Structural Characterization by Cross-linking Reveals the Detailed Architecture of a Coatomer-related Heptameric Module from the Nuclear Pore Complex

Molecular & Cellular Proteomics - Tập 13 - Trang 2927-2943 - 2014
Yi Shi1, Javier Fernandez-Martinez2, Elina Tjioe3, Riccardo Pellarin3, Seung Joong Kim3, Rosemary Williams2, Dina Schneidman-Duhovny3, Andrej Sali3, Michael P. Rout2, Brian T. Chait1
1From the Laboratory of Mass Spectrometry and Gaseous Ion Chemistry, The Rockefeller University, New York, New York 10065;
2Laboratory of Cellular and Structural Biology, The Rockefeller University, New York, New York 10065;
3Department of Bioengineering and Therapeutic Sciences, Department of Pharmaceutical Chemistry, California Institute for Quantitative Biosciences, Byers Hall, 1700 4th Street, Suite 503B, University of California, San Francisco, San Francisco, California 94158

Tài liệu tham khảo

Gavin, 2006, Proteome survey reveals modularity of the yeast cell machinery, Nature, 440, 631, 10.1038/nature04532 Krogan, 2006, Global landscape of protein complexes in the yeast Saccharomyces cerevisiae, Nature, 440, 637, 10.1038/nature04670 Malovannaya, 2011, Analysis of the human endogenous coregulator complexome, Cell, 145, 787, 10.1016/j.cell.2011.05.006 Robinson, 2007, The molecular sociology of the cell, Nature, 450, 973, 10.1038/nature06523 Alber, 2008, Integrating diverse data for structure determination of macromolecular assemblies, Annu. Rev. Biochem, 77, 443, 10.1146/annurev.biochem.77.060407.135530 Ward, 2013, Biochemistry. Integrative structural biology, Science, 339, 913, 10.1126/science.1228565 Alber, 2007, Determining the architectures of macromolecular assemblies, Nature, 450, 683, 10.1038/nature06404 Alber, 2007, The molecular architecture of the nuclear pore complex, Nature, 450, 695, 10.1038/nature06405 Duan, 2010, A three-dimensional model of the yeast genome, Nature, 465, 363, 10.1038/nature08973 Boura, 2011, Solution structure of the ESCRT-I complex by small-angle X-ray scattering, EPR, and FRET spectroscopy, Proc. Natl. Acad. Sci. U.S.A, 108, 9437, 10.1073/pnas.1101763108 Kalhor, 2012, Genome architectures revealed by tethered chromosome conformation capture and population-based modeling, Nat. Biotechnol, 30, 90, 10.1038/nbt.2057 Lander, 2012, Complete subunit architecture of the proteasome regulatory particle, Nature, 482, 186, 10.1038/nature10774 Lasker, 2012, Molecular architecture of the 26S proteasome holocomplex determined by an integrative approach, Proc. Natl. Acad. Sci. U.S.A, 109, 1380, 10.1073/pnas.1120559109 Fernandez-Martinez, 2012, Structure-function mapping of a heptameric module in the nuclear pore complex, J. Cell Biol, 196, 419, 10.1083/jcb.201109008 Tosi, 2013, Structure and subunit topology of the INO80 chromatin remodeler and its nucleosome complex, Cell, 154, 1207, 10.1016/j.cell.2013.08.016 Greber, 2014, Architecture of the large subunit of the mammalian mitochondrial ribosome, Nature, 505, 515, 10.1038/nature12890 Cohen, 2001, Mass spectrometry as a tool for protein crystallography, Annu. Rev. Biophys. Biomol. Struct, 30, 67, 10.1146/annurev.biophys.30.1.67 Young, 2000, High throughput protein fold identification by using experimental constraints derived from intramolecular cross-links and mass spectrometry, Proc. Natl. Acad. Sci. U.S.A, 97, 5802, 10.1073/pnas.090099097 Chen, 2010, Architecture of the RNA polymerase II-TFIIF complex revealed by cross-linking and mass spectrometry, EMBO J, 29, 717, 10.1038/emboj.2009.401 Herzog, 2012, Structural probing of a protein phosphatase 