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Quantitative and Systems-Based Approaches for Deciphering Bacterial Membrane Interactome and Gene Function

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Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 883))

Abstract

High-throughput genomic and proteomic methods provide a concise description of the molecular constituents of a cell, whereas systems biology strives to understand the way these components function as a whole. Recent developments, such as genome editing technologies and protein epitope-tagging coupled with high-sensitivity mass-spectrometry, allow systemic studies to be performed at an unprecedented scale. Available methods can be successfully applied to various goals, both expanding fundamental knowledge and solving applied problems. In this review, we discuss the present state and future of bacterial cell envelope interactomics, with a specific focus on host–pathogen interactions and drug target discovery. Both experimental and computational methods will be outlined together with examples of their practical implementation.

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References

  • Ahrens CH, Brunner E, Qeli E, Basler K, Aebersold R (2010) Generating and navigating proteome maps using mass spectrometry. Nat Rev Mol Cell Biol 11:789–801

    Article  CAS  PubMed  Google Scholar 

  • Albersmeier A, Bomholt C, Glaub A, Ruckert C, Soriano F, Fernandez-Natal I, Tauch A (2014) Draft genome sequence of the multidrug-resistant clinical isolate Dermabacter hominis 1368. Genome Announc 2

    Google Scholar 

  • Babu M, Musso G, Diaz-Mejia JJ, Butland G, Greenblatt JF, Emili A (2009) Systems-level approaches for identifying and analyzing genetic interaction networks in Escherichia coli and extensions to other prokaryotes. Mol Biosyst 12:1439–1455

    Article  CAS  Google Scholar 

  • Babu M, Díaz-Mejía JJ, Vlasblom J, Gagarinova A, Phanse S, Graham C, Arnold R, Yousif F, Ding H, Xiong X, Nazarians-Armavil A, Alamgir M, Ali M, Pogoutse O, Pe’er A, Parkinson J, Golshani A, Whitfield C, Wodak SJ, Moreno-Hagelsieb G, Greenblatt JF, Emili A (2011) Genetic interaction maps in Escherichia coli reveal functional crosstalk among cell envelope biogenesis pathways. PLoS Genet 7, e1002377

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Babu M, Vlasblom J, Pu S, Guo X, Graham C, Bean BDM, Burston HE, Vizeacoumar FJ, Snider J, Phanse S, Fong V, Tam YYC, Davey M, Hnatshak O, Bajaj N, Chandran S, Punna T, Christopolous C, Wong V, Yu A, Zhong G, Li J, Stagljar I, Conibear E, Wodak SJ, Emili A, Greenblatt JF (2012) Interaction landscape of membrane-protein complexes in Saccharomyces cerevisiae. Nature 489:585–589

    Article  CAS  PubMed  Google Scholar 

  • Babu M, Arnold R, Bundalovic-Torma C, Gagarinova A, Wong KS, Kumar A, Stewart G, Samanfar B, Aoki H, Wagih O, Vlasblom J, Phanse S, Lad K, Yeou Hsiung Yu A, Graham C, Jin K, Brown E, Golshani A, Kim P, Moreno-Hagelsieb G, Greenblatt J, Houry WA, Parkinson J, Emili A (2014) Quantitative genome-wide genetic interaction screens reveal global epistatic relationships of protein complexes in Escherichia coli. PLoS Genet 10, e1004120

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Baryshnikova A, Costanzo M, Myers CL, Andrews B, Boone C (2013) Genetic interaction networks: toward an understanding of heritability. Annu Rev Genomics Hum Genet 14:111–133

    Article  CAS  PubMed  Google Scholar 

  • Baspinar A, Cukuroglu E, Nussinov R, Keskin O, Gursoy A (2014) PRISM: a web server and repository for prediction of protein–protein interactions and modeling their 3D complexes. Nucleic Acids Res 42:W285–W289

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Becher D, Hempel K, Sievers S, Zuhlke D, Pane-Farre J, Otto A, Fuchs S, Albrecht D, Bernhardt J, Engelmann S, Volker U, van Dijl JM, Hecker M (2009) A proteomic view of an important human pathogen—towards the quantification of the entire Staphylococcus aureus proteome. PLoS One 4, e8176

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Beltrao P, Cagney G, Krogan NJ (2010) Quantitative genetic interactions reveal biological modularity. Cell 141:739–745

