On a bender-BARs, ESCRTs, COPs, and finally getting your coat

Journal of Cell Biology

Volumn 193, Issue 6, 2011, Pages 963-972

  Field, Mark C ^a   Sali, Andrej ^b,c   Rout, Michael P ^d  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b San Francisco   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; ESCRT PROTEIN; PROTEIN COP; UNCLASSIFIED DRUG; COAT PROTEIN COMPLEX I;

CELL MEMBRANE; CELL MIGRATION; CELL STRUCTURE; EUKARYOTE; GENOMICS; HUMAN; MEMBRANE; NONHUMAN; PRIORITY JOURNAL; PROTEOMICS; REVIEW; ANIMAL; CHEMISTRY; CYTOLOGY; EUKARYOTIC CELL; EVOLUTION; GENETICS; INTRACELLULAR MEMBRANE; METABOLISM; PHYSIOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

EUKARYOTA;

ANIMALS; BIOLOGICAL EVOLUTION; BIOLOGICAL TRANSPORT; COAT PROTEIN COMPLEX I; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; EUKARYOTIC CELLS; INTRACELLULAR MEMBRANES;

EID: 79959413234     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.201102042     Document Type: Review

References (105)

1. Abodeely, M., K.N. DuBois, A. Hehl, S. Stefanic, M. Sajid, W. DeSouza, M. Attias, J.C. Engel, I. Hsieh, R.D. Fetter, and J.H. McKerrow. 2009. A contiguous compartment functions as endoplasmic reticulum and endosome/ lysosome in Giardia lamblia. Eukaryot. Cell. 8:1665-1676.
2. Alber, F., S. Dokudovskaya, L.M. Veenhoff, W. Zhang, J. Kipper, D. Devos, A. Suprapto, O. Karni-Schmidt, R. Williams, B.T. Chait, et al. 2007a. Determining the architectures of macromolecular assemblies. Nature. 450:683-694.
3. Alber, F., S. Dokudovskaya, L.M. Veenhoff, W. Zhang, J. Kipper, D. Devos, A. Suprapto, O. Karni-Schmidt, R. Williams, B.T. Chait, et al. 2007b. The molecular architecture of the nuclear pore complex. Nature. 450:695- 701.
4. Alexander, D.L., J. Mital, G.E. Ward, P. Bradley, and J.C. Boothroyd. 2005. Identification of the moving junction complex of Toxoplasma gondii: a collaboration between distinct secretory organelles. PLoS Pathog. 1:e17.
5. Andrade, M.A., C. Perez-Iratxeta, and C.P. Ponting. 2001. Protein repeats: structures, functions, and evolution. J. Struct. Biol. 134:117-131.
6. Berke, I.C., T. Boehmer, G. Blobel, and T.U. Schwartz. 2004. Structural and functional analysis of Nup133 domains reveals modular building blocks of the nuclear pore complex. J. Cell Biol. 167:591-597.
7. Boehm, M., and J.S. Bonifacino. 2001. Adaptins: the final recount. Mol. Biol. Cell. 12:2907-2920.
8. Brighouse, A., J.B. Dacks, and M.C. Field. 2010. Rab protein evolution and the history of the eukaryotic endomembrane system. Cell. Mol. Life Sci. 67:3449-3465.
9. Brohawn, S.G., and T.U. Schwartz. 2009. Molecular architecture of the Nup84-Nup145C-Sec13 edge element in the nuclear pore complex lattice. Nat. Struct. Mol. Biol. 16:1173-1177.
10. Brohawn, S.G., J.R. Partridge, J.R. Whittle, and T.U. Schwartz. 2009. The nuclear pore complex has entered the atomic age. Structure. 17:1156-1168.
11. Budnik, A., and D.J. Stephens. 2009. ER exit sites-localization and control of COPII vesicle formation. FEBS Lett. 583:3796-3803.
12. Cabrera, M., L. Langemeyer, M. Mari, R. Rethmeier, I. Orban, A. Perz, C. Bröcker, J. Griffith, D. Klose, H.J. Steinhoff, et al. 2010. Phosphorylation of a membrane curvature-sensing motif switches function of the HOPS subunit Vps41 in membrane tethering. J. Cell Biol. 191:845-859.
