HIV-1 Nef downregulates MHC-I by a PACS-1- and PI3K-regulated ARF6 endocytic pathway

Cell

Volumn 111, Issue 6, 2002, Pages 853-866

  Blagoveshchenskaya, Anastassia D ^a   Thomas, Laurel ^a   Feliciangeli, Sylvain F ^a   Hung, Chien Hui ^a   Thomas, Gary ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NEF PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN; PROTEIN PACS 1; PROTEIN SH3; UNCLASSIFIED DRUG;

ANIMAL CELL; BINDING SITE; CELL SURFACE; CONTROLLED STUDY; DOWN REGULATION; ENDOCYTOSIS; GOLGI COMPLEX; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOSURVEILLANCE; INTERNALIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN TARGETING; REVIEW;

ANIMALIA; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; RNA VIRUSES;

EID: 0037074008     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(02)01162-5     Document Type: Article

References (49)

1. Baur A.S., Sass G., Laffert B., Willbold D., Cheng-Mayer C., Peterlin B.M. The N-terminus of Nef from HIV-1/SIV associates with a protein complex containing Lck and a serine kinase. Immunity. 6:1997;283-291.
2. 2+ and the beta-phosphate to destabilize GDP on ARF1. EMBO J. 17:1998;3651-3659.
3. Blagoveshchenskaya A.D., Hewitt E.W., Cutler D.F. A balance of opposing signals within the cytoplasmic tail controls the lysosomal targeting of P-selectin. J. Biol. Chem. 273:1998;27896-27903.
4. Blagoveshchenskaya A.D., Hewitt E.W., Cutler D.F. Di-leucine signals mediate targeting of tyrosinase and synaptotagmin to synaptic-like microvesicles within PC12 cells. Mol. Biol. Cell. 10:1999;3979-3990.
5. Capps G.G., Zuniga M.C. Phosphorylation of class I MHC molecules in the absence of phorbol esters is an intracellular event and may be characteristic of trafficking molecules. Mol. Immunol. 37:2000;59-71.
6. Carl S., Greenough T.C., Krumbiegel M., Greenberg M., Skowronski J., Sullivan J.L., Kirchhoff F. Modulation of different human immunodeficiency virus type 1 Nef functions during progression to AIDS. J. Virol. 75:2001;3657-3665.
7. Carreno S., Gouze M.E., Schaak S., Emorine L.J., Maridonneau-Parini I. Lack of palmitoylation redirects p59Hck from the plasma membrane to p61Hck-positive lysosomes. J. Biol. Chem. 275:2000;36223-36229.
8. Chang A.H., O'Shaughnessy M.V., Jirik F.R. Hck SH3 domain-dependent abrogation of Nef-induced class 1 MHC down-regulation. Eur. J. Immunol. 31:2001;2382-2387.
9. Chavrier P., Goud B. The role of ARF and Rab GTPases in membrane transport. Curr. Opin. Cell Biol. 11:1999;466-475.
10. Claing A., Chen W., Miller W.E., Vitale N., Moss J., Premont R.T., Lefkowitz R.J. beta-arrestin-mediated ADP-ribosylation factor 6 activation and beta 2-adrenergic receptor endocytosis. J. Biol. Chem. 276:2001;42509-42513.
11. Cohen G.B., Gandhi R.T., Davis D.M., Mandelboim O., Chen B.K., Strominger J.L., Baltimore D. The selective downregulation of class I major histocompatibility complex proteins by HIV-1 protects HIV-infected cells from NK cells. Immunity. 10:1999;661-671.
12. Collins K.L., Chen B.K., Kalams S.A., Walker B.D., Baltimore D. HIV-1 Nef protein protects infected primary cells against killing by cytotoxic T lymphocytes. Nature. 391:1998;397-401.
13. Coscoy L., Ganem D. Kaposi's sarcoma-associated herpesvirus encodes two proteins that block cell surface display of MHC class I chains by enhancing their endocytosis. Proc. Natl. Acad. Sci. USA. 97:2000;8051-8056.
