The ESCRT machinery: A cellular apparatus for sorting and scission

Biochemical Society Transactions

Volumn 38, Issue 6, 2010, Pages 1397-1412

  Carlton, Jeremy ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Cytokinesis; Endosomal sorting; Endosomal sorting complex required for transport (ESCRT); Membrane trafficking; Viral budding

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; BACULOVIRUS INHIBITOR OF APOPTOSIS REPEAT CONTAINING UBIQUITIN CONJUGATING ENZYME; CENTROMERE PROTEIN 55; EPIDERMAL GROWTH FACTOR; ESCRT PROTEIN; GAG PROTEIN; MEMBRANE PROTEIN; MITOTIC KINESIN LIKE PROTEIN 1; SNARE PROTEIN; SNF7 PROTEIN; SPASTIN; UBIQUITIN PROTEIN LIGASE NEDD4; UNCLASSIFIED DRUG;

ARTICLE; CYTOKINESIS; DAUGHTER CELL; ENDOSOME; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN TARGETING; RETROVIRUS; UBIQUITINATION;

ANIMALS; CELL MEMBRANE; CYTOKINESIS; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; ENDOSOMES; FUNGAL PROTEINS; PROTEIN SUBUNITS; PROTEIN TRANSPORT; VIRUSES;

EID: 78649738729     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST0381397     Document Type: Article

References (188)

1. Bankaitis, V.A., Johnson, L.M. and Emr, S.D. (1986) Isolation of yeast mutants defective in protein targeting to the vacuole. Proc. Natl. Acad. Sci. U.S.A. 83, 9075-9079
2. Robinson, J.S., Klionsky, D.J., Banta, L.M. and Emr, S.D. (1988) Protein sorting in Saccharomyces cerevisiae: isolation of mutants defective in the delivery and processing of multiple vacuolar hydrolases. Mol. Cell. Biol. 8, 4936-4948
3. Raymond, C.K., Howald-Stevenson, I., Vater, C.A. and Stevens, T.H. (1992) Morphological classification of the yeast vacuolar protein sorting mutants: evidence for a prevacuolar compartment in class E vps mutants. Mol. Biol. Cell 3, 1389-1402
4. Katzmann, D.J., Babst, M. and Emr, S.D. (2001) Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell 106, 145-155 (Pubitemid 32772626)
5. Babst, M., Katzmann, D.J., Snyder, W.B., Wendland, B. and Emr, S.D. (2002) Endosome-associated complex, ESCRT-II, recruits transport machinery for protein sorting at the multivesicular body. Dev. Cell 3, 283-289
6. Babst, M., Katzmann, D.J., Estepa-Sabal, E.J., Meerloo, T. and Emr, S.D. (2002) Escrt-III: an endosome-associated heterooligomeric protein complex required for MVB sorting. Dev. Cell 3, 271-282
7. Williams, R.L. and Urbé, S. (2007) The emerging shape of the ESCRT machinery. Nat. Rev. Mol. Cell Biol. 8, 355-368
8. Babst, M., Odorizzi, G., Estepa, E.J. and Emr, S.D. (2000) Mammalian tumor susceptibility gene 101 (TSG101) and the yeast homologue, Vps23p, both function in late endosomal trafficking. Traffic 1, 248-258
9. Bishop, N. and Woodman, P. (2001) TSG101/mammalian VPS23 and mammalian VPS28 interact directly and are recruited to VPS4-induced endosomes. J. Biol. Chem. 276, 11735-11742
10. Bishop, N., Horman, A. and Woodman, P. (2002) Mammalian class E vps proteins recognize ubiquitin and act in the removal of endosomal protein-ubiquitin conjugates. J. Cell Biol. 157, 91-101 (Pubitemid 34847832)
11. VerPlank, L., Bouamr, F., LaGrassa, T.J., Agresta, B., Kikonyogo, A., Leis, J. and Carter, C.A. (2001) Tsg101, a homologue of ubiquitin-conjugating (E2) enzymes, binds the L domain in HIV type 1 Pr55(Gag). Proc. Natl. Acad. Sci. U.S.A. 98, 7724-7729
12. Garrus, J.E., von Schwedler, U.K., Pornillos, O.W., Morham, S.G., Zavitz, K.H., Wang, H.E., Wettstein, D.A., Stray, K.M., Cote, M., Rich, R.L. et al. (2001) Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 107, 55-65
13. Martin-Serrano, J., Zang, T. and Bieniasz, P.D. (2001) HIV-1 and Ebola virus encode small peptide motifs that recruit Tsg101 to sites of particle assembly to facilitate egress. Nat. Med. 7, 1313-1319
14. Demirov, D.G., Ono, A., Orenstein, J.M. and Freed, E.O. (2002) Overexpression of the N-terminal domain of TSG101 inhibits HIV-1 budding by blocking late domain function. Proc. Natl. Acad. Sci. U.S.A. 99, 955-960
15. Morita, E. and Sundquist, W.I. (2004) Retrovirus budding. Annu. Rev. Cell Dev. Biol. 20, 395-425
16. Carlton, J.G. and Martin-Serrano, J. (2007) Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery. Science 316, 1908-1912
17. Morita, E., Sandrin, V., Chung, H.Y., Morham, S.G., Gygi, S.P., Rodesch, C.K. and Sundquist, W.I. (2007) Human ESCRT and ALIX proteins interact with proteins of the midbody and function in cytokinesis. EMBO J. 26, 4215-4227 (Pubitemid 47525161)
18. Carlton, J.G., Agromayor, M. and Martin-Serrano, J. (2008) Differential requirements for Alix and ESCRT-III in cytokinesis and HIV-1 release. Proc. Natl. Acad. Sci. U.S.A. 105, 10541-10546
19. Katzmann, D.J., Sarkar, S., Chu, T., Audhya, A. and Emr, S.D. (2004) Multivesicular body sorting: ubiquitin ligase Rsp5 is required for the modification and sorting of carboxypeptidase. Mol. Biol. Cell 15, 468-480
