The binary protein-protein interaction landscape of Escherichia coli

Efforts to map the Escherichia coli interactome have identified several hundred macromolecular complexes, but direct binary protein-protein interactions (PPIs) have not been surveyed on a large scale. Here we performed yeast two-hybrid screens of 3,305 baits against 3,606 preys (∼70% of the E. coli proteome) in duplicate to generate a map of 2,234 interactions, which approximately doubles the number of known binary PPIs in E. coli. Integration of binary PPI and genetic-interaction data revealed functional dependencies among components involved in cellular processes, including envelope integrity, flagellum assembly and protein quality control. Many of the binary interactions that we could map in multiprotein complexes were informative regarding internal topology of complexes and indicated that interactions in complexes are substantially more conserved than those interactions connecting different complexes. This resource will be useful for inferring bacterial gene function and provides a draft reference of the basic physical wiring network of this evolutionarily important model microbe.

[1]  J. Beckwith,et al.  E. coli mutant pleiotropically defective in the export of secreted proteins , 1981, Cell.

[2]  Joseph Christmas,et al.  The Decade and beyond , 1991 .

[3]  T. N. Bhat,et al.  The Protein Data Bank , 2000, Nucleic Acids Res..

[4]  M. Vidal,et al.  Identification of potential interaction networks using sequence-based searches for conserved protein-protein interactions or "interologs". , 2001, Genome research.

[5]  Christian E. V. Storm,et al.  Automatic clustering of orthologs and in-paralogs from pairwise species comparisons. , 2001, Journal of molecular biology.

[6]  P. Bork,et al.  Structure-Based Assembly of Protein Complexes in Yeast , 2004, Science.

[7]  Adam J. Smith,et al.  The Database of Interacting Proteins: 2004 update , 2004, Nucleic Acids Res..

[8]  Dale B. Wigley,et al.  Crystal structure of RecBCD enzyme reveals a machine for processing DNA breaks , 2004, Nature.

[9]  Patrick Aloy,et al.  Ten thousand interactions for the molecular biologist , 2004, Nature Biotechnology.

[10]  Marc Vidal,et al.  Increasing specificity in high-throughput yeast two-hybrid experiments. , 2004, Methods.

[11]  Natasa Przulj,et al.  High-Throughput Mapping of a Dynamic Signaling Network in Mammalian Cells , 2005, Science.

[12]  R. Karp,et al.  From the Cover : Conserved patterns of protein interaction in multiple species , 2005 .

[13]  A. Emili,et al.  Interaction network containing conserved and essential protein complexes in Escherichia coli , 2005, Nature.

[14]  S. L. Wong,et al.  Towards a proteome-scale map of the human protein–protein interaction network , 2005, Nature.

[15]  S. Kanaya,et al.  Large-scale identification of protein-protein interaction of Escherichia coli K-12. , 2006, Genome research.

[16]  B. Berger,et al.  Herpesviral Protein Networks and Their Interaction with the Human Proteome , 2006, Science.

[17]  J. Vandenhaute,et al.  Gateway-Based Destination Vectors for Functional Analyses of Bacterial ORFeomes: Application to the Min System in Brucella abortus , 2006, Applied and Environmental Microbiology.

[18]  Jacques van Helden,et al.  Evaluation of clustering algorithms for protein-protein interaction networks , 2006, BMC Bioinformatics.

[19]  P. Bork,et al.  Proteome survey reveals modularity of the yeast cell machinery , 2006, Nature.

[20]  H. Bussey,et al.  Exploring genetic interactions and networks with yeast , 2007, Nature Reviews Genetics.

[21]  Johannes Goll,et al.  The protein network of bacterial motility , 2007 .

[22]  Gary D Bader,et al.  BMC Biology BioMed Central , 2007 .

[23]  Peter Woollard,et al.  The minimum information required for reporting a molecular interaction experiment (MIMIx) , 2007, Nature Biotechnology.

[24]  Grant W. Brown,et al.  Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map , 2007, Nature.

[25]  Philip S. Yu,et al.  A new method to measure the semantic similarity of GO terms , 2007, Bioinform..

[26]  Aric Hagberg,et al.  Exploring Network Structure, Dynamics, and Function using NetworkX , 2008, Proceedings of the Python in Science Conference.

[27]  Jeremiah J. Faith,et al.  Many Microbe Microarrays Database: uniformly normalized Affymetrix compendia with structured experimental metadata , 2007, Nucleic Acids Res..

[28]  Trey Ideker,et al.  Functional Maps of Protein Complexes from Quantitative Genetic Interaction Data , 2008, PLoS Comput. Biol..

