HIV-1 Nef targets MHC-I and CD4 for degradation via a final common β-cop-dependent pathway in T cells

PLoS Pathogens

Volumn 4, Issue 8, 2008, Pages

  Schaefer, Malinda R ^a   Wonderlich, Elizabeth R ^a   Roeth, Jeremiah F ^a   Leonard, Jolie A ^a   Collins, Kathleen L ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; BETA COP PROTEIN; BINDING PROTEIN; CD4 ANTIGEN; CLATHRIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NEF PROTEIN; RAB7 PROTEIN; UNCLASSIFIED DRUG; COATOMER PROTEIN; HLA ANTIGEN CLASS 1; NEF PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; RAB PROTEIN; VESICULAR TRANSPORT ADAPTOR PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CELL SURFACE; CELL TRANSPORT; CONFORMATION; CONTROLLED STUDY; CYTOPLASM; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; INTERNALIZATION; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN TARGETING; T LYMPHOCYTE; ANIMAL; BIOLOGICAL MODEL; CELL LINE; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; METABOLISM; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT;

HUMAN IMMUNODEFICIENCY VIRUS 1;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; AMINO ACID MOTIFS; ANIMALS; ANTIGENS, CD4; CELL LINE; COATOMER PROTEIN; HISTOCOMPATIBILITY ANTIGENS CLASS I; HIV INFECTIONS; HIV-1; HUMANS; MODELS, BIOLOGICAL; NEF GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS;

EID: 50849129910     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000131     Document Type: Article

References (75)

