Immunodomination in the evolution of dominant epitope-specific CD8 + T lymphocyte responses in simian immunodeficiency virus-infected rhesus monkeys

Journal of Immunology

Volumn 176, Issue 1, 2006, Pages 319-328

  Newberg, Michael H ^a   McEvers, Kimberly J ^a   Gorgone, Darci A ^a   Lifton, Michelle A ^a   Baumeister, Susanne H C ^a   Veazey, Ronald S ^b   Schmitz, Jörn E ^a   Letvin, Norman L ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; GAG PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NEF PROTEIN; TRANSACTIVATOR PROTEIN;

ANTIGEN EXPRESSION; ANTIGEN RECOGNITION; ARTICLE; CD8+ T LYMPHOCYTE; EVOLUTION; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNE RESPONSE; NONHUMAN; PRIORITY JOURNAL; RHESUS MONKEY; SIMIAN IMMUNODEFICIENCY VIRUS; VIRUS INFECTION; VIRUS LOAD; VIRUS MUTATION; VIRUS REPLICATION;

EID: 29644433171     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.176.1.319     Document Type: Article

References (53)

1. + lymphocytes can control HIV infection in vitro by suppressing virus replication. Science 234: 1563-1566.
2. 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.
3. Kuroda, M. J., J. E. Schmitz, W. A. Charini, C. E. Nickerson, M. A. Lifton, C. I. Lord, M. A. Forman, and N. L. Letvin. 1999. Emergence of CTL coincides with clearance of virus during primary simian immunodeficiency virus infection in rhesus monkeys. J. Immunol. 162: 5127-5133.
4. Matano, T., R. Shibata, C. Siemon, M. Connors, H. C. Lane, and M. A. Martin. 1998. Administration of an anti-CD8 monoclonal antibody interferes with the clearance of chimeric simian/human immunodeficiency virus during primary infections of rhesus macaques. J. Virol. 72: 164-169.
5. + T cell depletion in simian immunodeficiency virus-infected macaques. J. Exp. Med. 189: 991-998.
6. + lymphocytes. Science 283: 857-860.
7. Goulder, P. J., R. E. Phillips, R. A. Colbert, S. McAdam, G. Ogg, M. A. Nowak, P. Giangrande, G. Luzzi, B. Morgan, A. Edwards, et al. 1997. Late escape from an immunodominant cytotoxic T-lymphocyte response associated with progression to AIDS. Nat. Med. 3: 212-217.
8. 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.
9. Barouch, D. H., J. Kunstman, J. Glowczwskie, K. J. Kunstman, M. A. Egan, F. W. Peyerl, S. Santra, M. J. Kuroda, J. E. Schmitz, K. Beaudry, et al. 2003. Viral escape from dominant simian immunodeficiency virus epitope-specific cytotoxic T lymphocytes in DNA-vaccinated rhesus monkeys. J. Virol. 77: 7367-7375.
10. Tang, J., C. Costello, I. P. Keet, C. Rivers, S. Leblanc, E. Karita, S. Allen, and R. A. Kaslow. 1999. HLA class I homozygosity accelerates disease progression in human immunodeficiency virus type 1 infection. AIDS Res. Hum. Retroviruses 15: 317-324.
11. Keet, I. P., J. Tang, M. R. Klein, S. LeBlanc, C. Enger, C. Rivers, R. J. Apple, D. Mann, J. J. Goedert, F. Miedema, and R. A. Kaslow. 1999. Consistent associations of HLA class I and II and transporter gene products with progression of human immunodeficiency virus type 1 infection in homosexual men. J. Infect. Dis. 180: 299-309.
12. Carrington, M., G. W. Nelson, M. P. Martin, T. Kissner, D. Vlahov, J. J. Goedert, R. Kaslow, S. Buchbinder, K. Hoots, and S. J. O'Brien. 1999. HLA and HIV-1: heterozygote advantage and B*35-Cw*04 disadvantage. Science 283: 1748-1752.
13. Amara, R. R., F. Villinger, J. D. Altman, S. L. Lydy, S. P. O'Neil, S. I. Staprans, D. C. Montefiori, Y. Xu, J. G. Herndon, L. S. Wyatt, et al. 2001. Control of a mucosal challenge and prevention of AIDS by a multiprotein DNA/MVA vaccine. Science 292: 69-74.
14. 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, et al. 2000. Control of viremia and prevention of clinical AIDS in rhesus monkeys by cytokine-augmented DNA vaccination. Science 290: 486-492.
15. Egan, M. A., W. A. Charini, M. J. Kuroda, J. E. Schmitz, P. Racz, K. Tenner-Racz, K. Manson, M. Wyand, M. A. Lifton, C. E. Nickerson, et al. 2000. Simian immunodeficiency virus (SIV) gag DNA-vaccinated rhesus monkeys develop secondary cytotoxic T-lymphocyte responses and control viral replication after pathogenic SIV infection. J. Virol. 74: 7485-7495.