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Berman HM, Coimbatore Narayanan B, Di Costanzo L, Dutta S, Ghosh S, Hudson BP, Lawson CL, Peisach E, Prlic A, Rose PW, Shao C, Yang H, Young J, Zardecki C (2013) Trendspotting in the Protein Data Bank. FEBS Lett 587:1036–1045

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bernsel A, Daley DO (2009) Exploring the inner membrane proteome of Escherichia coli: which proteins are eluding detection and why? Trends Microbiol 17:444–449

    Article  CAS  PubMed  Google Scholar 

  • Bracken C, Iakoucheva LM, Romero PR, Dunker AK (2004) Combining prediction, computation and experiment for the characterization of protein disorder. Curr Opin Struct Biol 14:570–576

    Article  CAS  PubMed  Google Scholar 

  • Bragazzi NL, Pechkova E, Nicolini C (2014) Proteomics and proteogenomics approaches for oral diseases. Adv Protein Chem Struct Biol 95:125–162

    Article  CAS  PubMed  Google Scholar 

  • Butland G, Babu M, Díaz-Mejía JJ, Bohdana F, Phanse S, Gold B, Yang W, Li J, Gagarinova AG, Pogoutse O, Mori H, Wanner BL, Lo H, Wasniewski J, Christopolous C, Ali M, Venn P, Safavi-Naini A, Sourour N, Caron S, Choi JY, Laigle L, Nazarians-Armavil A, Deshpande A, Joe S, Datsenko KA, Yamamoto N, Andrews BJ, Boone C, Ding H, Sheikh B, Moreno-Hagelseib G, Greenblatt JF, Emili A (2008) eSGA: E. coli synthetic genetic array analysis. Nat Methods 5:789–795

    Article  CAS  PubMed  Google Scholar 

  • Cabral MP, Soares NC, Aranda J, Parreira JR, Rumbo C, Poza M, Valle J, Calamia V, Lasa I, Bou G (2011) Proteomic and functional analyses reveal a unique lifestyle for Acinetobacter baumannii biofilms and a key role for histidine metabolism. J Proteome Res 10:3399–3417

    Article  CAS  PubMed  Google Scholar 

  • Caufield JH, Abreu M, Wimble C, Uetz P (2015) Protein complexes in bacteria. PLoS Comput Biol 11, e1004107

    Article  PubMed Central  PubMed  Google Scholar 

  • Curreem SO, Watt RM, Lau SK, Woo PC (2012) Two-dimensional gel electrophoresis in bacterial proteomics. Protein Cell 3:346–363

    Article  CAS  PubMed  Google Scholar 

  • Daley DO, Rapp M, Granseth E, Melen K, Drew D, von Heijne G (2005) Global topology analysis of the Escherichia coli inner membrane proteome. Science 308:1321–1323

    Article  CAS  PubMed  Google Scholar 

  • Davey NE, Haslam NJ, Shields DC, Edwards RJ (2011) SLiMSearch 2.0: biological context for short linear motifs in proteins. Nucleic Acids Res 39:W56–W60

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Davies J, Davies D (2010) Origins and evolution of antibiotic resistance. Microbiol Mol Biol Rev 74:417–433

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Díaz-Mejía JJ, Babu M, Emili A (2009) Computational and experimental approaches to chart the Escherichia coli cell-envelope-associated proteome and interactome. FEMS Microbiol Rev 33:66–97

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Domon B, Aebersold R (2010) Options and considerations when selecting a quantitative proteomics strategy. Nat Biotechnol 28:710–721

    Article  CAS  PubMed  Google Scholar 

  • Dresler J, Klimentova J, Stulik J (2011) Bacterial protein complexes investigation using blue native PAGE. Microbiol Res 166:47–62

    Article  CAS  PubMed  Google Scholar 

  • Edwards RJ, Davey NE, Shields DC (2007) SLiMFinder: a probabilistic method for identifying over-represented, convergently evolved, short linear motifs in proteins. PLoS One 2, e967

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Enright AJ, Iliopoulos I, Kyrpides NC, Ouzounis CA (1999) Protein interaction maps for complete genomes based on gene fusion events. Nature 402:86–90

    Article  CAS  PubMed  Google Scholar 

  • Flores-Mireles AL, Walker JN, Caparon M, Hultgren SJ (2015) Urinary tract infections: epidemiology, mechanisms of infection and treatment options. Nat Rev Microbiol 13:269–284

