ESCRTing proteins in the endocytic pathway

Trends in Biochemical Sciences

Volumn 32, Issue 12, 2007, Pages 561-573

  Saksena, Suraj ^a   Sun, Ji ^b   Chu, Tony ^b   Emr, Scott D ^a,b  

^a Department of Obstetrics Gynecology   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLATHRIN; PROTEIN ESCRT 1; PROTEIN ESCRT 2; PROTEIN ESCRT 3; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARABIDOPSIS; CARBOXY TERMINAL SEQUENCE; CELL BUDDING; COMPLEX FORMATION; DOWN REGULATION; DROSOPHILA; ENDOSOME; ENZYME ACTIVITY; EUKARYOTE; GENE MUTATION; HUMAN; MONKEY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN TRANSPORT; REGULATORY MECHANISM; RETROVIRUS; REVIEW; SIGNAL TRANSDUCTION; X RAY CRYSTALLOGRAPHY; YEAST;

ENDOCYTOSIS; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN SORTING SIGNALS; PROTEINS; UBIQUITIN;

EUKARYOTA;

EID: 36248991778     PISSN: 09680004     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tibs.2007.09.010     Document Type: Review

References (108)

1. Haigler H.T., et al. Direct visualization of the binding and internalization of a ferritin conjugate of epidermal growth factor in human carcinoma cells A-431. J. Cell Biol. 81 (1979) 382-395
2. Raymond C.K., et al. Morphological classification of the yeast vacuolar protein sorting mutants: evidence for a prevacuolar compartment in class E vps mutants. Mol. Biol. Cell 3 (1992) 1389-1402
3. Vida T.A., et al. Yeast vacuolar proenzymes are sorted in the late Golgi complex and transported to the vacuole via a prevacuolar endosome-like compartment. J. Cell Biol. 121 (1993) 1245-1256
4. Odorizzi G., et al. Fab1p PtdIns(3)P 5-kinase function essential for protein sorting in the multivesicular body. Cell 95 (1998) 847-858
5. Babst M. A protein's final ESCRT. Traffic 6 (2005) 2-9
6. Babst M., et al. Escrt-III: an endosome-associated heterooligomeric protein complex required for mvb sorting. Dev. Cell 3 (2002) 271-282
7. Babst M., et al. Endosome-associated complex, ESCRT-II, recruits transport machinery for protein sorting at the multivesicular body. Dev. Cell 3 (2002) 283-289
8. Katzmann D.J., et al. Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell 106 (2001) 145-155
9. Hurley J.H., and Emr S.D. The ESCRT complexes: structure and mechanism of a membrane-trafficking network. Annu. Rev. Biophys. Biomol. Struct. 35 (2006) 277-298
10. Katzmann D.J., et al. Receptor downregulation and multivesicular-body sorting. Nat. Rev. Mol. Cell Biol. 3 (2002) 893-905
11. Slagsvold T., et al. Endosomal and non-endosomal functions of ESCRT proteins. Trends Cell Biol. 16 (2006) 317-326
12. Reggiori F., and Pelham H.R. Sorting of proteins into multivesicular bodies: ubiquitin-dependent and -independent targeting. EMBO J. 20 (2001) 5176-5186
13. Urbanowski J.L., and Piper R.C. Ubiquitin sorts proteins into the intralumenal degradative compartment of the late-endosome/vacuole. Traffic 2 (2001) 622-630
14. Katzmann D.J., et al. Multivesicular body sorting: ubiquitin ligase Rsp5 is required for the modification and sorting of carboxypeptidase S. Mol. Biol. Cell 15 (2004) 468-480
15. Futter C.E., et al. Multivesicular endosomes containing internalized EGF-EGF receptor complexes mature and then fuse directly with lysosomes. J. Cell Biol. 132 (1996) 1011-1023
16. Kleijmeer M., et al. Reorganization of multivesicular bodies regulates MHC class II antigen presentation by dendritic cells. J. Cell Biol. 155 (2001) 53-63
17. Garrus J.E., et al. Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 107 (2001) 55-65
