Suppression of human immunodeficiency virus type 1 replication by CD8+ cells: Evidence for HLA class I-restricted triggering of cytolytic and noncytolytic mechanisms

Journal of Virology

Volumn 71, Issue 4, 1997, Pages 3120-3128

  Yang, Otto O ^a,b   Kalams, Spyros A ^a   Trocha, Alicja ^a   Cao, Huyen ^a   Luster, Andrew ^a   Johnson, R Paul ^a   Walker, Bruce D ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b Infectious Disease Unit   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; CHEMOKINE; HLA ANTIGEN CLASS 1; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; RANTES;

ANTIGEN SPECIFICITY; ARTICLE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; EFFECTOR CELL; HLA MATCHING; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; MAJOR HISTOCOMPATIBILITY COMPLEX RESTRICTION; PRIORITY JOURNAL; T LYMPHOCYTE SUBPOPULATION; VIRUS INHIBITION;

EID: 0030997137     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.71.4.3120-3128.1997     Document Type: Article

References (70)

1. Alkhatib, G., C. Combadiere, C. C. Broder, Y. Feng, P. E. Kennedy, P. M. Murphy, and E. A. Berger. 1996. CC CKR5: a RANTES, MIP-1α, MIP-1β receptor as a fusion cofactor for macrophage-tropic HIV-1. Science 272: 1955-1958.
2. Anderson, J., J. A. Byrne, R. Schreiber, S. Patterson, and M. B. A. Oldstone. 1985. Biology of cloned cytotoxic T lymphocytes specific for lymphocytic choriomeningitis virus: clearance of virus and in vitro properties. J. Virol. 53:552-560.
3. Baier, M., A. Werner, N. Bannert, K. Metzner, and R. Kurth. 1995. HIV suppression by interleukin-16. Nature 378:563.
4. Bleui, C. C., M. Farzan, H. Choe, C. Parolin, I. dark-Lewis, J. Sodroski, and T. A. Springer. 1996. The lymphocyte chemoattractant SDF-1 is a ligand for LESTR/fusin and blocks HIV-1 entry. Nature 382:829-832.
5. + cytotoxic T-lymphocyte activity associated with control of viremia in primary human immunodeficiency virus type 1 infection. J. Virol. 68:6103-6110.
6. Brinchmann, J. E., G. Gaudernack, and F. Vartdal. 1990. CD8+ T cells inhibit HIV replication in naturally infected CD4+ T cells. Evidence for a soluble inhibitor. J. Immunol. 144:2961-2966.
7. Carmichael, A., X. Jin, P. Sissons, and L. Borysiewicz. 1993. Quantitative analysis of the human immunodeficiency virus type 1 (HIV-1)-specific cytotoxic T lymphocyte (CTL) response at different stages of HIV-1 infection: differential CTL responses to HIV-1 and Epstein-Barr virus in late disease. J. Exp. Med. 177:249-256.
8. Chen, C.-H., K. Weinhold, J. A. Bartlett, D. P. Bolognesi, and M. L. Greenberg. 1993. CD8 T lymphocyte-mediated inhibition of HIV-1 long terminal repeat transcription: a novel antiviral mechanism. AIDS Res. Hum. Retroviruses 9:1079-1086.
9. Cocchi, F., A. L. DeVico, A. Garzino-Demo, S. K. Arya, R. C. Gallo, and P. Lusso. 1996. Identification of RANTES, MIP-1α, and MIP-1β as the major HIV-suppressive factors produced by CD8+ T cells. Science 270:1811-1815.
10. + A24-restricted cytotoxic T lymphocytes. J. Virol. 66:3151-3154.
11. Deng, H., R. Lui, W. Ellmeier, S. Choe, D. Unutmaz, M. Burkhart, P. Di Marzio, S. Marmon, R. E. Sutton, C. M. Hill, C. B. Davis, S. C. Peiper, T. J. Schall, D. R. Littman, and N. R. Landau. 1996. Identification of a major co-receptor for primary isolates of HIV-1. Nature 381:661-666.
12. Denner, J., S. Norley, and R. Kurth. 1994. The immunosuppressive peptide of HIV-1: functional domains and immune response in AIDS patients. AIDS 8:1063-1072.
13. Dragic, T., V. Litwin, G. P. Allaway, S. R. Martin, Y. Huang, K. A. Nagashima, C. Cayanan, P. J. Maddon, R. A. Koup, J. P. Moore, and W. A. Paxton. 1996. HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CC-CKR-5. Nature 381:667-673.
14. Feng, Y., C. C. Broder, P. E. Kennedy, and E. A. Berger. 1996. HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane. G protein-coupled receptor. Science 272:872-877.
