1932

Abstract

The endosomal sorting complexes required for transport (ESCRT) pathway mediates cellular membrane remodeling and fission reactions. The pathway comprises five core complexes: ALIX, ESCRT-I, ESCRT-II, ESCRT-III, and Vps4. These soluble complexes are typically recruited to target membranes by site-specific adaptors that bind one or both of the early-acting ESCRT factors: ALIX and ESCRT-I/ESCRT-II. These factors, in turn, nucleate assembly of ESCRT-III subunits into membrane-bound filaments that recruit the AAA ATPase Vps4. Together, ESCRT-III filaments and Vps4 remodel and sever membranes. Here, we review recent advances in our understanding of the structures, activities, and mechanisms of the ESCRT-III and Vps4 machinery, including the first high-resolution structures of ESCRT-III filaments, the assembled Vps4 enzyme in complex with an ESCRT-III substrate, the discovery that ESCRT-III/Vps4 complexes can promote both inside-out and outside-in membrane fission reactions, and emerging mechanistic models for ESCRT-mediated membrane fission.

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2018-10-06
2024-04-20
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Literature Cited

  1. Adell MAY, Migliano SM, Upadhyayula S, Bykov YS, Sprenger S et al. 2017. Recruitment dynamics of ESCRT-III and Vps4 to endosomes and implications for reverse membrane budding. eLife 6:e31652
    [Google Scholar]
  2. Allison R, Lumb JH, Fassier C, Connell JW, Ten Martin D et al. 2013. An ESCRT-spastin interaction promotes fission of recycling tubules from the endosome. J. Cell Biol. 202:527–43
    [Google Scholar]
  3. Babst M, Davies BA, Katzmann DJ 2011. Regulation of Vps4 during MVB sorting and cytokinesis. Traffic 12:1298–305
    [Google Scholar]
  4. Bajorek M, Schubert HL, McCullough J, Langelier C, Eckert DM et al. 2009. Structural basis for ESCRT-III protein autoinhibition. Nat. Struct. Mol. Biol. 16:754–62
    [Google Scholar]
  5. Barajas D, Jiang Y, Nagy PD 2009. A unique role for the host ESCRT proteins in replication of Tomato bushy stunt virus. PLOS Pathog 5:e1000705
    [Google Scholar]
  6. Baumgartel V, Ivanchenko S, Dupont A, Sergeev M, Wiseman PW et al. 2011. Live-cell visualization of dynamics of HIV budding site interactions with an ESCRT component. Nat. Cell Biol. 13:469–74
    [Google Scholar]
  7. Bleck M, Itano MS, Johnson DS, Thomas VK, North AJ et al. 2014. Temporal and spatial organization of ESCRT protein recruitment during HIV-1 budding. PNAS 111:12211–16
    [Google Scholar]
  8. Bryant NJ, Stevens TH 1998. Vacuole biogenesis in Saccharomyces cerevisiae: protein transport pathways to the yeast vacuole. Microbiol. Mol. Biol. Rev. 62:230–47
    [Google Scholar]
  9. Buchkovich NJ, Henne WM, Tang S, Emr SD 2013. Essential N-terminal insertion motif anchors the ESCRT-III filament during MVB vesicle formation. Dev. Cell 27:201–14
    [Google Scholar]
  10. Cannon KS, Woods BL, Gladfelter AS 2017. The unsolved problem of how cells sense micron-scale curvature. Trends Biochem. Sci. 42:961–76
    [Google Scholar]
  11. Carlson LA, Shen QT, Pavlin MR, Hurley JH 2015. ESCRT filaments as spiral springs. Dev. Cell 35:397–98
    [Google Scholar]
  12. Carlton JG, Caballe A, Agromayor M, Kloc M, Martin-Serrano J 2012. ESCRT-III governs the Aurora B–mediated abscission checkpoint through CHMP4C. Science 336:220–25
