2021
RNA chaperone activates Salmonella virulence program during infection
Choi J, Salvail H, Groisman EA. RNA chaperone activates Salmonella virulence program during infection. Nucleic Acids Research 2021, 49: 11614-11628. PMID: 34751407, PMCID: PMC8599858, DOI: 10.1093/nar/gkab992.Peer-Reviewed Original ResearchConceptsPhoP activationVirulence regulator PhoPWild-type virulenceBacterium Salmonella enterica serovar TyphimuriumWild-type S. typhimuriumSalmonella enterica serovar TyphimuriumRNA chaperonesEnterica serovar TyphimuriumRegulator PhoPRedundant proteinsMutant behavesVirulence programVirulence roleS. typhimuriumInside macrophagesSecondary structureSerovar TyphimuriumCritical functionsVirulence genesChaperonesPhoPMutantsRibosomesOrganismsCSPCHow the PhoP/PhoQ System Controls Virulence and Mg2+ Homeostasis: Lessons in Signal Transduction, Pathogenesis, Physiology, and Evolution
Groisman EA, Duprey A, Choi J. How the PhoP/PhoQ System Controls Virulence and Mg2+ Homeostasis: Lessons in Signal Transduction, Pathogenesis, Physiology, and Evolution. Microbiology And Molecular Biology Reviews 2021, 85: 10.1128/mmbr.00176-20. PMID: 34191587, PMCID: PMC8483708, DOI: 10.1128/mmbr.00176-20.Peer-Reviewed Original ResearchConceptsPhoP/PhoQ systemPhoP/PhoQSignal transductionAbundance of hundredsGram-negative bacterial speciesTwo-component systemSalmonella enterica serovar TyphimuriumRegulatory RNAsEnterica serovar TyphimuriumTranscription factorsProtease regulatorsTranscriptional effectsCationic antimicrobial peptidesInducing conditionsBacterial speciesSerovar TyphimuriumPhysiological consequencesAntimicrobial peptidesPhoQTransductionVirulenceHomeostasisAbundanceNovel formPhoPLow Cytoplasmic Magnesium Increases the Specificity of the Lon and ClpAP Proteases
Yeom J, Groisman EA. Low Cytoplasmic Magnesium Increases the Specificity of the Lon and ClpAP Proteases. Journal Of Bacteriology 2021, 203: 10.1128/jb.00143-21. PMID: 33941609, PMCID: PMC8223949, DOI: 10.1128/jb.00143-21.Peer-Reviewed Original ResearchConceptsBacterium Salmonella enterica serovar TyphimuriumCytoplasmic MgSalmonella enterica serovar TyphimuriumLon substratesClpAP proteaseEnterica serovar TyphimuriumAntibiotic persistenceEnteric bacteriaSerovar TyphimuriumSpectrum of substratesPhoP proteinProtease LonAcetyl coenzyme ATranscriptional regulatorsProtein bindsPhoP boxRegulatory proteinsProtease specificityPromoter regionCritical regulatorProtein synthesisLiving cellsLonPhoPEscherichia coli
2018
Reduction in adaptor amounts establishes degradation hierarchy among protease substrates
Yeom J, Gao X, Groisman EA. Reduction in adaptor amounts establishes degradation hierarchy among protease substrates. Proceedings Of The National Academy Of Sciences Of The United States Of America 2018, 115: e4483-e4492. PMID: 29686082, PMCID: PMC5948988, DOI: 10.1073/pnas.1722246115.Peer-Reviewed Original ResearchConceptsRegulatory protein PhoPATP-dependent proteaseCritical cellular processesExpression of genesCellular processesAntibiotic persistersCytoplasmic MgProtease substratesUvrYDifferential stabilityProteasePhoPPhysiological conditionsGenesAdaptorAbundanceUnfoldaseFtsATranscriptionSubunitsSubstrateProteolysisVirulenceProteinBinds
2017
Sequestration from Protease Adaptor Confers Differential Stability to Protease Substrate
