ESCRT and Membrane Protein Ubiquitination

  • Simona M. Migliano
  • David TeisEmail author
Part of the Progress in Molecular and Subcellular Biology book series (PMSB, volume 57)


The ubiquitin-dependent degradation of membrane proteins via the multivesicular body (MVB) pathway requires the Endosomal Sorting Complexes Required for Transport (ESCRT). This molecular machinery is composed of five distinct multi-subunit complexes. On the surface of endosomes, ESCRT-0, -I and -II bind to ubiquitinated membrane proteins, while ESCRT-III and Vps4 bud intraluminal vesicles (ILVs) into the lumen of the endosomes. By working together, ESCRTs package membrane proteins into ILVs and thereby generate MVBs. The fusion of mature MVBs with lysosomes delivers ILVs into the lysosomal lumen where the membrane proteins are degraded. Besides generating ILVs, the ESCRT machinery mediates for topologically related membrane budding processes at the plasma membrane and the nuclear envelop. In this chapter, we briefly discuss membrane protein ubiquitination, endocytosis, and summarize current knowledge on the ESCRT machinery in the MVB pathway.


  1. Adell MA, Vogel GF, Pakdel M, Muller M, Lindner H, Hess MW, Teis D (2014) Coordinated binding of Vps4 to ESCRT-III drives membrane neck constriction during MVB vesicle formation. J Cell Biol 205:33–49PubMedPubMedCentralCrossRefGoogle Scholar
  2. Adell M, Migliano SM, Teis D (2016) ESCRT-III and Vps4: a dynamic multipurpose tool for membrane budding and scission. FEBS JGoogle Scholar
  3. Adell MAY, Migliano SM, Upadhyayula S, Bykov YS, Sprenger S, Pakdel M, Vogel GF, Jih G, Skillern W, Behrouzi R, Babst M, Schmidt O, Hess MW, Briggs JA, Kirchhausen T, Teis D (2017) Recruitment dynamics of ESCRT-III and Vps4 to endosomes and implications for reverse membrane budding. Elife 6Google Scholar
  4. Agromayor M, Martin-Serrano J (2006) Interaction of AMSH with ESCRT-III and deubiquitination of endosomal cargo. J Biol Chem 281:23083–23091PubMedCrossRefGoogle Scholar
  5. Alfred V, Vaccari T (2016) When membranes need an ESCRT: endosomal sorting and membrane remodelling in health and disease, Swiss Med WklyGoogle Scholar
  6. Ali N, Zhang L, Taylor S, Mironov A, Urbé S, Woodman P (2013) Recruitment of UBPY and ESCRT exchange drive HD-PTP-dependent sorting of EGFR to the MVB. Curr Biol 23:453–461PubMedCrossRefGoogle Scholar
  7. Alvaro CG, O’Donnell AF, Prosser DC, Augustine AA, Goldman A, Brodsky JL, Cyert MS, Wendland B, Thorner J (2014) Specific alpha-arrestins negatively regulate Saccharomyces cerevisiae pheromone response by down-modulating the G-protein-coupled receptor Ste2. Mol Cell Biol 34:2660–2681PubMedPubMedCentralCrossRefGoogle Scholar
  8. Alwan HA, van Leeuwen JE (2007) UBPY-mediated epidermal growth factor receptor (EGFR) de-ubiquitination promotes EGFR degradation. J Biol Chem 282:1658–1669PubMedCrossRefGoogle Scholar
  9. Amerik AY, Li SJ, Hochstrasser M (2000a) Analysis of the deubiquitinating enzymes of the yeast Saccharomyces cerevisiae. Biol Chem 381:981–992PubMedCrossRefGoogle Scholar
  10. Amerik AY, Nowak J, Swaminathan S, Hochstrasser M (2000b) The Doa4 deubiquitinating enzyme is functionally linked to the vacuolar protein-sorting and endocytic pathways. Mol Biol Cell 11:3365–3380PubMedPubMedCentralCrossRefGoogle Scholar
  11. Arlt H, Perz A, Ungermann C (2011) An overexpression screen in Saccharomyces cerevisiae identifies novel genes that affect endocytic protein trafficking. Traffic 12:1592–1603PubMedCrossRefGoogle Scholar
  12. Audhya A, Desai A, Oegema K (2007) A role for Rab5 in structuring the endoplasmic reticulum. J Cell Biol 178:43–56PubMedPubMedCentralCrossRefGoogle Scholar
  13. Azmi I, Davies B, Dimaano C, Payne J, Eckert D, Babst M, Katzmann DJ (2006) Recycling of ESCRTs by the AAA-ATPase Vps4 is regulated by a conserved VSL region in Vta1. J Cell Biol 172:705–717PubMedPubMedCentralCrossRefGoogle Scholar
  14. Babst M (2005) A protein’s final ESCRT. Traffic 6:2–9PubMedCrossRefGoogle Scholar
  15. Babst M (2011) MVB vesicle formation: ESCRT-dependent, ESCRT-independent and everything in between. Curr Opin Cell Biol 23:452–457PubMedPubMedCentralCrossRefGoogle Scholar
  16. Babst M, Wendland B, Estepa EJ, Emr SD (1998) The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function. EMBO J 17:2982–2993PubMedPubMedCentralCrossRefGoogle Scholar
  17. Babst M, Katzmann DJ, Estepa-Sabal EJ, Meerloo T, Emr SD (2002) Escrt-III: an endosome-associated heterooligomeric protein complex required for MVB sorting. Dev Cell 3:271–282PubMedCrossRefGoogle Scholar
  18. Baietti MF, Zhang Z, Mortier E, Melchior A (2012) Syndecan-syntenin-ALIX regulates the biogenesis of exosomes. Nat CellGoogle Scholar
  19. Bajorek M, Morita E, Skalicky JJ, Morham SG, Babst M, Sundquist WI (2009a) Biochemical analyses of human IST1 and its function in cytokinesis. Mol Biol Cell 20:1360–1373PubMedPubMedCentralCrossRefGoogle Scholar
  20. Bajorek M, Schubert HL, Mccullough J, Langelier C, Eckert DM, Stubblefield WM, Uter NT, Myszka DG, Hill CP, Sundquist WI (2009b). Structural basis for ESCRT-III protein autoinhibition. Nat Struct Mol BiolGoogle Scholar
  21. Bauer I, Brune T, Preiss R, Kölling R (2015) Evidence for a nonendosomal function of the Saccharomyces cerevisiae ESCRT-III-like protein Chm7. Genetics 201:1439–1452PubMedPubMedCentralCrossRefGoogle Scholar
  22. Baumgärtel V, Ivanchenko S, Dupont A (2011) Live-cell visualization of dynamics of HIV budding site interactions with an ESCRT component. Nat cellGoogle Scholar
  23. Bays NW, Gardner RG, Seelig LP (2001) Hrd1p/Der3p is a membrane-anchored ubiquitin ligase required for ER-associated degradation. Nat CellGoogle Scholar
  24. Becuwe M, Herrador A, Haguenauer-Tsapis R, Vincent O, Leon S (2012a) Ubiquitin-mediated regulation of endocytosis by proteins of the arrestin family. Biochem Res Int 2012:242764PubMedPubMedCentralCrossRefGoogle Scholar
  25. Becuwe M, Vieira N, Lara D, Gomes-Rezende J, Soares-Cunha C, Casal M, Haguenauer-Tsapis R, Vincent O, Paiva S, Leon S (2012b) A molecular switch on an arrestin-like protein relays glucose signaling to transporter endocytosis. J Cell Biol 196:247–259PubMedPubMedCentralCrossRefGoogle Scholar
  26. Bedford MT, Frankel A, Yaffe MB, Clarke S, Leder P, Richard S (2000) Arginine methylation inhibits the binding of proline-rich ligands to Src homology 3, but not WW, domains. J Biol Chem 275:16030–16036PubMedCrossRefGoogle Scholar
