The downregulation of CD4 and MHC-I by primate lentiviruses: A paradigm for the modulation of cell surface receptors

Immunological Reviews

Volumn 168, Issue , 1999, Pages 51-63

  Piguet, Vincent ^a   Schwartz, Olivier ^b   Le Gall, Sylvie ^b   Trono, Didier ^a,c  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b INSTITUT PASTEUR   (France)

^c Center Médical Universitaire   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CLATHRIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NEF PROTEIN; VIRUS ENVELOPE PROTEIN; VIRUS PROTEIN; VPU PROTEIN;

ANTIGEN RECOGNITION; ARTICLE; COATED PIT; DOWN REGULATION; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; HUMAN IMMUNODEFICIENCY VIRUS 1; INTRACELLULAR TRANSPORT; LENTIVIRINAE; NONHUMAN; PRIMATE; PRIORITY JOURNAL; VIRUS INFECTIVITY;

ADAPTOR PROTEIN COMPLEX ALPHA SUBUNITS; ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; ANTIGENS, CD4; DOWN-REGULATION; GENE PRODUCTS, NEF; GENE PRODUCTS, VPU; HISTOCOMPATIBILITY ANTIGENS CLASS I; HIV-1; HUMANS; INTRACELLULAR FLUID; LENTIVIRUS; LYSOSOMES; MEMBRANE PROTEINS; PRIMATES; RECEPTORS, VIRUS; VIRAL ENVELOPE PROTEINS;

EID: 0032999976     PISSN: 01052896     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-065X.1999.tb01282.x     Document Type: Article

References (112)

1. 1. Maddon PJ, Littman DR, Godfrey M, Maddon DE, Chess L, Axel R. The isolation and nucleotide sequence of a cDNA encosing the T-cell surface protein T4: a new member of the immunoglobulin gene family. Cell 1985;42:93-104.
2. 2. Maddon P, Dalgliesh A, McDougal J, Clapham P, Weiss R, Axel R. The T4 gene encodes the AIDS virus receptor and is expressed in the immune system and the brain. Cell 1986;47;333-348.
3. 3. Wu H, Kwong PD, Hendrickson WA. Dimeric association and segmental variability in the structure of human CD4. Nature 1997;387:527-530.
4. 4. Li S, Satoh T, Korngold R, Huang Z. CD4 dimerization and oligomerization; implications for T-cell function and structure-based drug design. Immunol Today 1998;19:455-462.
5. 5. Dalgleish AG, Beverley PC, Clapham PR, Crawford DH, Greaves MF, Weiss RA. The CD4 (T4) antigen is an essential component of the receptor for the AIDS retrovirus. Nature 1984;312:763-767.
6. 6. Klatzman DE, et al. The CD4 (T4) is an essential component of the receptor for the AIDS retrovirus. Nature 1984;312:767-768.
7. 7. Littman DR. Chemokine receptors: keys to AIDS pathogenesis? Cell 1998;93:677-680.
8. 8. Weiss A, Littman D. Signal transduction by lymphocyte antigen receptors. Cell 1994;76:263-274.
9. 9. Doyle C, Strominger JL. Interaction between CD4 and class II MHC molecules mediates cell adhesion. Nature 1987;330:256-259.
10. 10. Veillette A, Bookman MA, Horak EM, Bolen JB. The CD4 and CD8 T cell surface antigens are associated with the internal membrane tyrosine-protein kinase p56lck. Cell 1988;55:301-308.
11. 11. Shaw A, Amrein K, Hammond C, Stern D, Sefton B, Rose J. The Lck tyrosine protein kinase interacts with the cytoplasmic tail of the CD4 glycoprotein through its unique amino terminal domain. Cell 1989;59:627-636.
12. 12. Turner J, Brodsky MH, Irving BA, Levin SD, Perlmutter RM, Littman DR. Interaction of the unique N-terminal region of tyrosine kinase p56lck with cytoplasmic domains of CD4 and CD8 is mediated by cysteine motifs. Cell 1990;60:755-765.
