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

Journal of Virology

Volumn 73, Issue 3, 1999, Pages 1964-1973

  Mangasarian, Aram ^a   Piguet, Vincent ^a   Wang, Jen Kuei ^a   Chen, Yen Liang ^a   Trono, Didier ^a,b  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b CMU ^*  (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NEF PROTEIN; VIRUS PROTEIN;

ARTICLE; CONTROLLED STUDY; FLOW CYTOMETRY; HUMAN IMMUNODEFICIENCY VIRUS 1; LENTIVIRINAE; MAJOR HISTOCOMPATIBILITY COMPLEX; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TRANSPORT; VIRUS MUTATION;

EID: 0033013962     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.73.3.1964-1973.1999     Document Type: Article

References (78)

1. Aiken, C., J. Konner, N. R. Landau, M. E. Lenburg, and D. Trono. 1994. Nef induces CD4 endocytosis: requirement for a critical dileucine motif in the membrane-proximal CD4 cytoplasmic domain. Cell 76:853-864.
2. Aiken, C., L. Krause, Y. L. Chen, and D. Trono. 1996. Mutational analysis of HIV-1 Nef: identification of two mutants that are temperature-sensitive for CD4 downregulation. Virology 217:293-300.
3. Aiken, C., and D. Trono. 1995. Nef stimulates human immunodeficiency virus type 1 proviral DNA synthesis. J. Virol. 69:5048-5056.
4. Ausubel, F., R. Brent, R. Kingston, D. Moore, J. Smith, J. Seidman, and K. Struhl. 1987. Current protocols in molecular biology. John Wiley & Sons, Inc., New York, N.Y.
5. Barnham, K. J., S. A. Monks, M. G. Hinds, A. A. Azad, and R. S. Norton. 1997. Solution structure of a polypeptide from the N terminus of the HIV protein Nef. Biochemistry 36:5970-5980.
6. Baur, A. S., G. Sass, B. Laffert, D. Willbold, M. C. Cheng, and B. M. Peterlin. 1997. The N-terminus of Nef from HIV-1/SIV associates with a protein complex containing Lck and a serine kinase. Immunity 6:283-291.
7. Baur, A. S., E. T. Sawai, P. Dazin, W. J. Fantl. M. C. Cheng, and B. M. Peterlin. 1994. HIV-1 Nef leads to inhibition or activation of T cells depending on its intracellular localization. Immunity 1:373-384.
8. Boll, W., H. Ohno, Z. Songyang, I. Rapoport, L. Cantley, J. Bonifacino, and T. Kirchhausen. 1996. Sequence requirements for the recognition of tyrosine-based endocytic signals by clathrin AP-2 complexes. EMBO J. 15: 5789-5795.
9. Brady, H. J., D. J. Pennington, C. G. Miles, and E. A. Dzierzak. 1993. CD4 cell surface downregulation in HIV-1 Nef transgenic mice is a consequence of intracellular sequestration. EMBO J. 12:4923-4932.
10. Bresnahan, P. A., W. Yonemoto, S. Ferrell, D. Williams-Herman, R. Geleziunas, and W. C. Greene. 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.
11. Chambers, J., S. Simon, E. Berger, L. Sklar, and K.-I. Arfors. 1993. Endocytosis of β2 integrins by stimulated human neutrophils analyzed by flow cytometry. J. Leukoc. Biol. 120:37-45.
12. Chen, Y. L., D. Trono, and D. Camaur. 1998. The proteolytic cleavage of human immunodeficiency virus type 1 Nef does not correlate with its ability to stimulate virion infectivity. J. Virol. 72:3178-3184.
13. Chowers, M. Y., C. A. Spina, T. J. Kwoh, N. J. Fitch, D. D. Richman, and J. C. Guatelli. 1994. Optimal infectivity in vitro of human immunodeficiency virus type 1 requires an intact nef gene. J. Virol. 68:2906-2914.
14. Collins, K. L., B. K. Chen, S. A. Kalams, B. D. Walker, and D. Baltimore. 1998. HIV-1 Nef protein protects infected primary cells against killing by cytotoxic T lymphocytes. Nature 391:397-401.
15. Cowles, C., G. Odorizzi, G. Payne, and E. SD. 1997. The AP-3 adaptor complex is essential for cargo-selective transport to the yeast vacuole. Cell 91:109-118.
16. Craig, H. M., M. W. Pandori, and J. C. Guatelli. 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. USA 95:11229-11234.
