HIV-1 Nef: A master manipulator of the membrane trafficking machinery mediating immune evasion

Biochimica et Biophysica Acta - General Subjects

Volumn 1850, Issue 4, 2015, Pages 733-741

  Pawlak, Emily N ^a   Dikeakos, Jimmy D ^a  

^a WESTERN UNIVERSITY   (Canada)

Author keywords

AIDS; HIV 1; Immune evasion; Membrane trafficking; MHC I; Nef

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NEF PROTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE; PHOSPHOFURIN ACIDIC CLUSTER SORTING PROTEIN 1; PHOSPHOFURIN ACIDIC CLUSTER SORTING PROTEIN 2; PROTEIN SERINE THREONINE KINASE; PROTEIN TYROSINE KINASE; TRANSCRIPTION FACTOR AP 1; UBIQUITIN PROTEIN LIGASE COP1; UNCLASSIFIED DRUG; HLA ANTIGEN CLASS 1; NEF PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ADAPTIVE IMMUNITY; DIMERIZATION; DISEASE COURSE; DOWN REGULATION; ENDOCYTOSIS; HOST RESISTANCE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNE EVASION; IMMUNOPATHOGENESIS; IMMUNOSURVEILLANCE; MEMBRANE TRANSPORT; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; REVIEW; SIGNAL TRANSDUCTION; TRANS GOLGI NETWORK; VIRUS GENOME; ACQUIRED IMMUNODEFICIENCY SYNDROME; CELL MEMBRANE; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT; TRANSPORT AT THE CELLULAR LEVEL;

HUMAN IMMUNODEFICIENCY VIRUS 1;

ACQUIRED IMMUNODEFICIENCY SYNDROME; BIOLOGICAL TRANSPORT; CELL MEMBRANE; DOWN-REGULATION; ENDOCYTOSIS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; IMMUNE EVASION; NEF GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; PROTEIN TRANSPORT;

EID: 84921324515     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2015.01.003     Document Type: Review

References (102)

1. P. Wong, E.G. Pamer, Cd8 T cell responses to infectious pathogens, Annu. Rev. Immunol. 21 (2003) 29-70.
2. J. Huotari, A. Helenius, Endosome maturation, EMBO J. 30 (2011) 3481-3500.
3. H. Hengel, J.O. Koopmann, T. Flohr, W. Muranyi, E. Goulmy, G.J. Hammerling, U.H. Koszinowski, F. Momburg, A viral ER-resident glycoprotein inactivates the MHC-encoded peptide transporter, Immunity 6 (1997) 623-632.
4. E.W. Hewitt, S. Sen Gupta, P.J. Lehner, The human cytomegalovirus gene product US6 inhibits ATP binding by TAP, EMBO J. 20 (2001) 387-396.
5. R. Tomazin, A.B. Hill, P. Jugovic, I. York, P. van Endert, H.L. Ploegh, D.W. Andrews, D.C. Johnson, Stable binding of the herpes simplex virus ICP47 protein to the peptide binding site of TAP, EMBO J. 15 (1996) 3256-3266.
6. K. Ahn, T.H. Meyer, S. Uebel, P. Sempe, H. Djaballah, Y. Yang, P.A. Peterson, K. Fruh, R. Tampe, Molecular mechanism and species specificity of TAP inhibition by herpes simplex virus protein ICP47, EMBO J. 15 (1996) 3247-3255.
7. I.A. York, C. Roop, D.W. Andrews, S.R. Riddell, F.L. Graham, D.C. Johnson, A cytosolic herpes-simplex virus protein inhibits antigen presentation to Cd8(+) T-lymphocytes, Cell 77 (1994) 525-535.
8. E.J.H.J. Wiertz, T.R. Jones, L. Sun, M. Bogyo, H.J. Geuze, H.L. Ploegh, The human cytomegalovirus US11 gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol, Cell 84 (1996) 769-779.