13. 13. Acres RB, Conlon PJ, Mochizuki DY, Gallis B. Rapid phosphorylation and modulation of the T4 antigen on cloned helper T cells induced by phorbol myristate acetate or antigen. J Biol Chem 1986;261:16210-16214.
14. 14. Veillette A, Bookman MA, Horak EM, Samelson LE, Bolen JB. Signal transduction through the CD4 receptor involves the activation of the internal membrane tyrosine-protein kinase p56lck. Nature 1989;338:257-259.
15. 15. Janeway CA Jr, et al. The co-receptor function of murine CD4. Immunol Rev 1989;109:77-92.
16. 16. Foti M, Lew DP, Carpentier JL, Krause KH. CD4 in non-lymphocytic cells: more than a HIV receptor? J Lab Clin Med 1995;126:233-239.
17. 17. Pelchen-Matthews A, Armes J, Griffiths G, Marsh M. Differential endocytosis of CD4 in lymphocytic and non-lymphocytic cells. J Exp Med 1991;173:575-587.
18. 18. Pelchen-Matthews A, Armes J, Marsh M. Internalization and recycling of CD4 transfected into HeLa and NIH3T3 cells. J Exp Med 1989;8:3641-3649.
19. 19. Shin J, Dunbrack R Jr, Lee S, Strominger J. Phosphorylation-dependent down-modulation of CD4 requires a specific structure within the cytoplasmic domain of CD4. J Biol Chem 1991;266:10658-10665.
20. 20. Aiken C, Konner J, Landau NR, Lenburg ME, Trono D. Nef induces CD4 endocytosis: requirement for a critical dileucine motif in the membrane-proximal CD4 cytoplasmic domain. Cell 1994;76:853-864.
21. 21. Pelchen-Matthews A, Parsons I, Marsh M. Phorbol ester-induced downregulation of CD4 is a multistep process involving dissociation from p56lck, increased association with clathrin-coated pits and and altered endosomal sorting. J Exp Med 1993;178:1209-1222.
22. 22. Chen BK, Gandhi RT, Baltimore D. CD4 down-modulation during infection of human T cells with human immunodeficiency virus type 1 involves independent activities of Vpu, Env, and Nef. J Virol 1996;70:6044-6053.
23. 23. Schwartz O, Rivière Y, Heard JM, Danos O. Reduced cell surface expression of processed human immunodeficiency virus type 1 envelope glycoprotein in the presence of Nef. J Virol 1993;67:3274-3280.
24. 1 orf encodes a phosphorylated GTP-binding protein resembling an oncogene product. Nature 1987;330:266-269.
25. 25. Niederman TM, Hastings WR, Ratner L. Myristoylation-enhanced binding of the HIV-1 Nef protein to T cell skeletal matrix. Virology 1993;197:420-425.
26. 26. Garcia J, Miller A. Serine phosphorylation independent downregulation of cell surface CD4 by Nef. Nature 1991;350:508-511.
27. 27. Oldridge J, Marsh M. Nef-an adaptor adaptor? Trends Cell Biol 1998;8:302-305.
28. 28. Rhee SS, Marsh JW. Human immunodeficiency virus type 1 Nef-induced down-modulation of CD4 is due to rapid internalization and degradation of surface CD4. J Virol 1994;68:5156-5163.
29. 29. Mangasarian A, Foti M, Aiken C, Chin D, Carpentier JL, Trono D. The HIV-1 Nef protein acts as a connector with sorting pathways in the Golgi and at the plasma membrane. Immunity 1997;6:67-77.
30. 30. Schwartz O, et al. Human immunodeficiency virus type 1 Nef induces accumulation of CD4 in early endosomes. J Virol 1995;69:528-533.
31. 31. Piguet V, Chen Y-L, Mangasarian A, Foti M, Carpentier J, Trono D. Mechanism of Nef induced CD4 endocytosis: Nef connects CD4 with the μ chain of adaptor complexes. EMBO J 1998;17:2472-2481.
