Determinants of HIV-1 mutational escape from cytotoxic T lymphocytes

Journal of Experimental Medicine

Volumn 197, Issue 10, 2003, Pages 1365-1375

  Yang, Otto O ^a   Sarki, Phuong Thi Nguyen ^b   Ali, Ayub ^a   Harlow, Jason D ^b   Brander, Christian ^b   Kalams, Spyros A ^b   Walker, Bruce D ^b  

^a UCLA MEDICAL CENTER   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Antigenic variation; Cellular immunity; T cell receptor; T cell receptor specificity

Indexed keywords

ANTIRETROVIRUS AGENT; CD8 ANTIGEN; EPITOPE; GAG PROTEIN; NEF PROTEIN; T LYMPHOCYTE RECEPTOR; RNA DIRECTED DNA POLYMERASE;

ANIMAL CELL; ANTIGEN RECOGNITION; ANTIGENIC VARIATION; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; FRAMESHIFT MUTATION; GENE MUTATION; GENOTYPE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR CLONING; MUTATIONAL ANALYSIS; NONHUMAN; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; RAT; VIRAL GENETICS; VIRUS REPLICATION; AMINO ACID SEQUENCE; CELL LINE; GENETICS; IMMUNOLOGY; MOLECULAR GENETICS; MUTATION;

AMINO ACID SEQUENCE; CELL LINE; EPITOPES; GENE PRODUCTS, GAG; GENE PRODUCTS, NEF; HIV-1; HIV-1 REVERSE TRANSCRIPTASE; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; T-LYMPHOCYTES, CYTOTOXIC;

EID: 0038190811     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20022138     Document Type: Article

References (62)

