Roles played by capsid-dependent induction of membrane curvature and Gag-ESCRT interactions in tetherin recruitment to HIV-1 assembly sites

Journal of Virology

Volumn 87, Issue 8, 2013, Pages 4650-4664

  Grover, Jonathan R ^a   Llewellyn, G Nicholas ^a,d   Soheilian, Ferri ^b   Nagashima, Kunio ^b   Veatch, Sarah L ^c   Ono, Akira ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b SAIC FREDERICK INC   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; ESCRT PROTEIN; GAG PROTEIN; INHIBITOR PROTEIN; TETHERIN; TUMOR SUSCEPTIBILITY GENE 101 PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; HUMAN IMMUNODEFICIENCY VIRUS 1; LIPID RAFT; MEMBRANE STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; VIRUS ASSEMBLY; VIRUS CAPSID; VIRUS RELEASE;

ANTIGENS, CD; CELL MEMBRANE; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; GPI-LINKED PROTEINS; HELA CELLS; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; MICROSCOPY, CONFOCAL; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; VIRUS ASSEMBLY;

HUMAN IMMUNODEFICIENCY VIRUS 1; MIRIDAE;

EID: 84875773685     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03526-12     Document Type: Article

References (90)

1. Neil SJ, Zang T, Bieniasz PD. 2008. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451:425-430.
2. Van Damme N, Goff D, Katsura C, Jorgenson RL, Mitchell R, Johnson MC, Stephens EB, Guatelli J. 2008. 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 3:245-252.
3. Fitzpatrick K, Skasko M, Deerinck TJ, Crum J, Ellisman MH, Guatelli J. 2010. Direct restriction of virus release and incorporation of the interferon- induced protein BST-2 into HIV-1 particles. PLoS Pathog. 6:e1000701.
4. Goffinet C, Allespach I, Homann S, Tervo HM, Habermann A, Rupp D, Oberbremer L, Kern C, Tibroni N, Welsch S, Krijnse-Locker J, Banting G, Krausslich HG, Fackler OT, Keppler OT. 2009. HIV-1 antagonism of CD317 is species specific and involves Vpu-mediated proteasomal degradation of the restriction factor. Cell Host Microbe 5:285-297.
5. Habermann A, Krijnse-Locker J, Oberwinkler H, Eckhardt M, Homann S, Andrew A, Strebel K, Krausslich HG. 2010. CD317/tetherin is enriched in the HIV-1 envelope and downregulated from the plasma membrane upon virus infection. J. Virol. 84:4646-4658.
6. Hammonds J, Wang JJ, Yi H, Spearman P. 2010. Immunoelectron microscopic evidence for Tetherin/BST2 as the physical bridge between HIV-1 virions and the plasma membrane. PLoS Pathog. 6:e1000749. doi: 10.1371/journal.ppat.1000749.
7. Jouvenet N, Neil SJ, Zhadina M, Zang T, Kratovac Z, Lee Y, McNatt M, Hatziioannou T, Bieniasz PD. 2009. Broad-spectrum inhibition of retroviral and filoviral particle release by tetherin. J. Virol. 83:1837-1844.
8. Mitchell RS, Katsura C, Skasko MA, Fitzpatrick K, Lau D, Ruiz A, Stephens EB, Margottin-Goguet F, Benarous R, Guatelli JC. 2009. Vpu antagonizes BST-2-mediated restriction of HIV-1 release via beta-TrCP and endo-lysosomal trafficking. PLoS Pathog. 5:e1000450. doi:10.1371 /journal.ppat.1000450.
9. Perez-Caballero D, Zang T, Ebrahimi A, McNatt MW, Gregory DA, Johnson MC, Bieniasz PD. 2009. Tetherin inhibits HIV-1 release by directly tethering virions to cells. Cell 139:499-511.
