A proteome-wide protein interaction map for Campylobacter jejuni

BackgroundData from large-scale protein interaction screens for humans and model eukaryotes have been invaluable for developing systems-level models of biological processes. Despite this value, only a limited amount of interaction data is available for prokaryotes. Here we report the systematic identification of protein interactions for the bacterium Campylobacter jejuni, a food-borne pathogen and a major cause of gastroenteritis worldwide.ResultsUsing high-throughput yeast two-hybrid screens we detected and reproduced 11,687 interactions. The resulting interaction map includes 80% of the predicted C. jejuni NCTC11168 proteins and places a large number of poorly characterized proteins into networks that provide initial clues about their functions. We used the map to identify a number of conserved subnetworks by comparison to protein networks from Escherichia coli and Saccharomyces cerevisiae. We also demonstrate the value of the interactome data for mapping biological pathways by identifying the C. jejuni chemotaxis pathway. Finally, the interaction map also includes a large subnetwork of putative essential genes that may be used to identify potential new antimicrobial drug targets for C. jejuni and related organisms.ConclusionThe C. jejuni protein interaction map is one of the most comprehensive yet determined for a free-living organism and nearly doubles the binary interactions available for the prokaryotic kingdom. This high level of coverage facilitates pathway mapping and function prediction for a large number of C. jejuni proteins as well as orthologous proteins from other organisms. The broad coverage also facilitates cross-species comparisons for the identification of evolutionarily conserved subnetworks of protein interactions.

[1]  P. McCullagh,et al.  Generalized Linear Models , 1972, Predictive Analytics.

[2]  S. Lovett,et al.  Genetic analysis of the recJ gene of Escherichia coli K-12 , 1984, Journal of bacteriology.

[3]  Identification and purification of a single-stranded-DNA-specific exonuclease encoded by the recJ gene of Escherichia coli. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[4]  D E Koshland,et al.  Identification of the site of phosphorylation of the chemotaxis response regulator protein, CheY. , 1989, The Journal of biological chemistry.

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

[6]  P. McCullagh,et al.  Generalized Linear Models, 2nd Edn. , 1990 .

[7]  P. Laine,et al.  The single-stranded DNA-binding protein of Escherichia coli. , 1990, Microbiological reviews.

[8]  Roger Brent,et al.  C dil, a Human Gl and S Phase Protein Phosphatase That Associates with Cdk2 , 2003 .

[9]  M Welch,et al.  Phosphorylation-dependent binding of a signal molecule to the flagellar switch of bacteria. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[10]  A. Varshavsky,et al.  Split ubiquitin as a sensor of protein interactions in vivo. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[11]  N. W. Davis,et al.  The complete genome sequence of Escherichia coli K-12. , 1997, Science.

[12]  M. Blaser,et al.  Epidemiologic and clinical features of Campylobacter jejuni infections. , 1997, The Journal of infectious diseases.

[13]  D. Ladant,et al.  A bacterial two-hybrid system based on a reconstituted signal transduction pathway. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[14]  D. Whelan,et al.  THE PROMISE ( AND PERIL ) , 2017 .

[15]  B. Barrell,et al.  The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences , 2000, Nature.

[16]  James R. Knight,et al.  A comprehensive analysis of protein–protein interactions in Saccharomyces cerevisiae , 2000, Nature.

[17]  Marc Vidal,et al.  Yeast Two-hybrid Systems and Protein Interaction Mapping Projects for Yeast and Worm , 2022 .

[18]  B. Schwikowski,et al.  A network of protein–protein interactions in yeast , 2000, Nature Biotechnology.

[19]  Ioannis Xenarios,et al.  DIP: the Database of Interacting Proteins , 2000, Nucleic Acids Res..

[20]  M. Ashburner,et al.  Gene Ontology: tool for the unification of biology , 2000, Nature Genetics.

[21]  T. Ito,et al.  Toward a protein-protein interaction map of the budding yeast: A comprehensive system to examine two-hybrid interactions in all possible combinations between the yeast proteins. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Hideyuki Suzuki,et al.  Aminopeptidases A, B, and N and Dipeptidase D Are the Four Cysteinylglycinases of Escherichia coliK-12 , 2001, Journal of bacteriology.

[23]  A. Barabasi,et al.  Lethality and centrality in protein networks , 2001, Nature.

[24]  S. Lovett,et al.  In vivo requirement for RecJ, ExoVII, ExoI, and ExoX in methyl-directed mismatch repair , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[25]  J. Wojcik,et al.  The protein–protein interaction map of Helicobacter pylori , 2001, Nature.

[26]  R. Ozawa,et al.  A comprehensive two-hybrid analysis to explore the yeast protein interactome , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[27]  V. DiRita,et al.  Transposon mutagenesis of Campylobacter jejuni identifies a bipartite energy taxis system required for motility , 2001, Molecular microbiology.

[28]  Gary D Bader,et al.  Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry , 2002, Nature.

[29]  B. Wren,et al.  Exploiting genome sequence: predictions for mechanisms of Campylobacter chemotaxis. , 2002, Trends in microbiology.

[30]  C. T. Lauhon.  Requirement for IscS in Biosynthesis of All Thionucleosides in Escherichia coli , 2002, Journal of bacteriology.

[31]  Yoshihide Hayashizaki,et al.  Interaction generality, a measurement to assess the reliability of a protein-protein interaction. , 2002, Nucleic acids research.

[32]  R. Finley,et al.  Regulated expression of proteins in yeast using the MAL61-62 promoter and a mating scheme to increase dynamic range. , 2002, Gene.