  27. Belgareh-Touzé N, Léon S, Erpapazoglou Z, Stawiecka-Mirota M, Urban-Grimal D, Haguenauer-Tsapis R (2008) Versatile role of the yeast ubiquitin ligase Rsp5p in intracellular trafficking. Biochem Soc Trans 36:791–796PubMedCrossRefGoogle Scholar
  28. Bilodeau PS, Urbanowski JL (2002) The Vps27p–Hse1p complex binds ubiquitin and mediates endosomal protein sorting. Nat CellGoogle Scholar
  29. Bilodeau PS, Winistorfer SC, Kearney WR, Robertson AD, Piper RC (2003) Vps27-Hse1 and ESCRT-I complexes cooperate to increase efficiency of sorting ubiquitinated proteins at the endosome. J Cell Biol 163:237–243PubMedPubMedCentralCrossRefGoogle Scholar
  30. Bissig C, Gruenberg J (2014) ALIX and the multivesicular endosome: ALIX in Wonderland. Trends Cell Biol 24:19–25PubMedCrossRefGoogle Scholar
  31. Boura E, Hurley JH (2012) Structural basis for membrane targeting by the MVB12-associated β-prism domain of the human ESCRT-I MVB12 subunit. Proc Natl Acad Sci USA 109:1901–1906PubMedCrossRefGoogle Scholar
  32. Boura E, Różycki B, Herrick DZ, Chung HS, Vecer J, Eaton WA, Cafiso DS, Hummer G, Hurley JH (2011) Solution structure of the ESCRT-I complex by small-angle X-ray scattering, EPR, and FRET spectroscopy. Proc Natl Acad Sci USA 108:9437–9442PubMedCrossRefGoogle Scholar
  33. Bowers K, Piper SC, Edeling MA, Gray SR, Owen DJ, Lehner PJ, Luzio JP (2006) Degradation of endocytosed epidermal growth factor and virally ubiquitinated major histocompatibility complex class I is independent of mammalian ESCRTII. J Biol Chem 281:5094–5105PubMedCrossRefGoogle Scholar
  34. Buchkovich NJ, Henne WM, Shaogeng T, Emr SD (2013) Essential N-terminal insertion motif anchors the ESCRT-III filament during MVB vesicle formation. Dev Cell 27:201–214PubMedCrossRefGoogle Scholar
  35. Caballe A, Wenzel DM, Agromayor M, Alam SL, Skalicky JJ, Kloc M, Carlton JG, Labrador L, Sundquist WI, Martin-Serrano J (2015) ULK3 regulates cytokinetic abscission by phosphorylating ESCRT-III proteins. Elife 4Google Scholar
  36. Campsteijn C, Vietri M, Stenmark H (2016) Novel ESCRT functions in cell biology: spiraling out of control? Curr Opin Cell Biol 41:1–8PubMedCrossRefGoogle Scholar
  37. Capalbo L, Montembault E, Takeda T, Bassi ZI, Glover DM, D’Avino PP (2012) The chromosomal passenger complex controls the function of endosomal sorting complex required for transport-III Snf7 proteins during cytokinesis. Open Biol 2:120070PubMedPubMedCentralCrossRefGoogle Scholar
  38. Carlton JG, Martin-Serrano J (2007) Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery. Science 316:1908–1912PubMedCrossRefGoogle Scholar
  39. Carlton JG, Agromayor M, Martin-Serrano J (2008) Differential requirements for Alix and ESCRT-III in cytokinesis and HIV-1 release. Proc Natl Acad Sci USA 105:10541–10546PubMedCrossRefGoogle Scholar
  40. Carvalho P, Goder V, Rapoport TA (2006) Distinct ubiquitin-ligase complexes define convergent pathways for the degradation of ER proteins. Cell 126:361–373PubMedCrossRefGoogle Scholar
  41. 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 3Google Scholar
  42. Chiaruttini N, Redondo-Morata L, Colom A, Humbert F, Lenz M, Scheuring S, Roux A (2015) Relaxation of loaded ESCRT-III spiral springs drives membrane deformation. Cell 163:866–879PubMedPubMedCentralCrossRefGoogle Scholar
  43. Cho KJ, Walseng E, Ishido S, Roche PA (2015) Ubiquitination by March-I prevents MHC class II recycling and promotes MHC class II turnover in antigen-presenting cells. Proc Natl Acad Sci USA 112:10449–10454PubMedCrossRefGoogle Scholar
  44. 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 42:42–56PubMedCrossRefGoogle Scholar
  45. Christianson JC, Ye Y (2014) Cleaning up in the endoplasmic reticulum: ubiquitin in charge. Nat Struct Mol BiolGoogle Scholar
  46. Chu T, Sun J, Saksena S, Emr SD (2006) New component of ESCRT-I regulates endosomal sorting complex assembly. J Cell Biol 175:815–823PubMedPubMedCentralCrossRefGoogle Scholar
  47. Clague MJ (2002) Membrane transport: a coat for ubiquitin. Curr Biol 12:R529–R531PubMedCrossRefGoogle Scholar
  48. Clague MJ, Urbe S (2006) Endocytosis: the DUB version. Trends Cell Biol 16:551–559PubMedCrossRefGoogle Scholar
  49. Colombo M, Moita C, van Niel G, Kowal J, Vigneron J, Benaroch P, Manel N, Moita LF, Thery C, Raposo G (2013) Analysis of ESCRT functions in exosomes biogenesis, composition and secretion highlights the heterogeneity of extracellular vesicles. J Cell Sci 126:5553–5565PubMedCrossRefGoogle Scholar
  50. Crapeau M, Merhi A, Andre B (2014) Stress conditions promote yeast Gap1 permease ubiquitylation and down-regulation via the arrestin-like Bul and Aly proteins. J Biol Chem 289:22103–22116PubMedPubMedCentralCrossRefGoogle Scholar
  51. Cruickshanks N (2014) When to screen and not to screen. Cancer Biol Ther 15:147–148PubMedPubMedCentralCrossRefGoogle Scholar
  52. Curtiss M, Jones C, Babst M (2007) Efficient cargo sorting by ESCRT-I and the subsequent release of ESCRT-I from multivesicular bodies requires the subunit Mvb12. Mol Biol Cell 18:636–645PubMedPubMedCentralCrossRefGoogle Scholar
  53. Curwin AJ, Brouwers N, Adell MAY, Teis D, Turacchio G, Parashuraman S, Ronchi P, Malhotra V, Schekman R (2016) ESCRT-III drives the final stages of CUPS maturation for unconventional protein secretion. Elife 5:e16299PubMedPubMedCentralCrossRefGoogle Scholar
  54. Denais CM, Gilbert RM, Isermann P, McGregor AL, te Lindert M, Weigelin B, Davidson PM, Friedl P, Wolf K, Lammerding J (2016) Nuclear envelope rupture and repair during cancer cell migration. Science 352:353–358PubMedPubMedCentralCrossRefGoogle Scholar
  55. Deshaies RJ, Joazeiro CAP (2009) RING domain E3 ubiquitin ligases 78:399–434Google Scholar
  56. Di Fiore PP, Polo S, Hofmann K (2003) When ubiquitin meets ubiquitin receptors: a signalling connection. Nat Rev Mol Cell BiolGoogle Scholar
  57. Dikic I, Robertson M (2012) Ubiquitin ligases and beyond. BMC Biol 10:22PubMedPubMedCentralCrossRefGoogle Scholar
  58. Dores MR, Chen B, Lin H, Soh UJ, Paing MM, Montagne WA, Meerloo T, Trejo J (2012) ALIX binds a YPX(3)L motif of the GPCR PAR1 and mediates ubiquitin-independent ESCRT-III/MVB sorting. J Cell Biol 197:407–419PubMedPubMedCentralCrossRefGoogle Scholar
  59. Doyotte A, Mironov A, McKenzie E, Woodman P (2008) The Bro1-related protein HD-PTP/PTPN23 is required for endosomal cargo sorting and multivesicular body morphogenesis. Proc Natl Acad Sci USA 105:6308–6313PubMedCrossRefGoogle Scholar
  60. Draheim KM, Chen HB, Tao Q, Moore N, Roche M, Lyle S (2010) ARRDC3 suppresses breast cancer progression by negatively regulating integrin beta4. Oncogene 29:5032–5047PubMedPubMedCentralCrossRefGoogle Scholar
