ESCRT-I Core and ESCRT-II GLUE Domain Structures Reveal Role for GLUE in Linking to ESCRT-I and Membranes

Cell

Volumn 125, Issue 1, 2006, Pages 99-111

  Teo, Hsiangling ^a   Gill, David J ^a   Sun, Ji ^c   Perisic, Olga ^a   Veprintsev, Dmitry B ^b   Vallis, Yvonne ^a   Emr, Scott D ^c   Williams, Roger L ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b MEDICAL RESEARCH COUNCIL   (United Kingdom)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN SUBUNIT; PROTEIN VPS23; PROTEIN VPS28; PROTEIN VPS36; TUMOR SUSCEPTIBILITY GENE 101 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; CRYSTAL STRUCTURE; ENDOSOME; MEMBRANE BINDING; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

EID: 33645981584     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2006.01.047     Document Type: Article

References (65)

1. 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. Ubiquitin interactions of NZF zinc fingers. EMBO J. 23 (2004) 1411-1421
2. Amit I., Yakir L., Katz M., Zwang Y., Marmor M.D., Citri A., Shtiegman K., Alroy I., Tuvia S., Reiss Y., et al. Tal, a Tsg101-specific E3 ubiquitin ligase, regulates receptor endocytosis and retrovirus budding. Genes Dev. 18 (2004) 1737-1752
3. Babst M., Wendland B., Estepa E.J., and Emr S.D. The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function. EMBO J. 17 (1998) 2982-2993
4. Babst M., Odorizzi G., Estepa E.J., and Emr S.D. Mammalian tumor susceptibility gene 101 (TSG101) and the yeast homologue, Vps23p, both function in late endosomal trafficking. Traffic 1 (2000) 248-258
5. Babst M., Katzmann D.J., Estepa-Sabal E.J., Meerloo T., and Emr S.D. ESCRT-III: an endosome-associated heterooligomeric protein complex required for MVB sorting. Dev. Cell 3 (2002) 271-282
6. Babst M., Katzmann D.J., Snyder W.B., Wendland B., and Emr S.D. Endosome-associated complex, ESCRT-II, recruits transport machinery for protein sorting at the multivesicular body. Dev. Cell 3 (2002) 283-289
7. Bache K.G., Brech A., Mehlum A., and Stenmark H. Hrs regulates multivesicular body formation via ESCRT recruitment to endosomes. J. Cell Biol. 162 (2003) 435-442
8. Bache K.G., Raiborg C., Mehlum A., and Stenmark H. STAM and Hrs are subunits of a multivalent ubiquitin-binding complex on early endosomes. J. Biol. Chem. 278 (2003) 12513-12521
9. Bache K.G., Slagsvold T., Cabezas A., Rosendal K.R., Raiborg C., and Stenmark H. 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
10. Bilodeau P.S., Winistorfer S.C., Kearney W.R., Robertson A.D., and Piper R.C. Vps27-Hse1 and ESCRT-I complexes cooperate to increase efficiency of sorting ubiquitinated proteins at the endosome. J. Cell Biol. 163 (2003) 237-243
11. 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
12. Bowers K., and Stevens T.H. Protein transport from the late Golgi to the vacuole in the yeast Saccharomyces cerevisiae. Biochim. Biophys. Acta 1744 (2005) 438-454
13. Bowers K., Lottridge J., Helliwell S.B., Goldthwaite L.M., Luzio J.P., and Stevens T.H. Protein-protein interactions of ESCRT complexes in the yeast Saccharomyces cerevisiae. Traffic 5 (2004) 194-210
14. Demirov D.G., and Freed E.O. Retrovirus budding. Virus Res. 106 (2004) 87-102
15. Di Lello P., Nguyen B.D., Jones T.N., Potempa K., Kobor M.S., Legault P., and Omichinski J.G. NMR structure of the amino-terminal domain from the Tfb1 subunit of TFIIH and characterization of its phosphoinositide and VP16 binding sites. Biochemistry 44 (2005) 7678-7686
16. Doyotte A., Russell M.R., Hopkins C.R., and Woodman P.G. Depletion of TSG101 forms a mammalian "Class E" compartment: a multicisternal early endosome with multiple sorting defects. J. Cell Sci. 118 (2005) 3003-3017
17. Eastman S.W., Martin-Serrano J., Chung W., Zang T., and Bieniasz P.D. Identification of human VPS37C, a component of endosomal sorting complex required for transport-I important for viral budding. J. Biol. Chem. 280 (2005) 628-636
18. Feng G.H., Lih C.J., and Cohen S.N. TSG101 protein steady-state level is regulated posttranslationally by an evolutionarily conserved COOH-terminal sequence. Cancer Res. 60 (2000) 1736-1741
