Expression of simian immunodeficiency virus Nef protein in CD4+ T cells leads to a molecular profile of viral persistence and immune evasion

Virology

Volumn 353, Issue 2, 2006, Pages 374-387

  Ndolo, Thomas ^a   George, Michael ^a   Nguyen, Hau ^a   Dandekar, Satya ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Antigen presentation; DNA microarray; Immune evasion; SIV Nef; Viral persistence

Indexed keywords

GLYCOLIPID; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MEMBRANE LIPID; NEF PROTEIN; PHOSPHOLIPID; T LYMPHOCYTE RECEPTOR; VIRUS PROTEIN;

ANTIGEN PRESENTATION; ARTICLE; CATALYSIS; CD4+ T LYMPHOCYTE; CELL CYCLE; CELL LINE; CELL SURVIVAL; CONTROLLED STUDY; DNA MICROARRAY; DOWN REGULATION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; LIPOGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PERSISTENT VIRUS INFECTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; SIMIAN IMMUNODEFICIENCY VIRUS; UNINDEXED SEQUENCE;

ANTIGEN PRESENTATION; CD4-POSITIVE T-LYMPHOCYTES; CELL CYCLE; GENE EXPRESSION REGULATION; GLYCOLIPIDS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; JURKAT CELLS; MEMBRANE PROTEINS; MICROARRAY ANALYSIS; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; TRANSFECTION; VIRAL REGULATORY PROTEINS; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 33748702282     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2006.06.008     Document Type: Article

References (99)

1. Aguado B., and Campbell R.D. Characterization of a human lysophosphatidic acid acyltransferase that is encoded by a gene located in the class III region of the human major histocompatibility complex. J. Biol. Chem. 273 7 (1998) 4096-4105
2. Aiken C., Konner J., Landau N.R., Lenburg M.E., and Trono D. Nef induces CD4 endocytosis: requirement for a critical dileucine motif in the membrane-proximal CD4 cytoplasmic domain. Cell 76 5 (1994) 853-864
3. Alexander L., Du Z., Howe A.Y., Czajak S., and Desrosiers R.C. Induction of AIDS in rhesus monkeys by a recombinant simian immunodeficiency virus expressing nef of human immunodeficiency virus type 1. J. Virol. 73 7 (1999) 5814-5825
4. Anazawa Y., Arakawa H., Nakagawa H., and Nakamura Y. Identification of STAG1 as a key mediator of a p53-dependent apoptotic pathway. Oncogene 23 46 (2004) 7621-7677
5. Arold S., Franken P., Strub M.P., Hoh F., Benichou S., Benarous R., and Dumas C. The crystal structure of HIV-1 Nef protein bound to the Fyn kinase SH3 domain suggests a role for this complex in altered T cell receptor signaling. Structure 5 10 (1997) 1361-1372
6. Bandres J.C., Shaw A.S., and Ratner L. HIV-1 Nef protein downregulation of CD4 surface expression: relevance of the lck binding domain of CD4. Virology 207 1 (1995) 338-341
7. Baur A.S., Sawai E.T., Dazin P., Fantl W.J., Cheng-Mayer C., and Peterlin B.M. HIV-1 Nef leads to inhibition or activation of T cells depending on its intracellular localization. Immunity 1 5 (1994) 373-384
8. Baur A.S., Sass G., Laffert B., Willbold D., Cheng-Mayer C., and Peterlin B.M. The N-terminus of Nef from HIV-1/SIV associates with a protein complex containing Lck and a serine kinase. Immunity 6 3 (1997) 283-291
9. Bresnahan P.A., Yonemoto W., Ferrell S., Williams-Herman D., Geleziunas R., and Greene W.C. 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 22 (1998) 1235-1238