  61. Dunn R, Klos DA, Adler AS, Hicke L (2004) The C2 domain of the Rsp5 ubiquitin ligase binds membrane phosphoinositides and directs ubiquitination of endosomal cargo. J Cell Biol 165:135–144PubMedPubMedCentralCrossRefGoogle Scholar
  62. Dupré S, Urban-Grimal D, Haguenauer-Tsapis R (2004) Ubiquitin and endocytic internalization in yeast and animal cells. Biochim Biophys Acta 1695:89–111PubMedCrossRefGoogle Scholar
  63. Effantin G, Dordor A, Sandrin V, Martinelli N, Sundquist WI, Schoehn G, Weissenhorn W (2013) ESCRT-III CHMP2A and CHMP3 form variable helical polymers in vitro and act synergistically during HIV-1 budding. Cell Microbiol 15:213–226PubMedCrossRefGoogle Scholar
  64. Elia N, Sougrat R, Spurlin T, Hurley J, Lippincott-Schwartz J (2011) Dynamics of endosomal sorting complex required for transport (ESCRT) machinery during cytokinesis and its role in abscission. PNAS 108:4846–4851PubMedCrossRefGoogle Scholar
  65. Elia N, Fabrikant G, Kozlov MM, Lippincott-Schwartz J (2012) Computational model of cytokinetic abscission driven by ESCRT-III polymerization and remodeling. Biophys J 102:2309–2320PubMedPubMedCentralCrossRefGoogle Scholar
  66. Foot N, Henshall T, Kumar S (2017) Ubiquitination and the regulation of membrane proteins. Physiol Rev 97:253–281PubMedCrossRefGoogle Scholar
  67. Galan JM, Moreau V, Andre B, Volland C, Haguenauer-Tsapis R (1996) Ubiquitination mediated by the Npi1p/Rsp5p ubiquitin-protein ligase is required for endocytosis of the yeast uracil permease. J Biol Chem 271:10946–10952PubMedCrossRefGoogle Scholar
  68. 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 107:55–65PubMedCrossRefGoogle Scholar
  69. Gay DL, Ramón H, Oliver PM (2008) Cbl- and Nedd4-family ubiquitin ligases: balancing tolerance and immunity. Immunol Res 42:51–64PubMedPubMedCentralCrossRefGoogle Scholar
  70. Géminard C, de Gassart A, Blanc L, Vidal M (2004) Degradation of AP2 during reticulocyte maturation enhances binding of Hsc70 and Alix to a common site on TfR for sorting into exosomes. Traffic 5:181–193PubMedCrossRefGoogle Scholar
  71. Ghaddar K, Merhi A, Saliba E, Krammer EM, Prevost M, Andre B (2014) Substrate-induced ubiquitylation and endocytosis of yeast amino acid permeases. Mol Cell Biol 34:4447–4463PubMedPubMedCentralCrossRefGoogle Scholar
  72. Ghazi-Tabatabai S, Saksena S, Short JM, Pobbati AV, Veprintsev DB, Crowther RA, Emr SD, Egelman EH, Williams RL (2008) Structure and disassembly of filaments formed by the ESCRT-III subunit Vps24. Structure 16:1345–1356PubMedCrossRefGoogle Scholar
  73. Gill DJ, Teo H, Sun J, Perisic O, Veprintsev DB, Emr SD, Williams RL (2007) Structural insight into the ESCRT-I/-II link and its role in MVB trafficking. EMBO J 26:600–612PubMedPubMedCentralCrossRefGoogle Scholar
  74. Godlee C, Kaksonen M (2013) From uncertain beginnings: initiation mechanisms of clathrin-mediated endocytosis. J Cell Biol 203:717–725PubMedPubMedCentralCrossRefGoogle Scholar
  75. Gonciarz MD, Whitby FG, Eckert DM, Kieffer C, Heroux A, Sundquist WI, Hill CP (2008) Biochemical and structural studies of yeast Vps4 oligomerization. J Mol Biol 384:878–895PubMedPubMedCentralCrossRefGoogle Scholar
  76. Gu M, Lajoie D, Chen OS, von Appen A, Ladinsky MS, Redd MJ, Nikolova L, Bjorkman PJ, Sundquist WI, Ullman KS, Frost A (2017) LEM2 recruits CHMP7 for ESCRT-mediated nuclear envelope closure in fission yeast and human cells. Proc Natl Acad Sci USA 114:E2166–E2175PubMedCrossRefGoogle Scholar
  77. Guizetti J, Schermelleh L, Mäntler J, Maar S, Poser I, Leonhardt H, Müller-Reichert T, Gerlich WD (2011) Cortical constriction during abscission involves helices Of ESCRT-III-dependent filaments. Science 331:1616–1620PubMedCrossRefGoogle Scholar
  78. Haglund K (2003) Distinct monoubiquitin signals in receptor endocytosis. Trends Biochem Sci 28:598–604PubMedCrossRefGoogle Scholar
  79. Haglund K, Dikic I (2012) The role of ubiquitylation in receptor endocytosis and endosomal sorting. J Cell Sci 125:265–275PubMedCrossRefGoogle Scholar
  80. Hamilton KL (2014) Cleavage: what’s up with prostasin and ENaC these days? Am J Physiol Renal Physiol 307:F1196–F1197PubMedCrossRefGoogle Scholar
  81. Hatakeyama R, Kamiya M, Takahara T, Maeda T (2010) Endocytosis of the aspartic acid/glutamic acid transporter Dip5 is triggered by substrate-dependent recruitment of the Rsp5 ubiquitin ligase via the arrestin-like protein Aly2. Mol Cell Biol 30:5598–5607PubMedPubMedCentralCrossRefGoogle Scholar
  82. Henne WM, Buchkovich NJ, Yingying Z, Emr SD (2012) The endosomal sorting complex ESCRT-II mediates the assembly and architecture of ESCRT-III helices. Cell 151:356–371PubMedCrossRefGoogle Scholar
  83. Hershko A, Ciechanover A (1998) The ubiquitin system. Annu Rev Biochem 67:425–479PubMedCrossRefGoogle Scholar
  84. Hicke L, Riezman H (1996) Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell 84:277–287PubMedCrossRefGoogle Scholar
  85. Hicke L, Schubert HL, Hill CP (2005) Ubiquitin-binding domains. Nat Rev Mol Cell Biol 6:610–621PubMedCrossRefGoogle Scholar
  86. Hierro A, Sun J, Rusnak AS, Kim J, Prag G, Emr SD, Hurley JH (2004) Structure of the ESCRT-II endosomal trafficking complex. Nature 431:221–225PubMedCrossRefGoogle Scholar
  87. Hofmann RM, Pickart CM (2001) In vitro assembly and recognition of Lys-63 polyubiquitin chains. J Biol Chem 276:27936–27943PubMedCrossRefGoogle Scholar
  88. Hovsepian J, Defenouillere Q, Albanese V, Vachova L, Garcia C, Palkova Z, Leon S (2017) Multilevel regulation of an alpha-arrestin by glucose depletion controls hexose transporter endocytosis. J Cell BiolGoogle Scholar
  89. Huang L, Kinnucan E, Wang G, Beaudenon S, Howley PM, Huibregtse JM, Pavletich NP (1999) Structure of an E6AP-UbcH7 complex: insights into ubiquitination by the E2-E3 enzyme cascade. Science 286:1321–1326PubMedCrossRefGoogle Scholar
  90. Hurley JH, Misra S (2000) Signaling and subcellular targeting by membrane-binding domains. Annu Rev Biophys Biomol Struct 29:49–79PubMedPubMedCentralCrossRefGoogle Scholar
  91. Im YJ, Hurley JH (2008) Integrated structural model and membrane targeting mechanism of the human ESCRT-II complex. Dev Cell 14:902–913PubMedPubMedCentralCrossRefGoogle Scholar
  92. Im YJ, Wollert T, Boura E, Hurley JH (2009) Structure and function of the ESCRT-II-III interface in multivesicular body biogenesis. Dev Cell 17:234–243PubMedPubMedCentralCrossRefGoogle Scholar
