In vivo mutational analysis of the N-terminal region of HIV-1 Nef reveals critical motifs for the development of an AIDS-like disease in CD4C/HIV transgenic mice

Virology

Volumn 327, Issue 2, 2004, Pages 273-286

  Hanna, Zaher ^a,b,c   Priceputu, Elena ^a   Kay, Denis G ^a   Poudrier, Johanne ^a   Chrobak, Pavel ^a   Jolicoeur, Paul ^a,b,c  

^a CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

AIDS; HIV 1; Nef; Transgenic mice

Indexed keywords

AMINO ACID; CD4 ANTIGEN; CD4C ANTIGEN; CD8 ANTIGEN; CELL SURFACE PROTEIN; NEF PROTEIN; UNCLASSIFIED DRUG;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ALLELE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CELL POPULATION; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE COURSE; DOWN REGULATION; EVALUATION; FLUORESCENCE ACTIVATED CELL SORTING; HISTOPATHOLOGY; HUMAN IMMUNODEFICIENCY VIRUS 1; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE DEPLETION; MIXED LYMPHOCYTE REACTION; MOLECULAR MECHANICS; MOUSE; MUTANT; MUTATIONAL ANALYSIS; MYRISTYLATION; NONHUMAN; ORGAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; SEQUENCE ANALYSIS; STIMULATION; T LYMPHOCYTE; TARGET CELL; THYMOCYTE; THYMUS; TRANSGENIC MOUSE;

ANIMALS; DNA MUTATIONAL ANALYSIS; DOWN-REGULATION; FLOW CYTOMETRY; GENE PRODUCTS, NEF; HIV INFECTIONS; HIV-1; HUMANS; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, TRANSGENIC; MYRISTIC ACID; SEQUENCE DELETION; SPLEEN; THYMUS GLAND;

HUMAN IMMUNODEFICIENCY VIRUS 1; MUS MUSCULUS;

EID: 4444273413     PISSN: 00426822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.virol.2004.06.028     Document Type: Article

References (67)