Yeom J, Wayne KJ, Groisman EA. Sequestration from Protease Adaptor Confers Differential Stability to Protease Substrate. Molecular Cell 2017, 66: 234-246.e5. PMID: 28431231, PMCID: PMC5424706, DOI: 10.1016/j.molcel.2017.03.009.Peer-Reviewed Original ResearchMeSH KeywordsAmino Acid SequenceBacterial ProteinsBinding, CompetitiveCation Transport ProteinsEndopeptidase ClpGene Expression Regulation, BacterialHalf-LifeModels, MolecularMutationProtein BindingProtein Interaction Domains and MotifsProtein StabilityProteolysisSalmonella typhimuriumStructure-Activity RelationshipSubstrate SpecificityTime FactorsTranscription, GeneticConceptsN-terminal residuesSpecific N-terminal residuesRegulatory protein PhoPN-end ruleProtease ClpAPTemporal transcriptionMgtC geneN-terminusPhoPSpecific substratesClpAPDifferential stabilityProtein levelsGenesMgtCResiduesTranscriptionTerminusProteolysisProteinSubstrateProteaseBacteriaDegradationSequestration
2013
Signal‐specific temporal response by the Salmonella PhoP/PhoQ regulatory system
Park S, Groisman EA. Signal‐specific temporal response by the Salmonella PhoP/PhoQ regulatory system. Molecular Microbiology 2013, 91: 135-144. PMID: 24256574, PMCID: PMC3890429, DOI: 10.1111/mmi.12449.Peer-Reviewed Original ResearchConceptsTransporter MgtATwo-component systems PhoP/PhoQPhoP-dependent genesAntimicrobial peptide C18G.PhoP/PhoQSalmonella enterica serovar TyphimuriumSensor PhoQEnterica serovar TyphimuriumVirulence functionsRepressing signalsGene setsPhoQMgtAGenesSerovar TyphimuriumElicit expressionPeriplasmPhoPActive formFull transcriptionExpressionPhoQ.TranscriptionCytoplasmicProtein
2012
The promoter architectural landscape of the Salmonella PhoP regulon
Zwir I, Latifi T, Perez JC, Huang H, Groisman EA. The promoter architectural landscape of the Salmonella PhoP regulon. Molecular Microbiology 2012, 84: 463-485. PMID: 22435712, PMCID: PMC3335776, DOI: 10.1111/j.1365-2958.2012.08036.x.Peer-Reviewed Original ResearchConceptsPromoter architectureDistinct promoter architecturesPathogen Salmonella enterica serovar TyphimuriumGene expression behaviorSalmonella enterica serovar TyphimuriumEnterica serovar TyphimuriumPhoP regulonPromoter featuresBiochemical functionsPhoPExpression behaviorPhysiological roleBacterial activatorsGenesSerovar TyphimuriumPromoterRegulonDifferent mechanismsTranscriptionVirulenceActivatorAncestryExpressionLarge numberLimited number
2010
An antisense RNA that governs the expression kinetics of a multifunctional virulence gene
Lee EJ, Groisman EA. An antisense RNA that governs the expression kinetics of a multifunctional virulence gene. Molecular Microbiology 2010, 76: 1020-1033. PMID: 20398218, PMCID: PMC2909850, DOI: 10.1111/j.1365-2958.2010.07161.x.Peer-Reviewed Original ResearchConceptsAntisense RNAGenome-wide transcriptome analysisRegulatory protein PhoPLong antisense RNAProtein levelsAntisense transcriptionMgtC proteinTranscriptome analysisRNase EAntisense transcriptsPolycistronic messageRNase IIISalmonella virulenceBacterial speciesPhysiological roleExpression kineticsTranscriptionRNAVirulence genesApparent roleVirulencePhoPSalmonella entericaMgtCAmgRS
2009
Activated by Different Signals, the PhoP/PhoQ Two-Component System Differentially Regulates Metal Uptake
Choi E, Groisman EA, Shin D. Activated by Different Signals, the PhoP/PhoQ Two-Component System Differentially Regulates Metal Uptake. Journal Of Bacteriology 2009, 191: 7174-7181. PMID: 19801407, PMCID: PMC2786564, DOI: 10.1128/jb.00958-09.Peer-Reviewed Original ResearchMeSH KeywordsAdenosine TriphosphatasesBacterial ProteinsBiological TransportBlotting, WesternCation Transport ProteinsGene Expression Regulation, BacterialHydrogen-Ion ConcentrationMagnesiumMembrane Transport ProteinsMetalsPhosphorylationReverse Transcriptase Polymerase Chain ReactionSalmonella typhimuriumConceptsPhoP/PhoQ systemPhoP/PhoQTwo-component systemTwo-component regulatory systemMgtA genePhoP proteinVirulence functionsMgtA transcriptionSalmonella genesLeader regionTransporter geneBiological consequencesGenesRegulatory systemAntimicrobial peptidesDistinct setsPhoQTranscriptionMetal uptakeSalmonella entericaMultiple signalsProteinExpressionPhoPMgtAEvolution of a Bacterial Regulon Controlling Virulence and Mg2+ Homeostasis
