Virus budding and the ESCRT pathway

Cell Host and Microbe

Volumn 14, Issue 3, 2013, Pages 232-241

  Votteler, Jörg ^a   Sundquist, Wesley I ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; ESCRT PROTEIN; FATTY ACID BINDING PROTEIN; GAG PROTEIN; HOST FACTOR; PROTEIN VP40; SYNTENIN; UBIQUITIN; VIRUS PROTEIN;

CELL DIVISION; CYTOKINESIS; ENDOSOME; INFLUENZA VIRUS A; MULTIVESICULAR BODY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; REVIEW; SIGNAL TRANSDUCTION; VIRUS ENTRY; VIRUS ENVELOPE; VIRUS RELEASE; VIRUS SHEDDING;

ANIMALS; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; HOST-PATHOGEN INTERACTIONS; HUMANS; MODELS, BIOLOGICAL; RETROVIRIDAE; VIRUS RELEASE;

EID: 84883894715     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2013.08.012     Document Type: Review

References (119)

1. M. Agromayor, and J. Martin-Serrano Knowing when to cut and run: mechanisms that control cytokinetic abscission Trends Cell Biol. 23 2013 433 441
2. J.C. Akers, D. Gonda, R. Kim, B.S. Carter, and C.C. Chen Biogenesis of extracellular vesicles (EV): exosomes, microvesicles, retrovirus-like vesicles, and apoptotic bodies J. Neurooncol. 113 2013 1 11
3. M. Babst, D.J. Katzmann, E.J. Estepa-Sabal, T. Meerloo, and S.D. Emr Escrt-III: an endosome-associated heterooligomeric protein complex required for mvb sorting Dev. Cell 3 2002 271 282
4. M.F. Baietti, Z. Zhang, E. Mortier, A. Melchior, G. Degeest, A. Geeraerts, Y. Ivarsson, F. Depoortere, C. Coomans, and E. Vermeiren Syndecan-syntenin-ALIX regulates the biogenesis of exosomes Nat. Cell Biol. 14 2012 677 685
5. V. Baumgärtel, S. Ivanchenko, A. Dupont, M. Sergeev, P.W. Wiseman, H.G. Kräusslich, C. Bräuchle, B. Müller, and D.C. Lamb Live-cell visualization of dynamics of HIV budding site interactions with an ESCRT component Nat. Cell Biol. 13 2011 469 474
6. N.F. Bello, V. Dussupt, P. Sette, V. Rudd, K. Nagashima, F. Bibollet-Ruche, C. Chen, R.C. Montelaro, B.H. Hahn, and F. Bouamr Budding of retroviruses utilizing divergent L domains requires nucleocapsid J. Virol. 86 2012 4182 4193
7. T.A. Bharat, N.E. Davey, P. Ulbrich, J.D. Riches, A. de Marco, M. Rumlova, C. Sachse, T. Ruml, and J.A. Briggs Structure of the immature retroviral capsid at 8 Å resolution by cryo-electron microscopy Nature 487 2012 385 389
8. C. Bissig, M. Lenoir, M.C. Velluz, I. Kufareva, R. Abagyan, M. Overduin, and J. Gruenberg Viral infection controlled by a calcium-dependent lipid-binding module in ALIX Dev. Cell 25 2013 364 373
9. G. Bodon, R. Chassefeyre, K. Pernet-Gallay, N. Martinelli, G. Effantin, D.L. Hulsik, A. Belly, Y. Goldberg, C. Chatellard-Causse, and B. Blot Charged multivesicular body protein 2B (CHMP2B) of the endosomal sorting complex required for transport-III (ESCRT-III) polymerizes into helical structures deforming the plasma membrane J. Biol. Chem. 286 2011 40276 40286
10. E. Boura, B. Rózycki, H.S. Chung, D.Z. Herrick, B. Canagarajah, D.S. Cafiso, W.A. Eaton, G. Hummer, and J.H. Hurley Solution structure of the ESCRT-I and -II supercomplex: implications for membrane budding and scission Structure 20 2012 874 886
11. E.A. Bruce, L. Medcalf, C.M. Crump, S.L. Noton, A.D. Stuart, H.M. Wise, D. Elton, K. Bowers, and P. Digard Budding of filamentous and non-filamentous influenza A virus occurs via a VPS4 and VPS28-independent pathway Virology 390 2009 268 278