  93. Inoue M, Kamikubo H, Kataoka M, Kato R, Yoshimori T, Wakatsuki S, Kawasaki M (2008) Nucleotide-dependent conformational changes and assembly of the AAA ATPase SKD1/VPS4b. Traffic 9:2180–2189PubMedCrossRefGoogle Scholar
  94. Jimenez AJ, Maiuri P, Lafaurie-Janvore J, Divoux S, Piel M, Perez F (2014) ESCRT machinery is required for plasma membrane repair. Science 343:1247136PubMedCrossRefGoogle Scholar
  95. Jones CB, Ott EM, Keener JM, Curtiss M, Sandrin V, Babst M (2012) Regulation of membrane protein degradation by starvation-response pathways. Traffic 13:468–482PubMedPubMedCentralCrossRefGoogle Scholar
  96. Jouvenet N, Simon SM, Bieniasz PD (2011) Visualizing HIV-1 assembly. J Mol Biol 410:501–511PubMedPubMedCentralCrossRefGoogle Scholar
  97. Kaliszewski P, Zoładek T (2008) The role of Rsp5 ubiquitin ligase in regulation of diverse processes in yeast cells. Acta Biochim Pol 55:649–662PubMedGoogle Scholar
  98. Kang DS, Tian X, Benovic JL (2014) Role of β-arrestins and arrestin domain-containing proteins in G protein-coupled receptor trafficking. Curr Opin Cell Biol 27:63–71PubMedCrossRefGoogle Scholar
  99. Kato M, Miyazawa K, Kitamura N (2000) A deubiquitinating enzyme UBPY interacts with the Src homology 3 domain of Hrs-binding protein via a novel binding motif PX(V/I)(D/N)RXXKP. J Biol Chem 275:37481–37487PubMedCrossRefGoogle Scholar
  100. Katzmann DJ, Babst M, Emr SD (2001) Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell 106:145–155PubMedCrossRefGoogle Scholar
  101. Katzmann DJ, Stefan CJ, Babst M, Emr SD (2003) Vps27 recruits ESCRT machinery to endosomes during MVB sorting. J Cell Biol 162:413–423PubMedPubMedCentralCrossRefGoogle Scholar
  102. Kerscher O, Felberbaum R, Hochstrasser M (2006) Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu Rev Cell Dev Biol 22:159–180PubMedCrossRefGoogle Scholar
  103. Kojima R, Obita T, Onoue K, Mizuguchi M (2016) Structural fine-tuning of MIT-interacting motif 2 (MIM2) and allosteric regulation of ESCRT-III by Vps4 in yeast. J Mol Biol 428:2392–2404PubMedCrossRefGoogle Scholar
  104. Komander D (2009) The emerging complexity of protein ubiquitination. Biochem Soc Trans 37:937–953PubMedCrossRefGoogle Scholar
  105. Kostelansky MS, Schluter C, Tam YY, Lee S, Ghirlando R, Beach B, Conibear E, Hurley JH (2007) Molecular architecture and functional model of the complete yeast ESCRT-I heterotetramer. Cell 129:485–498PubMedPubMedCentralCrossRefGoogle Scholar
  106. Kozlov G, Nguyen L, Lin T, de Crescenzo G, Park M, Gehring K (2007) Structural basis of ubiquitin recognition by the ubiquitin-associated (UBA) domain of the ubiquitin ligase EDD. J Biol Chem 282:35787–35795PubMedCrossRefGoogle Scholar
  107. Landsberg MJ, Vajjhala PR, Rothnagel R, Munn AL, Hankamer B (2009) Three-dimensional structure of AAA ATPase Vps4: advancing structural insights into the mechanisms of endosomal sorting and enveloped virus budding. Structure 17:427–437PubMedCrossRefGoogle Scholar
  108. Langelier C, von Schwedler UK, Fisher RD, de Domenico I, White PL, Hill CP, Kaplan J, Ward D, Sundquist WI (2006) Human ESCRT-II complex and its role in human immunodeficiency virus type 1 release. J Virol 80:9465–9480PubMedPubMedCentralCrossRefGoogle Scholar
  109. Lata S, Schoehn G, Jain A, Pires R, Piehler J, Gottlinger HG, Weissenhorn W (2008) Helical structures of ESCRT-III are disassembled by VPS4. Science 321:1354–1357PubMedPubMedCentralCrossRefGoogle Scholar
  110. 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 322:576–580PubMedPubMedCentralCrossRefGoogle Scholar
  111. Lee J, Oh K-J, Lee D, Kim BY, Choi JS, Ku B, Kim SJ (2016) Structural study of the HD-PTP Bro1 domain in a complex with the core region of STAM2, a subunit of ESCRT-0. PLoS ONE 11:e0149113PubMedPubMedCentralCrossRefGoogle Scholar
  112. Lemmon MA, Schlessinger J (2010) Cell signaling by receptor tyrosine kinases. Cell 141:1117–1134PubMedPubMedCentralCrossRefGoogle Scholar
  113. Levkowitz G, Waterman H, Zamir E, Kam Z, Oved S, Langdon WY, Beguinot L, Geiger B, Yarden Y (1998) c-Cbl/Sli-1 regulates endocytic sorting and ubiquitination of the epidermal growth factor receptor. Genes Dev 12:3663–3674PubMedPubMedCentralCrossRefGoogle Scholar
  114. Levkowitz G, Waterman H, Ettenberg SA, Katz M, Tsygankov AY, Alroy I, Lavi S, Iwai K, Reiss Y, Ciechanover A, Lipkowitz S, Yarden Y (1999) Ubiquitin ligase activity and tyrosine phosphorylation underlie suppression of growth factor signaling by c-Cbl/Sli-1. Mol Cell 4:1029–1040PubMedCrossRefPubMedCentralGoogle Scholar
  115. Li M, Koshi T, Emr SD (2015a) Membrane-anchored ubiquitin ligase complex is required for the turnover of lysosomal membrane proteins. J Cell Biol 211:jcb.201505062-652Google Scholar
  116. Li M, Rong Y, Chuang Y-S, Peng D, Emr SD (2015b) Ubiquitin-dependent lysosomal membrane protein sorting and degradation. Mol Cell 57:467–478PubMedCrossRefGoogle Scholar
  117. Lin CH, Macgurn JA, Chu T, Stefan CJ, Emr SD (2008) Arrestin-related ubiquitin-ligase adaptors regulate endocytosis and protein turnover at the cell surface. Cell 135:714–725PubMedCrossRefGoogle Scholar
  118. Loncle N, Agromayor M, Martin-Serrano J, Williams DW (2015) An ESCRT module is required for neuron pruning. Sci Rep 5:127CrossRefGoogle Scholar
  119. Lorick KL, Jensen JP, Fang S, Ong AM, Hatakeyama S, Weissman AM (1999) RING fingers mediate ubiquitin-conjugating enzyme (E2)-dependent ubiquitination. Proc Natl Acad Sci 96:11364–11369PubMedCrossRefGoogle Scholar
  120. Lottridge JM, Flannery AR, Vincelli JL, Stevens TH (2006) Vta1p and Vps46p regulate the membrane association and ATPase activity of Vps4p at the yeast multivesicular body. Proc Natl Acad Sci 103:6202–6207PubMedCrossRefGoogle Scholar
  121. Lu Y, Li X, Liang K, Luwor R, Siddik ZH, Mills GB, Mendelsohn J, Fan Z (2007) Epidermal growth factor receptor (EGFR) ubiquitination as a mechanism of acquired resistance escaping treatment by the anti-EGFR monoclonal antibody cetuximab. Cancer Res 67:8240–8247PubMedCrossRefGoogle Scholar
  122. Luhtala N, Odorizzi G (2004) Bro1 coordinates deubiquitination in the multivesicular body pathway by recruiting Doa4 to endosomes. J Cell Biol 166:717–729Google Scholar
  123. Macdonald C, Payne JA, Aboian M, Smith W, Katzmann DJ, Piper RC (2015) A family of tetraspans organizes cargo for sorting into multivesicular bodies. Dev Cell 33:328–342Google Scholar
  124. Macgurn JA, Hsu P-C, Smolka MB, Emr SD (2011) TORC1 regulates endocytosis via Npr1-mediated phosphoinhibition of a ubiquitin ligase adaptor. Cell 147:1104–1117PubMedCrossRefGoogle Scholar
