The Vpu-regulated endocytosis of HIV-1 Gag is clathrin-independent

Virology

Volumn 369, Issue 2, 2007, Pages 299-308

  Harila, Kirsi ^a,b   Salminen, Antti ^a   Prior, Ian ^c   Hinkula, Jorma ^b   Suomalainen, Maarit ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b KAROLINSKA INSTITUTE   (Sweden)

^c UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Endocytosis; Gag trafficking; HIV 1; Virus assembly; Vpu

Indexed keywords

CELL SURFACE PROTEIN; CHOLESTEROL; CLATHRIN; FILIPIN; GAG PROTEIN; VPU PROTEIN;

ADULT; ARTICLE; CELL FRACTIONATION; CELL MEMBRANE; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; HELA CELL; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; NONHUMAN; PHENOTYPE; PINOCYTOSIS; PRIORITY JOURNAL; PROGENY; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; VIRION; VIRUS CELL INTERACTION;

BASE SEQUENCE; CELL LINE; CHOLESTEROL; CLATHRIN; CLATHRIN HEAVY CHAINS; ENDOCYTOSIS; FILIPIN; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HELA CELLS; HIV INFECTIONS; HIV-1; HUMAN IMMUNODEFICIENCY VIRUS PROTEINS; HUMANS; PINOCYTOSIS; RNA INTERFERENCE; RNA, SMALL INTERFERING; VIRAL REGULATORY AND ACCESSORY PROTEINS; VIRUS ASSEMBLY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 36148992616     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2007.08.009     Document Type: Article

References (53)