12. E.A. Bruce, P. Digard, and A.D. Stuart The Rab11 pathway is required for influenza A virus budding and filament formation J. Virol. 84 2010 5848 5859
13. A. Calistri, C. Del Vecchio, C. Salata, M. Celestino, M. Celegato, H. Göttlinger, G. Palù, and C. Parolin Role of the feline immunodeficiency virus L-domain in the presence or absence of Gag processing: involvement of ubiquitin and Nedd4-2s ligase in viral egress J. Cell. Physiol. 218 2009 175 182
14. S. Campbell, and A. Rein In vitro assembly properties of human immunodeficiency virus type 1 Gag protein lacking the p6 domain J. Virol. 73 1999 2270 2279
15. L.A. Carlson, and J.H. Hurley In vitro reconstitution of the ordered assembly of the endosomal sorting complex required for transport at membrane-bound HIV-1 Gag clusters Proc. Natl. Acad. Sci. USA 109 2012 16928 16933
16. J.G. Carlton, and J. Martin-Serrano Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery Science 316 2007 1908 1912
17. H.Y. Chung, E. Morita, U. von Schwedler, B. Müller, H.G. Kräusslich, and W.I. Sundquist NEDD4L overexpression rescues the release and infectivity of human immunodeficiency virus type 1 constructs lacking PTAP and YPXL late domains J. Virol. 82 2008 4884 4897
18. J.J. Cockburn, N.G. Abrescia, J.M. Grimes, G.C. Sutton, J.M. Diprose, J.M. Benevides, G.J. Thomas Jr., J.K. Bamford, D.H. Bamford, and D.I. Stuart Membrane structure and interactions with protein and DNA in bacteriophage PRD1 Nature 432 2004 122 125
19. D.G. Demirov, A. Ono, J.M. Orenstein, and E.O. Freed Overexpression of the N-terminal domain of TSG101 inhibits HIV-1 budding by blocking late domain function Proc. Natl. Acad. Sci. USA 99 2002 955 960
20. K.A. Dilley, D. Gregory, M.C. Johnson, and V.M. Vogt An LYPSL late domain in the gag protein contributes to the efficient release and replication of Rous sarcoma virus J. Virol. 84 2010 6276 6287
21. M.J. Dobro, R.Y. Samson, Z. Yu, J. McCullough, H.J. Ding, P.L. Chong, S.D. Bell, and G.J. Jensen Electron cryotomography of ESCRT assemblies and dividing Sulfolobus cells suggests that spiraling filaments are involved in membrane scission Mol. Biol. Cell 24 2013 2319 2327
22. J.E. Dooher, B.L. Schneider, J.C. Reed, and J.R. Lingappa Host ABCE1 is at plasma membrane HIV assembly sites and its dissociation from Gag is linked to subsequent events of virus production Traffic 8 2007 195 211
23. M.R. Dores, B. Chen, H. Lin, U.J. Soh, M.M. Paing, W.A. Montagne, T. Meerloo, and J. Trejo ALIX binds a YPX(3)L motif of the GPCR PAR1 and mediates ubiquitin-independent ESCRT-III/MVB sorting J. Cell Biol. 197 2012 407 419
24. D.P. Dowlatshahi, V. Sandrin, S. Vivona, T.A. Shaler, S.E. Kaiser, F. Melandri, W.I. Sundquist, and R.R. Kopito ALIX is a Lys63-specific polyubiquitin binding protein that functions in retrovirus budding Dev. Cell 23 2012 1247 1254
25. M. Dreux, U. Garaigorta, B. Boyd, E. Décembre, J. Chung, C. Whitten-Bauer, S. Wieland, and F.V. Chisari Short-range exosomal transfer of viral RNA from infected cells to plasmacytoid dendritic cells triggers innate immunity Cell Host Microbe 12 2012 558 570
26. V. Dussupt, M.P. Javid, G. Abou-Jaoudé, J.A. Jadwin, J. de La Cruz, K. Nagashima, and F. Bouamr The nucleocapsid region of HIV-1 Gag cooperates with the PTAP and LYPXnL late domains to recruit the cellular machinery necessary for viral budding PLoS Pathog. 5 2009 e1000339
