Reconstruction of the temporal signaling network in Salmonella-infected human cells

Salmonella enterica is a bacterial pathogen that usually infects its host through food sources. Translocation of the pathogen proteins into the host cells leads to changes in the signaling mechanism either by activating or inhibiting the host proteins. Given that the bacterial infection modifies the response network of the host, a more coherent view of the underlying biological processes and the signaling networks can be obtained by using a network modeling approach based on the reverse engineering principles. In this work, we have used a published temporal phosphoproteomic dataset of Salmonella-infected human cells and reconstructed the temporal signaling network of the human host by integrating the interactome and the phosphoproteomic dataset. We have combined two well-established network modeling frameworks, the Prize-collecting Steiner Forest (PCSF) approach and the Integer Linear Programming (ILP) based edge inference approach. The resulting network conserves the information on temporality, direction of interactions, while revealing hidden entities in the signaling, such as the SNARE binding, mTOR signaling, immune response, cytoskeleton organization, and apoptosis pathways. Targets of the Salmonella effectors in the host cells such as CDC42, RHOA, 14-3-3δ, Syntaxin family, Oxysterol-binding proteins were included in the reconstructed signaling network although they were not present in the initial phosphoproteomic data. We believe that integrated approaches, such as the one presented here, have a high potential for the identification of clinical targets in infectious diseases, especially in the Salmonella infections.

[1]  A. Maldonado-Contreras,et al.  Salmonella Pathogenesis and Processing of Secreted Effectors by Caspase-3 , 2010, Science.

[2]  Joseph Avruch,et al.  Rheb Binds and Regulates the mTOR Kinase , 2005, Current Biology.

[3]  Y. A. Son,et al.  Reconstruction of the temporal signaling network in Salmonella -infected human cells , 2015 .

[4]  Lars Kaderali,et al.  Dynamic probabilistic threshold networks to infer signaling pathways from time-course perturbation data , 2014, BMC Bioinformatics.

[5]  Reinhard Guthke,et al.  Data- and knowledge-based modeling of gene regulatory networks: an update , 2015, EXCLI journal.

[6]  Christian Borgs,et al.  Simultaneous Reconstruction of Multiple Signaling Pathways via the Prize-Collecting Steiner Forest Problem , 2012, J. Comput. Biol..

[7]  Ernest Fraenkel,et al.  Linking Proteomic and Transcriptional Data through the Interactome and Epigenome Reveals a Map of Oncogene-induced Signaling , 2013, PLoS Comput. Biol..

[8]  L. Bry,et al.  IQGAP1 Regulates Salmonella Invasion through Interactions with Actin, Rac1, and Cdc42* , 2007, Journal of Biological Chemistry.

[9]  Thomas Brendan Murphy,et al.  Review of statistical network analysis: models, algorithms, and software , 2012, Stat. Anal. Data Min..

[10]  R. Nussinov,et al.  Predicting protein-protein interactions on a proteome scale by matching evolutionary and structural similarities at interfaces using PRISM , 2011, Nature Protocols.

[11]  Haiyuan Yu,et al.  INstruct: a database of high-quality 3D structurally resolved protein interactome networks , 2013, Bioinform..

[12]  Michael Hensel,et al.  Salmonella enterica: a surprisingly well-adapted intracellular lifestyle , 2012, Front. Microbio..

[13]  Hidde de Jong,et al.  Modeling and Simulation of Genetic Regulatory Systems: A Literature Review , 2002, J. Comput. Biol..

[14]  Ernest Fraenkel,et al.  SAMNet: a network-based approach to integrate multi-dimensional high throughput datasets. , 2012, Integrative biology : quantitative biosciences from nano to macro.

[15]  M. Kagnoff,et al.  Analysis by High Density cDNA Arrays of Altered Gene Expression in Human Intestinal Epithelial Cells in Response to Infection with the Invasive Enteric BacteriaSalmonella * , 2000, The Journal of Biological Chemistry.

[16]  Cristóbal Fresno,et al.  RDAVIDWebService: a versatile R interface to DAVID , 2013, Bioinform..

[17]  M E J Newman,et al.  Community structure in social and biological networks , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[18]  Ian M. Donaldson,et al.  iRefWeb: interactive analysis of consolidated protein interaction data and their supporting evidence , 2010, Database J. Biol. Databases Curation.

[19]  Lars Kaderali,et al.  lpNet: a linear programming approach to reconstruct signal transduction networks , 2015, Bioinform..

[20]  Tamer Kahveci,et al.  Large-Scale Signaling Network Reconstruction , 2012, IEEE/ACM Transactions on Computational Biology and Bioinformatics.

[21]  Ilya A Vakser,et al.  Protein-protein docking: from interaction to interactome. , 2014, Biophysical journal.

[22]  Tobias Müller,et al.  Identifying functional modules in protein–protein interaction networks: an integrated exact approach , 2008, ISMB.

