2019
Cardiomyocyte orientation modulated by the Numb family proteins–N-cadherin axis is essential for ventricular wall morphogenesis
Miao L, Li J, Li J, Lu Y, Shieh D, Mazurkiewicz JE, Barroso M, Schwarz JJ, Xin HB, Singer HA, Vincent PA, Zhong W, Radice GL, Wan LQ, Fan ZC, Huang G, Wu M. Cardiomyocyte orientation modulated by the Numb family proteins–N-cadherin axis is essential for ventricular wall morphogenesis. Proceedings Of The National Academy Of Sciences Of The United States Of America 2019, 116: 15560-15569. PMID: 31300538, PMCID: PMC6681736, DOI: 10.1073/pnas.1904684116.Peer-Reviewed Original ResearchConceptsWall morphogenesisMembrane localizationPlasma membraneCellular orientationSingle-cell lineage tracingMitotic spindle orientationDouble knockout heartsN-cadherin overexpressionPostendocytic recyclingSpindle orientationRecycling endosomesN-cadherin levelsEndocytic organellesKnockin lineLineage tracingMorphogenesisCellular behaviorTrabecular morphogenesisNull cardiomyocytesNumbVentricular compactionMosaic modelControl cellsLocalizationMdKOOpposing Gradients of MicroRNA Expression Temporally Pattern Layer Formation in the Developing Neocortex
Shu P, Wu C, Ruan X, Liu W, Hou L, Fu H, Wang M, Liu C, Zeng Y, Chen P, Yin B, Yuan J, Qiang B, Peng X, Zhong W. Opposing Gradients of MicroRNA Expression Temporally Pattern Layer Formation in the Developing Neocortex. Developmental Cell 2019, 49: 764-785.e4. PMID: 31080058, DOI: 10.1016/j.devcel.2019.04.017.Peer-Reviewed Original Research
2014
Precardiac deletion of Numb and Numblike reveals renewal of cardiac progenitors
Shenje LT, Andersen P, Uosaki H, Fernandez L, Rainer PP, Cho GS, Lee DI, Zhong W, Harvey RP, Kass DA, Kwon C. Precardiac deletion of Numb and Numblike reveals renewal of cardiac progenitors. ELife 2014, 3: e02164. PMID: 24843018, PMCID: PMC4007206, DOI: 10.7554/elife.02164.Peer-Reviewed Original Research
2013
Numb family proteins are essential for cardiac morphogenesis and progenitor differentiation
Zhao C, Guo H, Li J, Myint T, Pittman W, Yang L, Zhong W, Schwartz RJ, Schwarz JJ, Singer HA, Tallquist MD, Wu M. Numb family proteins are essential for cardiac morphogenesis and progenitor differentiation. Development 2013, 141: 281-295. PMID: 24335256, PMCID: PMC3879810, DOI: 10.1242/dev.093690.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsCell DifferentiationCell LineageCell ProliferationEmbryonic Stem CellsFemaleHeartHeart Defects, CongenitalIntracellular Signaling Peptides and ProteinsMaleMembrane ProteinsMiceMice, KnockoutMice, TransgenicMorphogenesisMyocardiumMyocytes, CardiacNerve Tissue ProteinsPregnancyReceptor, Notch1Signal TransductionConceptsNumb family proteinsCardiac progenitor differentiationCardiac progenitor cell differentiationSecond heart fieldProgenitor differentiationCardiac morphogenesisEndocytosis-dependent mannerProgenitor cell differentiationFamily proteinsCell differentiationOFT alignmentMultiple progenitor cell typesCell fate determinantsLate cardiac developmentEarly embryonic lethalityMRNA deep sequencingProgenitor cell typesSuppression of Notch1Fate determinantsNotch1 intracellular domainEmbryonic lethalEmbryonic lethalityReporter linesDifferentiation defectsHeart field
2008
Going Nuclear Is Again a Winning (Wnt) Strategy
Zhong W. Going Nuclear Is Again a Winning (Wnt) Strategy. Developmental Cell 2008, 15: 635-636. PMID: 19000826, DOI: 10.1016/j.devcel.2008.10.012.Peer-Reviewed Original Research
2007
The Mammalian Golgi Regulates Numb Signaling in Asymmetric Cell Division by Releasing ACBD3 during Mitosis