  125. Macgurn JA, Hsu PC, Emr SD (2012) Ubiquitin and membrane protein turnover: from cradle to grave. Annu Rev Biochem 81:231–259PubMedCrossRefGoogle Scholar
  126. Marqués MC, Zamarbide-Forés S (2015) A functional Rim101 complex is required for proper accumulation of the Ena1 Na+-ATPase protein in response to salt stress in Saccharomyces cerevisiae. FEMS Yeast ResGoogle Scholar
  127. Martin-Serrano J, Neil SJ (2011) Host factors involved in retroviral budding and release. Nat Rev Microbiol 9:519–531PubMedCrossRefGoogle Scholar
  128. 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 7:1313–1319PubMedCrossRefGoogle Scholar
  129. Martin-Serrano J, Eastman SW, Chung W, Bieniasz PD (2005) HECT ubiquitin ligases link viral and cellular PPXY motifs to the vacuolar protein-sorting pathway. J Cell Biol 168:89–101PubMedPubMedCentralCrossRefGoogle Scholar
  130. McCullough J, Clague MJ, Urbe S (2004) AMSH is an endosome-associated ubiquitin isopeptidase. J Cell Biol 166:487–492PubMedPubMedCentralCrossRefGoogle Scholar
  131. McCullough J, Fisher RD, Whitby FG, Sundquist WI, Hill CP (2008) ALIX-CHMP4 interactions in the human ESCRT pathway. Proc Natl Acad Sci USA 105:7687–7691PubMedCrossRefGoogle Scholar
  132. Merhi A, Andre B (2012) Internal amino acids promote Gap1 permease ubiquitylation via TORC1/Npr1/14-3-3-dependent control of the Bul arrestin-like adaptors. Mol Cell Biol 32:4510–4522PubMedPubMedCentralCrossRefGoogle Scholar
  133. Metzger MB, Hristova VA, Weissman AM (2012) HECT and RING finger families of E3 ubiquitin ligases at a glance. J Cell Sci 125:531–537PubMedPubMedCentralCrossRefGoogle Scholar
  134. Mevissen TET, Komander D (2016) Mechanisms of deubiquitinase specificity and regulation 86:annurev-biochem-061516-044916Google Scholar
  135. Mierzwa BE, Chiaruttini N, Redondo-Morata L, Moser Von Filseck J, Konig J, Larios J, Poser I, Muller-Reichert T, Scheuring S, Roux A, Gerlich DW (2017) Dynamic subunit turnover in ESCRT-III assemblies is regulated by Vps4 to mediate membrane remodelling during cytokinesis. Nat Cell BiolGoogle Scholar
  136. Mohapatra B, Ahmad G, Nadeau S, Zutshi N, An W, Scheffe S, Dong L, Feng D, Goetz B, Arya P, Bailey TA, Palermo N, Borgstahl GEO, Natarajan A, Raja SM, Naramura M, Band V, Band H (2013) Protein tyrosine kinase regulation by ubiquitination: Critical roles of Cbl-family ubiquitin ligases. Biochim Biophys Acta (BBA) Mol Cell Res 1833:122–139CrossRefGoogle Scholar
  137. Monroe N, Han H, Shen PS, Sundquist WI, Hill CP, Subramaniam S (2017) Structural basis of protein translocation by the Vps4-Vta1 AAA ATPase. Elife 6:e24487PubMedPubMedCentralCrossRefGoogle Scholar
  138. Morita E, Sandrin V, Chung HY, Morham SG, Gygi SP, Rodesch CK, Sundquist WI (2007) Human ESCRT and ALIX proteins interact with proteins of the midbody and function in cytokinesis. EMBO J 26:4215–4227PubMedPubMedCentralCrossRefGoogle Scholar
  139. 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 USA 107:12889–12894PubMedCrossRefGoogle Scholar
  140. 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 9:235–242PubMedPubMedCentralCrossRefGoogle Scholar
  141. Morrison JA, Pike LA, Sams SB, Sharma V, Zhou Q, Severson JJ, Tan AC, Wood WM, Haugen BR (2014) Thioredoxin interacting protein (TXNIP) is a novel tumor suppressor in thyroid cancer. Mol Cancer 13:62PubMedPubMedCentralCrossRefGoogle Scholar
  142. Muller M, Schmidt O, Angelova M, Faserl K, Weys S, Kremser L, Pfaffenwimmer T, Dalik T, Kraft C, Trajanoski Z, Lindner H, Teis D (2015) The coordinated action of the MVB pathway and autophagy ensures cell survival during starvation. Elife 4Google Scholar
  143. Muziol T, Pineda-Molina E, Ravelli RB, Zamborlini A, Usami Y, Gottlinger H, Weissenhorn W (2006) Structural basis for budding by the ESCRT-III factor CHMP3. Dev Cell 10:821–830PubMedCrossRefGoogle Scholar
  144. Myromslien FD, Grovdal LM, Raiborg C, Stenmark H, Madshus IH, Stang E (2006) Both clathrin-positive and -negative coats are involved in endosomal sorting of the EGF receptor. Exp Cell Res 312:3036–3048PubMedCrossRefGoogle Scholar
  145. Nabhan JF, Pan H, Lu Q (2010) Arrestin domain-containing protein 3 recruits the NEDD4 E3 ligase to mediate ubiquitination of the β2-adrenergic receptor. EMBO Rep 11:605–611PubMedPubMedCentralCrossRefGoogle Scholar
  146. 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. Proc Natl Acad Sci USA 109:4146–4151PubMedCrossRefGoogle Scholar
  147. Nakamura N (2011) The role of the transmembrane RING finger proteins in cellular and organelle function. Membranes 1:354–393PubMedPubMedCentralCrossRefGoogle Scholar
  148. Nakamura M, Tanaka N, Kitamura N, Komada M (2006) Clathrin anchors deubiquitinating enzymes, AMSH and AMSH-like protein, on early endosomes. Genes Cells: Devoted Mol Cell Mech 11:593–606CrossRefGoogle Scholar
  149. Nalefski EA, Falke JJ (1996) The C2 domain calcium-binding motif: structural and functional diversity. Protein Sci: Publ Protein Soc 5:2375–2390CrossRefGoogle Scholar
  150. Nathan JA, Lehner PJ (2009) The trafficking and regulation of membrane receptors by the RING-CH ubiquitin E3 ligases. Exp Cell Res 315:1593–1600PubMedCrossRefGoogle Scholar
  151. Nickerson DP, West M, Odorizzi G (2006) Did2 coordinates Vps4-mediated dissociation of ESCRT-III from endosomes. J Cell Biol 175:715–720PubMedPubMedCentralCrossRefGoogle Scholar
  152. Nickerson DP, West M, Henry R, Odorizzi G (2010) Regulators of Vps4 ATPase activity at endosomes differentially influence the size and rate of formation of intralumenal vesicles. Mol Biol Cell 21:1023–1032PubMedPubMedCentralCrossRefGoogle Scholar
  153. Niendorf S, Oksche A, Kisser A, Lohler J, Prinz M, Schorle H, Feller S, Lewitzky M, Horak I, Knobeloch KP (2007) Essential role of ubiquitin-specific protease 8 for receptor tyrosine kinase stability and endocytic trafficking in vivo. Mol Cell Biol 27:5029–5039PubMedPubMedCentralCrossRefGoogle Scholar
  154. Nikko E, Pelham HRB (2009) Arrestin-mediated endocytosis of yeast plasma membrane transporters. Traffic 10:1856–1867PubMedPubMedCentralCrossRefGoogle Scholar
  155. Nikko E, Sullivan JA, Pelham HR (2008) Arrestin-like proteins mediate ubiquitination and endocytosis of the yeast metal transporter Smf1. EMBO Rep 9:1216–1221PubMedPubMedCentralCrossRefGoogle Scholar
  156. O’Donnell AF, Apffel A, Gardner RG, Cyert MS (2010) Alpha-arrestins Aly1 and Aly2 regulate intracellular trafficking in response to nutrient signaling. Mol Biol Cell 21:3552–3566PubMedPubMedCentralCrossRefGoogle Scholar