1. G.M. Aldrovandi, L. Gao, G. Bristol, and J.A. Zack Regions of human immunodeficiency virus type 1 nef required for function in vivo J. Virol. 72 1998 7032 7039
2. L. Alexander, Z. Du, M. Rosenzweig, J.U. Jung, and R.C. Desrosiers A role for natural simian immunodeficiency virus and human immunodeficiency virus type 1 nef alleles in lymphocyte activation J. Virol. 71 1997 6094 6099
3. S.T. Arold, and A.S. Baur Dynamic Nef and Nef dynamics: how structure could explain the complex activities of this small HIV protein Trends Biochem. Sci. 26 2001 356 363
4. J.C. Bandres, and L. Ratner Human immunodeficiency virus type 1 Nef protein down-regulates transcription factors NF-kappa B and AP-1 in human T cells in vitro after T-cell receptor stimulation J. Virol. 68 1994 3243 3249
5. A.S. Baur, E.T. Sawai, P. Dazin, W.J. Fantl, C. Cheng-Mayer, and B.M. Peterlin HIV-1 Nef leads to inhibition or activation of T cells depending on its intracellular localization Immunity 1 1994 373 384
6. A.S. Baur, G. Sass, B. Laffert, D. Willbold, C. Cheng-Mayer, and B.M. Peterlin The N-terminus of Nef from HIV-1/SIV associates with a protein complex containing Lck and a serine kinase Immunity 6 1997 283 291
7. T. Biggs, C. Barton, and D. Mann A proposed mechanism for the induction of activator protein 1 (AP-1) binding by HIV-1 negative factor (Nef) in the macrophage cell line RAW267.4 cells Biochem. Soc. Trans. 26 1998 S263
8. P.A. Bresnahan, W. Yonemoto, S. Ferrell, D. Williams-Herman, R. Geleziunas, and W.C. Greene A dileucine motif in HIV-1 Nef acts as an internalization signal for CD4 downregulation and binds the AP-1 clathrin adaptor Curr. Biol. 8 1998 1235 1238
9. S.D. Briggs, M. Sharkey, M. Stevenson, and T.E. Smithgall SH3-mediated Hck tyrosine kinase activation and fibroblast transformation by the Nef protein of HIV-1 J. Biol. Chem. 272 1997 17899 17902
10. Y. Collette, H. Dutartre, A. Benziane, F. Ramos-Morales, R. Benarous, Ramos-morales, M. Harris, and D. Olive Physical and functional interaction of Nef with Lck. HIV-1 Nef-induced T-cell signaling defects J. Biol. Chem. 271 1996 6333 6341
11. B.R. Cullen The role of Nef in the replication cycle of the human and simian immunodeficiency viruses Virology 205 1994 1 6
12. S.K. De, and J.W. Marsh HIV-1 Nef inhibits a common activation pathway in NIH-3T3 cells J. Biol. Chem. 269 1994 6656 6660
13. N.J. Deacon, A. Tsykin, A. Solomon, K. Smith, M. Ludford-Menting, D.J. Hooker, D.A. McPhee, A.L. Greenway, A. Ellett, and C. Chatfield Genomic structure of an attenuated quasi species of hiv-1 from a blood transfusion donor and recipients Science 270 1995 988 991
14. Z. Du, S.M. Lang, V.G. Sasseville, A. Lackner, P.O. Ilyinskii, M.D.J.J. Daniel, and R.C. Desrosiers Identification of a nef allele that causes lymphocyte activation and acute disease in macaque monkeys Cell 82 1995 665 674
15. O.T. Fackler, and A.S. Baur Live and let die: Nef functions beyond HIV replication Immunity 16 2002 493 497
16. O.T. Fackler, N. Kienzle, E. Kremmer, A. Boese, B. Schramm, T. Klimkait, C. Kucherer, and N. Mueller-Lantzsch Association of human immunodeficiency virus Nef protein with actin is myristoylation dependent and influences its subcellular localization Eur. J. Biochem. 247 1997 843 851
17. O.T. Fackler, W. Luo, M. Geyer, A.S. Alberts, and B.M. Peterlin Activation of Vav by Nef induces cytoskeletal rearrangements and downstream effector functions Mol. Cell 3 1999 729 739
18. J. Freund, R. Kellner, T. Houthaeve, and H.R. Kalbitzer Stability and proteolytic domains of Nef protein from human immunodeficiency virus (HIV) type 1 Eur. J. Biochem. 221 1994 811 819
19. M. Geyer, O.T. Fackler, and B.M. Peterlin Structureâ€" function relationships in HIV-1 Nef EMBO J. Rep. 2 2001 580 585
20. M.A. Goldsmith, M.T. Warmerdam, R.E. Atchison, M.D. Miller, and W.C. Greene Dissociation of the CD4 downregulation and viral infectivity enhancement functions of human immunodeficiency virus type 1 Nef J. Virol. 69 1995 4112 4121
21. M. Greenberg, L. DeTulleo, and I. Rapoport A dileucine motif in HIV-1 Nef is essential for sorting into clathrin-coated pits and for downregulation of CD4 Curr. Biol. 8 1998 1239 1242
22. A.L. Greenway, D.A. McPhee, E. Grgacic, D. Hewish, A. Lucantoni, and I.A.A. Macreadie Nef 27, but not the Nef 25 isoform of human immunodeficiency virus-type 1 pNL4.3 down-regulates surface CD4 and IL-2R expression in peripheral blood mononuclear cells and transformed T cells Virology 198 1994 245 256
