Mechanism of Nef-induced CD4 endocytosis: Nef connects CD4 with the μ chain of adaptor complexes

EMBO Journal

Volumn 17, Issue 9, 1998, Pages 2472-2481

  Piguet, Vincent ^a   Chen, Yen Liang ^a   Mangasarian, Aram ^a   Foti, Michelangelo ^a   Carpentier, Jean Louis ^a   Trono, Didier ^a  

^a UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

Author keywords

Adaptor complexes; CD4; Lentivirus; MHC class I; Nef

Indexed keywords

ADAPTOR PROTEIN; CD4 ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MEMBRANE PROTEIN; NEF PROTEIN;

ANTIGEN EXPRESSION; ARTICLE; CONTROLLED STUDY; ENDOCYTOSIS; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 2; INTERNALIZATION; LENTIVIRINAE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; SIMIAN IMMUNODEFICIENCY VIRUS;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD4; CELL LINE; DOWN-REGULATION; ENDOCYTOSIS; GENE PRODUCTS, NEF; HIV-1; HIV-2; HUMANS; KINETICS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; PHENOTYPE; PRIMATES; RECOMBINANT FUSION PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SIMIAN IMMUNODEFICIENCY VIRUS; TRANSFECTION;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 2; LENTIVIRUS; PRIMATES; RNA VIRUSES; SIMIAE; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 0032079665     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.9.2472     Document Type: Article

References (47)