10. Lehmann M, Rocha S, Mangeat B, Blanchet F, Uji IH, Hofkens J, Piguet V. 2011. Quantitative Multicolor super-resolution microscopy reveals tetherin HIV-1 interaction. PLoS Pathog. 7:e1002456. doi:10.1371 /journal.ppat.1002456.
11. Andrew AJ, Miyagi E, Kao S, Strebel K. 2009. The formation of cysteinelinked dimers of BST-2/tetherin is important for inhibition of HIV-1 virus release but not for sensitivity to Vpu. Retrovirology 6:80. doi:10.1186 /1742-4690-6-80.
12. Hinz A, Miguet N, Natrajan G, Usami Y, Yamanaka H, Renesto P, Hartlieb B, McCarthy AA, Simorre JP, Gottlinger H, Weissenhorn W. 2010. Structural basis of HIV-1 tethering to membranes by the BST-2/ tetherin ectodomain. Cell Host Microbe 7:314-323.
13. Yang H, Wang J, Jia X, McNatt MW, Zang T, Pan B, Meng W, Wang HW, Bieniasz PD, Xiong Y. 2010. Structural insight into the mechanisms of enveloped virus tethering by tetherin. Proc. Natl. Acad. Sci. U. S. A. 107:18428-18432.
14. Swiecki M, Scheaffer SM, Allaire M, Fremont DH, Colonna M, Brett TJ. 2011. Structural and biophysical analysis of BST-2/tetherin ectodomains reveals an evolutionary conserved design to inhibit virus release. J. Biol. Chem. 286:2987-2997.
15. Schubert HL, Zhai Q, Sandrin V, Eckert DM, Garcia-Maya M, Saul L, Sundquist WI, Steiner RA, Hill CP. 2010. Structural and functional studies on the extracellular domain of BST2/tetherin in reduced and oxidized conformations. Proc. Natl. Acad. Sci. U. S. A. 107:17951-17956.
16. Kupzig S, Korolchuk V, Rollason R, Sugden A, Wilde A, Banting G. 2003. Bst-2/HM1.24 is a raft-associated apical membrane protein with an unusual topology. Traffic 4:694-709.
17. Lopez LA, Yang SJ, Exline CM, Rengarajan S, Haworth KG, Cannon PM. 2012. Anti-tetherin activities of HIV-1 Vpu and Ebola virus glycoprotein do not involve tetherin removal from lipid rafts. J. Virol. 86:5467-5480.
18. Masuyama N, Kuronita T, Tanaka R, Muto T, Hirota Y, Takigawa A, Fujita H, Aso Y, Amano J, Tanaka Y. 2009. HM1.24 is internalized from lipid rafts by clathrin-mediated endocytosis through interaction with alpha- adaptin. J. Biol. Chem. 284:15927-15941.
19. Douglas JL, Gustin JK, Viswanathan K, Mansouri M, Moses AV, Fruh K. 2010. The great escape: viral strategies to counter BST-2/tetherin. PLoS Pathog. 6:e1000913. doi:10.1371/journal.ppat.1000913.
20. Evans DT, Serra-Moreno R, Singh RK, Guatelli JC. 2010. BST-2/ tetherin: a new component of the innate immune response to enveloped viruses. Trends Microbiol. 18:388-396.
21. Dube M, Bego MG, Paquay C, Cohen EA. 2010. Modulation of HIV-1- host interaction: role of the Vpu accessory protein. Retrovirology 7:114. doi:10.1186/1742-4690-7-114.
22. Balasubramaniam M, Freed EO. 2011. New insights into HIV assembly and trafficking. Physiology (Bethesda) 26:236-251.
23. Bieniasz PD. 2009. The cell biology of HIV-1 virion genesis. Cell Host Microbe 5:550-558.
24. Chukkapalli V, Ono A. 2011. Molecular determinants that regulate plasma membrane association of HIV-1 Gag. J. Mol. Biol. 410:512-524.