23. A. Greenway, A. Azad, and D. McPhee Human immunodeficiency virus type 1 Nef protein inhibits activation pathways in peripheral blood mononuclear cells and T-cell lines J. Virol. 69 1995 1842 1850
24. S. Grzesiek, A. Bax, G.M. Clore, A.M. Gronenborn, J.S. Hu, J. Kaufman, I. Palmer, S.J. Stahl, and P.T. Wingfield The solution structure of HIV-1 Nef reveals an unexpected fold and permits delineation of the binding surface for the SH3 domain of Hck tyrosine protein kinase Nat. Struct. Biol. 3 1996 340 345
25. S. Grzesiek, S.J. Stahl, P.T. Wingfield, and A. Bax The CD4 determinant for downregulation by HIV-1 Nef directly binds to Nef. Mapping of the Nef binding surface by NMR Biochemistry 35 1996 10256 10261
26. B. Guy, M.P. Kieny, Y. Riviere, C. Le Peuch, K. Dott, M. Girard, L. Montagnier, and J.P. Lecocq HIV F/3′ orf encodes a phosphorylated GTP-binding protein resembling an oncogene product Nature 330 1987 266 269
27. Z. Hanna, D.G. Kay, M. Cool, S. Jothy, N. Rebai, and P. Jolicoeur Transgenic mice expressing human immunodeficiency virus type 1 in immune cells develop a severe AIDS-like disease J. Virol. 72 1998 121 132
28. Z. Hanna, D.G. Kay, N. Rebai, A. Guimond, S. Jothy, and P. Jolicoeur Nef harbors a major determinant of pathogenicity for an AIDS-like disease induced by HIV-1 in transgenic mice Cell 95 1998 163 175
29. + T cells, and in macrophages of transgenic mice Mol. Cell Biol. (Washington) 14 1994 1084 1094
30. Z. Hanna, N. Rebai, J. Poudrier, and P. Jolicoeur Distinct regulatory elements are required for faithful expression of human CD4 in T-cells, macrophages and dendritic cells of transgenic mice Blood 98 2001 2275 2278
31. Z. Hanna, X. Weng, D.G. Kay, J. Poudrier, C. Lowell, and P. Jolicoeur The Pathogenicity of Human Immunodeficiency Virus (HIV) type 1 Nef in CD4C/HIV transgenic mice is abolished by mutation of its SH3-binding domain, and disease development is delayed in the absence of Hck J. Virol. 75 2001 9378 9392
32. M. Harris From negative factor to a critical role in virus pathogenesis: the changing fortunes of Nef J. Gen. Virol. 77 1996 2379 2392
33. M. Harris HIV: a new role for Nef in the spread of HIV Curr. Biol. 9 1999 R459 R461
34. J. Hua, W. Blair, R. Truant, and B.R. Cullen Identification of regions in HIV-1 Nef required for efficient downregulation of cell surface CD4 Virology 231 1997 231 238
35. A.J. Iafrate, S. Bronson, and J. Skowronski Separable functions of Nef disrupt two aspects of T cell receptor machinery: CD4 expression and CD3 signaling EMBO J. 16 1997 673 684
36. D.G. Kay, P. Yue, Z. Hanna, S. Jothy, E. Tremblay, and P. Jolicoeur Cardiac disease in transgenic mice expressing human immunodeficiency virus-1 Nef in cells of the immune system Am. J. Pathol. 161 2002 321 335
37. H.W. Kestler, D.J. Ringler, K. Mori, D.L. Panicali, P.K. Sehgal, M.D. Daniel, and R.C. Desrosiers Importance of the nef gene for maintenance of high virus loads and for development of AIDS Cell 65 1991 651 662
38. F. Kirchhoff, T.C. Greenough, D.B. Brettler, J.L. Sullivan, and R.C. Desrosiers Brief report: absence of intact nef sequences in a long-term survivor with nonprogressive HIV-1 infection N. Engl. J. Med. 332 1995 228 232
39. S. Le Gall, J.M. Heard, and O. Schwartz Analysis of Nef-induced MHC-I endocytosis Res. Virol. 148 1997 43 47
40. C.H. Lee, K. Saksela, U.A. Mirza, B.T. Chait, and J. Kuriyan Crystal structure of the conserved core of HIV-1 Nef complexed with a Src family SH3 domain Cell 85 1996 931 942
41. M. Lock, M.E. Greenberg, A.J. Iafrate, T. Swigut, J. Muench, F. Kirchhoff, N. Shohdy, and J. Skowronski Two elements target SIV Nef to the AP-2 clathrin adaptor complex, but only one is required for the induction of CD4 endocytosis EMBO J. 18 1999 2722 2733
42. X. Lu, H. Yu, S.H. Liu, F.M. Brodsky, and B.M. Peterlin Interactions between HIV1 Nef and vacuolar ATPase facilitate the internalization of CD4 Immunity 8 1998 647 656
43. W. Luo, and B.M. Peterlin Activation of the T-cell receptor signaling pathway by Nef from an aggressive strain of simian immunodeficiency virus J. Virol. 71 1997 9531 9537
44. S. Luria, I. Chambers, and P. Berg Expression of the type 1 human immunodeficiency virus Nef protein in T cells prevents antigen receptor-mediated induction of interleukin 2 mRNA Proc. Natl. Acad. Sci. U.S.A. 88 1991 5326 5330
45. A.B. Lyons, and C.R. Parish Determination of lymphocyte division by flow cytometry J. Immunol. Methods 171 1994 131 137
