HIV immune evasion. Diruption of antigen presentation by the HIV nef protein

Advances in Virus Research

Volumn 80, Issue , 2011, Pages 103-127

  Wonderlich, Elizabeth R ^a,c   Leonard, Jolie A ^a   Collins, Kathleen L ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Antigen presentation; AP 1; HIV; MHC I; Nef

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; MEMBRANE ANTIGEN; NEF PROTEIN;

ANTIGEN PRESENTATION; BOOK; GENE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE EVASION; IMMUNOLOGY; METABOLISM; SIGNAL TRANSDUCTION; VIROLOGY;

ADP-RIBOSYLATION FACTORS; ANTIGEN PRESENTATION; ANTIGENS, SURFACE; GENE EXPRESSION REGULATION, VIRAL; GENES, MHC CLASS I; HIV INFECTIONS; HIV-1; HUMANS; IMMUNE EVASION; NEF GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; SIGNAL TRANSDUCTION;

EID: 79960255087     PISSN: 00653527     EISSN: 15578399     Source Type: Book Series    
DOI: 10.1016/B978-0-12-385987-7.00005-1     Document Type: Book

References (115)

1. Akari H., Arold S., Fukumori T., Okazaki T., Strebel K., Adachi A. Nef-induced major histocompatibility complex class I down-regulation is functionally dissociated from its virion incorporation, enhancement of viral infectivity, and CD4 down-regulation. J. Virol. 2000, 74:2907.
2. Aniento F., Gu F., Parton R.G., Gruenberg J. An endosomal beta COP is involved in the pH-dependent formation of transport vesicles destined for late endosomes. J. Cell Biol. 1996, 133:29.
3. Atkins K.M., Thomas L., Youker R.T., Harriff M.J., Pissani F., You H., Thomas G. HIV-1 Nef binds PACS-2 to assemble a multikinase cascade that triggers major histocompatibility complex class I (MHC-I) down-regulation: Analysis using short interfering RNA and knock-out mice. J. Biol. Chem. 2008, 283:11772.
4. Balch W.E., Kahn R.A., Schwaninger R. ADP-ribosylation factor is required for vesicular trafficking between the endoplasmic reticulum and the cis-Golgi compartment. J. Biol. Chem. 1992, 267:13053.
5. Baugh L.L., Garcia J.V., Foster J.L. Functional characterization of the human immunodeficiency virus type 1 Nef acidic domain. J. Virol. 2008, 82:9657.
6. Benichou S., Bomsel M., Bodeus M., Durand H., doute M., Letourneur F., Camonis J., Benarous R. Physical interaction of the HIV-1 Nef protein wih β-cop, a component of non-clathrin coated vesicles essential for membrane traffic. J. Biol. Chem. 1994, 269:30073.
7. Berke G. The CTL's kiss of death. Cell 1995, 81:9.
8. Birch M.R., Learmont J.C., Dyer W.B., Deacon N.J., Zaunders J.J., Saksena N., Cunningham A.L., Mills J., Sullivan J.S. An examination of signs of disease progression in survivors of the Sydney Blood Bank Cohort (SBBC). J. Clin. Virol. 2001, 22:263.
9. Blagoveshchenskaya A.D., Thomas L., Feliciangeli S.F., Hung C.H., Thomas G. HIV-1 Nef downregulates MHC-I by a PACS-1- and PI3K-regulated ARF6 endocytic pathway. Cell 2002, 111:853.
10. Bresnahan P.A., Yonemoto W., Ferrell S., Williams-Herman D., Geleziunas R., 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. 1998, 8:1235.
11. Carl S., Greenough T.C., Krumbiegel M., Greenberg M., Skowronski J., Sullivan J.L., Kirchhoff F. Modulation of different human immunodeficiency virus type 1 Nef functions during progression to AIDS. J. Virol. 2001, 75:3657.
12. Cohen G.B., Gandhi R.T., Davis D.M., Mandelboim O., Chen B.K., Strominger J.L., Baltimore D. The selective downregulation of class I major histocompatibility complex proteins by HIV-1 protects HIV-infected cells from NK cells. Immunity 1999, 10:661.
