Nef-induced CD4 degradation: A diacidic-based motif in Nef functions as a lysosomal targeting signal through the binding of β-COP in endosomes

Cell

Volumn 97, Issue 1, 1999, Pages 63-73

  Piguet, Vincent ^a   Gu, Feng ^a   Foti, Michelangelo ^a   Demaurex, Nicolas ^a   Gruenberg, Jean ^a   Carpentier, Jean Louis ^a   Trono, Didier ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; NEF PROTEIN; VIRUS PROTEIN;

ANTIGEN EXPRESSION; ARTICLE; DOWN REGULATION; ENDOCYTOSIS; HUMAN IMMUNODEFICIENCY VIRUS 1; INTERNALIZATION; LENTIVIRINAE; LYSOSOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION;

EID: 0033515427     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)80715-1     Document Type: Article

References (69)

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 fora critical dileucine motif in the membrane-proximal CD4 cytoplasmic domain. Cell 76, 853-864.
3. 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 downregulation. Virology 217, 293-300.
4. Aniento, F., Gu, F., Parton, R.G., and Gruenberg, J. (1996). An endosomal β COP is involved in the pH-dependent formation of transport vesicles destined for late endosomes. J. Cell Biol. 133, 29-41.
5. Baur, A.S., Sawai, E.T., Dazin, P., Fantl, W.J., Cheng, M.C., and Peterlin, B.M. (1994). HIV-1 Nef leads to inhibition or activation of T cells depending on its intracellular localization. Immunity 7, 373-384.
6. Benichou, S., Bomsel, M., Bodéus, M., Durand, H., Dout́, M., Letourneur, F., Camonis, J., and Benarous, R. (1994). Physical interaction of the HIV-1 Nef protein with β-COP, a component of nonclathrin-coated vesicles essential for membrane traffic. J. Biol. Chem. 269, 30073-30076.
7. Bremser, M., Nickel, W., Schweikert, M., Ravazzola, M., Amherdt, M., Hughes, C.A., Söllner, T.H., Rothman, J.E., and Wieland, F.T. (1999). Coupling of coat assembly and vesicle budding to packaging of putative cargo receptors. Cell 96, 495-506.
8. 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. 8, 1235-1238.
9. Chen, B.K., Gandhi, R.T., and Baltimore, D. (1996). 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. 70, 6044-6053.
10. 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 397, 397-401.
11. Cosson, P., and Letourneur, F. (1994). Coatomer interaction with dilysine endoplasmic reticulum retention motifs. Science 263, 1629-1631.
12. Cosson, P., Lefkir, Y., Demolliere, C., and Letourneur, F. (1998). New COP1-binding motifs involved in ER retrieval. EMBO J. 77, 6863-6870.
13. 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 95, 11229-11234.
14. Cullen, B.R. (1998). HIV-1 auxiliary proteins: making connections in a dying cell. Cell 93, 685-692.
15. Daro, E., Sheff, D., Gomez, M., Kreis, T., and Mellman, I. (1997). Inhibition of endosome function in CHO cells bearing a temperature-sensitive defect in the coatomer (COPI) component ε-COP. J. Cell Biol. 139, 1747-1759.
16. Deacon, N.J., Tsykin, A., Solomon, A., Smith, K., Ludford, M.M., Hooker, D.J., McPhee, D.A., Greenway, A.L., Ellett, A., Chatfield, C., et al. (1995). Genomic structure of an attenuated quasi species of HIV-1 from a blood transfusion donor and recipients. Science 270, 988-991.
17. Demaurex, N., Furuya, W., D'Souza, S., Bonifacino, J.S., and Grinstein, S. (1998). Mechanism of acidification of the trans-Golgi network (TGN). In situ measurements of pH using retrieval of TGN38 and furin from the cell surface. J. Biol. Chem. 273, 2044-2051.
18. Emerman, M., and Malim, M.H. (1998). HIV-1 regulatory/accessory genes: keys to unraveling viral and host cell biology. Science 280, 1880-1884.
19. Foti, M., Mangasarian, A., Piguet, V., Lew, D., Krause, K., Trono, D., and Carpentier, J. (1997). Nef-mediated clathrin coated pit formation. J. Cell Biol. 139, 37-47.
20. Futter, C.E., Pearse, A., Hewlett, L.J., and Hopkins, C.R. (1996). Multivesicular endosomes containing internalized EGF-EGF receptor complexes mature and then fuse directly with lysosomes. J. Cell Biol. 132, 1011-1023.
21. Garcia, J., and Miller, A. (1991). Serine phosphorylation independent downregulation of cell surface CD4 by Nef. Nature 350, 508-511.
22. Geuze, H.J. (1998). The role of endosomes and lysosomes in MHC class II functioning. Immunol. Today 79, 282-287.
23. Green, S.A., Setiadi, H., McEver, R.P., and Kelly, R.B. (1994). The cytoplasmic domain of P-selectin contains a sorting determinant that mediates rapid degradation in lysosomes. J. Cell Biol. 124, 435-448.