    [Google Scholar]
  13. Carlton JG, Martin-Serrano J 2007. Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery. Science 316:1908–12
    [Google Scholar]
  14. Cashikar AG, Shim S, Roth R, Maldazys MR, Heuser JE, Hanson PI 2014. Structure of cellular ESCRT-III spirals and their relationship to HIV budding. eLife 3:e02184
    [Google Scholar]
  15. Caspi Y, Dekker C 2018. Dividing the archaeal way: the ancient Cdv cell-division machinery. Front. Microbiol. 9:174
    [Google Scholar]
  16. Chiaruttini N, Redondo-Morata L, Colom A, Humbert F, Lenz M et al. 2015. Relaxation of loaded ESCRT-III spiral springs drives membrane deformation. Cell 163:866–79
    [Google Scholar]
  17. Chiaruttini N, Roux A 2017. Dynamic and elastic shape transitions in curved ESCRT-III filaments. Curr. Opin. Cell Biol. 47:126–35
    [Google Scholar]
  18. Choudhuri K, Llodra J, Roth EW, Tsai J, Gordo S et al. 2014. Polarized release of T-cell-receptor-enriched microvesicles at the immunological synapse. Nature 507:118–23
    [Google Scholar]
  19. Christ L, Raiborg C, Wenzel EM, Campsteijn C, Stenmark H 2017. Cellular functions and molecular mechanisms of the ESCRT membrane-scission machinery. Trends Biochem. Sci. 42:42–56
    [Google Scholar]
  20. Crespo-Yàñez X, Aguilar-Gurrieri C, Jacomin AC, Journet A, Mortier M et al. 2018. CHMP1B is a target of USP8/UBPY regulated by ubiquitin during endocytosis. PLOS Genet 14:6e1007456
    [Google Scholar]
  21. Curwin AJ, Brouwers N, Alonso YAM, Teis D, Turacchio G et al. 2016. ESCRT-III drives the final stages of CUPS maturation for unconventional protein secretion. eLife 5:e16299
    [Google Scholar]
  22. Denais CM, Gilbert RM, Isermann P, McGregor AL, te Lindert M et al. 2016. Nuclear envelope rupture and repair during cancer cell migration. Science 352:353–58
    [Google Scholar]
  23. Deville C, Carroni M, Franke KB, Topf M, Bukau B et al. 2017. Structural pathway of regulated substrate transfer and threading through an Hsp100 disaggregase. Sci. Adv. 3:e1701726
    [Google Scholar]
  24. Diaz A, Zhang J, Ollwerther A, Wang X, Ahlquist P 2015. Host ESCRT proteins are required for bromovirus RNA replication compartment assembly and function. PLOS Pathog 11:e1004742
    [Google Scholar]
  25. Diener DR, Lupetti P, Rosenbaum JL 2015. Proteomic analysis of isolated ciliary transition zones reveals the presence of ESCRT proteins. Curr. Biol. 25:379–84
    [Google Scholar]
  26. Drusenheimer N, Migdal B, Jackel S, Tveriakhina L, Scheider K et al. 2015. The mammalian orthologs of Drosophila Lgd, CC2D1A and CC2D1B, function in the endocytic pathway, but their individual loss of function does not affect Notch signalling. PLOS Genet 11:e1005749
    [Google Scholar]
  27. Effantin G, Dordor A, Sandrin V, Martinelli N, Sundquist WI et al. 2013. ESCRT-III CHMP2A and CHMP3 form variable helical polymers in vitro and act synergistically during HIV-1 budding. Cell. Microbiol. 15:213–26
    [Google Scholar]
  28. Elia N, Fabrikant G, Kozlov MM, Lippincott-Schwartz J 2012. Computational model of cytokinetic abscission driven by ESCRT-III polymerization and remodeling. Biophys. J. 102:2309–20
    [Google Scholar]
  29. Elia N, Sougrat R, Spurlin TA, Hurley JH, Lippincott-Schwartz J 2011. Dynamics of endosomal sorting complex required for transport (ESCRT) machinery during cytokinesis and its role in abscission. PNAS 108:4846–51
