CTL-mediated selective pressure influences dynamic evolution and pathogenic functions of HIV-1 Nef

Journal of Immunology

Volumn 180, Issue 2, 2008, Pages 1107-1116

  Ueno, Takamasa ^a   Motozono, Chihiro ^a   Dohki, Sachi ^a   Mwimanzi, Philip ^a   Rauch, Susanne ^c   Fackler, Oliver T ^c   Oka, Shinichi ^a,b   Takiguchi, Masafumi ^a  

^a KUMAMOTO UNIVERSITY   (Japan)

^b NATIONAL CENTER FOR GLOBAL HEALTH AND MEDICINE   (Japan)

^c UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; EPITOPE; HLA ANTIGEN CLASS 1; HLA B35 ANTIGEN; MUTANT PROTEIN; NEF PROTEIN; PHENYLALANINE; PHOSPHOTRANSFERASE; PROLINE; THREONINE; TYROSINE; IMMUNOGLOBULIN RECEPTOR; P21 ACTIVATED KINASE;

ANTIGEN RECOGNITION; ARTICLE; CLINICAL ARTICLE; CYTOTOXIC T LYMPHOCYTE; DISEASE PREDISPOSITION; DOWN REGULATION; HOST; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOSURVEILLANCE; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; MUTATION; PRIORITY JOURNAL; PROTEIN FUNCTION; T LYMPHOCYTE ACTIVATION; VIRUS REPLICATION; VIRUS VIRULENCE; AMINO ACID SEQUENCE; ANTIGENIC VARIATION; CHEMISTRY; EPITOPE MAPPING; FEMALE; GENETIC SELECTION; GENETICS; IMMUNOLOGY; MALE; METABOLISM; MOLECULAR GENETICS;

AMINO ACID SEQUENCE; ANTIGENIC VARIATION; DOWN-REGULATION; EPITOPE MAPPING; EVOLUTION, MOLECULAR; FEMALE; HIV INFECTIONS; HIV-1; HLA-B35 ANTIGEN; HUMANS; IMMUNOLOGIC SURVEILLANCE; MALE; MOLECULAR SEQUENCE DATA; MUTATION; NEF GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; P21-ACTIVATED KINASES; RECEPTORS, IMMUNOLOGIC; SELECTION (GENETICS); T-LYMPHOCYTES, CYTOTOXIC;

EID: 40449098834     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.180.2.1107     Document Type: Article

References (57)