20. Waterman, H., Levkowitz, G., Alroy, I. and Yarden, Y. (1999) The RING finger of c-Cbl mediates desensitization of the epidermal growth factor receptor. J. Biol. Chem. 274, 22151-22154
21. Lin, C.H., MacGurn, J.A., Chu, T., Stefan, C.J. and Emr, S.D. (2008) Arrestin-related ubiquitin-ligase adaptors regulate endocytosis and protein turnover at the cell surface. Cell 135, 714-725
22. Nikko, E., Sullivan, J.A. and Pelham, H.R. (2008) Arrestin-like proteins mediate ubiquitination and endocytosis of the yeast metal transporter Smf1. EMBO Rep. 9, 1216-1221
23. Razi, M. and Futter, C.E. (2006) Distinct roles for Tsg101 and Hrs in multivesicular body formation and inward vesiculation. Mol. Biol. Cell 17, 3469-3483
24. Doyotte, A., Russell, M.R., Hopkins, C.R. and Woodman, P.G. (2005) Depletion of TSG101 forms a mammalian "Class E" compartment: a multicisternal early endosome with multiple sorting defects. J. Cell Sci. 118, 3003-3017
25. Rodahl, L.M., Stuffers, S., Lobert, V.H. and Stenmark, H. (2009) The role of ESCRT proteins in attenuation of cell signalling. Biochem. Soc. Trans. 37, 137-142
26. Bache, K.G., Stuffers, S., Malerod, L., Slagsvold, T., Raiborg, C., Lechardeur, D., Walchli, S., Lukacs, G.L., Brech, A. and Stenmark, H. (2006) The ESCRT-III subunit hVps24 is required for degradation but not silencing of the epidermal growth factor receptor. Mol. Biol. Cell 17, 2513-2523
27. Bache, K.G., Slagsvold, T. and Stenmark, H. (2004) Defective downregulation of receptor tyrosine kinases in cancer. EMBO J. 23, 2707-2712 (Pubitemid 39013543)
28. Saksena, S. and Emr, S.D. (2009) ESCRTs and human disease. Biochem. Soc. Trans. 37, 167-172
29. Göttlinger, H.G., Dorfman, T., Sodroski, J.G. and Haseltine, W.A. (1991) Effect of mutations affecting the p6 gag protein on human immunodeficiency virus particle release. Proc. Natl. Acad. Sci. U.S.A. 88, 3195-3199
30. Huang, M., Orenstein, J.M., Martin, M.A. and Freed, E.O. (1995) p6Gag is required for particle production from full-length human immunodeficiency virus type 1 molecular clones expressing protease. J. Virol. 69, 6810-6818
31. Parent, L.J., Bennett, R.P., Craven, R.C., Nelle, T.D., Krishna, N.K., Bowzard, J.B., Wilson, C.B., Puffer, B.A., Montelaro, R.C. and Wills, J.W. (1995) Positionally independent and exchangeable late budding functions of the Rous sarcoma virus and human immunodeficiency virus Gag proteins. J. Virol. 69, 5455-5460
32. Strack, B., Calistri, A., Craig, S., Popova, E. and Göttlinger, H.G. (2003) AIP1/ALIX is a binding partner for HIV-1 p6 and EIAV p9 functioning in virus budding. Cell 114, 689-699 (Pubitemid 37186765)
33. Martin-Serrano, J., Yarovoy, A., Perez-Caballero, D. and Bieniasz, P.D. (2003) Divergent retroviral late-budding domains recruit vacuolar protein sorting factors by using alternative adaptor proteins. Proc. Natl. Acad. Sci. U.S.A. 100, 12414-12419
34. Pornillos, O., Alam, S.L., Davis, D.R. and Sundquist, W.I. (2002) Structure of the Tsg101 UEV domain in complex with the PTAP motif of the HIV-1 p6 protein. Nat. Struct. Biol. 9, 812-817
35. Pornillos, O., Alam, S.L., Rich, R.L., Myszka, D.G., Davis, D.R. and Sundquist, W.I. (2002) Structure and functional interactions of the Tsg101 UEV domain. EMBO J. 21, 2397-2406 (Pubitemid 34546712)
36. Munshi, U.M., Kim, J., Nagashima, K., Hurley, J.H. and Freed, E.O. (2007) An Alix fragment potently inhibits HIV-1 budding: characterization of binding to retroviral YPXL late domains. J. Biol. Chem. 282, 3847-3855
37. Fisher, R.D., Chung, H.Y., Zhai, Q., Robinson, H., Sundquist, W.I. and Hill, C.P. (2007) Structural and biochemical studies of ALIX/AIP1 and its role in retrovirus budding. Cell 128, 841-852 (Pubitemid 46341413)
38. Lee, S., Joshi, A., Nagashima, K., Freed, E.O. and Hurley, J.H. (2007) Structural basis for viral late-domain binding to Alix. Nat. Struct. Mol. Biol. 14, 194-199
39. Usami, Y., Popov, S. and Göttlinger, H.G. (2007) Potent rescue of human immunodeficiency virus type 1 late domain mutants by ALIX/AIP1 depends on its CHMP4 binding site. J. Virol. 81, 6614-6622 (Pubitemid 46878065)
40. McCullough, J., Fisher, R.D., Whitby, F.G., Sundquist, W.I. and Hill, C.P. (2008) ALIX-CHMP4 interactions in the human ESCRT pathway. Proc. Natl. Acad. Sci. U.S.A. 105, 7687-7691
41. Bouamr, F., Melillo, J.A., Wang, M.Q., Nagashima, K., de Los Santos, M., Rein, A. and Goff, S.P. (2003) PPPYVEPTAP motif is the late domain of human T-cell leukemia virus type 1 Gag and mediates its functional interaction with cellular proteins Nedd4 and Tsg101. J. Virol. 77, 11882-11895 (Pubitemid 37339842)
42. Harty, R.N., Brown, M.E., Wang, G., Huibregtse, J. and Hayes, F.P. (2000) A PPxY motif within the VP40 protein of Ebola virus interacts physically and functionally with a ubiquitin ligase: implications for filovirus budding. Proc. Natl. Acad. Sci. U.S.A. 97, 13871-13876