    Article  CAS  PubMed  Google Scholar 

  • Fruh V, Zhou Y, Chen D, Loch C, Ab E, Grinkova YN, Verheij H, Sligar SG, Bushweller JH, Siegal G (2010) Application of fragment-based drug discovery to membrane proteins: identification of ligands of the integral membrane enzyme DsbB. Chem Biol 17:881–891

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ghersi D, Sanchez R (2011) Beyond structural genomics: computational approaches for the identification of ligand binding sites in protein structures. J Struct Funct Genomics 12:109–117

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gokhale A, Perez-Cornejo P, Duran C, Hartzell HC, Faundez V (2012) A comprehensive strategy to identify stoichiometric membrane protein interactomes. Cell Logist 2:189–196

    Article  PubMed Central  PubMed  Google Scholar 

  • Gouw JW, Krijgsveld J, Heck AJ (2010) Quantitative proteomics by metabolic labeling of model organisms. Mol Cell Proteomics 9:11–24

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gstaiger M, Aebersold R (2009) Applying mass spectrometry-based proteomics to genetics, genomics and network biology. Nat Rev Genet 10:617–627

    Article  CAS  PubMed  Google Scholar 

  • Harrington ED, Jensen LJ, Bork P (2008) Predicting biological networks from genomic data. FEBS Lett 582:1251–1258

    Article  CAS  PubMed  Google Scholar 

  • Havugimana PC, Hart GT, Nepusz T, Yang H, Turinsky AL, Li Z, Wang PI, Boutz DR, Fong V, Phanse S, Babu M, Craig SA, Hu P, Wan C, Vlasblom J, Dar V-N, Bezginov A, Clark GW, Wu GC, Wodak SJ, Tillier ERM, Paccanaro A, Marcotte EM, Emili A (2012) A census of human soluble protein complexes. Cell 150:1068–1081

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hayat S, Walter P, Park Y, Helms V (2011) Prediction of the exposure status of transmembrane beta barrel residues from protein sequence. J Bioinform Comput Biol 9:43–65

    Article  CAS  PubMed  Google Scholar 

  • Hopkins AL (2008) Network pharmacology: the next paradigm in drug discovery. Nat Chem Biol 4:682–690

    Article  CAS  PubMed  Google Scholar 

  • Hu P, Janga SC, Babu M, Diaz-Mejia JJ, Butland G, Yang W, Pogoutse O, Guo X, Phanse S, Wong P, Chandran S, Christopoulos C, Nazarians-Armavil A, Nasseri NK, Musso G, Ali M, Nazemof N, Eroukova V, Golshani A, Paccanaro A, Greenblatt JF, Moreno-Hagelsieb G, Emili A (2009) Global functional atlas of Escherichia coli encompassing previously uncharacterized proteins. PLoS Biol 7, e96

    Article  PubMed  CAS  Google Scholar 

  • Hughes C, Krijgsveld J (2012) Developments in quantitative mass spectrometry for the analysis of proteome dynamics. Trends Biotechnol 30:668–676

    Article  CAS  PubMed  Google Scholar 

  • Hui S, Silverman JM, Chen SS, Erickson DW, Basan M, Wang J, Hwa T, Williamson JR (2015) Quantitative proteomic analysis reveals a simple strategy of global resource allocation in bacteria. Mol Syst Biol 11:784

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kall L, Vitek O (2011) Computational mass spectrometry-based proteomics. PLoS Comput Biol 7, e1002277

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kanj SS, Kanafani ZA (2011) Current concepts in antimicrobial therapy against resistant gram-negative organisms: extended-spectrum beta-lactamase-producing Enterobacteriaceae, carbapenem-resistant Enterobacteriaceae, and multidrug-resistant Pseudomonas aeruginosa. Mayo Clin Proc 86:250–259

    Article  PubMed Central  PubMed  Google Scholar 

  • Kawashima S, Pokarowski P, Pokarowska M, Kolinski A, Katayama T, Kanehisa M (2008) AAindex: amino acid index database, progress report 2008. Nucleic Acids Res 36:D202–D205

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kerppola TK (2006) Visualization of molecular interactions by fluorescence complementation. Nat Rev Mol Cell Biol 7:449–456

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Khan I, Chen Y, Dong T, Hong X, Takeuchi R, Mori H, Kihara D (2014) Genome-scale identification and characterization of moonlighting proteins. Biol Direct 9:30