1. Kestler, H. W., 3rd, 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.
2. Deacon, N. J., A. Tsykin, A. Solomon, K. Smith, M. Ludford-Menting, A. Ellett, D. J. Hooker, D. A. McPhee, A. L. Greenway, C. Chatfield, et al. 1995. Genomic structure of an attenuated quasi species of HIV-1 from a blood transfusion donor and recipients. Science 270: 988-991.
3. Kirchhoff, F., T. C. Greenough, D. B. Brettler, J. L. Sullivan, and R. C. Desrosiers. 1995. Absence of intact nef sequences in a long-term survivor with nonprogressive HIV-1 infection. N. Engl. J. Med. 332: 228-232.
4. Carl, S., T. C. Greenough, M. Krumbiegel, M. Greenberg, J. Skowronski, J. L. Sullivan, and F. Kirchhoff. 2001. Modulation of different human immunodeficiency virus type 1 Nef functions during progression to AIDS. J. Virol. 75: 3657-3665.
5. Das, S. R., and S. Jameel. 2005. Biology of the HIV Nef protein. Indian J. Med. Res. 121: 315-332.
6. Fackler, O. T., A. Alcover, and O. Schwartz. 2007. Modulation of the immunological synapse: a key to HIV-1 pathogenesis? Nat. Rev. Immunol. 7: 310-317.
7. Peterlin, B. M., and D. Trono. 2003. Hide, shield and strike back: how HIV-infected cells avoid immune eradication. Nat. Rev. Immunol. 3: 97-107.
8. Stevenson, M. 2003. HIV-1 pathogenesis. Nat. Med. 9: 853-860.
9. Thoulouze, M. I., N. Sol-Foulon, F. Blanchet, A. Dautry-Varsat, O. Schwartz, and A. Alcover. 2006. Human immunodeficiency virus type-1 infection impairs the formation of the immunological synapse. Immunity 24: 547-561.
10. Haller, C., S. Rauch, N. Michel, S. Hannemann, M. J. Lehmann, O. T. Keppler, and O. T. Fackler. 2006. The HIV-1 pathogenicity factor Nef interferes with maturation of stimulatory T-lymphocyte contacts by modulation of N-Wasp activity. J. Biol. Chem. 281: 19618-19630.
11. Schindler, M., J. Munch, O. Kutsch, H. Li, M. L. Santiago, F. Bibollet-Ruche, M. C. Muller-Trutwin, F. J. Novembre, M. Peeters, V. Courgnaud, et al. 2006. Nef-mediated suppression of T cell activation was lost in a lentiviral lineage that gave rise to HIV-1. Cell 125: 1055-1067.
12. Hung, C. H., L. Thomas, C. E. Ruby, K. M. Atkins, N. P. Morris, Z. A. Knight, I. Scholz, E. Barklis, A. D. Weinberg, K. M. Shokat, and G. Thomas. 2007. HIV-1 Nef assembles a Src family kinase-ZAP-70/Syk-PI3K cascade to downregulate cell-surface MHC-I. Cell Host Microbe. 1: 121-133.
13. Roeth, J. F., and K. L. Collins. 2006. Human immunodeficiency virus type 1 Nef: adapting to intracellular trafficking pathways. Microbiol. Mol. Biol. Rev. 70: 548-563.
14. 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.
15. + cytotoxic T-lymphocyte activity associated with control of viremia in primary human immunodeficiency virus type 1 infection. J. Virol. 68: 6103-6110.
16. 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.
17. + T-cell cytolytic activity and cytokine production. J. Virol. 76: 7535-7543.
18. + cells: evidence for HLA class I-restricted triggering of cytolytic and noncytolytic mechanisms. J. Virol. 71: 3120-3128.
19. + T cell depletion in simian immunodeficiency virus-infected macaques. J. Exp. Med. 189: 991-998.
20. + lymphocytes. Science 283: 857-860.
21. Klotman, M. E., S. Kim, A. Buchbinder, A. DeRossi, D. Baltimore, and F. Wong-Staal. 1991. Kinetics of expression of multiply spliced RNA in early human immunodeficiency virus type 1 infection of lymphocytes and monocytes. Proc. Natl. Acad. Sci. USA 88: 5011-5015.
22. + T cell epitopes: wealth of HLA-binding motifs and sensitivity to proteasome degradation. J. Immunol. 166: 6164-6169.
23. Lichterfeld, M., X. G. Yu, D. Cohen, M. M. Addo, J. Malenfant, B. Perkins, E. Pae, M. N. Johnston, D. Strick, T. M. Allen, et al. 2004. HIV-1 Nef is preferentially recognized by CD8 T cells in primary HIV-1 infection despite a relatively high degree of genetic diversity. AIDS 18: 1383-1392.
24. Culmann-Penciolelli, B., S. Lamhamedi-Cherradi, I. Couillin, N. Guegan, J. P. Levy, J. G. Guillet, and E. Gomard. 1994. Identification of multirestricted immunodominant regions recognized by cytolytic T lymphocytes in the human immunodeficiency virus type 1 Nef protein. J. Virol. 68: 7336-7343.
25. Fackler, O. T., D. Wolf, H. O. Weber, B. Laffert, P. D'Aloja, B. Schuler-Thurner, R. Geffin, K. Saksela, M. Geyer, and B. M. Peterlin. 2001. A natural variability in the proline-rich motif of Nef modulates HIV-1 replication in primary T cells. Curr. Biol. 11: 1294-1299.
26. + viruses but not for down-regulation of CD4. EMBO J. 14: 484-491.
27. Geyer, M., O. T. Fackler, and B. M. Peterlin. 2001. Structure-function relationships in HIV-1 Nef. EMBO Rep. 2: 580-585.
28. + T cell epitope-flanking mutations disrupt proteasomal processing of HIV-1 Nef. J. Immunol. 175: 4618-4626.
29. Ueno, T., Y. Idegami, C. Motozono, S. Oka, and M. Takiguchi. 2007. Altering effects of antigenic variations in HIV-1 on antiviral effectiveness of HIV-specific CTLs. J. Immunol. 178: 5513-5523.
30. Kumar, S., K. Tamura, and M. Nei. 2004. MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief. Bioinform. 5: 150-163.
31. Ueno, T., H. Tomiyama, and M. Takiguchi. 2002. Single T cell receptor-mediated recognition of an identical HIV-derived peptide presented by multiple HLA class I molecules. J. Immunol. 169: 4961-4969.