32. 32. Foti M, et al. Nef-mediated clathrin coated pit formation. J Cell Biol 1997;139:37-47.
33. 33. Grzesiek S, et al. 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 1996;3:340-345.
34. 34. Hua J, Cullen B. 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 1997;71:6742-6748.
35. 35. Grzesiek S, Stahl SJ, Wingfield PT, Bax A. The CD4 determinant for downregulation by HIV-1 Nef directly binds to Nef Mapping of the Nef binding surface by NMR. Biochemistry 1996;35:10256-10261.
36. 36. Harris MP, Neil JC. Myristoylation-dependent binding of HIV-1 Nef to CD4. J Mol Biol 1994;241:136-142.
37. 37. Rossi F, Gallina A, Milanesi G. Nef-CD4 physical interaction sensed with the yeast two-hybrid system. Virology 1996;217:397-403.
38. 38. Greenway A, Azad A, McPhee D. Human immunodeficiency virus type 1 Nef protein inhibits activation pathways in peripheral blood mononuclear cells and T-cell lines. J Virol 1995;69:1842-1850.
39. 39. Salghetti S, Mariani R, Skowronski J. Human immunodeficiency virus type 1 Nef and p56lck protein-tyrosine kinase interact with a common element in CD4 cytoplasmic tail. Proc Natl Acad Sci USA 1995;92:349-353.
40. 40. Baur AS, Sass G, Laffert B, Willbold D, Cheng MC, Peterlin BM. The N-terminus of Nef from HIV-1/SIV associates with a protein complex containing Lck and a serine kinase. Immunity 1997;6:283-291.
41. 41. Collette Y, et al. Physical and functional interaction of Nef with Lck. HIV-1 Nef-induced T-cell signaling defects. J Biol Chem 1996;271:6333-6341.
42. 41. Greenway A, Azad A, Mills J, McPhee D. Human immunodeficiency virus type 1 Nef binds directly to Lck and mitogen-activated protein kinase, inhibiting kinase activity. J Virol 1996;70:6701-6708.
43. + viruses but not for down-regulation of CD4. EMBO J 1995;14:484-491.
44. 44. Mangasarian A, Piguet V, Wang JK, Chen Y, Trono D. Nef-induced CD4 and MHC-I downregulation are governed by distinct determinants: N-terminal α-helix and proline repeat of Nef selectively regulate MHC-I trafficking. J Virol 1999;73:1964-1973.
45. 45. Le Gall S, et al. Nef interacts with the μ subunit of clathrin adaptor complexes and reveals a cryptic sorting signal in MHC-I molecules. Immunity 1998;8:483-495.
46. 46. Bresnahan PA, Yonemoto W, Ferrell S, Williams Herman D, Geleziunas R, Greene WC. 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;8:1235-1238.
47. 47. Greenberg M, DeTulleo L, Rapoport I, Skowronski J, Kichhausen T. A dileucine motif in HIV-1 Nef is essential for sorting into clathrin-coated pits and for downregulation of CD4. Curr Biol 1998;8:1239-1242.
48. 48. Robinson MS. The role of clathrin, adaptors and dynamin in endocytosis. Curr Opin Cell Biol 1994;6:538-544.
49. 49. Cowles C, Odorizzi G, Payne G, Emr S. The AP-3 adaptor complex is essential for cargo-selective transport to the yeast vacuole. Cell 1997;91:109-118.
50. 50. Simpson F, Bright NA, West MA, Newman LS, Darnell RB, Robinson MS. A novel adaptor-related protein complex. J Cell Biol 1996;133:749-760.
51. 51. Dell'Angelica E, Ohno H, Ooi C, Rabinovich E, Roche K, Bonifacino J. AP-3: an adaptor-like protein complex with ubiquitous expression. EMBO J 1997;16:917-928.