    [Google Scholar]
  30. Ettema TJ, Bernander R 2009. Cell division and the ESCRT complex: a surprise from the archaea. Commun. Integr. Biol. 2:86–88
    [Google Scholar]
  31. Fabrikant G, Lata S, Riches JD, Briggs JA, Weissenhorn W, Kozlov MM 2009. Computational model of membrane fission catalyzed by ESCRT-III. PLOS Comput. Biol. 5:e1000575
    [Google Scholar]
  32. Feng Z, Hensley L, McKnight KL, Hu F, Madden V et al. 2013. A pathogenic picornavirus acquires an envelope by hijacking cellular membranes. Nature 496:367–71
    [Google Scholar]
  33. Frankel EB, Audhya A 2018. ESCRT-dependent cargo sorting at multivesicular endosomes. Semin. Cell Dev. Biol. 74:4–10
    [Google Scholar]
  34. Frost A, Perera R, Roux A, Spasov K, Destaing O et al. 2008. Structural basis of membrane invagination by F-BAR domains. Cell 132:807–17
    [Google Scholar]
  35. Fyfe I, Schuh AL, Edwardson JM, Audhya A 2011. Association of the endosomal sorting complex ESCRT-II with the Vps20 subunit of ESCRT-III generates a curvature-sensitive complex capable of nucleating ESCRT-III filaments. J. Biol. Chem. 286:34262–70
    [Google Scholar]
  36. Gao C, Zhuang X, Shen J, Jiang L 2017. Plant ESCRT complexes: moving beyond endosomal sorting. Trends Plant Sci 22:986–98
    [Google Scholar]
  37. Gates SN, Yokom AL, Lin J, Jackrel ME, Rizo AN et al. 2017. Ratchet-like polypeptide translocation mechanism of the AAA+ disaggregase Hsp104. Science 357:273–79
    [Google Scholar]
  38. Goliand I, Dadosh T, Elia N 2017. Resolving ESCRT-III spirals at the intercellular bridge of dividing cells using 3D STORM imaging. bioRxiv 194613. https://doi.org/10.1101/194613
    [Crossref]
  39. Gu M, LaJoie D, Chen OS, von Appen A, Ladinsky MS et al. 2017. LEM2 recruits CHMP7 for ESCRT-mediated nuclear envelope closure in fission yeast and human cells. PNAS 114:E2166–75
    [Google Scholar]
  40. Guerrier S, Coutinho-Budd J, Sassa T, Gresset A, Jordan NV et al. 2009. The F-BAR domain of srGAP2 induces membrane protrusions required for neuronal migration and morphogenesis. Cell 138:990–1004
    [Google Scholar]
  41. Guizetti J, Schermelleh L, Mantler J, Maar S, Poser I et al. 2011. Cortical constriction during abscission involves helices of ESCRT-III-dependent filaments. Science 331:1616–20
    [Google Scholar]
  42. Han H, Monroe N, Sundquist WI, Shen PS, Hill CP 2017. The AAA ATPase Vps4 binds ESCRT-III substrates through a repeating array of dipeptide-binding pockets. eLife 6:e31324
    [Google Scholar]
  43. Han H, Monroe N, Votteler J, Shakya B, Sundquist WI, Hill CP 2015. Binding of substrates to the central pore of the Vps4 ATPase is autoinhibited by the microtubule interacting and trafficking (MIT) domain and activated by MIT interacting motifs (MIMs). J. Biol. Chem. 290:13490–99
    [Google Scholar]
  44. Hanson PI, Roth R, Lin Y, Heuser JE 2008. Plasma membrane deformation by circular arrays of ESCRT-III protein filaments. J. Cell Biol. 180:389–402
    [Google Scholar]
  45. Harrison SC 2004. Whither structural biology. ? Nat. Struct. Mol. Biol. 11:12–15
    [Google Scholar]
  46. Henne WM, Buchkovich NJ, Zhao Y, Emr SD 2012. The endosomal sorting complex ESCRT-II mediates the assembly and architecture of ESCRT-III helices. Cell 151:356–71
