Nef interacts with the μ subunit of clathrin adaptor complexes and reveals a cryptic sorting signal in MHC I molecules

Immunity

Volumn 8, Issue 4, 1998, Pages 483-495

  Le Gall, Sylvie ^a   Erdtmann, Lars ^b   Benichou, Serge ^b   Berlioz Torrent, Clarisse ^b   Liu, Langxia ^b   Benarous, Richard ^b   Heard, Jean Michel ^a   Schwartz, Olivier ^a  

^a INSTITUT PASTEUR   (France)

^b INSTITUT COCHIN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

HLA A ANTIGEN; HLA B ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1;

ANTIGEN EXPRESSION; ARTICLE; CONTROLLED STUDY; GOLGI COMPLEX; HELA CELL; HUMAN; HUMAN CELL; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN TARGETING; VIRUS CELL INTERACTION;

EID: 0032055774     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1074-7613(00)80553-1     Document Type: Article

References (42)

1. Aiken, C., and Trono, D. (1995). Nef stimulates human immunodeficiency virus type 1 proviral DNA synthesis. J. Virol. 69, 5048-5056.
2. Aiken, C., Konner, J., Landau, N.R., Lenburg, M.E., and Trono, D. (1994). Nef induces CD4 endocytosis: requirement for a critical dileucine motif in the membrane-proximal CD4 cytoplasmic domain. Cell 76, 853-864.
3. Bachelerie, F., Alcami, J., Hazan, U., Israël, N., Goud, B., Arenzana-Seisdedos, F., and Virelizier, J.L. (1990). Constitutive expression of human immunodeficiency virus (HIV) nef protein in human astrocytes does not influence basal or induced HIV long terminal repeat activity. J. Virol. 64, 3059-3062.
4. Benichou, S., Bomsel, M., Bodeus, M., Durand, H., Doute, M., Letourneur, F., Camonis, J., and Benarous, R. (1994). Physical interaction of the HIV-1 Nef protein with beta-COP, a component of non-clathrin-coated vesicle for membrane traffic. J. Biol. Chem. 269, 30073-30076.
5. Benmerah, A., Bègue, B., Dautry-Varsat, A., and Cerf-Bensussan, N. (1996). The ear of α-adaptin interacts with the COOH-terminal domain of the Eps15 protein. J. Biol. Chem. 271, 12111-12116.
6. Bijlmakers, M.J., and Ploegh, H.L. (1993). Putting together an MHC class I molecule. Curr. Opin. Immunol. 5, 21-26.
7. Bodeus, M., Marie-Cardine, A., Bougeret, C., Ramos-Morales, F., and Benarous, R. (1995). In vitro binding and phosphorylation of human immunodeficiency virus type 1 Nef protein by serine/threonine protein kinase. J. Gen. Virol. 76, 1337-1344.
8. Boll, W., Ohno, H., Songyang, Z., Rapoport, I., Cantley, L.C., Bonifacino, J.S., and Kirchhausen, T. (1996). Sequence requirements for the recognition of tyrosine-based endocytic signals by clathrin AP-2 complexes. EMBO J. 15, 5789-5795.
9. Brutkiewicz, R.R., and Welsh, R.M. (1995). Major histocompatibility complex class I antigens and the control of viral infections by natural killer cells. J. Virol. 69, 3967-3971.
10. Ciccone, E., Pende, D., Nanni, L., Di Donato, C., Viale, O., Beretta, A., Vitale, M., Sivori, S., Moretta, A., and Moretta, L. (1995). General role of HLA class I molecules in the protection of target cells from lysis by natural killer cells: evidence that the free heavy chains of class I molecules are not sufficient to mediate the protective effect. Int. Immunol. 7, 393-400.
11. Collins, K.L., Chen, B.K., Kalams, S.A., Walker, B.D., and Baltimore, D. (1998). HIV-1 Nef protein protects infected primary cells against killing by cytotoxic T lymphocytes. Nature 391, 397-401.
12. Colonna, M., Borsellino, G., Falco, M., Ferrara, G.B., and Strominger, J.L. (1993). 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 90, 12000-12004.
13. Ferrier, P., Layet, C., Caillol, D.H., Jordan, B.R., and Lemonnier, F.A. (1985). The association between murine β2-microglobulin and HLA class I heavy chains results in serologically detectable conformational changes of both chains. J. Immunol. 135, 1281-1287.
14. Foti, M., Mangasarian, A., Piguet, V., Lew, D.P., Krause, K.H., Trono, D., and Carpentier, J.L. (1997). Nef-mediated clathrin-coated pit formation. J. Cell Biol. 139, 37-47.
15. Garcia, J.V., and Miller, A.D. (1991). Serine phosphorylation-independent downregulation of cell-surface CD4 by nef. Nature 350, 508-511.
16. Goud, B., Zahraoui, A., Tavitian, A., and Saraste, J. (1990). Small GTP-binding proteins associated with Golgi cisternae. Nature 345, 553-556.
17. Greenberg, M.E., Bronson, S., Neumann, M., Pavlakis, G.N., and Skowronski, J. (1997). Co-localization of HIV-1 Nef with the AP-2 adaptor protein complex correlates with Nef-induced CD4 downregulation. EMBO J. 16, 6964-6976.