9. E.J.H.J. Wiertz, D. Tortorella, M. Bogyo, J. Yu, W. Mothes, T.R. Jones, T.A. Rapoport, H.L. Ploegh, Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction, Nature 384 (1996) 432-438.
10. C.E. Shamu, C.M. Story, T.A. Rapoport, H.L. Ploegh, The pathway of US11-dependent degradation of MHC class I heavy chains involves a ubiquitin-conjugated intermediate, J. Cell Biol. 147 (1999) 45-57.
11. M.H. Furman, H.L. Ploegh, D. Tortorella, Membrane-specific, host-derived factors are required for US2-and US11-mediated degradation of major histocompatibility complex class I molecules, J. Biol. Chem. 277 (2002) 3258-3267.
12. K. Oresic, C.L. Ng, D. Tortorella, TRAM1 participates in human cytomegalovirus US2-and US11-mediated dislocation of an endoplasmic reticulum membrane glycoprotein, J. Biol. Chem. 284 (2009) 5905-5914.
13. B.Y. Park, Y.K. Kim, J.W. Shin, S. Lee, K.M. Cho, K. Fruh, S. Lee, K.S. Ahn, Human cytomegalovirus inhibits tapasin-dependent peptide loading and optimization of the MHC class I peptide cargo for immune evasion, Immunity 20 (2004) 71-85.
14. K.S. Ahn, A. Angulo, P. Ghazal, P.A. Peterson, Y. Yang, K. Fruh, Human cytomegalovirus inhibits antigen presentation by a sequential multistep process, Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 10990-10995.
15. S. Lee, J. Yoon, B. Park, Y. Jun, M. Jin, H.C. Sung, I.H. Kim, S. Kang, E.J. Choi, B.Y. Ahn, K. Ahn, Structural and functional dissection of human cytomegalovirus US3 in binding major histocompatibility complex class I molecules, J. Virol. 74 (2000) 11262-11269.
16. E.M. Bennett, J.R. Bennink, J.W. Yewdell, F.M. Brodsky, Cutting edge: adenovirus E19 has two mechanisms for affecting class I MHC expression, J. Immunol. 162 (1999) 5049-5052.
17. J.H. Cox, J.R. Bennink, J.W. Yewdell, Retention of adenovirus-E19 glycoprotein in the endoplasmic-reticulum is essential to its ability to block antigen presentation, J. Exp. Med. 174 (1991) 1629-1637.
18. M. Sester, Z. Ruszics, E. Mackley, H. Burgert, The transmembrane domain of the adenovirus E3/19 K protein acts as an endoplasmic reticulum retention signal and contributes to intracellular sequestration of major histocompatibility complex class I molecules, J. Virol. 87 (2013) 6104-6117.
19. N.T. Georgopoulos, J.L. Proffitt, G.E. Blair, Transcriptional regulation of the major histocompatibility complex (MHC) class I heavy chain, TAP1 and LMP2 genes by the human papillomavirus (HPV) type 6b, 16 and 18 E7 oncoproteins, Oncogene 19 (2000) 4930-4935.
20. H. Li, X. Ou, J. Xiong, T. Wang, HPV16E7 mediates HADC chromatin repression and downregulation of MHC class I genes in HPV16 tumorigenic cells through interaction with an MHC class I promoter, Biochem. Biophys. Res. Commun. 349 (2006) 1315-1321.
21. W. Li, X.M. Deng, C.X. Wang, X. Zhang, G.X. Zheng, J. Zhang, J.B. Feng, Down-regulation of HLA class I antigen in human papillomavirus type 16 E7 expressing HaCaT cells: correlatewith TAP-1 expression, Int. J. Gynecol. Cancer 20 (2010) 227-232.
22. L. Coscoy, D.J. Sanchez, D. Ganem, A novel class of herpesvirus-encoded membrane-bound E3 ubiquitin ligases regulates endocytosis of proteins involved in immune recognition, J. Cell Biol. 155 (2001) 1265-1273.
23. S. Ishido, C.Y. Wang, B.S. Lee, G.B. Cohen, J.U. Jung, Downregulation of major histocompatibility complex class I molecules by Kaposi's sarcoma-associated herpesvirus K3 and K5 proteins, J. Virol. 74 (2000) 5300-5309.
