2021
Maternal Piwi regulates primordial germ cell development to ensure the fertility of female progeny in Drosophila
Gonzalez LE, Tang X, Lin H. Maternal Piwi regulates primordial germ cell development to ensure the fertility of female progeny in Drosophila. Genetics 2021, 219: iyab091. PMID: 34142134, PMCID: PMC8757300, DOI: 10.1093/genetics/iyab091.Peer-Reviewed Original ResearchConceptsPIWI-interacting RNAsGermline developmentPiwi knockdownPIWI proteinsEarly embryosPiwi/piRNA complexesPIWI/piRNA pathwayFemale progenyPrimordial germ cell developmentGermline sex determinationLoss of PiwiGermline stem cellsDrosophila early embryosGerm cell developmentGerm cell proliferationGonad coalescencePiRNA complexesPiRNA pathwayPiRNA poolTransposon suppressionZygotic genesEmbryonic germlineEmbryonic functionEarly embryogenesisPiwiGenome-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
2016
Tudor-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 fertilityPiwi 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
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 ResearchConceptsPIWI 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 ResearchConceptsSmall RNA pathwaysRNA pathwaysArgonaute protein familyChromatin-associated factorsChromatin immunoprecipitation methodChromatin immunoprecipitation assaysWhole-genome mappingArgonaute proteinsDrosophila PiwiEpigenetic regulationDevelopmental biologyProtein familyImmunoprecipitation assaysCell biologyImmunoprecipitation methodHigh-resolution mapsPiwiEffector componentsBiologyPathwayGeneral utilityDrosophilaEpigenomeBiogenesisEpigeneticsA 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
2011
Small Noncoding RNAs in the Germline
Saxe JP, Lin H. Small Noncoding RNAs in the Germline. Cold Spring Harbor Perspectives In Biology 2011, 3: a002717. PMID: 21669983, PMCID: PMC3181032, DOI: 10.1101/cshperspect.a002717.Peer-Reviewed Original ResearchConceptsRNA pathwaysSmall noncoding RNAsTarget mRNAsNoncoding RNAsSmall RNA pathwaysPiRNA pathwayGermline specificationMicroRNA pathwayMiRNA pathwayGene regulationMRNA translationSomatic tissuesEpigenetic programmingDiverse functionsGene expressionRegulatory functionsGermlinePotent regulatorPathwayRNAMRNARegulationPiwiBiogenesisTransposon
2010
Drosophila Piwi functions in Hsp90-mediated suppression of phenotypic variation
Gangaraju VK, Yin H, Weiner MM, Wang J, Huang XA, Lin H. Drosophila Piwi functions in Hsp90-mediated suppression of phenotypic variation. Nature Genetics 2010, 43: 153-158. PMID: 21186352, PMCID: PMC3443399, DOI: 10.1038/ng.743.Peer-Reviewed Original ResearchMeSH KeywordsAllelesAnimalsArgonaute ProteinsDNA Transposable ElementsDrosophila melanogasterDrosophila ProteinsElectrophoresis, Gel, Two-DimensionalEpigenesis, GeneticFemaleGene SilencingGenetic VariationGreen Fluorescent ProteinsHSP90 Heat-Shock ProteinsMaleOvaryPhenotypeRNA-Induced Silencing ComplexThe Yb Body, a Major Site for Piwi-associated RNA Biogenesis and a Gateway for Piwi Expression and Transport to the Nucleus in Somatic Cells*
Qi H, Watanabe T, Ku HY, Liu N, Zhong M, Lin H. The Yb Body, a Major Site for Piwi-associated RNA Biogenesis and a Gateway for Piwi Expression and Transport to the Nucleus in Somatic Cells*. Journal Of Biological Chemistry 2010, 286: 3789-3797. PMID: 21106531, PMCID: PMC3030380, DOI: 10.1074/jbc.m110.193888.Peer-Reviewed Original ResearchConceptsYb bodiesSomatic cellsPiRNA pathwayGerm lineEndo-siRNA pathwaySomatic niche cellsTudor-like domainGonadal somatic cellsPutative RNA helicaseCo-immunoprecipitation experimentsSomatic stem cellsFlamenco locusSomatic piRNAsPiRNA biogenesisEndo-siRNAsRNA biogenesisRNA pathwaysPiwi expressionRNA helicaseNovel proteinPiwiNiche cellsMolecular basisStem cellsBiogenesisA Drosophila Chromatin Factor Interacts With the Piwi-Interacting RNA Mechanism in Niche Cells to Regulate Germline Stem Cell Self-Renewal
Smulders-Srinivasan TK, Szakmary A, Lin H. A Drosophila Chromatin Factor Interacts With the Piwi-Interacting RNA Mechanism in Niche Cells to Regulate Germline Stem Cell Self-Renewal. Genetics 2010, 186: 573-583. PMID: 20647505, PMCID: PMC2954472, DOI: 10.1534/genetics.110.119081.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsArgonaute ProteinsChromatinChromosomal Proteins, Non-HistoneDNA-Binding ProteinsDrosophilaDrosophila ProteinsEpigenesis, GeneticFemaleGerm CellsHedgehog ProteinsMalePolycomb-Group ProteinsPolymerase Chain ReactionRepressor ProteinsRNA-Induced Silencing ComplexRNA, Small InterferingSignal TransductionStem Cell NicheStem CellsConceptsGermline stem cellsNiche cellsEpigenetic programmingStem Cell Self-RenewalEnhancer of PolycombTrithorax group genesPotential genetic interactionsCell Self-RenewalNovel epigenetic mechanismStem cellsDrosophila ovaryGSC divisionChromatin factorsNiche signalingChromatin proteinsGenetic interactionsPiwi expressionStem cell defectEpigenetic regulationPiwiEpigenetic mechanismsGroup genesRNA mechanismExpression of hedgehogSelf-Renewal