25. Weiss ER, Gottlinger H. 2011. The role of cellular factors in promoting HIV budding. J. Mol. Biol. 410:525-533.
26. Hogue IB, Grover JR, Soheilian F, Nagashima K, Ono A. 2011. Gag induces the coalescence of clustered lipid rafts and tetraspanin-enriched microdomains at HIV-1 assembly sites on the plasma membrane. J. Virol. 85:9749-9766.
27. Krementsov DN, Rassam P, Margeat E, Roy NH, Schneider-Schaulies J, Milhiet PE, Thali M. 2010. HIV-1 assembly differentially alters dynamics and partitioning of tetraspanins and raft components. Traffic 11:1401-1414.
28. Chen BJ, Lamb RA. 2008. Mechanisms for enveloped virus budding: can some viruses do without an ESCRT? Virology 372:221-232.
29. Hurley JH, Hanson PI. 2010. Membrane budding and scission by the ESCRT machinery it's all in the neck Nat. Rev. Mol. Cell Biol. 11:556-566.
30. Ono A. 2010. Relationships between plasma membrane microdomains and HIV-1 assembly. Biol. Cell 102:335-350.
31. Hammonds J, Spearman P. 2010. An imperfect rule for the particle roost. Cell Host Microbe 7:261-263.
32. Adachi A, Gendelman HE, Koenig S, Folks T, Willey R, Rabson A, Martin MA. 1986. Production of acquired immunodeficiency syndromeassociated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J. Virol. 59:284-291.
33. Klimkait T, Strebel K, Hoggan MD, Martin MA, Orenstein JM. 1990. The human immunodeficiency virus type 1-specific protein Vpu is required for efficient virus maturation and release. J. Virol. 64:621-629.
34. Chukkapalli V, Hogue IB, Boyko V, Hu WS, Ono A. 2008. Interaction between the human immunodeficiency virus type 1 Gag matrix domain and phosphatidylinositol-(4,5)-bisphosphate is essential for efficient gag membrane binding. J. Virol. 82:2405-2417.
35. Sun Z, Pan J, Hope WX, Cohen SN, Balk SP. 1999. Tumor susceptibility gene 101 protein represses androgen receptor transactivation and interacts with p300. Cancer 86:689-696.
36. Ott M, Schnolzer M, Garnica J, Fischle W, Emiliani S, Rackwitz HR, Verdin E. 1999. Acetylation of the HIV-1 Tat protein by p300 is important for its transcriptional activity. Curr. Biol. 9:1489-1492.
37. Ahmad N, Maitra RK, Venkatesan S. 1989. Rev-induced modulation of Nef protein underlies temporal regulation of human immunodeficiency virus replication. Proc. Natl. Acad. Sci. U. S. A. 86:6111-6115.
38. Ono A, Freed EO. 2001. Plasma membrane rafts play a critical role in HIV-1 assembly and release. Proc. Natl. Acad. Sci. U. S. A. 98:13925-13930.
39. Yee JK, Friedmann T, Burns JC. 1994. Generation of high-titer pseudotyped retroviral vectors with very broad host range. Methods Cell Biol. 43(Part A):99-112.
40. Kong LB, An D, Ackerson B, Canon J, Rey O, Chen IS, Krogstad P, Stewart PL. 1998. Cryoelectron microscopic examination of human immunodeficiency virus type 1 virions with mutations in the cyclophilin A binding loop. J. Virol. 72:4403-4407.
41. von Schwedler UK, Stray KM, Garrus JE, Sundquist WI. 2003. Functional surfaces of the human immunodeficiency virus type 1 capsid protein. J. Virol. 77:5439-5450.
42. Huang M, Orenstein JM, Martin MA, Freed EO. 1995. p6Gag is required for particle production from full-length human immunodeficiency virus type 1 molecular clones expressing protease. J. Virol. 69:6810-6818.
43. Popov S, Popova E, Inoue M, Gottlinger HG. 2008. Human immunodeficiency virus type 1 Gag engages the Bro1 domain of ALIX/AIP1 through the nucleocapsid. J. Virol. 82:1389-1398.