    [Google Scholar]
  47. Henne WM, Stenmark H, Emr SD 2013. Molecular mechanisms of the membrane sculpting ESCRT pathway. Cold Spring Harb. Perspect. Biol. 5:a016766
    [Google Scholar]
  48. Hierro A, Sun J, Rusnak AS, Kim J, Prag G et al. 2004. Structure of the ESCRT-II endosomal trafficking complex. Nature 431:221–25
    [Google Scholar]
  49. Hurley JH, Yang D 2008. MIT domainia. Dev. Cell 14:6–8
    [Google Scholar]
  50. Im YJ, Wollert T, Boura E, Hurley JH 2009. Structure and function of the ESCRT-II-III interface in multivesicular body biogenesis. Dev. Cell 17:234–43
    [Google Scholar]
  51. Jackson CE, Scruggs BS, Schaffer JE, Hanson PI 2017. Effects of inhibiting VPS4 support: a general role for ESCRTs in extracellular vesicle biogenesis. Biophys. J. 113:1342–52
    [Google Scholar]
  52. Jimenez AJ, Maiuri P, Lafaurie-Janvore J, Divoux S, Piel M, Perez F 2014. ESCRT machinery is required for plasma membrane repair. Science 343:1247136
    [Google Scholar]
  53. Johnson DS, Bleck M, Simon SM 2018. Timing of ESCRT-III protein recruitment and membrane scission during HIV-1 assembly. eLife 7e36221
  54. Jouvenet N, Zhadina M, Bieniasz PD, Simon SM 2011. Dynamics of ESCRT protein recruitment during retroviral assembly. Nat. Cell Biol. 13:394–401
    [Google Scholar]
  55. Juan T, Fürthauer M 2018. Biogenesis and function of ESCRT-dependent extracellular vesicles. Semin. Cell Dev. Biol. 74:66–77
    [Google Scholar]
  56. Kieffer C, Skalicky JJ, Morita E, De Domenico I, Ward DM et al. 2008. Two distinct modes of ESCRT-III recognition are required for VPS4 functions in lysosomal protein targeting and HIV-1 budding. Dev. Cell 15:62–73
    [Google Scholar]
  57. Kollman JM, Merdes A, Mourey L, Agard DA 2011. Microtubule nucleation by gamma-tubulin complexes. Nat. Rev. Mol. Cell Biol. 12:709–21
    [Google Scholar]
  58. Lata S, Roessle M, Solomons J, Jamin M, Gottlinger HG et al. 2008.a Structural basis for autoinhibition of ESCRT-III CHMP3. J. Mol. Biol. 378:818–27
    [Google Scholar]
  59. Lata S, Schoehn G, Jain A, Pires R, Piehler J et al. 2008.b Helical structures of ESCRT-III are disassembled by VPS4. Science 321:1354–57
    [Google Scholar]
  60. Lata S, Schoehn G, Solomons J, Pires R, Gottlinger HG, Weissenhorn W 2009. Structure and function of ESCRT-III. Biochem. Soc. Trans. 37:156–60
    [Google Scholar]
  61. Lee CP, Liu PT, Kung HN, Su MT, Chua HH et al. 2012. The ESCRT machinery is recruited by the viral BFRF1 protein to the nucleus-associated membrane for the maturation of Epstein-Barr Virus. PLOS Pathog 8:e1002904
    [Google Scholar]
  62. Lee HH, Elia N, Ghirlando R, Lippincott-Schwartz J, Hurley JH 2008. Midbody targeting of the ESCRT machinery by a noncanonical coiled coil in CEP55. Science 322:576–80
    [Google Scholar]
  63. Lee IH, Kai H, Carlson LA, Groves JT, Hurley JH 2015. Negative membrane curvature catalyzes nucleation of endosomal sorting complex required for transport (ESCRT)-III assembly. PNAS 112:15892–97
    [Google Scholar]
  64. Lenz M, Crow DJ, Joanny JF 2009. Membrane buckling induced by curved filaments. Phys. Rev. Lett. 103:038101
    [Google Scholar]
  65. Lin Y, Kimpler LA, Naismith TV, Lauer JM, Hanson PI 2005. Interaction of the mammalian endosomal sorting complex required for transport (ESCRT) III protein hSnf7-1 with itself, membranes, and the AAA+ ATPase SKD1. J. Biol. Chem. 280:12799–809