46. A. Mangasarian, V. Piguet, J.K. Wang, Y.L. Chen, and D. Trono Nef-induced CD4 and major histocompatibility complex class I (MHC-I) down-regulation are governed by distinct determinants: N-terminal alpha helix and proline repeat of Nef selectively regulate MHC-I trafficking J. Virol. 73 1999 1964 1973
47. + T-cell line Proc. Natl. Acad. Sci. U.S.A. 90 1993 11895 11899
48. T.M. Niederman, J.V. Garcia, W.R. Hastings, S. Luria, and L. Ratner Human immunodeficiency virus type 1 (HIV-1) Nef protein inhibits NF-kappa B induction in human T cells J. Virol. 66 1992 6213 6219
49. T.M. Niederman, W.R. Hastings, S. Luria, J.C. Bandres, and L. Ratner HIV-1 Nef protein inhibits the recruitment of AP-1 DNA-binding activity in human T-cells Virology 194 1993 338 344
50. T.M. Niederman, W.R. Hastings, and L. Ratner Myristoylation-enhanced binding of the HIV-1 Nef protein to T cell skeletal matrix Virology 197 1993 420 425
51. M.W. Pandori, N.J. Fitch, H.M. Craig, D.D. Richman, C.A. Spina, and J.C. Guatelli Producer-cell modification of human immunodeficiency virus type 1: Nef is a virion protein J. Virol. 70 1996 4283 4290
52. V. Piguet, O. Schwartz, S. Le Gall, and D. Trono The downregulation of CD4 and MHC-I by primate lentiviruses: a paradigm for the modulation of cell surface receptors Immunol. Rev. 168 1999 51 63
53. J. Poudrier, X. Weng, D.G. Kay, G. Paré, E.L. Calvo, Z. Hanna, M.H. Kosco-Vilbois, and P. Jolicoeur The AIDS disease of CD4C/HIV transgenic mice shows impaired germinal centers and autoantibodies and develops in the absence of IFN-γ and IL-6 Immunity 15 2001 173 185
54. hi dendritic cells J. Virol. 77 2003 11733 11744
55. J.A. Schrager, and J.W. Marsh HIV-1 Nef increases T cell activation in a stimulus-dependent manner Proc. Natl. Acad. Sci. U.S.A. 96 1999 8167 8172
56. J. Skowronski, M.E. Greenberg, M. Lock, R. Mariani, S. Salghetti, T. Swigut, and A.J. Iafrate HIV and SIV Nef modulate signal transduction and protein sorting in T cells Cold Spring Harbor Symp. Quant. Biol. vol. 64 1999 453 463
57. C.A. Stoddart, R. Geleziunas, S. Ferrell, V. Linquist-Stepps, M.E. Moreno, C. Bare, W. Xu, W. Yonemoto, P.A. Bresnahan, J.M. McCune, and W.C. Greene Human immunodeficiency virus type 1 Nef-mediated downregulation of CD4 correlates with Nef enhancement of viral pathogenesis J. Virol. 77 2003 2124 2133
58. V. Stove, E. Naessens, C. Stove, T. Swigut, J. Plum, and B. Verhasselt Signaling but not trafficking function of HIV-1 protein Nef is essential for Nef-induced defects in human intrathymic T-cell development Blood 102 2003 2925 2932
59. T. Swigut, N. Shohdy, and J. Skowronski Mechanism for down-regulation of CD28 by Nef EMBO J. 20 2001 1593 1604
60. D. Trono HIV accessory proteins: leading roles for the supporting cast Cell 82 1995 189 192
61. J.K. Wang, E. Kiyokawa, E. Verdin, and D. Trono The Nef protein of HIV-1 associates with rafts and primes T cells for activation Proc. Natl. Acad. Sci. U.S.A. 97 2000 394 399
62. R. Welker, H. Kottler, H.R. Kalbitzer, and H.G. Krausslich Human immunodeficiency virus type 1 Nef protein is incorporated into virus particles and specifically cleaved by the viral proteinase Virology 219 1996 228 236
63. R. Welker, M. Harris, B. Cardel, and H.G. Krausslich Virion incorporation of human immunodeficiency virus type 1 Nef is mediated by a bipartite membrane-targeting signal: analysis of its role in enhancement of viral infectivity J. Virol. 72 1998 8833 8840
64. X. Weng, E. Priceputu, P. Chrobak, J. Poudrier, D.G. Kay, Z. Hanna, T.W. Mak, and P. Jolicoeur CD4 T cells from CD4C/HIV nef transgenic mice show enhanced activation in vivo with impaired proliferation in vitro, but are dispensable for the development of a severe AIDS-like organ disease J. Virol. 78 2004 5244 5257
65. L. Whetter, F.J. Novembre, M. Saucier, S. Gummuluru, and S. Dewhurst Costimulatory pathways in lymphocyte proliferation induced by the simian immunodeficiency virus SIVsmmPBj14 J. Virol. 72 1998 6155 6158
66. M. Wiskerchen, and C. Cheng-Mayer HIV-1 Nef association with cellular serine kinase correlates with enhanced virion infectivity and efficient proviral DNA synthesis Virology 224 1996 292 301
67. V. Witte, B. Laffert, O. Rosorius, P. Lischka, K. Blume, G. Galler, A. Stilper, D. Willbold, P. D'Aloja, M. Sixt, J. Kolanus, M. Ott, W. Kolanus, G. Schuler, and A.S. Baur HIV-1 Nef mimics an integrin receptor signal that recruits the polycomb group protein Eed to the plasma membrane Mol. Cell 13 2004 179 190