52. 52. Trowbridge IS, Collawn JF, Hopkins CR. Signal-dependent membrane protein trafficking in the endocytic pathway. Annu Rev Cell Biol 1993;9:129-161.
53. 53. Letourneur F, Klausner R. A novel di-leucine motif and a tyrosine based motif independently mediate lysosomal targeting and endocytosis of CD3 chains. Cell 1992;69:1143-1157.
54. 54. Kirchhausen T, Bonifacino JS, Riezman H. Linking cargo to vesicle formation: receptor tail interactions with coat proteins. Curr Opin Cell Biol 1997;9:488-495.
55. 55. Ohno H, et al. Interaction of tyrosine based sorting signals with clathrin associated proteins. Science 195;269:1872-1875.
56. 56. Owen DJ, Evans PR, A structural explanation for the recognition of tyrosine-based endocytic signals. Science 1998;282:1327-1332.
57. 57. Bremnes T, Lauvrak V, Lindqvist B, Bakke O. A region from the medium chain adaptor subunit (μ) recognizes leucine-and tyrosine-based sorting signals. J Biol Chem 1998;273:8638-8645.
58. 58. Rapoport I, Chen YC, Cupers P, Shoelson SE, Kirchhausen T. Dileucine-based sorting signals bind to the β chain of AP-1 at a site distinct and regulated differently from the tyrosine-based motif-binding site. EMBO J 1998;17:2148-2155.
59. 59. Craig HM, Pandori MW, Guatelli JC. 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;95:11229-11234.
60. 60. Lu X, Yu H, Liu S, Brodsky FM, Peterlin BM. Interactions between HIV 1 Nef and vacuolar ATPase facilitate the internalization of CD4. Immunity 1998;8:647-656.
61. 61. Liu LX, et al. Binding of HIV-1 Nef to a novel thioesterase enzyme correlates with Nef-mediated CD4 down-regulation. J Biol Chem 1997;272:13779-13785.
62. 62. Luo T, Anderson SJ, Garcia JV. Inhibition of Nef-and phorbol ester-induced CD4 degradation by macrolide antibiotics. J Virol 1996;70:1527-1534.
63. 63. Piguet V, et al. Nef-induced D4 degradation: a diacidic-based motif in Nef functions as a lysosomal targeting signal through the binding of β-COP in endosomes. Cell 1999;9763-73.
64. 64. Benichou S, et al. Physical interaction of the HIV-1 Nef protein with β-COP, a component of non-clathrin-coated vesicles essential for membrane traffic. J Biol Chem 1994;269:30073-30076.
65. 65. Aniento F, Gu F, Parton RG, Gruenberg J. An endosomal β-COP is involved in the pH-dependent formation of transport vesicles destined for late endosomes. J Cell Biol 1996;133:29-41.
66. 66. Whitney JA, Gomez M, Sheff D, Kreis TE, Mellman I. Cytoplasmic coat proteins involved in endosome function. Cell 1995;83:703-713.
67. 67. Gu F, Aniento F, Parton RG, Gruenberg J. Functional dissection of COP I subunits in the biogenesis of multivesicular endosomes. J Cell Biol 1997;139:1183-1195.
68. 68. Daro E, Sheff D, Gomez M, Kreis T, McIlman J. Inhibition of endosome function in CHO cells bearing a temperature-sensitive defect in the coatomer (COPI) component ε-COP. J Cell Biol 1997;139:1747-1759.
69. 69. Schwartz S, Felber BK, Fenyo EM, Pavlakis GN. Env and Vpu are produced from multiple bicistronic mRNAs. J Virol 1990;64:5585-5593.
70. 70. Luciw P. Human immunodeficiency viruses and their replication. In: Fields B, Knipe D, Howley P, eds. Fields virology. Vol 2. Philadelphia: Lippincott-Raven; 1996. p. 1881-1952.
71. 71. Chan DC, Kim PS. HIV entry and its inhibition. Cell 1998;93:681-684.