    [Google Scholar]
  66. Lindas AC, Karlsson EA, Lindgren MT, Ettema TJ, Bernander R 2008. A unique cell division machinery in the Archaea. PNAS 105:18942–46
    [Google Scholar]
  67. Lippincott-Schwartz J, Freed EO, van Engelenburg SB 2017. A consensus view of ESCRT-mediated human immunodeficiency virus type 1 abscission. Annu. Rev. Virol. 4:309–25
    [Google Scholar]
  68. Loncle N, Agromayor M, Martin-Serrano J, Williams DW 2015. An ESCRT module is required for neuron pruning. Sci. Rep. 5:8461
    [Google Scholar]
  69. Martinelli N, Hartlieb B, Usami Y, Sabin C, Dordor A et al. 2012. CC2D1A is a regulator of ESCRT-III CHMP4B. J. Mol. Biol. 419:75–88
    [Google Scholar]
  70. Mast FD, Herricks T, Strehler KM, Miller LM, Saleem RA et al. 2018. ESCRT-III is required for scissioning new peroxisomes from the endoplasmic reticulum. J. Cell Biol. https://doi.org/10.1083/jcb.201706044
    [Crossref]
  71. Matusek T, Wendler F, Poles S, Pizette S, D'Angelo G et al. 2014. The ESCRT machinery regulates the secretion and long-range activity of Hedgehog. Nature 516:99–103
    [Google Scholar]
  72. McCullough J, Clippinger AK, Talledge N, Skowyra ML, Saunders MG et al. 2015. Structure and membrane remodeling activity of ESCRT-III helical polymers. Science 350:1548–51
    [Google Scholar]
  73. McCullough J, Fisher RD, Whitby FG, Sundquist WI, Hill CP 2008. ALIX-CHMP4 interactions in the human ESCRT pathway. PNAS 105:7687–91
    [Google Scholar]
  74. McMahon HT, Boucrot E 2015. Membrane curvature at a glance. J. Cell Sci. 128:1065–70
    [Google Scholar]
  75. McMillan BJ, Tibbe C, Drabek AA, Seegar TCM, Blacklow SC, Klein T 2017. Structural basis for regulation of ESCRT-III complexes by Lgd. Cell Rep 19:1750–57
    [Google Scholar]
  76. McMillan BJ, Tibbe C, Jeon H, Drabek AA, Klein T, Blacklow SC 2016. Electrostatic interactions between elongated monomers drive filamentation of Drosophila Shrub, a metazoan ESCRT-III protein. Cell Rep 16:1211–17
    [Google Scholar]
  77. Merrill SA, Hanson PI 2010. Activation of human VPS4A by ESCRT-III proteins reveals ability of substrates to relieve enzyme autoinhibition. J. Biol. Chem. 285:35428–38
    [Google Scholar]
  78. Mierzwa BE, Chiaruttini N, Redondo-Morata L, von Filseck JM, Konig J et al. 2017. Dynamic subunit turnover in ESCRT-III assemblies is regulated by Vps4 to mediate membrane remodelling during cytokinesis. Nat. Cell Biol. 19:787–98
    [Google Scholar]
  79. Mim C, Cui H, Gawronski-Salerno JA, Frost A, Lyman E et al. 2012. Structural basis of membrane bending by the N-BAR protein endophilin. Cell 149:137–45
    [Google Scholar]
  80. Mim C, Unger VM 2012. Membrane curvature and its generation by BAR proteins. Trends Biochem. Sci. 37:526–33
    [Google Scholar]
  81. Monroe N, Han H, Shen PS, Sundquist WI, Hill CP 2017. Structural basis of protein translocation by the Vps4-Vta1 AAA ATPase. eLife 6:e024487
    [Google Scholar]
  82. Monroe N, Hill CP 2016. Meiotic clade AAA ATPases: protein polymer disassembly machines. J. Mol. Biol. 428:1897–911
    [Google Scholar]
  83. Morita E, Sandrin V, Chung HY, Morham SG, Gygi SP et al. 2007. Human ESCRT and ALIX proteins interact with proteins of the midbody and function in cytokinesis. EMBO J 26:4215–27
