2019
Idiosyncrasies of Viral Noncoding RNAs Provide Insights into Host Cell Biology
Withers JB, Mondol V, Pawlica P, Rosa-Mercado NA, Tycowski KT, Ghasempur S, Torabi SF, Steitz JA. Idiosyncrasies of Viral Noncoding RNAs Provide Insights into Host Cell Biology. Annual Review Of Virology 2019, 6: 1-21. PMID: 31039329, PMCID: PMC6768742, DOI: 10.1146/annurev-virology-092818-015811.Peer-Reviewed Original ResearchConceptsHost cell biologyCell biologyMessenger RNA stabilityHost cell machineryHost gene expressionDiverse biological rolesHost immune evasionLong ncRNAsMicroRNA biogenesisCell machineryNoncoding RNAsRNA stabilityCircular RNAsCellular transformationCellular survivalNcRNAsViral noncoding RNAsBiological roleGene expressionAnimal virusesNoncanonical pathwayHost cellsViral ncRNAsNovel mechanismBiogenesis
2018
Kaposi's Sarcoma-Associated Herpesvirus mRNA Accumulation in Nuclear Foci Is Influenced by Viral DNA Replication and Viral Noncoding Polyadenylated Nuclear RNA
Vallery TK, Withers JB, Andoh JA, Steitz JA. Kaposi's Sarcoma-Associated Herpesvirus mRNA Accumulation in Nuclear Foci Is Influenced by Viral DNA Replication and Viral Noncoding Polyadenylated Nuclear RNA. Journal Of Virology 2018, 92: 10.1128/jvi.00220-18. PMID: 29643239, PMCID: PMC6002709, DOI: 10.1128/jvi.00220-18.Peer-Reviewed Original ResearchConceptsKaposi's sarcoma-associated herpesvirusViral replication compartmentsSarcoma-associated herpesvirusReplication compartmentsViral DNA replicationViral DNA synthesisPAN RNANuclear fociDNA replicationNuclear RNAViral mRNAsDNA synthesisViral transcriptsLytic phaseIntronless viral mRNAsHijack host machineryActive viral DNA replicationPolyadenylated Nuclear RNAHost cell nucleusViral noncoding RNAViral RNA accumulationShutoff effectHuman cell hostSpatiotemporal regulationViral life cycle
2015
Noncoding RNA‐guided recruitment of transcription factors: A prevalent but undocumented mechanism?
Lee N, Steitz JA. Noncoding RNA‐guided recruitment of transcription factors: A prevalent but undocumented mechanism? BioEssays 2015, 37: 936-941. PMID: 26200477, PMCID: PMC4721591, DOI: 10.1002/bies.201500060.Peer-Reviewed Original ResearchConceptsTranscription factorsDomains of TFsCognate binding motifsDNA target sitesAssociated transcription factorsRNA-RNA interactionsTarget siteNascent transcriptsCell identityTarget lociCellular processesNoncoding RNAsBinding motifProper regulationViral genomeUndocumented mechanismGenomeDNAViral DNARNARecruitmentNcRNAsNcRNARNAsLociProteomics and Transcriptomics of BJAB Cells Expressing the Epstein-Barr Virus Noncoding RNAs EBER1 and EBER2
Pimienta G, Fok V, Haslip M, Nagy M, Takyar S, Steitz JA. Proteomics and Transcriptomics of BJAB Cells Expressing the Epstein-Barr Virus Noncoding RNAs EBER1 and EBER2. PLOS ONE 2015, 10: e0124638. PMID: 26121143, PMCID: PMC4487896, DOI: 10.1371/journal.pone.0124638.Peer-Reviewed Original ResearchConceptsMRNA-seq dataHost cell nucleusBJAB cellsCell proliferationGene expression featuresPro-survival effectsProtein adaptersAlternative splicingMRNA transcriptomeUpregulated proteinsSILAC dataRich elementsAkt activationPI3K-AktBiochemical assaysCell nucleiEBV latencySwitch eventsProteinMaintenance of latencyCell linesVEGFA proteinMechanistic explanationUpregulated oncogenesPIK3AP1In silico discovery and modeling of non-coding RNA structure in viruses
Moss WN, Steitz JA. In silico discovery and modeling of non-coding RNA structure in viruses. Methods 2015, 91: 48-56. PMID: 26116541, PMCID: PMC4684774, DOI: 10.1016/j.ymeth.2015.06.015.Peer-Reviewed Original ResearchMeSH KeywordsComputer SimulationHerpesvirus 4, HumanInfluenza A virusNucleic Acid ConformationRNA, UntranslatedRNA, ViralViral noncoding RNAs: more surprises