13. Carlton, J.G., and J. Martin-Serrano. 2007. Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery. Science. 316:1908- 1912.
14. Cavalier-Smith, T. 2002. The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int. J. Syst. Evol. Microbiol. 52:297-354.
15. Cavalier-Smith, T. 2009. Predation and eukaryote cell origins: a coevolutionary perspective. Int. J. Biochem. Cell Biol. 41:307-322.
16. Cavalier-Smith, T. 2010. Origin of the cell nucleus, mitosis and sex: roles of intracellular coevolution. Biol. Direct. 5:7.
17. Chaudhuri, I., J. Söding, and A.N. Lupas. 2008. Evolution of the β-propeller fold. Proteins. 71:795-803.
18. Collins, B.M. 2008. The structure and function of the retromer protein complex. Traffic. 9:1811-1822.
19. Cook, A., F. Bono, M. Jinek, and E. Conti. 2007. Structural biology of nucleocytoplasmic transport. Annu. Rev. Biochem. 76:647-671.
20. Dacks, J.B., and M.C. Field. 2007. Evolution of the eukaryotic membranetrafficking system: origin, tempo and mode. J. Cell Sci. 120:2977-2985.
21. Debler, E.W., Y. Ma, H.S. Seo, K.C. Hsia, T.R. Noriega, G. Blobel, and A. Hoelz. 2008. A fence-like coat for the nuclear pore membrane. Mol. Cell. 32:815-826.
22. DeGrasse, J.A., K.N. DuBois, D. Devos, T.N. Siegel, A. Sali, M.C. Field, M.P. Rout, and B.T. Chait. 2009. Evidence for a shared nuclear pore complex architecture that is conserved from the last common eukaryotic ancestor. Mol. Cell. Proteomics. 8:2119-2130.
23. Devos, D., S. Dokudovskaya, F. Alber, R. Williams, B.T. Chait, A. Sali, and M.P. Rout. 2004. Components of coated vesicles and nuclear pore complexes share a common molecular architecture. PLoS Biol. 2:e380.
24. Devos, D., S. Dokudovskaya, R. Williams, F. Alber, N. Eswar, B.T. Chait, M.P. Rout, and A. Sali. 2006. Simple fold composition and modular architecture of the nuclear pore complex. Proc. Natl. Acad. Sci. USA. 103:2172- 2177.
25. Dokudovskaya, S., R. Williams, D. Devos, A. Sali, B.T. Chait, and M.P. Rout. 2006. Protease accessibility laddering: a proteomic tool for probing protein structure. Structure. 14:653-660.
26. Dokudovskaya, S., F. Waharte, A. Schlessinger, U. Pieper, D.P. Devos, I.M. Cristea, R. Williams, J. Salamero, B.T. Chait, A. Sali, et al. 2011. A conserved coatomer-related complex containing Sec13 and Seh1 dynamically associates with the vacuole in Saccharomyces cerevisiae. Mol. Cell. Proteomics.
27. Dolezal, P., O. Smíd, P. Rada, Z. Zubácová, D. Bursać, R. Suták, J. Nebesárová, T. Lithgow, and J. Tachezy. 2005. Giardia mitosomes and trichomonad hydrogenosomes share a common mode of protein targeting. Proc. Natl. Acad. Sci. USA. 102:10924-10929.
28. East, M.P., and R.A. Kahn. 2011. Models for the functions of Arf GAPs. Semin. Cell Dev. Biol. 22:3-9.
29. Elias, M. 2010. Patterns and processes in the evolution of the eukaryotic endomembrane system. Mol. Membr. Biol. 27:469-489.
30. Embley, T.M., and W. Martin. 2006. Eukaryotic evolution, changes and challenges. Nature. 440:623-630.
31. Fath, S., J.D. Mancias, X. Bi, and J. Goldberg. 2007. Structure and organization of coat proteins in the COPII cage. Cell. 129:1325-1336.