    [Google Scholar]
  84. Mu R, Dussupt V, Jiang J, Sette P, Rudd V et al. 2012. Two distinct binding modes define the interaction of Brox with the C-terminal tails of CHMP5 and CHMP4B. Structure 20:887–98
    [Google Scholar]
  85. Muziol T, Pineda-Molina E, Ravelli RB, Zamborlini A, Usami Y et al. 2006. Structural basis for budding by the ESCRT-III factor CHMP3. Dev. Cell 10:821–30
    [Google Scholar]
  86. Nabhan JF, Hu R, Oh RS, Cohen SN, Lu Q 2012. Formation and release of arrestin domain-containing protein 1–mediated microvesicles (ARMMs) at plasma membrane by recruitment of TSG101 protein. PNAS 109:4146–51
    [Google Scholar]
  87. Obita T, Saksena S, Ghazi-Tabatabai S, Gill DJ, Perisic O et al. 2007. Structural basis for selective recognition of ESCRT-III by the AAA ATPase Vps4. Nature 449:735–39
    [Google Scholar]
  88. Olmos Y, Hodgson L, Mantell J, Verkade P, Carlton JG 2015. ESCRT-III controls nuclear envelope reformation. Nature 522:236–39
    [Google Scholar]
  89. Olmos Y, Perdrix-Rosell A, Carlton JG 2016. Membrane binding by CHMP7 coordinates ESCRT-III-dependent nuclear envelope reformation. Curr. Biol. 26:2635–41
    [Google Scholar]
  90. Peel S, Macheboeuf P, Martinelli N, Weissenhorn W 2011. Divergent pathways lead to ESCRT-III-catalyzed membrane fission. Trends Biochem. Sci. 36:199–210
    [Google Scholar]
  91. Pires R, Hartlieb B, Signor L, Schoehn G, Lata S et al. 2009. A crescent-shaped ALIX dimer targets ESCRT-III CHMP4 filaments. Structure 17:843–56
    [Google Scholar]
  92. Puchades C, Rampello AJ, Shin M, Giuliano CJ, Wiseman RL et al. 2017. Structure of the mitochondrial inner membrane AAA+ protease YME1 gives insight into substrate processing. Science 358:eaao0464
    [Google Scholar]
  93. Pykalainen A, Boczkowska M, Zhao HX, Saarikangas J, Rebowski G et al. 2011. Pinkbar is an epithelial-specific BAR domain protein that generates planar membrane structures. Nat. Struct. Mol. Biol. 18:902–7
    [Google Scholar]
  94. Raab M, Gentili M, de Belly H, Thiam HR, Vargas P et al. 2016. ESCRT III repairs nuclear envelope ruptures during cell migration to limit DNA damage and cell death. Science 352:359–62
    [Google Scholar]
  95. Ripstein ZA, Huang R, Augustyniak R, Kay LE, Rubinstein JL 2017. Structure of a AAA+ unfoldase in the process of unfolding substrate. eLife 6:e25754
    [Google Scholar]
  96. Rottner K, Faix J, Bogdan S, Linder S, Kerkhoff E 2017. Actin assembly mechanisms at a glance. J. Cell Sci. 130:3427–35
    [Google Scholar]
  97. Saksena S, Wahlman J, Teis D, Johnson AE, Emr SD 2009. Functional reconstitution of ESCRT-III assembly and disassembly. Cell 136:97–109
    [Google Scholar]
  98. Samson RY, Obita T, Freund SM, Williams RL, Bell SD 2008. A role for the ESCRT system in cell division in archaea. Science 322:1710–13
    [Google Scholar]
  99. Sauer RT, Baker TA 2011. AAA+ proteases: ATP-fueled machines of protein destruction. Annu. Rev. Biochem. 80:587–612
    [Google Scholar]
  100. Scheffer LL, Sreetama SC, Sharma N, Medikayala S, Brown KJ et al. 2014. Mechanism of Ca2+-triggered ESCRT assembly and regulation of cell membrane repair. Nat. Commun. 5:5646
    [Google Scholar]
  101. Schoeneberg J, Yan S, Righini M, Pavlin MR, Lee I-H et al. 2018. ATP-dependent force generation and membrane scission by ESCRT-III and Vps4. bioRxiv ; https://doi.org/10.1101/262170