2A network by chemical cross-linking and mass spectrometry, Science, 337, 1348, 10.1126/science.1221483 Leitner, 2010, Probing native protein structures by chemical cross-linking, mass spectrometry, and bioinformatics, Mol. Cell. Proteomics, 9, 1634, 10.1074/mcp.R000001-MCP201 Sinz, 2006, Chemical cross-linking and mass spectrometry to map three-dimensional protein structures and protein-protein interactions, Mass Spectrom. Rev, 25, 663, 10.1002/mas.20082 Trnka, 2014, Matching cross-linked peptide spectra: only as good as the worse identification, Mol. Cell. Proteomics, 13, 420, 10.1074/mcp.M113.034009 Kao, 2011, Development of a novel cross-linking strategy for fast and accurate identification of cross-linked peptides of protein complexes, Mol. Cell. Proteomics, 10, 10.1074/mcp.M110.002212 Weisbrod, 2013, In vivo protein interaction network identified with a novel real-time cross-linked peptide identification strategy, J. Proteome Res, 12, 1569, 10.1021/pr3011638 Ghaemmaghami, 2003, Global analysis of protein expression in yeast, Nature, 425, 737, 10.1038/nature02046 Beck, 2011, The quantitative proteome of a human cell line, Mol. Syst. Biol, 7, 549, 10.1038/msb.2011.82 Leitner, 2014, Chemical cross-linking/mass spectrometry targeting acidic residues in proteins and protein complexes, Proc. Natl. Acad. Sci. U.S.A, 111, 9455, 10.1073/pnas.1320298111 Rout, 2000, The yeast nuclear pore complex: composition, architecture, and transport mechanism, J. Cell Biol, 635, 10.1083/jcb.148.4.635 Lutzmann, 2002, Modular self-assembly of a Y-shaped multiprotein complex from seven nucleoporins, EMBO J, 21, 387, 10.1093/emboj/21.3.387 Brohawn, 2008, Structural evidence for common ancestry of the nuclear pore complex and vesicle coats, Science, 322, 1369, 10.1126/science.1165886 Devos, 2004, Components of coated vesicles and nuclear pore complexes share a common molecular architecture, PLoS Biol, 2, e380, 10.1371/journal.pbio.0020380 Bilokapic, 2012, 3D ultrastructure of the nuclear pore complex, Curr. Opin. Cell Biol, 24, 86, 10.1016/j.ceb.2011.12.011 Hoelz, 2011, The structure of the nuclear pore complex, Annu. Rev. Biochem, 80, 613, 10.1146/annurev-biochem-060109-151030 Bui, 2013, Integrated structural analysis of the human nuclear pore complex scaffold, Cell, 155, 1233, 10.1016/j.cell.2013.10.055 Kampmann, 2009, Three-dimensional structure and flexibility of a membrane-coating module of the nuclear pore complex, Nat. Struct. Mol. Biol, 16, 782, 10.1038/nsmb.1618 Thierbach, 2013, Protein interfaces of the conserved Nup84 complex from Chaetomium thermophilum shown by crosslinking mass spectrometry and electron microscopy, Structure, 21, 1672, 10.1016/j.str.2013.07.004 Velazquez-Muriel, 2012, Assembly of macromolecular complexes by satisfaction of spatial restraints from electron microscopy images, Proc. Natl. Acad. Sci. U.S.A, 109, 18821, 10.1073/pnas.1216549109 Olsen, 2007, Higher-energy C-trap dissociation for peptide modification analysis, Nat. Methods, 4, 709, 10.1038/nmeth1060 Yang, 2012, Identification of cross-linked peptides from complex samples, Nat. Methods, 9, 904, 10.1038/nmeth.2099 Qin, 1995, Preferential fragmentation of protonated gas-phase peptide ions adjacent to acidic amino-acid-residues, J. Am. Chem. Soc, 117, 5411, 10.1021/ja00124a045 Michalski, 2012, A systematic investigation into the nature of tryptic HCD spectra, J. Proteome Res, 11, 5479, 10.1021/pr3007045 Lasker, 2010, Integrative structure modeling of macromolecular assemblies from proteomics data, Mol. Cell. Proteomics, 9, 1689, 10.1074/mcp.R110.000067 