27. G. Effantin, A. Dordor, V. Sandrin, N. Martinelli, W.I. Sundquist, G. Schoehn, and W. Weissenhorn ESCRT-III CHMP2A and CHMP3 form variable helical polymers in vitro and act synergistically during HIV-1 budding Cell. Microbiol. 15 2013 213 226
28. N. Elia, R. Sougrat, T.A. Spurlin, J.H. Hurley, and J. Lippincott-Schwartz Dynamics of endosomal sorting complex required for transport (ESCRT) machinery during cytokinesis and its role in abscission Proc. Natl. Acad. Sci. USA 108 2011 4846 4851
29. G. Fabrikant, S. Lata, J.D. Riches, J.A. Briggs, W. Weissenhorn, and M.M. Kozlov Computational model of membrane fission catalyzed by ESCRT-III PLoS Comput. Biol. 5 2009 e1000575
30. J.P. Fededa, and D.W. Gerlich Molecular control of animal cell cytokinesis Nat. Cell Biol. 14 2012 440 447
31. Z. Feng, L. Hensley, K.L. McKnight, F. Hu, V. Madden, L. Ping, S.H. Jeong, C. Walker, R.E. Lanford, and S.M. Lemon A pathogenic picornavirus acquires an envelope by hijacking cellular membranes Nature 496 2013 367 371
32. R.D. Fisher, H.Y. Chung, Q. Zhai, H. Robinson, W.I. Sundquist, and C.P. Hill Structural and biochemical studies of ALIX/AIP1 and its role in retrovirus budding Cell 128 2007 841 852
33. K. Fujii, U.M. Munshi, S.D. Ablan, D.G. Demirov, F. Soheilian, K. Nagashima, A.G. Stephen, R.J. Fisher, and E.O. Freed Functional role of Alix in HIV-1 replication Virology 391 2009 284 292
34. G. Gaietta, T.J. Deerinck, S.R. Adams, J. Bouwer, O. Tour, D.W. Laird, G.E. Sosinsky, R.Y. Tsien, and M.H. Ellisman Multicolor and electron microscopic imaging of connexin trafficking Science 296 2002 503 507
35. L. Garnier, J.W. Wills, M.F. Verderame, and M. Sudol WW domains and retrovirus budding Nature 381 1996 744 745
36. J.E. Garrus, U.K. von Schwedler, O.W. Pornillos, S.G. Morham, K.H. Zavitz, H.E. Wang, D.A. Wettstein, K.M. Stray, M. Côté, and R.L. Rich Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding Cell 107 2001 55 65
37. H.G. Göttlinger, T. Dorfman, J.G. Sodroski, and W.A. Haseltine Effect of mutations affecting the p6 gag protein on human immunodeficiency virus particle release Proc. Natl. Acad. Sci. USA 88 1991 3195 3199
38. E. Gottwein, J. Bodem, B. Müller, A. Schmechel, H. Zentgraf, and H.G. Kräusslich The Mason-Pfizer monkey virus PPPY and PSAP motifs both contribute to virus release J. Virol. 77 2003 9474 9485
39. S.J. Gould, A.M. Booth, and J.E. Hildreth The Trojan exosome hypothesis Proc. Natl. Acad. Sci. USA 100 2003 10592 10597
40. J.R. Grover, G.N. Llewellyn, F. Soheilian, K. Nagashima, S.L. Veatch, and A. Ono Roles played by capsid-dependent induction of membrane curvature and Gag-ESCRT interactions in tetherin recruitment to HIV-1 assembly sites J. Virol. 87 2013 4650 4664
41. P.I. Hanson, and A. Cashikar Multivesicular Body Morphogenesis Annu. Rev. Cell Dev. Biol. 28 2012 337 362
42. P.I. Hanson, R. Roth, Y. Lin, and J.E. Heuser Plasma membrane deformation by circular arrays of ESCRT-III protein filaments J. Cell Biol. 180 2008 389 402
43. W.M. Henne, N.J. Buchkovich, and S.D. Emr The ESCRT pathway Dev. Cell 21 2011 77 91
44. W.M. Henne, N.J. Buchkovich, Y. Zhao, and S.D. Emr The endosomal sorting complex ESCRT-II mediates the assembly and architecture of ESCRT-III helices Cell 151 2012 356 371
45. C.P. Hill, and M. Babst Structure and function of the membrane deformation AAA ATPase Vps4 Biochim. Biophys. Acta 1823 2012 172 181
