus macaques with a DNA prime/modified vaccinia virus Ankara boost regimen induces broad simian immunodeficiency virus (SIV)-specific T-cell responses and reduces initial viral replication but does not prevent disease progression following challenge with pathogenic SIVmac239. J. Virol. 76:7187-7202.
32. Jin, X., D. E. Bauer, S. E. Tuttleton, S. Lewin, A. Gettie, J. Blanchard, C. E. Irwin, J. T. Safrit, J. Mittler, L. Weinberger, L. G. Kostrikis, L. Zhang, A. S. Perelson, and D. D. Ho. 1999. Dramatic rise in plasma viremia after CD8(+) T cell depletion in simian immunodeficiency virus-infected macaques. J. Exp. Med. 189:991-998.
33. 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.
34. Klein, M. R., C. A. van Baalen, A. M. Holwerda, S. R. Kerkhof Garde, R. J. Bende, I. P. Keet, J. K. Eeftinck-Schattenkerk, A. D. Osterhaus, H. Schuitemaker, and F. Miedema. 1995. Kinetics of Gag-specific cytotoxic T lymphocyte responses during the clinical course of HIV-1 infection: a longitudinal analysis of rapid progressors and long-term asymptomatics. J. Exp. Med. 181:1365-1372.
35. Koup, R. A., J. T. Safrit, Y. Cao, C. A. Andrews, G. McLeod, W. Borkowsky, C. Farthing, and D. D. Ho. 1994. Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J. Virol. 68:4650-4655.
36. Mellors, J. W., C. R. Rinaldo, Jr., P. Gupta, R. M. White, J. A. Todd, and L. A. Kingsley. 1996. Prognosis in HIV-1 infection predicted by the quantity of virus in plasma. Science 272:1167-1170.
37. Meyerhans, A., G. Dadaglio, J. P. Vartanian, P. Langlade-Demoyen, R. Frank, B. Asjo, F. Plata, and S. Wain-Hobson. 1991. In vivo persistence of a HIV-1-encoded HLA-B27-restricted cytotoxic T lymphocyte epitope despite specific in vitro reactivity. Eur. J. Immunol. 21:2637-2640.
38. + 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.
39. Migueles, S. A., A. C. Laborico, W. L. Shupert, M. S. Sabbaghian, R. Rabin, C. W. Hallahan, D. Van Baarle, S. Kostense, F. Miedema, M. McLaughlin, L. Ehler, J. Metcalf, S. Liu, and M. Connors. 2002. HIV-specific CD8+ T cell proliferation is coupled to perforin expression and is maintained in nonprogressors. Nat. Immunol. 3:1061-1068.
40. 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, H. Horton, N. Wilson, A. L. Hughes, and D. I. Watkins. 2002. Acute phase cytotoxic T lymphocyte escape is a hallmark of simian immunodeficiency virus infection. Nat. Med. 8:493-499.
41. Ogg, G. S., X. Jin, S. Bonhoeffer, P. R. Dunbar, M. A. Nowak, S. Monard, J. P. Segal, Y. Cao, S. L. Rowland-Jones, V. Cerundolo, A. Hurley, M. Markowitz, D. D. Ho, D. F. Nixon, and A. J. McMichael. 1998. Quantitation of HIV-1-specific cytotoxic T lymphocytes and plasma load of viral RNA. Science 279:2103-2106.
42. Oxenius, A., D. A. Price, H. F. Gunthard, S. J. Dawson, C. Fagard, L. Perrin, M. Fischer, R. Weber, M. Plana, F. Garcia, B. Hirschel, A. McLean, and R. E. Phillips. 2002. Stimulation of HIV-specific cellular immunity by structured treatment interruption fails to enhance viral control in chronic HIV infection. Proc. Natl. Acad. Sci. USA 99:13747-13752.
43. Phillips, R. E. 2002. Immunology taught by Darwin. Nat. Immunol. 3:987-989.
44. Plata, F., B. Autran, L. P. Martins, S. Wain-Hobson, M. Raphael, C. Mayaud, M. Denis, J. M. Guillon, and P. Debre. 1987. AIDS virus-specific cytotoxic T lymphocytes in lung disorders. Nature 328:348-351.
45. 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.
