Pol-specific CD8+ T cells recognize simian immunodeficiency virus-infected cells prior to Nef-mediated major histocompatibility complex class I downregulation

Journal of Virology

Volumn 81, Issue 21, 2007, Pages 11703-11712

  Sacha, Jonah B ^a   Chung, Won ^a   Reed, Jason ^a   Jonas, Anna K ^a   Bean, Alexander T ^a   Spencer, Sean P ^a   Lee, Wonhee ^a   Vojnov, Lara ^a   Rudersdorf, Richard ^a   Friedrich, Thomas C ^a   Wilson, Nancy A ^a   Lifson, Jeffrey D ^b   Watkins, David I ^a,c  

^a UNIVERSITY OF WISCONSIN   (United States)

^b SAIC FREDERICK INC   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

GAG PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NEF PROTEIN; POL PROTEIN; VIRUS PROTEIN;

ANIMAL CELL; ANTIGEN RECOGNITION; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; NONHUMAN; PRIORITY JOURNAL; SIMIAN IMMUNODEFICIENCY VIRUS; STRUCTURAL GENE; VIRION; VIRUS PARTICLE;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; DOWN-REGULATION; EPITOPES; EPITOPES, T-LYMPHOCYTE; GENE EXPRESSION REGULATION, VIRAL; GENE PRODUCTS, POL; HISTOCOMPATIBILITY ANTIGENS CLASS I; MACACA MULATTA; MAJOR HISTOCOMPATIBILITY COMPLEX; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; TIME FACTORS; VIRAL REGULATORY AND ACCESSORY PROTEINS;

SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 35448995742     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00926-07     Document Type: Article

References (50)