Perez JC, Shin D, Zwir I, Latifi T, Hadley TJ, Groisman EA. Evolution of a Bacterial Regulon Controlling Virulence and Mg2+ Homeostasis. PLOS Genetics 2009, 5: e1000428. PMID: 19300486, PMCID: PMC2650801, DOI: 10.1371/journal.pgen.1000428.Peer-Reviewed Original ResearchConceptsRegulatory proteinsSpecies-specific traitsHorizontal gene transferDifferent gene setsSpecies-specific targetsPhoP proteinTranscriptional rewiringPhoP regulonRelated organismsPhoPQ operonGene setsVariable membersCell envelopeProtein activityRegulonBacterial speciesGene transferSpeciesProteinPhoPFamily EnterobacteriaceaeGenesVirulenceHomeostasisWidespread effectsTranscription factor function and promoter architecture govern the evolution of bacterial regulons
Perez JC, Groisman EA. Transcription factor function and promoter architecture govern the evolution of bacterial regulons. Proceedings Of The National Academy Of Sciences Of The United States Of America 2009, 106: 4319-4324. PMID: 19251636, PMCID: PMC2649204, DOI: 10.1073/pnas.0810343106.Peer-Reviewed Original ResearchConceptsRegulatory circuitsBacterial regulonsPhoP proteinRegulatory protein PhoPBacterial transcription factorsTranscription factor functionCis-regulatory elementsGene regulatory circuitsHorizontal gene transferPathogen Salmonella entericaPromoter architectureEvolutionary changeRelated organismsVirulence regulatorTranscription factorsRegulonPhenotypic differencesFactor functionGene transferYersinia pestisSalmonella entericaCore membersProteinEukaryotesPhoP
2008
Overcoming H-NS-mediated Transcriptional Silencing of Horizontally Acquired Genes by the PhoP and SlyA Proteins in Salmonella enterica *
Perez JC, Latifi T, Groisman EA. Overcoming H-NS-mediated Transcriptional Silencing of Horizontally Acquired Genes by the PhoP and SlyA Proteins in Salmonella enterica *. Journal Of Biological Chemistry 2008, 283: 10773-10783. PMID: 18270203, PMCID: PMC2447644, DOI: 10.1074/jbc.m709843200.Peer-Reviewed Original ResearchConceptsHistone-like nucleoid structuring proteinPagC geneSlyA proteinRNA polymeraseRNA polymerase recruitmentH-NS repressionNucleoid structuring proteinHorizontal gene transferDifferent regulatory proteinsSalmonella entericaPolymerase recruitmentTranscriptional silencingNew traitsForeign DNAGene transcriptionRegulatory proteinsUgtLRespective promotersTranscriptionPhoPRecipient organismGenesPagC promoterGene transferProtein
2006
A Mg2+-responding RNA That Controls the Expression of a Mg2+ Transporter
GROISMAN EA, CROMIE MJ, SHI Y, LATIFI T. A Mg2+-responding RNA That Controls the Expression of a Mg2+ Transporter. Cold Spring Harbor Symposia On Quantitative Biology 2006, 71: 251-258. PMID: 17381304, DOI: 10.1101/sqb.2006.71.005.Peer-Reviewed Original ResearchConceptsDifferent cellular compartmentsAbundant divalent cationPhoP/PhoQStem-loop structureDifferent stem-loop structuresSensor PhoQTransporter MgtAMgtA geneMgtA transcriptionCellular compartmentsGene transcriptionTranscriptionPhoPPhoQMgtATransportersDisparate stepsBiological systemsDivalent cationsAdditional Mg2Singular exampleExpressionEnzymatic reactionsRiboswitchCytoplasmic Mg2
2005
