2021
Genome-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 ResearchConceptsPIWI-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 functionMIWI prevents aneuploidy during meiosis by cleaving excess satellite RNA
Hsieh C, Xia J, Lin H. MIWI prevents aneuploidy during meiosis by cleaving excess satellite RNA. The EMBO Journal 2020, 39: embj2019103614. PMID: 32677148, PMCID: PMC7429737, DOI: 10.15252/embj.2019103614.Peer-Reviewed Original ResearchConceptsChromosome misalignmentSatellite RNAKinetochore assemblySatellite repeatsWild-type spermatocytesPericentromeric satellite repeatsFaithful chromosome segregationProper kinetochore assemblyChromosome mis-segregationPost-transcriptional regulationPiRNA biogenesisMeiotic functionsPIWI proteinsChromosome segregationMis-segregationMurine memberElevated aneuploidyMale meiosisPrevents aneuploidyDicer cleavageMIWIMetaphase IRNA fragmentsMeiosisRNAPIWI–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 RNA
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 viabilityThe Role of PIWIL4, an Argonaute Family Protein, in Breast Cancer*
Wang Z, Liu N, Shi S, Liu S, Lin H. The Role of PIWIL4, an Argonaute Family Protein, in Breast Cancer*. Journal Of Biological Chemistry 2016, 291: 10646-10658. PMID: 26957540, PMCID: PMC4865913, DOI: 10.1074/jbc.m116.723239.Peer-Reviewed Original ResearchConceptsP-element-induced wimpy testisPIWI-interacting RNAsPIWI proteinsMDA-MB-231 cellsArgonaute family proteinsGermline developmentDiverse organismsWimpy testisFamily proteinsProteome analysisClass II proteinsPIWIL4Potential therapeutic targetStem cellsProteinMHC class II proteinsMigration abilityRNATherapeutic targetPIWIL4 expressionCancer tissuesBreast cancer tissuesCellsKey roleBiogenesisPiwi maintains germline stem cells and oogenesis in Drosophila through negative regulation of Polycomb group proteins
Peng JC, Valouev A, Liu N, Lin H. Piwi maintains germline stem cells and oogenesis in Drosophila through negative regulation of Polycomb group proteins. Nature Genetics 2016, 48: 283-291. PMID: 26780607, PMCID: PMC4767590, DOI: 10.1038/ng.3486.Peer-Reviewed Original Research
2015
Piwi Is a Key Regulator of Both Somatic and Germline Stem Cells in the Drosophila Testis
Gonzalez J, Qi H, Liu N, Lin H. Piwi Is a Key Regulator of Both Somatic and Germline Stem Cells in the Drosophila Testis. Cell Reports 2015, 12: 150-161. PMID: 26119740, PMCID: PMC4497877, DOI: 10.1016/j.celrep.2015.06.004.Peer-Reviewed Original ResearchConceptsGermline stem cellsDrosophila testisSomatic cyst cellsPIWI-piRNA pathwayStem cell maintenanceCell-autonomous functionStem cellsGerm cell differentiationStem cell typesFasciclin 3GSC daughtersGermline functionSomatic rolePiwi expressionCyst cellsCell maintenanceEpigenetic mechanismsPiwiGenes keyNuclear localizationKey regulatorMolecular mechanismsCell differentiationGonadal developmentCell typesReassessment 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 Are Dispensable for Mouse Somatic Development and Reprogramming of Fibroblasts into Pluripotent Stem Cells
Cheng EC, Kang D, Wang Z, Lin H. PIWI Proteins Are Dispensable for Mouse Somatic Development and Reprogramming of Fibroblasts into Pluripotent Stem Cells. PLOS ONE 2014, 9: e97821. PMID: 25238487, PMCID: PMC4169525, DOI: 10.1371/journal.pone.0097821.Peer-Reviewed Original ResearchConceptsPIWI proteinsEmbryonic stem cellsInduced pluripotent stem cellsPluripotent stem cellsIPS cellsPiwi genesGermline stem cell maintenanceStem cellsControl iPS cellsDifferentiated somatic cellsStem cell maintenancePIWI protein familyReprogramming of fibroblastsExpression profiling revealsGermline developmentProtein familyKnockout embryosCell maintenanceFemale fertileSomatic cellsEmbryonic fibroblastsDirect reprogrammingProfiling revealsTeratoma assayGerm layersPiwi Is Required in Multiple Cell Types to Control Germline Stem Cell Lineage Development in the Drosophila Ovary
Ma X, Wang S, Do T, Song X, Inaba M, Nishimoto Y, Liu LP, Gao Y, Mao Y, Li H, McDowell W, Park J, Malanowski K, Peak A, Perera A, Li H, Gaudenz K, Haug J, Yamashita Y, Lin H, Ni JQ, Xie T. Piwi Is Required in Multiple Cell Types to Control Germline Stem Cell Lineage Development in the Drosophila Ovary. PLOS ONE 2014, 9: e90267. PMID: 24658126, PMCID: PMC3962343, DOI: 10.1371/journal.pone.0090267.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsArgonaute ProteinsCell DifferentiationCell LineageDNA DamageDrosophilaDrosophila ProteinsFemaleOvarySignal TransductionConceptsGerm cell differentiationDrosophila ovaryGermline stem cellsSomatic cellsCell differentiationGerm cellsPiRNA productionMultiple cell typesGSC maintenanceTransposable elementsGerm lineLineage developmentCell typesPiRNA pathway componentsGerm cell maintenanceCell lineage developmentUndifferentiated germ cellsCell-specific knockdownEscort cellsGSC establishmentGSC lossPiwi knockdownPiRNA pathwayGenome stabilityTE transcriptsPIWI 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 ResearchConceptsPIWI-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 actsPiwiPIWI proteins are essential for early Drosophila embryogenesis
Mani SR, Megosh H, Lin H. PIWI proteins are essential for early Drosophila embryogenesis. Developmental Biology 2013, 385: 340-349. PMID: 24184635, PMCID: PMC3915879, DOI: 10.1016/j.ydbio.2013.10.017.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsArgonaute ProteinsDrosophila melanogasterDrosophila ProteinsEmbryonic DevelopmentConceptsPIWI proteinsMitotic defectsEarly embryogenesisArgonaute/PIWI protein familySmall non-coding RNAsEarly Drosophila embryogenesisAsynchronous nuclear divisionPosttranscriptional gene regulationSevere mitotic defectsPIWI protein familyNon-coding RNAsCell cycle progressionCell cycle arrestGermline developmentDrosophila embryogenesisChromatin structureGene regulationSyncytial embryosMitotic machinerySomatic nucleiProtein familyPiwiNuclear divisionNuclear migrationEssential functionsChromatin Immunoprecipitation Assay of Piwi in Drosophila
Yin H, Lin H. Chromatin Immunoprecipitation Assay of Piwi in Drosophila. Methods In Molecular Biology 2013, 1093: 1-11. PMID: 24178552, DOI: 10.1007/978-1-62703-694-8_1.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsArgonaute ProteinsCell NucleusChromatin ImmunoprecipitationDrosophila melanogasterDrosophila ProteinsFemaleGenomicsConceptsSmall RNA pathwaysRNA pathwaysArgonaute protein familyChromatin-associated factorsChromatin immunoprecipitation methodChromatin immunoprecipitation assaysWhole-genome mappingArgonaute proteinsDrosophila PiwiEpigenetic regulationDevelopmental biologyProtein familyImmunoprecipitation assaysCell biologyImmunoprecipitation methodHigh-resolution mapsPiwiEffector componentsBiologyPathwayGeneral utilityDrosophilaEpigenomeBiogenesisEpigenetics