13. Collins K.L. Resistance of HIV-infected cells to cytotoxic T lymphocytes. Microbes Infect. 2004, 6:494.
14. Collins K., Chen B., Kalams S., Walker B., Baltimore D. HIV-1 Nef protein protects infected primary human cells from killing by cytotoxic T lymphocytes. Nature 1998, 391:397.
15. Craig H., Pandori M., Guatelli J. 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. USA 1998, 95:11229.
16. Craig H.M., Reddy T.R., Riggs N.L., Dao P.P., Guatelli J.C. Interactions of HIV-1 nef with the mu subunits of adaptor protein complexes 1, 2, and 3: Role of the dileucine-based sorting motif. Virology 2000, 271:9.
17. Crump C.M., Xiang Y., Thomas L., Gu F., Austin C., Tooze S.A., Thomas G. PACS-1 binding to adaptors is required for acidic cluster motif-mediated protein traffic. EMBO J. 2001, 20:2191.
18. Daro E., Sheff D., Gomez M., Kreis T., Mellman I. Inhibition of endosome function in CHO cells bearing a temperature-sensitive defect in the coatomer (COPI) component epsilon-COP. J. Cell Biol. 1997, 139:1747.
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., et al. Genomic structure of an attenuated quasi species of HIV-1 from a blood transfusion donor and recipients. Science 1995, 270:988.
20. Dikeakos J.D., Atkins K.M., Thomas L., Emert-Sedlak L., Byeon I.J., Jung J., Ahn J., Wortman M.D., Kukull B., Saito M., Koizumi H., Williamson D.M., et al. Small Molecule Inhibition of HIV-1-Induced MHC-I Downregulation Identifies a Temporally Regulated Switch in Nef Action. Mol Biol Cell 2010, 19:3279.
21. Donaldson J.G., Klausner R.D. ARF: A key regulatory switch in membrane traffic and organelle structure. Curr. Opin. Cell Biol. 1994, 6:527.
22. Donaldson J.G., Cassel D., Kahn R.A., Klausner R.D. ADP-ribosylation factor, a small GTP-binding protein, is required for binding of the coatomer protein beta-COP to Golgi membranes. Proc. Natl. Acad. Sci. USA 1992, 89:6408.
23. Doray B., Ghosh P., Griffith J., Geuze H.J., Kornfeld S. Cooperation of GGAs and AP-1 in packaging MPRs at the trans-Golgi network. Science 2002, 297:1700.
24. Douek D.C., Brenchley J.M., Betts M.R., Ambrozak D.R., Hill B.J., Okamoto Y., Casazza J.P., Kuruppu J., Kunstman K., Wolinsky S., Grossman Z., Dybul M., et al. HIV preferentially infects HIV-specific CD4+ T cells. Nature 2002, 417:95.
25. Douglas J.L., Gustin J.K., Viswanathan K., Mansouri M., Moses A.V., Fruh K. The great escape: Viral strategies to counter BST-2/tetherin. PLoS Pathog. 2010, 6:e1000913.
26. Dyer W.B., Geczy A.F., Kent S.J., McIntyre L.B., Blasdall S.A., Learmont J.C., Sullivan J.S. Lymphoproliferative immune function in the Sydney Blood Bank Cohort, infected with natural nef/long terminal repeat mutants, and in other long-term survivors of transfusion-acquired HIV-1 infection. AIDS 1997, 11:1565.
27. Eichholtz T., Vossebeld P., van Overveld M., Ploegh H. Activation of protein kinase C accelerates internalization of transferrin receptor but not of major histocompatibility complex class I, independent of their phosphorylation status. J. Biol. Chem. 1992, 267:22490.
28. Erdtmann L., Janvier K., Raposo G., Craig H.M., Benaroch P., Berlioz-Torrent C., Guatelli J.C., Benarous R., Benichou S. Two independent regions of HIV-1 Nef are required for connection with the endocytic pathway through binding to the mu 1 chain of AP1 complex. Traffic 2000, 1:871.
29. Fackler O.T., Luo W., Geyer M., Alberts A.S., Peterlin B.M. Activation of Vav by Nef induces cytoskeletal rearrangements and downstream effector functions. Mol. Cell 1999, 3:729.