72. 72. Crise BL, Buonocore L, Rose JK. CD4 is retained in the endoplasmic reticulum by the human immunodeficiency virus type 1 glyocoprotein precursor. J Virol 1990;64:5585-5593.
73. 73. Cohen EA, Terwilliger EF, Sodroski JG, Haseltine WA. Identification of a protein encoded by the vpu gene of HIV-1. Nature 1988;334;532-534.
74. 74. Strebel K, Klimkait K, Martin MA. A novel gene of HIV-1, vpu, and its 16-kilodalton product. Science 1988;241:1221-1223.
75. 75. Schubert U, Ferrer-Montiel AV, Oblatt-Montal M, Henklein P, Strebel K, Montal M. Identification of an ion channel activity of the Vpu transmembrane domain and its involvement in the regulation of virus release from HIV-1-infected cells. FEBS Lett 1996;398:12-18.
76. 76. Willey RL, Maldarelli F, Martin MA, Strebel K. Human immunodeficiency virus type 1 Vpu protein induces rapid degradation of CD4. J Virol 1992;66:7193-7200.
77. 77. Schubert U, Strebel K. Differential activities of the human immunodeficiency virus type 1 encoded Vpu protein are regulated by phosphorylation and occur in different cellular compartments. J Virol 1994;68:2260-2271.
78. 78. Schubert U, et al. CD4 glycoprotein degradation induced by human immunodeficiency virus type 1 Vpu protein requires the function of proteasomes and the ubiquitin-conjugating pathway. J Virol 1998;72:2280-2288.
79. 79. Bour S, Schubert U, Strebel K. The human immunodeficiency virus type 1 Vpu protein specifically binds to the cytoplasmic domain of CD4: implications for the mechanism of degradation. J Virol 1995;69:1510-1520.
80. 80. Margottin F, et al. Interaction between the cytoplasmic domains of HIV-1 Vpu and CD4: role of Vpu residues involved in CD4 interaction and in vitro CD4 degradation. Virology 1996;223:381-386.
81. 81. Marottin F, et al. A noel human WD protein, h-βTrCp, that interacts with HIV-1 Vpu connects CD4 to the ER degradation pathway through an F-box motif. Mol Cell 19981;565-574.
82. 82. Fujita K, Omura S, Silver J. Rapid degradation of CD4 in cells expressing human immunodeficiency virus type 1 Env and Vpu is blocked by proteasome inhibitors. J Gen Virol 1997;78:619-625.
83. + cell line, CEM-E5 after HIV-1 infection. J Immunol 1989;143:2858.
84. 84. Kerkan T, Schmitt-Landgraf R, Schimpl A, Wecker E. Downregulation of HLA class I antigens in HIV-1 infected cells. AIDS Res Hum Retroviruses 1989;5:613-620.
85. 85. Ploegh HL. Viral strategies of immune evasion. Science 1998;280:248-253.
86. 86. Bijlmakers MJ, Ploegh HL, Putting together an MHC class I molecule. Curr Opin Immunol 1993;5:21-26.
87. 87. Neefjes JJ, Stollorz V, Peters PJ, Geuze HJ, Ploegh HL. The biosynthetic pathway of MHC class II but not class I molecules intersects the endocytic route. Cell 1990;61:171-183.
88. 88. Reid PA, Watts C. Cycling of cell-surface MHC glycoproteins through primaquine-sensitive intracellular compartments. Nature 1990;346:655-657.
89. 89. Vega MA, Strominger JL. Constitutive endocytosis of HLA class I antigens requires a specific portion of the intracytoplasmic tail that shares structural features with other endocytosed molecules. Proc Natl Acad Sci USA 1989;86:2688-2692.
90. 90. Schwartz O, Maréchal V, Le Gall S, Lemonnier F, Heard JM. Endocytosis of major histocompatibility complex class I molecules is induced by the HIV-1 Nef protein. Nat Med 1996;2:338-342.
91. 91. Parham P, Adams EJ, Arnett KL. The origins of HLA-A,B,C polymorphism. Immunol Rev 1995;143:141-180.