46. J. Hoffmann, C. Boehm, K. Himmelsbach, C. Donnerhak, H. Roettger, T.S. Weiss, D. Ploen, and E. Hildt Identification of α-taxilin as an essential factor for the life cycle of hepatitis B virus J. Hepatol. 2013 Published online June 28, 2013
47. M. Huang, J.M. Orenstein, M.A. Martin, and E.O. Freed p6Gag is required for particle production from full-length human immunodeficiency virus type 1 molecular clones expressing protease J. Virol. 69 1995 6810 6818
48. J.H. Hurley, and P.I. Hanson Membrane budding and scission by the ESCRT machinery: it's all in the neck Nat. Rev. Mol. Cell Biol. 11 2010 556 566
49. Y.J. Im, T. Wollert, E. Boura, and J.H. Hurley Structure and function of the ESCRT-II-III interface in multivesicular body biogenesis Dev. Cell 17 2009 234 243
50. Y.J. Im, L. Kuo, X. Ren, P.V. Burgos, X.Z. Zhao, F. Liu, T.R. Burke Jr., J.S. Bonifacino, E.O. Freed, and J.H. Hurley Crystallographic and functional analysis of the ESCRT-I /HIV-1 Gag PTAP interaction Structure 18 2010 1536 1547
51. J.A. Jadwin, V. Rudd, P. Sette, S. Challa, and F. Bouamr Late domain-independent rescue of a release-deficient Moloney murine leukemia virus by the ubiquitin ligase itch J. Virol. 84 2010 704 715
52. J. Jose, J.E. Snyder, and R.J. Kuhn A structural and functional perspective of alphavirus replication and assembly Future Microbiol. 4 2009 837 856
53. A. Joshi, U. Munshi, S.D. Ablan, K. Nagashima, and E.O. Freed Functional replacement of a retroviral late domain by ubiquitin fusion Traffic 9 2008 1972 1983
54. N. Jouvenet, M. Zhadina, P.D. Bieniasz, and S.M. Simon Dynamics of ESCRT protein recruitment during retroviral assembly Nat. Cell Biol. 13 2011 394 401
55. T. Keren-Kaplan, I. Attali, M. Estrin, L.S. Kuo, E. Farkash, M. Jerabek-Willemsen, N. Blutraich, S. Artzi, A. Peri, and E.O. Freed Structure-based in silico identification of ubiquitin-binding domains provides insights into the ALIX-V:ubiquitin complex and retrovirus budding EMBO J. 32 2013 538 551
56. J. Kim, S. Sitaraman, A. Hierro, B.M. Beach, G. Odorizzi, and J.H. Hurley Structural basis for endosomal targeting by the Bro1 domain Dev. Cell 8 2005 937 947
57. Z. Kuang, E.J. Seo, and J. Leis Mechanism of inhibition of retrovirus release from cells by interferon-induced gene ISG15 J. Virol. 85 2011 7153 7161
58. S. Lata, G. Schoehn, A. Jain, R. Pires, J. Piehler, H.G. Gottlinger, and W. Weissenhorn Helical structures of ESCRT-III are disassembled by VPS4 Science 321 2008 1354 1357
59. I. Le Blanc, M.C. Prévost, M.C. Dokhélar, and A.R. Rosenberg The PPPY motif of human T-cell leukemia virus type 1 Gag protein is required early in the budding process J. Virol. 76 2002 10024 10029
60. I. Le Blanc, P.P. Luyet, V. Pons, C. Ferguson, N. Emans, A. Petiot, N. Mayran, N. Demaurex, J. Fauré, and R. Sadoul Endosome-to-cytosol transport of viral nucleocapsids Nat. Cell Biol. 7 2005 653 664
61. S. Lee, A. Joshi, K. Nagashima, E.O. Freed, and J.H. Hurley Structural basis for viral late-domain binding to Alix Nat. Struct. Mol. Biol. 14 2007 194 199
62. J. Leung, A. Yueh, F.S. Appah Jr., B. Yuan, K. de los Santos, and S.P. Goff Interaction of Moloney murine leukemia virus matrix protein with IQGAP EMBO J. 25 2006 2155 2166
63. K.F. Leung, J.B. Dacks, and M.C. Field Evolution of the multivesicular body ESCRT machinery; retention across the eukaryotic lineage Traffic 9 2008 1698 1716