15. Ferbas, J., A. H. Kaplan, M. A. Hausner, L. E. Hultin, J. L. Matud, L. Zhiyuan, D. L. Panicali, H. Nerng-Ho, R. Detels, and J. V. Giorgi. 1995. Virus burden in long-term survivors of human immunodeficiency virus (HIV) infection is a determinant of anti-HIV CD8+ lymphocyte activity. J. Infect. Dis. 172:329-339.
16. Gartner, S., and M. Popovic. 1990. Virus isolation and production, p. 53-66. In A. Aldovini and B. D. Walker (ed.). Techniques in HIV research. Stockton Press, New York, N.Y.
17. Griffith, T. S., T. Brunner, S. M. Fletcher, D. R. Green, and T. A. Ferguson. 1995. Fas ligand-induced apoptosis as a mechanism of immune privilege. Science 279:1189-1192.
18. Guidotti, L. G., T. Ishikawa, M. V. Hobbs, B. Matzke, R. Schreiber, and F. Chisari. 1946. Intracellular inactivation of hepatitis B virus by cytotoxic T lymphocytes. Immunity 4:25-36.
19. Harrer, T., E. Harrer, S. A. Kalams, P. Barbosa, A. Trocha, R. P. Johnson, T. Elbeik, M. B. Feinberg, S. P. Buchbinder, and B. D. Walker. 1996. Cytotoxic T lymphocytes in asymptomatic long-term nonprogressing HIV-1 infection. J. Immunol. 156:2616-2623.
20. Harrer, T., E. Harrer, S. A. Kalams, A. Trocha, R. P. Johnson, T. Elbeik, M. Feinberg, Y. Cao, D. D. Ho, S. Buchbinder, and B. Walker. 1996. Strong cytotoxic T cells and weak neutralizing antibodies in long-term non-progressing HIV-1 infection. AIDS Res. Hum. Retroviruses 12:585-592.
21. Ho, D. D., A. U. Neumann, A. S. Perelson, W. Chen, J. M. Leonard, and M. Markowitz. 1995. Rapid turnover of plasma virions and CD4 lymphocytes in HIV-1 infection. Nature 373:123-126.
22. Howcroft, T. K., K. Strebel, M. A. Martin, and D. S. Singer. 1993. Repression of MHC class I gene promoter activity by two-exon tat of HIV. Science 260:1320-1322.
23. Jassoy, C. J., T. Harrer, T. Rosenthal, B. A. Navia, J. Worth, R. P. Johnson, and B. D. Walker. 1993. HIV-1-specific cytotoxic T cells release interferon gamma, tumor necrosis factor (TNF)-alpha and TNF-beta when they encounter their target antigens. J. Virol. 67:2844-2852.
24. Johnson, R., and B. Walker. 1994. Cytotoxic T lymphocytes in HIV infection: responses to structural proteins. Curr. Opin. Microbiol. Immunol. 189:35-63.
25. Johnson, R. P., A. Trocha, T. M. Buchanan, and B. D. Walker. 1992. Identification of overlapping HLA class I-restricted cytotoxic T cell epitopes in a conserved region of the human immunodeficiency virus type 1 envelope glycoprotein: definition of minimum epitopes and analysis of the effects of sequence variation. J. Exp. Med. 175:961-971.
26. Johnson, R. P., A. Trocha, L. Yang, G. P. Mazzara, D. L. Panicali. T. M. Buchanan, and B. D. Walker. 1991. HIV-1 gag-specific cytotoxic T lymphocytes recognize multiple highly conserved epitopes. Fine specificity of the gag-specific response defined by using unstimulated peripheral blood mononuclear cells and cloned effector cells. J. Immunol. 147:1512-1521.
27. Johnson, V. A., and B. D. Walker. 1990. HIV-infected cell fusion assay, p. 92-94. In A. Aldovini and B. D. Walker (ed.), Techniques in HIV research. Stockton Press. New York, N.Y.
28. Kagi, D., B. Ledermann, K. Burki, R. M. Zinkernagel, and H. Hengartner. 1996. Molecular mechanisms of lymphocyte-mediated cytotoxicity and their role in immunological protection and pathogenesis in vivo. Annu. Rev. Immunol. 14:207-232.
29. Kalams, S. Unpublished data.
30. Kalams, S. A., R. P. Johnson, A. K. Trocha, M. J. Dynan, H. S. Ngo, R. T. D'Aquila, J. T. Kurnick, and B. D. Walker. 1994. Longitudinal analysis of T cell receptor (TCR) gene usage by human immunodeficiency virus 1 envelope-specific cytotoxic T lymphocyte clones reveals a limited TCR repertoire. J. Exp. Med. 179:1261-1271.
31. Kerkau, T., L. R. Schmitt, A. Schimpl, and E. Wecker. 1989. Downregulation of HLA class I antigens in HIV-1-infected cells. AIDS Res. Hum. Retroviruses 5:613-620.
32. Klein, M. R., and C. A. van Baalen. 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. 181:1356-1372.
