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
2016
Myriad Triple-Helix-Forming Structures in the Transposable Element RNAs of Plants and Fungi
Tycowski KT, Shu MD, Steitz JA. Myriad Triple-Helix-Forming Structures in the Transposable Element RNAs of Plants and Fungi. Cell Reports 2016, 15: 1266-1276. PMID: 27134163, PMCID: PMC4864102, DOI: 10.1016/j.celrep.2016.04.010.Peer-Reviewed Original ResearchConceptsTransposable elementsCellular noncoding RNAsPotential evolutionary consequencesCis-acting RNA structuresIntron lossEvolutionary consequencesBioinformatic identificationTE transcriptsReporter transcriptFish speciesNoncoding RNAsElement RNAHorizontal transferRNA structureTransposase geneRich tractHuman cellsTriple helix formationBase triplesRNAEne coreTranscriptsTriple helixIntronlessGenomeEBV noncoding RNA EBER2 interacts with host RNA-binding proteins to regulate viral gene expression
Lee N, Yario TA, Gao JS, Steitz JA. EBV noncoding RNA EBER2 interacts with host RNA-binding proteins to regulate viral gene expression. Proceedings Of The National Academy Of Sciences Of The United States Of America 2016, 113: 3221-3226. PMID: 26951683, PMCID: PMC4812724, DOI: 10.1073/pnas.1601773113.Peer-Reviewed Original ResearchConceptsNon-POU domain-containing octamer-binding proteinGene expressionNoncoding RNAsHost RNAAbundant noncoding RNAsCellular noncoding RNAsRNA-protein crosslinkingOctamer-binding proteinHost gene expressionBox protein 5Viral gene expressionHost transcription factorsGlutamine richFactor prolineIntermediary proteinsNuclear bodiesTranscription factorsRNA 2Host proteinsRecombinant proteinsProtein resultsProtein componentsProtein 5Protein 14RNA
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 DNARNARecruitmentNcRNAsNcRNARNAsLociViral 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 persistenceRNAProteinDNAVirusRegulationReplicationEBV Noncoding RNA Binds Nascent RNA to Drive Host PAX5 to Viral DNA
Lee N, Moss WN, Yario TA, Steitz JA. EBV Noncoding RNA Binds Nascent RNA to Drive Host PAX5 to Viral DNA. Cell 2015, 160: 607-618. PMID: 25662012, PMCID: PMC4329084, DOI: 10.1016/j.cell.2015.01.015.Peer-Reviewed Original ResearchConceptsTerminal repeatNascent RNANoncoding RNAsNuclear noncoding RNAB-cell transcription factor PAX5Greater sequence divergenceDNA target sitesTranscription factor Pax5Chromatin localizationTR lociSequence divergenceNascent transcriptsUndescribed functionTranscription factorsLatent EBV genomeRNATarget siteEssential rolePrimate herpesvirusesEBV lytic replicationPAX5Lytic replicationViral DNAEBER2Viral replication
2014
Virus Meets Host MicroRNA: the Destroyer, the Booster, the Hijacker
Guo YE, Steitz JA. Virus Meets Host MicroRNA: the Destroyer, the Booster, the Hijacker. Molecular And Cellular Biology 2014, 34: 3780-3787. PMID: 25047834, PMCID: PMC4187717, DOI: 10.1128/mcb.00871-14.Peer-Reviewed Original ResearchConceptsKey regulatory stepSmall noncoding RNAsVirus-host interactionsViral life cycleNoncoding RNAsCellular miRNAsMiRNA interactionsRegulatory stepGene expressionProtein productionHost microRNAsRNA virusesRecent discoveryLife cycleMicroRNAsMiRNAsRNADNAMRNAVirusExpressionInteractionMinireviewDiscoveryAlternative 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 ResearchConceptsBiological functionsRNA-protein complexesLevel of transcriptionForeign nucleic acidsMost ncRNAsLong ncRNAsNcRNA researchRNA processingGenome rearrangementsNucleic acidsNoncoding RNAsGene expressionRNA structureNcRNAsBase pairingDNA synthesisRemarkable varietySnoRNPsRiboswitchGenomeSnRNPsRNAsRibosomesTranscriptionTelomerase
2012
Formation of triple-helical structures by the 3′-end sequences of MALAT1 and MENβ noncoding RNAs
Brown JA, Valenstein ML, Yario TA, Tycowski KT, Steitz JA. Formation of triple-helical structures by the 3′-end sequences of MALAT1 and MENβ noncoding RNAs. Proceedings Of The National Academy Of Sciences Of The United States Of America 2012, 109: 19202-19207. PMID: 23129630, PMCID: PMC3511071, DOI: 10.1073/pnas.1217338109.Peer-Reviewed Original ResearchConceptsRich internal loopMetastasis-associated lung adenocarcinoma transcript 1Rich tractSarcoma-associated herpesvirusDuplex-triplex junctionsTriple helical structureCellular noncoding RNAsNuclear retention elementBase triplesInternal loopKaposi's sarcoma-associated herpesvirusU base triplesPAN RNATriple helixNoncoding RNAsNuclear RNAThermal denaturation profilesReporter RNALung adenocarcinoma transcript 1C nucleotidesC base pairsMolecular mechanismsUnpaired nucleotidesBase pairsRNAAUF1/hnRNP D is a novel protein partner of the EBER1 noncoding RNA of Epstein-Barr virus
Lee N, Pimienta G, Steitz JA. AUF1/hnRNP D is a novel protein partner of the EBER1 noncoding RNA of Epstein-Barr virus. RNA 2012, 18: 2073-2082. PMID: 23012480, PMCID: PMC3479396, DOI: 10.1261/rna.034900.112.Peer-Reviewed Original ResearchMeSH Keywords3' Untranslated RegionsAptamers, NucleotideAU Rich ElementsBinding, CompetitiveCell Line, TumorHerpesvirus 4, HumanHeterogeneous Nuclear Ribonucleoprotein D0Heterogeneous-Nuclear Ribonucleoprotein DHost-Pathogen InteractionsHumansImmunoprecipitationMutagenesis, InsertionalProtein BindingProtein IsoformsRNA StabilityRNA, ViralConceptsAU-rich elementsProtein partnersAUF1/hnRNP DUntranslated regionBacteriophage MS2 coat proteinNovel protein partnersHigh abundanceElectrophoretic mobility shift assaysEpstein-Barr virusMS2 coat proteinStable isotope labelingMobility shift assaysInteracting proteinMolecular functionsHnRNP DAlternative splicingNoncoding RNAsShift assaysCoat proteinIsotope labelingP40 isoformRNA aptamersRNA 1AUF1UV crosslinkingTracking 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 coreDown-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
Multiple 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 RaysThe Challenge of Viral snRNPs
CONRAD NK, FOK V, CAZALLA D, BORAH S, STEITZ JA. The Challenge of Viral snRNPs. Cold Spring Harbor Symposia On Quantitative Biology 2006, 71: 377-384. PMID: 17381320, DOI: 10.1101/sqb.2006.71.057.Peer-Reviewed Original ResearchConceptsNuclear noncoding RNAsHSURs 1Sarcoma-associated herpesvirusRibosomal protein L22Aggressive T-cell leukemiaT cell signalingViral gene expressionKaposi's sarcoma-associated herpesvirusHeterokaryon assayU RNADependent RNA degradationMammalian cellsNoncoding RNAsProtein L22Nuclear surveillanceRNA degradationHost mRNAsHost proteinsGene expressionMRNA transcriptsMutant virusHerpesvirus saimiriRNAImportant functionsRNAs