Two elements target SIV Nef to the AP-2 clathrin adaptor complex, but only one is required for the induction of CD4 endocytosis

EMBO Journal

Volumn 18, Issue 10, 1999, Pages 2722-2733

  Lock, Martin ^a   Greenberg, Michael E ^a   Lafrate, A John ^a   Swigut, Tomek ^a   Muench, Jan ^b   Kirchhoff, Frank ^b   Shohdy, Nadim ^a   Skowronski, Jacek ^a  

^a Watson School of Biological Sciences   (United States)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

CD4; Clathrin; Endocytosis; HIV; Nef

Indexed keywords

ADAPTOR PROTEIN; CD4 ANTIGEN; DNA (APURINIC OR APYRIMIDINIC SITE) LYASE; LEUCINE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MUTANT PROTEIN; NEF PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CYTOPLASM; ENDOCYTOSIS; GENE CONTROL; GENETIC SELECTION; HUMAN IMMUNODEFICIENCY VIRUS 1; LIFE CYCLE; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; SIGNAL TRANSDUCTION; SIMIAN IMMUNODEFICIENCY VIRUS; VIRUS ACTIVATION;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; AMINO ACID SEQUENCE; ANTIGENS, CD4; BASE SEQUENCE; CLATHRIN; DOWN-REGULATION; ENDOCYTOSIS; FIBROBLASTS; GENE PRODUCTS, NEF; GREEN FLUORESCENT PROTEINS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HIV-1; HUMANS; JURKAT CELLS; LUMINESCENT PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; NERVE TISSUE PROTEINS; PHOSPHOPROTEINS; PROTEIN BINDING; RECOMBINANT FUSION PROTEINS; SIMIAN IMMUNODEFICIENCY VIRUS; TYROSINE;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; SIMIAE; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 0033577730     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.10.2722     Document Type: Article

References (47)