Tycowski KT, Guo YE, Lee N, Moss WN, Vallery TK, Xie M, Steitz JA. Viral noncoding RNAs: more surprises. Genes & Development 2015, 29: 567-584. PMID: 25792595, PMCID: PMC4378190, DOI: 10.1101/gad.259077.115.Peer-Reviewed Original ResearchConceptsDiverse biological rolesSmall noncoding RNAsMultitude of functionsHost immune evasionEukaryotic cellsCellular transformationNoncoding RNAsHost counterpartsAnimal virusesBiological roleNcRNAsRNA virusesViral ncRNAsMechanism of actionImmune evasionViral replicationMore surprisesBiogenesisViral persistenceRNAProteinDNAVirusRegulationReplication
2014
Alternative Capture of Noncoding RNAs or Protein-Coding Genes by Herpesviruses to Alter Host T Cell Function
Guo YE, Riley KJ, Iwasaki A, Steitz JA. Alternative Capture of Noncoding RNAs or Protein-Coding Genes by Herpesviruses to Alter Host T Cell Function. Molecular Cell 2014, 54: 67-79. PMID: 24725595, PMCID: PMC4039351, DOI: 10.1016/j.molcel.2014.03.025.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsAntigens, CDAntigens, Differentiation, T-LymphocyteBase SequenceCallithrixEnzyme ActivationGene Expression RegulationGPI-Linked ProteinsGRB2 Adaptor ProteinHEK293 CellsHerpesvirus 2, SaimiriineHigh-Throughput Nucleotide SequencingHost-Pathogen InteractionsHumansImmunoprecipitationInterferon-gammaJurkat CellsLectins, C-TypeLymphocyte ActivationMicroRNAsMitogen-Activated Protein KinasesMolecular Sequence DataReceptors, Antigen, T-CellRNA StabilityRNA, UntranslatedRNA, ViralSemaphorinsSequence Analysis, RNASignal TransductionTime FactorsT-LymphocytesTransfectionConceptsMitogen-activated protein kinaseMiR-27Protein coding genesHerpesvirus saimiriHigh-throughput sequencingTCR-induced activationCell functionHSUR 1Γ-herpesvirusesNoncoding RNAsProtein kinaseEctopic expressionOncogenic γ-herpesvirusesTarget genesInduction of CD69MicroRNA-27Key modulatorRNACommon targetAlHV-1GenesCell receptorDiverse strategiesHost T-cell functionCellsThe Noncoding RNA Revolution—Trashing Old Rules to Forge New Ones
Cech TR, Steitz JA. The Noncoding RNA Revolution—Trashing Old Rules to Forge New Ones. Cell 2014, 157: 77-94. PMID: 24679528, DOI: 10.1016/j.cell.2014.03.008.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsChromatinGene Expression RegulationGenomeHumansRibonucleoproteinsRNA, CatalyticRNA, Long NoncodingRNA, UntranslatedConceptsBiological functionsRNA-protein complexesLevel of transcriptionForeign nucleic acidsMost ncRNAsLong ncRNAsNcRNA researchRNA processingGenome rearrangementsNucleic acidsNoncoding RNAsGene expressionRNA structureNcRNAsBase pairingDNA synthesisRemarkable varietySnoRNPsRiboswitchGenomeSnRNPsRNAsRibosomesTranscriptionTelomerase
2013
RNA families in Epstein–Barr virus
Moss WN, Lee N, Pimienta G, Steitz JA. RNA families in Epstein–Barr virus. RNA Biology 2013, 11: 10-17. PMID: 24441309, PMCID: PMC3929418, DOI: 10.4161/rna.27488.Peer-Reviewed Original ResearchConceptsEpstein-Barr virusFunctional importanceSmall regulatory RNAsNovel Epstein-Barr virusSmall nucleolar RNAsLikely functional importanceInternal ribosomal entry siteRNA-seq studiesHuman γ-herpesvirusEvolutionary conservationNovel ncRNARegulatory RNAsShort intronsRecent bioinformaticsNucleolar RNAsOncogenic typesRNA familiesTumorigenic phenotypeStructured RNAsEBV genomeEBNA1 mRNARepetitive regionsViral latencyHigh abundanceLatency maintenance
2012
Conservation of a Triple-Helix-Forming RNA Stability Element in Noncoding and Genomic RNAs of Diverse Viruses