1. 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.
2. Aiken,C., Krause,L., Chen,Y.-L. and Trono,D. (1996) Mutational analysis of HIV-1 Nef: identification of two mutants that are temperature-sensitive for CD4 down-regulation. Virology, 217, 293-300.
3. Ausubel,F., Brent,R., Kingston,R.E., Moore,D.D., Smith,J.A., Seidman,J.G. and Struhl,K. (1987) Current Protocols in Molecular Biology. John Wiley & Sons, New York.
4. Bartel,P. and Fields,S. (1993) Analyzing protein-protein interactions using two-hybrid system. Methods Enzymol., 254, 241-263.
5. Benmerah,A., Begue,B., Dautry-Varsat,A. and Cerf-Benussan,N. (1996) The ear of α-adaptin interacts with the COOH-terminal domain of the Eps15 protein. J. Biol. Chem., 271, 12111-12116.
6. Chambers,J.D., Simon,S.I., Berger,E.M., Sklar,L.A. and Arfors,K.-I. (1993) Endocytosis of beta-2 integrins by stimulated human neutrophils analyzed by flow cytometry. J. Leukocyte Biol., 53, 462-469.
7. 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.
8. Cowles,C.R., Odorizzi,G., Payne,G.S. and Emr,S. (1997) The AP-3 adaptor complex is essential for cargo-selective transport to the yeast vacuole. Cell, 91, 109-118.
9. Deacon,N.J. et al. (1995) Genomic structure of an attenuated quasi species of HIV-1 from a blood transfusion donor and recipients. Science, 270, 988-991.
10. Dietrich,J., Kastrup,J., Nielsen,B.L., Ødum,N. and Geisler,C. (1997) Regulation and function of the CD3g DxxxLL motif: a binding site for adaptor protein-1 and adaptor protein-2 in vitro. J. Cell Biol., 138, 271-281
11. Durfee,T., Becherer,K., Chen,P.-L., Yeh,S.-H., Yang, Y., Kilburn,A.E., Lee,W.-H. and Elledge,S. (1993) The retinoblastoma protein associates with the protein phosphatase type 1 catalytic subunit. Genes Dev., 7, 555-569.
12. Ferguson,S.S., Downey,W.E., Colapietro,A.M., Barak,L.S., Menard,L. and Caron,M.G. (1996) The role of beta-arrestin in mediating agonist-promoted G protein-coupled receptor internalization. Science, 271, 363-366.
13. 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.
14. Gallusser,A. and Kirchhausen,T. (1993) The beta 1 and beta 2 subunits of the AP complexes are the clathrin coat assembly components. EMBO J., 12, 5237-5244.
15. Garcia,J.V. and Miller,A.D. (1991) Serine phosphorylation independent down-regulation of cell-surface CD4 by Nef. Nature, 350, 508-551.
16. Goldstein,J.L., Brown,M.S., Anderson,R.G., Russell,D.W. and Schneider, W.J. (1985) Receptor-mediated endocytosis: concepts emerging from the LDL receptor system. Annu. Rev. Cell Biol., 1, 1-39.
17. Goodman,O.B., Krupnick,J.G., Santini,F., Gurevitch,V.V., Penn,R.B., Gagnon,A.W., Keen,J.H. and Benovic,J.L. (1996) Beta-arrestin acts as a clathrin adaptor in endocytosis of the beta2-adrenergic receptor. Nature, 383, 447-450.
18. Greenway,A., Azad,A. and McPhee,D. (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.
19. Grzesiek,S., Stahl,S.J., Wingfield,P.T. and Bax,A. (1996) The CD4 determinant for down-regulation by HIV-1 Nef directly binds to Nef. Mapping of the Nef binding surface by NMR. Biochemistry, 35, 10256-10261.
20. Guy,B., Kieny,M.P., Riviere,Y., Peuch,C.L., Dott,K., Girard,M., Montagnier,L. and Lecocq,J.-P. (1987) HIV F/3′ orf encodes a phosphorylated GTP-binding protein resembling an oncogene product. Nature, 330, 266-269.
21. Harper,J.W., Adami,G.R., Wei,N., Keyomarsi,K. and Elledge,S.J. (1993) The p21 Cdk-interacting protein Cip 1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell, 75, 805-816.
22. Harris,M.P.G. and Neil,J.C. (1994) Myristoylation dependent binding of HIV-1 Nef to CD4. J. Mol. Biol. 241, 136-142.
23. Iafrate,A.J., Bronson,S. and Skowronski,J. (1997) Separable functions of Nef disrupt two aspects of T cell receptor machinery: CD4 expression and CD3 signaling. EMBO J., 16, 673-684.
24. Keen,J.H., Beck,K.A., Kirchhausen,T. and Jarrett,T. (1991) Clathrin domains involved in recognition by assembly protein AP-2. J. Biol. Chem., 266, 7950-7956.
25. Kestler,H.W., Ringler,D.J., Mori,K., Panicali,D.L. 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.
26. Kirchhoff,F., Greenough,T.C., Brettler,D.B., Sullivan,J.L. and Desrosiers,R.C. (1995) Absence of intact nef sequences in a long-term survivor with nonprogressive HIV-1 infection. N. Engl. J. Med., 332, 228-232.
27. Letourneur,F. and Klausner,R.D. (1992) A novel di-leucine motif and a tyrosine-based motif independently mediate lysosomal targeting and endocytosis of CD3 chains. Cell, 69, 1143-1157.
28. 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.
29. Ohno,H. et al. (1995) Interaction of tyrosine-based signals with clathrin-associated proteins. Science, 269, 1872-1874.
30. Ohno,H., Fournier,M.-C., Poy,G. and Bonifacino,J.S. (1996) Structural determinants of interaction of tyrosine-based signals with the adaptor medium chains. J. Biol. Chem., 271, 29009-29015.
31. Okabayashi,Y., Sugimoto,Y., Totty,N.F., Hsuan,J., Kido,Y., Sakaguchi,K., Gout,I., Waterfield,M.D. and Kasuga,M. (1996) Interaction of She with adaptor protein adaptins. J. Biol. Chem., 271, 5265-5269.
32. Peeler,J.S., Donzell,W.C. and Anderson,R.G. (1993) The appendage domain of the AP-2 subunit is not required for assembly or invagination of clathrin-coated pits. J. Cell Biol., 120, 47-54.
33. Pelchen-Matthews,A., Armes,J.E. and Marsh,M. (1989) Internalization and recycling of CD4 transfected into HeLa and NIH3T3 cells. EMBO J., 8, 3641-3649.
34. Pelchen-Matthews,A., Armes,J.E., Griffiths,G. and Marsh,M. (1991) Differential endocytosis of CD4 in lymphocytic and nonlymphocytic cells. J. Exp. Med., 173, 575-587.
35. Rapoport,I., Miyazaki,M., Boll,W., Duckworth,B., Cantley,L.C., Shoelson,S. and Kirchhausen,T. (1997) Regulatory interactions in the recognition of endocytic sorting signals by AP-2 complexes. EMBO J., 16, 2240-2250.
36. Rhee,S.S. and Marsh,J.W. (1994) Human immunodeficiency virus type 1 Nef-induced down-modulation of CD4 is due to rapid internalization and degradation of surface CD4. J. Virol., 68, 5156-5163.
37. Robinson,M. (1994) The role of clathrin, adaptors and dynamin in endocytosis. Curr. Biol., 6, 538-544.
38. Rodman,J.S., Mercer,R.W. and Stahl,P.D. (1990) Endocytosis and transcytosis. Curr. Opin. Cell Biol., 2, 664-672.
39. Rossi,F., Gallina,A. and Milanesi,G. (1996) Nef-CD4 physical interaction sensed with the yeast two-hybrid system. Virology, 217, 397-403.
40. lck protein-tyrosine kinase interact with a common element in CD4 cytoplasmic tail. Proc. Natl Acad. Sci. USA, 92, 349-353.
41. + T cell line, CEM E5, after HIV-1 infection. J. Immunol., 143, 2858-2866.
42. Schwartz,O., Dautry-Varsat,A., Goud,B., Marechal,V., Subtil,A., Heard,J.-M. and Danos,O. (1995) Human immunodeficiency virus type 1 Nef induces accumulation of CD4 in early endosomes. J. Virol., 69, 528-533.
43. Schwartz,O., Marechal,V., Le Gall,S., Lemonnier,F. and Heard,J.-M. (1996) Endocytosis of major histocompatibility complex class I molecules is induced by HIV-1 Nef protein. Nature Med., 2, 338-342.
44. Shiratori,T., Miyatake,S., Ohno,H., Nakaseko,C., Isono,K., Bonifacino,J. and Saito,T. (1997) Tyrosine phosphorylation controls internalization of CTLA-4 by regulating its interaction with clathrin-associated adaptor complex AP-2. Immunity, 6, 583-589.
45. Trowbridge,J.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.
46. Umesono,K., Murakami,K.K., Thompson,C.C. and Evans,R.M. (1991) Direct repeats as selective response elements for the thyroid hormone, retinoic acid, and vitamin D3 receptors. Cell, 65, 1255-1266.
47. Van Delft,S., Schumacher,C., Hage,W., Verkleij,A.J. and van Bergen en Henegouwen,P.M.P. (1997) Association and colocalization of Eps 15 with adaptor protein-2 and clathrin. J. Cell Biol., 136, 811-821.