44. Gottlinger HG, Dorfman T, Sodroski JG, Haseltine WA. 1991. Effect of mutations affecting the p6 gag protein on human immunodeficiency virus particle release. Proc. Natl. Acad. Sci. U. S. A. 88:3195-3199.
45. Zhang M, Chang H, Zhang Y, Yu J, Wu L, Ji W, Chen J, Liu B, Lu J, Liu Y, Zhang J, Xu P, Xu T. 2012. Rational design of true monomeric and bright photoactivatable fluorescent proteins. Nat. Methods 9:727-729.
46. Kiernan RE, Ono A, Freed EO. 1999. Reversion of a human immunodeficiency virus type 1 matrix mutation affecting Gag membrane binding, endogenous reverse transcriptase activity, and virus infectivity. J. Virol. 73:4728-4737.
47. Hogue IB, Hoppe A, Ono A. 2009. Quantitative fluorescence resonance energy transfer microscopy analysis of the human immunodeficiency virus type 1 Gag-Gag interaction: relative contributions of the CA and NC domains and membrane binding. J. Virol. 83:7322-7336.
48. Janvier K, Pelchen-Matthews A, Renaud JB, Caillet M, Marsh M, Berlioz-Torrent C. 2011. The ESCRT-0 component HRS is required for HIV-1 Vpu-mediated BST-2/tetherin down-regulation. PLoS Pathog. 7:e1001265. doi:10.1371/journal.ppat.1001265.
49. Pan S, Wang R, Zhou X, He G, Koomen J, Kobayashi R, Sun L, Corvera J, Gallick GE, Kuang J. 2006. Involvement of the conserved adaptor protein Alix in actin cytoskeleton assembly. J. Biol. Chem. 281:34640-34650.
50. Morita E, Colf LA, Karren MA, Sandrin V, Rodesch CK, Sundquist WI. 2010. Human ESCRT-III and VPS4 proteins are required for centrosome and spindle maintenance. Proc. Natl. Acad. Sci. U. S. A. 107:12889-12894.
51. Miyagi E, Andrew AJ, Kao S, Strebel K. 2009. Vpu enhances HIV-1 virus release in the absence of Bst-2 cell surface down-modulation and intracellular depletion. Proc. Natl. Acad. Sci. U. S. A. 106:2868-2873.
52. Llewellyn GN, Hogue IB, Grover JR, Ono A. 2010. Nucleocapsid promotes localization of HIV-1 gag to uropods that participate in virological synapses between T cells. PLoS Pathog. 6:e1001167. doi:10.1371/journal .ppat.1001167.
53. Ono A, Waheed AA, Joshi A, Freed EO. 2005. Association of human immunodeficiency virus type 1 gag with membrane does not require highly basic sequences in the nucleocapsid: use of a novel Gag multimerization assay. J. Virol. 79:14131-14140.
54. Bolte S, Cordelieres FP. 2006. A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc. 224:213-232.
55. Gonda MA, Aaronson SA, Ellmore N, Zeve VH, Nagashima K. 1976. Ultrastructural studies of surface features of human normal and tumor cells in tissue culture by scanning and transmission electron microscopy. J. Natl. Cancer Inst. 56:245-263.
56. Rust MJ, Bates M, Zhuang X. 2006. Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat. Methods 3:793-795.
57. Endesfelder U, Malkusch S, Flottmann B, Mondry J, Liguzinski P, Verveer PJ, Heilemann M. 2011. Chemically induced photoswitching of fluorescent probes-a general concept for super-resolution microscopy. Molecules 16:3106-3118.
58. Churchman LS, Okten Z, Rock RS, Dawson JF, Spudich JA. 2005. Single molecule high-resolution colocalization of Cy3 and Cy5 attached to macromolecules measures intramolecular distances through time. Proc. Natl. Acad. Sci. U. S. A. 102:1419-1423.