43. Kikonyogo, A., Bouamr, F., Vana, M.L., Xiang, Y., Aiyar, A., Carter, C. and Leis, J. (2001) Proteins related to the Nedd4 family of ubiquitin protein ligases interact with the L domain of Rous sarcoma virus and are required for gag budding from cells. Proc. Natl. Acad. Sci. U.S.A. 98, 11199-11204
44. Martin-Serrano, J., Eastman, S.W., Chung, W. and Bieniasz, P.D. (2005) HECT ubiquitin ligases link viral and cellular PPXY motifs to the vacuolar protein-sorting pathway. J. Cell Biol. 168, 89-101 (Pubitemid 40111060)
45. Schmitt, A.P., Leser, G.P., Morita, E., Sundquist, W.I. and Lamb, R.A. (2005) Evidence for a new viral late-domain core sequence, FPIV, necessary for budding of a paramyxovirus. J. Virol. 79, 2988-2997 (Pubitemid 40270578)
46. Martin-Serrano, J. (2007) The role of ubiquitin in retroviral egress. Traffic 8, 1297-1303
47. Strack, B., Calistri, A., Accola, M.A., Palu, G. and Göttlinger, H.G. (2000) A role for ubiquitin ligase recruitment in retrovirus release. Proc. Natl. Acad. Sci. U.S.A. 97, 13063-13068
48. Strack, B., Calistri, A. and Göttlinger, H.G. (2002) Late assembly domain function can exhibit context dependence and involves ubiquitin residues implicated in endocytosis. J. Virol. 76, 5472-5479 (Pubitemid 34517897)
49. Joshi, A., Munshi, U., Ablan, S.D., Nagashima, K. and Freed, E.O. (2008) Functional replacement of a retroviral late domain by ubiquitin fusion. Traffic 9, 1972-1983
50. Zhadina, M., McClure, M.O., Johnson, M.C. and Bieniasz, P.D. (2007) Ubiquitin-dependent virus particle budding without viral protein ubiquitination. Proc. Natl. Acad. Sci. U.S.A. 104, 20031-20036
51. Martin-Serrano, J. and Bieniasz, P.D. (2003) A bipartite late-budding domain in human immunnodeficiency virus type 1. J. Virol. 77, 12373-12377 (Pubitemid 37339892)
52. Usami, Y., Popov, S., Popova, E. and Göttlinger, H.G. (2008) Efficient and specific rescue of human immunodeficiency virus type 1 budding defects by a Nedd4-like ubiquitin ligase. J. Virol. 82, 4898-4907 (Pubitemid 351657051)
53. Chung, H.Y., Morita, E., von Schwedler, U., Muller, B., Krausslich, H.G. and Sundquist, W.I. (2008) NEDD4L overexpression rescues the release and infectivity of human immunodeficiency virus type 1 constructs lacking PTAP and YPXL late domains. J. Virol. 82, 4884-4897 (Pubitemid 351657050)
54. Popov, S., Popova, E., Inoue, M. and Göttlinger, H.G. (2008) Human immunodeficiency virus type 1 Gag engages the Bro1 domain of ALIX/AIP1 through the nucleocapsid. J. Virol. 82, 1389-1398
55. Dussupt, V., Javid, M.P., Abou-Jaoude, G., Jadwin, J.A., de La Cruz, J., Nagashima, K. and Bouamr, F. (2009) 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, e1000339
56. Popova, E., Popov, S. and Göttlinger, H.G. (2010) Human immunodeficiency virus type 1 nucleocapsid p1 confers ESCRT pathway dependence. J. Virol. 84, 6590-6597
57. Popov, S., Popova, E., Inoue, M. and Göttlinger, H.G. (2009) Divergent Bro1 domains share the capacity to bind human immunodeficiency virus type 1 nucleocapsid and to enhance virus-like particle production. J. Virol. 83, 7185-7193
58. Barr, F.A. and Gruneberg, U. (2007) Cytokinesis: placing and making the final cut. Cell 131, 847-860
59. Glotzer, M. (2001) Animal cell cytokinesis. Annu. Rev. Cell Dev. Biol. 17, 351-386
60. Pollard, T.D. (2010) Mechanics of cytokinesis in eukaryotes. Curr. Opin. Cell Biol. 22, 50-56
61. Matuliene, J. and Kuriyama, R. (2002) Kinesin-like protein CHO1 is required for the formation of midbody matrix and the completion of cytokinesis in mammalian cells. Mol. Biol. Cell 13, 1832-1845
62. Gromley, A., Jurczyk, A., Sillibourne, J., Halilovic, E., Mogensen, M., Groisman, I., Blomberg, M. and Doxsey, S. (2003) A novel human protein of the maternal centriole is required for the final stages of cytokinesis and entry into S phase. J. Cell Biol. 161, 535-545 (Pubitemid 36578578)
63. Pohl, C. and Jentsch, S. (2008) Final stages of cytokinesis and midbody ring formation are controlled by BRUCE. Cell 132, 832-845 (Pubitemid 351312799)
64. Fabbro, M., Zhou, B.B., Takahashi, M., Sarcevic, B., Lal, P., Graham, M.E., Gabrielli, B.G., Robinson, P.J., Nigg, E.A., Ono, Y. and Khanna, K.K. (2005) Cdk1/Erk2- and Plk1-dependent phosphorylation of a centrosome protein, Cep55, is required for its recruitment to midbody and cytokinesis. Dev. Cell 9, 477-488 (Pubitemid 41430731)
65. Zhao, W.M., Seki, A. and Fang, G. (2006) Cep55, a microtubule-bundling protein, associates with centralspindlin to control the midbody integrity and cell abscission during cytokinesis. Mol. Biol. Cell 17, 3881-3896
66. Martinez-Garay, I., Rustom, A., Gerdes, H.H. and Kutsche, K. (2006) The novel centrosomal associated protein CEP55 is present in the spindle midzone and the midbody. Genomics 87, 243-253
67. Gromley, A., Yeaman, C., Rosa, J., Redick, S., Chen, C.T., Mirabelle, S., Guha, M., Sillibourne, J. and Doxsey, S.J. (2005) Centriolin anchoring of exocyst and SNARE complexes at the midbody is required for secretory-vesicle- mediated abscission. Cell 123, 75-87