1. Borrow, P., H. Lewicki, B.H. Hahn, G.M. Shaw, and M.B. Oldstone. 1994. Virus-specific CD8+ cytotoxic T-lymphocyte activity associated with control of viremia in primary human immunodeficiency virus type 1 infection. J. Virol. 68:6103-6110.
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. Harrer, T., E. Harrer, S.A. Kalams, T. Elbeik, S.I. Staprans, M.B. Feinberg, Y. Cao, D.D. Ho, T. Yilma, A.M. Caliendo, et al. 1996. Strong cytotoxic T cell and weak neutralizing antibody responses in a subset of persons with stable nonprogressing HIV type 1 infection. AIDS Res. Hum. Retroviruses. 12:585-592.
4. Rinaldo, C., X.L. Huang, Z.F. Fan, M. Ding, L. Beltz, A. Logar, D. Panicali, G. Mazzara, J. Liebmann, M. Cottrill, et al. 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.
5. 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, et al. 1998. Quantitation of HIV-1-specific cytotoxic T lymphocytes and plasma load of viral RNA. Science. 279:2103-2106.
6. Rowland-Jones, S., J. Sutton, K. Ariyoshi, T. Dong, F. Gotch, S. McAdam, D. Whitby, S. Sabally, A. Gallimore, T. Corrah, et al. 1995. HIV-specific cytotoxic T-cells in HIV-exposed but uninfected Gambian women. Nat. Med. 1:59-64.
7. Langlade-Demoyen, P., N. Ngo-Giang-Huong, F. Ferchal, and E. Oksenhendler. 1994. Human immunodeficiency virus (HIV) nef-specific cytotoxic T lymphocytes in noninfected heterosexual contact of HIV-infected patients. J. Clin. Invest. 93:1293-1297.
8. Schmechel, S.C., N. Russell, F. Hladik, J. Lang, A. Wilson, R. Ha, A. Desbien, and M.J. McElrath. 2001. Immune defence against HIV-1 infection in HIV-1-exposed seronegative persons. Immunol. Lett. 79:21-27.
9. Buseyne, F., M. Fevrier, S. Garcia, M.L. Gougeon, and Y. Riviere. 1996. Dual function of a human immunodeficiency virus (HIV)-specific cytotoxic T-lymphocyte clone: inhibition of HIV replication by noncytolytic mechanisms and lysis of HIV-infected CD4+ cells. Virology. 225:248-253.
10. 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.
11. van Baalen, C.A., M. Schutten, R.C. Huisman, P.H. Boers, R.A. Gruters, and A.D. Osterhaus. 1998. Kinetics of antiviral activity by human immunodeficiency virus type 1-specific cytotoxic T lymphocytes (CTL) and rapid selection of CTL escape virus in vitro. J. Virol. 72:6851-6857.
12. Koup, R.A. 1994. Virus escape from CTL recognition. J. Exp. Med. 180:779-782.
13. Bevan, M.J., and T.J. Braciale. 1995. Why can't cytotoxic T cells handle HIV? Proc. Natl. Acad. Sci. USA. 92:5765-5767.
14. McMichael, A.J., and R.E. Phillips. 1997. Escape of human immunodeficiency virus from immune control. Annu. Rev. Immunol. 15:271-296.
15. Walker, B.D., and P.J. Goulder. 2000. AIDS. Escape from the immune system. Nature. 407:313-314.
16. Lieberman, J., P. Shankar, N. Manjunath, and J. Andersson. 2001. Dressed to kill? A review of why antiviral CD8 T lymphocytes fail to prevent progressive immunodeficiency in HIV-1 infection. Blood. 98:1667-1677.
17. O'Connor, D.H., and D.I. Watkins. 1999. Houdini's box: towards an understanding of AIDS virus escape from the cytotoxic T-lymphocyte response. Immunogenetics. 50:237-241.
18. Phillips, R.E., S. Rowland-Jones, D.F. Nixon, F.M. Gotch, J.P. Edwards, A.O. Ogunlesi, J.G. Elvin, J.A. Rothbard, C.R. Bangham, C.R. Rizza, et al. 1991. Human immunodeficiency virus genetic variation that can escape cytotoxic T cell recognition. Nature. 354:453-459.
19. Koenig, S., A.J. Conley, Y.A. Brewah, G.M. Jones, S. Leath, L.J. Boots, V. Davey, G. Pantaleo, J.F. Demarest, C. Carter, et al. 1995. Transfer of HIV-1-specific cytotoxic T lymphocytes to an AIDS patient leads to selection for mutant HIV variants and subsequent disease progression. Nat. Med. 1:330-336.
20. 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.
21. 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.
22. 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.
23. Goulder, P.J., C. Brander, Y. Tang, C. Tremblay, R.A. Colbert, M.M. Addo, E.S. Rosenberg, T. Nguyen, R. Allen, A. Trocha, et al. 2001. Evolution and transmission of stable CTL escape mutations in HIV infection. Nature. 412:334-338.
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. 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.
26. 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, et al. 2001. Substantial differences in specificity of HIV-specific cytotoxic T cells in acute and chronic HIV infection. J. Exp. Med. 193:181-194.
27. 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.
28. Safrit, J.T., C.A. Andrews, T. Zhu, D.D. Ho, and R.A. Koup. 1994. Characterization of human immunodeficiency virus type 1-specific cytotoxic T lymphocyte clones isolated during acute seroconversion: recognition of autologous virus sequences within a conserved immunodominant epitope. J. Exp. Med. 179:463-472.
29. Nietfield, W., M. Bauer, M. Fevrier, R. Maier, B. Holzwarth, R. Frank, B. Maier, Y. Riviere, and A. Meyerhans. 1995. Sequence constraints and recognition by CTL of an HLA-B27-restricted HIV-1 gag epitope. J. Immunol. 154:2189-2197.
30. Seibert, S.A., C.Y. Howell, M.K. Hughes, and A.L. Hughes. 1995. Natural selection on the gag, pol, and env genes of human immunodeficiency virus 1 (HIV-1). Mol. Biol. Evol. 12:803-813.
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. 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.
33. 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.
34. Salter, R.D., and P. Cresswell. 1986. Impaired assembly and transport of HLA-A and -B antigens in a mutant TxB cell hybrid. EMBO J. 5:943-949.