59. Veatch SL, Machta BB, Shelby SA, Chiang EN, Holowka DA, Baird BA. 2012. Correlation functions quantify super-resolution images and estimate apparent clustering due to over-counting. PLoS One 7:e31457. doi: 10.1371/journal.pone.0031457.
60. Hammond S, Wagenknecht-Wiesner A, Veatch SL, Holowka D, Baird B. 2009. Roles for SH2 and SH3 domains in Lyn kinase association with activated FceRI in RBL mast cells revealed by patterned surface analysis. J. Struct. Biol. 168:161-167.
61. Miyagi E, Andrew A, Kao S, Yoshida T, Strebel K. 2011. Antibodymediated enhancement of HIV-1 and HIV-2 production from BST-2/ tetherin-positive cells. J. Virol. 85:11981-11994.
62. Fritz JV, Tibroni N, Keppler OT, Fackler OT. 2012. HIV-1 Vpu's lipid raft association is dispensable for counteraction of the particle release restriction imposed by CD317/Tetherin. Virology 424:33-44.
63. Ruiz A, Hill MS, Schmitt K, Stephens EB. 2010. Membrane raft association of the Vpu protein of human immunodeficiency virus type 1 correlates with enhanced virus release. Virology 408:89-102.
64. Ono A, Waheed AA, Freed EO. 2007. Depletion of cellular cholesterol inhibits membrane binding and higher-order multimerization of human immunodeficiency virus type 1 Gag. Virology 360:27-35.
65. Garrus JE, von Schwedler UK, Pornillos OW, Morham SG, Zavitz KH, Wang HE, Wettstein DA, Stray KM, Cote M, Rich RL, Myszka DG, Sundquist WI. 2001. Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 107:55-65.
66. Martin-Serrano J, Zang T, Bieniasz PD. 2001. HIV-1 and Ebola virus encode small peptide motifs that recruit Tsg101 to sites of particle assembly to facilitate egress. Nat. Med. 7:1313-1319.
67. Demirov DG, Ono A, Orenstein JM, Freed EO. 2002. Overexpression of the N-terminal domain of TSG101 inhibits HIV-1 budding by blocking late domain function. Proc. Natl. Acad. Sci. U. S. A. 99:955-960.
68. Strack B, Calistri A, Craig S, Popova E, Gottlinger HG. 2003. AIP1/ALIX is a binding partner for HIV-1 p6 and EIAV p9 functioning in virus budding. Cell 114:689-699.
69. von Schwedler UK, Stuchell M, Muller B, Ward DM, Chung HY, Morita E, Wang HE, Davis T, He GP, Cimbora DM, Scott A, Krausslich HG, Kaplan J, Morham SG, Sundquist WI. 2003. The protein network of HIV budding. Cell 114:701-713.
70. Pornillos O, Alam SL, Davis DR, Sundquist WI. 2002. Structure of the Tsg101 UEV domain in complex with the PTAP motif of the HIV-1 p6 protein. Nat. Struct. Biol. 9:812-817.
71. Stuchell MD, Garrus JE, Muller B, Stray KM, Ghaffarian S, McKinnon R, Krausslich HG, Morham SG, Sundquist WI. 2004. The human endosomal sorting complex required for transport (ESCRT-I) and its role in HIV-1 budding. J. Biol. Chem. 279:36059-36071.
72. VerPlank L, Bouamr F, LaGrassa TJ, Agresta B, Kikonyogo A, Leis J, Carter CA. 2001. Tsg101, a homologue of ubiquitin-conjugating (E2) enzymes, binds the L domain in HIV type 1 Pr55(Gag). Proc. Natl. Acad. Sci. U. S. A. 98:7724-7729.
73. Demirov DG, Orenstein JM, Freed EO. 2002. The late domain of human immunodeficiency virus type 1 p6 promotes virus release in a cell typedependent manner. J. Virol. 76:105-117.
74. Dussupt V, Sette P, Bello NF, Javid MP, Nagashima K, Bouamr F. 2011. Basic residues in the nucleocapsid domain of Gag are critical for late events of HIV-1 budding. J. Virol. 85:2304-2315.