68. Low, S.H., Li, X., Miura, M., Kudo, N., Quinones, B. and Weimbs, T. (2003) Syntaxin 2 and endobrevin are required for the terminal step of cytokinesis in mammalian cells. Dev. Cell 4, 753-759
69. Wilson, G.M., Fielding, A.B., Simon, G.C., Yu, X., Andrews, P.D., Hames, R.S., Frey, A.M., Peden, A.A., Gould, G.W. and Prekeris, R. (2005) The FIP3-Rab11 protein complex regulates recycling endosome targeting to the cleavage furrow during late cytokinesis. Mol. Biol. Cell 16, 849-860
70. Kouranti, I., Sachse, M., Arouche, N., Goud, B. and Echard, A. (2006) Rab35 regulates an endocytic recycling pathway essential for the terminal steps of cytokinesis. Curr. Biol. 16, 1719-1725
71. Fielding, A.B., Schonteich, E., Matheson, J., Wilson, G., Yu, X., Hickson, G.R., Srivastava, S., Baldwin, S.A., Prekeris, R. and Gould, G.W. (2005) Rab11-FIP3 and FIP4 interact with Arf6 and the exocyst to control membrane traffic in cytokinesis. EMBO J. 24, 3389-3399
72. Yu, X., Prekeris, R. and Gould, G.W. (2007) Role of endosomal Rab GTPases in cytokinesis. Eur. J. Cell Biol. 86, 25-35
73. Lee, H.H., Elia, N., Ghirlando, R., Lippincott-Schwartz, J. and Hurley, J.H. (2008) Midbody targeting of the ESCRT machinery by a noncanonical coiled coil in CEP55. Science 322, 576-580
74. Dukes, J.D., Richardson, J.D., Simmons, R. and Whitley, P. (2008) A dominant-negative ESCRT-III protein perturbs cytokinesis and trafficking to lysosomes. Biochem. J. 411, 233-239
75. McDonald, B. and Martin-Serrano, J. (2009) No strings attached: the ESCRT machinery in viral budding and cytokinesis. J. Cell Sci. 122, 2167-2177
76. Agromayor, M., Carlton, J.G., Phelan, J.P., Matthews, D.R., Carlin, L.M., Ameer-Beg, S., Bowers, K. and Martin-Serrano, J. (2009) Essential role of hIST1 in cytokinesis. Mol. Biol. Cell 20, 1374-1387
77. Bajorek, M., Morita, E., Skalicky, J.J., Morham, S.G., Babst, M. and Sundquist, W.I. (2009) Biochemical analyses of human IST1 and its function in cytokinesis. Mol. Biol. Cell 20, 1360-1373
78. Steigemann, P., Wurzenberger, C., Schmitz, M.H., Held, M., Guizetti, J., Maar, S. and Gerlich, D.W. (2009) Aurora B-mediated abscission checkpoint protects against tetraploidization. Cell 136, 473-484
79. Reid, E., Connell, J., Edwards, T.L., Duley, S., Brown, S.E. and Sanderson, C.M. (2005) The hereditary spastic paraplegia protein spastin interacts with the ESCRT-III complex-associated endosomal protein CHMP1B. Hum. Mol. Genet. 14, 19-38
80. Iwaya, N., Kuwahara, Y., Fujiwara, Y., Goda, N., Tenno, T., Akiyama, K., Mase, S., Tochio, H., Ikegami, T., Shirakawa, M. and Hiroaki, H. (2010) A common substrate recognition mode conserved between katanin P60 and VPS4 governs microtubule severing and membrane skeleton reorganization. J. Biol. Chem. 285, 16822-16829
81. Roll-Mecak, A. and McNally, F.J. (2010) Microtubule-severing enzymes. Curr. Opin. Cell Biol. 22, 96-103
82. Errico, A., Claudiani, P., D'Addio, M. and Rugarli, E.I. (2004) Spastin interacts with the centrosomal protein NA14, and is enriched in the spindle pole, the midbody and the distal axon. Hum. Mol. Genet. 13, 2121-2132
83. Yang, D., Rismanchi, N., Renvoise, B., Lippincott-Schwartz, J., Blackstone, C. and Hurley, J.H. (2008) Structural basis for midbody targeting of spastin by the ESCRT-III protein CHMP1B. Nat. Struct. Mol. Biol. 15, 1278-1286
84. Connell, J.W., Lindon, C., Luzio, J.P. and Reid, E. (2009) Spastin couples microtubule severing to membrane traffic in completion of cytokinesis and secretion. Traffic 10, 42-56
85. Spitzer, C., Schellmann, S., Sabovljevic, A., Shahriari, M., Keshavaiah, C., Bechtold, N., Herzog, M., Muller, S., Hanisch, F.G. and Hulskamp, M. (2006) The Arabidopsis elch mutant reveals functions of an ESCRT component in cytokinesis. Development 133, 4679-4689
86. Obita, T., Saksena, S., Ghazi-Tabatabai, S., Gill, D.J., Perisic, O., Emr, S.D. and Williams, R.L. (2007) Structural basis for selective recognition of ESCRT-III by the AAA ATPase Vps4. Nature 449, 735-739
87. Samson, R.Y., Obita, T., Freund, S.M., Williams, R.L. and Bell, S.D. (2008) A role for the ESCRT system in cell division in archaea. Science 322, 1710-1713
88. Lindas, A.C., Karlsson, E.A., Lindgren, M.T., Ettema, T.J. and Bernander, R. (2008) A unique cell division machinery in the Archaea. Proc. Natl. Acad. Sci. U.S.A. 105, 18942-18946
89. Mullins, J.M. and Biesele, J.J. (1977) Terminal phase of cytokinesis in D-98s cells. J. Cell Biol. 73, 672-684
90. Bilodeau, P.S., Urbanowski, J.L., Winistorfer, S.C. and Piper, R.C. (2002) The Vps27p Hse1p complex binds ubiquitin and mediates endosomal protein sorting. Nat. Cell Biol. 4, 534-539
91. Bache, K.G., Raiborg, C., Mehlum, A. and Stenmark, H. (2003) STAM and Hrs are subunits of a multivalent ubiquitin-binding complex on early endosomes. J. Biol. Chem. 278, 12513-12521
92. Kanazawa, C., Morita, E., Yamada, M., Ishii, N., Miura, S., Asao, H., Yoshimori, T. and Sugamura, K. (2003) Effects of deficiencies of STAMs and Hrs, mammalian class E Vps proteins, on receptor downregulation. Biochem. Biophys. Res. Commun. 309, 848-856