92. 92. Sandoval IV, et al. The residues Leu(Ile)475-Ile(Leu, Val, Ala)476, contained in the extended carboxyl cytoplasmic tail, are critical for targeting of the resident lysosomal membrane protein LIMP II to lysosomes. J Biol Chem 1994;269:6622-6631.
93. 93. Marks MS, Woodruff L, Ohno H, Bonifacino JS. Protein targeting by tyrosine-and di-leucine-based signals: evidence for distinct saturable components. J Cell Biol 1996;135:341-354.
94. 94. Brutkiewicz RR, Welsh RM. Major histocompatibility complex class I antigens and the control of viral infections by natural killer cells. J Virol 1995;69:3967-3971.
95. 95. Kerkau T, et al. The human immunodeficiency virus type 1 (HIV-1) Vpu protein interferes with an early step in the biosynthesis of major histocompatability complex (MHC) class I molecules. J Exp Med 1997;185:1295-1305.
96. 96. Collins KL, Chen BK, Kalams SA, Walker BD, Baltimore D. HIV-1 Nef protein protects infected primary cells against killing by cytotoxic T lymphocytes. Nature 1998;391:397-401.
97. 97. Hengel H, Brune W, Koszinowski UH. Immune evasion by cytomegalovirus survival strategies of a highly adapted opportunist. Trends Microbiol 1998;6:190-197.
98. 98. Moss PA, et al. Persistent high frequency of human immunodeficiency virus-specific cytotoxic T cells in peripheral blood of infected donors. Proc Natl Acad Sci USA 1995;92:5773-5777.
99. 1 T cells. Science 1998;280:227.
100. 100. McMichael A. T cell responses and viral escape. Cell 1998;93:673-676.
101. 101. Colonna M, Borsellino G, Falco M, Ferrara GB, Strominger JL. HLA-C is the inhibitory ligand that determines dominant resistance to lysis by NK1-and NK2-specific natural killer cells. Proc Natl Acad Sci USA 1993;90:12000-12004.
102. + T-cell responses associated with control of viremia. Science 1997;27:1447-1450.
103. 103. Ho D, Neumann A, Perelson A, Chen W, Leonard J, Markowitz M. Rapid turnover of plasma virions and CD4 lymphocytes in HIV-1 infection. Nature 1995;373:123-126.
104. 104. Perelson A, Neumann A, Markowitz M, Leonard J, Ho D. HIV-1 dynamics in vivo: virion clearance rate, infected cell life span, and viral generation time. Science 1996;271:1582-1586.
105. 105. Wei X, et al. Viral dynamics in human immunodeficiency virus type 1 infection. Nature 1995;373:117-122.
106. 106. Finzi D, et al. Identification of a reservoir for HIV-1 in patients on highly active antiretroviral therapy. Science 1998;278:1295-1300.
107. 107. Wong J, et al. Recovery of replication-competent HIV despite prolonged suppression of plasma viremia. Science 1998;278:1291-1295.
108. 108. Pomerantz R, Trono D, Feinberg M, Baltimore D. Cells nonproductively infected with HIV-1 exhibit an aberrant pattern of viral RNA expression: a molecular model for latency. Cell 1990;61:1271-1276.
109. 109. Ferguson SS, Downey WE3, Colapietro AM, Barak LS, Menard L, Caron MG. Role of β-arrestin in mediating agonist-promoted G protein-coupled receptor internalization. Science 1996;271:363-366.
110. 110. Goodman O, Keen J. The a-chain of the AP-2 adaptor is a clathrin binding subunit. J Biol Chem 1995;270:23768-23773.
111. 111. Okabayashi Y, et al. Interaction of She with adaptor protein adaptins. J Biol Chem 1996;271:5265-5269.
112. 112. Van Delft S, Schumacher C, Hage W, Verkleij AJ, van Bergen en Henegouwen PM. Association and colocalization of Eps15 with adaptor protein-2 and clathrin. J Cell Biol 1997;136:811-821.