30. Faure J., Stalder R., Borel C., Sobo K., Piguet V., Demaurex N., Gruenberg J., Trono D. ARF1 regulates Nef-induced CD4 degradation. Curr. Biol. 2004, 14:1056.
31. Ganser-Pornillos B.K., Yeager M., Sundquist W.I. The structural biology of HIV assembly. Curr. Opin. Struct. Biol. 2008, 18:203.
32. Garcia J.V., Miller A.D. Serine phosphorylation-independent downregulation of cell-surface CD4 by nef. Nature 1991, 350:508.
33. Geldmacher C., Currier J.R., Herrmann E., Haule A., Kuta E., McCutchan F., Njovu L., Geis S., Hoffmann O., Maboko L., Williamson C., Birx D., et al. CD8 T-cell recognition of multiple epitopes within specific Gag regions is associated with maintenance of a low steady-state viremia in human immunodeficiency virus type 1-seropositive patients. J. Virol. 2007, 81:2440.
34. Greenberg M., DeTulleo L., Rapoport I., Skowronski J., Kirchhausen T. A dileucine motif in HIV-1 Nef is essential for sorting into clathrin-coated pits and for downregulation of CD4. Curr. Biol. 1998, 8:1239.
35. Greenberg M., Iafrate A., Skowronski J. The SH3 domain-binding surface and an acidic motif in HIV-1 Nef regulate trafficking of class I MHC complexes. EMBO J. 1998, 17:2777.
36. Gu F., Gruenberg J. ARF1 regulates pH-dependent COP functions in the early endocytic pathway. J. Biol. Chem. 2000, 275:8154.
37. Gu F., Aniento F., Parton R.G., Gruenberg J. Functional dissection of COP-I subunits in the biogenesis of multivesicular endosomes. J. Cell Biol. 1997, 139:1183.
38. Hansen T.H., Bouvier M. MHC class I antigen presentation: Learning from viral evasion strategies. Nat. Rev. Immunol. 2009, 9:503.
39. Helms J.B., Rothman J.E. Inhibition by brefeldin A of a Golgi membrane enzyme that catalyses exchange of guanine nucleotide bound to ARF. Nature 1992, 360:352.
40. Hill M., Tachedjian G., Mak J. The packaging and maturation of the HIV-1 Pol proteins. Curr. HIV Res. 2005, 3:73.
41. Hinners I., Wendler F., Fei H., Thomas L., Thomas G., Tooze S.A. AP-1 recruitment to VAMP4 is modulated by phosphorylation-dependent binding of PACS-1. EMBO Rep. 2003, 4:1182.
42. Hung C.H., Thomas L., Ruby C.E., Atkins K.M., Morris N.P., Knight Z.A., Scholz I., Barklis E., Weinberg A.D., Shokat K.M., Thomas G. HIV-1 Nef assembles a Src family kinase-ZAP-70/Syk-PI3K cascade to downregulate cell-surface MHC-I. Cell Host Microbe 2007, 1:121.
43. Jackson C.L., Casanova J.E. Turning on ARF: The Sec7 family of guanine-nucleotide-exchange factors. Trends Cell Biol. 2000, 10:60.
44. Janvier K., Craig H., Le Gall S., Benarous R., Guatelli J., Schwartz O., Benichou S. Nef-induced CD4 downregulation: A diacidic sequence in human immunodeficiency virus type 1 Nef does not function as a protein sorting motif through direct binding to beta-COP. J. Virol. 2001, 75:3971.
45. Janvier K., Craig H., Hitchin D., Madrid R., Sol-Foulon N., Renault L., Cherfils J., Cassel D., Benichou S., Guatelli J. HIV-1 Nef stabilizes the association of adaptor protein complexes with membranes. J. Biol. Chem. 2003, 278:8725.
46. Janvier K., Kato Y., Boehm M., Rose J.R., Martina J.A., Kim B.Y., Venkatesan S., Bonifacino J.S. Recognition of dileucine-based sorting signals from HIV-1 Nef and LIMP-II by the AP-1 gamma-sigma1 and AP-3 delta-sigma3 hemicomplexes. J. Cell Biol. 2003, 163:1281.