93. Prag, G., Watson, H., Kim, Y.C., Beach, B.M., Ghirlando, R., Hummer, G., Bonifacino, J.S. and Hurley, J.H. (2007) The Vps27/Hse1 complex is a GAT domain-based scaffold for ubiquitin-dependent sorting. Dev. Cell 12, 973-986
94. Raiborg, C., Bremnes, B., Mehlum, A., Gillooly, D.J., D'Arrigo, A., Stang, E. and Stenmark, H. (2001) FYVE and coiled-coil domains determine the specific localisation of Hrs to early endosomes. J. Cell Sci. 114, 2255-2263
95. Stahelin, R.V., Long, F., Diraviyam, K., Bruzik, K.S., Murray, D. and Cho, W. (2002) Phosphatidylinositol 3-phosphate induces the membrane penetration of the FYVE domains of Vps27p and Hrs. J. Biol. Chem. 277, 26379-26388
96. Katzmann, D.J., Stefan, C.J., Babst, M. and Emr, S.D. (2003) Vps27 recruits ESCRT machinery to endosomes during MVB sorting. J. Cell Biol. 162, 413-423
97. Bilodeau, P.S., Winistorfer, S.C., Kearney, W.R., Robertson, A.D. and Piper, R.C. (2003) Vps27-Hse1 and ESCRT-I complexes cooperate to increase efficiency of sorting ubiquitinated proteins at the endosome. J. Cell Biol. 163, 237-243
98. Bache, K.G., Brech, A., Mehlum, A. and Stenmark, H. (2003) Hrs regulates multivesicular body formation via ESCRT recruitment to endosomes. J. Cell Biol. 162, 435-442
99. Pornillos, O., Higginson, D.S., Stray, K.M., Fisher, R.D., Garrus, J.E., Payne, M., He, G.P., Wang, H.E., Morham, S.G. and Sundquist, W.I. (2003) HIV Gag mimics the Tsg101-recruiting activity of the human Hrs protein. J. Cell Biol. 162, 425-434
100. Urbé, S., Sachse, M., Row, P.E., Preisinger, C., Barr, F.A., Strous, G., Klumperman, J. and Clague, M.J. (2003) The UIM domain of Hrs couples receptor sorting to vesicle formation. J. Cell Sci. 116, 4169-4179
101. Hirano, S., Kawasaki, M., Ura, H., Kato, R., Raiborg, C., Stenmark, H. and Wakatsuki, S. (2006) Double-sided ubiquitin binding of Hrs-UIM in endosomal protein sorting. Nat. Struct. Mol. Biol. 13, 272-277
102. Ren, X. and Hurley, J.H. (2010) VHS domains of ESCRT-0 cooperate in high-avidity binding to polyubiquitinated cargo. EMBO J. 29, 1045-1054
103. Raiborg, C., Bache, K.G., Mehlum, A., Stang, E. and Stenmark, H. (2001) Hrs recruits clathrin to early endosomes. EMBO J. 20, 5008-5021
104. Sachse, M., Urbé, S., Oorschot, V., Strous, G.J. and Klumperman, J. (2002) Bilayered clathrin coats on endosomal vacuoles are involved in protein sorting toward lysosomes. Mol. Biol. Cell 13, 1313-1328
105. McCullough, J., Row, P.E., Lorenzo, O., Doherty, M., Beynon, R., Clague, M.J. and Urbé, S. (2006) Activation of the endosome-associated ubiquitin isopeptidase AMSH by STAM, a component of the multivesicular body-sorting machinery. Curr. Biol. 16, 160-165
106. Luhtala, N. and Odorizzi, G. (2004) Bro1 coordinates deubiquitination in the multivesicular body pathway by recruiting Doa4 to endosomes. J. Cell Biol. 166, 717-729
107. Kato, M., Miyazawa, K. and 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, 37481-37487
108. Swaminathan, S., Amerik, A.Y. and Hochstrasser, M. (1999) The Doa4 deubiquitinating enzyme is required for ubiquitin homeostasis in yeast. Mol. Biol. Cell 10, 2583-2594
109. Kostelansky, M.S., Schluter, C., Tam, Y.Y., Lee, S., Ghirlando, R., Beach, B., Conibear, E. and Hurley, J.H. (2007) Molecular architecture and functional model of the complete yeast ESCRT-I heterotetramer. Cell 129, 485-498
110. Kostelansky, M.S., Sun, J., Lee, S., Kim, J., Ghirlando, R., Hierro, A., Emr, S.D. and Hurley, J.H. (2006) Structural and functional organization of the ESCRT-I trafficking complex. Cell 125, 113-126
111. Gill, D.J., Teo, H., Sun, J., Perisic, O., Veprintsev, D.B., Emr, S.D. and Williams, R.L. (2007) Structural insight into the ESCRT-I/-II link and its role in MVB trafficking. EMBO J. 26, 600-612
112. Teo, H., Gill, D.J., Sun, J., Perisic, O., Veprintsev, D.B., Vallis, Y., Emr, S.D. and Williams, R.L. (2006) ESCRT-I core and ESCRT-II GLUE domain structures reveal role for GLUE in linking to ESCRT-I and membranes. Cell 125, 99-111
113. Morita, E., Sandrin, V., Alam, S.L., Eckert, D.M., Gygi, S.P. and Sundquist, W.I. (2007) Identification of human MVB12 proteins as ESCRT-I subunits that function in HIV budding. Cell Host Microbe 2, 41-53
114. Lu, Q., Hope, L.W., Brasch, M., Reinhard, C. and Cohen, S.N. (2003) TSG101 interaction with HRS mediates endosomal trafficking and receptor down-regulation. Proc. Natl. Acad. Sci. U.S.A. 100, 7626-7631
115. Teo, H., Veprintsev, D.B. and Williams, R.L. (2004) Structural insights into endosomal sorting complex required for transport (ESCRT-I) recognition of ubiquitinated proteins. J. Biol. Chem. 279, 28689-28696
116. Sundquist, W.I., Schubert, H.L., Kelly, B.N., Hill, G.C., Holton, J.M. and Hill, C.P. (2004) Ubiquitin recognition by the human TSG101 protein. Mol. Cell 13, 783-789