24. Greenberg, M., DeTulleo, L, Rapoport, I., Skowronski, J., and Kirchhausen, T. (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.
25. Griffiths, G., Hoflack, B., Simons, K., Mellman, I., and Kornfeld, S. (1988). The mannose 6-phosphate receptor and the biogenesis of lysosomes. Cell 52, 329-341.
26. Gruenberg, J., Griffiths, G., and Howell, K.E. (1989). Characterization of the early endosome and putative endocytic carrier vesicles in vivo and with an assay of vesicle fusion in vitro. J. Cell Biol. 108, 1301-1316.
27. Grzesiek, S., Bax, A., Clore, G.M., Gronenborn, A.M., Hu, J.S., Kaufman, J., Palmer, I., Stahl, S.J., and Wingfield, P.T. (1996a). 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. 3, 340-345.
28. Grzesiek, S., Stahl, S.J., Wingfield, P.T., and Bax, A. (1996b). 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.
29. Gu, F., Aniento, F., Parton, R.G., and Gruenberg, J. (1997). Functional dissection of COP-I subunits in the biogenesis of multivesicular endosomes. J. Cell Biol. 139, 1183-1195.
30. Guy, B., Kieny, M., Riviere, Y., Peuch, C., Dott, K., Girard, M., Montagnier, L, and Lecocq, J. (1987). HIVF/3′ orf encodes a phosphorylated GTP-binding protein resembling an oncogene product. Nature 330, 266-269.
31. Hanna, Z., Kay, D.G., Rebai, N., Guimond, A., Jothy, S., and Jolicoeur, P. (1998). Nef harbors a major determinant of pathogenicity for an AIDS-like disease induced by HIV-1 in transgenic mice. Cell 95, 163-175.
32. Hansen, K., Ronnstrand, L, Rorsman, C., Hellman, U., and Heldin, C.H. (1997). Association of coatomer proteins with the beta-receptor for platelet-derived growth factor. Biochem. Biophys. Res. Commun. 235, 455-460.
33. Hopkins, C.R., Gibson, A., Shipman, M., Strickland, D.K., and Trowbridge, I.S. (1994). In migrating fibroblasts, recycling receptors are concentrated in narrow tubules in the pericentriolar area, and then routed to the plasma membrane of the leading lamella. J. Cell Biol. 725, 1265-1274.
34. 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. 76, 673-684.
35. Kestler, H., Ringler, D., Mori, K., Panicali, D., and Desrosiers, R. (1991). Importance of the Nef gene for maintainance of high viral loads and for development of AIDS. Cell 65, 651-662.
36. 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.
37. Kirchhoff, F., Greenough, T.C., Brettler, D.B., Sullivan, J.L, and Desrosiers, R.C. (1995). Brief report: absence of intact nef sequences in a long-term survivor with nonprogressive HIV-1 infection. N. Engl. J. Med. 332, 228-232.
38. Kobayashi, T., Stang, E., Fang, K.S., de Moerloose, P., Parton, R.G., and Gruenberg, J. (1998). A lipid associated with the antiphospholipid syndrome regulates endosome structure and function. Nature 392, 193-197.
39. Le Gall, S., Erdtmann, L, Benichou, S., Berlioz-Torrent, C., Liu, L, Benarous, R., Heard, J.-M., and Schwarz, O. (1998). Nef interacts with the |j. subunit of clathrin adaptor complexes and reveals a cryptic sorting signal in MHC-I molecules. Immunity 8, 483-495.
40. 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.
41. Letourneur, F., and Klausner, R. (1992). A novel Di-leucine motif and a tyrosine based motif independently mediate lysosomal targeting and endocytosis of CD3 chains. Cell 69, 1143-1157.
42. Letourneur, F., Gaynor, E.C., Hennecke, S., Demolliere, C., Duden, R., Emr, S.D., Riezman, H., and Cosson, P. (1994). Coatomer is essential for retrieval of dilysine-tagged proteins to the endoplasmic reticulum. Cell 79, 1199-1207.
43. Lu, X., Yu, H., Liu, S., Brodsky, F.M., and Peterlin, B.M. (1998). Interactions between HIV1 Nef and vacuolar ATPase facilitate the internalization of CD4. Immunity 8, 647-656.
44. Maddon, P., Dalgleish, A., McDougal, J., Clapham, P., Weiss, R., and Axel, R. (1986). The T4 gene encodes the AIDS virus receptor and is expressed in the immune system and the brain. Cell 47, 333-348.
45. 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.
46. Mangasarian, A., Piguet, V., Wang, J.K., Chen, Y., and Trono, D. (1999). Nef-induced CD4 and MHC-I downregulation are governed by distinct determinants: N-terminal alpha-helix and proline repeat of Nef selectively regulate MHC-I trafficking. J. Virol. 73,1964-1973.