10. Campos-Martin Y., Gomez del Moral M., Gozalbo-Lopez B., Suela J., and Martinez-Naves E. Expression of human CD1d molecules protects target cells from NK cell-mediated cytolysis. J. Immunol. 172 12 (2004) 7297-7305
11. Chang C.S., Brossay L., Kronenberg M., and Kane K.P. The murine nonclassical class I major histocompatibility complex-like CD1.1 molecule protects target cells from lymphokine-activated killer cell cytolysis. J. Exp. Med. 189 3 (1999) 483-491
12. + T cells in viremic versus aviremic HIV-infected individuals. Proc. Natl. Acad. Sci. U. S. A. 100 4 (2003) 190813-190819
13. Cohen G.B., Gandhi R.T., Davis D.M., Mandelboim O., Chen B.K., Strominger J.L., and Baltimore D. The selective downregulation of class I major histocompatibility complex proteins by HIV-1 protects HIV-infected cells from NK cells. Immunity 10 6 (1999) 661-671
14. Collins K.L., Chen B.K., Kalams S.A., Walker B.D., and Baltimore D. HIV-1 Nef protein protects infected primary cells against killing by cytotoxic T lymphocytes. Nature 391 6665 (1998) 397-401
15. Craig H.M., Pandori M.W., and Guatelli J.C. Interaction of HIV-1 Nef with the cellular dileucine-based sorting pathway is required for CD4 down-regulation and optimal viral infectivity. Proc. Natl. Acad. Sci. U.S.A. 95 19 (1998) 11229-11234
16. Cujec T.P., Cho H., Maldonado E., Meyer J., Reinberg D., and Peterlin B.M. The human immunodeficiency virus transactivator Tat interacts with the RNA polymerase II holoenzyme. Mol. Cell. Biol. 17 4 (1997) 1817-1823
17. de la Fuente C., Santiago F., Deng L., Eadie C., Zilberman I., Kehn K., Maddukuri A., Baylor S., Wu K., Lee C.G., Pumfery A., and Kashanchi F. Gene expression profile of HIV-1 Tat expressing cells: a close interplay between proliferative and differentiation signals. BMC Biochem. 3 (2002) 14
18. de Noronha C.M., Sherman M.P., Lin H.W., Cavrois M.V., Moir R.D., Goldman R.D., and Greene W.C. Dynamic disruptions in nuclear envelope architecture and integrity induced by HIV-1 Vpr. Science 294 5544 (2001) 1105-1108
19. Deacon N.J., Tsykin A., Solomon A., Smith K., Ludford-Menting M., Hooker D.J., McPhee D.A., Greenway A.L., Ellett A., Chatfield C., Lawson V.A., Crowe S., Maerz A., Sonza S., Learmont J., Sullivan J.S., Cunningham A., Dwyer D., Dowton D., and Mills J. Genomic structure of an attenuated quasi species of HIV-1 from a blood transfusion donor and recipients. Science 270 5238 (1995) 988-991
20. Elder R.T., Yu M., Chen M., Zhu X., Yanagida M., and Zhao Y. HIV-1 Vpr induces cell cycle G2 arrest in fission yeast (Schizosaccharomyces pombe) through a pathway involving regulatory and catalytic subunits of PP2A and acting on both Wee1 and Cdc25. Virology 287 2 (2001) 359-370
21. Esau C., Boes M., Youn H.D., Tatterson L., Liu J.O., and Chen J. Deletion of calcineurin and myocyte enhancer factor 2 (MEF2) binding domain of Cabin1 results in enhanced cytokine gene expression in T cells. J. Exp. Med. 194 10 (2001) 1449-1459
22. Foerster M., Haefner D., and Kroegel C. Bcl-2-mediated regulation of CD69-induced apoptosis of human eosinophils: identification and characterization of a novel receptor-induced mechanism and relationship to CD95-transduced signalling. Scand. J. Immunol. 56 4 (2002) 417-428