  157. O’Donnell AF, Huang L, Thorner J, Cyert MS (2013) A calcineurin-dependent switch controls the trafficking function of alpha-arrestin Aly1/Art6. J Biol Chem 288:24063–24080PubMedPubMedCentralCrossRefGoogle Scholar
  158. O’Donnell AF, McCartney RR, Chandrashekarappa DG, Zhang BB, Thorner J, Schmidt MC (2015) 2-Deoxyglucose impairs Saccharomyces cerevisiae growth by stimulating Snf1-regulated and alpha-arrestin-mediated trafficking of hexose transporters 1 and 3. Mol Cell Biol 35:939–955PubMedPubMedCentralCrossRefGoogle Scholar
  159. Oestreich AJ, Davies BA, Payne JA, Katzmann DJ (2007) Mvb12 is a novel member of ESCRT-I involved in cargo selection by the multivesicular body pathway. Mol Biol Cell 18:646–657PubMedPubMedCentralCrossRefGoogle Scholar
  160. Oh J, Wu N, Baravalle G, Cohn B, Ma J, Lo B, Mellman I, Ishido S, Anderson M, Shin JS (2013) MARCH1-mediated MHCII ubiquitination promotes dendritic cell selection of natural regulatory T cells. J Exp Med 210:1069–1077PubMedPubMedCentralCrossRefGoogle Scholar
  161. Olmos Y, Hodgson L, Mantell J, Verkade P, Carlton JG (2015) ESCRT-III controls nuclear envelope reformation. Nature 522:236–239PubMedPubMedCentralCrossRefGoogle Scholar
  162. Olmos Y, Perdrix-Rosell A, Carlton JG (2016) Membrane binding by CHMP7 coordinates ESCRT-III-dependent nuclear envelope reformation. Curr Biol 26:2635–2641PubMedPubMedCentralCrossRefGoogle Scholar
  163. Papa FR, Amerik AY, Hochstrasser M (1999) Interaction of the Doa4 deubiquitinating enzyme with the yeast 26S proteasome. Mol Biol Cell 10:741–756PubMedPubMedCentralCrossRefGoogle Scholar
  164. Pareja F, Ferraro DA, Rubin C, Cohen-Dvashi H, Zhang F, Aulmann S, Ben-Chetrit N, Pines G, Navon R, Crosetto N, Köstler W, Carvalho S, Lavi S, Schmitt F, Dikic I, Yakhini Z, Sinn P, Mills GB, Yarden Y (2012) Deubiquitination of EGFR by Cezanne-1 contributes to cancer progression. Oncogene 31:4599–4608PubMedCrossRefPubMedCentralGoogle Scholar
  165. Piper RC, Lehner PJ (2011) Endosomal transport via ubiquitination. Trends Cell Biol 21:647–655PubMedPubMedCentralCrossRefGoogle Scholar
  166. Polo S, Sigismund S, Faretta M, Guidi M, Capua MR, Bossi G, Chen H, de Camilli P, di Fiore PP (2002) A single motif responsible for ubiquitin recognition and monoubiquitination in endocytic proteins. Nature 416:451–455PubMedCrossRefGoogle Scholar
  167. Pornillos O, Higginson DS, Stray KM, Fisher RD, Garrus JE, Payne M, He G-P, Wang HE, Morham SG, Sundquist WI (2003) HIV Gag mimics the Tsg101-recruiting activity of the human Hrs protein. J Cell Biol 162:425–434PubMedPubMedCentralCrossRefGoogle Scholar
  168. Prag G, Watson H, Kim YC, Beach BM, Ghirlando R, Hummer G, Bonifacino JS, Hurley JH (2007) The Vps27/Hse1 complex is a GAT domain-based scaffold for ubiquitin-dependent sorting. Dev Cell 12:973–986PubMedPubMedCentralCrossRefGoogle Scholar
  169. Prescher J, Baumgartel V, Ivanchenko S, Torrano AA, Brauchle C, Muller B, Lamb DC (2015) Super-resolution imaging of ESCRT-proteins at HIV-1 assembly sites. PLoS Pathog 11:e1004677PubMedPubMedCentralCrossRefGoogle Scholar
  170. Raab M, Gentili M, de Belly H, Thiam HR, Vargas P, Jimenez AJ, Lautenschlaeger F, Voituriez R, Lennon-Dumenil AM, Manel N, Piel M (2016) ESCRT III repairs nuclear envelope ruptures during cell migration to limit DNA damage and cell death. Science 352:359–362PubMedCrossRefPubMedCentralGoogle Scholar
  171. Raiborg C, Stenmark H (2009) The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 458:445–452PubMedCrossRefPubMedCentralGoogle Scholar
  172. Raiborg C, Bache KG, Mehlum A, Stenmark H (2001a) Function of Hrs in endocytic trafficking and signalling. Biochem Soc Trans 29:472–475PubMedCrossRefGoogle Scholar
  173. Raiborg C, Bremnes B, Mehlum A, Gillooly DJ, D’Arrigo A, Stang E, Stenmark H (2001b) FYVE and coiled-coil domains determine the specific localisation of Hrs to early endosomes. J Cell Sci 114:2255–2263PubMedGoogle Scholar
  174. Raiborg C, Bache KG, Gillooly DJ, Madshus IH, Stang E, Stenmark H (2002) Hrs sorts ubiquitinated proteins into clathrin-coated microdomains of early endosomes. Nat Cell Biol 4:394–398PubMedCrossRefPubMedCentralGoogle Scholar
  175. Rauch S, Martin-Serrano J (2011) Multiple interactions between the ESCRT machinery and arrestin-related proteins: implications for PPXY-dependent budding. J Virol 85:3546–3556PubMedCrossRefGoogle Scholar
  176. Ravid T, Hochstrasser M (2007) Autoregulation of an E2 enzyme by ubiquitin-chain assembly on its catalytic residue. Nat Cell Biol 9:422–427PubMedCrossRefGoogle Scholar
  177. Reggiori F, Pelham HRB (2002) A transmembrane ubiquitin ligase required to sort membrane proteins into multivesicular bodies. Nat Cell Biol 4:117–123PubMedCrossRefGoogle Scholar
  178. Reid E, Connell J, Edwards TL, Duley S, Brown SE, Sanderson CM (2005) The hereditary spastic paraplegia protein spastin interacts with the ESCRT-III complex-associated endosomal protein CHMP1B. Hum Mol Genet 14:19–38PubMedCrossRefGoogle Scholar
  179. Ren X, Kloer DP, Kim YC, Ghirlando R, Saidi LF, Hummer G, Hurley JH (2009) Hybrid structural model of the complete human ESCRT-0 complex. Structure 17:406–416PubMedPubMedCentralCrossRefGoogle Scholar
  180. Richter C, West M, Odorizzi G (2007) Dual mechanisms specify Doa4-mediated deubiquitination at multivesicular bodies. EMBO J 26:2454–2464PubMedPubMedCentralCrossRefGoogle Scholar
  181. Rotin D, Kumar S (2009) Physiological functions of the HECT family of ubiquitin ligases. Nat Rev Mol Cell Biol 10:398–409PubMedCrossRefGoogle Scholar
  182. Rotin D, Staub O, Haguenauer-Tsapis R (2000) Ubiquitination and endocytosis of plasma membrane proteins: role of Nedd4/Rsp5p family of ubiquitin-protein ligases. J Membr Biol 176:1–17PubMedCrossRefGoogle Scholar
  183. Roucourt B, Meeussen S, Bao J, Zimmermann P, David G (2015) Heparanase activates the syndecan-syntenin-ALIX exosome pathway. Cell Res 25:412–428PubMedPubMedCentralCrossRefGoogle Scholar
  184. Row PE, Prior IA, McCullough J, Clague MJ, Urbe S (2006) The ubiquitin isopeptidase UBPY regulates endosomal ubiquitin dynamics and is essential for receptor down-regulation. J Biol Chem 281:12618–12624PubMedCrossRefPubMedCentralGoogle Scholar
  185. Row PE, Liu H, Hayes S, Welchman R, Charalabous P, Hofmann K, Clague MJ, Sanderson CM, Urbé S (2007) The MIT domain of UBPY constitutes a CHMP binding and endosomal localization signal required for efficient epidermal growth factor receptor degradation. J Biol Chem 282:30929–30937PubMedCrossRefGoogle Scholar