1. Garcia JV, Miller AD (1991) Serine phosphorylation-independent downregulation of cell-surface CD4 by nef. Nature 350: 508-511.
2. Schwartz O, Marechal V, Le Gall S, Lemonnier F, Heard J (1996) Endocytosis of major histocompatibility complex class I molecules is induced by the HIV-1 Nef protein. Nature Medicine 2: 338-342.
3. Sol-Foulon N, Moris A, Nobile C, Boccaccio C, Engering A, et al. (2002) HIV-1 Nef-induced upregulation of DC-SIGN in dendritic cells promotes lymphocyte clustering and viral spread. Immunity 16: 145-155.
4. Stumptner-Cuvelette P, Morchoisne S, Dugast M, Le Gall S, Raposo G, et al. (2001) HIV-1 Nef impairs MHC class II antigen presentation and surface expression. Proc Natl Acad Sci U S A 98: 12144-12149.
5. Swigut T, Shohdy N, Skowronski J (2001) Mechanism for down-regulation of CD28 by Nef. EMBO J 20: 1593-1604.
6. Collins K, Chen B, Kalams S, Walker B, Baltimore D (1998) HIV-1 Nef protein protects infected primary human cells from killing by cytotoxic T lymphocytes. Nature 391: 397-401.
7. Carl S, Daniels R, Iafrate AJ, Easterbrook P, Greenough TC, et al. (2000) Partial "repair" of defective NEF genes in a long-term nonprogressor with human immunodeficiency virus type 1 infection. J Infect Dis 181: 132-140.
8. Casartelli N, Di Matteo G, Potesta M, Rossi P, Doria M (2003) CD4 and major histocompatibility complex class I downregulation by the human immunodeficiency virus type 1 nef protein in pediatric AIDS progression. J Virol 77: 11536-11545.
9. Munch J, Stolte N, Fuchs D, Stahl-Hennig C, Kirchhoff F (2001) 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 75: 10532-10536.
10. Swigut T, Alexander L, Morgan J, Lifson J, Mansfield KG, et al. (2004) Impact of Nef-mediated downregulation of major histocompatibility complex class I on immune response to simian immunodeficiency virus. J Virol 78: 13335-13344.
11. Benson RE, Sanfridson A, Ottinger JS, Doyle C, Cullen BR (1993) Downregulation of cell-surface CD4 expression by simian immunodeficiency virus Nef prevents viral super infection. J Exp Med 177: 1561-1566.
12. Lama J, Mangasarian A, Trono D (1999) Cell-surface expression of CD4 reduces HIV-1 infectivity by blocking Env incorporation in a Nef- and Vpu-inhibitable manner. Curr Biol 9: 622-631.
13. Ross TM, Oran AE, Cullen BR (1999) Inhibition of HIV-1 progeny virion release by cell-surface CD4 is relieved by expression of the viral Nef protein. Curr Biol 9: 613-621.
14. Greenberg M, Iafrate A, Skowronski J (1998) The SH3 domain-binding surface and an acidic motif in HIV-1 Nef regulate trafficking of class I MHC complexes. EMBO J 17: 2777-2789.
15. Mangasarian A, Piguet V, Wang JK, Chen YL, Trono D (1999) 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: 1964-1973.
16. Bresnahan PA, Yonemoto W, Ferrell S, Williams-Herman D, Geleziunas R, et al. (1998) 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: 1235-1238.
17. Craig H, Pandori M, Guatelli J (1998) 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: 11229-11234.
18. Piguet V, Gu F, Foti M, Demaurex N, Gruenberg J, et al. (1999) 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 97: 63-73.
19. Aiken C, Konner J, Landau N, Lenburg M, Trono D (1994) Nef induces CD4 endocytosis: requirement for a critical dileucine motif in the membrane-proximal CD4 cytoplasmic domain. 76: 853-864.
20. Peng B, Robert-Guroff M (2001) Deletion of N-terminal myristoylation site of HIV Nef abrogates both MHC-1 and CD4 down-regulation. Immunol Lett 78: 195-200.
21. Liu LX, Heveker N, Fackler OT, Arold S, Le Gall S, et al. (2000) 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 74: 5310-5319.
22. Kasper MR, Collins KL (2003) Nef-mediated disruption of HLA-A2 transport to the cell surface in T cells. J Virol 77: 3041-3049.
23. Kasper MR, Roeth JF, Williams M, Filzen TM, Fleis RI, et al. (2005) HIV-1 Nef disrupts antigen presentation early in the secretory pathway. J Biol Chem 280: 12840-12848.
24. Williams M, Roeth JF, Kasper MR, Fleis RI, Przybycin CG, et al. (2002) 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: 12173-12184.
25. Roeth JF, Kasper MR, Williams M, Filzen TM, Collins KL (2004) HIV-1 Nef disrupts MHC-I trafficking by recruiting AP-1 to the MHC-I cytoplasmic tail. J Cell Biol 167: 903-913.