23. Geiss G.K., Bumgarner R.E., An M.C., Agy M.B., van't Wout A.B., Hammersmark E., Carter V.S., Upchurch D., Mullins J.I., and Katze M.G. Large-scale monitoring of host cell gene expression during HIV-1 infection using cDNA microarrays. Virology 266 1 (2000) 8-16
24. George M.D., Sankaran S., Reay E., Gelli A.C., and Dandekar S. High-throughput gene expression profiling indicates dysregulation of intestinal cell cycle mediators and growth factors during primary simian immunodeficiency virus infection. Virology 312 1 (2003) 84-94
25. + T-cell restoration and enhanced gene expression regulating mucosal repair and regeneration. J. Virol. 79 5 (2005) 2709-2719
26. Gilbreth M., Yang P., Bartholomeusz G., Pimental R.A., Kansra S., Gadiraju R., and Marcus S. Negative regulation of mitosis in fission yeast by the shk1 interacting protein skb1 and its human homolog, Skb1Hs. Proc. Natl. Acad. Sci. U. S. A. 95 25 (1998) 14781-14786
27. Greenberg M.E., Iafrate A.J., and Skowronski J. The SH3 domain-binding surface and an acidic motif in HIV-1 Nef regulate trafficking of class I MHC complexes. EMBO J. 17 10 (1998) 2777-2789
28. Greenway A.L., Dutartre H., Allen K., McPhee D.A., Olive D., and Collette Y. Simian immunodeficiency virus and human immunodeficiency virus type 1 nef proteins show distinct patterns and mechanisms of Src kinase activation. J. Virol. 73 7 (1999) 6152-6158
29. Guy B., Kieny M.P., Riviere Y., Le Peuch C., Dott K., Girard M., Montagnier L., and Lecocq J.P. HIV F/3′ orf encodes a phosphorylated GTP-binding protein resembling an oncogene product. Nature 330 6145 (1987) 266-269
30. Haas A.L., Ahrens P., Bright P.M., and Ankel H. Interferon induces a 15-kilodalton protein exhibiting marked homology to ubiquitin. J. Biol. Chem. 262 23 (1987) 11315-11323
31. Haering C.H., Lowe J., Hochwagen A., and Nasmyth K. Molecular architecture of SMC proteins and the yeast cohesin complex. Mol. Cell 9 4 (2002) 773-788
32. Hanes J., von der Kammer H., Klaudiny J., and Scheit K.H. Characterization by cDNA cloning of two new human protein kinases. Evidence by sequence comparison of a new family of mammalian protein kinases. J. Mol. Biol. 244 5 (1994) 665-672
33. Hua J., and Cullen B.R. Human immunodeficiency virus types 1 and 2 and simian immunodeficiency virus Nef use distinct but overlapping target sites for downregulation of cell surface CD4. J. Virol. 71 9 (1997) 6742-6748
34. Iafrate A.J., Bronson S., and Skowronski J. Separable functions of Nef disrupt two aspects of T cell receptor machinery: CD4 expression and CD3 signaling. EMBO J. 16 4 (1997) 673-684
35. Kawano T., Cui J., Koezuka Y., Toura I., Kaneko Y., Motoki K., Ueno H., Nakagawa R., Sato H., Kondo E., Koseki H., and Taniguchi M. CD1d-restricted and TCR-mediated activation of valpha14 NKT cells by glycosylceramides. Science 278 5343 (1997) 1626-1629
36. Kestler III H.W., Ringler D.J., Mori K., Panicali D.L., Sehgal P.K., Daniel M.D., and Desrosiers R.C. Importance of the nef gene for maintenance of high virus loads and for development of AIDS. Cell 65 4 (1991) 651-662
37. Kirchhoff F., Greenough T.C., Brettler D.B., Sullivan J.L., and Desrosiers R.C. Brief report: absence of intact nef sequences in a long-term survivor with nonprogressive HIV-1 infection. N. Engl. J. Med. 332 4 (1995) 228-232