18. Irion U., and St Johnston D. bicoid RNA localization requires specific binding of an endosomal sorting complex. Nature 445 (2007) 554-558
19. Carlton J.G., and Martin-Serrano J. Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery. Science 316 (2007) 1908-1912
20. Williams R.L., and Urbe S. The emerging shape of the ESCRT machinery. Nat. Rev. Mol. Cell Biol. 8 (2007) 355-368
21. Misra S., and Hurley J.H. Crystal structure of a phosphatidylinositol 3-phosphate-specific membrane-targeting motif, the FYVE domain of Vps27p. Cell 97 (1999) 657-666
22. Stahelin R.V., et al. Phosphatidylinositol 3-phosphate induces the membrane penetration of the FYVE domains of Vps27p and Hrs. J. Biol. Chem. 277 (2002) 26379-26388
23. Stack J.H., et al. Vesicle-mediated protein transport: regulatory interactions between the Vps15 protein kinase and the Vps34 PtdIns 3-kinase essential for protein sorting to the vacuole in yeast. J. Cell Biol. 129 (1995) 321-334
24. Schu P.V., et al. Phosphatidylinositol 3-kinase encoded by yeast VPS34 gene essential for protein sorting. Science 260 (1993) 88-91
25. Prag G., et al. The Vps27/Hse1 complex is a GAT domain-based scaffold for ubiquitin-dependent sorting. Dev. Cell 12 (2007) 973-986
26. Ren J., et al. Hse1, a component of the yeast Hrs-STAM ubiquitin-sorting complex, associates with ubiquitin peptidases and a ligase to control sorting efficiency into multivesicular bodies. Mol. Biol. Cell 18 (2007) 324-335
27. Katzmann D.J., et al. Vps27 recruits ESCRT machinery to endosomes during MVB sorting. J. Cell Biol. 162 (2003) 413-423
28. Bache K.G., et al. Hrs regulates multivesicular body formation via ESCRT recruitment to endosomes. J. Cell Biol. 162 (2003) 435-442
29. Bilodeau P.S., et al. Vps27-Hse1 and ESCRT-I complexes cooperate to increase efficiency of sorting ubiquitinated proteins at the endosome. J. Cell Biol. 163 (2003) 237-243
30. Pornillos O., et al. HIV Gag mimics the Tsg101-recruiting activity of the human Hrs protein. J. Cell Biol. 162 (2003) 425-434
31. ter Haar E., et al. Peptide-in-groove interactions link target proteins to the beta-propeller of clathrin. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 1096-1100
32. Raiborg C., et al. Hrs recruits clathrin to early endosomes. EMBO J. 20 (2001) 5008-5021
33. Sachse M., et al. ATPase-deficient hVPS4 impairs formation of internal endosomal vesicles and stabilizes bilayered clathrin coats on endosomal vacuoles. J. Cell Sci. 117 (2004) 1699-1708
34. Teo H., et al. Structural insights into endosomal sorting complex required for transport (ESCRT-I) recognition of ubiquitinated proteins. J. Biol. Chem. 279 (2004) 28689-28696
35. Amit I., et al. Tal, a Tsg101-specific E3 ubiquitin ligase, regulates receptor endocytosis and retrovirus budding. Genes Dev. 18 (2004) 1737-1752
36. Strack B., et al. AIP1/ALIX is a binding partner for HIV-1 p6 and EIAV p9 functioning in virus budding. Cell 114 (2003) 689-699
37. von Schwedler U.K., et al. The protein network of HIV budding. Cell 114 (2003) 701-713
38. Pornillos O., et al. Structure of the Tsg101 UEV domain in complex with the PTAP motif of the HIV-1 p6 protein. Nat. Struct. Biol. 9 (2002) 812-817
39. Kostelansky M.S., et al. Molecular architecture and functional model of the complete yeast ESCRT-I heterotetramer. Cell 129 (2007) 485-498
40. Chu T., et al. New component of ESCRT-I regulates endosomal sorting complex assembly. J. Cell Biol. 175 (2006) 815-823