Tycowski KT, Shu MD, Borah S, Shi M, Steitz JA. Conservation of a Triple-Helix-Forming RNA Stability Element in Noncoding and Genomic RNAs of Diverse Viruses. Cell Reports 2012, 2: 26-32. PMID: 22840393, PMCID: PMC3430378, DOI: 10.1016/j.celrep.2012.05.020.Peer-Reviewed Original ResearchConceptsPAN RNAKaposi's sarcoma-associated herpesvirusSarcoma-associated herpesvirusStructure-based bioinformaticsRNA decay pathwaysDiverse viral genomesRNA stability elementNuclear retention elementPositive-strand RNA virusesReporter transcriptMammalian herpesvirusesGenomic RNAStability elementDNA virusesHuman cellsTriple helix formationRNA virusesDiverse virusesViral genomeRNAAbundant expressionDecay pathwaysTriple helixRetention elementsRapid identificationTracking expression and subcellular localization of RNA and protein species using high-throughput single cell imaging flow cytometry
Borah S, Nichols LA, Hassman LM, Kedes DH, Steitz JA. Tracking expression and subcellular localization of RNA and protein species using high-throughput single cell imaging flow cytometry. RNA 2012, 18: 1573-1579. PMID: 22745225, PMCID: PMC3404377, DOI: 10.1261/rna.033126.112.Peer-Reviewed Original ResearchConceptsKaposi's sarcoma-associated herpesvirusSarcoma-associated herpesvirusSubcellular localizationProtein moleculesHigh-throughput approachPAN RNAProtein speciesNoncoding RNAsNuclear RNAProtein C1Imaging Flow CytometryFlow cytometryRNANuclear translocationHigh-throughput applicationsLytic phaseViral RNATranslocationExpressionLocalizationCellsHeterogeneous populationPABPC1CytometryMolecules
2011
A Viral Nuclear Noncoding RNA Binds Re-localized Poly(A) Binding Protein and Is Required for Late KSHV Gene Expression
Borah S, Darricarrère N, Darnell A, Myoung J, Steitz JA. A Viral Nuclear Noncoding RNA Binds Re-localized Poly(A) Binding Protein and Is Required for Late KSHV Gene Expression. PLOS Pathogens 2011, 7: e1002300. PMID: 22022268, PMCID: PMC3192849, DOI: 10.1371/journal.ppat.1002300.Peer-Reviewed Original ResearchConceptsPAN RNAKaposi's Sarcoma-Associated HerpesvirusNuclear noncoding RNANuclear noncoding RNAsShutoff effectLytic phaseKSHV gene expressionRepertoire of functionsTail of mRNATransient transfection experimentsConsequence of expressionLate viral proteinsNoncoding RNAsExonuclease proteinNuclear RNAProtein C1Translation efficiencyHost mRNAsMRNA stabilityGene expressionUnknown functionTransfection experimentsViral mRNAsPABPC1Binding proteinA Primate Herpesvirus Uses the Integrator Complex to Generate Viral MicroRNAs
Cazalla D, Xie M, Steitz JA. A Primate Herpesvirus Uses the Integrator Complex to Generate Viral MicroRNAs. Molecular Cell 2011, 43: 982-992. PMID: 21925386, PMCID: PMC3176678, DOI: 10.1016/j.molcel.2011.07.025.Peer-Reviewed Original ResearchConceptsEnd processing signalsHerpesvirus saimiriMature viral miRNAsPre-miRNA hairpinsCis-acting elementsMarmoset T cellsIntegrator complexAGO proteinsMiRNA biogenesisMicroprocessor complexU RNAExportin-5Noncoding RNAsViral miRNAsProcessing assaysHost miRNAsDeep sequencingViral noncoding RNAsProtein componentsComplex cleavesHairpin structureHSURsPrimate herpesvirusesMiRNAsRNA
2010
Poly(A) Tail Recognition by a Viral RNA Element Through Assembly of a Triple Helix