33. Klenerman, P., S. Rowland-Jones, S. McAdam, J. Edwards, S. Daenke, D. Lalloo, B. Koppe, W. Rosenberg, D. Boyd, A. Edwards, P. Giagrande, R. E. Phillips, and A. J. McMichael. 1994. Naturally occurring HIV-1 gag variants antagonise cytotoxic T cell activity. Nature 369:403-406.
34. 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.
35. Kovacs, J. A., M. Baseler, R. J. Dewar, S. Vogel, R. T. Davey, J. Falloon, M. A. Polis, R. E. Walker, R. Stevens, N. P. Salzman, J. A. Metcalf, H. Masur, and H. C. Lane. 1996. Increases in CD4 T lymphocytes with intermittent courses of interleukin-2 in patients with human immunodeficiency virus infection. A preliminary study. N. Engl. J. Med. 332:567-575.
36. Koyanagi, Y., S. Miles, R. T. Mitsuyasu, J. E. Merrill, H. V. Vinters, and I. S. Y. Chen. 1987. Dual infection of the central nervous system by AIDS viruses with distinct cellular tropisms. Science 236:819-822.
37. Koziel, M. J., D. Dudley, J. T. Wong, J. Dienstag, M. Houghton, R. Ralston, and B. D. Walker. 1992. Intrahepatic cytotoxic T lymphocytes specific for hepatitis C virus in persons with chronic hepatitis. J. Immunol. 149:3339-3344.
38. Langlade-Demoyen, P., N. Ngo-Giang-Huong, F. Ferchal, and E. Oksenhendler. 1993. Human immunodeficiency virus (HIV) nef-specific cytotoxic T lymphocytes in noninfected heterosexual contacts of HIV-infected patients. J. Clin. Invest. 93:1293-1297.
39. Levy, J. A., C. E. Mackewicz, and E. Barker. 1996. Controlling HIV pathogenesis: the role of the noncytotoxic anti-HIV response of CD8+ T cells. Immunol. Today 17:217-224.
40. + T-cell clone (PM1): failure to downregulate CD4 and to interfere with cell-line-tropic HIV-1. J. Virol. 69:3712-3720.
41. Mackewicz, C., and J. A. Levy. 1992. CD8+ cell anti-HIV activity: nonlytic suppression of virus replication. AIDS Res. Hum. Retroviruses 8:1039-1050.
42. Mackewicz, C. E., D. J. Blackbourn, and J. A. Levy. 1995. CDS+ T cells suppress human immunodeficiency virus replication by inhibiting viral transcription. Proc. Natl. Acad. Sci. USA 92:2308-2312.
43. Moskophidis, D., F. Lechner, H. Pircher, and R. M. Zinkernagel. 1993. Virus persistence in acutely infected immunocompetent mice by exhaustion of antiviral cytotoxic effector T cells. Nature 362:758-761.
44. Moss, P. A., 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.
45. Oberlin, E., A. Amara, F. Bachelerie, C. Bessia, J. Verelizier, F. Arenzana-Seisdedos, O. Schwartz, J. Heard, I. dark-Lewis, D. F. Legler, M. Loetscher, M. Baggiolini, and B. Moser. 1996. The CXC chemokine SDF-1 is the ligand for LESTR/fusin and prevents infection by T-cell-adapted line HIV-1. Nature 382:833-835.
46. Oldstone, M. B. A. 1986. Cytoimmunotherapy for persistent virus infection reveals a unique clearance pattern from the central nervous system. Nature 321:239-243.
47. Perelson, A. S., A. U. Neumann, M. Markowitz, J. M. Leonard, and D. D. Ho. 1996. HIV-1 dynamics in vivo: virion clearance rate, infected cell lifespan, and viral generation time. Science 271:1582-1586.
48. Phillips, R. E., J. S. Rowland, 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.
49. Pinto, L. A., J. Sullivan, J. A. Berzofsky, M. Clerici, H. A. Kessler, A. L. Landay, and G. M. Shearer. 1995. Env-specific cytotoxic T lymphocyte responses in HIV seronegative health care workers occupationally exposed to HIV-contaminated body fluids. J. Clin. Invest. 96:867-876.
50. Reusser, P., S. R. Riddell, J. D. Meyers, and P. D. Greenberg. 1991. Cytotoxic T-lymphocyte response to cytomegalovirus after human allogeneic bone marrow transplantation: pattern of recovery and correlation with cytomegalovirus infection and disease. Blood 78:1373-1380.
51. 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-human immunodeficiency virus type 1 (HIV-1) memory cytotoxic T-lymphocyte activity and low viral load are associated with lack of disease in HIV-1-infected long-term nonprogressors. J. Virol. 69:5838-5842.