    [Crossref]
  102. Schöneberg J, Lee IH, Iwasa JH, Hurley JH 2017. Reverse-topology membrane scission by the ESCRT proteins. Nat. Rev. Mol. Cell Biol. 18:5–17
    [Google Scholar]
  103. Schuh AL, Hanna M, Quinney K, Wang L, Sarkeshik A et al. 2015. The VPS-20 subunit of the endosomal sorting complex ESCRT-III exhibits an open conformation in the absence of upstream activation. Biochem. J. 466:625–37
    [Google Scholar]
  104. Scourfield EJ, Martin-Serrano J 2017. Growing functions of the ESCRT machinery in cell biology and viral replication. Biochem. Soc. Trans. 45:613–34
    [Google Scholar]
  105. Shen QT, Schuh AL, Zheng Y, Quinney K, Wang L et al. 2014. Structural analysis and modeling reveals new mechanisms governing ESCRT-III spiral filament assembly. J. Cell Biol. 206:763–77
    [Google Scholar]
  106. Shim S, Merrill SA, Hanson PI 2008. Novel interactions of ESCRT-III with LIP5 and VPS4 and their implications for ESCRT-III disassembly. Mol. Biol. Cell 19:2661–72
    [Google Scholar]
  107. Shimada A, Niwa H, Tsujita K, Suetsugu S, Nitta K et al. 2007. Curved EFC/F-BAR-domain dimers are joined end to end into a filament for membrane invagination in endocytosis. Cell 129:761–72
    [Google Scholar]
  108. Simunovic M, Voth GA, Callan-Jones A, Bassereau P 2015. When physics takes over: BAR proteins and membrane curvature. Trends Cell Biol 25:780–92
    [Google Scholar]
  109. Skalicky JJ, Arii J, Wenzel DM, Stubblefield WM, Katsuyama A et al. 2012. Interactions of the human LIP5 regulatory protein with endosomal sorting complexes required for transport. J. Biol. Chem. 287:43910–26
    [Google Scholar]
  110. Skowyra ML, Schlesinger PH, Naismith TV, Hanson PI 2018. Triggered recruitment of ESCRT machinery promotes endolysosomal repair. Science 359:aar5708
    [Google Scholar]
  111. Solomons J, Sabin C, Poudevigne E, Usami Y, Hulsik DL et al. 2011. Structural basis for ESCRT-III CHMP3 recruitment of AMSH. Structure 19:1149–59
    [Google Scholar]
  112. Sporny M, Guez-Haddad J, Kreusch A, Shakartzi S, Neznansky A et al. 2017. Structural history of human SRGAP2 proteins. Mol. Biol. Evol. 34:1463–78
    [Google Scholar]
  113. Stoten CL, Carlton JG 2018. ESCRT-dependent control of membrane remodelling during cell division. Semin. Cell Dev. Biol. 74:50–65
    [Google Scholar]
  114. Stuchell-Brereton MD, Skalicky JJ, Kieffer C, Karren MA, Ghaffarian S, Sundquist WI 2007. ESCRT-III recognition by VPS4 ATPases. Nature 449:740–44
    [Google Scholar]
  115. Su M, Guo EZ, Ding X, Li Y, Tarrasch JT et al. 2017. Mechanism of Vps4 hexamer function revealed by cryo-EM. Sci. Adv. 3:e1700325
    [Google Scholar]
  116. Sun S, Li L, Yang F, Wang X, Fan F et al. 2017. Cryo-EM structures of the ATP-bound Vps4(E233Q) hexamer and its complex with Vta1 at near-atomic resolution. Nat. Commun. 8:16064
    [Google Scholar]
  117. Talledge N, McCullough J, Wenzel D, Nguyen HC, Lalonde JM et al. 2018. The ESCRT-III proteins IST1 and CHMP1B assemble around nucleic acids. bioRxiv 386532. https://doi.org/10.1101/386532
    [Crossref]
  118. Tang S, Buchkovich NJ, Henne WM, Banjade S, Kim YJ, Emr SD 2016. ESCRT-III activation by parallel action of ESCRT-I/II and ESCRT-0/Bro1 during MVB biogenesis. eLife 5:e15507
    [Google Scholar]