38. Kirchhoff F., Munch J., Carl S., Stolte N., Matz-Rensing K., Fuchs D., Haaft P.T., Heeney J.L., Swigut T., Skowronski J., and Stahl-Hennig C. The human immunodeficiency virus type 1 nef gene can to a large extent replace simian immunodeficiency virus nef in vivo. J. Virol. 73 10 (1999) 8371-8383
39. Kramer-Hammerle S., Hahn A., Brack-Werner R., and Werner T. Elucidating effects of long-term expression of HIV-1 Nef on astrocytes by microarray, promoter, and literature analyses. Gene 358 (2005) 31-38
40. Lama J., Mangasarian A., and Trono D. Cell-surface expression of CD4 reduces HIV-1 infectivity by blocking Env incorporation in a Nef- and Vpu-inhibitable manner. Curr. Biol. 9 12 (1999) 622-631
41. Lang S.M., Iafrate A.J., Stahl-Hennig C., Kuhn E.M., Nisslein T., Kaup F.J., Haupt M., Hunsmann G., Skowronski J., and Kirchhoff F. Association of simian immunodeficiency virus Nef with cellular serine/threonine kinases is dispensable for the development of AIDS in rhesus macaques. Nat. Med. 3 8 (1997) 860-865
42. Le Gall S., Erdtmann L., Benichou S., Berlioz-Torrent C., Liu L., Benarous R., Heard J.M., and Schwartz O. Nef interacts with the mu subunit of clathrin adaptor complexes and reveals a cryptic sorting signal in MHC I molecules. Immunity 8 4 (1998) 483-495
43. Lee C.H., Leung B., Lemmon M.A., Zheng J., Cowburn D., Kuriyan J., and Saksela K. A single amino acid in the SH3 domain of Hck determines its high affinity and specificity in binding to HIV-1 Nef protein. EMBO J. 14 20 (1995) 5006-5015
44. Li C., and Wong W.H. Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc. Natl. Acad Sci. U.S.A. 98 1 (2001) 31-36
45. Lock M., Greenberg M.E., Iafrate A.J., Swigut T., Muench J., Kirchhoff F., Shohdy N., and Skowronski J. 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 10 (1999) 2722-2733
46. Lopez-Cabrera M., Santis A.G., Fernandez-Ruiz E., Blacher R., Esch F., Sanchez-Mateos P., and Sanchez-Madrid F. Molecular cloning, expression, and chromosomal localization of the human earliest lymphocyte activation antigen AIM/CD69, a new member of the C-type animal lectin superfamily of signal-transmitting receptors. J. Exp. Med. 178 2 (1993) 537-547
47. Lopez-Cabrera M., Munoz E., Blazquez M.V., Ursa M.A., Santis A.G., and Sanchez-Madrid F. Transcriptional regulation of the gene encoding the human C-type lectin leukocyte receptor AIM/CD69 and functional characterization of its tumor necrosis factor-alpha-responsive elements. J. Biol. Chem. 270 37 (1995) 21545-21551
48. Mahalingam S., Ayyavoo V., Patel M., Kieber-Emmons T., Kao G.D., Muschel R.J., and Weiner D.B. HIV-1 Vpr interacts with a human 34-kDa mov34 homologue, a cellular factor linked to the G2/M phase transition of the mammalian cell cycle. Proc. Natl. Acad. Sci. U.S.A. 95 7 (1998) 3419-3424
49. Mandell C.P., Reyes R.A., Cho K., Sawai E.T., Fang A.L., Schmidt K.A., and Luciw P.A. SIV/HIV Nef recombinant virus (SHIVnef) produces simian AIDS in rhesus macaques. Virology 265 2 (1999) 235-251
50. Mariani R., and Skowronski J. CD4 down-regulation by nef alleles isolated from human immunodeficiency virus type 1-infected individuals. Proc. Natl. Acad. Sci. U.S.A. 90 12 (1993) 5549-5553
51. Matsusaka T., and Pines J. Chfr acts with the p38 stress kinases to block entry to mitosis in mammalian cells. J. Cell Biol. 166 4 (2004) 507-516