14. Crump C.M., Xiang Y., Thomas L., Gu F., Austin C., Tooze S.A., Thomas G. PACS-1 binding to adaptors is required for acidic cluster motif-mediated protein traffic. EMBO J. 20:2001;2191-2201.
15. Doms R.W., Trono D. The plasma membrane as a combat zone in the HIV battlefield. Genes Dev. 14:2000;2677-2688.
16. Dyer W.B., Ogg G.S., Demoitie M.A., Jin X., Geczy A.F., Rowland-Jones S.L., McMichael A.J., Nixon D.F., Sullivan J.S. Strong human immunodeficiency virus (HIV)-specific cytotoxic T-lymphocyte activity in Sydney Blood Bank Cohort patients infected with nef-defective HIV type 1. J. Virol. 73:1999;436-443.
17. Fackler O.T., Baur A.S. Live and let die. Nef functions beyond HIV replication. Immunity. 16:2002;493-497.
18. Geyer M., Fackler O.T., Peterlin B.M. Structure-function relationships in HIV-1 Nef. EMBO Rep. 2:2001;580-585.
19. Greenberg M.E., Iafrate A.J., Skowronski J. The SH3 domain-binding surface and an acidic motif in HIV-1 Nef regulate trafficking of class I MHC complexes. EMBO J. 17:1998;2777-2789.
20. Gromme M., Uytdehaag F.G., Janssen H., Calafat J., van Binnendijk R.S., Kenter M.J., Tulp A., Verwoerd D., Neefjes J. Recycling MHC class I molecules and endosomal peptide loading. Proc. Natl. Acad. Sci. USA. 96:1999;10326-10331.
21. Hitt M.M., Addison C.L., Graham F.L. Human adenovirus vectors for gene transfer into mammalian cells. Adv. Pharmacol. 40:1997;137-206.
22. Jondal M., Schirmbeck R., Reimann J. MHC class I-restricted CTL responses to exogenous antigens. Immunity. 5:1996;295-302.
23. Kedl R.M., Schaefer B.C., Kappler J.W., Marrack P. T cells down-modulate peptide-MHC complexes on APCs in vivo. Nat. Immunol. 3:2002;27-32.
24. Langille S.E., Patki V., Klarlund J.K., Buxton J.M., Holik J.J., Chawla A., Corvera S., Czech M.P. ADP-ribosylation factor 6 as a target of guanine nucleotide exchange factor GRP1. J. Biol. Chem. 274:1999;27099-27104.
25. Le Gall S., Erdtmann L., Benichou S., Berlioz-Torrent C., Liu L., Benarous R., Heard J.M., Schwartz O. Nef interacts with the mu subunit of clathrin adaptor complexes and reveals a cryptic sorting signal in MHC I molecules. Immunity. 8:1998;483-495.
26. Le Gall S., Buseyne F., Trocha A., Walker B.D., Heard J.M., Schwartz O. Distinct trafficking pathways mediate Nef-induced and clathrin-dependent major histocompatibility complex class I down-regulation. J. Virol. 74:2000;9256-9266.
27. Lerner E.C., Smithgall T.E. SH3-dependent stimulation of Src-family kinase autophosphorylation without tail release from the SH2 domain in vivo. Nat. Struct. Biol. 9:2002;365-369.
28. Linnemann T., Zheng Y.H., Mandic R., Peterlin B.M. Interaction between Nef and phosphatidylinositol-3-kinase leads to activation of p21-activated kinase and increased production of HIV. Virology. 294:2002;246-255.
29. Mangasarian A., Piguet V., Wang J.K., Chen Y.L., Trono D. 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. 73:1999;1964-1973.
30. Marsh M., Pelchen-Matthews A. Endocytosis in viral replication. Traffic. 1:2000;525-532.
31. Matafora V., Paris S., Dariozzi S., de Curtis I. Molecular mechanisms regulating the subcellular localization of p95-APP1 between the endosomal recycling compartment and sites of actin organization at the cell surface. J. Cell Sci. 114:2001;4509-4520.