1. Adnan, S., A. Balamurugan, A. Trocha, M. S. Bennett, H. L. Ng, A. Ali, C. Brander, and O. O. Yang. 2006. Nef interference with HIV-1-specific CTL antiviral activity is epitope specific. Blood 108:3414-3419.
2. Anderson, S., D. C. Shugars, R. Swanstrom, and J. V. Garcia. 1993. Nef from primary isolates of human immunodeficiency virus type 1 suppresses surface CD4 expression in human and mouse T cells. J. Virol. 67:4923-4931.
3. Baur, A. S., E. T. Sawai, P. Dazin, W. J. Fantl, C. Cheng-Mayer, and B. M. Peterlin. 1994. HIV-1 Nef leads to inhibition or activation of T cells depending on its intracellular localization. Immunity 1:373-384.
4. Bell, I., C. Ashman, J. Maughan, E. Hooker, F. Cook, and T. A. Reinhart. 1998. Association of simian immunodeficiency virus Nef with the T-cell receptor (TCR) zeta chain leads to TCR down-modulation. J. Gen. Virol. 79:2717-2727.
5. Briggs, J. A., M. N. Simon, I. Gross, H. G. Krausslich, S. D. Fuller, V. M. Vogt, and M. C. Johnson. 2004. The stoichiometry of Gag protein in HIV-1. Nat. Struct. Mol. Biol. 11:672-675.
6. + T cells suppress simian immunodeficiency virus replication. J. Virol. 81:1517-1523.
7. 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.
8. Costa, L. J., Y. H. Zheng, J. Sabotic, J. Mak, O. T. Fackler, and B. M. Peterlin. 2004. Nef binds p6* in GagPol during replication of human immunodeficiency virus type 1. J. Virol. 78:5311-5323.
9. Daniel, M. D., F. Kirchhoff, S. C. Czajak, P. K. Sehgal, and R. C. Desrosiers. 1992. Protective effects of a live attenuated SIV vaccine with a deletion in the nef gene. Science 258:1938-1941.
10. Freund, J., R. Kellner, J. Konvalinka, V. Wolber, H. G. Krausslich, and H. R. Kalbitzer. 1994. A possible regulation of negative factor (Nef) activity of human immunodeficiency virus type 1 by the viral protease. Eur. J. Biochem. 223:589-593.
11. Friedrich, T. C., E. J. Dodds, L. J. Yant, L. Vojnov, R. Rudersdorf, C. Cullen, D. T. Evans, R. C. Desrosiers, B. R. Mothe, J. Sidney, A. Sette, K. Kunstman, S. Wolinsky, M. Piatak, J. Lifson, A. L. Hughes, N. Wilson, D. H. O'Connor, and D.I. Watkins. 2004. Reversion of CTL escape-variant immunodeficiency viruses in vivo. Nat. Med. 10:275-281.
12. + T-cell responses are involved in durable control of AIDS virus replication. J. Virol. 81:3465-3476.
13. Gaedigk-Nitschko, K., A. Schon, G. Wachinger, V. Erfle, and B. Kohleisen. 1995. Cleavage of recombinant and cell derived human immunodeficiency virus 1 (HIV-1) Nef protein by HIV-1 protease. FEBS Lett. 357:275-278.
14. Grossman, Z., M. Meier-Schellersheim, W. E. Paul, and L. J. Picker. 2006. Pathogenesis of HIV infection: what the virus spares is as important as what it destroys. Nat. Med. 12:289-295.
15. Herberts, C. A., J. J. Neijssen, J. de Haan, L. Janssen, J. W. Drijfhout, E. A. Reits, and J. J. Neefjes. 2006. Cutting edge: HLA-B27 acquires many N-terminal dibasic peptides: coupling cytosolic peptide stability to antigen presentation. J. Immunol. 176:2697-2701.
16. Jacks, T., M. D. Power, F. R. Masiarz, P. A. Luciw, P. J. Barr, and H. E. Varmus. 1988. Characterization of ribosomal frameshifting in HIV-1 gag-pol expression. Nature 331:280-283.
17. + T cell epitopes. Immunogenetics, in press.
18. Kestler, H. W. R., D. J. Ringler, K. Mori, D. L. Panicali, P. K. Sehgal, M. D. Daniel, and R. C. Desrosiers. 1991. Importance of the nef gene for maintenance of high virus loads and for development of AIDS. Cell 65:651-662.
19. + T-cell responses to different HIV proteins have discordant associations with viral load. Nat. Med. 13:46-53.
20. Kirchhoff, F., T. C. Greenough, D. B. Brettler, J. L. Sullivan, and R. C. Desrosiers. 1995. Brief report: absence of intact nef sequences in a long-term survivor with nonprogressive HIV-1 infection. N. Engl. J. Med. 332:228-232.
21. 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.
22. Layne, S. P., M. J. Merges, M. Dembo, J. L. Spouge, S. R. Conley, J. P. Moore, J. L. Raina, H. Renz, H. R. Gelderblom, and P. L. Nara. 1992. Factors underlying spontaneous inactivation and susceptibility to neutralization of human immunodeficiency virus. Virology 189:695-714.
23. Lifson, J. D., J. L. Rossio, M. Piatak, Jr., J. Bess, Jr., E. Chertova, D. K. Schneider, V. J. Coalter, B. Poore, R. F. Kiser, R. J. Imming, A. J. Scarzello, L. E. Henderson, W. G. Alvord, V. M. Hirsch, R. E. Benveniste, and L. O. Arthur. 2004. Evaluation of the safety, immunogenicity, and protective efficacy of whole inactivated simian immunodeficiency virus (SIV) vaccines with conformationally and functionally intact envelope glycoproteins. AIDS Res. Hum. Retroviruses 20:772-787.
24. + T cells is unrelated to epitope specificity and is abrogated by viral escape. J. Virol. 81:2624-2634.
25. + T lymphocytes at suppressing simian immunodeficiency virus replication in a functional in vitro assay. J. Virol. 79:14986-14991.
