2021
Roles of piRNAs in transposon and pseudogene regulation of germline mRNAs and lncRNAs
Wang C, Lin H. Roles of piRNAs in transposon and pseudogene regulation of germline mRNAs and lncRNAs. Genome Biology 2021, 22: 27. PMID: 33419460, PMCID: PMC7792047, DOI: 10.1186/s13059-020-02221-x.Peer-Reviewed Original ResearchConceptsPIWI-interacting RNAsPIWI proteinsRole of piRNAsPIWI-piRNA pathwayRNA-binding proteinSmall noncoding RNAsGermline mRNAsGermline developmentNoncoding RNAsRegulatory relationshipsGerm cellsRNAProteinTransposonMajor classesRNA levelsRecent studiesExpressionGenomeSubfamiliesGermlineLncRNAsMajor constituentsMRNARegulationGenome-wide mapping of Piwi association with specific loci in Drosophila ovaries
Liu N, Neuenkirchen N, Zhong M, Lin H. Genome-wide mapping of Piwi association with specific loci in Drosophila ovaries. G3: Genes, Genomes, Genetics 2021, 11: jkaa059. PMID: 33609367, PMCID: PMC8022938, DOI: 10.1093/g3journal/jkaa059.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsArgonaute ProteinsDNA Transposable ElementsDrosophilaDrosophila melanogasterDrosophila ProteinsEpigenesis, GeneticFemaleOvaryRNA, Small InterferingConceptsPIWI-interacting RNAsProtein-coding genesDrosophila ovaryGermline stem cell maintenanceRole of piRNAsTermination sitesGenome-wide mappingGenomic binding profileTranscriptional termination sitesSpecific genomic sitesStem cell maintenanceRNA pathwaysTransposon repressionTranscriptional startEuchromatic regionsGene regulationEpigenetic regulationGenomic sitesCell maintenancePiwiSpecific lociMethylation signalsDiverse mechanismsTarget siteBinding sites
2020
PIWIL1 promotes gastric cancer via a piRNA-independent mechanism
Shi S, Yang ZZ, Liu S, Yang F, Lin H. PIWIL1 promotes gastric cancer via a piRNA-independent mechanism. Proceedings Of The National Academy Of Sciences Of The United States Of America 2020, 117: 22390-22401. PMID: 32848063, PMCID: PMC7486755, DOI: 10.1073/pnas.2008724117.Peer-Reviewed Original ResearchConceptsPIWI-interacting RNAsPIWI proteinsGastric cancer cellsNonsense-mediated mRNA decay mechanismPiRNA-independent mechanismDomain protein familyMRNA decay mechanismMammalian somatic tissuesRNA deep sequencingGastric cancer cell line SNU-1Cancer cellsGastric cancer cell proliferationRNA pathwaysPPD proteinsProtein familyPiwil1 geneSomatic tissuesSomatic cancersCancer cell proliferationDeep sequencingRegulatory mechanismsOncogenic functionPIWIL1Gastric cancer tissuesDetectable functionPIWI–piRNA pathway-mediated transposable element repression in Hydra somatic stem cells
Teefy BB, Siebert S, Cazet JF, Lin H, Juliano CE. PIWI–piRNA pathway-mediated transposable element repression in Hydra somatic stem cells. RNA 2020, 26: 550-563. PMID: 32075940, PMCID: PMC7161359, DOI: 10.1261/rna.072835.119.Peer-Reviewed Original ResearchConceptsPIWI-piRNA pathwayTE expressionSomatic stem cellsTransposable elementsTE transcriptsStem cellsFreshwater cnidarianSmall RNA pathwaysTransposable element repressionSomatic cell lineagesGermline of animalsInterstitial stem cellsStem cell populationInterstitial lineageSomatic piRNAsDegradome sequencingEpithelial cellsAncestral functionRNA pathwaysGermline piRNAsPIWI proteinsTE repressionGermline competenceSequence signaturesRNA immunoprecipitation
2019
Heat shock protein DNAJA1 stabilizes PIWI proteins to support regeneration and homeostasis of planarian Schmidtea mediterranea