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Koch EN, Costanzo M, Bellay J, Deshpande R, Chatfield-Reed K, Chua G, D’Urso G, Andrews BJ, Boone C, Myers CL (2012) Conserved rules govern genetic interaction degree across species. Genome Biol 13:R57

    Article  PubMed Central  PubMed  Google Scholar 

  • Kohanski MA, Dwyer DJ, Collins JJ (2010) How antibiotics kill bacteria: from targets to networks. Nat Rev Microbiol 8:423–435

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kotlyar M, Pastrello C, Pivetta F, Lo Sardo A, Cumbaa C, Li H, Naranian T, Niu Y, Ding Z, Vafaee F, Broackes-Carter F, Petschnigg J, Mills GB, Jurisicova A, Stagljar I, Maestro R, Jurisica I (2015) In silico prediction of physical protein interactions and characterization of interactome orphans. Nat Methods 12:79–84

    Article  CAS  PubMed  Google Scholar 

  • Kuzmanov U, Emili A (2013) Protein–protein interaction networks: probing disease mechanisms using model systems. Genome Med 5:37

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lam MH, Stagljar I (2012) Strategies for membrane interaction proteomics: no mass spectrometry required. Proteomics 12:1519–1526

    Article  CAS  PubMed  Google Scholar 

  • Lee D, Redfern O, Orengo C (2007) Predicting protein function from sequence and structure. Nat Rev Mol Cell Biol 8:995–1005

    Article  CAS  PubMed  Google Scholar 

  • Lee SY, Yun SH, Lee YG, Choi CW, Leem SH, Park EC, Kim GH, Lee JC, Kim SI (2014) Proteogenomic characterization of antimicrobial resistance in extensively drug-resistant Acinetobacter baumannii DU202. J Antimicrob Chemother 69:1483–1491

    Article  CAS  PubMed  Google Scholar 

  • Liebler DC, Zimmerman LJ (2013) Targeted quantitation of proteins by mass spectrometry. Biochemistry 52:3797–3806

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lima TB, Pinto MF, Ribeiro SM, de Lima LA, Viana JC, Gomes Junior N, Candido Ede S, Dias SC, Franco OL (2013) Bacterial resistance mechanism: what proteomics can elucidate. FASEB J 27:1291–1303

    Article  CAS  PubMed  Google Scholar 

  • Mills CL, Beuning PJ, Ondrechen MJ (2015) Biochemical functional predictions for protein structures of unknown or uncertain function. Comput Struct Biotechnol J 13:182–191

    Article  PubMed Central  PubMed  Google Scholar 

  • Miteva YV, Budayeva HG, Cristea IM (2013) Proteomics-based methods for discovery, quantification, and validation of protein–protein interactions. Anal Chem 85:749–768

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mitra K, Carvunis AR, Ramesh SK, Ideker T (2013) Integrative approaches for finding modular structure in biological networks. Nat Rev Genet 14:719–732

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mosca R, Pache RA, Aloy P (2012) The role of structural disorder in the rewiring of protein interactions through evolution. Mol Cell Proteomics 11:M111.014969

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Needham BD, Trent MS (2013) Fortifying the barrier: the impact of lipid A remodelling on bacterial pathogenesis. Nat Rev Microbiol 11:467–481

    Article  CAS  PubMed  Google Scholar 

  • Ngounou Wetie AG, Sokolowska I, Woods AG, Roy U, Loo JA, Darie CC (2013) Investigation of stable and transient protein–protein interactions: past, present, and future. Proteomics 13:538–557

    Article  CAS  PubMed  Google Scholar 

  • Nichols RJ, Sen S, Choo YJ, Beltrao P, Zietek M, Chaba R, Lee S, Kazmierczak KM, Lee KJ, Wong A, Shales M, Lovett S, Winkler ME, Krogan NJ, Typas A, Gross CA (2011) Phenotypic landscape of a bacterial cell. Cell 144:143–156

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • O’Brien KT, Haslam NJ, Shields DC (2013) SLiMScape: a protein short linear motif analysis plugin for Cytoscape. BMC Bioinformatics 14:224

    Article  PubMed Central  PubMed  Google Scholar 

  • Ozer EA, Fitzpatrick MA, Hauser AR (2014) Draft genome sequence of Acinetobacter baumannii strain ABBL099, a multidrug-resistant clinical outbreak isolate with a novel multilocus sequence type. Genome Announc 2