[23]  W. J. Wu,et al.  Epidermal Growth Factor-dependent Regulation of Cdc42 Is Mediated by the Src Tyrosine Kinase* , 2003, Journal of Biological Chemistry.

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

[25]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[26]  Ozlem Keskin,et al.  Fast and accurate modeling of protein–protein interactions by combining template‐interface‐based docking with flexible refinement , 2012, Proteins.

[27]  P. Shannon,et al.  Cytoscape: a software environment for integrated models of biomolecular interaction networks. , 2003, Genome research.

[28]  G. Shulman,et al.  Syntaxin 4 heterozygous knockout mice develop muscle insulin resistance. , 2001, The Journal of clinical investigation.

[29]  A. Hall,et al.  Rho GTPases and the actin cytoskeleton. , 1998, Science.

[30]  S. Cohen,et al.  Epidermal growth factor , 1972, The Journal of investigative dermatology.

[31]  Haiyuan Yu,et al.  Three-dimensional reconstruction of protein networks provides insight into human genetic disease , 2012, Nature Biotechnology.

[32]  Steffen Klamt,et al.  Detecting and Removing Inconsistencies between Experimental Data and Signaling Network Topologies Using Integer Linear Programming on Interaction Graphs , 2013, PLoS Comput. Biol..

[33]  Alexander Junge,et al.  KeyPathwayMiner 4.0: condition-specific pathway analysis by combining multiple omics studies and networks with Cytoscape , 2014, BMC Systems Biology.

[34]  Illés J. Farkas,et al.  CFinder: locating cliques and overlapping modules in biological networks , 2006, Bioinform..

[35]  Jean-Loup Guillaume,et al.  Fast unfolding of communities in large networks , 2008, 0803.0476.

[36]  Gary D. Bader,et al.  Cytoscape Web: an interactive web-based network browser , 2010, Bioinform..

[37]  S. Auweter,et al.  Oxysterol-binding protein (OSBP) enhances replication of intracellular Salmonella and binds the Salmonella SPI-2 effector SseL via its N-terminus. , 2012, Microbes and infection.

[38]  T. Vicsek,et al.  Uncovering the overlapping community structure of complex networks in nature and society , 2005, Nature.

[39]  B. Finlay,et al.  Cytoskeletal rearrangements accompanying salmonella entry into epithelial cells. , 1991, Journal of cell science.

[40]  Yinglin Xia,et al.  Eukaryotic signaling pathways targeted by Salmonella effector protein AvrA in intestinal infection in vivo , 2010, BMC Microbiology.

[41]  G. Davidson,et al.  Role of SPI-1 Secreted Effectors in Acute Bovine Response to Salmonella enterica Serovar Typhimurium: A Systems Biology Analysis Approach , 2011, PloS one.

[42]  D. Karger,et al.  Bridging high-throughput genetic and transcriptional data reveals cellular responses to alpha-synuclein toxicity , 2009, Nature Genetics.

[43]  Dominique Douguet,et al.  DOCKGROUND system of databases for protein recognition studies: Unbound structures for docking , 2007, Proteins.

[44]  Zhongming Zhao,et al.  The current Salmonella‐host interactome , 2012, Proteomics. Clinical applications.

[45]  M E J Newman,et al.  Finding and evaluating community structure in networks. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

[46]  Sam A. Johnson,et al.  Phosphoproteomics finds its timing , 2004, Nature Biotechnology.

[47]  E. Fraenkel,et al.  Integrating Proteomic, Transcriptional, and Interactome Data Reveals Hidden Components of Signaling and Regulatory Networks , 2009, Science Signaling.

[48]  Brad T. Sherman,et al.  Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources , 2008, Nature Protocols.

[49]  Ozlem Keskin,et al.  Towards inferring time dimensionality in protein–protein interaction networks by integrating structures: the p53 example† †This article is part of a Molecular BioSystems themed issue on Computational and Systems Biology. , 2009, Molecular bioSystems.

[50]  Zhiping Weng,et al.  Evaluating template-based and template-free protein-protein complex structure prediction , 2014, Briefings Bioinform..

[51]  S. Khaitlina Functional specificity of actin isoforms. , 2001, International review of cytology.

[52]  Christian Borgs,et al.  Finding undetected protein associations in cell signaling by belief propagation , 2010, Proceedings of the National Academy of Sciences.

[53]  M. Yaffe,et al.  Bacteria‐generated PtdIns(3)P Recruits VAMP8 to Facilitate Phagocytosis , 2007, Traffic.

[54]  Tolga Can,et al.  A Divide and Conquer Approach for Construction of Large-Scale Signaling Networks from PPI and RNAi Data Using Linear Programming , 2013, IEEE/ACM Transactions on Computational Biology and Bioinformatics.

[55]  Takeshi Kawabata,et al.  HOMCOS: a server to predict interacting protein pairs and interacting sites by homology modeling of complex structures , 2008, Nucleic Acids Res..