Wang C, Yang ZZ, Guo FH, Shi S, Han XS, Zeng A, Lin H, Jing Q. Heat shock protein DNAJA1 stabilizes PIWI proteins to support regeneration and homeostasis of planarian Schmidtea mediterranea. Journal Of Biological Chemistry 2019, 294: 9873-9887. PMID: 31076507, PMCID: PMC6597837, DOI: 10.1074/jbc.ra118.004445.Peer-Reviewed Original ResearchConceptsPIWI proteinsPIWI-interacting RNA (piRNA) biogenesisPlanarian adult stem cellsHeat shock protein 40 family membersDifferent evolutionary lineagesPlanarian Schmidtea mediterraneaStem cell maintenanceStem cell regulationCo-immunoprecipitation assaysStem cellsSomatic stem cellsControl of proteinAdult stem cellsHuman gastric cancer cellsPiRNA biogenesisRNA biogenesisEvolutionary lineagesPiwi-like RNASchmidtea mediterraneaTwo-hybridSMEDWI-1Planarian speciesCell maintenanceGastric cancer cellsPlanarian regeneration
2018
MIWI2 targets RNAs transcribed from piRNA‐dependent regions to drive DNA methylation in mouse prospermatogonia
Watanabe T, Cui X, Yuan Z, Qi H, Lin H. MIWI2 targets RNAs transcribed from piRNA‐dependent regions to drive DNA methylation in mouse prospermatogonia. The EMBO Journal 2018, 37: embj201695329. PMID: 30108053, PMCID: PMC6138435, DOI: 10.15252/embj.201695329.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsArgonaute ProteinsChromatinDNA MethylationEpigenesis, GeneticMaleMiceMice, TransgenicRetroelementsRNA, Small InterferingSpermatogoniaConceptsDNA methylationRetrotransposon sequencesSmall RNAsArgonaute/Piwi proteinsPiwi protein MIWI2Suppressive epigenetic marksMouse prospermatogoniaChromatin statePIWI proteinsUnderlying molecular mechanismsDiverse organismsEpigenetic marksPiRNA clustersNascent RNAEpigenetic regulationTranslational regulationMIWI2RNA degradationRepeat sequencesGene expressionMolecular mechanismsTarget RNAMethylationRNAPiRNAsA critical role for nucleoporin 358 (Nup358) in transposon silencing and piRNA biogenesis in Drosophila
Parikh RY, Lin H, Gangaraju VK. A critical role for nucleoporin 358 (Nup358) in transposon silencing and piRNA biogenesis in Drosophila. Journal Of Biological Chemistry 2018, 293: 9140-9147. PMID: 29735528, PMCID: PMC6005430, DOI: 10.1074/jbc.ac118.003264.Peer-Reviewed Original ResearchMeSH KeywordsActive Transport, Cell NucleusAnimalsArgonaute ProteinsDNA Transposable ElementsDrosophilaDrosophila ProteinsFemaleGene Expression RegulationGene SilencingGenomic InstabilityGerm CellsMaleMolecular ChaperonesNuclear Pore Complex ProteinsProtein Interaction MapsRNA, Small InterferingTranscription, GeneticConceptsPIWI-interacting RNAsPing-pong cycleNuclear pore complexPiRNA biogenesisGermline knockdownPiRNA pathwayAntisense Piwi-interacting RNAsPiRNA precursor transcriptionSmall noncoding RNAsPiwi functionSilence transposonsPIWI proteinsShort hairpin RNACritical roleArgonaute 3Pore complexNoncoding RNAsGenomic instabilityNuclear localizationGene expressionTransposonNup358Germ cellsBiogenesisHairpin RNANovel evidence for a PIWI-interacting RNA (piRNA) as an oncogenic mediator of disease progression, and a potential prognostic biomarker in colorectal cancer
Weng W, Liu N, Toiyama Y, Kusunoki M, Nagasaka T, Fujiwara T, Wei Q, Qin H, Lin H, Ma Y, Goel A. Novel evidence for a PIWI-interacting RNA (piRNA) as an oncogenic mediator of disease progression, and a potential prognostic biomarker in colorectal cancer. Molecular Cancer 2018, 17: 16. PMID: 29382334, PMCID: PMC5791351, DOI: 10.1186/s12943-018-0767-3.Peer-Reviewed Original ResearchMeSH KeywordsAgedAged, 80 and overApoptosisBiomarkers, TumorCell DeathCell ProliferationColorectal NeoplasmsDisease ProgressionFemaleGene Expression ProfilingGene Expression Regulation, NeoplasticHumansMaleMiddle AgedNeoplasm MetastasisNeoplasm StagingOncogenesPrognosisRNA InterferenceRNA, Small InterferingConceptsPIWI-interacting RNAsSmall RNA sequencingGene expression profiling resultsImportant epigenetic regulatorsDownstream target genesExpression profiling resultsCell survival pathwaysColorectal cancerPotential prognostic biomarkerTumor suppressor genePrognostic biomarkerEpigenetic regulatorsSequence complementarityNoncoding RNAsRNA sequencingTarget genesExpression profilingBiological functionsGene expressionSurvival pathwaysSuppressor geneClinical significanceDirect targetNovel oncogeneOncogenic mediators