32. Fackler, O. T., A. Moris, N. Tibroni, S. I. Giese, B. Glass, O. Schwartz, and H.-G. Krausslich. 2006. Functional characterization of HIV-1 Nef mutants in the context of viral infection. Virology 351: 322-339.
33. Ueno, T., H. Tomiyama, M. Fujiwara, S. Oka, and M. Takiguchi. 2003. HLA class I-restricted recognition of an HIV-derived epitope peptide by a human T cell receptor α chain having a Vδ1 variable segment. Eur. J. Immunol. 33: 2910-2916.
34. Krautkramer, E., S. I. Giese, J. E. Gasteier, W. Muranyi, and O. T. Fackler. 2004. Human immunodeficiency virus type 1 Nef activates p21-activated Kinase via recruitment into lipid rafts. J. Virol. 78: 4085-4097.
35. 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.
36. Tomiyama, H., K. Miwa, H. Shiga, Y. I. Moore, S. Oka, A. Iwamoto, Y. Kaneko, and M. Takiguchi. 1997. Evidence of presentation of multiple HIV-1 cytotoxic T lymphocyte epitopes by HLA-B*3501 molecules that are associated with the accelerated progression of AIDS. J. Immunol. 158: 5026-5034.
37. Ueno, T., H. Tomiyama, M. Fujiwara, S. Oka, and M. Takiguchi. 2004. Functionally impaired HIV-specific CD8 T cells show high affinity TCR-ligand interactions. J. Immunol. 173: 5451-5457.
38. 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.
39. Kirchhoff, F., M. Schindler, N. Bailer, G. H. Renkema, K. Saksela, V. Knoop, M. C. Muller-Trutwin, M. L. Santiago, F. Bibollet-Ruche, M. T. Dittmar, et al. 2004. Nef proteins from simian immunodeficiency virus-infected chimpanzees interact with p21-activated kinase 2 and modulate cell surface expression of various human receptors. J. Virol. 78: 6864-6874.
40. Fackler, O. T., W. Luo, M. Geyer, A. S. Alberts, and B. M. Peterlin. 1999. Activation of Vav by Nef induces cytoskeletal rearrangements and downstream effector functions. Mol. Cell 3: 729-739.
41. Wolf, D., V. Witte, B. Laffert, K. Blume, E. Stromer, S. Trapp, P. d'Aloja, A. Schurmann, and A. S. Baur. 2001. HIV-1 Nef associated PAK and PI3-kinases stimulate Akt-independent Bad-phosphorylation to induce anti-apoptotic signals. Nat. Med. 7: 1217-1224.
42. 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.
43. Spina, C. A., T. J. Kwoh, M. Y. Chowers, J. C. Guatelli, and D. D. Richman. 1994. The importance of nef in the induction of human immunodeficiency virus type 1 replication from primary quiescent CD4 lymphocytes. J. Exp. Med. 179: 115-123.
44. Furutsuki, T., N. Hosoya, A. Kawana-Tachikawa, M. Tomizawa, T. Odawara, M. Goto, Y. Kitamura, T. Nakamura, A. D. Kelleher, D. A. Cooper, and A. Iwamoto. 2004. Frequent transmission of cytotoxic-T-lymphocyte escape mutants of human immunodeficiency virus type 1 in the highly HLA-A24-positive Japanese population. J. Virol. 78: 8437-8445.
45. Leslie, A., D. Kavanagh, I. Honeyborne, K. Pfafferott, C. Edwards, T. Pillay, L. Hilton, C. Thobakgale, D. Ramduth, R. Draenert, et al. 2005. Transmission and accumulation of CTL escape variants drive negative associations between HIV polymorphisms and HLA. J. Exp. Med. 201: 891-902.
46. Bhattacharya, T., M. Daniels, D. Heckerman, B. Foley, N. Frahm, C. Kadie, J. Carlson, K. Yusim, B. McMahon, B. Gaschen, et al. 2007. Founder effects in the assessment of HIV polymorphisms and HLA allele associations. Science 315: 1583-1586.
47. Brumme, Z. L., C. J. Brumme, D. Heckerman, B. T. Korber, M. Daniels, J. Carlson, C. Kadie, T. Bhattacharya, C. Chui, J. Szinger, et al. 2007. Evidence of differential HLA class I-mediated viral evolution in functional and accessory/regulatory genes of HIV-1. PLoS Pathog. 3: e94.
48. + T-cell responses to different HIV proteins have discordant associations with viral load. Nat. Med. 13: 46-53.
49. Bansal, A., E. Gough, S. Sabbaj, D. Ritter, K. Yusim, G. Sfakianos, G. Aldrovandi, R. A. Kaslow, C. M. Wilson, M. J. Mulligan, et al. 2005. CD8 T-cell responses in early HIV-1 infection are skewed towards high entropy peptides. AIDS 19: 241-250.
50. Goulder, P. J. R., 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.
51. Nowak, M. A., R. M. May, R. E. Phillips, S. Rowland-Jones, D. G. Lalloo, S. McAdam, P. Klenerman, B. Koppe, K. Sigmund, C. R. M. Bangham, and A. J. McMichael. 1995. Antigenic oscillations and shifting immunodominance in HIV-1 infections. Nature 375: 606-611.
52. 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.
53. Gao, X., G. W. Nelson, P. Karacki, M. M. P. J. Phair, R. Kaslow, J. J. Goedert, S. Buchbinder, K. Hoots, D. Vlahov, S. J. O'Brien, and M. Carrington. 2001. Effect of a single amino acid change in MHC class I molecules on the rate of progression to AIDS. N. Engl. J. Med. 344: 1668-1675.
54. Ali, A., S. Pillai, H. Ng, R. Lubong, D. D. Richman, B. D. Jamieson, Y. Ding, M. J. McElrath, J. C. Guatelli, and O. O. Yang. 2003. Broadly increased sensitivity to cytotoxic T lymphocytes resulting from Nef epitope escape mutations. J. Immunol. 171: 3999-4005.
55. 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.
56. Campbell, E. M., R. Nunez, and T. J. Hope. 2004. Disruption of the actin cytoskeleton can complement the ability of Nef to enhance human immunodeficiency virus type 1 infectivity. J. Virol. 78: 5745-5755.
57. Wiskerchen, M., and C. Cheng-Mayer. 1996. HIV-1 Nef association with cellular serine kinase correlates with enhanced virion infectivity and efficient proviral DNA synthesis. Virology 224: 292-301.