64. M. Li, P.T. Schmitt, Z. Li, T.S. McCrory, B. He, and A.P. Schmitt Mumps virus matrix, fusion, and nucleocapsid proteins cooperate for efficient production of virus-like particles J. Virol. 83 2009 7261 7272
65. C.H. Lin, J.A. MacGurn, T. Chu, C.J. Stefan, and S.D. Emr Arrestin-related ubiquitin-ligase adaptors regulate endocytosis and protein turnover at the cell surface Cell 135 2008 714 725
66. M. Lorizate, and H.G. Kräusslich Role of lipids in virus replication Cold Spring Harb. Perspect. Biol. 3 2011 a004820
67. J. Lu, Y. Qu, Y. Liu, R. Jambusaria, Z. Han, G. Ruthel, B.D. Freedman, and R.N. Harty Host IQGAP1 and Ebola virus VP40 interactions facilitate virus-like particle egress J. Virol. 87 2013 7777 7780
68. M.J. Macias, S. Wiesner, and M. Sudol WW and SH3 domains, two different scaffolds to recognize proline-rich ligands FEBS Lett. 513 2002 30 37
69. J. Martin-Serrano, T. Zang, and P.D. Bieniasz 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
70. J. Martin-Serrano, S.W. Eastman, W. Chung, and P.D. Bieniasz HECT ubiquitin ligases link viral and cellular PPXY motifs to the vacuolar protein-sorting pathway J. Cell Biol. 168 2005 89 101
71. J. McCullough, L.A. Colf, and W.I. Sundquist Membrane fission reactions of the mammalian ESCRT pathway Annu. Rev. Biochem. 82 2013 663 692
72. H.T. McMahon, and E. Boucrot Molecular mechanism and physiological functions of clathrin-mediated endocytosis Nat. Rev. Mol. Cell Biol. 12 2011 517 533
73. E. Morita, V. Sandrin, H.Y. Chung, S.G. Morham, S.P. Gygi, C.K. Rodesch, and W.I. Sundquist Human ESCRT and ALIX proteins interact with proteins of the midbody and function in cytokinesis EMBO J. 26 2007 4215 4227
74. E. Morita, V. Sandrin, J. McCullough, A. Katsuyama, I. Baci Hamilton, and W.I. Sundquist ESCRT-III protein requirements for HIV-1 budding Cell Host Microbe 9 2011 235 242
75. J.F. Nabhan, R. Hu, R.S. Oh, S.N. Cohen, and Q. Lu Formation and release of arrestin domain-containing protein 1-mediated microvesicles (ARMMs) at plasma membrane by recruitment of TSG101 protein Proc. Natl. Acad. Sci. USA 109 2012 4146 4151
76. M. Okumura, A.M. Katsuyama, H. Shibata, and M. Maki VPS37 Isoforms Differentially Modulate the Ternary Complex Formation of ALIX, ALG-2, and ESCRT-I Biosci. Biotechnol. Biochem. 77 2013 1715 1721
77. L.J. Parent, R.P. Bennett, R.C. Craven, T.D. Nelle, N.K. Krishna, J.B. Bowzard, C.B. Wilson, B.A. Puffer, R.C. Montelaro, and J.W. Wills Positionally independent and exchangeable late budding functions of the Rous sarcoma virus and human immunodeficiency virus Gag proteins J. Virol. 69 1995 5455 5460
78. N. Pashkova, L. Gakhar, S.C. Winistorfer, A.B. Sunshine, M. Rich, M.J. Dunham, L. Yu, and R.C. Piper The yeast Alix homolog Bro1 functions as a ubiquitin receptor for protein sorting into multivesicular endosomes Dev. Cell 25 2013 520 533
79. A. Patnaik, V. Chau, and J.W. Wills Ubiquitin is part of the retrovirus budding machinery Proc. Natl. Acad. Sci. USA 97 2000 13069 13074
80. Z. Pei, Y. Bai, and A.P. Schmitt PIV5 M protein interaction with host protein angiomotin-like 1 Virology 397 2010 155 166
81. R. Pires, B. Hartlieb, L. Signor, G. Schoehn, S. Lata, M. Roessle, C. Moriscot, S. Popov, A. Hinz, and M. Jamin A crescent-shaped ALIX dimer targets ESCRT-III CHMP4 filaments Structure 17 2009 843 856
82. S. Popov, E. Popova, M. Inoue, and H.G. Göttlinger Human immunodeficiency virus type 1 Gag engages the Bro1 domain of ALIX/AIP1 through the nucleocapsid J. Virol. 82 2008 1389 1398