1. Ahle, S., Mann, A., Eichelsbacher, U. and Ungewickell, E. (1988) Structural relationships between clathrin assembly proteins from the Golgi and the plasma membrane. EMBO J., 7, 919-929.
2. Alexander, L., Du, Z., Rosenzweig, M., Jung, J.U. and Desrosiers, R.C. (1998) A role for natural simian immunodeficiency virus and human immunodeficiency virus type 1 nef alleles in lymphocyte activation. J. Virol., 8, 6094-6099.
3. Benson, R.E., Sanfridson, A., Ottinger, J.S., Doyle, C. and Cullen, B.R. (1993) Downregulation of cell-surface CD4 expression by simian immunodeficiency virus Nef prevents viral super infection. J. Exp. Med., 177, 1561-1566.
4. 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.
5. Bresnahan, P.A., Yonemoto, W., Ferrell, S., Williams-Herman, D., Geleziunas, R. and Greene, W.C. (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., 22, 1235-1238.
6. Campbell, C., Squicciarini, J., Shia, M., Pilch, P.F. and Fine, R.E. (1984) Identification of a protein kinase as an intrinsic component of rat coated vesicles. Biochemistry, 23, 4420-4426.
7. Chackerian, B., Haigwood, N.L. and Overbaugh, J. (1995) Characterization of a CD4 expressing macaque cell line that can detect virus after a single replication cycle and can be infected by diverse simian immunodeficiency virus isolates. Virology, 213, 386-394.
8. Collins, K.L., Chen, B.K., 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.
9. Craig, H.M, Pandori, M.W. and Guatelli, J.C. (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, 19, 11229-11234.
10. Emerman, M. and Malim, M.H. (1998) HIV-1 regulatory/accessory genes: keys to unraveling viral and host cell biology. Science, 280, 1880-1884.
11. Frankel, A.D. and Young, J.A. (1998) HIV-1: fifteen proteins and an RNA. Anna. Rev. Biochem., 67, 1-25.
12. Garcia, J.V. and Miller, A.D. (1991) Serine phosphorylation-independent downregulation of cell-surface CD4 by nef. Nature, 350, 508-511.
13. Greenberg, M.E., Bronson, S., Lock, M., 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 down-regulation. EMBO J., 16, 6964-6976.
14. Greenberg, M., DeTulleo, L., Rapoport, I., Skowronski, J. and Kirchhausen, T. (1998a) A dileucine motif in HIV-1 Nef is essential for sorting into clathrin-coated pits and for downregulation of CD4. Curr. Biol., 22, 1239-1242.
15. Greenberg, M.E., Iafrate, A.J. and Skowronski, J. (1998b) 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.
16. Grzesiek, S., Bax, A., Clore, G.M., Gronenborn, A.M., Hu, J.S., Kaufman, J., Palmer, I., Stahl, S.J. and Wingfield, P.T. (1996) 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. Nature Struct. Biol., 3, 340-345.
17. Gundlach, B.R. et al. (1997) Construction, replication and immunogenic properties of a simian immunodeficiency virus expressing interleukin-2. J. Virol., 71, 2225-2232.
18. Hua, J. and Cullen, B.R. (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.
19. 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.
20. Kimpton, J. and Emerman, M. (1992) Detection of replication-competent and pseudotyped human immunodeficiency virus with a sensitive cell line on the basis of activation of an integrated β-galactosidase gene. J. Virol., 4, 2232-2239.
21. Kirchhausen, T., Bonifacino, J.S. and Riezman, H. (1997) Linking cargo to vesicle formation: receptor tail interactions with coat proteins. Curr. Opin. Cell Biol., 9, 488-495.
22. Lang, S.M. et al. (1997) Association of simian immunodeficiency virus Nef with cellular serine/threonine kinases is dispensable for the development of AIDS in rhesus macaques. Nature Med., 3, 860-865.
23. Lee, C.-H., Saksela, K., Mirza, U.A., Chait, B.T. and Kuryan, J. (1996) Crystal structure of the conserved core of HIV-1 Nef complexed with a Src family SH3 domain. Cell, 85, 931-942.
24. Le Gall, S., Erdtmann, L., Benichou, S., Berlioz-Torrent, C., Liu, L., Benarous, R., Heard, J.M. and Schwartz, O. (1998) Nef interacts with the μ subunit of clathrin adaptor complexes and reveals a cryptic sorting signal in MHC I molecules. Immunity, 8, 483-495.
25. Littman, D.R. (1996) The CD4 Molecule. Roles in T Lymphocytes and in HIV Disease. Springer-Verlag, Berlin, Germany.
26. Lu, X., Yu, H., Liu, S.H., Brodsky, F.M. and Peterlin, B.M. (1998) Interactions between HIV 1 Nef and vacuolar ATPase facilitate the internalization of CD4. Immunity, 5, 647-656.
27. Mariani, R. and Skowronski, J. (1993) CD4 down-regulation by nef alleles isolated from human immunodeficiency virus type I-infected individuals. Proc. Natl Acad. Sci USA, 90, 5549-5553.
28. 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.
29. Marsh, M. and Pelchen-Matthews, A. (1996) Endocytotic and exocytotic regulation of CD4. Curr. Top. Microbiol. Immunol., 205, 107-135.
30. Matsui, W. and Kirchhausen, T. (1990) Stabilization of clathrin coats by the core of the clathrin-associated protein complex AP-2. Biochemistry, 48, 10791-10798.
31. Miller, M.D., Warmerdam, M.T., Gaston, I., Greene, W.C. and Feinberg, M.B. (1994) The human immunodeficiency virus-1 nef gene product: a positive factor for viral infection and replication in primary lymphocytes and macrophages. J. Exp. Med., 179, 101-113.
32. Myers, G., Berzofsky, J.A., Rabson, A.B. and Smith, T.E. (1993) Human Retroviruses and AIDS. Los Alamos National Laboratory, Los Alamos, NM.
33. Oldridge, J. and Marsh, M. ( 1998) Nef-an adaptor adaptor? Trends Cell Biol., 8, 302-305.
34. Owen, D.J. and Evans, P.R. (1998) A structural explanation for the recognition of tyrosine-based endocytotic signals. Science, 282, 1327-1332.
35. lck, increased association with clathrin-coated pits and altered endosomal sorting. J. Exp. Med., 178, 1209-1222.
36. Piguet, V., Chen, Y.L., Mangasarian, A., Foti, M., Carpentier, J.L. and Trono, D. (1998) Mechanism of Nef-induced CD4 endocytosis: Nef connects CD4 with the mu chain of adaptor complexes. EMBO J., 17, 2472-2481.
37. Rapoport, I., Chen, Y.C., Cupers, P., Shoelson,S.E. and Kirchhausen, T. (1998) 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., 17, 2148-2155.
38. Sambrook, J., Fritsch, E.F. and Manialis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
39. Schenk, P.M., Baumann, S., Mattes, R. and Steinbiss, H.H. (1995) Improved high-level expression system for eukaryotic genes in Escherichia coli using T7 RNA polymerase and rare ArgtRNAs. Biotechniques, 19, 196-200.
40. Schmid, S.L. ( 1997) Clathrin-coated vesicle formation and protein sorting: an integrated process. Annu. Rev. Biochem., 66, 511-548.
41. Schwartz, O., Marechal, V., LeGall, S., Lemonnier, F. and Heard, J.M. (1996) Endocytosis of major histocompatibility complex class I molecules is induced by the HIV-1 Nef protein. Nature Med., 2, 338-342.
42. Sinclair, E., Barbosa, P. and Feinberg, M.B. (1997) The nef gene products of both simian and human immunodeficiency viruses enhance virus infectivity and are functionally interchangeable. J. Virol., 5, 3641-3651.
43. Skowronski, J., Parks, D. and Mariani, R. (1993) Altered T cell activation and development in transgenic mice expressing the HIV-1 nef gene. EMBO J., 12, 703-713.
44. Spina, C.A., Kwoh, T.J., Chowers, M.Y, Guatelli, J.C. and Richman, D.D. (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.
45. Stauber, R.H., Horie, K., Carney, P., Hudson, E.A., Tarasova, N.I., Gaitanaris, G.A. and Pavlakis, G.N. (1998) Development and applications of enhanced green fluorescent protein mutants. Bintechniques, 3, 462-466, 468-471.
46. Studier, F.W., Rosenberg, A.H., Dunn, J.J. and Dubendorff, J.W. (1990) Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol., 185, 60-89.
47. Tanaka, M. and Herr, W. (1990) Differential transcriptional activation by Oct-1 and Oct-2: interdependent activation domains induce Oct-2 phosphorylation. Cell, 60, 375-386.