47. Kahn R.A., Randazzo P., Serafini T., Weiss O., Rulka C., Clark J., Amherdt M., Roller P., Orci L., Rothman J.E. The amino terminus of ADP-ribosylation factor (ARF) is a critical determinant of ARF activities and is a potent and specific inhibitor of protein transport. J. Biol. Chem. 1992, 267:13039.
48. Kasper M.R., Collins K.L. Nef-mediated disruption of HLA-A2 transport to the cell surface in T cells. J. Virol. 2003, 77:3041.
49. Kasper M.R., Roeth J.F., Williams M., Filzen T.M., Fleis R.I., Collins K.L. HIV-1 Nef disrupts antigen presentation early in the secretory pathway. J. Biol. Chem. 2005, 280:12840.
50. Kelly B.T., McCoy A.J., Spate K., Miller S.E., Evans P.R., Honing S., Owen D.J. A structural explanation for the binding of endocytic dileucine motifs by the AP2 complex. Nature 2008, 456:976.
51. Kestler H.W., Ringler D.J., Mori K., Panicali D.L., Sehgal P.K., Daniel M.D., Desrosiers R.C. Importance of the nef gene for maintenance of high virus loads and for development of AIDS. Cell 1991, 65:651.
52. Kiepiela P., Ngumbela K., Thobakgale C., Ramduth D., Honeyborne I., Moodley E., Reddy S., de Pierres C., Mncube Z., Mkhwanazi N., Bishop K., van der Stok M., et al. CD8+ T-cell responses to different HIV proteins have discordant associations with viral load. Nat. Med. 2007, 13:46.
53. Kirchhoff F. Immune evasion and counteraction of restriction factors by HIV-1 and other primate lentiviruses. Cell Host Microbe 2010, 8:55.
54. Kirchoff F., Greenough T., Brettler D., Sullivan J., Desrosiers R. Absence of intact nef sequences in a long-term survivor with nonprogressive HIV-1 infection. N. Engl. J. Med. 1995, 332:228.
55. Klumperman J., Hille A., Veenendaal T., Oorschot V., Stoorvogel W., von Figura K., Geuze H.J. Differences in the endosomal distributions of the two mannose 6-phosphate receptors. J. Cell Biol. 1993, 121:997.
56. Larsen J.E., Massol R.H., Nieland T.J., Kirchhausen T. HIV Nef-mediated major histocompatibility complex class I down-modulation is independent of Arf6 activity. Mol. Biol. Cell 2004, 15:323.
57. Le Gall S., Erdtmann L., Benichou S., Berlloz-Torrent C., Liu L., Benarous R., Heard J., Schwartz O. Nef interacts with mu subunit of clathrin adaptor complexes and reveals a cryptic sorting signal in MHC I molecules. Immunity 1998, 8:483.
58. Le Gall S., Buseyne F., Trocha A., Walker B.D., Heard J.M., Schwartz O. Distinct trafficking pathways mediate Nef-induced and clathrin-dependent major histocompatibility complex class I down-regulation. J. Virol. 2000, 74:9256.
59. Learmont J., Tindall B., Evans L., Cunningham A., Cunningham P., Wells J., Penny R., Kaldor J., Cooper D.A. Long-term symptomless HIV-1 infection in recipients of blood products from a single donor. Lancet 1992, 340:863. [see comments].
60. Learmont J.C., Geczy A.F., Mills J., Ashton L.J., Raynes-Greenow C.H., Garsia R.J., Dyer W.B., McIntyre L., Oelrichs R.B., Rhodes D.I., Deacon N.J., Sullivan J.S. Immunologic and virologic status after 14 to 18 years of infection with an attenuated strain of HIV-1. A report from the Sydney Blood Bank Cohort. N. Engl. J. Med. 1999, 340:1715.
61. Lewinsohn D.A., Lines R., Lewinsohn D.M., Riddell S.R., Greenberg P.D., Emerman M., Bartz S.R. HIV-1 Vpr does not inhibit CTL-mediated apoptosis of HIV-1 infected cells. Virology 2002, 294:13.
62. Lewis M.J., Balamurugan A., Ohno A., Kilpatrick S., Ng H.L., Yang O.O. Functional adaptation of Nef to the immune milieu of HIV-1 infection in vivo. J. Immunol. 2008, 180:4075.