    Google Scholar 

  • Palopoli N, Lythgow KT, Edwards RJ (2015) QSLiMFinder: improved short linear motif prediction using specific query protein data. Bioinformatics 31:2284–2293

    Article  PubMed Central  PubMed  Google Scholar 

  • Pan JY, Li H, Ma Y, Chen P, Zhao P, Wang SY, Peng XX (2010) Complexome of Escherichia coli envelope proteins under normal physiological conditions. J Proteome Res 9:3730–3740

    Article  CAS  PubMed  Google Scholar 

  • Papanastasiou M, Orfanoudaki G, Koukaki M, Kountourakis N, Sardis MF, Aivaliotis M, Karamanou S, Economou A (2013) The Escherichia coli peripheral inner membrane proteome. Mol Cell Proteomics 12:599–610

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pawar H, Sahasrabuddhe NA, Renuse S, Keerthikumar S, Sharma J, Kumar GS, Venugopal A, Sekhar NR, Kelkar DS, Nemade H, Khobragade SN, Muthusamy B, Kandasamy K, Harsha HC, Chaerkady R, Patole MS, Pandey A (2012) A proteogenomic approach to map the proteome of an unsequenced pathogen – Leishmania donovani. Proteomics 12:832–844

    Article  CAS  PubMed  Google Scholar 

  • Pelletier DA, Hurst GB, Foote LJ, Lankford PK, McKeown CK, Lu TY, Schmoyer DD, Shah MB, Hervey WJt, McDonald WH, Hooker BS, Cannon WR, Daly DS, Gilmore JM, Wiley HS, Auberry DL, Wang Y, Larimer FW, Kennel SJ, Doktycz MJ, Morrell-Falvey JL, Owens ET, Buchanan MV (2008) A general system for studying protein–protein interactions in Gram-negative bacteria. J Proteome Res 7:3319–3328

    Google Scholar 

  • Perica T, Chothia C, Teichmann SA (2012) Evolution of oligomeric state through geometric coupling of protein interfaces. Proc Natl Acad Sci U S A 109:8127–8132

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Petriz BA, Franco OL (2014) Application of cutting-edge proteomics technologies for elucidating host-bacteria interactions. Adv Protein Chem Struct Biol 95:1–24

    Article  CAS  PubMed  Google Scholar 

  • Pogozheva ID, Tristram-Nagle S, Mosberg HI, Lomize AL (2013) Structural adaptations of proteins to different biological membranes. Biochim Biophys Acta 1828:2592–2608

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pujol A, Mosca R, Farres J, Aloy P (2010) Unveiling the role of network and systems biology in drug discovery. Trends Pharmacol Sci 31:115–123

    Article  CAS  PubMed  Google Scholar 

  • Pyndiah S, Lasserre JP, Menard A, Claverol S, Prouzet-Mauleon V, Megraud F, Zerbib F, Bonneu M (2007) Two-dimensional blue native/SDS gel electrophoresis of multiprotein complexes from Helicobacter pylori. Mol Cell Proteomics 6:193–206

    Article  CAS  PubMed  Google Scholar 

  • Qin T, Matmati N, Tsoi LC, Mohanty BK, Gao N, Tang J, Lawson AB, Hannun YA, Zheng WJ (2014) Finding pathway-modulating genes from a novel Ontology Fingerprint-derived gene network. Nucleic Acids Res 42, e138

    Article  PubMed Central  PubMed  Google Scholar 

  • Rabilloud T (2009) Membrane proteins and proteomics: love is possible, but so difficult. Electrophoresis 30(Suppl 1):S174–S180

    Article  PubMed  Google Scholar 

  • Rabilloud T, Lelong C (2011) Two-dimensional gel electrophoresis in proteomics: a tutorial. J Proteomics 74:1829–1841

    Article  CAS  PubMed  Google Scholar 

  • Radosevich TJ, Reinhardt TA, Lippolis JD, Bannantine JP, Stabel JR (2007) Proteome and differential expression analysis of membrane and cytosolic proteins from Mycobacterium avium subsp. paratuberculosis strains K-10 and 187. J Bacteriol 189:1109–1117

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rajagopala SV, Sikorski P, Kumar A, Mosca R, Vlasblom J, Arnold R, Franca-Koh J, Pakala SB, Phanse S, Ceol A, Hauser R, Siszler G, Wuchty S, Emili A, Babu M, Aloy P, Pieper R, Uetz P (2014) The binary protein–protein interaction landscape of Escherichia coli. Nat Biotechnol 32:285–290

