HIV Nef-mediated Major Histocompatibility Complex Class I Down-Modulation is Independent of Arf6 Activity

Molecular Biology of the Cell

Volumn 15, Issue 1, 2004, Pages 323-331

  Larsen, Jakob E ^a   Massol, Ramiro H ^a   Nieland, Thomas J F ^a   Kirchhausen, Tomas ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARF PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MUTANT PROTEIN; NEF PROTEIN; PHOSPHATIDYLINOSITOL 3 PHOSPHATE KINASE; PHOSPHOTRANSFERASE; UNCLASSIFIED DRUG;

ARTICLE; ASTROCYTOMA CELL; DOWN REGULATION; EMBRYO; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; INTERNALIZATION; KIDNEY CELL; LYMPHATIC LEUKEMIA; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; TRANS GOLGI NETWORK;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ADP-RIBOSYLATION FACTORS; CELLS, CULTURED; CLATHRIN; CLONING, MOLECULAR; DOWN-REGULATION; ENDOCYTOSIS; ENZYME ACTIVATION; FLOW CYTOMETRY; GENES, MHC CLASS I; GENES, NEF; GOLGI APPARATUS; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; HIV; HUMANS; JURKAT CELLS; MUTATION; PROTEIN TRANSPORT;

HUMAN IMMUNODEFICIENCY VIRUS;

EID: 0347990558     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E03-08-0578     Document Type: Article

References (44)