47. Marks, M.S., Roche, P.A., van Donselaar, E., Woodruff, L., Peters, P.J., and Bonifacino, J.S. (1995). A lysosomal targeting signal in the cytoplasmic tail of the beta chain directs HLA-DM to MHC class II compartments. J. Cell Biol. 737, 351-369.
48. Matter, K., Yamamoto, E.M., and Mellman, I. (1994). Structural requirements and sequence motifs for polarized sorting and endocytosis of LDL and Fc receptors in MDCK cells. J. Cell Biol. 726, 991-1004.
49. Mukherjee, S., Ghosh, R.N., and Maxfield, F.R. (1997). Endocytosis. Physiol. Rev. 77, 759-803.
50. Niederman, T.M., Hastings, W.R., and Ratner, L. (1993). Myristoylation-enhanced binding of the HIV-1 Nef protein to T cell skeletal matrix. Virology 797, 420-425.
51. Oldridge, J., and Marsh, M. (1998). Nef-an adaptor adaptor?Trends Cell Biol. 8, 302-305.
52. Opresko, L.K., Chang, C.P., Will, B.H., Burke, P.M., Gill, G.N., and Wiley, H.S. (1995). Endocytosis and lysosomal targeting of epidermal growth factor receptors are mediated by distinct sequences independent of the tyrosine kinase domain. J. Biol. Chem. 270, 4325-4333.
53. Orci, L, Palmer, D.U., Ravazzola, M., Perrelet, A., Amherdt, M., and Rothman, J.E. (1993). Budding from Golgi membranes requires the coatomer complex of non-clathrin coat proteins. Nature 362, 648-652.
54. Pelchen-Matthews, A., Armes, J., and Marsh, M. (1989). Internalization and recycling of CD4 transfected into HeLa and NIH3T3 cells. J. Exp. Med. 8, 3641-3649.
55. Pepperkok, R., Scheel, J., Horstmann, H., Hauri, H.P., Griffiths, G., and Kreis, T.E. (1993). ß-COP is essential for biosynthetic membrane transport from the endoplasmic reticulum to the Golgi complex in vivo. Cell 74, 71-82.
56. Peters, C., Braun, M., Weber, B., Wendland, M., Schmidt, B., Pohlmann, R., Waheed, A., and von Figura, K. (1990). Targeting of a lysosomal membrane protein: a tyrosine-containing endocytosis signal in the cytoplasmic tail of lysosomal acid phosphatase is necessary and sufficient for targeting to lysosomes. EM BO J. 9, 3497-3506.
57. Piguet, V., Chen, Y.-L, Mangasarian, A., Foti, M., Carpentier, J., and Trono, D. (1998). Mechanism of Nef induced CD4 endocytosis: Nef connects CD4 with the μ chain of adaptor complexes. EMBO J. 17, 2472-2481.
58. Pond, L, Kuhn, LA., Teyton, L, Schutze, M.P., Tainer, J.A., Jackson, M.R., and Peterson, P.A. (1995). A role for acidic residues in dileucine motif-based targeting to the endocytic pathway. J. Biol. Chem. 270, 19989-19997.
59. Radhakrishna, H., and Donaldson, J.G. (1997). ADP-ribosylationfactor 6 regulates a novel plasma membrane recycling pathway. J. Cell Biol. 739, 49-61.
60. 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.
61. Robinson, M.S. (1994). The role of clathrin, adaptors and dynamin in endocytosis. Curr. Opin. Cell Biol. 6, 538-544.
62. Schwartz, O., Maréchal, V., Danos, O., and Heard, J.M. (1995). Human immunodeficiency virus type 1 Nef increases the efficiency of reverse transcription in the infected cell. J. Virol. 69, 4053-4059.
63. Schwartz, O., Maréchal, V., Le Gall, S., Lemonnier, F., and Heard, J.M. (1996). Endocytosis of major histocompatibility complex class I molecules is induced by the HIV-1 Nef protein. Nat. Med. 2,338-342.
64. Subtil, A., Delepierre, M., and Dautry-Varsat, A. (1997). An alpha-helical signal in the cytosolic domain of the interleukin 2 receptor beta chain mediates sorting towards degradation after endocytosis. J. Cell Biol. 736, 583-595.
65. Tooze, J., and Hollinshead, M. (1991 ). Tubular early endosomal networks in AtT20 and other cells. J. Cell Biol. 775, 635-653.
66. Voorhees, P., Deignan, E., van Donselaar, E., Humphrey, J., Marks, M.S., Peters, P.J., and Bonifacino, J.S. (1995). An acidic sequence within the cytoplasmic domain of furin functions as a determinant of trans-Golgi network localization and internalization from the cell surface. EMBO J. 14, 4961-4975.
67. Wan, L, Molloy, S.S., Thomas, L, Liu, G., Xiang, Y., Rybak, S.L, and Thomas, G. (1998). PACS-1 defines a novel gene family of cytosolic sorting proteins required for trans-Golgi network localization. Cell 94, 205-216.
68. Weiss, A., and Littman, D. (1994). Signal transduction by lymphocyte antigen receptors. Cell 76, 263-274.
69. Whitney, J.A., Gomez, M., Sheff, D., Kreis, T.E., and Mellman, I. (1995). Cytoplasmic coat proteins involved in endosome function. Cell 83, 703-713.