The PhoP/PhoQ system controls the intramacrophage type three secretion system of Salmonella enterica
Bijlsma JJ, Groisman EA. The PhoP/PhoQ system controls the intramacrophage type three secretion system of Salmonella enterica. Molecular Microbiology 2005, 57: 85-96. PMID: 15948951, DOI: 10.1111/j.1365-2958.2005.04668.x.Peer-Reviewed Original ResearchConceptsSPI-2 pathogenicity islandPhoP/PhoQ systemType three secretion systemThree secretion systemPhoP proteinSecretion systemSsa genesPathogenicity islandTwo-component regulatory systemResponse regulator SsrBPhoP/PhoQRegulatory systemTwo-component systemSalmonella entericaEukaryotic cellsChromatin immunoprecipitationCentral roleDifferent regulatory systemsSalmonella virulenceUntranslated regionDistinct signalsPhoPGenesEffectorsProtein
2004
Signal-dependent Binding of the Response Regulators PhoP and PmrA to Their Target Promoters in Vivo *
Shin D, Groisman EA. Signal-dependent Binding of the Response Regulators PhoP and PmrA to Their Target Promoters in Vivo *. Journal Of Biological Chemistry 2004, 280: 4089-4094. PMID: 15569664, DOI: 10.1074/jbc.m412741200.Peer-Reviewed Original ResearchConceptsResponse regulator PhoPPmrA proteinPhoP proteinRegulator PhoPTranscription of PhoPWild-type strainTarget promotersPromoter occupancyChromatin immunoprecipitationPromotes phosphorylationRegulatory regionsTarget genesPhoPValine residueLow Mg2GenesPhosphorylationPromoterProteinAsp 52TranscriptionSalmonella entericaVivoImmunoprecipitationMg2Connecting two-component regulatory systems by a protein that protects a response regulator from dephosphorylation by its cognate sensor
Kato A, Groisman EA. Connecting two-component regulatory systems by a protein that protects a response regulator from dephosphorylation by its cognate sensor. Genes & Development 2004, 18: 2302-2313. PMID: 15371344, PMCID: PMC517523, DOI: 10.1101/gad.1230804.Peer-Reviewed Original ResearchMeSH KeywordsAllelesBacterial ProteinsBase SequenceGene Expression Regulation, BacterialMagnesiumMolecular Sequence DataPhosphorylationPromoter Regions, GeneticProtein Processing, Post-TranslationalProtein Structure, TertiarySalmonella entericaSignal TransductionTranscription FactorsTranscription, GeneticConceptsTwo-component systemResponse regulatorPhosphorylated formTwo-component regulatory systemTranscription of PmrAResponse regulator PmrAPhoP/PhoQPmrA/PmrBPmrA proteinTarget promotersCognate sensorProtein bindsSignal transductionCellular responsesDephosphorylationRegulatory systemPmrAProteinTranscriptionMultiple signalsRegulatorHigh affinityPmrA.Fundamental questionsPhoPTranscriptional Control of the Antimicrobial Peptide Resistance ugtL Gene by the Salmonella PhoP and SlyA Regulatory Proteins*
Shi Y, Latifi T, Cromie MJ, Groisman EA. Transcriptional Control of the Antimicrobial Peptide Resistance ugtL Gene by the Salmonella PhoP and SlyA Regulatory Proteins*. Journal Of Biological Chemistry 2004, 279: 38618-38625. PMID: 15208313, DOI: 10.1074/jbc.m406149200.Peer-Reviewed Original ResearchMeSH KeywordsAntimicrobial Cationic PeptidesBacterial ProteinsBase SequenceBeta-GalactosidaseBinding SitesBlotting, SouthernDeoxyribonuclease IGene Expression Regulation, BacterialMagaininsMagnesiumMembrane ProteinsModels, BiologicalMolecular Sequence DataMutationPeptidesPlasmidsPolymyxin BPromoter Regions, GeneticProtein BindingSalmonellaSingle-Strand Specific DNA and RNA EndonucleasesTranscription FactorsTranscription, GeneticTranscriptional ActivationXenopus ProteinsConceptsPhoP proteinSlyA mutantSlyA proteinPhoP/PhoQTranscription start siteAntimicrobial peptidesTwo-component systemMagainin 2Transcriptional activatorAbility of SalmonellaTranscriptional controlStart siteMaster regulatorRegulatory proteinsTranscriptionVirulence attenuationAntimicrobial peptide magainin 2PhoPGenesProteinPromoterMutantsSlyA.PhoQPeptides