1. Akari, H., Arold, S., Fukumori, T., Okazaki, T., Strebel, K., and Adachi, A. (2000). Nef-induced major histocompatibility complex class I down-regulation is functionally dissociated from its virion incorporation, enhancement of viral infectivity, and CD4 down-regulation. J. Virol. 74, 2907-2912.
2. Arold, S., Franken, P., Strub, M.P., Hoh, F., Benichou, S., Benarous, R., and Dumas, C. (1997). The crystal structure of HIV-1 Nef protein bound to the Fyn kinase SH3 domain suggests a role for this complex in altered T cell receptor signaling. Structure 5, 1361-1372.
3. Benmerah, A., Bayrou, M., Cerf-Bensussan, N., and Dautry-Varsat, A. (1999). Inhibition of clathrin-coated pit assembly by an Eps15 mutant. J. Cell Sci. 112, 1303-1311.
4. Blagoveshchenskaya, A.D., Thomas, L., Feliciangeli, S.F., Hung, C.H., and Thomas, G. (2002). HIV-1 Nef downregulates MHC-I by a PACS-1- and PI3K-regulated ARF6 endocytic pathway. Cell 111, 853-866.
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. 8, 1235-1238.
6. Brown, F.D., Rozelle, A.L., Yin, H.L., Balla, T., and Donaldson, J.G. (2001). Phosphatidylinositol 4, 5-bisphosphate and Arf6-regulated membrane traffic. J. Cell Biol. 154, 1007-1017.
7. Campbell, R.E., Tour, O., Palmer, A.E., Steinbach, P.A., Baird, G.S., Zacharias, D.A., and Tsien, R.Y. (2002). A monomeric red fluorescent protein. Proc. Natl. Acad. Sci. USA 99, 7877-7882.
8. Caplan, S., Naslavsky, N., Hartnell, L.M., Lodge, R., Polishchuk, R.S., Donaldson, J.G., and Bonifacino, J.S. (2002). A tubular EHD1-containing compartment involved in the recycling of major histocompatibility complex class I molecules to the plasma membrane. EMBO J. 21, 2557-2567.
9. Cohen, G.B., Gandhi, R.T., Davis, D.M., Mandelboim, O., Chen, B.K., Strominger, J.L., and Baltimore, D. (1999). The selective downregulation of class I major histocompatibility complex proteins by HIV-1 protects HIV-infected cells from NK cells. Immunity 10, 661-671.
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 391, 397-401.
11. Crump, C.M., Xiang, Y., Thomas, L., Gu, F., Austin, C., Tooze, S.A., and Thomas, G. (2001). PACS-1 binding to adaptors is required for acidic cluster motif-mediated protein traffic. EMBO J. 20, 2191-2201.
12. D'Souza-Schorey, C., Li, G., Colombo, M.I., and Stahl, P.D. (1995). A regulatory role for ARF6 in receptor-mediated endocytosis. Science 267, 1175-1178.
13. Fackler, O.T., Luo, W., Geyer, M., Alberts, A.S., and Peterlin, B.M. (1999). Activation of Vav by Nef induces cytoskeletal rearrangements and downstream effector functions. Mol. Cell 3, 729-739.
14. Galperin, E., Benjamin, S., Rapaport, D., Rotem-Yehudar, R., Tolchinsky, S., and Horowitz, M. (2002). EHD 3, a protein that resides in recycling tubular and vesicular membrane structures and interacts with EHD1. Traffic 3, 575-589.
15. 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. 8, 1239-1242.
16. 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.
17. 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.
18. 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. Nat. Struct. Biol. 3, 340-345.
19. Ktistakis, N.T., Brown, H.A., Waters, M.G., Sternweis, P.C., and Roth, M.G. (1996). Evidence that phospholipase D mediates ADP ribosylation factor-dependent formation of Golgi coated vesicles. J. Cell Biol. 134, 295-306.
20. Lauvrak, S.U., Llorente, A., Iversen, T.G., and Sandvig, K. (2002). Selective regulation of the Rab9-independent transport of ricin to the Golgi apparatus by calcium. J. Cell Sci. 115, 3449-3456.
21. Le Gall, S., Buseyne, F., Trocha, A., Walker, B.D., Heard, J.M., and Schwartz, O. (2000). Distinct trafficking pathways mediate Nef-induced and clathrin-dependent major histocompatibility complex class I down-regulation. J. Virol. 74, 9256-9266.
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. Legesse-Miller, A., Massol, R.H., and Kirchhausen, T. (2003). Constriction and dnm1p recruitment are distinct processes in mitochondrial fission. Mol. Biol. Cell 14, 1953-1963.
24. Liu, X., Schrager, J.A., Lange, G.D., and Marsh, J.W. (2001). HIV Nef-mediated cellular phenotypes are differentially expressed as a function of intracellular Nef concentrations. J. Biol. Chem. 276, 32763-32770.
25. Machy, P., Truneh, A., Gennaro, D., and Hoffstein, S. (1987). Major histocompatibility complex class I molecules internalized via coated pits in T lymphocytes. Nature 328, 724-726.
26. Mangasarian, A., Piguet, V., Wang, J.K., Chen, Y.L., and Trono, D. (1999). 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. J. Virol. 73, 1964-1973.
27. Massenburg, D., Han, J.S., Liyanage, M., Patton, W.A., Rhee, S.G., Moss, J., and Vaughan, M. (1994). Activation of rat brain phospholipase D by ADP-ribosylation factors 1, 5, and 6, separation of ADP-ribosylation factor-dependent and oleate-dependent enzymes. Proc. Natl. Acad. Sci. USA 91, 11718-11722.
28. Naslavsky, N., Weigert, R., and Donaldson, J.G. (2003). Convergence of non-clathrin- and clathrin-derived endosomes involves Arf6 inactivation and changes in phosphoinositides. Mol. Biol. Cell 14, 417-431.
29. Pear, W.S., et al. (1998). Efficient and rapid induction of a chronic myelogenous leukemia-like myeloproliferative disease in mice receiving P210 bcr/abl-transduced bone marrow. Blood 92, 3780-3792.
30. Pear, W.S., Nolan, G.P., Scott, M.L., and Baltimore, D. (1993). Production of high-titer helper-free retroviruses by transient transfection. Proc. Natl. Acad. Sci. USA 90, 8392-8396.
31. Piguet, V., Wan, L., Borel, C., Mangasarian, A., Demaurex, N., Thomas, G., and Trono, D. (2000). HIV-1 Nef protein binds to the cellular protein PACS-1 to downregulate class I major histocompatibility complexes. Nat. Cell Biol. 2, 163-167.
32. Radhakrishna, H., and Donaldson, J.G. (1997). ADP-ribosylation factor 6 regulates a novel plasma membrane recycling pathway. J. Cell Biol. 139, 49-61.
33. Saksela, K., Cheng, G., and Baltimore, D. (1995). Proline-rich (PxxP) motifs in HIV-1 Nef bind to SH3 domains of a subset of Src kinases and are required for the enhanced growth of Nef+ viruses but not for down-regulation of CD4. EMBO J. 14, 484-491.
34. Santy, L.C. (2002). Characterization of a fast cycling ADP-ribosylation factor 6 mutant. J. Biol. Chem. 277, 40185-40188.
35. 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 the HIV-1 Nef protein. Nat. Med. 2, 338-342.
36. Shen, Y., Xu, L., and Foster, D.A. (2001). Role for phospholipase D in receptor-mediated endocytosis. Mol. Cell. Biol. 21, 595-602.
37. Soneoka, Y., Cannon, P.M., Ramsdale, E.E., Griffiths, J.C., Romano, G., Kingsman, S.M., and Kingsman, A.J. (1995). A transient three-plasmid expression system for the production of high titer retroviral vectors. Nucleic Acids Res. 23, 628-633.
38. Spiro, D.J., Boll, W., Kirchhausen, T., and Wessling-Resnick, M. (1996). Wortmannin alters the transferrin receptor endocytic pathway in vivo and in vitro. Mol. Biol. Cell 7, 355-367.
39. Swann, S.A., Williams, M., Story, C.M., Bobbitt, K.R., Fleis, R., and Collins, K.L. (2001). HIV-1 Nef blocks transport of MHC class I molecules to the cell surface via a PI 3-kinase-dependent pathway. Virology 282, 267-277.
40. Swigut, T., Iafrate, A.J., Muench, J., Kirchhoff, F., and Skowronski, J. (2000). Simian and human immunodeficiency virus Nef proteins use different surfaces to downregulate class I major histocompatibility complex antigen expression. J. Virol. 74, 5691-5701.
41. Swigut, T., Shohdy, N., and Skowronski, J. (2001). Mechanism for downregulation of CD28 by Nef. EMBO J. 20, 1593-1604.
42. Vitale, N., Chasserot-Golaz, S., Bailly, Y., Morinaga, N., Frohman, M.A., and Bader, M.F. (2002). Calcium-regulated exocytosis of dense-core vesicles requires the activation of ADP-ribosylation factor (ARF)6 by ARF nucleotide binding site opener at the plasma membrane. J. Cell Biol. 159, 79-89.
43. Weber, K.S., Weber, C., Ostermann, G., Dierks, H., Nagel, W., and Kolanus, W. (2001). Cytohesin-1 is a dynamic regulator of distinct LFA-1 functions in leukocyte arrest and transmigration triggered by chemokines. Curr. Biol. 11, 1969-1974.
44. Zhang, Q., Cox, D., Tseng, C.C., Donaldson, J.G., and Greenberg, S. (1998). A requirement for ARF6 in Fcgamma receptor-mediated phagocytosis in macrophages. J. Biol. Chem. 273, 19977-19981.