18. Guild, B., and Strominger, J.L. (1984). Human and murine class I MHC antigens share conserved serine 335, the site of HLA phosphorylation in vivo. J. Biol. Chem. 259, 9235-9240.
19. Harris, M. (1996). From negative factor to a critical role in virus pathogenesis: the changing fortune of Nef. J. Gen. Virol. 77, 2379-2392.
20. Heilker, R., Manning-Krieg, U., Zuber, J.F., and Spiess, M. (1996). In vitro binding of clathrin adaptors to sorting signals correlates with endocytosis and basolateral sorting. EMBO J. 15, 2893-2899.
21. Kestler, H.W., Ringler, D.J., Mori, K., Panicali, D.L., Sehgal, P.K., Daniel, M.D., and Desrosiers, R.C. (1991). Importance of the nef gene for maintenance of high virus loads and for development of AIDS. Cell 65, 651-662.
22. Lee, C.H., Saksela, K., Mirza, U.A., Chait, B.T., and Kuriyan, J. (1996). Crystal structure of the conserved core of HIV-1 Nef complexed with a Src family SH3 domain. Cell 85, 931-942.
23. Mangasarian, A., Foti, M., Aiken, C., Chin, D., Carpentier, J.L., and Trono, D. (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.
24. Marks, M.S., Ohno, H., Kirchhausen, T., and Bonifacino, J.S. (1997). Protein sorting by tyrosine-based signals: adapting to the Ys and wherefores. Trends Cell Biol. 7, 124-128.
25. Neefjes, J.J., Stollorz, V., Peters, P.J., Geuze, H.J., and Ploegh, H.L. (1990). The biosynthetic pathway of MHC class II but not class I molecules intersects the endocytic route. Cell 61, 171-183.
26. Ohno, H., Stewart, J., Fournier, M.C., Bosshart, H., Rhee, I., Miyakate, S., Saito, T., Gallusser, A., Kirchhausen, T., and Bonifacino, J.S. (1995). Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science 269, 1872-1875.
27. Ohno, H., Fournier, M.C., Poy, G., and Bonifacino, J.S. (1996). Structural determinants of interaction of tyrosine-based sorting signals with the adaptor medium chains. J. Biol. Chem. 271, 29009-29015.
28. Parham, P., Adams, E.J., and Arnett, K.L. (1995). The origins of HLA-A,B,C polymorphism. Immunol. Rev. 143, 141-180.
29. lck, increased association with clathrin-coated pits, and altered endosomal sorting. J. Exp. Med. 178, 1209-1222.
30. Reid, P.A., and Watts, C. (1990). Cycling of cell-surface MHC glycoproteins through primaquine-sensitive intracellular compartments. Nature 346, 655-657.
31. Robinson, M.S. (1987). 100-kD coated vesicle proteins: molecular heterogeneity and intracellular distribution studied with monoclonal antibodies. J. Cell Biol. 104, 887-95.
32. Robinson, M.S. (1993). Assembly and targeting of adaptin chimeras in transfected cells. J. Cell Biol. 723, 67-77.
33. Robinson, M.S. (1994). The role of clathrin, adaptors and dynamin in endocytosis. Curr. Opin. Cell Biol. 6, 538-544.
34. Sandoval, I.V., and Bakke, O. (1994). Targeting of membrane proteins to endosomes and lysosomes. Trends Cell Biol. 4, 292-297.
35. Schwartz, O., Rivière, Y., Heard, J.M., and Danos, O. (1993). Reduced cell surface expression of processed HIV-1 envelope glycoprotein in the presence of Nef. J. Virol. 67, 3274-3280.
36. Schwartz, O., Dautry-Varsat, A., Goud, B., Maréchal, V., Subtil, A., Heard, J.M., and Danos, O. (1995a). HIV-1 Nef induces accumulation of CD4 in early endosomes. J. Virol. 69, 528-533.
37. Schwartz, O., Maréchal, V., Danos, O., and Heard, J.M. (1995b). Human immunodeficiency virus type 1 Nef increases the efficiency of reverse transcription in the infected cell. J. Virol. 69, 4053-4059.
38. Schwartz, O., Maréchal, V., Le Gall, S., Lemonnier, F., and Heard, J.M. (1996). Endocytosis of MHC I molecules is induced by HIV-1 Nef. Nat. Med. 2, 338-342.
39. Stang, E., Kartenbeck, J., and Parton, R.G. (1997). Major histocompatibility complex class I molecules mediate association of SV40 with caveolae. Mol. Biol. Cell 8, 47-57.
40. Trowbridge, I.S., Collawn, J.F., and Hopkins, C.R. (1993). Signal-dependent membrane protein trafficking in the endocytic pathway. Annu. Rev. Cell Biol. 9, 129-161.
41. Vega, M.A., and Strominger, J.L. (1989). Constitutive endocytosis of HLA class I antigens requires a specific portion of the intracy-toplasmic tail that shares structural features with other endocytosed molecules. Proc. Natl. Acad. Sci. USA 86, 2688-2692.
42. Wilde, A., and Brodsky, F.M. (1996). In vivo phosphorylation of adaptors regulates their interaction with clathrin. J. Cell Biol. 135, 635-645.