19. Ferguson K.M., Kavran J.M., Sankaran V.G., Fournier E., Isakoff S.J., Skolnik E.Y., and Lemmon M.A. Structural basis for discrimination of 3-phosphoinositides by pleckstrin homology domains. Mol. Cell 6 (2000) 373-384
20. Fernandez-Borja M., Wubbolts R., Calafat J., Janssen H., Divecha N., Dusseljee S., and Neefjes J. Multivesicular body morphogenesis requires phosphatidyl-inositol 3-kinase activity. Curr. Biol. 9 (1999) 55-58
21. Futter C.E., Collinson L.M., Backer J.M., and Hopkins C.R. Human VPS34 is required for internal vesicle formation within multivesicular endosomes. J. Cell Biol. 155 (2001) 1251-1264
22. Gillooly D.J., Morrow I.C., Lindsay M., Gould R., Bryant N.J., Gaullier J.M., Parton R.G., and Stenmark H. Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. EMBO J. 19 (2000) 4577-4588
23. Goila-Gaur R., Demirov D.G., Orenstein J.M., Ono A., and Freed E.O. Defects in human immunodeficiency virus budding and endosomal sorting induced by TSG101 overexpression. J. Virol. 77 (2003) 6507-6519
24. Hicke L., and Dunn R. Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu. Rev. Cell Dev. Biol. 19 (2003) 141-172
25. Hierro A., Sun J., Rusnak A.S., Kim J., Prag G., Emr S.D., and Hurley J.H. Structure of the ESCRT-II endosomal trafficking complex. Nature 431 (2004) 221-225
26. 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
27. Hyvonen M., Macias M.J., Nilges M., Oschkinat H., Saraste M., and Wilmanns M. Structure of the binding site for inositol phosphates in a PH domain. EMBO J. 14 (1995) 4676-4685
28. Johnson M.C., Spidel J.L., Ako-Adjei D., Wills J.W., and Vogt V.M. The C-terminal half of TSG101 blocks Rous sarcoma virus budding and sequesters Gag into unique nonendosomal structures. J. Virol. 79 (2005) 3775-3786
29. Katoh K., Shibata H., Suzuki H., Nara A., Ishidoh K., Kominami E., Yoshimori T., and Maki M. The ALG-2-interacting protein Alix associates with CHMP4b, a human homologue of yeast Snf7 that is involved in multivesicular body sorting. J. Biol. Chem. 278 (2003) 39104-39113
30. Katzmann D.J., Babst M., and Emr S.D. 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
31. Katzmann D.J., Odorizzi G., and Emr S.D. Receptor downregulation and multivesicular-body sorting. Nat. Rev. Mol. Cell Biol. 3 (2002) 893-905
32. Katzmann D.J., Stefan C.J., Babst M., and Emr S.D. Vps27 recruits ESCRT machinery to endosomes during MVB sorting. J. Cell Biol. 162 (2003) 413-423
33. Kim J., Sitaraman S., Hierro A., Beach B.M., Odorizzi G., and Hurley J.H. Structural basis for endosomal targeting by the Bro1 domain. Dev. Cell 8 (2005) 937-947
34. Lemmon M.A. Pleckstrin homology domains: two halves make a hole?. Cell 120 (2005) 574-576
35. Lietzke S.E., Bose S., Cronin T., Klarlund J., Chawla A., Czech M.P., and Lambright D.G. Structural basis of 3-phosphoinositide recognition by pleckstrin homology domains. Mol. Cell 6 (2000) 385-394
36. Lin Y., Kimpler L.A., Naismith T.V., Lauer J.M., and Hanson P.I. Interaction of the mammalian endosomal sorting complex required for transport (ESCRT) III protein hSnf7-1 with itself, membranes, and the AAA+ ATPase SKD1. J. Biol. Chem. 280 (2005) 12799-12809
37. 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
38. Martin-Serrano J., Yaravoy A., Perez-Caballero D., and Bieniasz P.D. Divergent retroviral late-budding domains recruit vacuolar protein sorting factors by using alternative adaptor proteins. Proc. Natl. Acad. Sci. USA 100 (2003) 12414-12419
39. Martin-Serrano J., Zang T., and Bieniasz P.D. Role of ESCRT-I in retroviral budding. J. Virol. 77 (2003) 4794-4804
40. Meyer H.H., Wang Y., and Warren G. Direct binding of ubiquitin conjugates by the mammalian p97 adaptor complexes, p47 and Ufd1-Npl4. EMBO J. 21 (2002) 5645-5652
41. Morita E., and Sundquist W.I. Retrovirus budding. Annu. Rev. Cell Dev. Biol. 20 (2004) 395-425
42. Odorizzi G., Babst M., and Emr S.D. Fab1p PtdIns(3)P 5-kinase function essential for protein sorting in the multivesicular body. Cell 95 (1998) 847-858