16. Seth, A., I. Ourmanov, M. J. Kuroda, J. E. Schmitz, M. W. Carroll, L. S. Wyatt, B. Moss, M. A. Forman, V. M. Hirsch, and N. L. Letvin. 1998. Recombinant modified vaccinia virus Ankara-simian immunodeficiency virus gag pol elicits cytotoxic T lymphocytes in rhesus monkeys detected by a major histocompatibility complex class I/peptide tetramer. Proc. Natl. Acad. Sci. USA 95: 10112-10116.
17. Letvin, N. L. 2005. Progress toward an HIV vaccine. Annu. Rev. Med. 56: 213-223.
18. 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.
19. von Herrath, M. G., J. Dockter, M. Nerenberg, J. E. Gairin, and M. B. Oldstone. 1994. Thymic selection and adaptability of cytotoxic T lymphocyte responses in transgenic mice expressing a viral protein in the thymus. J. Exp. Med. 180: 1901-1910.
20. + T cell epitopes, virus load, and kinetics of primary antiviral CTL response. J. Immunol. 160: 2923-2931.
21. van der Most, R. G., L. E. Harrington, V. Giuggio, P. L. Mahar, and R. Ahmed. 2002. Yellow fever virus 17D envelope and NS3 proteins are major targets of the antiviral T cell response in mice. Virology 296: 117-124.
22. Kuroda, M. J., J. E. Schmitz, D. H. Barouch, A. Craiu, T. M. Allen, A. Sette, D. I. Watkins, M. A. Forman, and N. L. Letvin. 1998. Analysis of Gag-specific cytotoxic T lymphocytes in simian immunodeficiency virus-infected rhesus monkeys by cell staining with a tetrameric major histocompatibility complex class I-peptide complex. J. Exp. Med. 187: 1373-1381.
23. + cytotoxic T lymphocytes specific for dominant and nondominant viral epitopes in simian-human immunodeficiency virus-infected rhesus monkeys. J. Virol. 73: 5466-5472.
24. 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.
25. Newberg, M. H., M. J. Kuroda, W. A. Charini, A. Miura, C. I. Lord, J. E. Schmitz, D. A. Gorgone, M. A. Lifton, K. Kuus-Reichel, and N. L. Letvin. 2002. A simian immunodeficiency virus nef peptide is a dominant cytotoxic T lymphocyte epitope in Indian-origin rhesus monkeys expressing the common MHC class I allele mamu-A*02. Virology 301: 365-373.
26. Garboczi, D. N., D. T. Hung, and D. C. Wiley. 1992. HLA-A2-peptide complexes: refolding and crystallization of molecules expressed in Escherichia coli and complexed with single antigenic peptides. Proc. Natl. Acad. Sci. USA 89: 3429-3433.
27. Knapp, L. A., E. Lehmann, M. S. Piekarczyk, J. A. Urvater, and D. I. Watkins. 1997. A high frequency of Mamu-A*01 in the rhesus macaque detected by polymerase chain reaction with sequence-specific primers and direct sequencing. Tissue Antigens 50: 657-661.
28. Robinson, S., W. A. Charini, M. H. Newberg, M. J. Kuroda, C. I. Lord, and N. L. Letvin. 2001. A commonly recognized simian immunodeficiency virus Nef epitope presented to cytotoxic T lymphocytes of Indian-origin rhesus monkeys by the prevalent major histocompatibility complex class I allele Mamu-A*02. J. Virol. 75: 10179-10186.
29. 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.
30. Mothe, B. R., H. Horton, D. K. Carter, T. M. Allen, M. E. Liebl, P. Skinner, T. U. Vogel, S. Fuenger, K. Vielhuber, W. Rehrauer, et al. 2002. Dominance of CD8 responses specific for epitopes bound by a single major histocompatibility complex class I molecule during the acute phase of viral infection. J. Virol. 76: 875-884.
31. Miller, M. D., H. Yamamoto, A. L. Hughes, D. I. Watkins, and N. L. Letvin. 1991. Definition of an epitope and MHC class 1 molecule recognized by gag-specific cytotoxic T lymphocytes in SIVmac-infected rhesus monkeys. J. Immunol. 147: 320-329.
32. Allen, T. M., J. Sidney, M. F. del Guercio, R. L. Glickman, G. L. Lensmeyer, D. A. Wiebe, R. DeMars, C. D. Pauza, R. P. Johnson, A. Sette, and D. I. Watkins. 1998. Characterization of the peptide binding motif of a rhesus MHC class I molecule (Mamu-A*01) that binds an immunodominant CTL epitope from simian immunodeficiency virus. J. Immunol. 160: 6062-6071.
33. + lymphocytes from simian immunodeficiency virus-infected rhesus macaques recognize 14 different epitopes bound by the major histocompatibility complex class I molecule mamu-A*01: implications for vaccine design and testing. J. Virol. 75: 738-749.
34. Furchner, M., A. L. Erickson, T. Allen, D. I. Watkins, A. Sette, P. R. Johnson, and C. M. Walker. 1999. The simian immunodeficiency virus envelope glycoprotein contains two epitopes presented by the Mamu-A*01 class I molecule. J. Virol. 73: 8035-8039.