63. Lindwasser O.W., Smith W.J., Chaudhuri R., Yang P., Hurley J.H., Bonifacino J.S. A diacidic motif in human immunodeficiency virus type 1 Nef is a novel determinant of binding to AP-2. J. Virol. 2008, 82:1166.
64. Liu L.X., Heveker N., Fackler O.T., Arold S., Le Gall S., Janvier K., Peterlin B.M., Dumas C., Schwartz O., Benichou S., Benarous R. Mutation of a conserved residue (D123) required for oligomerization of human immunodeficiency virus type 1 Nef protein abolishes interaction with human thioesterase and results in impairment of Nef biological functions. J. Virol. 2000, 74:5310.
65. Lubben N.B., Sahlender D.A., Motley A.M., Lehner P.J., Benaroch P., Robinson M.S. HIV-1 Nef-induced down-regulation of MHC class I requires AP-1 and clathrin but not PACS-1 and is impeded by AP-2. Mol. Biol. Cell 2007, 18:3351.
66. Machy P., Truneh A., Gennaro D., Hoffstein S. Major histocompatibility complex class I molecules internalized via coated pits in T lymphocytes. Nature 1987, 328:724.
67. Mangasarian A., Piguet V., Wang J.K., Chen Y.L., Trono D. 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. 1999, 73:1964.
68. Mellors J.W., Rinaldo C., Gupta P., White R.M., Todd J.A., Kingsley L.A. Prognosis in HIV-1 infection predicted by the quantity of virus in plasma. Science 1996, 272:1167.
69. Munch J., Stolte N., Fuchs D., Stahl-Hennig C., Kirchhoff F. 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. 2001, 75:10532.
70. Natarajan K., Dimasi N., Wang J., Mariuzza R.A., Margulies D.H. Structure and function of natural killer cell receptors: Multiple molecular solutions to self, nonself discrimination. Annu. Rev. Immunol. 2002, 20:853.
71. Nekhai S., Jeang K.T. Transcriptional and post-transcriptional regulation of HIV-1 gene expression: Role of cellular factors for Tat and Rev. Future Microbiol. 2006, 1:417.
72. Noviello C.M., Benichou S., Guatelli J.C. Cooperative binding of the class I major histocompatibility complex cytoplasmic domain and human immunodeficiency virus type 1 Nef to the endosomal AP-1 complex via its mu subunit. J. Virol. 2008, 82:1249.
73. Orcl L., Palmer D.J., Amherdt M., Rothman J.E. Coated vesicle assembly in the Golgi requires only coatomer and ARF proteins from the cytosol. Nature 1993, 364:732.
74. Owen D.J., Evans P.R. A structural explanation for the recognition of tyrosine-based endocytotic signals. Science 1998, 282:1327.
75. Palmer D.J., Helms J.B., Beckers C.J., Orci L., Rothman J.E. Binding of coatomer to Golgi membranes requires ADP-ribosylation factor. J. Biol. Chem. 1993, 268:12083.
76. Peden A.A., Oorschot V., Hesser B.A., Austin C.D., Scheller R.H., Klumperman J. Localization of the AP-3 adaptor complex defines a novel endosomal exit site for lysosomal membrane proteins. J. Cell Biol. 2004, 164:1065.
77. Piguet V., Chen Y.L., Mangasarian A., Foti M., Carpentier J.L., Trono D. Mechanism of Nef-induced CD4 endocytosis: Nef connects CD4 with the mu chain of adaptor complexes. EMBO J. 1998, 17:2472.
78. Piguet V., Gu F., Foti M., Demaurex N., Gruenberg J., Carpentier J.L., Trono D. Nef-induced CD4 degradation: A diacidic-based motif in Nef functions as a lysosomal targeting signal through the binding of beta-COP in endosomes. Cell 1999, 97:63.
79. Piguet V., Wan L., Borel C., Mangasarian A., Demaurex N., Thomas G., Trono D. HIV-1 Nef protein binds to the cellular protein PACS-1 to downregulate class I major histocompatibility complexes. Nat. Cell Biol. 2000, 2:163.