Zhou Y, Atkins JB, Rompani SB, Bancescu DL, Petersen PH, Tang H, Zou K, Stewart SB, Zhong W. The Mammalian Golgi Regulates Numb Signaling in Asymmetric Cell Division by Releasing ACBD3 during Mitosis. Cell 2007, 129: 163-178. PMID: 17418793, DOI: 10.1016/j.cell.2007.02.037.Peer-Reviewed Original ResearchMeSH KeywordsAdaptor Proteins, Signal TransducingAnimalsAnimals, Genetically ModifiedCell DivisionCell LineageCytosolDrosophilaEmbryo, MammalianEmbryo, NonmammalianEmbryonic DevelopmentGolgi ApparatusMembrane ProteinsMiceMitosisNerve Tissue ProteinsNeuronsPhenotypeProtein Structure, TertiaryReceptors, GABA-ASignal TransductionStem CellsConceptsCell fate specificationNumb proteinDaughter cellsGolgi fragmentationCell cycleMammalian neural progenitor cellsAsymmetric cell divisionProgenitor cell cycleProgenitor cellsCell cycle progressionNeural progenitor cellsMammalian GolgiCell fateCell divisionNeuronal fateACBD3Golgi apparatusSubcellular distributionNeuronal differentiationPhenotypic similarityNumbMitosisNeuron productionProteinCells
2006
The Enigma of the Numb-Notch Relationship during Mammalian Embryogenesis
Petersen PH, Tang H, Zou K, Zhong W. The Enigma of the Numb-Notch Relationship during Mammalian Embryogenesis. Developmental Neuroscience 2006, 28: 156-168. PMID: 16508312, DOI: 10.1159/000090761.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsBody PatterningCell DifferentiationCell DivisionCell LineageDrosophila melanogasterEmbryo, MammalianEmbryo, NonmammalianEmbryonic DevelopmentGene Expression Regulation, DevelopmentalGenes, HomeoboxMammalsMembrane ProteinsMesodermMiceMice, Mutant StrainsMutationNerve Tissue ProteinsProtein IsoformsReceptors, NotchSomitesStem CellsConceptsAsymmetric cell divisionAntagonistic rolesCell divisionCell fate specificationStem cell maintenanceDefective Notch signalingEmbryonic nervous systemStem/progenitor cellsMammalian embryogenesisNeural stem/progenitor cellsFate specificationCell fateNumb proteinCell maintenanceNumb isoformsMammalian neurogenesisMolecular basisNotch signalingDifferent fatesNumbDifferential regulationStem cellsProgenitor cellsEmbryogenesisPremature depletion
2005
Numb Proteins Specify Asymmetric Cell Fates via an Endocytosis- and Proteasome-Independent Pathway
Tang H, Rompani SB, Atkins JB, Zhou Y, Osterwalder T, Zhong W. Numb Proteins Specify Asymmetric Cell Fates via an Endocytosis- and Proteasome-Independent Pathway. Molecular And Cellular Biology 2005, 25: 2899-2909. PMID: 15798180, PMCID: PMC1069617, DOI: 10.1128/mcb.25.8.2899-2909.2005.Peer-Reviewed Original ResearchMeSH KeywordsAmino Acid MotifsAmino Acid SequenceAnimalsCell DivisionDrosophila melanogasterDrosophila ProteinsEndocytosisJuvenile HormonesMembrane ProteinsMiceMolecular Sequence DataNerve Tissue ProteinsNeuropeptidesProteasome Endopeptidase ComplexProteasome InhibitorsReceptors, NotchSignal TransductionTwo-Hybrid System TechniquesVesicular Transport ProteinsConceptsNumb proteinProteasome-independent pathwayAsymmetric cell fate specificationAsymmetric cell fatesCell fate specificationEps15 homology (EH) domainE3 ubiquitin ligasesNotch protein levelsCell-cell communicationAlpha-adaptinFate specificationEndocytic proteinsDistinct binding motifsDrosophila melanogasterAsymmetric divisionCell fateHomology domainUbiquitin ligasesDaughter cellsNotch activityBinding motifEndocytosisHomologue 1Proteasome activityCell surfaceEffects of canonical Wnt signaling on dorso-ventral specification of the mouse telencephalon
Backman M, Machon O, Mygland L, van den Bout CJ, Zhong W, Taketo MM, Krauss S. Effects of canonical Wnt signaling on dorso-ventral specification of the mouse telencephalon. Developmental Biology 2005, 279: 155-168. PMID: 15708565, DOI: 10.1016/j.ydbio.2004.12.010.Peer-Reviewed Original ResearchThe Notch Regulator Numb Links the Notch and TCR Signaling Pathways