  186. Rue SM, Mattei S, Saksena S, Emr SD (2008) Novel Ist1-Did2 complex functions at a late step in multivesicular body sorting. Mol Biol Cell 19:475–484PubMedPubMedCentralCrossRefGoogle Scholar
  187. Samji T, Hong S, Means RE (2014) The membrane associated RING-CH proteins: a family of E3 ligases with diverse roles through the cell. Int Sch Res Not 2014:637295–637323Google Scholar
  188. Scheffer LL, Sreetama SC, Sharma N, Medikayala S, Brown KJ, Defour A, Jaiswal JK (2014) Mechanism of Ca2+-triggered ESCRT assembly and regulation of cell membrane repair. Nat Commun 5:5646PubMedPubMedCentralCrossRefGoogle Scholar
  189. Schmidt MHH, Dikic I (2005) The Cbl interactome and its functions. Nat Rev Mol Cell Biol 6:907–918PubMedCrossRefPubMedCentralGoogle Scholar
  190. Schmidt O, Teis D (2012) The ESCRT machinery. Curr Biol: CB 22:R116–R120PubMedCrossRefGoogle Scholar
  191. Schnell JD, Hicke L (2003) Non-traditional functions of ubiquitin and ubiquitin-binding proteins. J Biol Chem 278:35857–35860PubMedCrossRefGoogle Scholar
  192. Schöneberg J, Lee I-H, Iwasa JH, Hurley JH (2017) Reverse-topology membrane scission by the ESCRT proteins. Nat Rev Mol Cell Biol 18:5–17PubMedCrossRefGoogle Scholar
  193. Scott A, Chung HY, Gonciarz-Swiatek M, Hill GC, Whitby FG, Gaspar J, Holton JM, Viswanathan R, Ghaffarian S, Hill CP, Sundquist WI (2005) Structural and mechanistic studies of VPS4 proteins. EMBO J 24:3658–3669PubMedPubMedCentralCrossRefGoogle Scholar
  194. Shen QT, Schuh AL, Zheng Y, Quinney K, Wang L, Hanna M, Mitchell JC, Otegui MS, Ahlquist P, Cui Q, Audhya A (2014) Structural analysis and modeling reveals new mechanisms governing ESCRT-III spiral filament assembly. J Cell Biol 206:763–777PubMedPubMedCentralCrossRefGoogle Scholar
  195. Shen Q-T, Ren X, Zhang R, Lee I-H, Hurley JH (2015) HIV-1 Nef hijacks clathrin coats by stabilizing AP-1:Arf1 polygons. Science 350:aac5137Google Scholar
  196. Shestakova A, Hanono A, Drosner S, Curtiss M, Davies BA, Katzmann DJ, Babst M (2010) Assembly of the AAA ATPase Vps4 on ESCRT-III. Mol Biol Cell 21:1059–1071PubMedPubMedCentralCrossRefGoogle Scholar
  197. Shiflett SL, Ward DM, Huynh D, Vaughn MB, Simmons JC, Kaplan J (2004) Characterization of Vta1p, a class E Vps protein in Saccharomyces cerevisiae. J Biol Chem 279:10982–10990PubMedCrossRefGoogle Scholar
  198. Shih SC, Katzmann DJ, Schnell JD, Sutanto M, Emr SD, Hicke L (2002) Epsins and Vps27p/Hrs contain ubiquitin-binding domains that function in receptor endocytosis. Nat Cell Biol 4:389–393PubMedCrossRefGoogle Scholar
  199. Shim S, Kimpler LA, Hanson PI (2007) Structure/function analysis of four core ESCRT-III proteins reveals common regulatory role for extreme C-terminal domain. Traffic 8:1068–1079PubMedCrossRefGoogle Scholar
  200. Shukla AK, Westfield GH, Xiao K, Reis RI, Huang LY, Tripathi-Shukla P, Qian J, Li S, Blanc A, Oleskie AN, Dosey AM, Su M, Liang CR, Gu LL, Shan JM, Chen X, Hanna R, Choi M, Yao XJ, Klink BU, Kahsai AW, Sidhu SS, Koide S, Penczek PA, Kossiakoff AA, Woods VL Jr, Kobilka BK, Skiniotis G, Lefkowitz RJ (2014) Visualization of arrestin recruitment by a G-protein-coupled receptor. Nature 512:218–222PubMedPubMedCentralCrossRefGoogle Scholar
  201. Sigismund S, Woelk T, Puri C, Maspero E, Tacchetti C, Transidico P, di Fiore PP, Polo S (2005) Clathrin-independent endocytosis of ubiquitinated cargos. Proc Natl Acad Sci 102:2760–2765PubMedCrossRefGoogle Scholar
  202. Sigismund S, Argenzio E, Tosoni D, Cavallaro E, Polo S, di Fiore PP (2008) Clathrin-mediated internalization is essential for sustained EGFR signaling but dispensable for degradation. Dev Cell 15:209–219PubMedCrossRefPubMedCentralGoogle Scholar
  203. Skowyra ML, Schlesinger PH, Naismith TV, Hanson PI (2018) Triggered recruitment of ESCRT machinery promotes endolysosomal repair. Science 360Google Scholar
  204. Smardon AM, Kane PM (2014) Loss of vacuolar H+-ATPase activity in organelles signals ubiquitination and endocytosis of the yeast plasma membrane proton pump Pma1p. J Biol Chem 289:32316–32326PubMedPubMedCentralCrossRefGoogle Scholar
  205. Staub O, Abriel H, Plant P, Ishikawa T, Kanelis V, Saleki R, Horisberger JD, Schild L, Rotin D (2000) Regulation of the epithelial Na+ channel by Nedd4 and ubiquitination. Kidney Int 57:809–815PubMedCrossRefGoogle Scholar
  206. Stefani F, Zhang L, Taylor S, Donovan J, Rollinson S, Doyotte A, Brownhill K, Bennion J, Pickering-Brown S, Woodman P (2011) UBAP1 is a component of an endosome-specific ESCRT-I complex that is essential for MVB sorting. Curr Biol: CB 21:1245–1250PubMedCrossRefGoogle Scholar
  207. Stewart EV, Nwosu CC, Tong Z, Roguev A, Cummins TD, Kim D-U, Hayles J, Park H-O, Hoe K-L, Powell DW, Krogan NJ, Espenshade PJ (2011) Yeast SREBP cleavage activation requires the Golgi Dsc E3 ligase complex. Mol Cell 42:160–171PubMedPubMedCentralCrossRefGoogle Scholar
  208. 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 114:689–699PubMedCrossRefGoogle Scholar
  209. Su M, Guo EZ, Ding X, Li Y, Tarrasch JT, Brooks CL, Xu Z, Skiniotis G (2017) Mechanism of Vps4 hexamer function revealed by cryo-EM. Sci Adv 3:e1700325PubMedPubMedCentralCrossRefGoogle Scholar
  210. Suzuki A, Mochizuki T, Uemura S, Hiraki T, Abe F (2013) Pressure-induced endocytic degradation of the Saccharomyces cerevisiae low-affinity tryptophan permease Tat1 is mediated by Rsp5 ubiquitin ligase and functionally redundant PPxY motif proteins. Eukaryot Cell 12:990–997PubMedPubMedCentralCrossRefGoogle Scholar
  211. Swatek KN, Komander D (2016) Ubiquitin modifications. Cell Res 26:399–422Google Scholar
  212. Tanaka N, Kaneko K, Asao H, Kasai H, Endo Y, Fujita T, Takeshita T, Sugamura K (1999) Possible involvement of a novel STAM-associated molecule “AMSH” in intracellular signal transduction mediated by cytokines. J Biol Chem 274:19129–19135PubMedCrossRefGoogle Scholar
  213. Tang G, Zhang Z, Qian H, Chen J, Wang Y, Chen X, Chen B, Chen Y (2015) (-)-Epigallocatechin-3-gallate inhibits osteosarcoma cell invasiveness by inhibiting the MEK/ERK signaling pathway in human osteosarcoma cells. J Environ Pathol Toxicol Oncol 34:85–93PubMedCrossRefGoogle Scholar
  214. 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 5Google Scholar
  215. Teis D, Saksena S, Emr SD (2008) Ordered assembly of the ESCRT-III complex on endosomes is required to sequester cargo during MVB formation. Dev Cell 15:578–589PubMedCrossRefGoogle Scholar