24. K. Brulois, Z. Toth, L. Wong, P. Feng, S. Gao, A. Ensser, J.U. Jung, Kaposi's sarcoma-associated herpes virus K3 and K5 Ubiquitin E3 Ligases have stagespecific immune evasion roles during lytic replication, J. Virol. 88 (2014) 9335-9349.
25. V. Noriega, V. Redmann, T. Gardner, D. Tortorella, Diverse immune evasion strategies by human cytomegalovirus, Immunol. Res. 54 (2012) 140-151.
26. O. Schwartz, V. Marechal, S. LeGall, F. Lemonnier, J.M. Heard, Endocytosis of major histocompatibility complex class I molecules is induced by the HIV-1 Nef protein, Nat. Med. 2 (1996) 338-342.
27. H.W. Kestler, D.J. Ringler, K. Mori, D.L. Panicali, P.K. Sehgal, M.D. Daniel, R.C. Desrosiers, Importance of the Nef gene for maintenance of high virus loads and for development of aids, Cell 65 (1991).
28. K.M. Atkins, L. Thomas, R.T. Youker, M.J. Harriff, F. Pissani, H. You, G. Thomas, 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. 283 (2008) 11772-11784.
29. R.P. Trible, L. Emert-Sedlak, T.E. Smithgall, HIV-1 Nef selectively activates Src family kinases Hck, Lyn, and c-Src through direct SH3 domain interaction, J. Biol. Chem. 281 (2006) 27029-27038.
30. J.D. Dikeakos, K.M. Atkins, L. Thomas, L. Emert-Sedlak, I.L. Byeon, J. Jung, J. Ahn, M.D. Wortman, B. Kukull, M. Saito, H. Koizumi, D.M. Williamson, M. Hiyoshi, E. Barklis, M. Takiguchi, S. Suzu, A.M. Gronenborn, T.E. Smithgall, G. Thomas, Small molecule inhibition of HIV-1-induced MHC-I down-regulation identifies a temporally regulated switch in Nef action, Mol. Biol. Cell 21 (2010) 3279-3292.
31. C.H. Hung, L. Thomas, C.E. Ruby, K.M. Atkins, N.P. Morris, Z.A. Knight, I. Scholz, E. Barklis, A.D. Weinberg, K.M. Shokat, G. Thomas, HIV-1 Nef assembles a Src family kinase-ZAP-70/Syk-PI3K cascade to downregulate cell-surface MHC-I, Cell Host Microbe 1 (2007) 121-133.
32. S.A. Swann, M. Williams, C.M. Story, K.R. Bobbitt, R. Fleis, K.L. Collins, HIV-1 Nef blocks transport of MHC class I molecules to the cell surface via a PI 3-kinase dependent pathway, Virology 282 (2001) 267-277.
33. E.R. Wonderlich, J.A. Leonard, D.A. Kulpa, K.E. Leopold, J.M. Norman, K.L. Collins, ADP ribosylation factor 1 activity is required to recruit AP-1 to themajor histocompatibility complex class I (MHC-I) cytoplasmic tail and disrupt MHC-I trafficking in HIV-1-infected primary T cells, J. Virol. 85 (2011) 12216-12226.
34. L. Yi, T. Rosales, J.J. Rose, B. Chowdhury, J.R. Knutson, S. Venkatesan, HIV-1 Nef binds a subpopulation of MHC-I throughout its trafficking itinerary and downregulates MHC-I by perturbing both anterograde and retrograde trafficking, J. Biol. Chem. 285 (2010) 30884-30905.
35. C.M. Noviello, S. Benichou, J.C. Guatelli, 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. 82 (2008) 1249-1258.
36. X. Jia, R. Singh, S. Homann, H. Yang, J. Guatelli, Y. Xiong, Structural basis of evasion of cellular adaptive immunity by HIV-1 Nef, Nat. Struct. Mol. Biol. 19 (2012) 701-+.