41. Curtiss M., et al. Efficient cargo sorting by ESCRT-I and the subsequent release of ESCRT-I from multivesicular bodies requires the subunit Mvb12. Mol. Biol. Cell 18 (2007) 636-645
42. Bouamr F., et al. The C-terminal portion of the Hrs protein interacts with Tsg101 and interferes with human immunodeficiency virus type 1 Gag particle production. J. Virol. 81 (2007) 2909-2922
43. Alam S.L., et al. Ubiquitin interactions of NZF zinc fingers. EMBO J. 23 (2004) 1411-1421
44. Slagsvold T., et al. Eap45 in mammalian ESCRT-II binds ubiquitin via a phosphoinositide-interacting GLUE domain. J. Biol. Chem. 280 (2005) 19600-19606
45. Hirano S., et al. Structural basis of ubiquitin recognition by mammalian Eap45 GLUE domain. Nat. Struct. Mol. Biol. 13 (2006) 1031-1032
46. Gill D.J., et al. Structural insight into the ESCRT-I/-II link and its role in MVB trafficking. EMBO J. 26 (2007) 600-612
47. Teo H., et al. ESCRT-II, an endosome-associated complex required for protein sorting: crystal structure and interactions with ESCRT-III and membranes. Dev. Cell 7 (2004) 559-569
48. Teo H., et al. ESCRT-I core and ESCRT-II GLUE domain structures reveal role for GLUE in linking to ESCRT-I and membranes. Cell 125 (2006) 99-111
49. Gill D.J., et al. Structural studies of phosphoinositide 3-kinase-dependent traffic to multivesicular bodies. Biochem. Soc. Symp. 2007 74 (2007) 47-57
50. Hierro A., et al. Structure of the ESCRT-II endosomal trafficking complex. Nature 431 (2004) 221-225
51. Yorikawa C., et al. Human CHMP6, a myristoylated ESCRT-III protein, interacts directly with an ESCRT-II component EAP20 and regulates endosomal cargo sorting. Biochem. J. 387 (2005) 17-26
52. Tsang H.T., et al. A systematic analysis of human CHMP protein interactions: additional MIT domain-containing proteins bind to multiple components of the human ESCRT III complex. Genomics 88 (2006) 333-346
53. Martin-Serrano J., et al. Divergent retroviral late-budding domains recruit vacuolar protein sorting factors by using alternative adaptor proteins. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 12414-12419
54. Muziol T., et al. Structural basis for budding by the ESCRT-III factor CHMP3. Dev. Cell 10 (2006) 821-830
55. Whitley P., et al. Identification of mammalian Vps24p as an effector of phosphatidylinositol 3,5-bisphosphate-dependent endosome compartmentalization. J. Biol. Chem. 278 (2003) 38786-38795
56. Shim S., et al. Structure/function analysis of four core ESCRT-III proteins reveals common regulatory role for extreme C-terminal domain. Traffic 8 (2007) 1068-1079
57. Nickerson D.P., et al. Did2 coordinates Vps4-mediated dissociation of ESCRT-III from endosomes. J. Cell Biol. 175 (2006) 715-720
58. Obita T., et al. Structural basis for selective recognition of ESCRT-III by the AAA-ATPase Vps4. Nature 449 (2007) 735-739
59. Amerik A.Y., and Hochstrasser M. Mechanism and function of deubiquitinating enzymes. Biochim. Biophys. Acta 1695 (2004) 189-207
60. Kato M., et al. 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 (2000) 37481-37487
61. McCullough J., et al. Activation of the endosome-associated ubiquitin isopeptidase AMSH by STAM, a component of the multivesicular body-sorting machinery. Curr. Biol. 16 (2006) 160-165
62. Tanaka N., et al. Possible involvement of a novel STAM-associated molecule "AMSH" in intracellular signal transduction mediated by cytokines. J. Biol. Chem. 274 (1999) 19129-19135
63. Luhtala N., and Odorizzi G. Bro1 coordinates deubiquitination in the multivesicular body pathway by recruiting Doa4 to endosomes. J. Cell Biol. 166 (2004) 717-729