17. Cullen, B. R. 1998. HIV-1 Auxiliary proteins: making connections in a dying cell. Cell 93:685-692.
18. Dell'Angelica, E., H. Ohno, C. Ooi, E. Rabinovich, K. Roche, and J. Bonifacino. 1997. AP-3: an adaptor-like protein complex with ubiquitous expression. EMBO J. 16:917-928.
19. Finzi, D., M. Hermankova, T. Pierson, L. Carruth, C. Buck, R. Chaisson, T. Quinn, K. Chadwick, J. Margolick, R. Brookmeyer, J. Gallant, M. Markowitz, D. Ho, D. Richman, and R. Siliciano. 1998. Identification of a reservoir for HIV-1 in patients on highly active antiretroviral therapy. Science 278: 1295-1300.
20. Foti, M., A. Mangasarian, V. Piguet, D. Lew, K. Krause, D. Trono, and J. Carpentier. 1997. Nef-mediated clathrin coated pit formation. J. Cell Biol. 139:37-47.
21. Franchini, G., M. Robert-Guroff, J. Ghrayeb, N. Chang, and F. Wong-Staal. 1986. Cytoplasmic localization of the HTLV-III 3′ orf protein in cultured T-cells. Virology 155:593-599.
22. 14C]herbimycin A and its use in the elucidation of the kinase inactivation mechanism. FEBS Lett. 340:155-158.
23. Gallay, P., T. Hope, D. Chin, and D. Trono. 1997. HIV-1 infection of nondividing cells through the recognition of integrase by the importin/karyopherin pathway. Proc. Natl. Acad. Sci. USA 94:9825-9835.
24. Gallusser, A., and T. Kirchhausen. 1993. The β1 and β2 subunits of the AP complexes are the clathrin coat assembly components. EMBO J 12:5237-5244.
25. Garcia, J., and A. Miller. 1991. Serine phosphorylation independent downregulation of cell surface CD4 by Nef. Nature 350:508-511.
26. Gervaix, A., D. West, L. Leoni, D. Richman, F. Wong-Staal, and J. Corbeil. 1997. A new cell line to monitor HIV-1 infection and drug susceptibility in vitro. Proc. Natl. Acad. Sci. USA 94:4653-4658.
27. Glickman, J., E. Conibear, and B. Pearse. 1989. Specificity of binding clathrin adapters to signals on the mannose-6-phosphate/insulin-like growth factor II receptor. EMBO J. 8:1041-1047.
28. Goodman, O., and J. Keen. 1995. The α-chain of the AP-2 adaptor is a clathrin binding subunit. J. Biol. Chem. 270:23768-23773.
29. Greenberg, M., S. Bronson, M. Lock, M. Neumann, G. Pavlakis, and J. Skowronski. 1997. Co-localization of HIV-1 Nef with the AP-2 adaptor protein complex correlates with Nef-induced CD4 down-regulation. EMBO J. 16:6964-6976.
30. Greenberg, M., L. DeTulleo, I. Rapoport, J. Skowronski, and T. Kirchhausen. 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.
31. Greenberg, M. E., A. J. Iafrate, and J. Skowronski. 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.
32. Greenway, A., A. Azad, and D. McPhee. 1995. Human immunodeficiency virus type 1 Nef protein inhibits activation pathways in peripheral blood mononuclear cells and T-cell lines. J. Virol. 69:1842-1850.
33. Grzesiek, S., A. Bax, J. Hu, J. Kaufman, I. Palmer, S. Stahl, N. Tjandra, and P. Wingfield. 1997. Refined solution structure and backbone dynamics of HIV-1 Nef. Protein Sci. 6:1248-1263.
34. Grzesiek, S., A. Bax, J. S. Hu, J. Kaufman, I. Palmer, S. J. Stahl, N. Tjandra, and P. T. Wingfield. 1997. Refined solution structure and backbone dynamics of HIV-1 Nef. Protein Sci. 6:1248-1263.
35. Grzesiek, S., S. J. Stahl, P. T. Wingfield, and A. Bax. 1996. The CD4 determinant for downregulation by HIV-1 Nef directly binds to Nef. Mapping of the Nef binding surface by NMR. Biochemistry 35:10256-10261.
36. Guy, B., M. Kieny, Y. Riviere, C. Peuch, K. Dott, M. Girard, L. Montagnier, and J. Lecocq. 1987. HIV F/3′ orf encodes a phosphorylated GTP-binding protein resembling an oncogene product. Nature 330:266-269.
37. Hanna, Z., D. G. Kay, N. Rebai, A. Guimond, S. Jothy, and P. Jolicoeur. 1998. Nef harbors a major determinant of pathogenicity for an AIDS-like disease induced by HIV-1 in transgenic mice. Cell 95:163-175.