37. J.D. Dikeakos, L. Thomas, G. Kwon, J. Elferich, U. Shinde, G. Thomas, An interdomain binding site on HIV-1 Nef interacts with PACS-1 and PACS-2 on endosomes to down-regulate MHC-I, Mol. Biol. Cell 23 (2012) 2184-2197.
38. N. Michel, K. Ganter, S. Venzke, J. Bitzegeio, O.T. Fackler, O.T. Keppler, The nef protein of human immunodeficiency virus is a broad-spectrum modulator of chemokine receptor cell surface levels that acts independently of classical motifs for receptor endocytosis and G alpha(i) signaling, Mol. Biol. Cell 17 (2006) 3578-3590.
39. N. Michel, I. Allespach, S. Venzke, O.T. Fackler, O.T. Keppler, The Nef protein of human immunode ficiency virus establishes superinfection immunity by a dual strategy to downregulate cell-surface CCR5 and CD4, Curr. Biol. 15 (2005) 714-723.
40. R. Chaudhuri, O.W. Lindwasser, W.J. Smith, J.H. Hurley, J.S. Bonifacino, Downregulation of CD4 by human immunodeficiency virus type 1 Nef is dependent on clathrin and involves direct interaction of Nef with the AP2 clathrin adaptor, J. Virol. 81 (2007) 3877-3890.
41. M.R. Kasper, J.F. Roeth, M. Williams, T.M. Filzen, R.I. Fleis, K.L. Collins, HIV-1 Nef disrupts antigen presentation early in the secretory pathway, J. Biol. Chem. 280 (2005) 12840-12848.
42. M.R. Schaefer, E.R. Wonderlich, J.F. Roeth, J.A. Leonard, K.L. Collins, HIV-1 Nef targets MHC-I and CD4 for degradation via a final common beta-COP-dependent pathway in T cells, PLoS Pathog. 4 (2008) e1000131.
43. J.A. Leonard, T. Filzen, C.C. Carter, M. Schaefer, K.L. Collins, HIV-1 Nef disrupts intracellular trafficking of major histocompatibility complex class I, CD4, CD8, and CD28 by distinct pathways that share common elements, J. Virol. 85 (2011) 6867-6881.
44. J.F. Roeth, M. Williams, M.R. Kasper, T.M. Filzen, K.L. Collins, HIV-1 Nef disrupts MHC-1 trafficking by recruiting AP-1 to the MHC-1 cytoplasmic tail, J. Cell Biol. 167 (2004) 903-913.
45. M. Stevenson, HIV-1 pathogenesis, Nat. Med. 9 (2003) 853-860.
46. M. Williams, J.F. Roeth, M.R. Kasper, R.I. Fleis, C.G. Przybycin, K.L. Collins, 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. 76 (2002) 12173-12184.
47. S. Benichou, M. Bomsel, M. Bodeus, H. Durand, M. Doute, F. Letourneur, J. Camonis, R. Benarous, Physical interaction of the HIV-1 Nef protein with beta-cop, a component of non-clathrin-coated vesicles essential for membrane traffic, J. Biol. Chem. 269 (1994) 30073-30076.
48. K. Saksela, P. Permi, SH3 domain ligand binding:what's the consensus and where's the specificity? FEBS Lett. 586 (2012) 2609-2614.
49. C. Lee, B. Leung, M. Lemmon, J. Zheng, D. Cowburn, J. Kuriyan, K. Saksela, 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 (1995) 5006-5015.
50. S. Arold, P. Franken, M.P. Strub, F. Hoh, S. Benichou, R. Benarous, C. Dumas, 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 (1997) 1361-1372.
51. C.H. Lee, K. Saksela, U.A. Mirza, B.T. Chait, J. Kuriyan, Crystal structure of the conserved core of HIV-1 Nef complexed with a Src family SH3 domain, Cell 85 (1996) 931-942.
52. R.P. Trible, L. Emert-Sedlak, T.E. Wales, V. Ayyavoo, J.R. Engen, T.E. Smithgall, Allosteric loss-of-function mutations in HIV-1 Nef from a long-term non-progressor, J. Mol. Biol. 374 (2007) 121-129.