64. Richter C., et al. Dual mechanisms specify Doa4-mediated deubiquitination at multivesicular bodies. EMBO J. 26 (2007) 2454-2464
65. Tsuda M., et al. POSH, a scaffold protein for JNK signaling, binds to ALG-2 and ALIX in Drosophila. FEBS Lett. 580 (2006) 3296-3300
66. van der Goot F.G., and Gruenberg J. Intra-endosomal membrane traffic. Trends Cell Biol. 16 (2006) 514-521
67. Chen C., et al. Functions of early (AP-2) and late (AIP1/ALIX) endocytic proteins in equine infectious anemia virus budding. J. Biol. Chem. 280 (2005) 40474-40480
68. Vincent O., et al. YPXL/I is a protein interaction motif recognized by aspergillus PalA and its human homologue, AIP1/Alix. Mol. Cell. Biol. 23 (2003) 1647-1655
69. Fisher R.D., et al. Structural and biochemical studies of ALIX/AIP1 and its role in retrovirus budding. Cell 128 (2007) 841-852
70. Erzberger J.P., and Berger J.M. Evolutionary relationships and structural mechanisms of AAA+ proteins. Annu. Rev. Biophys. Biomol. Struct. 35 (2006) 93-114
71. Hanson P.I., and Whiteheart S.W. AAA+ proteins: have engine, will work. Nat. Rev. Mol. Cell Biol. 6 (2005) 519-529
72. Azmi I., et al. Recycling of ESCRTs by the AAA-ATPase Vps4 is regulated by a conserved VSL region in Vta1. J. Cell Biol. 172 (2006) 705-717
73. Bishop N., and Woodman P. TSG101/mammalian VPS23 and mammalian VPS28 interact directly and are recruited to VPS4-induced endosomes. J. Biol. Chem. 276 (2001) 11735-11742
74. Fujita H., et al. A dominant negative form of the AAA ATPase SKD1/VPS4 impairs membrane trafficking out of endosomal/lysosomal compartments: class E vps phenotype in mammalian cells. J. Cell Sci. 116 (2003) 401-414
75. Scott A., et al. Structural and mechanistic studies of VPS4 proteins. EMBO J. 24 (2005) 3658-3669
76. Yeo S.C., et al. Vps20p and Vta1p interact with Vps4p and function in multivesicular body sorting and endosomal transport in Saccharomyces cerevisiae. J. Cell Sci. 116 (2003) 3957-3970
77. Ward D.M., et al. The role of LIP5 and CHMP5 in multivesicular body formation and HIV-1 budding in mammalian cells. J. Biol. Chem. 280 (2005) 10548-10555
78. Schafer B., et al. Multiple G-protein-coupled receptor signals converge on the epidermal growth factor receptor to promote migration and invasion. Oncogene 23 (2004) 991-999
79. Babst M., et al. Mammalian tumor susceptibility gene 101 (TSG101) and the yeast homologue, Vps23p, both function in late endosomal trafficking. Traffic 1 (2000) 248-258
80. Bache K.G., et al. STAM and Hrs are subunits of a multivalent ubiquitin-binding complex on early endosomes. J. Biol. Chem. 278 (2003) 12513-12521
81. Kanazawa C., et al. Effects of deficiencies of STAMs and Hrs, mammalian class E Vps proteins, on receptor downregulation. Biochem. Biophys. Res. Commun. 309 (2003) 848-856
82. Carstens M.J., et al. Cell cycle arrest and cell death are controlled by p53-dependent and p53-independent mechanisms in Tsg101-deficient cells. J. Biol. Chem. 279 (2004) 35984-35994
83. Krempler A., et al. Targeted deletion of the Tsg101 gene results in cell cycle arrest at G1/S and p53-independent cell death. J. Biol. Chem. 277 (2002) 43216-43223
84. Li L., et al. A TSG101/MDM2 regulatory loop modulates MDM2 degradation and MDM2/p53 feedback control. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 1619-1624
85. Oh H., et al. Negative regulation of cell growth and differentiation by TSG101 through association with p21(Cip1/WAF1). Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 5430-5435