2016
PIWI-Interacting RNAs in Gliomagenesis: Evidence from Post-GWAS and Functional Analyses
Jacobs DI, Qin Q, Lerro MC, Fu A, Dubrow R, Claus EB, DeWan AT, Wang G, Lin H, Zhu Y. PIWI-Interacting RNAs in Gliomagenesis: Evidence from Post-GWAS and Functional Analyses. Cancer Epidemiology Biomarkers & Prevention 2016, 25: 1073-1080. PMID: 27197292, DOI: 10.1158/1055-9965.epi-16-0047.Peer-Reviewed Original ResearchConceptsPIWI-interacting RNAsRole of piRNAsPIWI-piRNA pathwayFunctional analysisGenome-wide association studiesCell death/survivalExpression of genesTumor suppressive functionDeath/survivalGermline developmentPIWI proteinsGenetic association analysisGrowth-promoting propertiesInsertional mutationAssociation signalsAssociation studiesAssociation analysisIndex variantsGenetic variantsColony formationFunctional impactCell proliferationGlioma cell viabilityVariant allelesCell viabilityTudor-SN Interacts with Piwi Antagonistically in Regulating Spermatogenesis but Synergistically in Silencing Transposons in Drosophila
Ku HY, Gangaraju VK, Qi H, Liu N, Lin H. Tudor-SN Interacts with Piwi Antagonistically in Regulating Spermatogenesis but Synergistically in Silencing Transposons in Drosophila. PLOS Genetics 2016, 12: e1005813. PMID: 26808625, PMCID: PMC4726654, DOI: 10.1371/journal.pgen.1005813.Peer-Reviewed Original ResearchConceptsPiRNA biogenesisPrimordial germ cellsPiwi expressionTudor-SNSomatic cellsGerm cellsDiverse molecular functionsPost-transcriptional regulationEmbryonic somatic cellsPiwi mutantsDosage-dependent mannerGermline developmentPIWI proteinsMutant phenotypeMeiotic cytokinesisMolecular functionsSpliceosome assemblyPiwiEpigenetic programmingDiverse functionsBiological functionsAdult ovariesBiogenesisTransposonMale fertility
2015
Reassessment of Piwi Binding to the Genome and Piwi Impact on RNA Polymerase II Distribution
Lin H, Chen M, Kundaje A, Valouev A, Yin H, Liu N, Neuenkirchen N, Zhong M, Snyder M. Reassessment of Piwi Binding to the Genome and Piwi Impact on RNA Polymerase II Distribution. Developmental Cell 2015, 32: 772-774. PMID: 25805139, PMCID: PMC4472434, DOI: 10.1016/j.devcel.2015.03.004.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsArgonaute ProteinsBase SequenceBinding SitesChromatin ImmunoprecipitationChromobox Protein Homolog 5Chromosomal Proteins, Non-HistoneDNA-Binding ProteinsDrosophila melanogasterDrosophila ProteinsGenomeHigh-Throughput Nucleotide SequencingHistone MethyltransferasesHistone-Lysine N-MethyltransferaseMethyltransferasesRNA InterferenceRNA Polymerase IIRNA, Small InterferingSequence Analysis, DNAConceptsRNA polymerase II distributionGenomic targetsHeterochromatin protein 1aRNA polymerase IICurrent bioinformatics methodsPiwi mutantsDrosophila PiwiPolymerase IIDevelopmental cellsPericentric regionsHistone methyltransferaseBioinformatics methodsBioinformatics pipelineProtein 1APiwiGenomePiRNAsEuchromatinMutantsMethyltransferaseSites
2014
Retrotransposons and pseudogenes regulate mRNAs and lncRNAs via the piRNA pathway in the germline