2003
Signal-dependent Requirement for the Co-activator Protein RcsA in Transcription of the RcsB-regulated ugd Gene*
Mouslim C, Latifi T, Groisman EA. Signal-dependent Requirement for the Co-activator Protein RcsA in Transcription of the RcsB-regulated ugd Gene*. Journal Of Biological Chemistry 2003, 278: 50588-50595. PMID: 14514676, DOI: 10.1074/jbc.m309433200.Peer-Reviewed Original ResearchMeSH KeywordsBacterial ProteinsBase SequenceBeta-GalactosidaseBinding SitesChromosomesDeoxyribonuclease IEscherichia coli ProteinsGene DeletionIronMagnesiumModels, BiologicalModels, GeneticMolecular Sequence DataMutationPeriplasmic ProteinsPlasmidsPromoter Regions, GeneticSalmonellaSequence Homology, Amino AcidSingle-Strand Specific DNA and RNA EndonucleasesTemperatureTranscription FactorsTranscription, GeneticConceptsUgd genePmrA/PmrB systemTwo-component systems PhoP/PhoQS1 mapping experimentsPhoP/PhoQPmrA/PmrBUDP-glucose dehydrogenasePhoP proteinPhosphorelay systemIndependent transcriptionVariety of signalsPmrA mutantMembrane proteinsSame promoterCps operonRcsBGene expressionRcsATranscriptionGenesMapping experimentsCps transcriptionPhoPPromoterLow Mg2Closing the loop: The PmrA/PmrB two-component system negatively controls expression of its posttranscriptional activator PmrD
Kato A, Latifi T, Groisman EA. Closing the loop: The PmrA/PmrB two-component system negatively controls expression of its posttranscriptional activator PmrD. Proceedings Of The National Academy Of Sciences Of The United States Of America 2003, 100: 4706-4711. PMID: 12676988, PMCID: PMC153620, DOI: 10.1073/pnas.0836837100.Peer-Reviewed Original ResearchMeSH KeywordsAmino Acid SequenceArtificial Gene FusionBacterial ProteinsBase SequenceBinding SitesDNA, BacterialFeedbackGene Expression Regulation, BacterialGenes, BacterialModels, GeneticMolecular Sequence DataMutationPlasmidsPromoter Regions, GeneticProtein BindingSalmonella typhimuriumTranscription FactorsConceptsPmrA proteinTwo-component systemResponse regulator PmrAAppropriate cellular responsesPmrA/PmrBPhoQ proteinPhoP proteinRegulatory circuitsPosttranscriptional levelPromoter upstreamNegative regulationCellular responsesPmrB proteinCellular levelProteinPmrASalmonella entericaGenesMultiple signalsPmrDFeedback loopSingular exampleExpressionPhoPFundamental questionsMg2+ Sensing by the Mg2+ Sensor PhoQ of Salmonella enterica
Chamnongpol S, Cromie M, Groisman EA. Mg2+ Sensing by the Mg2+ Sensor PhoQ of Salmonella enterica. Journal Of Molecular Biology 2003, 325: 795-807. PMID: 12507481, DOI: 10.1016/s0022-2836(02)01268-8.Peer-Reviewed Original ResearchMeSH KeywordsAmino Acid SequenceAmino Acid SubstitutionBacterial ProteinsBase SequenceBinding SitesConserved SequenceDNA, BacterialMagnesiumMolecular Sequence DataMutagenesis, Site-DirectedPhosphorylationProtein Structure, TertiaryRecombinant ProteinsSalmonella entericaSequence Homology, Amino AcidTranscription, GeneticConceptsTranscription of PhoPPhoQ proteinSensor PhoQPeriplasmic domainTwo-component regulatory systemResponse regulator PhoPExpression of phoPPhoP/PhoQWild-type responseWild-type abilityAmino acid residuesGram-negative speciesRegulator PhoPGene transcriptionPhoPAcid residuesTranscriptionHistidine residuesPhoQGenesAcetyl phosphateRegulatory systemProteinMutantsSalmonella enterica