32. Munch J., Stolte N., Fuchs D., Stahl-Hennig C., Kirchhoff F. Efficient class I major histocompatibility complex down-regulation by simian immunodeficiency virus Nef is associated with a strong selective advantage in infected rhesus macaques. J. Virol. 75:2001;10532-10536.
33. Nesterov A., Carter R.E., Sorkina T., Gill G.N., Sorkin A. Inhibition of the receptor-binding function of clathrin adaptor protein AP-2 by dominant-negative mutant mu2 subunit and its effects on endocytosis. EMBO J. 18:1999;2489-2499.
34. Ostergaard H.L., Lou O., Arendt C.W., Berg N.N. Paxillin phosphorylation and association with Lck and Pyk2 in anti-CD3- or anti-CD45-stimulated T cells. J. Biol. Chem. 273:1998;5692-5696.
35. Peters P.J., Gao M., Gaschet J., Ambach A., van Donselaar E., Traverse J.F., Bos E., Wolffe E.J., Hsu V.W. Characterization of coated vesicles that participate in endocytic recycling. Traffic. 2:2001;885-895.
36. Piguet V., Gu F., Foti M., Demaurex N., Gruenberg J., Carpentier J.L., Trono D. Nef-induced CD4 degradation. a diacidic-based motif in Nef functions as a lysosomal targeting signal through the binding of beta-COP in endosomes Cell. 97:1999;67-73.
37. Piguet V., Wan L., Borel C., Mangasarian A., Demaurex N., Thomas G., Trono D. HIV-1 Nef protein binds to the cellular protein PACS-1 to downregulate class I major histocompatibility complexes. Nat. Cell Biol. 2:2000;163-167.
38. Ploegh H.L. Viral strategies of immune evasion. Science. 280:1998;248-253.
39. Radhakrishna H., Donaldson J.G. ADP-ribosylation factor 6 regulates a novel plasma membrane recycling pathway. J. Cell Biol. 139:1997;49-61.
40. Radhakrishna H., Klausner R.D., Donaldson J.G. Aluminum fluoride stimulates surface protrusions in cells overexpressing the ARF6 GTPase. J. Cell Biol. 134:1996;935-947.
41. Reid P.A., Watts C. Cycling of cell-surface MHC glycoproteins through primaquine-sensitive intracellular compartments. Nature. 346:1990;655-657.
42. Schibeci S.D., Clegg A.O., Biti R.A., Sagawa K., Stewart G.J., Williamson P. HIV-Nef enhances interleukin-2 production and phosphatidylinositol 3-kinase activity in a human T cell line. AIDS. 14:2000;1701-1707.
43. Swann S.A., Williams M., Story C.M., Bobbitt K.R., Fleis R., Collins K.L. HIV-1 Nef blocks transport of MHC class I molecules to the cell surface via a PI 3-kinase-dependent pathway. Virology. 282:2001;267-277.
44. Tortorella D., Gewurz B.E., Furman M.H., Schust D.J., Ploegh H.L. Viral subversion of the immune system. Annu. Rev. Immunol. 18:2000;861-926.
45. Venkateswarlu K., Cullen P.J. Signalling via ADP-ribosylation factor 6 lies downstream of phosphatidylinositide 3-kinase. Biochem. J. 345:2000;719-724.
46. Venkateswarlu K., Oatey P.B., Tavare J.M., Cullen P.J. Insulin-dependent translocation of ARNO to the plasma membrane of adipocytes requires phosphatidylinositol 3-kinase. Curr. Biol. 8:1998;463-466.
47. Wan L., Molloy S.S., Thomas L., Liu G., Xiang Y., Rybak S.L., Thomas G. PACS-1 defines a novel gene family of cytosolic sorting proteins required for trans-Golgi network localization. Cell. 94:1998;205-216.
48. Xu X.N., Laffert B., Screaton G.R., Kraft M., Wolf D., Kolanus W., Mongkolsapay J., McMichael A.J., Baur A.S. Induction of Fas ligand expression by HIV involves the interaction of Nef with the T cell receptor zeta chain. J. Exp. Med. 189:1999;1489-1496.
49. Zhang Q., Cox D., Tseng C.C., Donaldson J.G., Greenberg S. A requirement for ARF6 in Fcgamma receptor-mediated phagocytosis in macrophages. J. Biol. Chem. 273:1998;19977-19981.