26. Williams M, Roeth JF, Kasper MR, Filzen T, Collins KL (2005) 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: 632-636.
27. Wonderlich ER, Williams M, Collins KL (2008) 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 283: 3011-3022.
28. Noviello CM, Benichou S, Guatelli JC (2008) 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: 1249-1258.
29. Piguet V, Chen YL, Mangasarian A, Foti M, Carpentier JL, et al. (1998) Mechanism of Nef-induced CD4 endocytosis: Nef connects CD4 with the mu chain of adaptor complexes. EMBO J 17: 2472-2481.
30. Le Gall S, Erdtmann L, Benichou S, Berlloz-Torrent C, Liu L, et al. (1998) Nef interacts with mu subunit of clathrin adaptor complexes and reveals a cryptic sorting signal in MHC I molecules. Immunity 8: 483-495.
31. Greenberg M, DeTulleo L, Rapoport I, Skowronski J, Kirchhausen T (1998) A dileucine motif in HIV-1 Nef is essential for sorting into clathrin-coated pits and for downregulation of CD4. Curr Biol 8: 1239-1242.
32. Craig HM, Reddy TR, Riggs NL, Dao PP, Guatelli JC (2000) 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 271: 9-17.
33. Janvier K, Kato Y, Boehm M, Rose JR, Martina JA, et al. (2003) 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 163: 1281-1290.
34. Janvier K, Craig H, Hitchin D, Madrid R, Sol-Foulon N, et al. (2003) HIV-1 Nef stabilizes the association of adaptor protein complexes with membranes. J Biol Chem 278: 8725-8732.
35. Erdtmann L, Janvier K, Raposo G, Craig HM, Benaroch P, et al. (2000) 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 1: 871-883.
36. Akagawa KS, Takasuka N, Nozaki Y, Komuro I, Azuma M, et al. (1996) Generation of CD1+RelB+ dendritic cells and tartrate-resistant acid phosphatase-positive osteoclast-like multinucleated giant cells from human monocytes. Blood 88: 4029-4039.
37. Lindwasser OW, Smith WJ, Chaudhuri R, Yang P, Hurley JH, et al. (2008) A diacidic motif in human immunodeficiency virus type 1 Nef is a novel determinant of binding to AP-2. J Virol 82: 1166-1174.
38. Lu X, Yu H, Liu S, Brodsky F, Peterlin B (1998) Interactions between HIV1 Nef and vacuolar ATPase facilitate the internalization of CD4. Immunity 8: 647-656.
39. Geyer M, Yu H, Mandic R, Linnemann T, Zheng YH, et al. (2002) Subunit H of the V-ATPase binds to the medium chain of adaptor protein complex 2 and connects Nef to the endocytic machinery. J Biol Chem 277: 28521-28529.
40. Chaudhuri R, Lindwasser OW, Smith WJ, Hurley JH, Bonifacino JS (2007) 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: 3877-3890.
41. Jin YJ, Cai CY, Zhang X, Zhang HT, Hirst JA, et al. (2005) HIV Nef-mediated CD4 down-regulation is adaptor protein complex 2 dependent. J Immunol 175: 3157-3164.
42. Stove V, Van de Walle I, Naessens E, Coene E, Stove C, et al. (2005) Human immunodeficiency virus Nef induces rapid internalization of the T-cell coreceptor CD8alphabeta. J Virol 79: 11422-11433.
43. Daro E, Sheff D, Gomez M, Kreis T, Mellman I (1997) Inhibition of endosome function in CHO cells bearing a temperature-sensitive defect in the coatomer (COPI) component epsilon-COP. J Cell Biol 139: 1747-1759.
44. Aniento F, Gu F, Parton RG, Gruenberg J (1996) An endosomal beta COP is involved in the pH-dependent formation of transport vesicles destined for late endosomes. J Cell Biol 133: 29-41.
45. Gu F, Aniento F, Parton RG, Gruenberg J (1997) Functional dissection of COPI subunits in the biogenesis of multivesicular endosomes. J Cell Biol 139: 1183-1195.
46. Benichou S, Bomsel M, Bodeus M, Durand H, doute M, et al. (1994) 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 269: 30073-30076.
47. Faure J, Stalder R, Borel C, Sobo K, Piguet V, et al. (2004) ARF1 regulates Nef-induced CD4 degradation. Curr Biol 14: 1056-1064.
48. Janvier K, Craig H, Le Gall S, Benarous R, Guatelli J, et al. (2001) 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 75: 3971-3976.
49. Swann SA, Williams M, Story CM, Bobbitt KR, Fleis R, et al. (2001) HIV-1 Nef blocks transport of MHC class I molecules to the cell surface via a PI 3-kinase-dependent pathway. Virology 282: 267-277.
50. Qin XF, An DS, Chen IS, Baltimore D (2003) Inhibiting HIV-1 infection in human T cells by lentiviral-mediated delivery of small interfering RNA against CCR5. Proc Natl Acad Sci U S A 100: 183-188.
