Membrane raft association of the Vpu protein of human immunodeficiency virus type 1 correlates with enhanced virus release

Virology

Volumn 408, Issue 1, 2010, Pages 89-102

  Ruiz, Autumn ^a   Hill, M Sarah ^a   Schmitt, Kimberly ^a   Stephens, Edward B ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

CD4 down regulation; HIV 1; Lipid rafts; Membrane rafts; Virus release; Vpu

Indexed keywords

BETA CYCLODEXTRIN; CHOLESTEROL; MEVINOLIN; MUTANT PROTEIN; VPU PROTEIN;

ARTICLE; CD4+ T LYMPHOCYTE; CELL MEMBRANE; CONTROLLED STUDY; DOWN REGULATION; HELA CELL; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; LIPID RAFT; MEMBRANE RESISTANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; VIRION;

ANTICHOLESTEREMIC AGENTS; CELL LINE; CHOLESTEROL; HIV-1; HUMAN IMMUNODEFICIENCY VIRUS PROTEINS; HUMANS; LOVASTATIN; MEMBRANE MICRODOMAINS; VIRAL REGULATORY AND ACCESSORY PROTEINS; VIRUS RELEASE;

HUMAN IMMUNODEFICIENCY VIRUS 1; SIMIAN-HUMAN IMMUNODEFICIENCY VIRUS;

EID: 78049268481     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2010.08.031     Document Type: Article

References (59)