Russel, 2012, Putting the pieces together: integrative modeling platform software for structure determination of macromolecular assemblies, PLoS Biol, 10, e1001244, 10.1371/journal.pbio.1001244 Berke, 2004, Structural and functional analysis of Nup133 domains reveals modular building blocks of the nuclear pore complex, J. Cell Biol, 167, 591, 10.1083/jcb.200408109 Whittle, 2009, Architectural nucleoporins Nup157/170 and Nup133 are structurally related and descend from a second ancestral element, J. Biol. Chem, 284, 28442, 10.1074/jbc.M109.023580 Boehmer, 2008, Structural and functional studies of Nup107/Nup133 interaction and its implications for the architecture of the nuclear pore complex, Mol. Cell, 30, 721, 10.1016/j.molcel.2008.04.022 Sampathkumar, 2011, Structure of the C-terminal domain of Saccharomyces cerevisiae Nup133, a component of the nuclear pore complex, Proteins, 79, 1672, 10.1002/prot.22973 Brohawn, 2009, Molecular architecture of the Nup84-Nup145C-Sec13 edge element in the nuclear pore complex lattice, Nat. Struct. Mol. Biol, 16, 1173, 10.1038/nsmb.1713 Nagy, 2009, Structure of a trimeric nucleoporin complex reveals alternate oligomerization states, Proc. Natl. Acad. Sci. U.S.A, 106, 17693, 10.1073/pnas.0909373106 Seo, 2009, Structural and functional analysis of Nup120 suggests ring formation of the Nup84 complex, Proc. Natl. Acad. Sci. U.S.A, 106, 14281, 10.1073/pnas.0907453106 Leksa, 2009, The structure of the scaffold nucleoporin Nup120 reveals a new and unexpected domain architecture, Structure, 17, 1082, 10.1016/j.str.2009.06.003 Debler, 2008, A fence-like coat for the nuclear pore membrane, Mol. Cell, 32, 815, 10.1016/j.molcel.2008.12.001 Fath, 2007, Structure and organization of coat proteins in the COPII cage, Cell, 129, 1325, 10.1016/j.cell.2007.05.036 Jeudy, 2007, Crystal structure of nucleoporin Nic96 reveals a novel, intricate helical domain architecture, J. Biol. Chem, 282, 34904, 10.1074/jbc.M705479200 Lee, 2013, Crystal structure and versatile functional roles of the COP9 signalosome subunit 1, Proc. Natl. Acad. Sci. U.S.A, 110, 11845, 10.1073/pnas.1302418110 Soding, 2005, Protein homology detection by HMM-HMM comparison, Bioinformatics, 21, 951, 10.1093/bioinformatics/bti125 Soding, 2005, The HHpred interactive server for protein homology detection and structure prediction, Nucleic Acids Res, 33, W244, 10.1093/nar/gki408 Jones, 1999, Protein secondary structure prediction based on position-specific scoring matrices, J. Mol. Biol, 292, 195, 10.1006/jmbi.1999.3091 Buchan, 2013, Scalable web services for the PSIPRED Protein Analysis Workbench, Nucleic Acids Res, 41, W349, 10.1093/nar/gkt381 Ward, 2004, The DISOPRED server for the prediction of protein disorder, Bioinformatics, 20, 2138, 10.1093/bioinformatics/bth195 Sali, 1993, Comparative protein modelling by satisfaction of spatial restraints, J. Mol. Biol, 234, 779, 10.1006/jmbi.1993.1626 Erzberger, 2014, Molecular architecture of the 40S-eIF1-eIF3 Translation Initiation Complex, Cell, 158, 1123, 10.1016/j.cell.2014.07.044 Shen, 2006, Statistical potential for assessment and prediction of protein structures, Protein Sci, 15, 2507, 10.1110/ps.062416606 Schneidman-Duhovny, 2012, A method for integrative structure determination of protein-protein complexes, Bioinformatics, 28, 3282, 10.1093/bioinformatics/bts628 Rieping, 2005, Inferential structure determination, Science, 309, 303, 10.1126/science.1110428 Humphrey, 1996, VMD: visual molecular dynamics, J. Mol. Graphics, 14, 33, 10.1016/0263-7855(96)00018-5 Heyer, 1999, Exploring