52. Rowland-Jones, S., J. Sutton, K. Ariyoski, T. Dong, F. Gotch, S. McAdam, D. Whitby, S. Sabally, A. Gallimore, T. Corrah, M. Takiguchi, T. Schultz, A. McMichael, and H. Whittle. 1995. HIV-specific cytotoxic T-cells in HIV-exposed but uninfected Gambian women. Nat. Med. 1:59-64.
53. Salter, R. D., D. N. Howell, and P. Cresswell. 1985. Genes regulating HLA class I antigen expression in T-B lymphoblast hybrids. Immunogenetics 21: 235-246.
54. Scheppler, J. A., J. K. Nicholson, D. C. Swan, A. A. Ahmed, and J. S. McDougal. 1989. Down-modulation of MHC-I in a CD4+ T cell line, CEM-E5, after HIV-1 infection. J. Immunol. 143:2858-2866.
55. 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.
56. Takahashi, H., S. Merli, S. D. Putney, R. Houghten, B. Moss, R. N. Germain, and J. A. Berzofsky. 1989. A single amino acid interchange yields reciprocal CTL specificities for HIV-1 gp160. Science 246:118-121.
57. Toso, J. F., C.-H. Chen, J. R. Mohr, L. Piglia, C. Oei, G. Ferrari, M. L. Greenberg, and K. J. Weinhold. 1995. Oliguclonal CD8 lymphocytes from persons with asymptomatic human immunodeficiency virus (HIV) type 1 infection inhibit HIV-1 replication. J. Infect. Dis. 172:964-973.
58. Tsubota, H., C. I. Lord, D. I. Watkins, C. Morimoto, and N. L. Letvin. 1989. A cytotoxic T lymphocyte inhibits acquired immunodeficiency syndrome virus replication in peripheral blood lymphocytes. J. Exp. Med. 169:1421-1434.
59. Walker, B. D., C. Flexner, L. K. Birch, L. Fisher, T. J. Paradis, A. Aldovini, R. Young, B. Moss, and R. T. Schooley. 1989. Long-term culture and fine specificity of human cytotoxic T-lymphocyte clones reactive with human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. USA 86:9514-9518.
60. + cells involves a noncytotoxic mechanism. J. Virol. 65:5921-5927.
61. Walker, C. M., and J. A. Levy. 1989. A diffusible lymphokine produced by CDS+ T lymphocytes suppresses HIV replication. Immunology 66:628-630.
62. Walker, C. M., D. J. Moody, D. P. Stites, and J. A. Levy. 1986. CD8+ lymphocytes can control HIV infection in vitro by suppressing virus replication. Science 234:1563-1566.
63. Walker, C. M., G. A. Thomson-Honnebier, F. C. Hsueh, A. L. Erickson, L. Z. Pan, and J. A. Levy. 1991. CD8+ T cells from HIV-1-infected individuals inhibit acute infection by human and primate immunodeficiency viruses. Cell Immunol. 137:420-428.
64. Wei, X., S. K. Ghosh, M. E. Taylor, V. A. Johnson, E. A. Emini, P. Deutsch, J. D. Lifson, S. Bonhoeffer, M. A. Nowak, B. H. Hahn, M. S. Saag, and G. M. Shaw. 1995. Viral dynamics in human immunodeficiency virus type 1 infection. Nature 373:117-122.
65. Wilson, C. C., J. T. Wong, D. Girard, D. P. Merril, M. Dynan, D. An, S. A. Kalams, R. P. Johnson, M. S. Hirsch, R. T. D'Aquila, and B. D. Walker. 1995. Ex vivo expansion of CD4+ lymphocytes from HIV-1 infected persons in the presence of combination untiretroviral therapy. J. Infect. Dis. 172:88-96.
66. Wiviott, L. D., C. M. Walker, and J. A. Levy. 1990. CD8+ lymphocytes suppress HIV production by autologous CD4+ cells without eliminating the infected cells from culture. Cell. Immunol. 128:628-634.
67. Wong, J. T., and R. B. Colvin. 1987. Bi-specific monoclonal antibodies: selective binding and complement fixation to cells that express two different surface antigens. J. Immunol. 139:1369-1374.
68. Yang, O. O., S. Kalams, M. Rosenzwieg, A. Trocha, M. Koziel, B. D. Walker, and R. P. Johnson. 1996. Efficient lysis of HIV-1 infected cells by cytotoxic T lymphocytes. J. Virol. 70:5799-5806.
69. Yap, K. L., G. L. Ada, and I. F. McKenzie. 1978. Transfer of specific cytotoxic T lymphocytes protects mice inoculated with influenza virus. Nature 273: 238-239.
70. Zinkernagel, R. M., and A. Althage. 1977. Antiviral protection by virus-immune cytotoxic T cells. Infected target cells are lysed before infectious virus progeny is assembled. J. Exp. Med. 145:644-651.