1. Alfalah M., Wetzel G., Fischer I., Busche R., Sterchi E.E., Zimmer K.P., Sallmann H.P., Naim H.Y. A novel type of detergent-resistant membranes may contribute to an early protein sorting event in epithelial cells. J. Biol. Chem. 2005, 280:42636-42643.
2. Aloia R.C., Tian H., Jensen F.C. Lipid composition and fluidity of the human immunodeficiency virus envelope and host cell plasma membranes. Proc. Natl. Acad. Sci. USA 1993, 90:5181-5185.
3. Barman S., Nayak D.P. Analysis of the transmembrane domain of influenza virus neuraminidase, a type II transmembrane glycoprotein, for apical sorting and raft association. J. Virol. 2000, 74:6538-6545.
4. Bavari S., Bosio C.M., Wiegand E., Ruthel G., Will A.B., Geisbert T.W., Hevey M., Schmaljohn C., Schmaljohn A., Aman M.J. Lipid raft microdomains: a gateway for compartmentalized trafficking of Ebola and Marburg viruses. J. Exp. Med. 2002, 195:593-602.
5. Bender F.C., Whitbeck J.C., Ponce de Leon M., Lou H., Eisenberg R.J., Cohen G.H. Specific association of glycoprotein B with lipid rafts during herpes simplex virus entry. J. Virol. 2003, 77:9542-9552.
6. Bhattacharya J., Peters P.J., Clapham P.R. Human immunodeficiency virus type 1 envelope glycoproteins that lack cytoplasmic domain cysteines: impact on association with membrane lipid rafts and incorporation onto budding virus particles. J. Virol. 2004, 78:5500-5506.
7. Bhattacharya J., Repik A., Clapham P.R. Gag regulates association of human immunodeficiency virus type 1 envelope with detergent-resistant membranes. J. Virol. 2006, 80:5292-5300.
8. Browman D.T., Resek M.E., Zajchowski L.D., Robbins S.M. Erlin-1 and erlin-2 are novel members of the prohibitin family of proteins that define lipid-raft-like domains of the ER. J. Cell Sci. 2006, 119:3149-3160.
9. Brown E.L., Lyles D.S. Organization of the vesicular stomatitis virus glycoprotein into membrane microdomains occurs independently of intracellular viral components. J. Virol. 2003, 77:3985-3992.
10. Brugger B., Glass B., Haberkant P., Leibrecht I., Wieland F.T., Krausslich H.-G. The HIV lipidome: a raft with an unusual composition. Proc. Natl. Acad. Sci. USA 2005, 103:2641-2646.
11. Candler A., Featherstone M., Ali R., Maloney L., Watts A., Fischer W.B. Computational analysis of mutations in the transmembrane region of Vpu from HIV-1. Biochim. Biophys. Acta 2005, 1716:1-10.
12. Chan W.E., Lin H.H., Chen S.S. Wild-type-like viral replication potential of human immunodeficiency virus type 1 envelope mutants lacking palmitoylation signals. J. Virol. 2005, 79:8374-8387.
13. Chen X., Jen A., Warley A., Lawrence M.J., Quinn P.J., Morris R.J. Isolation at physiological temperature of detergent-resistant membranes with properties expected of lipid rafts: the influence of buffer composition. Biochem. J. 2009, 417:525-533.
14. Chung C.S., Huang C.Y., Chang W. Vaccinia virus penetration requires cholesterol and results in specific viral envelope proteins associated with lipid rafts. J. Virol. 2005, 79:1623-1634.
15. Douglas J.L., Viswanathan K., McCarroll M.N., Gustin J.K., Früh K., Moses A.V. Vpu directs the degradation of the human immunodeficiency virus restriction factor BST-2/Tetherin via a β-TrCP-dependent mechanism. J. Virol. 2009, 83:7931-7947.
16. Drevot P., Langlet C., Guo X.J., Bernard A.M., Colard O., Chauvin J.P., Lasserre R., He H.T. TCR signal initiation machinery is pre-assembled and activated in a subset of membrane rafts. EMBO J. 2002, 21:1899-1908.
17. Dubé M., Roy B.B., Guiot-Guillain P., Mercier J., Binette J., Leung G., Cohen E.A. Suppression of Tetherin-restricting activity upon human immunodeficiency virus type 1 particle release correlates with localization of Vpu in the trans-Golgi network. J. Virol. 2009, 83:4574-4590.
18. Epand R.F., Thomas A., Brasseur R., Vishwanathan S.A., Hunter E., Epand R.M. Juxtamembrane protein segments that contribute to recruitment of cholesterol into domains. Biochemistry 2006, 45:6105-6114.
19. Fujita K., Omura S., Silver J. Rapid degradation of CD4 in cells expressing human immunodeficiency virus type 1 Env and Vpu is blocked by proteasome inhibitors. J. Gen. Virol. 1997, 78:619-625.
20. Gkantiragas I., Brügger B., Stüven E., Kaloyanova D., Li X.Y., Löhr K., Lottspeich F., Wieland F.T., Helms J.B. Sphingomyelin-enriched microdomains at the Golgi complex. Mol. Biol. Cell 2001, 12:1819-1833.
21. cpz strains. Virology 2005, 335:46-60.
22. TM) that is less pathogenic for pig-tailed macaques. Virology 2005, 339:56-69.
23. Keller P., Simons K. Cholesterol is required for surface transport of influenza virus hemagglutinin. J. Cell Biol. 1998, 140:1357-1367.
24. Klimkait T., Strebel K., Hoggan M.D., Martin M.A., Orenstein J.M. The human immunodeficiency virus type 1-specific protein Vpu is required for efficient virus maturation and release. J. Virol. 1990, 64:621-629.
25. Knorr R., Karacsonyi C., Lindner R.J. Endocytosis of MHC molecules by distinct membrane rafts. Cell Sci. 2009, 122:1584-1594.
26. Kruger J., Fischer W.B. Exploring the conformational space of Vpu from HIV-1: a versatile adaptable protein. J. Comput. Chem. 2008, 29:2416-2424.
27. Kupzig S., Korolchuk V., Rollason R., Sugden A., Wilde A., Banting G. Bst-2/HM1.24 is a raft-associated apical membrane protein with an unusual topology. Traffic 2003, 4:694-709.
28. Kusumi A., Suzuki K. Toward understanding the dynamics of membrane-raft-based molecular interactions. Biochim. Biophys. Acta 2005, 1746:234-251.
29. Li M., Yang C., Tong S., Weidmann A., Compans R.W. Palmitoylation of the murine leukemia virus envelope protein is critical for lipid raft association and surface expression. J. Virol. 2002, 76:11845-11852.