expression data: identification and analysis of coexpressed genes, Genome Res, 9, 1106, 10.1101/gr.9.11.1106 Levitt, 1983, Molecular dynamics of native protein. II. Analysis and nature of motion, J. Mol. Biol, 168, 621, 10.1016/S0022-2836(83)80306-4 Oeffinger, 2007, Comprehensive analysis of diverse ribonucleoprotein complexes, Nat. Methods, 4, 951, 10.1038/nmeth1101 Leitner, 2012, Expanding the chemical cross-linking toolbox by the use of multiple proteases and enrichment by size exclusion chromatography, Mol. Cell. Proteomics, 11, 10.1074/mcp.M111.014126 Merkley, 2014, Distance restraints from crosslinking mass spectrometry: mining a molecular dynamics simulation database to evaluate lysine-lysine distances, Protein Sci, 23, 747, 10.1002/pro.2458 Hsia, 2007, Architecture of a coat for the nuclear pore membrane, Cell, 131, 1313, 10.1016/j.cell.2007.11.038 Algret, 2014, Molecular architecture and function of the SEA complex, a modulator of the TORC1 pathway, Mol. Cell. Proteomics, 10.1074/mcp.M114.039388 Yang, 1998, Three-dimensional architecture of the isolated yeast nuclear pore complex: functional and evolutionary implications, Mol. Cell, 1, 223, 10.1016/S1097-2765(00)80023-4 Sampathkumar, 2013, Structure, dynamics, evolution, and function of a major scaffold component in the nuclear pore complex, Structure, 21, 560, 10.1016/j.str.2013.02.005 Brohawn, 2009, The nuclear pore complex has entered the atomic age, Structure, 17, 1156, 10.1016/j.str.2009.07.014 Lee, 2010, Structure of coatomer cage proteins and the relationship among COPI, COPII, and clathrin vesicle coats, Cell, 142, 123, 10.1016/j.cell.2010.05.030 Devos, 2006, Simple fold composition and modular architecture of the nuclear pore complex, Proc. Natl. Acad. Sci. U.S.A, 103, 2172, 10.1073/pnas.0506345103 Field, 2011, Evolution: on a bender—BARs, ESCRTs, COPs, and finally getting your coat, J. Cell Biol, 193, 963, 10.1083/jcb.201102042 Dokudovskaya, 2011, A conserved coatomer-related complex containing Sec13 and Seh1 dynamically associates with the vacuole in Saccharomyces cerevisiae, Mol. Cell. Proteomics, 10, 10.1074/mcp.M110.006478 van Dam, 2013, Evolution of modular intraflagellar transport from a coatomer-like progenitor, Proc. Natl. Acad. Sci. U.S.A, 110, 6943, 10.1073/pnas.1221011110 Faini, 2013, Vesicle coats: structure, function, and general principles of assembly, Trends Cell Biol, 23, 279, 10.1016/j.tcb.2013.01.005 Fotin, 2004, Molecular model for a complete clathrin lattice from electron cryomicroscopy, Nature, 432, 573, 10.1038/nature03079 Siniossoglou, 2000, Structure and assembly of the Nup84p complex, J. Cell Biol, 149, 41, 10.1083/jcb.149.1.41 Leksa, 2010, Membrane-coating lattice scaffolds in the nuclear pore and vesicle coats: commonalities, differences, challenges, Nucleus, 1, 314, 10.4161/nucl.1.4.11798 Hirst, 2014, Characterization of TSET, an ancient and widespread membrane trafficking complex, eLife, 3, e02866, 10.7554/eLife.02866 Drin, 2007, A general amphipathic alpha-helical motif for sensing membrane curvature, Nat. Struct. Mol. Biol, 14, 138, 10.1038/nsmb1194 Drin, 2010, Amphipathic helices and membrane curvature, FEBS Lett, 584, 1840, 10.1016/j.febslet.2009.10.022 Akey, 1993, Architecture of the Xenopus nuclear pore complex revealed by three-dimensional cryo-electron microscopy, J. Cell Biol, 122, 1, 10.1083/jcb.122.1.1 Kim, 2014, Integrative structure-function mapping of the nucleoporin Nup133 suggests a conserved mechanism for membrane anchoring of the nuclear pore complex, Mol. Cell. Proteomics, 10.1074/mcp.M114.040915