[56]  O. Keskin,et al.  Predicting Protein-Protein Interactions from the Molecular to the Proteome Level. , 2016, Chemical reviews.

[57]  F. Koch-Nolte,et al.  Actin is ADP‐ribosylated by the Salmonella enterica virulence‐associated protein SpvB , 2001, Molecular microbiology.

[58]  Bernhard O. Palsson,et al.  Constraint-based analysis of metabolic capacity of Salmonella typhimurium during host-pathogen interaction , 2009, BMC Systems Biology.

[59]  Yves Deville,et al.  NeAT: a toolbox for the analysis of biological networks, clusters, classes and pathways , 2008, Nucleic Acids Res..

[60]  Teresa M. Przytycka,et al.  Identifying Causal Genes and Dysregulated Pathways in Complex Diseases , 2011, PLoS Comput. Biol..

[61]  Sergey Nepomnyachiy,et al.  CyToStruct: Augmenting the Network Visualization of Cytoscape with the Power of Molecular Viewers. , 2015, Structure.

[62]  Leon Danon,et al.  Comparing community structure identification , 2005, cond-mat/0505245.

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

[64]  M. Collins,et al.  Analysis of protein phosphorylation on a proteome‐scale , 2007, Proteomics.

[65]  Ronald C. Taylor,et al.  A Network Inference Workflow Applied to Virulence‐Related Processes in Salmonella typhimurium , 2009, Annals of the New York Academy of Sciences.

[66]  Michael Hecker,et al.  Gene regulatory network inference: Data integration in dynamic models - A review , 2009, Biosyst..

[67]  Holger Fröhlich,et al.  Deterministic Effects Propagation Networks for reconstructing protein signaling networks from multiple interventions , 2009, BMC Bioinformatics.

[68]  O. Steele‐Mortimer Exploitation of the Ubiquitin System by Invading Bacteria , 2011, Traffic.

[69]  P. Aloy,et al.  Interactome3D: adding structural details to protein networks , 2013, Nature Methods.

[70]  Conrad C. Huang,et al.  UCSF Chimera—A visualization system for exploratory research and analysis , 2004, J. Comput. Chem..

[71]  Harri Lähdesmäki,et al.  Sorad: a systems biology approach to predict and modulate dynamic signaling pathway response from phosphoproteome time-course measurements , 2013, Bioinform..

[72]  C. Borgs,et al.  Simultaneous Reconstruction of Multiple Signaling Pathways via the Prize-Collecting Steiner Forest Problem , 2012, J. Comput. Biol..

[73]  Olga G. Troyanskaya,et al.  Nested effects models for high-dimensional phenotyping screens , 2007, ISMB/ECCB.

[74]  J. Galán,et al.  Striking a balance: modulation of the actin cytoskeleton by Salmonella. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[75]  Reinhard Schneider,et al.  Using graph theory to analyze biological networks , 2011, BioData Mining.

[76]  Pornpimol Charoentong,et al.  ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks , 2009, Bioinform..

[77]  Sudipto Saha,et al.  Dynamic Modularity of Host Protein Interaction Networks in Salmonella Typhi Infection , 2014, PloS one.

[78]  Damian Szklarczyk,et al.  STRING v9.1: protein-protein interaction networks, with increased coverage and integration , 2012, Nucleic Acids Res..

[79]  F. Ramos-Morales Impact of Salmonella enterica Type III Secretion System Effectors on the Eukaryotic Host Cell , 2012 .

[80]  Holger Fröhlich,et al.  Dynamic deterministic effects propagation networks: learning signalling pathways from longitudinal protein array data , 2010, Bioinform..

[81]  Brad T. Sherman,et al.  DAVID-WS: a stateful web service to facilitate gene/protein list analysis , 2012, Bioinform..

[82]  J. Skolnick,et al.  Structural space of protein–protein interfaces is degenerate, close to complete, and highly connected , 2010, Proceedings of the National Academy of Sciences.

[83]  A. Califano,et al.  Dialogue on Reverse‐Engineering Assessment and Methods , 2007, Annals of the New York Academy of Sciences.

[84]  J. Galán,et al.  Salmonella Modulation of Host Cell Gene Expression Promotes Its Intracellular Growth , 2013, PLoS pathogens.

[85]  Lars Kaderali,et al.  Reconstruction of Cellular Signal Transduction Networks Using Perturbation Assays and Linear Programming , 2013, PloS one.

[86]  Leonard J Foster,et al.  Phosphoproteomic Analysis of Salmonella-Infected Cells Identifies Key Kinase Regulators and SopB-Dependent Host Phosphorylation Events , 2011, Science Signaling.

[87]  Hyunjin Yoon,et al.  Coordinated Regulation of Virulence during Systemic Infection of Salmonella enterica Serovar Typhimurium , 2009, PLoS pathogens.

[88]  C. Lee,et al.  Salmonella induce autophagy in melanoma by the downregulation of AKT/mTOR pathway , 2014, Gene Therapy.