2007
An epigenetic activation role of Piwi and a Piwi-associated piRNA in Drosophila melanogaster
Yin H, Lin H. An epigenetic activation role of Piwi and a Piwi-associated piRNA in Drosophila melanogaster. Nature 2007, 450: 304-308. PMID: 17952056, DOI: 10.1038/nature06263.Peer-Reviewed Original ResearchDrosophila PIWI associates with chromatin and interacts directly with HP1a
Brower-Toland B, Findley SD, Jiang L, Liu L, Yin H, Dus M, Zhou P, Elgin SC, Lin H. Drosophila PIWI associates with chromatin and interacts directly with HP1a. Genes & Development 2007, 21: 2300-2311. PMID: 17875665, PMCID: PMC1973144, DOI: 10.1101/gad.1564307.Peer-Reviewed Original ResearchMeSH KeywordsAmino Acid MotifsAnimalsArgonaute ProteinsBinding SitesChromatinChromobox Protein Homolog 5Chromosomal Proteins, Non-HistoneDrosophila melanogasterDrosophila ProteinsEmbryo, NonmammalianFemaleGene SilencingMaleModels, MolecularNuclear ProteinsProtein BindingProteinsRNA-Induced Silencing ComplexConceptsHeterochromatin protein 1aPIWI-interacting RNAsEpigenetic changesChromatin-associated proteinsProtein family membersNormal silencingHeterochromatic genesFly genomeHeterochromatin componentsChromatin modifiersEpigenetic stateEpigenetic regulationRNA mechanismFruit flyPiwiTerminal domainProtein 1ACentral playerRNASpecific sequencesDirect interactionGenomeGenesMotifCellular systems
2006
The Role of PIWI and the miRNA Machinery in Drosophila Germline Determination
Megosh HB, Cox DN, Campbell C, Lin H. The Role of PIWI and the miRNA Machinery in Drosophila Germline Determination. Current Biology 2006, 16: 1884-1894. PMID: 16949822, DOI: 10.1016/j.cub.2006.08.051.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsArgonaute ProteinsBody PatterningCell DifferentiationDEAD-box RNA HelicasesDrosophilaDrosophila ProteinsEmbryo, NonmammalianEmbryonic DevelopmentFragile X Mental Retardation ProteinGene Expression Regulation, DevelopmentalGerm CellsMicroRNAsProteinsRibonuclease IIIRNA HelicasesRNA-Induced Silencing ComplexRNA, Small InterferingConceptsGermline determinationDicer-1Dicer-2MiRNA pathwayRole of PiwiReduced PGC numbersNumber of PGCsMiRISC complexesRasiRNA pathwayGermline specificationDrosophila PiwiSiRNA pathwayAbdominal patterningVasa expressionTranslational regulationPGC numberPiwiMiRNA machineryGerm plasmMolecular activityPolar granuleDFMRPCell formationOSKMaternal component
2005
Regulatory Relationship among piwi, pumilio, and bag-of-marbles in Drosophila Germline Stem Cell Self-Renewal and Differentiation
Szakmary A, Cox DN, Wang Z, Lin H. Regulatory Relationship among piwi, pumilio, and bag-of-marbles in Drosophila Germline Stem Cell Self-Renewal and Differentiation. Current Biology 2005, 15: 171-178. PMID: 15668175, DOI: 10.1016/j.cub.2005.01.005.Peer-Reviewed Original ResearchConceptsGermline stem cellsPiwi functionDrosophila ovarian germline stem cellsOvarian germline stem cellsStem Cell Self-RenewalFunction of PiwiDifferentiated daughter cellsCell Self-RenewalGerm cell divisionBam proteinCystoblast differentiationBam expressionMutant ovariesNiche signalsDouble mutantDaughter cellsDifferentiation genesPiwiCell divisionNiche cellsRegulatory relationshipsSelf-RenewalGerm cellsMutantsCystoblasts
2004
Mili, a mammalian member of piwi family gene, is essential for spermatogenesis
Kuramochi-Miyagawa S, Kimura T, Ijiri TW, Isobe T, Asada N, Fujita Y, Ikawa M, Iwai N, Okabe M, Deng W, Lin H, Matsuda Y, Nakano T. Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development 2004, 131: 839-849. PMID: 14736746, DOI: 10.1242/dev.00973.Peer-Reviewed Original ResearchConceptsPiwi family genesFamily genesPrimordial germ cell developmentPost-transcriptional regulationGerm cell developmentGerm cell productionPhysical binding propertiesMammalian homologPIWI domainMammalian membersTranslational regulationMouse homologDifferentiation of spermatocytesEarly prophaseMILIFunctional associationTargeted mutationsCell developmentFirst meiosisGenesPiwiEarly pachyteneStem cellsSpermatocyte stageHomolog