32. Field, M.C., and J.B. Dacks. 2009. First and last ancestors: reconstructing evolution of the endomembrane system with ESCRTs, vesicle coat proteins, and nuclear pore complexes. Curr. Opin. Cell Biol. 21:4-13.
33. Field, M.C., C. Gabernet-Castello, and J.B. Dacks. 2007. Reconstructing the evolution of the endocytic system: insights from genomics and molecular cell biology. Adv. Exp. Med. Biol. 607:84-96.
34. Forwood, J.K., A. Lange, U. Zachariae, M. Marfori, C. Preast, H. Grubmüller, M. Stewart, A.H. Corbett, and B. Kobe. 2010. Quantitative structural analysis of importin-β flexibility: paradigm for solenoid protein structures. Structure. 18:1171-1183.
35. Fotin, A., Y. Cheng, P. Sliz, N. Grigorieff, S.C. Harrison, T. Kirchhausen, and T. Walz. 2004. Molecular model for a complete clathrin lattice from electron cryomicroscopy. Nature. 432:573-579.
36. Fuerst, J.A. 2005. Intracellular compartmentation in planctomycetes. Annu. Rev. Microbiol. 59:299-328.
37. Funes, S., E. Davidson, A. Reyes-Prieto, S. Magallón, P. Herion, M.P. King, and D. González-Halphen. 2002. A green algal apicoplast ancestor. Science. 298:2155.
38. Gabernet-Castello, C., J.B. Dacks, and M.C. Field. 2009. The single ENTHdomain protein of trypanosomes; endocytic functions and evolutionary relationship with epsin. Traffic. 10:894-911.
39. Gallop, J.L., and H.T. McMahon. 2005. BAR domains and membrane curvature: bringing your curves to the BAR. Biochem. Soc. Symp. (72):223-231.
40. Ghazi-Tabatabai, S., S. Saksena, J.M. Short, A.V. Pobbati, D.B. Veprintsev, R.A. Crowther, S.D. Emr, E.H. Egelman, and R.L. Williams. 2008. Structure and disassembly of filaments formed by the ESCRT-III subunit Vps24. Structure. 16:1345-1356.
41. Gould, S.B., R.F. Waller, and G.I. McFadden. 2008. Plastid evolution. Annu. Rev. Plant Biol. 59:491-517.
42. Graumann, P.L. 2007. Cytoskeletal elements in bacteria. Annu. Rev. Microbiol. 61:589-618.
43. Groves, M.R., and D. Barford. 1999. Topological characteristics of helical repeat proteins. Curr. Opin. Struct. Biol. 9:383-389.
44. Hager, K.M., B. Striepen, L.G. Tilney, and D.S. Roos. 1999. The nuclear envelope serves as an intermediary between the ER and Golgi complex in the intracellular parasite Toxoplasma gondii. J. Cell Sci. 112:2631-2638.
45. Hart, D.T., O. Misset, S.W. Edwards, and F.R. Opperdoes. 1984. A comparison of the glycosomes (microbodies) isolated from Trypanosoma brucei bloodstream form and cultured procyclic trypomastigotes. Mol. Biochem. Parasitol. 12:25-35.
46. Holm, L., and P. Rosenström. 2010. Dali server: conservation mapping in 3D. Nucleic Acids Res. 38:W545-W549.
47. Holstein, S.E., and P. Oliviusson. 2005. Sequence analysis of Arabidopsis thaliana E/ANTH-domain-containing proteins: membrane tethers of the clathrin-dependent vesicle budding machinery. Protoplasma. 226:13-21.
48. Hsia, K.C., P. Stavropoulos, G. Blobel, and A. Hoelz. 2007. Architecture of a coat for the nuclear pore membrane. Cell. 131:1313-1326.
49. Hurley, J.H. 2010. The ESCRT complexes. Crit. Rev. Biochem. Mol. Biol. 45:463-487.
50. Hurley, J.H., and S.D. Emr. 2006. The ESCRT complexes: structure and mechanism of a membrane-trafficking network. Annu. Rev. Biophys. Biomol. Struct. 35:277-298.