  119. Tang S, Henne WM, Borbat PP, Buchkovich NJ, Freed JH et al. 2015. Structural basis for activation, assembly and membrane binding of ESCRT-III Snf7 filaments. eLife 4:e12548
    [Google Scholar]
  120. Teis D, Saksena S, Judson BL, Emr SD 2010. ESCRT-II coordinates the assembly of ESCRT-III filaments for cargo sorting and multivesicular body vesicle formation. EMBO J 29:871–83
    [Google Scholar]
  121. Teo H, Perisic O, Gonzalez B, Williams RL 2004. ESCRT-II, an endosome-associated complex required for protein sorting: crystal structure and interactions with ESCRT-III and membranes. Dev. Cell 7:559–69
    [Google Scholar]
  122. Traer CJ, Rutherford AC, Palmer KJ, Wassmer T, Oakley J et al. 2007. SNX4 coordinates endosomal sorting of TfnR with dynein-mediated transport into the endocytic recycling compartment. Nat. Cell Biol. 9:1370–80
    [Google Scholar]
  123. Troost T, Jaeckel S, Ohlenhard N, Klein T 2012. The tumour suppressor Lethal (2) giant discs is required for the function of the ESCRT-III component Shrub/CHMP4. J. Cell Sci. 125:763–76
    [Google Scholar]
  124. Usami Y, Popov S, Weiss ER, Vriesema-Magnuson C, Calistri A, Gottlinger HG 2012. Regulation of CHMP4/ESCRT-III function in human immunodeficiency virus type 1 budding by CC2D1A. J. Virol. 86:3746–56
    [Google Scholar]
  125. Vietri M, Schink KO, Campsteijn C, Wegner CS, Schultz SW et al. 2015. Spastin and ESCRT-III coordinate mitotic spindle disassembly and nuclear envelope sealing. Nature 522:231–35
    [Google Scholar]
  126. Webster BM, Colombi P, Jäger J, Lusk CP 2014. Surveillance of nuclear pore complex assembly by ESCRT-III/Vps4. Cell 159:388–401
    [Google Scholar]
  127. Webster BM, Thaller DJ, Jäger J, Ochmann SES, Borah S, Lusk CP 2016. Chm7 and Heh1 collaborate to link nuclear pore complex quality control with nuclear envelope sealing. EMBO J 35:2447–67
    [Google Scholar]
  128. Wendler P, Ciniawsky S, Kock M, Kube S 2012. Structure and function of the AAA+ nucleotide binding pocket. Biochim. Biophys. Acta 1823:2–14
    [Google Scholar]
  129. Wood CR, Huang K, Diener DR, Rosenbaum JL 2013. The cilium secretes bioactive ectosomes. Curr. Biol. 23:906–11
    [Google Scholar]
  130. Xiao J, Chen XW, Davies BA, Saltiel AR, Katzmann DJ, Xu Z 2009. Structural basis of Ist1 function and Ist1-Did2 interaction in the multivesicular body pathway and cytokinesis. Mol. Biol. Cell 20:3514–24
    [Google Scholar]
  131. Yang B, Stjepanovic G, Shen Q, Martin A, Hurley JH 2015. Vps4 disassembles an ESCRT-III filament by global unfolding and processive translocation. Nat. Struct. Mol. Biol. 22:492–98
    [Google Scholar]
  132. Yang D, Rismanchi N, Renvoise B, Lippincott-Schwartz J, Blackstone C, Hurley JH 2008. Structural basis for midbody targeting of spastin by the ESCRT-III protein CHMP1B. Nat. Struct. Mol. Biol. 15:1278–86
    [Google Scholar]
  133. Zamborlini A, Usami Y, Radoshitzky SR, Popova E, Palu G, Gottlinger H 2006. Release of autoinhibition converts ESCRT-III components into potent inhibitors of HIV-1 budding. PNAS 103:19140–45
    [Google Scholar]
  134. Zhu L, Jorgensen JR, Li M, Chuang YS, Emr SD 2017. ESCRTs function directly on the lysosome membrane to downregulate ubiquitinated lysosomal membrane proteins. eLife 6:e026403
    [Google Scholar]
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