In planta chemical cross‐linking and mass spectrometry analysis of protein structure and interaction in Arabidopsis

Site‐specific chemical cross‐linking in combination with mass spectrometry analysis has emerged as a powerful proteomic approach for studying the three‐dimensional structure of protein complexes and in mapping protein–protein interactions (PPIs). Building on the success of MS analysis of in vitro cross‐linked proteins, which has been widely used to investigate specific interactions of bait proteins and their targets in various organisms, we report a workflow for in vivo chemical cross‐linking and MS analysis in a multicellular eukaryote. This approach optimizes the in vivo protein cross‐linking conditions in Arabidopsis thaliana, establishes a MudPIT procedure for the enrichment of cross‐linked peptides, and develops an integrated software program, exhaustive cross‐linked peptides identification tool (ECL), to identify the MS spectra of in planta chemical cross‐linked peptides. In total, two pairs of in vivo cross‐linked peptides of high confidence have been identified from two independent biological replicates. This work demarks the beginning of an alternative proteomic approach in the study of in vivo protein tertiary structure and PPIs in multicellular eukaryotes.

[1]  W. F. Thompson,et al.  Rapid isolation of high molecular weight plant DNA. , 1980, Nucleic acids research.

[2]  S. Fields,et al.  A novel genetic system to detect protein–protein interactions , 1989, Nature.

[3]  A. Jagendorf,et al.  Chloroplast molecular chaperone-assisted refolding and reconstitution of an active multisubunit coupling factor CF1 core. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[4]  R. Huber,et al.  Structure of 20S proteasome from yeast at 2.4Å resolution , 1997, Nature.

[5]  T. Hisabori,et al.  The β subunit of chloroplast ATP synthase (CF0CF1‐ATPase) is phosphorylated by casein kinase II , 1998 .

[6]  D. N. Perkins,et al.  Probability‐based protein identification by searching sequence databases using mass spectrometry data , 1999, Electrophoresis.

[7]  P. Quail,et al.  A simple, rapid and quantitative method for preparing Arabidopsis protein extracts for immunoblot analysis. , 1999, The Plant journal : for cell and molecular biology.

[8]  T. Steitz,et al.  The complete atomic structure of the large ribosomal subunit at 2.4 A resolution. , 2000, Science.

[9]  Malin M. Young,et al.  High throughput protein fold identification by using experimental constraints derived from intramolecular cross-links and mass spectrometry , 2000, Proc. Natl. Acad. Sci. USA.

[10]  Bernhard O. Palsson,et al.  Metabolic flux balance analysis and the in silico analysis of Escherichia coli K-12 gene deletions , 2000, BMC Bioinformatics.

[11]  N. Yalpani,et al.  Prohibitins, Stomatins, and Plant Disease Response Genes Compose a Protein Superfamily That Controls Cell Proliferation, Ion Channel Regulation, and Death* , 2000, The Journal of Biological Chemistry.

[12]  P. Cramer,et al.  Structural Basis of Transcription: RNA Polymerase II at 2.8 Ångstrom Resolution , 2001, Science.

[13]  A. Minton,et al.  The Influence of Macromolecular Crowding and Macromolecular Confinement on Biochemical Reactions in Physiological Media* , 2001, The Journal of Biological Chemistry.

[14]  A. Verkman.  Solute and macromolecule diffusion in cellular aqueous compartments. , 2002, Trends in biochemical sciences.

[15]  Bernhard Kuster,et al.  Affinity purification‐mass spectrometry , 2003 .

[16]  Jean B. Smith,et al.  Unexpected products from the reaction of the synthetic cross-linker 3,3′-dithiobis(sulfosuccinimidyl propionate), DTSSP with peptides , 2004, Journal of the American Society for Mass Spectrometry.

[17]  Chris F. Taylor,et al.  A common open representation of mass spectrometry data and its application to proteomics research , 2004, Nature Biotechnology.

[18]  Ruth Nussinov,et al.  PatchDock and SymmDock: servers for rigid and symmetric docking , 2005, Nucleic Acids Res..

[19]  Peter G Schultz,et al.  Efficient incorporation of unnatural amino acids into proteins in Escherichia coli , 2006, Nature Methods.

[20]  Lan Huang,et al.  An Integrated Mass Spectrometry-based Proteomic Approach , 2006, Molecular & Cellular Proteomics.

[21]  William Stafford Noble,et al.  Semi-supervised learning for peptide identification from shotgun proteomics datasets , 2007, Nature Methods.

[22]  S. Robbins,et al.  The SPFH domain-containing proteins: more than lipid raft markers. , 2007, Trends in cell biology.

[23]  Hyungwon Choi,et al.  False discovery rates and related statistical concepts in mass spectrometry-based proteomics. , 2008, Journal of proteome research.

[24]  William Stafford Noble,et al.  Posterior error probabilities and false discovery rates: two sides of the same coin. , 2008, Journal of proteome research.

[25]  Ruedi Aebersold,et al.  Identification of cross-linked peptides from large sequence databases , 2008, Nature Methods.

[26]  Ruedi Aebersold,et al.  Corrigendum: Identification of cross-linked peptides from large sequence databases , 2008 .

[27]  W. Gruissem,et al.  Large-Scale Arabidopsis Phosphoproteome Profiling Reveals Novel Chloroplast Kinase Substrates and Phosphorylation Networks1[W] , 2009, Plant Physiology.

[28]  Lila M Gierasch,et al.  Post-reductionist protein science, or putting Humpty Dumpty back together again. , 2009, Nature chemical biology.

[29]  James E Bruce,et al.  A new cross-linking strategy: protein interaction reporter (PIR) technology for protein-protein interaction studies. , 2010, Molecular bioSystems.