43. Peck J.W., Bowden E.T., and Burbelo P.D. Structure and function of human Vps20 and Snf7 proteins. Biochem. J. 377 (2004) 693-700
44. 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. HIV Gag mimics the Tsg101-recruiting activity of the human Hrs protein. J. Cell Biol. 162 (2003) 425-434
45. Puertollano R. Interactions of TOM1L1 with the multivesicular body sorting machinery. J. Biol. Chem. 280 (2005) 9258-9264
46. Raiborg C., Rusten T.E., and Stenmark H. Protein sorting into multivesicular endosomes. Curr. Opin. Cell Biol. 15 (2003) 446-455
47. Raymond C.K., Howald-Stevenson I., Vater C.A., and Stevens T.H. 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
48. Rink J., Ghigo E., Kalaidzidis Y., and Zerial M. Rab conversion as a mechanism of progression from early to late endosomes. Cell 122 (2005) 735-749
49. Schu P.V., Takegawa K., Fry M.J., Stack J.H., Waterfield M.D., and Emr S.D. Phosphatidylinositol 3-kinase encoded by yeast VPS34 gene essential for protein sorting. Science 260 (1993) 88-91
50. 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. Structural and mechanistic studies of VPS4 proteins. EMBO J. 24 (2005) 3658-3669
51. Shirk A.J., Anderson S.K., Hashemi S.H., Chance P.F., and Bennett C.L. SIMPLE interacts with NEDD4 and TSG101: Evidence for a role in lysosomal sorting and implications for Charcot-Marie-Tooth disease. J. Neurosci. Res. 82 (2005) 43-50
52. Slagsvold T., Aasland R., Hirano S., Bache K.G., Raiborg C., Trambaiolo D., Wakatsuki S., and Stenmark H. Eap45 in mammalian ESCRT-II binds ubiquitin via a phosphoinositide-interacting GLUE domain. J. Biol. Chem. 280 (2005) 19600-19606
53. Strack B., Calistri A., Craig S., Popova E., and Gottlinger H.G. AIP1/ALIX is a binding partner for HIV-1 p6 and EIAV p9 functioning in virus budding. Cell 114 (2003) 689-699
54. Stuchell M.D., Garrus J.E., Muller B., Stray K.M., Ghaffarian S., McKinnon R., Krausslich H.-G., Morham S.G., and Sundquist W.I. The human endosomal sorting complex required for transport (ESCRT-I) and its role in HIV-1 budding. J. Biol. Chem. 279 (2004) 36059-36071
55. Sundquist W.I., Schubert H.L., Kelly B.N., Hill G.C., Holton J.M., and Hill C.P. Ubiquitin recognition by the human TSG101 protein. Mol. Cell 13 (2004) 783-789
56. Tan S. A modular polycistronic expression system for overexpressing protein complexes in Escherichia coli. Protein Expr. Purif. 21 (2001) 224-234
57. Teo H., Perisic O., Gonzalez B., and Williams R.L. 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
58. Teo H., Veprintsev D.B., and Williams R.L. Structural insights into endosomal sorting complex required for transport (ESCRT-I) recognition of ubiquitinated proteins. J. Biol. Chem. 279 (2004) 28689-28696
59. Thompson B.J., Mathieu J., Sung H.H., Loeser E., Rorth P., and Cohen S.M. Tumor suppressor properties of the ESCRT-II complex component Vps25 in Drosophila. Dev. Cell 9 (2005) 711-720
60. Vaccari T., and Bilder D. The Drosophila tumor suppressor vps25 prevents nonautonomous overproliferation by regulating notch trafficking. Dev. Cell 9 (2005) 687-698
61. 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. The protein network of HIV budding. Cell 114 (2003) 701-713
62. Whitley P., Reaves B.J., Hashimoto M., Riley A.M., Potter B.V.L., and Holman G.D. Identification of mammalian Vps24p as an effector of phosphatidylinositol 3,5-bisphosphate-dependent endosome compartmentalization. J. Biol. Chem. 278 (2003) 38786-38795
63. Yorikawa C., Shibata H., Waguri S., Hatta K., Horii M., Katoh K., Kobayashi T., Uchiyama Y., and Maki M. 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
64. Yu J.W., Mendrola J.M., Audhya A., Singh S., Keleti D., DeWald D.B., Murray D., Emr S.D., and Lemmon M.A. Genome-wide analysis of membrane targeting by S. cerevisiae pleckstrin homology domains. Mol. Cell 13 (2004) 677-688
65. Zhou H., and Zhou Y. Fold recognition by combining sequence profiles derived from evolution and from depth-dependent structural alignment of fragments. Proteins 58 (2005) 321-328