117. Shields, S.B., Oestreich, A.J., Winistorfer, S., Nguyen, D., Payne, J.A., Katzmann, D.J. and Piper, R. (2009) ESCRT ubiquitin-binding domains function cooperatively during MVB cargo sorting. J. Cell Biol. 185, 213-224
118. Wright, E.R., Schooler, J.B., Ding, H.J., Kieffer, C., Fillmore, C., Sundquist, W.I. and Jensen, G.J. (2007) Electron cryotomography of immature HIV-1 virions reveals the structure of the CA and SP1 Gag shells. EMBO J. 26, 2218-2226
119. Carlson, L.A., Briggs, J.A., Glass, B., Riches, J.D., Simon, M.N., Johnson, M.C., Muller, B., Grunewald, K. and Krausslich, H.G. (2008) Three-dimensional analysis of budding sites and released virus suggests a revised model for HIV-1 morphogenesis. Cell Host Microbe 4, 592-599
120. Hierro, A., Sun, J., Rusnak, A.S., Kim, J., Prag, G., Emr, S.D. and Hurley, J.H. (2004) Structure of the ESCRT-II endosomal trafficking complex. Nature 431, 221-225
121. Teo, H., Perisic, O., Gonzalez, B. and Williams, R.L. (2004) ESCRT-II, an endosome-associated complex required for protein sorting: crystal structure and interactions with ESCRT-III and membranes. Dev. Cell 7, 559-569
122. Im, Y.J. and Hurley, J.H. (2008) Integrated structural model and membrane targeting mechanism of the human ESCRT-II complex. Dev. Cell 14, 902-913
123. Bowers, K., Lottridge, J., Helliwell, S.B., Goldthwaite, L.M., Luzio, J.P. and Stevens, T.H. (2004) Protein-protein interactions of ESCRT complexes in the yeast Saccharomyces cerevisiae. Traffic 5, 194-210
124. von Schwedler, U.K., Stuchell, M., Muller, B., Ward, D.M., Chung, H.Y., Morita, E., Wang, H.E., Davis, T., He, G.P., Cimbora, D.M. et al. (2003) The protein network of HIV budding. Cell 114, 701-713
125. Alam, S.L., Sun, J., Payne, M., Welch, B.D., Blake, B.K., Davis, D.R., Meyer, H.H., Emr, S.D. and Sundquist, W.I. (2004) Ubiquitin interactions of NZF zinc fingers. EMBO J. 23, 1411-1421
126. Slagsvold, T., Aasland, R., Hirano, S., Bache, K.G., Raiborg, C., Trambaiolo, D., Wakatsuki, S. and Stenmark, H. (2005) Eap45 in mammalian ESCRT-II binds ubiquitin via a phosphoinositide-interacting GLUE domain. J. Biol. Chem. 280, 19600-19606
127. Hirano, S., Suzuki, N., Slagsvold, T., Kawasaki, M., Trambaiolo, D., Kato, R., Stenmark, H. and Wakatsuki, S. (2006) Structural basis of ubiquitin recognition by mammalian Eap45 GLUE domain. Nat. Struct. Mol. Biol. 13, 1031-1032
128. Alam, S.L., Langelier, C., Whitby, F.G., Koirala, S., Robinson, H., Hill, C.P. and Sundquist, W.I. (2006) Structural basis for ubiquitin recognition by the human ESCRT-II EAP45 GLUE domain. Nat. Struct. Mol. Biol. 13, 1029-1030
129. Im, Y.J., Wollert, T., Boura, E. and Hurley, J.H. (2009) Structure and function of the ESCRT-II-III interface in multivesicular body biogenesis. Dev. Cell 17, 234-243
130. Teis, D., Saksena, S., Judson, B.L. and Emr, S.D. (2010) ESCRT-II coordinates the assembly of ESCRT-III filaments for cargo sorting and multivesicular body vesicle formation. EMBO J. 29, 871-883
131. Saksena, S., Wahlman, J., Teis, D., Johnson, A.E. and Emr, S.D. (2009) Functional reconstitution of ESCRT-III assembly and disassembly. Cell 136, 97-109
132. Langelier, C., von Schwedler, U.K., Fisher, R.D., De Domenico, I., White, P.L., Hill, C.P., Kaplan, J., Ward, D. and Sundquist, W.I. (2006) Human ESCRT-II complex and its role in human immunodeficiency virus type 1 release. J. Virol. 80, 9465-9480
133. Yorikawa, C., Shibata, H., Waguri, S., Hatta, K., Horii, M., Katoh, K., Kobayashi, T., Uchiyama, Y. and Maki, M. (2005) Human CHMP6, a myristoylated ESCRT-III protein, interacts directly with an ESCRT-II component EAP20 and regulates endosomal cargo sorting. Biochem. J. 387, 17-26
134. Pineda-Molina, E., Belrhali, H., Piefer, A.J., Akula, I., Bates, P. and Weissenhorn, W. (2006) The crystal structure of the C-terminal domain of Vps28 reveals a conserved surface required for Vps20 recruitment. Traffic 7, 1007-1016
135. Doyotte, A., Mironov, A., McKenzie, E. and Woodman, P. (2008) The Bro1-related protein HD-PTP/PTPN23 is required for endosomal cargo sorting and multivesicular body morphogenesis. Proc. Natl. Acad. Sci. U.S.A. 105, 6308-6313
136. Ichioka, F., Takaya, E., Suzuki, H., Kajigaya, S., Buchman, V.L., Shibata, H. and Maki, M. (2007) HD-PTP and Alix share some membrane-traffic related proteins that interact with their Bro1 domains or proline-rich regions. Arch. Biochem. Biophys. 457, 142-149
137. Lloyd, T.E., Atkinson, R., Wu, M.N., Zhou, Y., Pennetta, G. and Bellen, H.J. (2002) Hrs regulates endosome membrane invagination and tyrosine kinase receptor signaling in Drosophila. Cell 108, 261-269
138. Vaccari, T. and Bilder, D. (2005) The Drosophila tumor suppressor vps25 prevents nonautonomous overproliferation by regulating notch trafficking. Dev. Cell 9, 687-698
139. Thompson, B.J., Mathieu, J., Sung, H.H., Loeser, E., Rorth, P. and Cohen, S.M. (2005) Tumor suppressor properties of the ESCRT-II complex component Vps25 in Drosophila. Dev. Cell 9, 711-720