53. H.J. Choi, T.E. Smithgall, Conserved residues in the HIV-1 Nef hydrophobic pocket are essential for recruitment and activation of the Hck tyrosine kinase, J. Mol. Biol. 343 (2004) 1255-1268.
54. P.S. Narute, T.E. Smithgall, Nef alleles from all major HIV-1 clades activate Srcfamily kinases and enhance HIV-1 replication in an inhibitor-sensitive manner, PLoS ONE 7 (2012) e32561.
55. M. Foti, L. Cartier, V. Piguet, D.P. Lew, J.L. Carpentier, D. Trono, K.H. Krause, The HIV Nef protein alters Ca2+ signaling in myelomonocytic cells through SH3-mediated protein-protein interactions, J. Biol. Chem. 274 (1999) 34765-34772.
56. N. Chutiwitoonchai, M. Hiyoshi, P. Mwimanzi, T. Ueno, A. Adachi, H. Ode, H. Sato, O.T. Fackler, S. Okada, S. Suzu, The identification of a small molecule compound that reduces HIV-1 Nef-mediated viral infectivity enhancement, PLoS ONE 6 (2011) e27696.
57. R.P. Trible, P. Narute, L.A. Emert-Sedlak, J.J. Alvarado, K. Atkins, L. Thomas, T. Kodama, N. Yanamala, V. Korotchenko, B.W. Day, G. Thomas, T.E. Smithgall, Discovery of a diaminoquinoxaline benzenesulfonamide antagonist of HIV-1 Nef function using a yeast-based phenotypic screen, Retrovirology 10 (2013) 135.
58. T.E. Biggs, S.J. Cooke, C.H. Barton, M.P.G. Harris, K. Saksela, D.A. Mann, Induction of activator protein 1 (AP-1) in macrophages by human immunodeficiency virus type-1 NEF is a cell-type-specific response that requires both Hck and MAPK signaling events, J. Mol. Biol. 290 (1999) 21-35.
59. A. Greenway, A. Azad, J. Mills, D. McPhee, Human immunodeficiency virus type 1 Nef binds directly to Lck and mitogen-activated protein kinase, inhibiting kinase activity, J. Virol. 70 (1996) 6701-6708.
60. K.C. Olivieri, J. Mukerji, D. Gabuzda, Nef-mediated enhancement of cellular activation and human immunodeficiency virus type 1 replication in primary T cells is dependent on association with p21-activated kinase 2, Retrovirology 8 (2011) 64.
61. X. Pan, J.M. Rudolph, L. Abraham, A. Habermann, C. Haller, J. Krijnse-Locker, O.T. Fackler, HIV-1 Nef compensates for disorganization of the immunological synapse by inducing trans-Golgi network-associated Lck signaling, Blood 119 (2012) 786-797.
62. T.E. Smithgall, G. Thomas, Small molecule inhibitors of the HIV-1 virulence factor, Nef, Drug Discov. Today Technol. 10 (2013) e523-e529.
63. S. Betzi, A. Restouin, S. Opi, S.T. Arold, I. Parrot, F. Guerlesquin, X. Morelli, Y. Collette, Protein-protein interaction inhibition (2P2I) combining high throughput and virtual screening: application to the HIV-1 Nef protein, Proc. Natl. Acad. Sci. U. S. A. 104 (2007).
64. L. Emert-Sedlak, T. Kodama, E.C. Lerner, W. Dai, C. Foster, B.W. Day, J.S. Lazo, T.E. Smithgall, Chemical library screens targeting an HIV-1 accessory factor/host cell kinase complex identify novel antiretroviral compounds, ACS Chem. Biol. 4 (2009) 939-947.
65. L.A. Emert-Sedlak, P. Narute, S.T. Shu, J.A. Poe, H. Shi, N. Yanamala, J.J. Alvarado, J.S. Lazo, J.I. Yeh, P.A. Johnston, T.E. Smithgall, Effector kinase coupling enables high-throughput screens for direct HIV-1 Nef antagonists with antiretroviral activity, Chem. Biol. 20 (2013) 82-91.