38. Hardwick, J. S., and B. M. Sefton. 1995. Activation of the Lck tyrosine protein kinase by hydrogen peroxide requires the phosphorylation of Tyr-394. Proc. Natl. Acad. Sci. USA 92:4527-4531.
39. Harris, M. P., and J. C. Neil. 1994. Myristoylation-dependent binding of HIV-1 Nef to CD4. J. Mol. Biol. 241:136-142.
40. Heilker, R., U. Manning-Krieg, J. Zuber, and M. Spiess. 1996. In vitro binding of clathrin adaptors to sorting signals correlates with endocytosis and basolateral sorting. EMBO J. 15:2893-2899.
41. Ho, D., A. Neumann, A. Perelson, W. Chen, J. Leonard, and M. Markowitz. 1995. Rapid turnover of plasma virions and CD4 lymphocytes in HIV-1 infection. Nature 373:123-126.
42. Hua, J., W. Blair, R. Truant, and B. R. Cullen. 1997. Identification of regions in HIV-1 Nef required for efficient downregulation of cell surface CD4. Virology 231:231-238.
43. Hua, J., and B. Cullen. 1997. 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. 71:6742-6748.
44. Iafrate, A. J., S. Bronson, and J. Skowronski. 1997. Separable functions of Nef disrupt two aspects of T cell receptor machinery: CD4 expression and CD3 signaling. EMBO J. 16:673-684.
45. June, C., M. Fletcher, J. Ledbetter, G. Schieven, J. Siegel, A. Phillips, and L. Samuelson. 1990. Inhibition of tyrosine phosphorylation prevents T-cell receptor-mediated signal transduction. Proc. Natl. Acad. Sci. USA 87:7722-7726.
46. Kaminchik, J., N. Bashan, A. I. Sarver, N. Gorecki, and A. Panet. 1991. Genetic characterization of human immunodeficiency virus type 1 nef gene productas in vitro and expressed in mammalian cells. J. Virol. 65:583-588.
47. Lee, C. H., B. Leung, M. A. Lemmon, J. Zheng, D. Cowburn, J. Kuriyan, and K. Saksela. 1995. 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. 14:5006-5015.
48. Le Gall, S., L. Erdtmann, S. Benichou, C. Berlioz-Torrent, L. Liu, R. Benarous, J.-M. Heard, and O. Schwarz. 1998. Nef interacts with the mu subunit of clathrin adapter complexes and reveals a cryptic sorting signal in MHC-I molecules. Immunity 8:483-495.
49. Le Gall, S., J. M. Heard, and O. Schwartz. 1997. Analysis of Nef-induced MHC-I endocytosis. Res Virol. 148:43-47.
50. Le Gall, S., M. C. Prevost, J. M. Heard, and O. Schwartz. 1997. Human immunodeficiency virus type I Nef independently affects virion incorporation of major histocompatibility complex class I molecules and virus infectivity. Virology 229:295-301.
51. Lindemann, D., R. Wilhelm, P. Renard, A. Althage, R. Zinkernagel, and J. Mous. 1994. Severe immunodeficiency associated with a human immunodeficiency virus 1 NEF/3′-long terminal repeat transgene. J. Exp. Med. 179: 797-807.
52. Lu, X., H. Yu, S. Liu, F. M. Brodsky, and B. M. Peterlin. 1998. Interactions between HIV1 Nef and vacuolar ATPase facilitate the internalization of CD4. Immunity 8:647-656.
53. Mangasarian, A., M. Foti, C. Aiken, D. Chin, J. L. Carpentier, and D. Trono. 1997. The HIV-1 Nef protein acts as a connector with sorting pathways in the Golgi and at the plasma membrane. Immunity 6:67-77.
54. Miller, M. D., M. B. Feinberg, and W. C. Greene. 1994. The HIV-1 nef gene acts as a positive viral infectivity factor. Trends Microbiol. 2:294-298.
55. Naldini, L., U. Blomer, P. Gallay, D. Ory, R. Mulligan, F. Gage, I. Verma, and D. Trono. 1996. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272:263-267.
56. Pearse, B. 1988. Receptors compete for adaptors found in plasma membrane coated pits. EMBO J. 7:3331-3336.
57. Pelchen-Matthews, A., J. Armes, G. Griffiths, and M. Marsh. 1991. Differential endocytosis of CD4 in lymphocytic and non-lymphocytic cells. J. Exp. Med. 173:575-587.
58. Pelchen-Matthews, A., J. Armes, and M. Marsh. 1989. Internalization and recycling of CD4 transfected into HeLa and NIH3T3 cells. J. Exp. Med. 8:3641-3649.