46. Schmitz, J. E., M. J. Kuroda, S. Santra, V. G. Sasseville, M. A. Simon, M. A. Lifton, P. Racz, K. Tenner-Racz, M. Dalesandro, B. J. Scallon, J. Ghrayeb, M. A. Forman, D. C. Montefiori, E. P. Rieber, N. L. Letvin, and K. A. Reimann. 1999. Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes. Science 283:857-860.
47. Schmitz, J. E., M. J. Kuroda, S. Santra, M. A. Simon, M. A. Lifton, W. Lin, R. Khunkhun, M. Piatak, J. D. Lifson, G. Grosschupff, R. S. Gelman, P. Racz, K. Tenner-Racz, K. A. Mansfield, N. L. Letvin, D. C. Montefiori, and K. A. Reimann. 2003. Effect of humoral immune responses on controlling viremia during primary infection of rhesus monkeys with simian immunodeficiency virus. J. Virol. 77:2165-2173.
48. Schwartz, O., V. Marechal, S. Le Gall, F. Lemonnier, and J. M. Heard. 1996. Endocytosis of major histocompatibility complex class I molecules is induced by the HIV-1 Nef protein. Nat. Med. 2:338-342.
49. Shankar, P., M. Russo, B. Harnisch, M. Patterson, P. Skolnik, and J. Lieberman. 2000. Impaired function of circulating HIV-specific CD8(+) T cells in chronic human immunodeficiency virus infection. Blood 96:3094-3101.
50. van Baalen, C. A., O. Pontesilli, R. C. Huisman, A. M. Geretti, M. R. Klein, F. de Wolf, F. Miedema, R. A. Gruters, and A. D. Osterhaus. 1997. Human immunodeficiency virus type 1 Rev- and Tat-specific cytotoxic T lymphocyte frequencies inversely correlate with rapid progression to AIDS. J. Gen. Virol. 78:1913-1918.
51. van Baarle, D., S. Kostense, E. Hovenkamp, G. Ogg, N. Nanlohy, M. F. Callan, N. H. Dukers, A. J. McMichael, M. H. van Oers, and F. Miedema. 2002. Lack of Epstein-Barr virus- and HIV-specific CD27- CD8+ T cells is associated with progression to viral disease in HIV-infection. AIDS 16:2001-2011.
52. Vogel, T. U., H. Horton, D. H. Fuller, D. K. Carter, K. Vielhuber, D. H. O'Connor, T. Shipley, J. Fuller, G. Sutter, V. Erfie, N. Wilson, L. J. Picker, and D. I. Watkins. 2002. Differences between T cell epitopes recognized after immunization and after infection. J. Immunol. 169:4511-4521.
53. Wagner, R., B. Leschonsky, E. Harrer, C. Paulus, C. Weber, B. D. Walker, S. Buchbinder, H. Wolf, J. R. Kalden, and T. Harrer. 1999. Molecular and functional analysis of a conserved CTL epitope in HIV-1 p24 recognized from a long-term nonprogressor: constraints on immune escape associated with targeting a sequence essential for viral replication. J. Immunol. 162:3727-3734.
54. Walker, B. D., S. Chakrabarti, B. Moss, T. J. Paradis, T. Flynn, A. G. Durno, R. S. Blumberg, J. C. Kaplan, M. S. Hirsch, and R. T. Schooley. 1987. HIV-specific cytotoxic T lymphocytes in seropositive individuals. Nature 328:345-348.
55. Wherry, E. J., J. N. Blattman, K. Murali-Krishna, R. van der Most, and R. Ahmed. 2003. Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment. J. Virol. 77:4911-4927.
56. Wodarz, D., and V. A. Jansen. 2001. The role of T cell help for anti-viral CTL responses. J. Theor. Biol. 211:419-432.
57. Yang, O. O., P. T. Sarkis, A. Ali, J. D. Harlow, C. Brander, S. A. Kalams, and B. D. Walker. 2003. Determinants of HIV-1 mutational escape from cytotoxic T lymphocytes. J. Exp. Med. 197:1365-1375.
58. Zhang, D., P. Shankar, Z. Xu, B. Harnisch, G. Chen, C. Lange, S. J. Lee, H. Valdez, M. M. Lederman, and J. Lieberman. 2003. Most antiviral CD8 T cells during chronic viral infection do not express high levels of perforin and are not directly cytotoxic. Blood 101:226-235.