66. J. Bouchet, S.E. Basmaciogullari, P. Chrobak, B. Stolp, N. Bouchard, O.T. Fackler, P. Chames, P. Jolicoeur, S. Benichou, D. Baty, Inhibition of the Nef regulatory protein of HIV-1 by a single-domain antibody, Blood 117 (2011) 3559-3568.
67. A. Jarviluoma, T. Strandin, S. Luelf, J. Bouchet, A.R. Makela, M. Geyer, S. Benichou, K. Saksela, High-affinity target binding engineered via fusion of a single-domain antibody fragment with a ligand-tailored SH3 domain, PLoS ONE 7 (2012) e40331.
68. J. Bouchet, C. Herate, C.A. Guenzel, C. Verollet, A. Jarviluoma, J. Mazzolini, S. Rafie, P. Chames, D. Baty, K. Saksela, F. Niedergang, I. Maridonneau-Parini, S. Benichou, Single-domain antibody-SH3 fusions for efficient neutralization of HIV-1 Nef functions, J. Virol. 86 (2012) 4856-4867.
69. P.S. Pennings, HIV drug resistance: problems and perspectives, Infect. Dis. Rep. 5 (2013) e5.
70. S. Iijima, Y. Lee, H. Ode, S.T. Arold, N. Kimura, M. Yokoyama, H. Sato, Y. Tanaka, K. Strebel, H. Akari, A noncanonical mu-1A-binding motif in the N terminus of HIV-1 Nef determines its ability to downregulate major histocompatibility complex class I in T lymphocytes, J. Virol. 86 (2012) 3944-3951.
71. M. Williams, J.F. Roeth, M.R. Kasper, T.M. Filzen, K.L. Collins, 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. 79 (2005) 632-636.
72. L. Wan, S.S. Molloy, L. Thomas, G.P. Liu, Y. Xiang, S.L. Rybak, G. Thomas, PACS-1 defines a novel gene family of cytosolic sorting proteins required for trans-Golgi network localization, Cell 94 (1998) 205-216.
73. V. Piguet, L. Wan, C. Borel, A. Mangasarian, N. Demaurex, G. Thomas, D. Trono, HIV-1 Nef protein binds to the cellular protein PACS-1 to downregulate class I major histocompatibility complexes, Nat. Cell Biol. 2 (2000) 163-167.
74. C.M. Crump, Y. Xiang, L. Thomas, F. Gu, C. Austin, S.A. Tooze, G. Thomas, PACS-1 binding to adaptors is required for acidic cluster motif-mediated protein traffic, EMBO J. 20 (2001) 2191-2201.
75. G.K. Scott, F. Gu, C.M. Crump, L. Thomas, L. Wan, Y. Xiang, G. Thomas, The phosphorylation state of an autoregulatory domain controls PACS-1-directed protein traffic, EMBO J. 22 (2003) 6234-6244.
76. N. Kienzle, J. Freund, H.R. Kalbitzer, N. Muellerlantzsch, Oligomerization of the Nef protein from human-immunodeficiency-virus (HIV) type-1, Eur. J. Biochem. 214 (1993) 451-457.
77. L.X. Liu, N. Heveker, O.T. Fackler, S. Arold, S. Le Gall, K. Janvier, B.M. Peterlin, C. Dumas, O. Schwartz, S. Benichou, R. Benarous, Mutation of a conserved residue (D123) required for oligomerization of human immunode ficiency virus type 1 Nef protein abolishes interaction with human thioesterase and results in impairment of Nef biological functions, J. Virol. 74 (2000) 5310-5319.
78. J.A. Poe, T.E. Smithgall, HIV-1 Nef dimerization is required for Nef-mediated receptor downregulation and viral replication, J. Mol. Biol. 394 (2009) 329-342.