140. Herz, H.M., Chen, Z., Scherr, H., Lackey, M., Bolduc, C. and Bergmann, A. (2006) vps25 mosaics display non-autonomous cell survival and overgrowth, and autonomous apoptosis. Development 133, 1871-1880
141. Bowers, K., Piper, S.C., Edeling, M.A., Gray, S.R., Owen, D.J., Lehner, P.J. and Luzio, J.P. (2006) Degradation of endocytosed epidermal growth factor and virally ubiquitinated major histocompatibility complex class I is independent of mammalian ESCRTII. J. Biol. Chem. 281, 5094-5105
142. Malerod, L., Stuffers, S., Brech, A. and Stenmark, H. (2007) Vps22/EAP30 in ESCRT-II mediates endosomal sorting of growth factor and chemokine receptors destined for lysosomal degradation. Traffic 8, 1617-1629
143. Irion, U. and St Johnston, D. (2007) bicoid RNA localization requires specific binding of an endosomal sorting complex. Nature 445, 554-558
144. Muziol, T., Pineda-Molina, E., Ravelli, R.B., Zamborlini, A., Usami, Y., Göttlinger, H. and Weissenhorn, W. (2006) Structural basis for budding by the ESCRT-III factor CHMP3. Dev. Cell 10, 821-830
145. Zamborlini, A., Usami, Y., Radoshitzky, S.R., Popova, E., Palu, G. and Göttlinger, H. (2006) Release of autoinhibition converts ESCRT-III components into potent inhibitors of HIV-1 budding. Proc. Natl. Acad. Sci. U.S.A. 103, 19140-19145
146. Shim, S., Kimpler, L.A. and Hanson, P.I. (2007) Structure/function analysis of four core ESCRT-III proteins reveals common regulatory role for extreme C-terminal domain. Traffic 8, 1068-1079
147. Lata, S., Roessle, M., Solomons, J., Jamin, M., Göttlinger, H.G., Svergun, D.I. and Weissenhorn, W. (2008) Structural basis for autoinhibition of ESCRT-III CHMP3. J. Mol. Biol. 378, 818-827
148. Whitley, P., Reaves, B.J., Hashimoto, M., Riley, A.M., Potter, B.V. and Holman, G.D. (2003) Identification of mammalian Vps24p as an effector of phosphatidylinositol 3,5-bisphosphate-dependent endosome compartmentalization. J. Biol. Chem. 278, 38786-38795
149. Babst, M., Wendland, B., Estepa, E.J. and Emr, S.D. (1998) The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function. EMBO J. 17, 2982-2993
150. Scott, A., Chung, H.Y., Gonciarz-Swiatek, M., Hill, G.C., Whitby, F.G., Gaspar, J., Holton, J.M., Viswanathan, R., Ghaffarian, S., Hill, C.P. and Sundquist, W.I. (2005) Structural and mechanistic studies of VPS4 proteins. EMBO J. 24, 3658-3669
151. Scott, A., Gaspar, J., Stuchell-Brereton, M.D., Alam, S.L., Skalicky, J.J. and Sundquist, W.I. (2005) Structure and ESCRT-III protein interactions of the MIT domain of human VPS4A. Proc. Natl. Acad. Sci. U.S.A. 102, 13813-13818
152. Stuchell-Brereton, M.D., Skalicky, J.J., Kieffer, C., Karren, M.A., Ghaffarian, S. and Sundquist, W.I. (2007) ESCRT-III recognition by VPS4 ATPases. Nature 449, 740-744
153. Yu, Z., Gonciarz, M.D., Sundquist, W.I., Hill, C.P. and Jensen, G.J. (2008) Cryo-EM structure of dodecameric Vps4p and its 2:1 complex with Vta1p. J. Mol. Biol. 377, 364-377
154. Azmi, I.F., Davies, B.A., Xiao, J., Babst, M., Xu, Z. and Katzmann, D.J. (2008) ESCRT-III family members stimulate Vps4 ATPase activity directly or via Vta1. Dev. Cell 14, 50-61
155. Azmi, I., Davies, B., Dimaano, C., Payne, J., Eckert, D., Babst, M. and Katzmann, D.J. (2006) Recycling of ESCRTs by the AAA-ATPase Vps4 is regulated by a conserved VSL region in Vta1. J. Cell Biol. 172, 705-717
156. Lottridge, J.M., Flannery, A.R., Vincelli, J.L. and Stevens, T.H. (2006) Vta1p and Vps46p regulate the membrane association and ATPase activity of Vps4p at the yeast multivesicular body. Proc. Natl. Acad. Sci. U.S.A. 103, 6202-6207
157. Xiao, J., Xia, H., Zhou, J., Azmi, I.F., Davies, B.A., Katzmann, D.J. and Xu, Z. (2008) Structural basis of Vta1 function in the multivesicular body sorting pathway. Dev. Cell 14, 37-49
158. Rue, S.M., Mattei, S., Saksena, S. and Emr, S.D. (2008) Novel Ist1-Did2 complex functions at a late step in multivesicular body sorting. Mol. Biol. Cell 19, 475-484
159. Dimaano, C., Jones, C.B., Hanono, A., Curtiss, M. and Babst, M. (2008) Ist1 regulates Vps4 localization and assembly. Mol. Biol. Cell 19, 465-474
160. Nickerson, D.P., West, M., Henry, R. and Odorizzi, G. Regulators of vps4 ATPase activity at endosomes differentially influence the size and rate of formation of intralumenal vesicles. Mol. Biol. Cell 21, 1023-1032
161. Shim, S., Merrill, S.A. and Hanson, P.I. (2008) Novel interactions of ESCRT-III with LIP5 and VPS4 and their implications for ESCRT-III disassembly. Mol. Biol. Cell 19, 2661-2672
162. Ward, D.M., Vaughn, M.B., Shiflett, S.L., White, P.L., Pollock, A.L., Hill, J., Schnegelberger, R., Sundquist, W.I. and Kaplan, J. (2005) The role of LIP5 and CHMP5 in multivesicular body formation and HIV-1 budding in mammalian cells. J. Biol. Chem. 280, 10548-10555
163. Teis, D., Saksena, S. and Emr, S.D. (2008) Ordered assembly of the ESCRT-III complex on endosomes is required to sequester cargo during MVB formation. Dev. Cell 15, 578-589