52. Meyerson M., and Harlow E. Identification of G1 kinase activity for cdk6, a novel cyclin D partner. Mol. Cell. Biol. 14 3 (1994) 2077-2086
53. Motomura K., Toyoda N., Oishi K., Sato H., Nagai S., Hashimoto S., Tugume S., Enzama B., Mugewa R., Mutuluuza R., Mugyeyi C.K., Nagatake P., and Matsushima T. Identification of a host gene subset related to disease prognosis of HIV-1 infected individuals. Int. Immunopharmacol. 4 14 (2004) 1829-1836
54. + T cells through G1/S phase of the cell cycle. J. Virol. 76 8 (2002) 3587-3595
55. Oehme I., Bosser S., and Zornig M. Agonists of an ecdysone-inducible mammalian expression system inhibit Fas Ligand- and TRAIL-induced apoptosis in the human colon carcinoma cell line RKO. Cell Death Differ. 13 2 (2006) 189-201
56. Okayama H., Nagata A., Jinno S., Murakami H., Tanaka K., and Nakashima N. Cell cycle control in fission yeast and mammals: identification of new regulatory mechanisms. Adv. Cancer Res. 69 (1996) 17-62
57. Piguet V., Chen Y.L., Mangasarian A., Foti M., Carpentier J.L., and Trono D. Mechanism of Nef-induced CD4 endocytosis: Nef connects CD4 with the mu chain of adaptor complexes. EMBO J. 17 9 (1998) 2472-2481
58. Piguet V., and Trono D. The Nef protein of primate lentiviruses. Rev. Med. Virol. 9 2 (1999) 111-120
59. Piguet V., Wan L., Borel C., Mangasarian A., Demaurex N., Thomas G., and Trono D. HIV-1 Nef protein binds to the cellular protein PACS-1 to downregulate class I major histocompatibility complexes. Nat. Cell Biol. 2 3 (2000) 163-167
60. Porcelli S.A., and Modlin R.L. The CD1 system: antigen-presenting molecules for T cell recognition of lipids and glycolipids. Annu. Rev. Immunol. 17 (1999) 297-329
61. Qiao X., He B., Chiu A., Knowles D.M., Chadburn A., and Cerutti A. Human immunodeficiency virus 1 Nef suppresses CD40-dependent immunoglobulin class switching in bystander B cells. Nat. Immunol. 7 3 (2006) 302-310
62. Renkema G.H., and Saksela K. Interactions of HIV-1 NEF with cellular signal transducing proteins. Front Biosci. 5 (2000) D268-D283
63. Rhee S.S., and Marsh J.W. Human immunodeficiency virus type 1 Nef-induced down-modulation of CD4 is due to rapid internalization and degradation of surface CD4. J. Virol. 68 8 (1994) 5156-5163
64. Roeth J.F., Williams M., Kasper M.R., Filzen T.M., and Collins K.L. HIV-1 Nef disrupts MHC-I trafficking by recruiting AP-1 to the MHC-I cytoplasmic tail. J. Cell Biol. 167 5 (2004) 903-913
65. Rollins S.A., and Sims P.J. The complement-inhibitory activity of CD59 resides in its capacity to block incorporation of C9 into membrane C5b-9. J. Immunol. 144 9 (1990) 3478-3483
66. Ross T.M., Oran A.E., and Cullen B.R. Inhibition of HIV-1 progeny virion release by cell-surface CD4 is relieved by expression of the viral Nef protein. Curr. Biol. 9 12 (1999) 613-621
67. Sadhu K., Reed S.I., Richardson H., and Russell P. Human homolog of fission yeast cdc25 mitotic inducer is predominantly expressed in G2. Proc. Natl. Acad. Sci. U. S. A. 87 13 (1990) 5139-5143
68. + viruses but not for down-regulation of CD4. EMBO J. 14 3 (1995) 484-491
69. Sankaran S., Guadalupe M., Reay E., George M.D., Flamm J., Prindiville T., and Dandekar S. Gut mucosal T cell responses and gene expression correlate with protection against disease in long-term HIV-1-infected nonprogressors. Proc. Natl. Acad. Sci. U. S. A. 102 28 (2005) 9860-9865