[33]  P. Bork,et al.  Functional organization of the yeast proteome by systematic analysis of protein complexes , 2002, Nature.

[34]  Jian Zhang,et al.  The Protein Information Resource: an integrated public resource of functional annotation of proteins , 2002, Nucleic Acids Res..

[35]  B. Snel,et al.  Comparative assessment of large-scale data sets of protein–protein interactions , 2002, Nature.

[36]  Pierre Legrain,et al.  Prediction, assessment and validation of protein interaction maps in bacteria. , 2002, Journal of molecular biology.

[37]  L. Claret,et al.  The FliS chaperone selectively binds the disordered flagellin C-terminal D0 domain central to polymerisation. , 2003, FEMS microbiology letters.

[38]  S. Ehrlich,et al.  Essential Bacillus subtilis genes , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[39]  Matthew Pokross,et al.  Similar modes of polypeptide recognition by export chaperones in flagellar biosynthesis and type III secretion , 2003, Nature Structural Biology.

[40]  James R. Knight,et al.  A Protein Interaction Map of Drosophila melanogaster , 2003, Science.

[41]  D. Goldberg,et al.  Assessing experimentally derived interactions in a small world , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[42]  Steen Knudsen,et al.  GenePublisher: automated analysis of DNA microarray data , 2003, Nucleic Acids Res..

[43]  Gerard Tromp,et al.  A strategy for constructing large protein interaction maps using the yeast two-hybrid system: regulated expression arrays and two-phase mating. , 2003, Genome research.

[44]  M. Gerstein,et al.  A Bayesian Networks Approach for Predicting Protein-Protein Interactions from Genomic Data , 2003, Science.

[45]  Jianjun Li,et al.  The crucial role of Campylobacter jejuni genes in anti-ganglioside antibody induction in Guillain-Barre syndrome. , 2004, The Journal of clinical investigation.

[46]  S. L. Wong,et al.  A Map of the Interactome Network of the Metazoan C. elegans , 2004, Science.

[47]  Matteo Pellegrini,et al.  Prolinks: a database of protein functional linkages derived from coevolution , 2004, Genome Biology.

[48]  L. A. Ward,et al.  FlaC, a protein of Campylobacter jejuni TGH9011 (ATCC43431) secreted through the flagellar apparatus, binds epithelial cells and influences cell invasion , 2004, Molecular microbiology.

[49]  Julie A. Hines,et al.  High-throughput cloning of Campylobacter jejuni ORfs by in vivo recombination in Escherichia coli. , 2004, Journal of proteome research.

[50]  Zhang-Zhi Hu,et al.  The iProClass integrated database for protein functional analysis , 2004, Comput. Biol. Chem..

[51]  J. Rothberg,et al.  Gaining confidence in high-throughput protein interaction networks , 2004, Nature Biotechnology.

[52]  Kara Dolinski,et al.  Saccharomyces Genome Database (SGD) provides tools to identify and analyze sequences from Saccharomyces cerevisiae and related sequences from other organisms , 2004, Nucleic Acids Res..

[53]  Bernardo A Mangiola,et al.  A Drosophila protein-interaction map centered on cell-cycle regulators , 2004, Genome Biology.

[54]  O. Lortholary,et al.  Immunoproliferative small intestinal disease associated with Campylobacter jejuni. , 2012, Digestive and liver disease : official journal of the Italian Society of Gastroenterology and the Italian Association for the Study of the Liver.

[55]  S. Fields.  High‐throughput two‐hybrid analysis , 2005, The FEBS journal.

[56]  David A Rasko,et al.  Major Structural Differences and Novel Potential Virulence Mechanisms from the Genomes of Multiple Campylobacter Species , 2005, PLoS biology.

[57]  M. Vidal,et al.  Interactome: gateway into systems biology. , 2005, Human molecular genetics.

[58]  J. Doyle,et al.  Some protein interaction data do not exhibit power law statistics , 2005, FEBS letters.

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

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

[61]  Farshad Fotouhi,et al.  A database and tool, IM Browser, for exploring and integrating emerging gene and protein interaction data for Drosophila , 2006, BMC Bioinformatics.

[62]  J. Poehlsgaard,et al.  The bacterial ribosome as a target for antibiotics , 2005, Nature Reviews Microbiology.

[63]  R. Chanet,et al.  Protein interaction mapping: a Drosophila case study. , 2005, Genome research.

[64]  S. Lovett,et al.  RecJ exonuclease: substrates, products and interaction with SSB , 2006, Nucleic acids research.

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

[66]  Bonnie L. Bassler,et al.  Bacterial Small-Molecule Signaling Pathways , 2006, Science.

[67]  T. Ideker,et al.  Comprehensive curation and analysis of global interaction networks in Saccharomyces cerevisiae , 2006, Journal of biology.

[68]  Jodi R Parrish,et al.  Yeast two-hybrid contributions to interactome mapping. , 2006, Current opinion in biotechnology.

[69]  Sean R. Collins,et al.  Global landscape of protein complexes in the yeast Saccharomyces cerevisiae , 2006, Nature.

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

[71]  K. N. Chandrika,et al.  Analysis of the human protein interactome and comparison with yeast, worm and fly interaction datasets , 2006, Nature Genetics.

[72]  H. Mori,et al.  Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection , 2006, Molecular systems biology.

[73]  Farshad Fotouhi,et al.  Automated Segmentation and Classification of High Throughput Yeast Assay Spots , 2007, IEEE Transactions on Medical Imaging.