Watanabe T, Cheng EC, Zhong M, Lin H. Retrotransposons and pseudogenes regulate mRNAs and lncRNAs via the piRNA pathway in the germline. Genome Research 2014, 25: 368-380. PMID: 25480952, PMCID: PMC4352877, DOI: 10.1101/gr.180802.114.Peer-Reviewed Original ResearchConceptsPIWI-interacting RNAsPiRNA pathwayRetrotransposon sequencesIntergenic regionMammalian PIWI-interacting RNAsRNA regulatory networkLate spermatocytesVivo functional analysisDegradation of mRNAUTR of mRNAsSlicer activityEukaryotic genomesLncRNA transcriptomeRegulatory networksRegulatory sequencesRepetitive sequencesPseudogenesMRNA stabilityFunctional analysisLncRNAsWidespread expressionSpermatid stageRetrotransposonsMRNATransposonPosttranscriptional Regulation of Gene Expression by Piwi Proteins and piRNAs
Watanabe T, Lin H. Posttranscriptional Regulation of Gene Expression by Piwi Proteins and piRNAs. Molecular Cell 2014, 56: 18-27. PMID: 25280102, PMCID: PMC4185416, DOI: 10.1016/j.molcel.2014.09.012.Peer-Reviewed Original ResearchConceptsPIWI-interacting RNAsPIWI proteinsPosttranscriptional regulationPiRNA biogenesisPiRNA pathwayTransposon RNARNA regulationSex determinationCell maintenancePosttranscriptional levelGene expressionDevelopmental transitionsBiological processesProteinRNAGametogenesisRegulationRecent findingsMRNAPotential importancePsuedogenesBiogenesisEmbryogenesisTransposonPathwayPIWI proteins and PIWI-interacting RNAs in the soma
Ross RJ, Weiner MM, Lin H. PIWI proteins and PIWI-interacting RNAs in the soma. Nature 2014, 505: 353-359. PMID: 24429634, PMCID: PMC4265809, DOI: 10.1038/nature12987.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsArgonaute ProteinsCiliophoraDrosophila melanogasterDrosophila ProteinsEpigenesis, GeneticFemaleGenomeHumansNeoplasmsOvaryPhenotypeRNA, Small InterferingConceptsPIWI-interacting RNAsPIWI proteinsPIWI-piRNA pathwayDiscovery of millionsWhole-body regenerationStem cell functionSomatic functionsDiverse organismsLower eukaryotesGenome rearrangementsSomatic cellsEpigenetic programmingBiological rolePathwayRNAProteinRecent studiesEukaryotesTransposonOrganismsBiologyUnanticipated dimensionsFunctionCellsRearrangement
2013
PIWI proteins and PIWI-interacting RNAs function in Hydra somatic stem cells
Juliano CE, Reich A, Liu N, Götzfried J, Zhong M, Uman S, Reenan RA, Wessel GM, Steele RE, Lin H. PIWI proteins and PIWI-interacting RNAs function in Hydra somatic stem cells. Proceedings Of The National Academy Of Sciences Of The United States Of America 2013, 111: 337-342. PMID: 24367095, PMCID: PMC3890812, DOI: 10.1073/pnas.1320965111.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsArgonaute ProteinsCell DifferentiationCell LineageCell SeparationCytoplasmEpithelial CellsFlow CytometryGene Expression RegulationHydraPhylogenyRecombinant ProteinsRNARNA InterferenceRNA Processing, Post-TranscriptionalRNA, Small InterferingSpecies SpecificityStem CellsTranscriptomeTransgenesConceptsPIWI-interacting RNAsPIWI proteinsStem/progenitor cellsProgenitor cellsPIWI-piRNA pathwayPing-pong signatureSomatic stem/progenitor cellsStem cell functionalitySomatic stem cellsInterstitial lineageNonbilaterian animalsPiwi functionPiRNA biogenesisAnimal germlineTransposon transcriptsSimple metazoanCnidarian HydraSmall RNAsEndodermal lineagesRNA functionPosttranscriptional regulatorsEpithelial lineageLineagesLikely actsPiwiTdrkh is essential for spermatogenesis and participates in primary piRNA biogenesis in the germline
Saxe JP, Chen M, Zhao H, Lin H. Tdrkh is essential for spermatogenesis and participates in primary piRNA biogenesis in the germline. The EMBO Journal 2013, 32: 1869-1885. PMID: 23714778, PMCID: PMC3981179, DOI: 10.1038/emboj.2013.121.Peer-Reviewed Original ResearchConceptsPrimary piRNA biogenesisPiRNA biogenesisKH domain-containing proteinPiRNA biogenesis pathwayPing-pong cycleDomain-containing proteinsMature piRNAsPIWI proteinsBiogenesis pathwayMitochondrial proteinsEpigenetic programmingNuclear localizationCytoplasmic localizationZygotene stageBiogenesisTDRKHArginine residuesMeiotic arrestMIWI2MIWIDistinct populationsProteinMutantsGermlineRNABeyond transposons: the epigenetic and somatic functions of the Piwi-piRNA mechanism