35. 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 histocompatibility complex class I molecule, Mamu-A*02: a paradigm for virus evolution and persistence? J. Virol. 76: 11623-11636.
36. + T cell epitopes restricted by the high frequency molecule, Mamu-A*02, and potential escape from CTL recognition. J. Immunol. 173: 5064-5076.
37. Mothe, B. R., J. Weinfurter, C. Wang, W. Rehrauer, N. Wilson, T. M. Allen, D. B. Allison, and D. I. Watkins. 2003. Expression of the major histocompatibility complex class I molecule Mamu-A*01 is associated with control of simian immunodeficiency virus SIVmac239 replication. J. Virol. 77: 2736-2740.
38. Muhl, T., M. Krawczak, P. Ten Haaft, G. Hunsmann, and U. Sauermann. 2002. MHC class I alleles influence set-point viral load and survival time in simian immunodeficiency virus-infected rhesus monkeys. J. Immunol. 169: 3438-3446.
39. O'Connor, D. H., B. R. Mothe, J. T. Weinfurter, S. Fuenger, W. M. Rehrauer, P. Jing, R. R. Rudersdorf, M. E. Liebl, K. Krebs, J. Vasquez, et al. 2003. Major histocompatibility complex class I alleles associated with slow simian immunodeficiency virus disease progression bind epitopes recognized by dominant acute-phase cytotoxic-T-lymphocyte responses. J. Virol. 77: 9029-9040.
40. Pal, R., D. Venzon, N. L. Letvin, S. Santra, D. C. Montefiori, N. R. Miller, E. Tryniszewska, M. G. Lewis, T. C. VanCott, V. Hirsch, et al. 2002. ALVAC-SIV-gag-pol-env-based vaccination and macaque major histocompatibility complex class I (A*01) delay simian immunodeficiency virus SIVmac-induced immunodeficiency. J. Virol. 76: 292-302.
41. Zhang, Z. Q., T. M. Fu, D. R. Casimiro, M. E. Davies, X. Liang, W. A. Schleif, L. Handt, L. Tussey, M. Chen, A. Tang, et al. 2002. Mamu-A*01 allele-mediated attenuation of disease progression in simian-human immunodeficiency virus infection. J. Virol. 76: 12845-12854.
42. Sandberg, J. K., P. Grufman, E. Z. Wolpert, L. Franksson, B. J. Chambers, and K. Karre. 1998. Superdominance among immunodominant H-2Kb-restricted epitopes and reversal by dendritic cell-mediated antigen delivery. J. Immunol. 160: 3163-3169.
43. Kedl, R. M., W. A. Rees, D. A. Hildeman, B. Schaefer, T. Mitchell, J. Kappler, and P. Marrack. 2000. T cells compete for access to antigen-bearing antigen-presenting cells. J. Exp. Med. 192: 1105-1113.
44. Kedl, R. M., B. C. Schaefer, J. W. Kappler, and P. Marrack. 2002. T cells downmodulate peptide-MHC complexes on APCs in vivo. Nat. Immunol. 3: 27-32.
45. Loyer, V., P. Fontaine, S. Pion, F. Hetu, D. C. Roy, and C. Perreault. 1999. The in vivo fate of APCs displaying minor H antigen and/or MHC differences is regulated by CTLs specific for immunodominant class 1-associated epitopes. J. Immunol. 163: 6462-6467.
46. Roy-Proulx, G., M. C. Meunier, A. M. Lanteigne, S. Brochu, and C. Perreault. 2001. Immunodomination results from functional differences between competing CTL. Eur. J. Immunol. 31: 2284-2292.
47. + T cell responses to influenza A virus: roles for cross-presentation and lysis-independent immunodomination. J. Immunol. 173: 5021-5027.
48. Eberl, G., B. Kessler, L. P. Eberl, M. J. Brunda, D. Valmori, and G. Corradin. 1996. Immunodominance of cytotoxic T lymphocyte epitopes co-injected in vivo and modulation by interleukin-12. Eur. J. Immunol. 26: 2709-2716.
49. Rowley, D. A., and R. M. Stach. 1993. A first or dominant immunization. I. Suppression of simultaneous cytolytic T cell responses to unrelated alloantigens. J. Exp. Med. 178: 835-840.
50. Stach, R. M., and D. A. Rowley. 1993. A first or dominant immunization. II. Induced immunoglobulin carries transforming growth factor-β and suppresses cytolytic T cell responses to unrelated alloantigens. J. Exp. Med. 178: 841-852.
51. Rowley, D. A., and R. M. Stach. 1998. B lymphocytes secreting IgG linked to latent transforming growth factor-β prevent primary cytolytic T lymphocyte responses. Int. Immunol. 10: 355-363.
52. + T-cell responses against Epstein-Barr virus. Scand. J. Immunol. 55: 189-195.
53. + T-lymphocyte immune responses to human cytomegalovirus pp65 in persons sharing HLA-A*02 and HLA-B*07 alleles. Hum. Immunol. 64: 440-452.