Structural and Functional Organization of the ESCRT-I Trafficking Complex

Cell

Volumn 125, Issue 1, 2006, Pages 113-126

  Kostelansky, Michael S ^a   Sun, Ji ^b   Lee, Sangho ^a   Kim, Jaewon ^a   Ghirlando, Rodolfo ^a   Hierro, Aitor ^a   Emr, Scott D ^b   Hurley, James H ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN; PROTEIN VPS23; PROTEIN VPS28; PROTEIN VPS37; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

EID: 33646116786     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2006.01.049     Document Type: Article

References (60)

1. Alam S.L., Sun J., Payne M., Welch B.D., Black 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., 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
4. 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
5. 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
6. 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
7. 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
8. 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
9. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., Jiang J.S., Kuszewski J., Nilges M., Pannu N.S., et al. Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54 (1998) 905-921
10. CCP4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. A 50 (1994) 760-763
11. Collins B.M., McCoy A.J., Kent H.M., Evans P.R., and Owen D.J. Molecular architecture and functional model of the endocytic AP2 complex. Cell 109 (2002) 523-535
12. Conibear E. An ESCRT into the endosome. Mol. Cell 10 (2002) 215-216
13. Demirov D.G., Ono A., Orenstein J.M., and Freed E.O. Overexpression of the N-terminal domain of TSG101 inhibits HIV-1 budding by blocking late domain function. Proc. Natl. Acad. Sci. USA 99 (2002) 955-960
14. 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
15. 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
16. Freed E.O. The HIV-TSG101 interface: recent advances in a budding field. Trends Microbiol. 11 (2003) 56-59
17. 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. Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 107 (2001) 55-65
18. 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
19. Gonzalez A., Pedelacq J.D., Sola M., Gomis-Ruth F.X., Coll M., Samama J.P., and Benini S. Two-wavelength MAD phasing: in search of the optimal choice of wavelengths. Acta Crystallogr. D Biol. Crystallogr. 55 (1999) 1449-1458
20. Gorden P., Carpentier J.L., Cohen S., and Orci L. Epidermal growth factor: morphological demonstration of binding, internalization, and lysosomal association in human fibroblasts. Proc. Natl. Acad. Sci. USA 75 (1978) 5025-5029
21. Gruenberg J., and Stenmark H. The biogenesis of multivesicular endosomes. Nat. Rev. Mol. Cell Biol. 5 (2004) 317-323
22. Haglund K., Di Fiore P.P., and Dikic I. Distinct monoubiquitin signals in receptor endocytosis. Trends Biochem. Sci. 28 (2003) 598-603
23. Haigler H.T., McKanna J.A., and Cohen S. 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
24. Heldwein E.E., Macia E., Jing W., Yin H.L., Kirchhausen T., and Harrison S.C. Crystal structure of the clathrin adaptor protein 1 core. Proc. Natl. Acad. Sci. USA 101 (2004) 14108-14113
25. Hershko A., Ciechanover A., and Varshavsky A. The ubiquitin system. Nat. Med. 6 (2000) 1073-1081
26. Hicke L. Protein regulation by monoubiquitin. Nat. Rev. Mol. Cell Biol. 2 (2001) 195-201
27. 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
28. 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
29. Hierro A., Kim J., and Hurley J.H. Polycistronic expression and purification of the ESCRT-II endosomal trafficking complex. Methods Enzymol. 403 (2005) 322-332
30. Hochstrasser M. Evolution and function of ubiquitin-like protein-conjugation systems. Nat. Cell Biol. 2 (2000) E153-E157
31. Hurley J.H., and Emr S.D. The ESCRT complexes: structure and mechanism of a membrane-trafficking network. Annu. Rev. Biophys. Biomol. Struct. (2006) 10.1146/annurev.biophys.35.040405.102126 in press. Published online February 7, 2006
32. Jones T.A., Zou J.Y., Cowan S.W., and Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47 (1991) 110-119
33. 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
34. Katzmann D.J., Odorizzi G., and Emr S.D. Receptor downregulation and multivesicular-body sorting. Nat. Rev. Mol. Cell Biol. 3 (2002) 893-905
35. 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
36. Martin-Serrano J., Zang T., and Bieniasz P.D. HIV-I and Ebola virus encode small peptide motifs that recruit Tsg101 to sites of particle assembly to facilitate egress. Nat. Med. 7 (2001) 1313-1319
37. Martin-Serrano J., Zang T., and Bieniasz P.D. Role of ESCRT-I in retroviral budding. J. Virol. 77 (2003) 4794-4804
38. Morita E., and Sundquist W.I. Retrovirus budding. Annu. Rev. Cell Dev. Biol. 20 (2004) 395-425
39. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53 (1997) 240-255
40. 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
41. Pickart C.M. Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 70 (2001) 503-533
42. Pommier Y., and Cherfils J. Interfacial inhibition of macromolecular interactions: nature's paradigm for drug discovery. Trends Pharmacol. Sci. 26 (2005) 138-145
43. Pornillos O., Alam S.L., Davis D.R., and Sundquist W.I. 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
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. Raiborg C., Rusten T.E., and Stenmark H. Protein sorting into multivesicular endosomes. Curr. Opin. Cell Biol. 15 (2003) 446-455
46. Scarlata S., and Carter C. Role of HIV-1 Gag domains in viral assembly. Biochim. Biophys. Acta 1614 (2003) 62-72
47. Sigismund S., Polo S., and Di Fiore P.P. Signaling through monoubiquitination. In: Madshus I.H. (Ed). Signalling from Internalized Growth Factor Receptors (2004), Springer-Verlag, Berlin 149-185
48. Slagsvold T., Aasland R., Hirano S., Bache K.G., Raiborg C., Trambaiano 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
49. 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
50. 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
51. 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
52. Tan S. A Modular Polycistronic Expression System for Overexpressing Protein Complexes in Escherichia coli. Protein Expr. Purif. 21 (2001) 224-234
53. 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
54. 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
55. Terwilliger T.C. Maximum-likelihood density modification. Acta Crystallogr. D Biol. Crystallogr. 56 (2000) 965-972
56. Terwilliger T.C. Using prime-and-switch phasing to reduce model bias in molecular replacement. Acta Crystallogr. D Biol. Crystallogr. 60 (2004) 2144-2149
57. Terwilliger T.C., and Berendzen J. Automated MAD and MIR structure solution. Acta Crystallogr. D Biol. Crystallogr. 55 (1999) 849-861
58. Vagin A.A., and Teplyakov A. MOLREP: an automated program for molecular replacement. J. Appl. Crystallogr. 30 (1997) 1022-1025
59. VerPlank L., Bouamr F., LaGrassa T.J., Agresta B., Kikonyogo A., Leis J., and Carter C.A. Tsg101, a homologue of ubiquitin-conjugating (E2) enzymes, binds the L domain in HIV type 1 Pr55(Gag). Proc. Natl. Acad. Sci. USA 98 (2001) 7724-7729
60. 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