51. Hurley, J.H., and P.I. Hanson. 2010. Membrane budding and scission by the ESCRT machinery: it's all in the neck. Nat. Rev. Mol. Cell Biol. 11:556- 566.
52. Jékely, G., and D. Arendt. 2006. Evolution of intraflagellar transport from coated vesicles and autogenous origin of the eukaryotic cilium. Bioessays. 28:191-198.
53. Kampmann, M., and G. Blobel. 2009. Three-dimensional structure and flexibility of a membrane-coating module of the nuclear pore complex. Nat. Struct. Mol. Biol. 16:782-788.
54. Karpenahalli, M.R., A.N. Lupas, and J. Söding. 2007. TPRpred: a tool for prediction of TPR-, PPR- and SEL1-like repeats from protein sequences. BMC Bioinformatics. 8:2.
55. Kats, L.M., B.M. Cooke, R.L. Coppel, and C.G. Black. 2008. Protein trafficking to apical organelles of malaria parasites - building an invasion machine. Traffic. 9:176-186.
56. Kobe, B., and A.V. Kajava. 2000. When protein folding is simplified to protein coiling: the continuum of solenoid protein structures. Trends Biochem. Sci. 25:509-515.
57. Koumandou, V.L., J.B. Dacks, R.M.R. Coulson, and M.C. Field. 2007. Control systems for membrane fusion in the ancestral eukaryote; evolution of tethering complexes and SM proteins. BMC Evol. Biol. 7:29.
58. Koumandou, V.L., S.K.A. Natesan, T. Sergeenko, and M.C. Field. 2008. The trypanosome transcriptome is remodelled during differentiation but displays limited responsiveness within life stages. BMC Genomics. 9:298.
59. Koumandou, V.L., M.J. Klute, E.K. Herman, R. Nunez-Miguel, J.B. Dacks, and M.C. Field. 2011. Evolutionary reconstruction of the retromer complex and its function in Trypanosoma brucei. J. Cell Sci. 124:1496-1509.
60. Ladinsky, M.S., D.N. Mastronarde, J.R. McIntosh, K.E. Howell, and L.A. Staehelin. 1999. Golgi structure in three dimensions: functional insights from the normal rat kidney cell. J. Cell Biol. 144:1135-1149.
61. Lee, C., and J. Goldberg. 2010. Structure of coatomer cage proteins and the relationship among COPI, COPII, and clathrin vesicle coats. Cell. 142:123- 132.
62. Leksa, N.C., S.G. Brohawn, and T.U. Schwartz. 2009. The structure of the scaffold nucleoporin Nup120 reveals a new and unexpected domain architecture. Structure. 17:1082-1091.
63. Leung, K.F., J.B. Dacks, and M.C. Field. 2008. Evolution of the multivesicular body ESCRT machinery; retention across the eukaryotic lineage. Traffic. 9:1698-1716.
64. Lindås, A.C., E.A. Karlsson, M.T. Lindgren, T.J. Ettema, and R. Bernander. 2008. A unique cell division machinery in the Archaea. Proc. Natl. Acad. Sci. USA. 105:18942-18946.
65. Low, H.H., and J. Löwe. 2006. A bacterial dynamin-like protein. Nature. 444:766-769.
66. Makarova, K.S., N. Yutin, S.D. Bell, and E.V. Koonin. 2010. Evolution of diverse cell division and vesicle formation systems in Archaea. Nat. Rev. Microbiol. 8:731-741.
67. Manneville, J.B., J.F. Casella, E. Ambroggio, P. Gounon, J. Bertherat, P. Bassereau, J. Cartaud, B. Antonny, and B. Goud. 2008. COPI coat assembly occurs on liquid-disordered domains and the associated membrane deformations are limited by membrane tension. Proc. Natl. Acad. Sci. USA. 105:16946-16951.