1. Adachi A., Gendelman H.E., Koenig S., Folks S., Willey R., Rabson A., and Martin M.A. Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular retrovirus clone. J. Virol. 59 (1986) 284-291
2. Batonick M., Favre M., Boge M., Spearman P., Höning S., and Thali M. Interaction of HIV-1 Gag with the clathrin-associated adaptor AP-2. Virology 342 (2005) 190-200
3. Bour S., and Strebel K. The HIV-1 Vpu protein: a multifunctional enhancer of viral particle release. Microbes Infect. 5 (2003) 1029-1039
4. Bryant M., and Ratner L. Myristoylation-dependent replication and assembly of human immunodeficiency virus 1. Proc. Natl. Acad. Sci. U. S. A. 87 (1990) 523-527
5. Chertova E.N., Chertov O., Coren L.V., Roser J.D., Trubey C.M., Bess Jr. J.W., Sowder II R.C., Barsov E., Hood B.L., Fisher R.D., Nagashima K., Conrads T.P., Veenstra T.D., Lifson J.D., and Ott D.E. Proteomic and biochemical analysis of purified human immunodeficiency virus type 1 produced from infected monocyte-derived macrophages. J. Virol. 80 (2006) 9039-9052
6. Costa L.J., Chen N., Lopes A., Aguiar R.S., Tanuri A., Plemenitas A., and Peterlin B.M. Interactions between Nef and AIP1 proliferate multivesicular bodies and facilitate egress of HIV-1. Retrovirology 2006 3:33 (2006)
7. Deneka M., Pelchen-Matthews A., Byland R., Ruiz-Mateos E., and Marsh M. In macrophages, HIV-1 assembles into an intracellular plasma membrane domain containing the tetraspanins CD81, CD9 and CD53. J. Cell Biol. 177 (2007) 329-341
8. Ding L., Derdowski A., Wang J.-J., and Spearman P. Independent segregation of human immunodeficiency virus type 1 Gag protein complexes and lipid rafts. J. Virol. 77 (2003) 1916-1926
9. Dong X., Li H., Derdowski A., Ding L., Burnett A., Chen X., Peters T.R., Dermody T.S., Woodruff E., Wang J.-J., and Spearman P. AP-3 directs the intracellular trafficking of HIV-1 Gag and plays a key role in particle assembly. Cell 120 (2005) 663-674
10. Finzi A., Orthwein A., Mercier J., and Cohen E.A. Productive human immunodeficiency virus type 1 assembly takes place at the plasma membrane. J. Virol. 81 (2007) 7476-7490
11. Garrus J.E., von Schwedler U.K., Pornillos O.W., Morham S.G., Zavitz K.H., Wang H.E., Wettstein D.A., Stray K.M., Cöte M., Rich R.L., Myszka D.G., and Sundquist W.I. Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 107 (2001) 55-65
12. Gheysen D., Jacobs E., Foresta F.d., Thiriart C., Francotte M., Thines D., and Wilde M.D. Assembly and release of HIV-1 precursor Pr55gag virus-like particles from recombinant Baculovirus-infected cells. Cell 59 (1989) 103-112
13. Greene Nguyen D., Booth A.M., Gould S.J., and Hildreth J.E.K. Evidence that HIV budding in primary macrophages occurs through the exosome release pathway. J. Biol. Chem. 278 (2003) 52347-52354
14. Grigorov B., Arcanger F., Roingeard P., Darlix J.-L., and Muriaux D. Assembly of infectious HIV-1 in human epithelial and T-lymphoblastic cell lines. J. Mol. Biol. 359 (2006) 848-862
15. Göttlinger H.G. The HIV-1 assembly machine. AIDS 15 Suppl. 5 (2001) S13-S20
16. Göttlinger H.G., Sodroski J.G., and Haseltine W.A. Role of capsid precursor processing and myristoylation in morphogenesis and infectivity of human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. U. S. A. 86 (1989) 3195-3199
17. Halwani R., Khorchid A., Cen S., and Kleiman L. Rapid localization of Gag/GagPol complexes to detergent-resistant membrane during the assembly of human immunodeficiency virus type 1. J. Virol. 77 (2003) 3973-3984
18. Hammarstedt M., and Garoff H. Passive and active inclusion of host proteins in human immunodeficiency virus type 1 gag particles during budding at the plasma membrane. J. Virol. 78 (2004) 5686-5697
19. Harila K., Prior I., Sjöberg E.M., Salminen A., Hinkula J., and Suomalainen M. Vpu and Tsg101 regulate intracellular targeting of human immunodeficiency virus type 1 core protein precursor Pr55Gag. J. Virol. 80 (2006) 3765-3772
20. Hinkula J., Rosen L., Sundqvist V.-A., Stigbrand T., and Wahren B. Epitope mapping of the HIV-1 Gag region with monoclonal antibodies. Mol. Immunol. 27 (1990) 395-403
21. Hinrichsen L., Harborth J., Andrees L., Weber K., and Ungewickell E.J. Effect of clathrin heavy chain- and a-adaptin-specific small inhibitory RNAs on endocytic accessory proteins and receptor trafficking in HeLa cells. J. Biol. Chem. 278 (2003) 45160-45170
22. Holm K., Weclewicz K., Hewson R., and Suomalainen M. HIV-1 assembly and lipid rafts: Pr55gag complexes associate with membrane-domains that are largely resistant to Brij 98, but sensitive to triton X-100. J. Virol. 77 (2003) 4805-4817
23. Jouvenet N., Neil S.J.D., Bess C., Johnson M.C., Virgen C.A., Simon S.M., and Bieniasz P.D. Plasma membrane is the site of productive HIV-1 particle assembly. PLoS Biol. 4 12 (2006) e435
24. Kaplan A.H., Manchester M., and Swanstrom R. The activity of the protease of human immunodeficiency virus type 1 is initiated at the membrane of infected cells before the release of viral proteins and is required for release to occur with maximum efficiency. J. Virol. 68 (1994) 6782-6786
25. Klimkait T., Strebel K., Hoggan M.D., Martin M.A., and Orenstein J.M. The human immunodeficiency virus type 1-specific protein vpu is required for efficient virus maturation and release. J. Virol. 64 (1990) 621-629
26. Lindwasser O.W., and Resh M.D. Multimerization of human immunodeficiency virus type 1 Gag promotes its localization to barges, raft-like membrane microdomains. J. Virol. 75 (2001) 7913-7924