30. Manié S.N., de Breyne S., Vincent S., Gerlier D. Measles virus structural components are enriched intolipid raft microdomains: a potential cellular location for virus assembly. J. Virol. 2000, 74:305-311.
31. Marty A., Meanger J., Mills J., Shields B., Ghildyal R. Association of matrix protein of respiratory syncytial virus with the host cell membrane of infected cells. Arch. Virol. 2004, 149:199-210.
32. + T cell loss and neuroAIDS in pig-tailed macaques. Virology 2000, 272:112-126.
33. Medigeshi G.R., Hirsch A.J., Streblow D.N., Nikolich-Zugich J., Nelson J.A. West Nile virus entry requires cholesterol-rich membrane microdomains and is independent of alphavbeta3 integrin. J. Virol. 2008, 82:5212-5219.
34. Neil S.J., Zang T., Bieniasz P.D. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 2008, 451:425-430.
35. Nguyen D.H., Hildreth J.E. Evidence for budding of human immunodeficiency virus type 1 selectively from glycolipid-enriched membrane lipid rafts. J. Virol. 2000, 74:3264-3272.
36. Nguyen K.-L., Llano M., Akari H., Miyagi E., Poeschla E.M., Strebel K., Bour S. Codon optimization of the HIV-1 vpu and vif genes stabilizes their messenger RNA and allows for highly efficient Rev-independent expression. Virology 2004, 319:163-175.
37. Ono A., Freed E.O. Plasma membrane rafts play a critical role in HIV-1 assembly and release. Proc. Natl. Acad. Sci. USA 2001, 98:13925-13930.
38. Pacyniak E., Gomez M., Gomez L., Mulcahy E., Jackson M., Flick M., Hout D.R., Stephens E.B. Identification of a region within the cytoplasmic domain of the subtype B Vpu protein of human immunodeficiency virus type 1 (HIV-1) that responsible for retention in the Golgi complex and its absence in subtype C Vpu proteins. AIDS Res. Hum. Retro. 2005, 21:379-394.
39. Patil A., Gautam A., Bhattacharya J. Evidence that Gag facilitates HIV-1 envelope association both in GPI-enriched plasma membrane and detergent resistant membranes and facilitates envelope incorporation onto virions in primary CD4+ T cells. Virol. J. 2010, 7:3.
40. Perez-Caballero D., Zang T., Ebrahimi A., McNatt M.W., Gregory D.A., Johnson M.C., Bieniasz P.D. Tetherin inhibits HIV-1 release by directly tethering virions to cells. Cell 2009, 139:499-511.
41. Pralle A., Keller P., Florin E.L., Simons K., Horber J.K. Sphingolipid-cholesterol rafts diffuse as small entities in the plasma membrane of mammalian cells. J. Cell Biol. 2000, 148:997-1008.
42. Prior I.A., Muncke C., Parton R.G., Hancock J.F. Direct visualization of Ras proteins in spatially distinct cell surface microdomains. J. Cell Biol. 2003, 160:165-170.
43. Rollason R., Korolchuk V., Hamilton C., Schu P., Banting G. Clathrin-mediated endocytosis of a lipid-raft-associated protein is mediated through a dual tyrosine motif. J. Cell Sci. 2007, 120:3850-3858.
44. Rouso I., Mixon M.B., Chen B.K., Kim P.S. Palmitoylation of the HIV-1 envelope glycoprotein is critical for viral infectivity. Proc. Natl. Acad. Sci. USA 2000, 97:13523-13525.
45. Ruiz A., Hill M.S., Schmitt K., Guatelli J., Stephens E.B. Requirements of membrane proximal tyrosine and dileucine sorting signals for efficient transport of the subtype C Vpu proteins to the plasma membrane and virus release. Virology 2008, 378:58-68.
46. Ruiz A., Guatelli J.C., Stephens E.B. The Vpu protein: new concepts in virus release and CD4 down-modulation. Curr. HIV-1 Res. 2010, 8:240-252.
47. Scheiffele P., Rietveld A., Wilk T., Simons K. Influenza viruses select ordered lipid domains during budding from the plasma membrane. J. Biol. Chem. 1999, 274:2038-2044.
48. Schubert U., Bour S., Ferrer-Montiel A.V., Montal M., Maldarell F., Strebel K. The two biological activities of human immunodeficiency virus type 1 Vpu protein involve two separable structural domains. J. Virol. 1996, 70:809-819.
49. Schubert U., Anton L.C., Bacik I., Cox J.H., Bour S., Bennink J.R., Orlowski M., Strebel K., Yewdell J.W. CD4 glycoprotein degradation induced by human immunodeficiency virus type 1 Vpu protein requires the function of proteasomes and the ubiquitin-conjugating pathway. J. Virol. 1998, 72:2280-2288.
50. Schuck S., Honsho M., Ekroos K., Shevchenko A., Simons K. Resistance of cell membranes to different detergents. Proc. Natl. Acad. Sci. USA 2003, 100:5795-5800.
51. Sharma P., Varma R., Sarasij R.C., Ira, Gousset K., Krishnamoorthy G., Rao M., Mayor S. Nanoscale organization of multiple GPI-anchored proteins in living cell membranes. Cell 2004, 116:577-589.
52. Shogomori H., Brown D.A. Use of detergents to study membrane rafts: the good, the bad, and the ugly. J. Biol. Chem. 2003, 384:1259-1263.
53. Simons K., van Meer G. Lipid sorting in epithelial cells. Biochemistry 1988, 27:6197-6202.
54. KU-1bMC33) in pig-tailed macaques. Virology 2003, 313:435-451.
55. Sramala I., Lemaitre V., Faraldo-Gomez J.D., Vincent S., Watts A., Fischer W.B. Molecular dynamics simulations on the first two helices of Vpu from HIV-1. Biophys. J. 2003, 84:3276-3284.
56. KU1bMC33) results in enhanced Env biosynthesis in lymphocytes but is less pathogenic in pig-tailed macaques. Virology 2002, 293:252-261.
57. Strebel K., Klimkait T., Martin M.A. A novel gene of HIV-1, vpu, and its 16-kilodalton product. Science 1988, 241:1221-1223.
58. Van Damme N., Goff D., Katsura C., Jorgenson R.L., Mitchell R., Johnson M.C., Stephens E.B., Guatelli J.C. The interferon-induced protein BST-2 restricts HIV-1 release and is downregulated from the cell surface by the viral Vpu protein. Cell Host Microbe 2008, 3:245-252.
59. Vishwanathan S.A., Thomas A., Brasseur R., Epand R.F., Hunter E., Epand R.M. Hydrophobic substitutions in the first residue of the CRAC segment of the gp41 protein of HIV. Biochemistry 2008, 47:124-130.