[29]  Peter Uetz,et al.  MPIDB: the microbial protein interaction database , 2008, Bioinform..

[30]  P. Uetz,et al.  The Binary Protein Interactome of Treponema pallidum – The Syphilis Spirochete , 2008, PloS one.

[31]  Johannes Goll,et al.  MPI-LIT: a literature-curated dataset of microbial binary protein--protein interactions , 2008, Bioinform..

[32]  Andrew Emili,et al.  eSGA: E. coli Synthetic Genetic Array analysis , 2008 .

[33]  A. Barabasi,et al.  High-Quality Binary Protein Interaction Map of the Yeast Interactome Network , 2008, Science.

[34]  Julie M. Sahalie,et al.  An experimentally derived confidence score for binary protein-protein interactions , 2008, Nature Methods.

[35]  Peter Uetz,et al.  Improving the yeast two-hybrid system with permutated fusions proteins: the Varicella Zoster Virus interactome , 2010, Proteome Science.

[36]  B. Andrews,et al.  Systematic mapping of genetic interaction networks. , 2009, Annual review of genetics.

[37]  Zhao Xu,et al.  CVTree update: a newly designed phylogenetic study platform using composition vectors and whole genomes , 2009, Nucleic Acids Res..

[38]  A. Emili,et al.  Global Functional Atlas of Escherichia coli Encompassing Previously Uncharacterized Proteins , 2009, PLoS biology.

[39]  Albert-László Barabási,et al.  Scale-Free Networks: A Decade and Beyond , 2009, Science.

[40]  A. Barabasi,et al.  An empirical framework for binary interactome mapping , 2008, Nature Methods.

[41]  Nevan J. Krogan,et al.  Quantitative Genetic Interactions Reveal Biological Modularity , 2010, Cell.

[42]  Ben M. Webb,et al.  Integrative Structure Modeling of Macromolecular Assemblies from Proteomics Data* , 2010, Molecular & Cellular Proteomics.

[43]  Peter Uetz,et al.  Exhaustive benchmarking of the yeast two-hybrid system , 2010, Nature Methods.

[44]  Peter Uetz,et al.  The Escherichia coli K-12 ORFeome: a resource for comparative molecular microbiology , 2010, BMC Genomics.

[45]  Waldemar Vollmer,et al.  Regulation of peptidoglycan synthesis by outer membrane proteins , 2010, Cell.

[46]  Gary D Bader,et al.  The Genetic Landscape of a Cell , 2010, Science.

[47]  A. Emili,et al.  Genetic Interaction Maps in Escherichia coli Reveal Functional Crosstalk among Cell Envelope Biogenesis Pathways , 2011, PLoS genetics.

[48]  N. Krogan,et al.  Phenotypic Landscape of a Bacterial Cell , 2011, Cell.

[49]  Gary D. Bader,et al.  The Biomolecular Interaction Network Database in PSI-MI 2.5 , 2011, Database J. Biol. Databases Curation.

[50]  G. Cingolani,et al.  Structure of the ATP synthase catalytic complex (F1) from Escherichia coli in an auto-inhibited conformation , 2011, Nature Structural &Molecular Biology.

[51]  Peter Uetz,et al.  Analysis of protein-protein interactions using high-throughput yeast two-hybrid screens. , 2011, Methods in molecular biology.

[52]  Shelby L. Bidwell,et al.  Corrigendum: Protein interaction data curation: the International Molecular Exchange (IMEx) consortium , 2012, Nature Methods.

[53]  Livia Perfetto,et al.  MINT, the molecular interaction database: 2012 update , 2011, Nucleic Acids Res..

[54]  Peter Uetz,et al.  Studying protein complexes by the yeast two-hybrid system. , 2012, Methods.

[55]  P. Braun.  Interactome mapping for analysis of complex phenotypes: Insights from benchmarking binary interaction assays , 2012, Proteomics.

[56]  Vladimir Makarenkov,et al.  T-REX: a web server for inferring, validating and visualizing phylogenetic trees and networks , 2012, Nucleic Acids Res..

[57]  Rafael C. Jimenez,et al.  The IntAct molecular interaction database in 2012 , 2011, Nucleic Acids Res..

[58]  Johannes Goll,et al.  Protein interaction data curation: the International Molecular Exchange (IMEx) consortium , 2012, Nature Methods.

[59]  Jingwen Zhou,et al.  Protein quality control acts on folding intermediates to shape the effects of mutations on organismal fitness. , 2013, Molecular cell.

[60]  Philip M. Kim,et al.  Quantitative Genome-Wide Genetic Interaction Screens Reveal Global Epistatic Relationships of Protein Complexes in Escherichia coli , 2014, PLoS genetics.