35. Popovic, M., M.G. Sarngadharan, E. Read, and R.C. Gallo. 1984. Detection, isolation, and continuous production of cytopathic retroviruses (HTLV-III) from patients with AIDS and pre-AIDS. Science. 224:497-500.
36. Adachi, A., H.E. Gendelman, S. Koenig, T. Folks, R. Willey, A. Rabson, and M.A. Martin. 1986. Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J. Virol. 59:284-291.
37. Saiki, R.K., D.H. Gelfand, S. Stoffel, S.J. Scharf, R. Higuchi, G.T. Horn, K.B. Mullis, and H.A. Erlich. 1988. Primerdirected enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 239:487-491.
38. Gibbs, J.S., D.A. Regier, and R.C. Desrosiers. 1994. Construction and in vitro properties of HIV-1 mutants with deletions in "nonessential" genes. AIDS Res. Hum. Retroviruses. 10:343-350.
39. Johnson, V.A., and B.D. Walker. 1990. HIV-infected cell fusion assay. In Techniques in HIV Research. B.D. Walker, editor. Stockton Press, New York. 92-94.
40. Walker, B.D., C. Flexner, K. Birch-Limberger, 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.
41. Yang, O.O., S.A. Kalams, M. Rosenzweig, A. Trocha, N. Jones, M. Koziel, B.D. Walker, and R.P. Johnson. 1996. Efficient lysis of human immunodeficiency virus type 1-infected cells by cytotoxic T lymphocytes. J. Virol. 70:5799-5806.
42. Del Val, M., H.J. Schlicht, T. Ruppert, M.J. Reddehase, and U.H. Koszinowski. 1991. Efficient processing of an antigenic sequence for presentation by MHC class I molecules depends on its neighboring residues in the protein. Cell. 66:1145-1153.
43. 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.
44. 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, et al. 1995. Viral dynamics in human immunodeficiency virus type 1 infection. Nature. 373:117-122.
45. Yang, O.O., P.T. Nguyen, S.A. Kalams, T. Dorfman, H.G. Gottlinger, S. Stewart, I.S. Chen, S. Threlkeld, and B.D. Walker. 2002. Nef-mediated resistance of human immunodeficiency virus type 1 to antiviral cytotoxic T lymphocytes. J. Virol. 76:1626-1631.
46. Coffin, J.M. 1995. HIV population dynamics in vivo: implications for genetic variation, pathogenesis, and therapy. Science. 267:483-489.
47. Kelleher, A.D., C. Long, E.C. Holmes, R.L. Allen, J. Wilson, C. Conlon, C. Workman, S. Shaunak, K. Olson, P. Goulder, et al. 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.
48. Aebischer, T., D. Moskophidis, U.H. Rohrer, R.M. Zinkernagel, and H. Hengartner. 1991. In vitro selection of lymphocytic choriomeningitis virus escape mutants by cytotoxic T lymphocytes. Proc. Natl. Acad. Sci. USA. 88:11047-11051.
49. Eisen, H.N., Y. Sykulev, and T.J. Tsomides. 1996. Antigenspecific T-cell receptors and their reactions with complexes formed by peptides with major histocompatibility complex proteins. Adv. Protein Chem. 49:1-56.
50. Goulder, P.J., A.K. Sewell, D.G. Lalloo, D.A. Price, J.A. Whelan, J. Evans, G.P. Taylor, G. Luzzi, P. Giangrande, R.E. Phillips, and A.J. McMichael. 1997. Patterns of immunodominance in HIV-1-specific cytotoxic T lymphocyte responses in two human histocompatibility leukocyte antigens (HLA)-identical siblings with HLA-A*0201 are influenced by epitope mutation. J. Exp. Med. 185:1423-1433.
51. 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.
52. van Baalen, C.A., C. Guillon, M. van Baalen, E.J. Verschuren, P.H.M. Boers, A.D.M.E. Osterhaus, and R.A. Gruters. 2002. Impact of antigen expression kinetics on the effectiveness of HIV-specific cytotoxic T lymphocytes. Eur. J. Immunol. 32:2644-2652.
53. Trono, D. 1995. HIV accessory proteins: leading roles for the supporting cast. Cell. 82:189-192.
54. Emerman, M., and M.H. Malim. 1998. HIV-1 regulatory/accessory genes: keys to unraveling viral and host cell biology. Science. 280:1880-1884.
55. 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.
56. Rosenberg, E.S., J.M. Billingsley, A.M. Caliendo, S.L. Boswell, P.E. Sax, S.A. Kalams, and B.D. Walker. 1997. Vigorous HIV-1-specific CD4+ T cell responses associated with control of viremia. Science. 278:1447-1450.
57. Kalams, S.A., S.P. Buchbinder, E.S. Rosenberg, J.M. Billingsley, D.S. Colbert, N.G. Jones, A.K. Shea, A.K. Trocha, and B.D. Walker. 1999. Association between virus-specific cytotoxic T-lymphocyte and helper responses in human immunodeficiency virus type 1 infection. J. Virol. 73:6715-6720.
58. Appay, V., D.F. Nixon, S.M. Donahoe, G.M. Gillespie, T. Dong, A. King, G.S. Ogg, H.M. Spiegel, C. Conlon, C.A. Spina, et al. 2000. HIV-specific CD8(+) T cells produce antiviral cytokines but are impaired in cytolytic function. J. Exp. Med. 192:63-75.
59. Hamann, D., P.A. Baars, M.H. Rep, B. Hooibrink, S.R. Kerkhof-Garde, M.R. Klein, and R.A. van Lier. 1997. Phenotypic and functional separation of memory and effector human CD8+ T cells. J. Exp. Med. 186:1407-1418.
60. Trimble, L.A., and J. Lieberman. 1998. Circulating CD8 T lymphocytes in human immunodeficiency virus-infected individuals have impaired function and downmodulate CD3 zeta, the signaling chain of the T-cell receptor complex. Blood. 91:585-594.
61. Chen, G., P. Shankar, C. Lange, H. Valdez, P.R. Skolnik, L. Wu, N. Manjunath, and J. Lieberman. 2001. CD8 T cells specific for human immunodeficiency virus, Epstein-Barr virus, and cytomegalovirus lack molecules for homing to lymphoid sites ofinfection. Blood. 98:156-164.
62. Alexander, L., E. Weiskopf, T.C. Greenough, N.C. Gaddis, M.R. Auerbach, M.H. Malim, S.J. O'Brien, B.D. Walker, J.L. Sullivan, and R.C. Desrosiers. 2000. Unusual polymorphisms in human immunodeficiency virus type 1 associated with nonprogressive infection. J. Virol. 74:4361-4376.