75. Kafaie J, Song R, Abrahamyan L, Mouland AJ, Laughrea M. 2008. Mapping of nucleocapsid residues important for HIV-1 genomic RNA dimerization and packaging. Virology 375:592-610.
76. Grigorov B, Decimo D, Smagulova F, Pechoux C, Mougel M, Muriaux D, Darlix JL. 2007. Intracellular HIV-1 Gag localization is impaired by mutations in the nucleocapsid zinc fingers. Retrovirology 4:54. doi:10 .1186/1742-4690-4-54.
77. Betzig E, Patterson GH, Sougrat R, Lindwasser OW, Olenych S, Bonifacino JS, Davidson MW, Lippincott-Schwartz J, Hess HF. 2006. Imaging intracellular fluorescent proteins at nanometer resolution. Science 313:1642-1645.
78. McKinney SA, Murphy CS, Hazelwood KL, Davidson MW, Looger LL. 2009. A bright and photostable photoconvertible fluorescent protein. Nat. Methods 6:131-133.
79. Martin-Serrano J, Yarovoy A, Perez-Caballero D, Bieniasz PD. 2003. Divergent retroviral late-budding domains recruit vacuolar protein sorting factors by using alternative adaptor proteins. Proc. Natl. Acad. Sci. U. S. A. 100:12414-12419.
80. Morita E, Sandrin V, McCullough J, Katsuyama A, Baci Hamilton I, Sundquist WI. 2011. ESCRT-III protein requirements for HIV-1 budding. Cell Host Microbe 9:235-242.
81. van Rheenen J, Jalink K. 2002. Agonist-induced PIP(2) hydrolysis inhibits cortical actin dynamics: regulation at a global but not at a micrometer scale. Mol. Biol. Cell 13:3257-3267.
82. Malim MH, Emerman M. 2008. HIV-1 accessory proteins- ensuring viral survival in a hostile environment. Cell Host Microbe 3:388-398.
83. Reil H, Bukovsky AA, Gelderblom HR, Gottlinger HG. 1998. Efficient HIV-1 replication can occur in the absence of the viral matrix protein. EMBO J. 17:2699-2708.
84. Andrew AJ, Kao S, Strebel K. 2011. C-terminal hydrophobic region in human bone marrow stromal cell antigen 2 (BST-2)/tetherin protein functions as second transmembrane motif. J. Biol. Chem. 286:39967-39981.
85. Chojnacki J, Staudt T, Glass B, Bingen P, Engelhardt J, Anders M, Schneider J, Muller B, Hell SW, Krausslich HG. 2012. Maturationdependent HIV-1 surface protein redistribution revealed by fluorescence nanoscopy. Science 338:524-528.
86. Hammonds J, Ding L, Chu H, Geller K, Robbins A, Wang JJ, Yi H, Spearman P. 2012. The tetherin/BST-2 coiled-coil ectodomain mediates plasma membrane microdomain localization and restriction of particle release. J. Virol. 86:2259-2272.
87. Baumgartel V, Ivanchenko S, Dupont A, Sergeev M, Wiseman PW, Krausslich HG, Brauchle C, Muller B, Lamb DC. 2011. Live-cell visualization of dynamics of HIV budding site interactions with an ESCRT component. Nat. Cell Biol. 13:469-474.
88. Jouvenet N, Zhadina M, Bieniasz PD, Simon SM. 2011. Dynamics of ESCRT protein recruitment during retroviral assembly. Nat. Cell Biol. 13:394-401.
89. Bhatia VK, Hatzakis NS, Stamou D. 2010. A unifying mechanism accounts for sensing of membrane curvature by BAR domains, amphipathic helices and membrane-anchored proteins. Semin. Cell Dev. Biol. 21:381-390.
90. Antonny B. 2011. Mechanisms of membrane curvature sensing. Annu. Rev. Biochem. 80:101-123.