68. Margulis, L. 1993. Symbiosis in cell evolution. W.H. Freeman, New York. 452 pp.
69. Marsh, M.E. 1999. Biomineralization in coccolithophores. Gravit. Space Biol. Bull. 12:5-14.
70. Martin, W. 1999. A briefly argued case that mitochondria and plastids are descendants of endosymbionts, but that the nuclear compartment is not. Proc. R. Soc. London Sci. Ser. B. 266:1387-1395.
71. Martin, W., and E.V. Koonin. 2006. Introns and the origin of nucleus-cytosol compartmentalization. Nature. 440:41-45.
72. Masuda, M., and N. Mochizuki. 2010. Structural characteristics of BAR domain superfamily to sculpt the membrane. Semin. Cell Dev. Biol. 21:391-398.
73. McFadden, G.I. 2010. The apicoplast. Protoplasma.
74. Michels, P.A., and F.R. Opperdoes. 1991. The evolutionary origin of glycosomes. Parasitol. Today (Regul. Ed.). 7:105-109.
75. Miyagishima, S.Y., H. Kuwayama, H. Urushihara, and H. Nakanishi. 2008. Evolutionary linkage between eukaryotic cytokinesis and chloroplast division by dynamin proteins. Proc. Natl. Acad. Sci. USA. 105:15202- 15207.
76. Morita, E., V. Sandrin, H.Y. Chung, S.G. Morham, S.P. Gygi, C.K. Rodesch, and W.I. Sundquist. 2007. Human ESCRT and ALIX proteins interact with proteins of the midbody and function in cytokinesis. EMBO J. 26:4215- 4227.
77. Murzin, A.G., S.E. Brenner, T. Hubbard, and C. Chothia. 1995. SCOP: a structural classification of proteins database for the investigation of sequences and structures. J. Mol. Biol. 247:536-540.
78. Nagy, V., K.C. Hsia, E.W. Debler, M. Kampmann, A.M. Davenport, G. Blobel, and A. Hoelz. 2009. Structure of a trimeric nucleoporin complex reveals alternate oligomerization states. Proc. Natl. Acad. Sci. USA. 106:17693- 17698.
79. Nickerson, D.P., C.L. Brett, and A.J. Merz. 2009. Vps-C complexes: gatekeepers of endolysosomal traffic. Curr. Opin. Cell Biol. 21:543-551.
80. Orengo, C.A., A.D. Michie, S. Jones, D.T. Jones, M.B. Swindells, and J.M. Thornton. 1997. CATH-a hierarchic classification of protein domain structures. Structure. 5:1093-1108.
81. Petrey, D., and B. Honig. 2009. Is protein classification necessary? Toward alternative approaches to function annotation. Curr. Opin. Struct. Biol. 19:363-368.
82. Pinot, M., B. Goud, and J.B. Manneville. 2010. Physical aspects of COPI vesicle formation. Mol. Membr. Biol. 27:428-442.
83. Raiborg, C., and H. Stenmark. 2009. The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature. 458:445-452.
84. Ren, G., P. Vajjhala, J.S. Lee, B. Winsor, and A.L. Munn. 2006. The BAR domain proteins: molding membranes in fission, fusion, and phagy. Microbiol. Mol. Biol. Rev. 70:37-120.
85. Sampathkumar, P., T. Gheyi, S.A. Miller, K.T. Bain, M. Dickey, J.B. Bonanno, S.J. Kim, J. Phillips, U. Pieper, J. Fernandez-Martinez, et al. 2011. Structure of the C-terminal domain of Saccharomyces cerevisiae Nup133, a component of the nuclear pore complex. Proteins. 79:1672-1677.
86. Samson, R.Y., T. Obita, S.M. Freund, R.L. Williams, and S.D. Bell. 2008. A role for the ESCRT system in cell division in archaea. Science. 322:1710- 1713.
87. Santarella-Mellwig, R., J. Franke, A. Jaedicke, M. Gorjanacz, U. Bauer, A. Budd, I.W. Mattaj, and D.P. Devos. 2010. The compartmentalized bacteria of the planctomycetes-verrucomicrobia-chlamydiae superphylum have membrane coat-like proteins. PLoS Biol. 8:e1000281.