70. Santis A.G., Lopez-Cabrera M., Sanchez-Madrid F., and Proudfoot N. Expression of the early lymphocyte activation antigen CD69, a C-type lectin, is regulated by mRNA degradation associated with AU-rich sequence motifs. Eur. J. Immunol. 25 8 (1995) 2142-2146
71. Sawai E.T., Baur A., Struble H., Peterlin B.M., Levy J.A., and Cheng-Mayer C. Human immunodeficiency virus type 1 Nef associates with a cellular serine kinase in T lymphocytes. Proc. Natl. Acad. Sci. U. S. A. 91 4 (1994) 1539-1543
72. Sawai E.T., Baur A.S., Peterlin B.M., Levy J.A., and Cheng-Mayer C. A conserved domain and membrane targeting of Nef from HIV and SIV are required for association with a cellular serine kinase activity. J. Biol. Chem. 270 25 (1995) 15307-15314
73. Schwartz O., Marechal V., Le Gall S., Lemonnier F., and Heard J.M. Endocytosis of major histocompatibility complex class I molecules is induced by the HIV-1 Nef protein. Nat. Med. 2 3 (1996) 338-342
74. Shaffer A.L., Yu X., He Y., Boldrick J., Chan E.P., and Staudt L.M. BCL-6 represses genes that function in lymphocyte differentiation, inflammation, and cell cycle control. Immunity 13 2 (2000) 199-212
75. Shaheduzzaman S., Krishnan V., Petrovic A., Bittner M., Meltzer P., Trent J., Venkatesan S., and Zeichner S. Effects of HIV-1 Nef on cellular gene expression profiles. J. Biomed. Sci. 9 1 (2002) 82-96
76. Shibata R., Kawamura M., Sakai H., Hayami M., Ishimoto A., and Adachi A. Generation of a chimeric human and simian immunodeficiency virus infectious to monkey peripheral blood mononuclear cells. J. Virol. 65 7 (1991) 3514-3520
77. Shibata R., Maldarelli F., Siemon C., Matano T., Parta M., Miller G., Fredrickson T., and Martin M.A. Infection and pathogenicity of chimeric simian-human immunodeficiency viruses in macaques: determinants of high virus loads and CD4 cell killing. J. Infect. Dis. 176 2 (1997) 362-373
78. Shugars D.C., Smith M.S., Glueck D.H., Nantermet P.V., Seillier-Moiseiwitsch F., and Swanstrom R. Analysis of human immunodeficiency virus type 1 nef gene sequences present in vivo. J. Virol. 67 8 (1993) 4639-4650
79. Simmons A., Aluvihare V., and McMichael A. Nef triggers a transcriptional program in T cells imitating single-signal T cell activation and inducing HIV virulence mediators. Immunity 14 6 (2001) 763-777
80. Sinclair E., Barbosa P., and Feinberg M.B. The nef gene products of both simian and human immunodeficiency viruses enhance virus infectivity and are functionally interchangeable. J. Virol. 71 5 (1997) 3641-3651
81. Skowronski J., Parks D., and Mariani R. Altered T cell activation and development in transgenic mice expressing the HIV-1 nef gene. EMBO J. 12 2 (1993) 703-713
82. Strausfeld U., Labbe J.C., Fesquet D., Cavadore J.C., Picard A., Sadhu K., Russell P., and Doree M. Dephosphorylation and activation of a p34cdc2/cyclin B complex in vitro by human CDC25 protein. Nature 351 6323 (1991) 242-245
83. Swigut T., Iafrate A.J., Muench J., Kirchhoff F., and Skowronski J. Simian and human immunodeficiency virus Nef proteins use different surfaces to downregulate class I major histocompatibility complex antigen expression. J. Virol. 74 12 (2000) 5691-5701