79. S. Arold, F. Hoh, S. Domergue, C. Birck, M.A. Delsuc, M. Jullien, C. Dumas, Characterization and molecular basis of the oligomeric structure of HIV-1 Nef protein, Protein Sci. 9 (2000) 1137-1148.
80. J.J. Alvarado, S. Tarafdar, J.I. Yeh, T.E. Smithgall, Interaction with the SH3-SH2 region of the Src-family kinase Hck structures the HIV-1 Nef dimer for kinase activation and effector recruitment, J. Biol. Chem. 289 (2014) 28539-28553.
81. H.H. Ye, H.J. Choi, J. Poe, T.E. Smithgall, Oligomerization is required for HIV-1 nef-induced activation of the Src family protein-tyrosine kinase, Hck, Biochemistry (N. Y.) 43 (2004) 15775-15784.
82. O.O. Yang, P.T. Nguyen, S.A. Kalams, T. Dorfman, H.G. Gottlinger, S. Stewart, I.S.Y. Chen, S. Threlkeld, B.D. Walker, Nef-mediated resistance of human immunodeficiency virus type 1 to antiviral cytotoxic T lymphocytes, J. Virol. 76 (2002) 1626-1631.
83. K.L. Collins, B.K. Chen, S.A. Kalams, B.D. Walker, D. Baltimore, HIV-1 Nef protein protects infected primary cells against killing by cytotoxic T lymphocytes, Nature 391 (1998) 397-401.
84. X.T. Kuang, X. Li, G. Anmole, P. Mwimanzi, A. Shahid, A.Q. Le, L. Chong, H. Qian, T. Miura, T. Markle, B. Baraki, E. Connick, E.S. Daar, H. Jessen, A.D. Kelleher, S. Little, M. Markowitz, F. Pereyra, E.S. Rosenberg, B.D. Walker, T. Ueno, Z.L. Brumme, M.A. Brockman, Impaired Nef function is associated with early control of HIV-1 viremia, J. Virol. 88 (2014) 10200-10213.
85. P. Gupta, M. Husain, C. Hans, H. Ram, S. Verma, M. Misbah, L. Chauhan, A. Rai, Sequence heterogeneity in human immunodeficiency virus type 1 nef in patients presenting with rapid progression and delayed progression to AIDS, Arch. Virol. 19 (Apr 2014).
86. E. Nou, Y. Zhou, D.D. Nou, J.N. Blankson, Effective downregulation of HLA-A∗2 and HLA-B∗57 by primary human immunodeficiency virus type 1 isolates cultured from elite suppressors, J. Virol. 83 (2009) 6941-6946.
87. A. Heigele, D. Camerini, A.B. van't Wout, F. Kirchhoff, Viremic long-term nonprogressive HIV-1 infection is not associated with abnormalities in known Nef functions, Retrovirology 11 (2014) 13.
88. N. Casartelli, G. Di Matteo, M. Potesta, P. Rossi, M. Doria, CD4 and major histocompatibility complex class I downregulation by the human immunodeficiency virus type 1 Nef protein in pediatric AIDS progression, J. Virol. 77 (2003) 11536-11545.
89. T. Swigut, A.J. Iafrate, J. Muench, F. Kirchhoff, J. Skowronski, Simian and human immunodeficiency virus Nef proteins use different surfaces to downregulate class I major histocompatibility complex antigen expression, J. Virol. 74 (2000) 5691-5701.
90. D.E. Kaufmann, P.M. Bailey, J. Sidney, B. Wagner, P.J. Norris, M.N. Johnston, L.A. Cosimi, M.M. Addo, M. Lichterfeld, M. Altfeld, N. Frahm, C. Brander, A. Sette, B.D. Walker, E.S. Rosenberg, Comprehensive analysis of human immunodeficiency virus type 1-specific CD4 responses reveals marked immunodominance of gag and nef and the presence of broadly recognized peptides, J. Virol. 78 (2004) 4463-4477.