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Reddy TB, Thomas AD, Stamatis D, Bertsch J, Isbandi M, Jansson J, Mallajosyula J, Pagani I, Lobos EA, Kyrpides NC (2015) The Genomes OnLine Database (GOLD) v.5: a metadata management system based on a four level (meta)genome project classification. Nucleic Acids Res 43:D1099–D1106

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ribet D, Cossart P (2015) How bacterial pathogens colonize their hosts and invade deeper tissues. Microbes Infect/Institut Pasteur 17:173–183

    Article  CAS  Google Scholar 

  • Riedel T, Bunk B, Thurmer A, Sproer C, Brzuszkiewicz E, Abt B, Gronow S, Liesegang H, Daniel R, Overmann J (2015) Genome resequencing of the virulent and multidrug-resistant reference strain Clostridium difficile 630. Genome Announc 3

    Google Scholar 

  • Ryan CJ, Cimermancic P, Szpiech ZA, Sali A, Hernandez RD, Krogan NJ (2013) High-resolution network biology: connecting sequence with function. Nat Rev Genet 14:865–879

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Salzano AM, Novi G, Arioli S, Corona S, Mora D, Scaloni A (2013) Mono-dimensional blue native-PAGE and bi-dimensional blue native/urea-PAGE or/SDS-PAGE combined with nLC-ESI-LIT-MS/MS unveil membrane protein heteromeric and homomeric complexes in Streptococcus thermophilus. J Proteomics 94:240–261

    Article  CAS  PubMed  Google Scholar 

  • Sauer S, Kliem M (2010) Mass spectrometry tools for the classification and identification of bacteria. Nat Rev Microbiol 8:74–82

    Article  CAS  PubMed  Google Scholar 

  • Schlegel S, Klepsch M, Wickstrom D, Wagner S, de Gier JW (2010) Comparative analysis of cytoplasmic membrane proteomes of Escherichia coli using 2D blue native/SDS-PAGE. Methods Mol Biol 619:257–269

    Article  CAS  PubMed  Google Scholar 

  • Schneider A, Seidl MF, Snel B (2013) Shared protein complex subunits contribute to explaining disrupted co-occurrence. PLoS Comput Biol 9, e1003124

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shui W, Gilmore SA, Sheu L, Liu J, Keasling JD, Bertozzi CR (2009) Quantitative proteomic profiling of host–pathogen interactions: the macrophage response to Mycobacterium tuberculosis lipids. J Proteome Res 8:282–289

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Silhavy TJ, Kahne D, Walker S (2010) The bacterial cell envelope. Cold Spring Harb Perspect Biol 2:a000414

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Stenberg F, Chovanec P, Maslen SL, Robinson CV, Ilag LL, von Heijne G, Daley DO (2005) Protein complexes of the Escherichia coli cell envelope. J Biol Chem 280:34409–34419

    Article  CAS  PubMed  Google Scholar 

  • Tan SY, Chua SL, Chen Y, Rice SA, Kjelleberg S, Nielsen TE, Yang L, Givskov M (2013) Identification of five structurally unrelated quorum-sensing inhibitors of Pseudomonas aeruginosa from a natural-derivative database. Antimicrob Agents Chemother 57:5629–5641

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Taniguchi Y, Choi PJ, Li GW, Chen H, Babu M, Hearn J, Emili A, Xie XS (2010) Quantifying E. coli proteome and transcriptome with single-molecule sensitivity in single cells. Science 329:533–538

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tillier ER, Charlebois RL (2009) The human protein coevolution network. Genome Res 19:1861–1871

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tuncbag N, Gursoy A, Nussinov R, Keskin O (2011) Predicting protein–protein interactions on a proteome scale by matching evolutionary and structural similarities at interfaces using PRISM. Nat Protoc 6:1341–1354

    Article  CAS  PubMed  Google Scholar 

  • van der Lee R, Buljan M, Lang B, Weatheritt RJ, Daughdrill GW, Dunker AK, Fuxreiter M, Gough J, Gsponer J, Jones DT, Kim PM, Kriwacki RW, Oldfield CJ, Pappu RV, Tompa P, Uversky VN, Wright PE, Babu MM (2014) Classification of intrinsically disordered regions and proteins. Chem Rev 114:6589–6631