84. Swingler S., Brichacek B., Jacque J.M., Ulich C., Zhou J., and Stevenson M. HIV-1 Nef intersects the macrophage CD40L signalling pathway to promote resting-cell infection. Nature 424 6945 (2003) 213-219
85. Toby G.G., Gherraby W., Coleman T.R., and Golemis E.A. A novel RING finger protein, human enhancer of invasion 10, alters mitotic progression through regulation of cyclin B levels. Mol. Cell. Biol. 23 6 (2003) 2109-2122
86. van't Wout A.B., Lehrman G.K., Mikheeva S.A., O'Keeffe G.C., Katze M.G., Bumgarner R.E., Geiss G.K., and Mullins J.I. Cellular gene expression upon human immunodeficiency virus type 1 infection of CD4(+)-T-cell lines. J. Virol. 77 2 (2003) 1392-1402
87. van't Wout A.B., Swain J.V., Schindler M., Rao U., Pathmajeyan M.S., Mullins J.I., and Kirchhoff F. Nef induces multiple genes involved in cholesterol synthesis and uptake in human immunodeficiency virus type 1-infected T cells. J. Virol. 79 15 (2005) 10053-10058
88. Walk S.F., Alexander M., Maier B., Hammarskjold M.L., Rekosh D.M., and Ravichandran K.S. Design and use of an inducibly activated human immunodeficiency virus type 1 Nef to study immune modulation. J. Virol. 75 2 (2001) 834-843
89. Walsh G.M., Williamson M.L., Symon F.A., Willars G.B., and Wardlaw A.J. Ligation of CD69 induces apoptosis and cell death in human eosinophils cultured with granulocyte-macrophage colony-stimulating factor. Blood 87 7 (1996) 2815-2821
90. Wan L., Molloy S.S., Thomas L., Liu G., Xiang Y., Rybak S.L., and Thomas G. PACS-1 defines a novel gene family of cytosolic sorting proteins required for trans-Golgi network localization. Cell 94 2 (1998) 205-216
91. Wang H., Moon E.Y., Azouz A., Wu X., Smith A., Schneider H., Hogg N., and Rudd C.E. SKAP-55 regulates integrin adhesion and formation of T cell-APC conjugates. Nat. Immunol. 4 4 (2003) 366-374
92. Weeks R., Dowhan W., Shen H., Balantac N., Meengs B., Nudelman E., and Leung D.W. Isolation and expression of an isoform of human CDP-diacylglycerol synthase cDNA. DNA Cell Biol. 16 3 (1997) 281-289
93. Wen W., Chen S., Cao Y., Zhu Y., and Yamamoto Y. HIV-1 infection initiates changes in the expression of a wide array of genes in U937 promonocytes and HUT78 T cells. Virus Res. 113 1 (2005) 26-35
94. Wolf D., Witte V., Laffert B., Blume K., Stromer E., Trapp S., d'Aloja P., Schurmann A., and Baur A.S. HIV-1 Nef associated PAK and PI3-kinases stimulate Akt-independent Bad-phosphorylation to induce anti-apoptotic signals. Nat. Med. 7 11 (2001) 1217-1224
95. Wu L., Fu J., and Shen S.H. SKAP55 coupled with CD45 positively regulates T-cell receptor-mediated gene transcription. Mol. Cell. Biol. 22 8 (2002) 2673-2686
96. Xu Y., and Song G. The role of CD40-CD154 interaction in cell immunoregulation. J. Biomed. Sci. 11 4 (2004) 426-438
97. Yoon K., Jeong J.G., and Kim S. Stable expression of human immunodeficiency virus type 1 Nef confers resistance against Fas-mediated apoptosis. AIDS Res. Hum. Retroviruses 17 2 (2001) 99-104
98. Zheng Y.H., Plemenitas A., Linnemann T., Fackler O.T., and Peterlin B.M. Nef increases infectivity of HIV via lipid rafts. Curr. Biol. 11 11 (2001) 875-879
99. Zheng Y.H., Plemenitas A., Fielding C.J., and Peterlin B.M. Nef increases the synthesis of and transports cholesterol to lipid rafts and HIV-1 progeny virions. Proc. Natl. Acad. Sci. U. S. A. 100 14 (2003) 8460-8465