80. Radhakrishna H., Donaldson J.G. ADP-ribosylation factor 6 regulates a novel plasma membrane recycling pathway. J. Cell Biol. 1997, 139:49.
81. Robinson M.S. Adaptable adaptors for coated vesicles. Trends Cell Biol. 2004, 14:167.
82. Robinson M.S., Bonifacino J.S. Adaptor related proteins. Curr. Opin. Cell Biol. 2001, 13:444.
83. Robinson M.S., Kreis T.E. Recruitment of coat proteins onto Golgi membranes in intact and permeabilized cells: Effects of brefeldin A and G protein activators. Cell 1992, 69:129.
84. Roeth J.F., Collins K.L. Human immunodeficiency virus type 1 Nef: Adapting to intracellular trafficking pathways. Microbiol. Mol. Biol. Rev. 2006, 70:548.
85. Roeth J.F., Kasper M.R., Williams M., Filzen T.M., Collins K.L. HIV-1 Nef disrupts MHC-I trafficking by recruiting AP-1 to the MHC-I cytoplasmic tail. J. Cell Biol. 2004, 167:903.
86. Rothman J.E. Mechanisms of intracellular protein transport. Nature 1994, 372:55.
87. Schaefer M.R., Williams M., Kulpa D.A., Blakely P.K., Yaffee A.Q., Collins K.L. A novel trafficking signal within the HLA-C cytoplasmic tail allows regulated expression upon differentiation of macrophages. J. Immunol. 2008, 180:7804-7817.
88. Schaefer M.R., Wonderlich E.R., Roeth J.F., Leonard J.A., Collins K.L. HIV-1 Nef targets MHC-I and CD4 for degradation via a final common beta-COP-dependent pathway in T cells. PLoS Pathog. 2008, 4:e1000131.
89. Schmid S.L. Clathrin-coated vesicle formation and protein sorting: An integrated process. Annu. Rev. Biochem. 1997, 66:511.
90. Schwartz O., Marechal V., Le Gall S., Lemonnier F., Heard J. Endocytosis of major histocompatibility complex class I molecules is induced by the HIV-1 Nef protein. Nat. Med. 1996, 2:338.
91. Shankar P., Xu Z., Lieberman J. Viral-specific cytotoxic T lymphocytes lyse human immunodeficiency virus-infected primary T lymphocytes by the granule exocytosis pathway. Blood 1999, 94:3084.
92. Singh R.K., Lau D., Noviello C.M., Ghosh P., Guatelli J.C. An MHC-I cytoplasmic domain/HIV-1 Nef fusion protein binds directly to the mu subunit of the AP-1 endosomal coat complex. PLoS ONE 2009, 4:e8364.
93. Stove V., Van de Walle I., Naessens E., Coene E., Stove C., Plum J., Verhasselt B. Human immunodeficiency virus Nef induces rapid internalization of the T-cell coreceptor CD8alphabeta. J. Virol. 2005, 79:11422.
94. Swann S.A., Williams M., Story C.M., Bobbitt K.R., Fleis R., Collins K.L. HIV-1 Nef blocks transport of MHC class I molecules to the cell surface via a PI 3-kinase-dependent pathway. Virology 2001, 282:267.
95. Swigut T., Shohdy N., Skowronski J. Mechanism for down-regulation of CD28 by Nef. EMBO J. 2001, 20:1593.
96. Swigut T., Alexander L., Morgan J., Lifson J., Mansfield K.G., Lang S., Johnson R.P., Skowronski J., Desrosiers R. Impact of Nef-mediated downregulation of major histocompatibility complex class I on immune response to simian immunodeficiency virus. J. Virol. 2004, 78:13335.
97. Taylor T.C., Kahn R.A., Melancon P. Two distinct members of the ADP-ribosylation factor family of GTP-binding proteins regulate cell-free intra-Golgi transport. Cell 1992, 70:69.
98. Tomiyama H., Akari H., Adachi A., Takiguchi M. Different effects of Nef-mediated HLA class I down-regulation on human immunodeficiency virus type 1-specific CD8(+) T-cell cytolytic activity and cytokine production. J. Virol. 2002, 76:7535.
99. Traub L.M. Sorting it out: AP-2 and alternate clathrin adaptors in endocytic cargo selection. J. Cell Biol. 2003, 163:203.