Peng JC, Lin H. Beyond transposons: the epigenetic and somatic functions of the Piwi-piRNA mechanism. Current Opinion In Cell Biology 2013, 25: 190-194. PMID: 23465540, PMCID: PMC3651849, DOI: 10.1016/j.ceb.2013.01.010.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsArgonaute ProteinsDNA Transposable ElementsDrosophila ProteinsEpigenesis, GeneticGene SilencingHistonesRNA, Small InterferingConceptsPIWI-interacting RNAsPIWI-piRNA pathwayBiogenesis of piRNAsSmall non-coding RNAsPost-transcriptional regulationNon-coding RNAsPIWI proteinsGene regulationSomatic cellsPiwi familyGene expressionGeneral mechanismSomatic functionsTransposonPathwayRNARegulationNovel classRecent studiesBiogenesisNew findingsProteinMechanismExpressionFunctionA Major Epigenetic Programming Mechanism Guided by piRNAs
Huang XA, Yin H, Sweeney S, Raha D, Snyder M, Lin H. A Major Epigenetic Programming Mechanism Guided by piRNAs. Developmental Cell 2013, 24: 502-516. PMID: 23434410, PMCID: PMC3600162, DOI: 10.1016/j.devcel.2013.01.023.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsAnimals, Genetically ModifiedArgonaute ProteinsChromatinChromatin ImmunoprecipitationChromobox Protein Homolog 5Chromosomal Proteins, Non-HistoneDNA Transposable ElementsDrosophilaDrosophila ProteinsEpigenomicsGenomeGenomicsMethyltransferasesMutationReal-Time Polymerase Chain ReactionReverse Transcriptase Polymerase Chain ReactionRNA Polymerase IIRNA, MessengerRNA, Small InterferingConceptsSpecific genomic sitesEpigenetic factorsGenomic sitesRNA polymerase II associationPiwi-piRNA complexDrosophila genomeEpigenetic stateEpigenetic landscapeComplex associatesPiwiGenomePiRNAsCentral enigmaMajor mechanismEctopic sitesSequenceHP1aDrosophilaPiRNASitesEpigeneticsMechanismProgramming mechanismAssociatesRecruitmentFunction of Piwi, a nuclear Piwi/Argonaute protein, is independent of its slicer activity
Darricarrère N, Liu N, Watanabe T, Lin H. Function of Piwi, a nuclear Piwi/Argonaute protein, is independent of its slicer activity. Proceedings Of The National Academy Of Sciences Of The United States Of America 2013, 110: 1297-1302. PMID: 23297219, PMCID: PMC3557079, DOI: 10.1073/pnas.1213283110.Peer-Reviewed Original ResearchConceptsPIWI proteinsPiRNA biogenesisSlicer activityPIWI-interacting RNA (piRNA) biogenesisEndonuclease activityFunction of PiwiNuclear Piwi proteinSecondary piRNA biogenesisGerm line developmentPiwi functionPiwi membersArgonaute proteinsRNA biogenesisArgonaute 3Transgenic fliesPiwiSomatic cellsCatalytic triadEpigenetic factorsRegulatory functionsBiogenesisOnly memberProteinTransposonRecent evidence
2012
piRNA biogenesis during adult spermatogenesis in mice is independent of the ping-pong mechanism
Beyret E, Liu N, Lin H. piRNA biogenesis during adult spermatogenesis in mice is independent of the ping-pong mechanism. Cell Research 2012, 22: 1429-1439. PMID: 22907665, PMCID: PMC3463270, DOI: 10.1038/cr.2012.120.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsArgonaute ProteinsCluster AnalysisDown-RegulationGenetic LociMaleMeiosisMiceRNA, Small InterferingSpermatogenesisTestisUp-RegulationConceptsPIWI proteinsPing-pong mechanismSmall non-coding RNAsSame DNA strandNon-coding RNAsPiRNA biogenesisGermline developmentDiverse organismsEpigenetic regulationPiRNAsMIWIRepeat sequencesMILISame locusSequence featuresNucleotide positionsPostnatal testisBroad functionsAdult testisMouse testisDNA strandsAdult spermatogenesisProteinBiogenesisPrimary pathway