27. Madrid R., Janvier K., Hitchin D., Day J., Coleman S., Noviello C., Bouchet J., Benmerah A., Guatelli J., and Benichou S. Nef-induced alteration of the early/recycling endosomal compartment correlates with enhancement of HIV-1 infectivity. J. Biol. Chem. 280 (2005) 5032-5044
28. Marsh M., and Helenius A. Virus entry: open sesame. Cell 124 (2006) 729-740
29. Martin-Serrano J., Zang T., and Bieniasz P.D. HIV-1 and Ebola virus encode small peptide motifs that recruit Tsg101 to sites of particle assembly to facilitate egress. Nat. Med. 7 (2001) 1313-1319
30. Meier O., Boucke K., Vig Hammer S., Keller S., Stidwill R.P., Hemmi S., and Greber U.F. Adenovirus triggers macropinocytosis and endosomal leakage together with its clathrin-mediated uptake. J. Cell Biol. 158 (2002) 1119-1131
31. Neil S.J.D., Eastman S.W., Jouvenet N., and Bieniasz P.D. HIV-1 Vpu promotes release and prevents endocytosis of nascent retrovirus particles from the plasma membrane. PLoS Pathog. 2 5 (2006) e39
32. Nguyen D.H., and Hildreth J.E.K. Evidence for budding of human immunodeficiency virus type 1 selectively from glycolipid-enriched membrane lipid rafts. J. Virol. 74 (2000) 3264-3272
33. Nydegger S., Foti M., Derdowski A., Spearman P., and Thali M. HIV-1 egress is gated through late endosomal membranes. Traffic 4 (2003) 902-910
34. Ono A., and Freed E.O. Plasma membrane rafts play a critical role in HIV-1 assembly and release. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 13925-13930
35. Ono A., and Freed E.O. Cell-type-dependent targeting of human immunodeficiency virus type 1 assembly to the plasma membrane and the multivesicular body. J. Virol. 78 (2004) 1552-1563
36. Ono A., Waheed A.A., and Freed E.O. Depletion of cellular cholesterol inhibits membrane binding and higher-order multimerization of human immunodeficiency virus type 1 Gag. Virology 360 (2007) 27-35
37. Orenstein J.M., Meltzer M.S., Phipps T., and Gendelman H.E. Cytoplasmic assembly and accumulation of human immunodeficiency virus types 1 and 2 in recombinant human colony-stimulating-factor-1-treated human monocytes: an ultrastructural study. J. Virol. 62 (1988) 2578-2586
38. Pelchen-Matthews A., Kramer B., and Marsh M. Infectious HIV-1 assembles in late endosomes in primary macrophages. J. Cell Biol. 162 (2003) 443-455
39. Pelkmans L., and Helenius A. Insider information: what viruses tell us about endocytosis. Curr. Opin. Cell Biol. 15 (2003) 414-422
40. Perlman M., and Resh M.D. Identification of an intracellular trafficking and assembly pathway for HIV-1 Gag. Traffic 7 (2006) 731-745
41. Raposo G., Moore M.S., Innes D., Leijendekker R., Leigh-Brown A., Benaroch P., and Geuze H.J. Human macrophages accumulate HIV-1 particles in MHC II compartments. Traffic 3 (2002) 718-729
42. Resh M.D. Intracellular trafficking of HIV-1 Gag: how Gag interacts with cell membranes and makes viral particles. AIDS Rev. 7 (2005) 84-91
43. Rudner L., Nydegger S., Coren L.V., Nagashima K., Thali M., and Ott D.E. Dynamic fluorescent imaging of human immunodeficiency virus type 1 Gag in live cells by biarsenical labeling. J. Virol. 79 (2005) 4055-4065
44. Sherer N.M., Lehmann M.J., Jimenez-Soto L.F., Ingmundson A., Horner S.M., Cicchetti G., Allen P.G., Pypaert M., Cunningman J.M., and Mothes W. Visualization of retroviral replication in living cells reveals budding into multivesicular bodies. Traffic 4 (2003) 785-801
45. Spearman P., Wang J.-J., Vander Heyden N., and Ratner L. Identification of Human immunodeficiency virus type 1 Gag protein domains essential to membrane binding and particle assembly. J. Virol. 68 (1994) 3232-3242
46. Subtil A., Gaidarov I., Kobylarz K., Lampson M.A., Keen J.H., and McGraw T.E. Acute cholesterol depletion inhibits clathrin-coated pit budding. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 6775-6780
47. Tritel M., and Resh M.D. Kinetic analysis of human immunodeficiency virus type 1 assembly reveals the presence of sequential intermediates. J. Virol. 74 13 (2000) 5845-5855
48. Varthakavi V., Smith R.M., Martin K.L., Derdowski A., Lapierre L.A., Goldenring J.R., and Spearman P. The pericentriolar recycling endosome plays a key role in Vpu-mediated enhancement of HIV-1 particle release. Traffic 7 (2006) 298-307
49. Ward D.M., Vaughn M.B., Shiflett S.L., White P.L., Pollock A.L., Hill J., Schnegelberger R., Sundquist W.I., and Kaplan J. The role of LIP5 and CHMP5 in multivesicular body formation and HIV-1 budding in mammalian cells. J. Biol. Chem. 280 (2005) 10548-10555
50. Welsch S., Keppler O.T., Habermann A., Allespach I., Krijnse-Locker J., and Kräusslich H.-G. HIV-1 buds predominantly at the plasma membrane of primary human macrophages. PLoS Pathog. 3 3 (2007) e36
51. West M.A., Bretscher M.S., and Watts C. Distinct endocytotic pathways in epidermal growth factor-stimulated human carcinoma A431 cells. J. Cell Biol. 109 (1989) 2731-2739
52. Zheng Y.-H., Plemenitas A., Linnemann T., Fackler O.T., and Peterlin B.M. Nef increases infectivity of HIV via lipid rafts. Curr. Biol. 11 (2001) 875-879
53. Zhou W., Parent L.J., Wills J.W., and Resh M. Identification of a membrane-binding domain within the amino-terminal region of human immunodeficiency virus type 1 Gag protein which interacts with acidic phospholipids. J. Virol. 68 (1994) 2556-2569