  216. Teis D, Saksena S, Judson B, Emr S (2010) ESCRT-II coordinates the assembly of ESCRT-III filaments for cargo sorting and multivesicular body vesicle formation. EMBO J 29(5):871–883PubMedPubMedCentralCrossRefGoogle Scholar
  217. 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 7:559–569PubMedCrossRefGoogle Scholar
  218. Teo H, Gill DJ, Sun J, Perisic O, Veprintsev DB, Vallis Y, Emr SD, Williams RL (2006) ESCRT-I core and ESCRT-II GLUE domain structures reveal role for GLUE in linking to ESCRT-I and membranes. Cell 125:99–111PubMedCrossRefGoogle Scholar
  219. Thien CB, Langdon WY (2001) Cbl: many adaptations to regulate protein tyrosine kinases. Nat Rev Mol Cell Biol 2:294–307PubMedCrossRefGoogle Scholar
  220. Vashist S, Ng DTW (2004) Misfolded proteins are sorted by a sequential checkpoint mechanism of ER quality control. J Cell Biol 165:41–52PubMedPubMedCentralCrossRefGoogle Scholar
  221. 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 USA 98:7724–7729PubMedCrossRefGoogle Scholar
  222. Vietri M, Schink KO, Campsteijn C, Wegner CS, Schultz SW, Christ L, Thoresen SB, Brech A, Raiborg C, Stenmark H (2015) Spastin and ESCRT-III coordinate mitotic spindle disassembly and nuclear envelope sealing. Nature 522:231–235PubMedCrossRefPubMedCentralGoogle Scholar
  223. Vild CJ, Xu Z (2014) Vfa1 binds to the N-terminal microtubule-interacting and trafficking (MIT) domain of Vps4 and stimulates its ATPase activity. J Biol Chem 289:10378–10386PubMedPubMedCentralCrossRefGoogle Scholar
  224. von Schwedler UK, Stuchell M, Müller B, Ward DM, Chung HY, Morita E, Wang HE, Davis T, He G-P, Cimbora DM, Scott A, Kräusslich H-G, Kaplan J, Morham SG, Sundquist WI (2003) The protein network of HIV budding. Cell 114:701–713CrossRefGoogle Scholar
  225. Wang M, Pickart CM (2005) Different HECT domain ubiquitin ligases employ distinct mechanisms of polyubiquitin chain synthesis. EMBO J 24:4324–4333PubMedPubMedCentralCrossRefGoogle Scholar
  226. Webster BM, Colombi P, Jager J, Lusk CP (2014) Surveillance of nuclear pore complex assembly by ESCRT-III/Vps4. Cell 159:388–401PubMedPubMedCentralCrossRefGoogle Scholar
  227. Webster BM, Thaller DJ, Jager J, Ochmann SE, Borah S, Lusk CP (2016) Chm7 and Heh1 collaborate to link nuclear pore complex quality control with nuclear envelope sealing. EMBO J 35:2447–2467PubMedPubMedCentralCrossRefGoogle Scholar
  228. Wee P, Wang Z (2017) Epidermal growth factor receptor cell proliferation signaling pathways. Cancers 9:52PubMedCentralCrossRefPubMedGoogle Scholar
  229. Wehman AM, Poggioli C, Schweinsberg P, Grant BD, Nance J (2011) The P4-ATPase TAT-5 inhibits the budding of extracellular vesicles in C. elegans embryos. Curr Biol: CB 21:1951–1959PubMedCrossRefGoogle Scholar
  230. Wemmer M, Azmi I, West M, Davies B, Katzmann D, Odorizzi G (2011) Bro1 binding to Snf7 regulates ESCRT-III membrane scission activity in yeast. J Cell Biol 192(2):295–306PubMedPubMedCentralCrossRefGoogle Scholar
  231. Wollert T, Hurley JH (2010) Molecular mechanism of multivesicular body biogenesis by ESCRT complexes. Nature 464:864–869PubMedPubMedCentralCrossRefGoogle Scholar
  232. Wright MH, Berlin I, Nash PD (2011) Regulation of endocytic sorting by ESCRT-DUB-mediated deubiquitination. Cell Biochem Biophys 60:39–46PubMedCrossRefGoogle Scholar
  233. Wu N, Zheng B, Shaywitz A, Dagon Y, Tower C, Bellinger G, Shen C-H, Wen J, Asara J, McGraw TE, Kahn BB, Cantley LC (2013) AMPK-dependent degradation of TXNIP upon energy stress leads to enhanced glucose uptake via GLUT1. Mol Cell 49:1167–1175PubMedPubMedCentralCrossRefGoogle Scholar
  234. Wunderley L, Brownhill K, Stefani F, Tabernero L, Woodman P (2014) The molecular basis for selective assembly of the UBAP1-containing endosome-specific ESCRT-I complex. J Cell Sci 127:663–672PubMedPubMedCentralCrossRefGoogle Scholar
  235. Xiao J, Xia H, Yoshino-Koh K, Zhou J, Xu Z (2007) Structural characterization of the ATPase reaction cycle of endosomal AAA protein Vps4. J Mol Biol 374:655–670PubMedPubMedCentralCrossRefGoogle Scholar
  236. Yamada-Inagawa T, Okuno T, Karata K, Yamanaka K, Ogura T (2003) Conserved pore residues in the AAA protease FtsH are important for proteolysis and its coupling to ATP hydrolysis. J Biol Chem 278:50182–50187PubMedCrossRefGoogle Scholar
  237. Yang DEA (2008) Structural basis for midbody targeting of spastin by the ESCRT-III protein CHMP1B. Nat Struct Mol Biol 15:1278–1286PubMedPubMedCentralCrossRefGoogle Scholar
  238. 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 22:492–498PubMedPubMedCentralCrossRefGoogle Scholar
  239. Yeo SC, Xu L, Ren J, Boulton VJ, Wagle MD, Liu C, Ren G, Wong P, Zahn R, Sasajala P, Yang H, Piper RC, Munn AL (2003) Vps20p and Vta1p interact with Vps4p and function in multivesicular body sorting and endosomal transport in Saccharomyces cerevisiae. J Cell Sci 116:3957–3970PubMedCrossRefGoogle Scholar
  240. Yokouchi M, Kondo T, Houghton A, Bartkiewicz M, Horne WC, Zhang H, Yoshimura A, Baron R (1999) Ligand-induced ubiquitination of the epidermal growth factor receptor involves the interaction of the c-Cbl RING finger and UbcH7. J Biol Chem 274:31707–31712PubMedCrossRefGoogle Scholar
  241. Zakalskiy A, Hogenauer G, Ishikawa T, Wehrschutz-Sigl E, Wendler F, Teis D, Zisser G, Steven AC, Bergler H (2002) Structural and enzymatic properties of the AAA protein Drg1p from Saccharomyces cerevisiae. Decoupling of intracellular function from ATPase activity and hexamerization. J Biol Chem 277:26788–26795PubMedCrossRefGoogle Scholar
  242. 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. Proc Natl Acad Sci USA 103:19140–19145PubMedCrossRefGoogle Scholar
  243. Zhang H, Wang Y, Wong JJ, Lim KL, Liou YC, Wang H, Yu F (2014) Endocytic pathways downregulate the L1-type cell adhesion molecule neuroglian to promote dendrite pruning in Drosophila. Dev Cell 30:463–478PubMedCrossRefGoogle Scholar
  244. Zhao Y, Macgurn JA, Liu M, Emr S (2013) The ART-Rsp5 ubiquitin ligase network comprises a plasma membrane quality control system that protects yeast cells from proteotoxic stress. Elife 2:e00459PubMedPubMedCentralCrossRefGoogle Scholar
  245. Zhongzheng Y, Cody V, Jiaying J, Xu Z, Jianping L, Jie S, Bin Z, Wenxian L, Fuchung G, Maili L, Chunyang C, Zhaohui X (2012) Structural basis of molecular recognition between ESCRT-III like protein Vps60 and AAA-ATPase regulator Vta1 in the multi-vesicular body pathway. JBC 287:43899–43908CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Division of Cell Biology, BiocenterMedical University of InnsbruckInnsbruckAustria

Personalised recommendations