86. Ruland J., et al. p53 accumulation, defective cell proliferation, and early embryonic lethality in mice lacking tsg101. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 1859-1864
87. Li L., and Cohen S.N. Tsg101: a novel tumor susceptibility gene isolated by controlled homozygous functional knockout of allelic loci in mammalian cells. Cell 85 (1996) 319-329
88. Li L., et al. The TSG101 tumor susceptibility gene is located in chromosome 11 band p15 and is mutated in human breast cancer. Cell 88 (1997) 143-154
89. Lin P.M., et al. Aberrant TSG101 transcripts in acute myeloid leukaemia. Br. J. Haematol. 102 (1998) 753-758
90. Sun Z., et al. Frequent abnormalities of TSG101 transcripts in human prostate cancer. Oncogene 15 (1997) 3121-3125
91. Bache K.G., et al. The growth-regulatory protein HCRP1/hVps37A is a subunit of mammalian ESCRT-I and mediates receptor down-regulation. Mol. Biol. Cell 15 (2004) 4337-4346
92. Jekely G., and Rorth P. Hrs mediates downregulation of multiple signalling receptors in Drosophila. EMBO Rep. 4 (2003) 1163-1168
93. Lloyd T.E., et al. Hrs regulates endosome membrane invagination and tyrosine kinase receptor signaling in Drosophila. Cell 108 (2002) 261-269
94. Moberg K.H., et al. Mutations in erupted, the Drosophila ortholog of mammalian tumor susceptibility gene 101, elicit non-cell-autonomous overgrowth. Dev. Cell 9 (2005) 699-710
95. Thompson B.J., et al. Tumor suppressor properties of the ESCRT-II complex component Vps25 in Drosophila. Dev. Cell 9 (2005) 711-720
96. Vaccari T., and Bilder D. The Drosophila tumor suppressor vps25 prevents nonautonomous overproliferation by regulating notch trafficking. Dev. Cell 9 (2005) 687-698
97. Chao J.L., et al. Localized Notch signal acts through eyg and upd to promote global growth in Drosophila eye. Development 131 (2004) 3839-3847
98. Reynolds-Kenneally J., and Mlodzik M. Notch signaling controls proliferation through cell-autonomous and non-autonomous mechanisms in the Drosophila eye. Dev. Biol. 285 (2005) 38-48
99. Tsai Y.C., and Sun Y.H. Long-range effect of upd, a ligand for Jak/STAT pathway, on cell cycle in Drosophila eye development. Genesis 39 (2004) 141-153
100. Sevrioukov E.A., et al. A mutation in dVps28 reveals a link between a subunit of the endosomal sorting complex required for transport-I complex and the actin cytoskeleton in Drosophila. Mol. Biol. Cell 16 (2005) 2301-2312
101. Cabezas A., et al. Alix regulates cortical actin and the spatial distribution of endosomes. J. Cell Sci. 118 (2005) 2625-2635
102. Schmidt M.H., et al. Alix/AIP1 antagonizes epidermal growth factor receptor downregulation by the Cbl-SETA/CIN85 complex. Mol. Cell. Biol. 24 (2004) 8981-8993
103. Sweeney N.T., et al. The coiled-coil protein shrub controls neuronal morphogenesis in Drosophila. Curr. Biol. 16 (2006) 1006-1011
104. Reid E., et al. The hereditary spastic paraplegia protein spastin interacts with the ESCRT-III complex-associated endosomal protein CHMP1B. Hum. Mol. Genet. 14 (2005) 19-38
105. Skibinski G., et al. Mutations in the endosomal ESCRTIII-complex subunit CHMP2B in frontotemporal dementia. Nat. Genet. 37 (2005) 806-808
106. Freed E.O. Viral late domains. J. Virol. 76 (2002) 4679-4687
107. Lee J.A., et al. ESCRT-III dysfunction causes autophagosome accumulation and neurodegeneration. Curr. Biol. 17 (2007) 1651-1567
108. Spitzer C., et al. The Arabidopsis elch mutant reveals functions of an ESCRT component in cytokinesis. Development 133 (2006) 4679-4689