83. S. Popov, E. Popova, M. Inoue, and H.G. Göttlinger Divergent Bro1 domains share the capacity to bind human immunodeficiency virus type 1 nucleocapsid and to enhance virus-like particle production J. Virol. 83 2009 7185 7193
84. B.A. Puffer, L.J. Parent, J.W. Wills, and R.C. Montelaro Equine infectious anemia virus utilizes a YXXL motif within the late assembly domain of the Gag p9 protein J. Virol. 71 1997 6541 6546
85. D. Putterman, R.B. Pepinsky, and V.M. Vogt Ubiquitin in avian leukosis virus particles Virology 176 1990 633 637
86. V. Ramakrishnaiah, C. Thumann, I. Fofana, F. Habersetzer, Q. Pan, P.E. de Ruiter, R. Willemsen, J.A. Demmers, V. Stalin Raj, and G. Jenster Exosome-mediated transmission of hepatitis C virus between human hepatoma Huh7.5 cells Proc. Natl. Acad. Sci. USA 110 2013 13109 13113
87. G. Raposo, and W. Stoorvogel Extracellular vesicles: exosomes, microvesicles, and friends J. Cell Biol. 200 2013 373 383
88. S. Rauch, and J. Martin-Serrano Multiple interactions between the ESCRT machinery and arrestin-related proteins: implications for PPXY-dependent budding J. Virol. 85 2011 3546 3556
89. J.S. Rossman, X. Jing, G.P. Leser, and R.A. Lamb Influenza virus M2 protein mediates ESCRT-independent membrane scission Cell 142 2010 902 913
90. D. Rotin, and S. Kumar Physiological functions of the HECT family of ubiquitin ligases Nat. Rev. Mol. Cell Biol. 10 2009 398 409
91. R.K. Rowe, J.W. Suszko, and A. Pekosz Roles for the recycling endosome, Rab8, and Rab11 in hantavirus release from epithelial cells Virology 382 2008 239 249
92. S. Saksena, J. Wahlman, D. Teis, A.E. Johnson, and S.D. Emr Functional reconstitution of ESCRT-III assembly and disassembly Cell 136 2009 97 109
93. R.Y. Samson, and S.D. Bell Ancient ESCRTs and the evolution of binary fission Trends Microbiol. 17 2009 507 513
94. A.P. Schmitt, G.P. Leser, E. Morita, W.I. Sundquist, and R.A. Lamb Evidence for a new viral late-domain core sequence, FPIV, necessary for budding of a paramyxovirus J. Virol. 79 2005 2988 2997
95. U. Schubert, L.C. Antón, J. Gibbs, C.C. Norbury, J.W. Yewdell, and J.R. Bennink Rapid degradation of a large fraction of newly synthesized proteins by proteasomes Nature 404 2000 770 774
96. P. Sette, K. Nagashima, R.C. Piper, and F. Bouamr Ubiquitin conjugation to Gag is essential for ESCRT-mediated HIV-1 budding Retrovirology 10 2013 79
97. S.B. Shields, and R.C. Piper How ubiquitin functions with ESCRTs Traffic 12 2011 1306 1317
98. J.C. Snyder, R.Y. Samson, S.K. Brumfield, S.D. Bell, and M.J. Young Functional interplay between a virus and the ESCRT machinery in Archaea Proc. Natl. Acad. Sci. USA 110 2013 10783 10787
99. J.L. Spidel, R.C. Craven, C.B. Wilson, A. Patnaik, H. Wang, L.M. Mansky, and J.W. Wills Lysines close to the Rous sarcoma virus late domain critical for budding J. Virol. 78 2004 10606 10616
100. B. Strack, A. Calistri, M.A. Accola, G. Palu, and H.G. Gottlinger A role for ubiquitin ligase recruitment in retrovirus release Proc. Natl. Acad. Sci. USA 97 2000 13063 13068
101. B. Strack, A. Calistri, S. Craig, E. Popova, and H.G. Göttlinger AIP1/ALIX is a binding partner for HIV-1 p6 and EIAV p9 functioning in virus budding Cell 114 2003 689 699
102. W.I. Sundquist, and H.G. Kräusslich HIV-1 assembly, budding, and maturation Cold Spring Harb Perspect Med 2 2012 a006924