91. E.W. Rud, M. Cranage, J. Yon, J. Quirk, L. Ogilvie, N. Cook, S. Webster, M. Dennis, B.E. Clarke, Molecular and biological characterization of Simian Immunodeficiency Virus Macaque Strain 32 h proviral clones containing Nef size variants, J. Gen. Virol. 75 (1994) 529-543.
92. J. Munch, N. Stolte, D. Fuchs, C. Stahl-Hennig, F. Kirchhoff, Efficient class Imajor histocompatibility complex down-regulation by simian immunodeficiency virus Nef is associated with a strong selective advantage in infected rhesus macaques, J. Virol. 75 (2001) 10532-10536.
93. T.C. Friedrich, S.M. Piaskowski, E.J. Leon, J.R. Furlott, N.J. Maness, K.L. Weisgrau, C.E. Mac Nair, A.M. Weiler, J.T. Loffredo, M.R. Reynolds, K.Y. Williams, Y.C. Klimentidis, N.A. Wilson, D.B. Allison, E.G. Rakasz, High viremia is associated with high levels of in vivo major histocompatibility complex class I downregulation in Rhesus Macaques infected with Simian Immunodeficiency Virus SIVmac239, J. Virol. 84 (2010) 5443-5447.
94. M. Schindler, J. Schmoekel, A. Specht, H. Li, J. Muench, M. Khalid, D.L. Sodora, B.H. Hahn, G. Silvestri, F. Kirchhoff, Inefficient Nef-mediated downmodulation of CD3 and MHC-I correlates with loss of CD4(+) T cells in natural SIV infection, PLoS Pathog. 4 (2008) e1000107.
95. T. Swigut, L. Alexander, J. Morgan, J. Lifson, K.G. Mansfield, S. Lang, R.P. Johnson, J. Skowronski, R. Desrosiers, Impact of Nef-mediated downregulation of major histocompatibility complex class I on immune response to simian immunodeficiency virus, J. Virol. 78 (2004) 13335-13344.
96. A. Ali, H.L. Ng, M.D. Dagarag, O.O. Yang, Evasion of cytotoxic T lymphocytes is a functional constraint maintaining HIV-1 Nef expression, Eur. J. Immunol. 35 (2005) 3221-3228.
97. Y. Kusunoki, S. Kyoizumi, M. Honma, Y. Kubo, H. Ohnishi, T. Hayashi, T. Seyama, NK-mediated elimination of mutant lymphocytes that have lost expression of MHC class I molecules, J. Immunol. 165 (2000) 3555-3563.
98. A. Specht, M.Q. DeGottardi, M. Schindler, B. Hahn, D.T. Evans, F. Kirchhoff, Selective downmodulation of HLA-A and -B by Nef alleles from different groups of primate lentiviruses, Virology 373 (2008) 229-237.
99. N. Pizzato, M. Derrien, F. Lenfant, The short cytoplasmic tail of HLA-G determines its resistance to HIV-1 Nef-mediated cell surface downregulation, Hum. Immunol. 65 (2004) 1389-1396.
100. G.B. Cohen, R.T. Gandhi, D.M. Davis, O. Mandelboim, B.K. Chen, J.L. Strominger, D. Baltimore, The selective downregulation of class I major histocompatibility complex proteins by HIV-1 protects HIV-infected cells from NK cells, Immunity 10 (1999) 661-671.
101. T.E. Dudek, T.M. Allen, HIV-specific CD8(+) T-cell immunity in humanized bone marrow-liver-thymus mice, J. Infect. Dis. 208 (2013) S150-S154.
102. J.K. Mann, H. Byakwaga, X.T. Kuang, A.Q. Le, C.J. Brumme, P. Mwimanzi, S. Omarjee, E. Martin, G.Q. Lee, B. Baraki, R. Danroth, R. McCloskey, C. Muzoora, D.R. Bangsberg, P.W. Hunt, P.J.R. Goulder, B.D. Walker, P.R. Harrigan, J.N. Martin, T. Ndung'u, M.A. Brockman, Z.L. Brumme, Ability of HIV-1 Nef to downregulate CD4 and HLA class I differs among viral subtypes, Retrovirology 10 (2013) 100.