164. Teis, D., Saksena, S. and Emr, S.D. (2009) SnapShot: the ESCRT machinery. Cell 137, 182-182, e181
165. Hanson, P.I., Shim, S. and Merrill, S.A. (2009) Cell biology of the ESCRT machinery. Curr. Opin. Cell Biol. 21, 568-574
166. Hanson, P.I., Roth, R., Lin, Y. and Heuser, J.E. (2008) Plasma membrane deformation by circular arrays of ESCRT-III protein filaments. J. Cell Biol. 180, 389-402
167. Ghazi-Tabatabai, S., Saksena, S., Short, J.M., Pobbati, A.V., Veprintsev, D.B., Crowther, R.A., Emr, S.D., Egelman, E.H. and Williams, R.L. (2008) Structure and disassembly of filaments formed by the ESCRT-III subunit Vps24. Structure 16, 1345-1356
168. Lata, S., Schoehn, G., Jain, A., Pires, R., Piehler, J., Göttlinger, H.G. and Weissenhorn, W. (2008) Helical structures of ESCRT-III are disassembled by VPS4. Science 321, 1354-1357
169. Wollert, T., Wunder, C., Lippincott-Schwartz, J. and Hurley, J.H. (2009) Membrane scission by the ESCRT-III complex. Nature 458, 172-177
170. Wollert, T. and Hurley, J.H. (2010) Molecular mechanism of multivesicular body biogenesis by ESCRT complexes. Nature 464, 864-869
171. Sun, W., Vida, T.A., Sirisaengtaksin, N., Merrill, S.A., Hanson, P.I. and Bean, A.J. (2010) Cell-free reconstitution of multivesicular body formation and receptor sorting. Traffic 11, 867-876
172. Falguieres, T., Luyet, P.P., Bissig, C., Scott, C.C., Velluz, M.C. and Gruenberg, J. (2008) In vitro budding of intralumenal vesicles into late endosomes is regulated by Alix and Tsg101. Mol. Biol. Cell 19, 4942-4955
173. Nickerson, D.P., Russell, M.R. and Odorizzi, G. (2007) A concentric circle model of multivesicular body cargo sorting. EMBO Rep. 8, 644-650
174. Fabrikant, G., Lata, S., Riches, J.D., Briggs, J.A., Weissenhorn, W. and Kozlov, M.M. (2009) Computational model of membrane fission catalyzed by ESCRT-III. PLoS Comput. Biol. 5, e1000575
175. Stuffers, S., Sem Wegner, C., Stenmark, H. and Brech, A. (2009) Multivesicular endosome biogenesis in the absence of ESCRTs. Traffic 10, 925-937
176. Shim, J.H., Xiao, C., Hayden, M.S., Lee, K.Y., Trombetta, E.S., Pypaert, M., Nara, A., Yoshimori, T., Wilm, B., Erdjument-Bromage, H. et al. (2006) CHMP5 is essential for late endosome function and down-regulation of receptor signaling during mouse embryogenesis. J. Cell Biol. 172, 1045-1056
177. White, I.J., Bailey, L.M., Aghakhani, M.R., Moss, S.E. and Futter, C.E. (2006) EGF stimulates annexin 1-dependent inward vesiculation in a multivesicular endosome subpopulation. EMBO J. 25, 1-12
178. Morel, E., Parton, R.G. and Gruenberg, J. (2009) Annexin A2-dependent polymerization of actin mediates endosome biogenesis. Dev. Cell 16, 445-57
179. Theos, A.C., Truschel, S.T., Tenza, D., Hurbain, I., Harper, D.C., Berson, J.F., Thomas, P.C., Raposo, G. and Marks, M.S. (2006) A lumenal domain-dependent pathway for sorting to intralumenal vesicles of multivesicular endosomes involved in organelle morphogenesis. Dev. Cell 10, 343-54
180. Chen, B.J., Leser, G.P., Morita, E. and Lamb, R.A. (2007) Influenza virus hemagglutinin and neuraminidase, but not the matrix protein, are required for assembly and budding of plasmid-derived virus-like particles. J. Virol. 81, 7111-7123
181. Bruce, E.A., Medcalf, L., Crump, C.M., Noton, S.L., Stuart, A.D., Wise, H.M., Elton, D., Bowers, K. and Digard, P. (2009) Budding of filamentous and non-filamentous influenza A virus occurs via a VPS4 and VPS28-independent pathway. Virology 390, 268-278
182. Bruce, E.A., Digard, P. and Stuart, A.D. (2010) The Rab11 pathway is required for influenza A viral budding and filament formation. J. Virol. 84, 5848-5859
183. Krzyzaniak, M.A., Mach, M. and Britt, W.J. (2009) HCMV-encoded glycoprotein M (UL100) interacts with Rab11 effector protein FIP4. Traffic 10, 1439-1457
184. Utley, T.J., Ducharme, N.A., Varthakavi, V., Shepherd, B.E., Santangelo, P.J., Lindquist, M.E., Goldenring, J.R. and Crowe, Jr, J.E. (2008) Respiratory syncytial virus uses a Vps4-independent budding mechanism controlled by Rab11-FIP2. Proc. Natl. Acad. Sci. U.S.A. 105, 10209-10214
185. Rowe, R.K., Suszko, J.W. and Pekosz, A. (2008) Roles for the recycling endosome, Rab8, and Rab11 in hantavirus release from epithelial cells. Virology 382, 239-249
186. Odorizzi, G., Babst, M. and Emr, S.D. (1998) Fab1p PtdIns(3)P 5-kinase function essential for protein sorting in the multivesicular body. Cell 95, 847-858
187. Matsuo, H., Chevallier, J., Mayran, N., Le Blanc, I., Ferguson, C., Faure, J., Blanc, N.S., Matile, S., Dubochet, J., Sadoul, R. et al. (2004) Role of LBPA and Alix in multivesicular liposome formation and endosome organization. Science 303, 531-534
188. Trajkovic, K., Hsu, C., Chiantia, S., Rajendran, L., Wenzel, D., Wieland, F., Schwille, P., Brugger, B. and Simons, M. (2008) Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 319, 1244-1247 (Pubitemid 351323020)