Mitton-Fry RM, DeGregorio SJ, Wang J, Steitz TA, Steitz JA. Poly(A) Tail Recognition by a Viral RNA Element Through Assembly of a Triple Helix. Science 2010, 330: 1244-1247. PMID: 21109672, PMCID: PMC3074936, DOI: 10.1126/science.1195858.Peer-Reviewed Original ResearchConceptsSarcoma-associated herpesvirusBox H/ACA small nucleolar RNAsMajor-groove triple helixNuclear noncoding RNANuclear retention elementSmall nucleolar RNAsViral RNA elementsRich internal loopTriple helixKaposi's sarcoma-associated herpesvirusPAN RNADeadenylation assaysRNA decayRNA clampNucleolar RNAsNoncoding RNAsNuclear RNATail recognitionRNA elementsFunctional importanceAngstrom resolutionRich loopSecondary structureRNAEne coreNoncoding RNPs of Viral Origin
Steitz J, Borah S, Cazalla D, Fok V, Lytle R, Mitton-Fry R, Riley K, Samji T. Noncoding RNPs of Viral Origin. Cold Spring Harbor Perspectives In Biology 2010, 3: a005165. PMID: 20719877, PMCID: PMC3039937, DOI: 10.1101/cshperspect.a005165.Peer-Reviewed Original ResearchDown-Regulation of a Host MicroRNA by a Herpesvirus saimiri Noncoding RNA
Cazalla D, Yario T, Steitz JA. Down-Regulation of a Host MicroRNA by a Herpesvirus saimiri Noncoding RNA. Science 2010, 328: 1563-1566. PMID: 20558719, PMCID: PMC3075239, DOI: 10.1126/science.1187197.Peer-Reviewed Original ResearchConceptsHSURs 1Noncoding RNAsHost cell gene expressionMiR-27Binding-dependent mannerPotential binding sitesMiRNA pathwayHost cell microRNAsCoimmunoprecipitation experimentsEctopic expressionTarget genesTransient knockdownGene expressionUnknown functionHost microRNAsViral strategiesDown regulationBinding sitesMiRNAsMicroRNAsRNAExpressionCellsT cellsNcRNADown-Regulation of a Host microRNA by a Viral Noncoding RNA
Cazalla D, Steitz JA. Down-Regulation of a Host microRNA by a Viral Noncoding RNA. Cold Spring Harbor Symposia On Quantitative Biology 2010, 75: 321-324. PMID: 21139068, PMCID: PMC5647998, DOI: 10.1101/sqb.2010.75.009.Peer-Reviewed Original ResearchConceptsHerpesvirus saimiriNoncoding RNAsHost cell gene expressionMiR-27Binding-dependent mannerAU-rich elementsViral noncoding RNAMarmoset T cellsMiRNA pathwayHost cell microRNAsViral life cycleConserved sequencesEctopic expressionMammalian virusesTarget genesTransient knockdownMutational analysisGene expressionHost microRNAsHSUR1Viral strategiesBase pairingDown regulationPrimate herpesvirusesLytic phase
2006
Epstein-Barr virus noncoding RNAs are confined to the nucleus, whereas their partner, the human La protein, undergoes nucleocytoplasmic shuttling
Fok V, Friend K, Steitz JA. Epstein-Barr virus noncoding RNAs are confined to the nucleus, whereas their partner, the human La protein, undergoes nucleocytoplasmic shuttling. Journal Of Cell Biology 2006, 173: 319-325. PMID: 16682524, PMCID: PMC2063832, DOI: 10.1083/jcb.200601026.Peer-Reviewed Original ResearchMeSH KeywordsActive Transport, Cell NucleusAnimalsAntibiotics, AntineoplasticAutoantigensCell LineCell Line, TumorCell NucleusDactinomycinFatty Acids, UnsaturatedFemaleHeLa CellsHerpesvirus 4, HumanHumansKaryopherinsMiceNIH 3T3 CellsOocytesProtein BindingRibonucleoproteinsRNA TransportRNA, UntranslatedRNA, ViralXenopus laevisMultiple domains of EBER 1, an Epstein-Barr virus noncoding RNA, recruit human ribosomal protein L22
Fok V, Mitton-Fry RM, Grech A, Steitz JA. Multiple domains of EBER 1, an Epstein-Barr virus noncoding RNA, recruit human ribosomal protein L22. RNA 2006, 12: 872-882. PMID: 16556938, PMCID: PMC1440895, DOI: 10.1261/rna.2339606.Peer-Reviewed Original ResearchMeSH KeywordsBinding SitesCarrier ProteinsCell LineCross-Linking ReagentsElectrophoretic Mobility Shift AssayHerpesvirus 4, HumanHumansIn Vitro TechniquesMaltose-Binding ProteinsNucleic Acid ConformationPlasmidsProtein BindingProtein Structure, TertiaryRecombinant Fusion ProteinsRibosomal ProteinsRNA, UntranslatedRNA, ViralRNA-Binding ProteinsSequence DeletionTranscription, GeneticTransfectionUltraviolet Rays