59. Perelson, A., A. Neumann, M. Markowitz, J. Leonard, and D. Ho. 1996. HIV-1 dynamics in vivo: virion clearance rate, infected cell life span, and viral generation time. Science 271:1582-1586.
60. Piguet, V., Y.-L. Chen, A. Mangasarian, M. Foti, J. Carpentier, and D. Trono. 1998. Mechanism of Nef induced CD4 endocytosis: Nef connects CD4 with the mu chain of adaptor complexes. EMBO J. 17:2472-2481.
61. Pomerantz, R., D. Trono, M. Feinberg, and D. Baltimore. 1990. Cells non-productively infected with HIV-1 exhibit an aberrant pattern of viral RNA expression: a molecular model for latency. Cell 61:1271-1276.
62. Robinson, M., and B. Pearse. 1980. Immunofluorescent localization of 100k coated vesicle proteins. J. Cell Biol. 102:48-52.
63. + T-cell responses associated with control of viremia. Science 278:1447-1450.
64. Rossi, F., A. Gallina, and G. Milanesi. 1996. Nef-CD4 physical interaction sensed with the yeast two-hybrid system. Virology 217:397-403.
65. + viruses but not for down-regulation of CD4. EMBO J. 14:484-491.
66. Schwartz, O., V. Maréchal, S. Le Gall, F. Lemonnier, and J. M. Heard. 1996. Endocytosis of major histocompatihility complex class I molecules is induced by the HIV-1 Nef protein. Nat. Med. 2:338-342.
67. Sepp-Lorenzino, L., Z. Ma, D. Lebwohl, A. Vinitsky, and N. Rosen. 1995. Herbimycin A induces the 20S proteasome-and ubiquitin-dependent degradation of receptor tyrosine kinases. J. Biol. Chem. 270:16580-16587.
68. Seshamma, T., O. Bagasra, D. Trono, D. Baltimore, and R. J. Pomerantz. 1992. Blocked early-stage latency in the peripheral blood cells of certain individuals infected with human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. USA 89:10663-10667.
69. Shih, W., A. Gallusser, and T. Kirchhausen. 1995. A clathrin binding site in the hinge of the beta-2 chain of mammalian AP-2 complexes. J. Biol. Chem. 270:31083-31090.
70. Simpson, F., A. Peden, L. Christopoulou, and M. Robinson. 1997. Characterization of the adaptor-related protein complex AP-3. J. Cell Biol. 137: 835-845.
71. Skowronski, J., D. Parks, and R. Mariani. 1993. Altered T cell activation and development in transgenic mice expressing the HIV-1 nef gene. EMBO J. 12:703-713.
72. Spina, C. A., T. J. Kwoh, M. Y. Chowers, J. C. Guatelli, and D. D. Richman. 1994. The importance of nef in the induction of human immunodeficiency virus type 1 replication from primary quiescent CD4 lymphocytes. J. Exp. Med. 179:115-123.
73. Swingler, S., P. Gallay, D. Camaur, J. Song, A. Abo, and D. Trono. 1997. The Nef protein of human immunodeficiency virus type 1 enhances serine phosphorylation of the viral matrix. J. Virol. 71:4372-4377.
74. Uehara, Y., and H. Fukazawa. 1991. Use and selectivity of herbimycin A as inhibitor of protein-tyrosine kinases. Methods Enzymol. 201:370-379.
75. Umesono, K., K. Murakami, C. Thompson, and R. Evans. 1991. Direct repeats as selective response elements for the thyroid hormone, retinoic acid and vitamin D3 receptors. Cell 65:1255-1266.
76. Wei, X., S. Hhosh, M. Taylor, V. Johnson, E. Emini, P. Deutsch, J. Lifson, S. Nonhoeffer, M. Nowak, B. Hahn, M. Saag, and G. Shaw. 1995. Viral dynamics in human immunodeficiency virus type 1 infection. Nature 373: 117-122.
77. Wong, J., M. Hezareh, H. Gunthard, D. Havlir, C. Ignacio, C. Spina, and D. Richman. 1998. Recovery of replication-competent HIV despite prolonged suppression of plasma viremia. Science 278:1291-1295.
78. Yurchak, L. K., J. S. Hardwick, K. Amrein, K. Pierno, and B. M. Sefton. 1996. Stimulation of phosphorylation of Tyr394 by hydrogen peroxide reactivates biologically inactive, non-membrane-bound forms of Lck. J. Biol. Chem. 271:12549-12554.