26. Matano, T., M. Kobayashi, H. Igarashi, A. Takeda, H. Nakamura, M. Kano, C. Sugimoto, K. Mori, A. Iida, T. Hirata, M. Hasegawa, T. Yuasa, M. Miyazawa, Y. Takahashi, M. Yasunami, A. Kimura, D. H. O'Connor, D. I. Watkins, and Y. Nagai. 2004. Cytotoxic T lymphocyte-based control of simian immunodeficiency virus replication in a preclinical AIDS vaccine trial. J. Exp. Med. 199:1709-1718.
27. Miller, M. D., M. T. Warmerdam, I. Gaston, W. C. Greene, and M. B. Feinberg. 1994. The human immunodeficiency virus-1 nef gene product: a positive factor for viral infection and replication in primary lymphocytes and macrophages. J. Exp. Med. 179:101-113.
28. Munch, J., N. Stolte, D. Fuchs, C. Stahl-Hennig, and F. Kirchhoff. 2001. Efficient class I major histocompatibility complex down-regulation by simian immunodeficiency virus Nef is associated with a strong selective advantage in infected rhesus macaques. J. Virol. 75:10532-10536.
29. Pandori, M. W., N. J. Fitch, H. M. Craig, D. D. Richman, C. A. Spina, and J. C. Guatelli. 1996. Producer-cell modification of human immunodeficiency virus type 1: Nef is a virion protein. J. Virol. 70:4283-4290.
30. Piatak, M., Jr., M. S. Saag, L. C. Yang, S. J. Clark, J. C. Kappes, K. C. Luk, B. H. Hahn, G. M. Shaw, and J. D. Lifson. 1993. High levels of HIV-1 in plasma during all stages of infection determined by competitive PCR. Science 259:1749-1754.
31. Rhodes, D. I., L. Ashton, A. Solomon, A. Carr, D. Cooper, J. Kaldor, N. Deacon, et al. 2000. Characterization of three nef-defective human immunodeficiency virus type 1 strains associated with long-term nonprogression. J. Virol. 74:10581-10588.
32. Roos, J. W., M. F. Maughan, Z. Liao, J. E. Hildreth, and J. E. Clements. 2000. LuSIV cells: a reporter cell line for the detection and quantitation of a single cycle of HIV and SIV replication. Virology 273:307-315.
33. + T lymphocytes recognize infected cells before AIDS-virus integration and viral protein expression. J. Immunol. 178:2746-2754.
34. Schaeffer, E., V. B. Soros, and W. C. Greene. 2004. Compensatory link between fusion and endocytosis of human immunodeficiency virus type 1 in human CD4 T lymphocytes. J. Virol. 78:1375-1383.
35. 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.
36. Stumptner-Cuvelette, P., S. Morchoisne, M. Dugast, S. Le Gall, G. Raposo, O. Schwartz, and P. Benaroch. 2001. HIV-1 Nef impairs MHC class II antigen presentation and surface expression. Proc. Natl. Acad. Sci. USA 98:12144-12149.
37. Swigut, T., A. J. Iafrate, J. Muench, F. Kirchhoff, and J. Skowronski. 2000. Simian and human immunodeficiency virus Nef proteins use different surfaces to downregulate class I major histocompatibility complex antigen expression. J. Virol. 74:5691-5701.
38. Swigut, T., L. Alexander, J. Morgan, J. Lifson, K. G. Mansfield, S. Lang, R. P. Johnson, J. Skowronski, and R. Desrosiers. 2004. Impact of Nef-mediated downregulation of major histocompatibility complex class I on immune response to simian immunodeficiency virus. J. Virol. 78:13335- 13344.
39. Thomas, J. A., D. E. Ott, and R. J. Gorelick. 2007. Efficiency of human immunodeficiency virus type 1 postentry infection processes: evidence against disproportionate numbers of defective virions. J. Virol. 81:4367-4370.
40. + T-cell cytolytic activity and cytokine production. J. Virol. 76:7535-7543.
41. Tomiyama, H., M. Fujiwara, S. Oka, and M. Takiguchi. 2005. Cutting edge: epitope-dependent effect of Nef-mediated HLA class I down-regulation on ability of HIV-1-specific CTLs to suppress HIV-1 replication. J. Immunol. 174:36-40.
42. van Baalen, C. A., C. Guillon, M. van Baalen, E. J. Verschuren, P. H. Boers, A. D. 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.
43. 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.
44. Walk, S. F., M. Alexander, B. Maier, M. L. Hammarskjold, D. M. Rekosh, and K. S. Ravichandran. 2001. Design and use of an inducibly activated human immunodeficiency virus type 1 Nef to study immune modulation. J. Virol. 75:834-843.
45. Welker, R., H. Kottler, H. R. Kalbitzer, and H. G. Krausslich. 1996. Human immunodeficiency virus type 1 Nef protein is incorporated into virus particles and specifically cleaved by the viral proteinase. Virology 219:228-236.
46. Wilson, N. A., J. Reed, G. S. Napoe, et al. 2006. Vaccine-induced cellular immune responses reduce plasma viral concentrations after repeated low-dose challenge with pathogenic simian immunodeficiency virus SIVmac239. J. Virol. 80:5875-5885.
47. Wright, E. R., J. B. Schooler, H. J. Ding, C. Kieffer, C. Fillmore, W. I. Sundquist, and G. J. Jensen. 2007. Electron cryotomography of immature HIV-1 virions reveals the structure of the CA and SP1 Gag shells. EMBO J. 26:2218-2226.
48. 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.
49. 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.
50. Zhu, P., E. Chertova, J. J. Bess, J. D. Lifson, L. O. Arthur, J. Liu, K. A. Taylor, and K. H. Roux. 2003. Electron tomography analysis of envelope glycoprotein trimers on HIV and simian immunodeficiency virus virions. Proc. Natl. Acad. Sci. USA 100:15812-15817.