[30]  Yang Zhang,et al.  I-TASSER: a unified platform for automated protein structure and function prediction , 2010, Nature Protocols.

[31]  Ilpo Vattulainen,et al.  Defect-mediated trafficking across cell membranes: insights from in silico modeling. , 2010, Chemical reviews.

[32]  J Richard McIntosh,et al.  Arrangement of Photosystem II and ATP Synthase in Chloroplast Membranes of Spinach and Pea[W][OA] , 2010, Plant Cell.

[33]  Michael R Hoopmann,et al.  Cross-linking Measurements of In Vivo Protein Complex Topologies* , 2011, Molecular & Cellular Proteomics.

[34]  Jan C. Refsgaard,et al.  CrossWork: software-assisted identification of cross-linked peptides. , 2011, Journal of proteomics.

[35]  Ning Li,et al.  Relative and accurate measurement of protein abundance using 15N stable isotope labeling in Arabidopsis (SILIA). , 2011, Phytochemistry.

[36]  J. Glazebrook,et al.  Physical Association of Arabidopsis Hypersensitive Induced Reaction Proteins (HIRs) with the Immune Receptor RPS2* , 2011, The Journal of Biological Chemistry.

[37]  Hyong Woo Choi,et al.  The hypersensitive induced reaction and leucine-rich repeat proteins regulate plant cell death associated with disease and plant immunity. , 2011, Molecular plant-microbe interactions : MPMI.

[38]  Hugh-George Patterton,et al.  Bioinformatics tools for the structural elucidation of multi-subunit protein complexes by mass spectrometric analysis of protein-protein cross-links , 2011, Briefings Bioinform..

[39]  S. Baginsky,et al.  Signal integration by chloroplast phosphorylation networks: an update , 2012, Front. Plant Sci..

[40]  M. Dong,et al.  Identification of cross-linked peptides from complex samples , 2012, Nature Methods.

[41]  Friedrich Förster,et al.  False discovery rate estimation for cross-linked peptides identified by mass spectrometry , 2012, Nature Methods.

[42]  James E Bruce,et al.  In vivo protein complex topologies: Sights through a cross‐linking lens , 2012, Proteomics.

[43]  R. Aebersold,et al.  Structural Probing of a Protein Phosphatase 2A Network by Chemical Cross-Linking and Mass Spectrometry , 2012, Science.

[44]  R. Aebersold,et al.  Expanding the Chemical Cross-Linking Toolbox by the Use of Multiple Proteases and Enrichment by Size Exclusion Chromatography , 2012, Molecular & Cellular Proteomics.

[45]  Chunxiang Zheng,et al.  Protein Interactions, Post-translational Modifications and Topologies in Human Cells* , 2013, Molecular & Cellular Proteomics.

[46]  Juri Rappsilber,et al.  Quantitative cross-linking/mass spectrometry using isotope-labelled cross-linkers☆ , 2013, Journal of proteomics.

[47]  M. Gross,et al.  Phycobilisomes Supply Excitations to Both Photosystems in a Megacomplex in Cyanobacteria , 2013, Science.

[48]  Carol V. Robinson,et al.  Comparative cross-linking and mass spectrometry of an intact F-type ATPase suggest a role for phosphorylation , 2013, Nature Communications.

[49]  Henry Lam,et al.  Stable Isotope Metabolic Labeling-based Quantitative Phosphoproteomic Analysis of Arabidopsis Mutants Reveals Ethylene-regulated Time-dependent Phosphoproteins and Putative Substrates of Constitutive Triple Response 1 Kinase* , 2013, Molecular & Cellular Proteomics.

[50]  Lan Huang,et al.  Developing New Isotope-Coded Mass Spectrometry-Cleavable Cross-Linkers for Elucidating Protein Structures , 2014, Analytical chemistry.

[51]  Seung Joong Kim,et al.  Structural Characterization by Cross-linking Reveals the Detailed Architecture of a Coatomer-related Heptameric Module from the Nuclear Pore Complex* , 2014, Molecular & Cellular Proteomics.

[52]  Ruedi Aebersold,et al.  Lysine-specific chemical cross-linking of protein complexes and identification of cross-linking sites using LC-MS/MS and the xQuest/xProphet software pipeline , 2013, Nature Protocols.

[53]  C. D. de Koster,et al.  A gas phase cleavage reaction of cross-linked peptides for protein complex topology studies by peptide fragment fingerprinting from large sequence database. , 2014, Journal of proteomics.

[54]  S. Rupp,et al.  An In Vivo Photo-Cross-Linking Approach Reveals a Homodimerization Domain of Aha1 in S. cerevisiae , 2014, PloS one.

[55]  C. Ihling,et al.  Reliable Identification of Cross-Linked Products in Protein Interaction Studies by 13C-Labeled p-Benzoylphenylalanine , 2014, Journal of The American Society for Mass Spectrometry.

[56]  Hailong Zhu,et al.  Predicting protein functions using incomplete hierarchical labels , 2015, BMC Bioinformatics.

[57]  Albert J R Heck,et al.  Proteome-wide profiling of protein assemblies by cross-linking mass spectrometry , 2015, Nature Methods.

[58]  D. Leister,et al.  Assembly of F1F0-ATP synthases. , 2015, Biochimica et biophysica acta.

[59]  William Stafford Noble,et al.  Improved False Discovery Rate Estimation Procedure for Shotgun Proteomics , 2015, Journal of proteome research.

[60]  Sabine Kahlau,et al.  Photosynthetic complex stoichiometry dynamics in higher plants: biogenesis, function, and turnover of ATP synthase and the cytochrome b6f complex. , 2015, Journal of experimental botany.

[61]  Ning Li,et al.  ECL: an exhaustive search tool for the identification of cross-linked peptides using whole database , 2016, BMC Bioinformatics.