88. Satir, P., D.R. Mitchell, and G. Jékely. 2008. How did the cilium evolve? Curr. Top. Dev. Biol. 85:63-82.
89. Seo, H.S., Y. Ma, E.W. Debler, D. Wacker, S. Kutik, G. Blobel, and A. Hoelz. 2009. Structural and functional analysis of Nup120 suggests ring formation of the Nup84 complex. Proc. Natl. Acad. Sci. USA. 106:14281- 14286.
90. Seufferheld, M., C.R. Lea, M. Vieira, E. Oldfield, and R. Docampo. 2004. The H(+)-pyrophosphatase of Rhodospirillum rubrum is predominantly located in polyphosphate-rich acidocalcisomes. J. Biol. Chem. 279:51193- 51202.
91. Shimada, A., H. Niwa, K. Tsujita, S. Suetsugu, K. Nitta, K. Hanawa-Suetsugu, R. Akasaka, Y. Nishino, M. Toyama, L. Chen, et al. 2007. Curved EFC/F-BAR-domain dimers are joined end to end into a filament for membrane invagination in endocytosis. Cell. 129:761-772.
92. Smith, T.F. 2008. Diversity of WD-repeat proteins. Subcell. Biochem. 48:20-30.
93. Söding, J., A. Biegert, and A.N. Lupas. 2005. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 33:W244-W248.
94. Stagg, S.M., P. LaPointe, A. Razvi, C. Gürkan, C.S. Potter, B. Carragher, and W.E. Balch. 2008. Structural basis for cargo regulation of COPII coat assembly. Cell. 134:474-484.
95. Stenmark, H. 2009. Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol. Cell Biol. 10:513-525.
96. Stolz, J.F. 1998. Bacterial intracellular membranes. In Nature Encyclopedia of Life Sciences. A. Mitchell, J. Trapnell, S. Hadfield, V. Kerguelen, and F. Richmond, editors. Wiley, Chichester, UK. pp 1-5.
97. ter Haar, E., A. Musacchio, S.C. Harrison, and T. Kirchhausen. 1998. Atomic structure of clathrin: a beta propeller terminal domain joins an alpha zigzag linker. Cell. 95:563-573.
98. Tovar, J., A. Fischer, and C.G. Clark. 1999. The mitosome, a novel organelle related to mitochondria in the amitochondrial parasite Entamoeba histolytica. Mol. Microbiol. 32:1013-1021.
99. Tovar, J., G. León-Avila, L.B. Sánchez, R. Sutak, J. Tachezy, M. van der Giezen, M. Hernández, M. Müller, and J.M. Lucocq. 2003. Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature. 426:172-176.
100. Vedovato, M., V. Rossi, J.B. Dacks, and F. Filippini. 2009. Comparative analysis of plant genomes allows the definition of the " Phytolongins" : a novel non-SNARE longin domain protein family. BMC Genomics. 10:510.
101. Whittle, J.R., and T.U. Schwartz. 2009. Architectural nucleoporins Nup157/170 and Nup133 are structurally related and descend from a second ancestral element. J. Biol. Chem. 284:28442-28452.
102. Wilbur, J.D., P.K. Hwang, and F.M. Brodsky. 2005. New faces of the familiar clathrin lattice. Traffic. 6:346-350.
103. Wilbur, J.D., P.K. Hwang, J.A. Ybe, M. Lane, B.D. Sellers, M.P. Jacobson, R.J. Fletterick, and F.M. Brodsky. 2010. Conformation switching of clathrin light chain regulates clathrin lattice assembly. Dev. Cell. 18:841-848.
104. Wilson, R.J., P.W. Denny, P.R. Preiser, K. Rangachari, K. Roberts, A. Roy, A. Whyte, M. Strath, D.J. Moore, P.W. Moore, and D.H. Williamson. 1996. Complete gene map of the plastid-like DNA of the malaria parasite Plasmodium falciparum. J. Mol. Biol. 261:155-172.
105. Zhao, H., A. Pykäläinen, and P. Lappalainen. 2011. I-BAR domain proteins: linking actin and plasma membrane dynamics. Curr. Opin. Cell Biol. 23:14-21.