100. Tse D.B., Pernis B. Spontaneous internalization of Class I major histocompatibility complex molecules in T lymphoid cells. J. Exp. Med. 1984, 159:193.
101. Turner C.E., West K.A., Brown M.C. Paxillin-ARF GAP signaling and the cytoskeleton. Curr. Opin. Cell Biol. 2001, 13:593.
102. UNAIDS AIDS epidemic update http://www.unaids.org/en/KnowledgeCentre/HIVData/EpiUpdate/EpiUpdArchive/2009/default.asp.
103. Venkateswarlu K., Cullen P.J. Signalling via ADP-ribosylation factor 6 lies downstream of phosphatidylinositide 3-kinase. Biochem. J 2000, 345(Pt. 3):719.
104. Waguri S., Dewitte F., Le Borgne R., Rouille Y., Uchiyama Y., Dubremetz J.F., Hoflack B. Visualization of TGN to endosome trafficking through fluorescently labeled MPR and AP-1 in living cells. Mol. Biol. Cell 2003, 14:142.
105. Wan L., Molloy S., Thomas L., Liu G., Xiang Y., Rybak S., Thomas G. PACS-1 defines a novel gene family of cytosolic sorting proteins required for trans-Golgi network localization. Cell 1998, 94:205.
106. Waters M.G., Serafini T., Rothman J.E. "Coatomer": A cytosolic protein complex containing subunits of non-clathrin-coated Golgi transport vesicles. Nature 1991, 349:248.
107. Williams M., Roeth J.F., Kasper M.R., Fleis R.I., Przybycin C.G., Collins K.L. Direct binding of human immunodeficiency virus type 1 Nef to the major histocompatibility complex class I (MHC-I) cytoplasmic tail disrupts MHC-I trafficking. J. Virol. 2002, 76:12173.
108. Williams M., Roeth J.F., Kasper M.R., Filzen T., Collins K.L. Human immunodeficiency virus type 1 Nef domains required for disruption of major histocompatibility complex class I trafficking are also necessary for coprecipitation of Nef with HLA-A2. J. Virol. 2005, 79:632.
109. Wonderlich E.R., Williams M., Collins K.L. The tyrosine binding pocket in the adaptor protein 1 (AP-1) mu1 subunit is necessary for Nef to recruit AP-1 to the major histocompatibility complex class I cytoplasmic tail. J. Biol. Chem. 2008, 283:3011.
110. Wong J.K., Strain M.C., Porrata R., Reay E., Sankaran-Walters S., Ignacio C.C., Russell T., Pillai S.K., Looney D.J., Dandekar S. In vivo CD8+ T-cell suppression of siv viremia is not mediated by CTL clearance of productively infected cells. PLoS Pathog. 2010, 6:e1000748.
111. Yang O., Kalams S., Rosenzweig M., Trocha A., Jones N., Koziel M., Walker B., Johnson R.P. Efficient lysis of human immunodeficiency virus type 1-infected cells by cytotoxic T lymphocytes. J. Virol. 1996, 70:5799.
112. Yang O.O., Tran A.C., Kalams S.A., Johnson R.P., Roberts M.R., Walker B.D. Lysis of HIV-1-infected cells and inhibition of viral replication by universal receptor T cells. Proc. Natl. Acad. Sci. USA 1997, 94:11478.
113. Yang O.O., Nguyen P.T., Kalams S.A., Dorfman T., Gottlinger H.G., Stewart S., Chen I.S., Threlkeld S., Walker B.D. Nef-mediated resistance of human immunodeficiency virus type 1 to antiviral cytotoxic T lymphocytes. J. Virol. 2002, 76:1626.
114. Yi L., Rosales T., Rose J.J., Chaudhury B., Knutson J.R., Venkatesan S. HIV-1 Nef binds a subpopulation of MHC-I throughout its trafficking itinerary and down-regulates MHC-I by perturbing both anterograde and retrograde trafficking. J. Biol. Chem. 2010, 285:30884.
115. Youker R.T., Shinde U., Day R., Thomas G. At the crossroads of homoeostasis and disease: Roles of the PACS proteins in membrane traffic and apoptosis. Biochem. J. 2009, 421:1.