51. Linstedt AD, Hauri HP (1993) Giantin, a novel conserved Golgi membrane protein containing a cytoplasmic domain of at least 350 kDa. Mol Biol Cell 4: 679-693.
52. Folsch H, Pypaert M, Schu P, Mellman I (2001) Distribution and function of AP-1 clathrin adaptor complexes in polarized epithelial cells. J Cell Biol 152: 595-606.
53. Tomiyama H, Akari H, Adachi A, Takiguchi M (2002) 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 76: 7535-7543.
54. Piguet V, Wan L, Borel C, Mangasarian A, Demaurex N, et al. (2000) HIV-1 Nef protein binds to the cellular protein PACS-1 to downregulate class I major histocompatibility complexes. Nat Cell Biol 2: 163-167.
55. Vivithanaporn P, Yan S, Swanson GT (2006) Intracellular trafficking of KA2 kainate receptors mediated by interactions with coatomer protein complex I (COPI) and 14-3-3 chaperone systems. J Biol Chem 281: 15475-15484.
56. Roeth JF, Collins KL (2006) Human immunodeficiency virus type 1 Nef: adapting to intracellular trafficking pathways. Microbiol Mol Biol Rev 70: 548-563.
57. Donaldson JG, Lippincott-Schwartz J, Bloom GS, Kreis TE, Klausner RD (1990) Dissociation of a 110-kD peripheral membrane protein from the Golgi apparatus is an early event in brefeldin A action. J Cell Biol 111: 2295-2306.
58. Lippincott-Schwartz J, Donaldson JG, Schweizer A, Berger EG, Hauri HP, et al. (1990) Microtubule-dependent retrograde transport of proteins into the ER in the presence of brefeldin A suggests an ER recycling pathway. Cell 60: 821-836.
59. Graham TR, Scott PA, Emr SD (1993) Brefeldin A reversibly blocks early but not late protein transport steps in the yeast secretory pathway. EMBO J 12: 869-877.
60. Donaldson JG, Finazzi D, Klausner RD (1992) Brefeldin A inhibits Golgi membrane-catalysed exchange of guanine nucleotide onto ARF protein. Nature 360: 350-352.
61. Helms JB, Rothman JE (1992) Inhibition by brefeldin A of a Golgi membrane enzyme that catalyses exchange of guanine nucleotide bound to ARF. Nature 360: 352-354.
62. Donaldson JG, Cassel D, Kahn RA, Klausner RD (1992) 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 U S A 89: 6408-6412.
63. Lubben NB, Sahlender DA, Motley AM, Lehner PJ, Benaroch P, et al. (2007) 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 18: 3351-3365.
64. Hung C, Thomas L, Ruby C, Atkins K, Morris N, et al. (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.
65. Willey RL, Maldarelli F, Martin MA, Strebel K (1992) Human immunodeficiency virus type 1 Vpu protein induces rapid degradation of CD4. J Virol 66: 7193-7200.
66. Henry RM, Hoppe AD, Joshi N, Swanson JA (2004) The uniformity of phagosome maturation in macrophages. J Cell Biol 164: 185-194.
67. Hawley R, Lieu F, Fong A, Hawley T (1994) Versatile retroviral vectors for potential use in gene therapy. Gene Ther 1: 136-138.
68. Van Parijs L, Refaeli Y, Lord JD, Nelson BH, Abbas AK, et al. (1999) Uncoupling IL-2 signals that regulate T cell proliferation, survival, and Fas-mediated activation-induced cell death. Immunity 11: 281-288.
69. Kamradt MC, Lu M, Werner ME, Kwan T, Chen F, et al. (2005) The small heat shock protein alpha B-crystallin is a novel inhibitor of TRAIL-induced apoptosis that suppresses the activation of caspase-3. J Biol Chem 280: 11059-11066.
70. Dull T, Zufferey R, Kelly M, Mandel RJ, Nguyen M, et al. (1998) A third-generation lentivirus vector with a conditional packaging system. J Virol 72: 8463-8471.
71. Hopkins N (1993) High titers of retrovirus (vesicular stomatitis virus) pseudotypes, at last. Proc Natl Acad Sci 90: 8759-8760.
72. Parham P, Brodsky FM (1981) Partial purification and some properties of BB7.2. A cytotoxic monoclonal antibody with specificity for HLA-A2 and a variant of HLA-A28. Hum Immunol 3: 277-299.
73. Chang AH, Hoxie JA, Cassol S, O'Shaughnessy M, Jirik F (1998) Construction of single-chain antibodies that bind an overlapping epitope of HIV-1 Nef. FEBS Lett 441: 307-312.
74. Allan VJ, Kreis TE (1986) A microtubule-binding protein associated with membranes of the Golgi apparatus. J Cell Biol 103: 2229-2239.
75. Traub LM, Kornfeld S, Ungewickell E (1995) Different domains of the AP-1 adaptor complex are required for Golgi membrane binding and clathrin recruitment. J Biol Chem 270: 4933-4942.