103. G.M. Taylor, P.I. Hanson, and M. Kielian Ubiquitin depletion and dominant-negative VPS4 inhibit rhabdovirus budding without affecting alphavirus budding J. Virol. 81 2007 13631 13639
104. D. Teis, S. Saksena, and S.D. Emr Ordered assembly of the ESCRT-III complex on endosomes is required to sequester cargo during MVB formation Dev. Cell 15 2008 578 589
105. Y. Usami, S. Popov, and H.G. Göttlinger Potent rescue of human immunodeficiency virus type 1 late domain mutants by ALIX/AIP1 depends on its CHMP4 binding site J. Virol. 81 2007 6614 6622
106. Y. Usami, S. Popov, E. Popova, and H.G. Göttlinger Efficient and specific rescue of human immunodeficiency virus type 1 budding defects by a Nedd4-like ubiquitin ligase J. Virol. 82 2008 4898 4907
107. T.J. Utley, N.A. Ducharme, V. Varthakavi, B.E. Shepherd, P.J. Santangelo, M.E. Lindquist, J.R. Goldenring, and J.E. Crowe Jr. Respiratory syncytial virus uses a Vps4-independent budding mechanism controlled by Rab11-FIP2 Proc. Natl. Acad. Sci. USA 105 2008 10209 10214
108. L. VerPlank, F. Bouamr, T.J. LaGrassa, B. Agresta, A. Kikonyogo, J. Leis, and C.A. Carter Tsg101, a homologue of ubiquitin-conjugating (E2) enzymes, binds the L domain in HIV type 1 Pr55(Gag) Proc. Natl. Acad. Sci. USA 98 2001 7724 7729
109. O. Vincent, L. Rainbow, J. Tilburn, H.N. Arst Jr., and M.A. Peñalva YPXL/I is a protein interaction motif recognized by aspergillus PalA and its human homologue, AIP1/Alix Mol. Cell. Biol. 23 2003 1647 1655
110. E.R. Weiss, E. Popova, H. Yamanaka, H.C. Kim, J.M. Huibregtse, and H. Göttlinger Rescue of HIV-1 release by targeting widely divergent NEDD4-type ubiquitin ligases and isolated catalytic HECT domains to Gag PLoS Pathog. 6 2010 e1001107
111. W. Weissenhorn, E. Poudevigne, G. Effantin, and P. Bassereau How to get out: ssRNA enveloped viruses and membrane fission Curr Opin Virol 3 2013 159 167
112. C. Wirblich, B. Bhattacharya, and P. Roy Nonstructural protein 3 of bluetongue virus assists virus release by recruiting ESCRT-I protein Tsg101 J. Virol. 80 2006 460 473
113. T. Wollert, and J.H. Hurley Molecular mechanism of multivesicular body biogenesis by ESCRT complexes Nature 464 2010 864 869
114. M. Zhadina, M.O. McClure, M.C. Johnson, and P.D. Bieniasz Ubiquitin-dependent virus particle budding without viral protein ubiquitination Proc. Natl. Acad. Sci. USA 104 2007 20031 20036
115. Q. Zhai, R.D. Fisher, H.Y. Chung, D.G. Myszka, W.I. Sundquist, and C.P. Hill Structural and functional studies of ALIX interactions with YPX(n)L late domains of HIV-1 and EIAV Nat. Struct. Mol. Biol. 15 2008 43 49
116. Q. Zhai, M.B. Landesman, H.Y. Chung, A. Dierkers, C.M. Jeffries, J. Trewhella, C.P. Hill, and W.I. Sundquist Activation of the retroviral budding factor ALIX J. Virol. 85 2011 9222 9226
117. Q. Zhai, M.B. Landesman, H. Robinson, W.I. Sundquist, and C.P. Hill Identification and structural characterization of the ALIX-binding late domains of simian immunodeficiency virus SIVmac239 and SIVagmTan-1 J. Virol. 85 2011 632 637
118. F. Zhang, T. Zang, S.J. Wilson, M.C. Johnson, and P.D. Bieniasz Clathrin facilitates the morphogenesis of retrovirus particles PLoS Pathog. 7 2011 e1002119
119. X. Zhou, J. Si, J. Corvera, G.E. Gallick, and J. Kuang Decoding the intrinsic mechanism that prohibits ALIX interaction with ESCRT and viral proteins Biochem. J. 432 2010 525 534