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Vignaroli C, Luna GM, Rinaldi C, Di Cesare A, Danovaro R, Biavasco F (2012) New sequence types and multidrug resistance among pathogenic Escherichia coli isolates from coastal marine sediments. Appl Environ Microbiol 78:3916–3922

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vlasblom J, Zuberi K, Rodriguez H, Arnold R, Gagarinova A, Deineko V, Kumar A, Leung E, Rizzolo K, Samanfar B, Chang L, Phanse S, Golshani A, Greenblatt JF, Houry WA, Emili A, Morris Q, Bader G, Babu M (2015) Novel function discovery with GeneMANIA: a new integrated resource for gene function prediction in Escherichia coli. Bioinformatics 31:306–310

    Article  PubMed  Google Scholar 

  • Wenzel M, Bandow JE (2011) Proteomic signatures in antibiotic research. Proteomics 11:3256–3268

    Article  CAS  PubMed  Google Scholar 

  • Wong WR, Oliver AG, Linington RG (2012) Development of antibiotic activity profile screening for the classification and discovery of natural product antibiotics. Chem Biol 19:1483–1495

    Article  CAS  PubMed  Google Scholar 

  • Wright PE, Dyson HJ (2015) Intrinsically disordered proteins in cellular signalling and regulation. Nat Rev Mol Cell Biol 16:18–29

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wuchty S, Uetz P (2014) Protein–protein interaction networks of E. coli and S. cerevisiae are similar. Sci Rep 4:7187

    Article  CAS  PubMed  Google Scholar 

  • Ye X, Luke B, Andresson T, Blonder J (2009) 18O stable isotope labeling in MS-based proteomics. Brief Funct Genomic Proteomic 8:136–144

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yildirim MA, Goh KI, Cusick ME, Barabasi AL, Vidal M (2007) Drug-target network. Nat Biotechnol 25:1119–1126

    Article  CAS  PubMed  Google Scholar 

  • Yu H, Braun P, Yildirim MA, Lemmens I, Venkatesan K, Sahalie J, Hirozane-Kishikawa T, Gebreab F, Li N, Simonis N, Hao T, Rual JF, Dricot A, Vazquez A, Murray RR, Simon C, Tardivo L, Tam S, Svrzikapa N, Fan C, de Smet AS, Motyl A, Hudson ME, Park J, Xin X, Cusick ME, Moore T, Boone C, Snyder M, Roth FP, Barabasi AL, Tavernier J, Hill DE, Vidal M (2008) High-quality binary protein interaction map of the yeast interactome network. Science 322:104–110

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yun SH, Choi CW, Kwon SO, Park GW, Cho K, Kwon KH, Kim JY, Yoo JS, Lee JC, Choi JS, Kim S, Kim SI (2011) Quantitative proteomic analysis of cell wall and plasma membrane fractions from multidrug-resistant Acinetobacter baumannii. J Proteome Res 10:459–469

    Article  CAS  PubMed  Google Scholar 

  • Zahedi RP, Moebius J, Sickmann A (2007) Two-dimensional BAC/SDS-PAGE for membrane proteomics. Subcell Biochem 43:13–20

    Article  PubMed  Google Scholar 

  • Zhang QC, Petrey D, Garzon JI, Deng L, Honig B (2013) PrePPI: a structure-informed database of protein–protein interactions. Nucleic Acids Res 41:D828–D833

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zheng J, Wei C, Zhao L, Liu L, Leng W, Li W, Jin Q (2011) Combining blue native polyacrylamide gel electrophoresis with liquid chromatography tandem mass spectrometry as an effective strategy for analyzing potential membrane protein complexes of Mycobacterium bovis bacillus Calmette-Guerin. BMC Genomics 12:40

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported in part by funds from the Natural Sciences and Engineering Research Council of Canada (DG-20234) to MB. JV was supported by a Saskatchewan Postdoctoral Research Fellowship. MB holds a Canadian Institute of Health Research New Investigator award.

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Correspondence to Mohan Babu .

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Deineko, V., Kumar, A., Vlasblom, J., Babu, M. (2015). Quantitative and Systems-Based Approaches for Deciphering Bacterial Membrane Interactome and Gene Function. In: Krogan, PhD, N., Babu, PhD, M. (eds) Prokaryotic Systems Biology. Advances in Experimental Medicine and Biology, vol 883. Springer, Cham. https://doi.org/10.1007/978-3-319-23603-2_8

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