Anderson AC, Kitchens EA, Chan SW, St. Hill C, Jan YN, Zhong W, Robey EA. The Notch Regulator Numb Links the Notch and TCR Signaling Pathways. The Journal Of Immunology 2005, 174: 890-897. PMID: 15634911, DOI: 10.4049/jimmunol.174.2.890.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsAntigen-Presenting CellsCell DifferentiationCells, CulturedGene DeletionIntracellular Signaling Peptides and ProteinsMembrane ProteinsMiceMice, TransgenicNerve Tissue ProteinsReceptor, Notch1Receptors, Antigen, T-CellReceptors, Cell SurfaceSignal TransductionT-LymphocytesThymus GlandTranscription FactorsConceptsT cell developmentTCR signaling pathwaysCell developmentSignaling pathwaysAbsence of NumbT cell-APC interactionsInhibitor of NotchProtein NumbImportant adapterRelated proteinsNumbAPC contactMature T cellsTCR signalsCell membraneT cell activationPhysical interactionPathwayCell activationNotchImportant roleNumblikeProteinMutationsCoclusters
2004
Targeted deletion of numb and numblike in sensory neurons reveals their essential functions in axon arborization
Huang EJ, Li H, Tang AA, Wiggins AK, Neve RL, Zhong W, Jan LY, Jan YN. Targeted deletion of numb and numblike in sensory neurons reveals their essential functions in axon arborization. Genes & Development 2004, 19: 138-151. PMID: 15598981, PMCID: PMC540232, DOI: 10.1101/gad.1246005.Peer-Reviewed Original ResearchConceptsNuclear Notch1Sensory neuronsAxon arborizationAccumulation of Notch1Conditional mouse mutantsAxon branch pointsAfferent fibersSensory gangliaAxonal arborizationAxonal lengthSevere reductionAxon lengthArborizationCre recombinaseNotch1Endocytic-lysosomal pathwayTargeted deletionSignificant increaseUnknown mechanismNeuronsOverexpression of NumbMouse mutantsGangliaNeurogenesisPathwayContinuing role for mouse Numb and Numbl in maintaining progenitor cells during cortical neurogenesis
Petersen PH, Zou K, Krauss S, Zhong W. Continuing role for mouse Numb and Numbl in maintaining progenitor cells during cortical neurogenesis. Nature Neuroscience 2004, 7: 803-811. PMID: 15273690, DOI: 10.1038/nn1289.Peer-Reviewed Original ResearchConceptsMouse NumbProgenitor cellsEarly neurogenesisAsymmetric cell divisionProgenitor cell maintenanceLoss of NumbNeural progenitor cellsProgenitor cell depletionDrosophila melanogasterCell fateCell divisionNeuronal fateNumblNumbCortical neurogenesisStem cellsGeneral mechanismDorsal forebrainNeurogenesisCellsNervous systemFateSpecific malformationsDifferent neuronsMelanogasterMajor Molecular Differences between Mammalian Sexes Are Involved in Drug Metabolism and Renal Function
Rinn JL, Rozowsky JS, Laurenzi IJ, Petersen PH, Zou K, Zhong W, Gerstein M, Snyder M. Major Molecular Differences between Mammalian Sexes Are Involved in Drug Metabolism and Renal Function. Developmental Cell 2004, 6: 791-800. PMID: 15177028, DOI: 10.1016/j.devcel.2004.05.005.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsDNAFemaleGene Expression ProfilingGene Expression RegulationGenitaliaHumansHypothalamusKidneyLiverMaleMetabolic Clearance RateMiceOligonucleotide Array Sequence AnalysisOrgan SpecificityOvaryPharmaceutical PreparationsReceptors, Cell SurfaceSerpinsSex CharacteristicsTestisTranscortinConceptsMolecular differencesGene expressionExtensive differential gene expressionReproductive tissuesDifferential gene expressionGene expression differencesCellular rolesMammalian sexMouse geneMajor molecular differencesExpression differencesAdult tissuesOsmotic regulationExpression patternsFemale hypothalamusMolecular levelPhysiological differencesGenesDifferent hormonal environmentsRenal functionHormonal environmentExpressionSteroid metabolismMetabolismDrug metabolismNestin promoter/enhancer directs transgene expression to precursors of adult generated periglomerular neurons
Beech RD, Cleary MA, Treloar HB, Eisch AJ, Harrist AV, Zhong W, Greer CA, Duman RS, Picciotto MR. Nestin promoter/enhancer directs transgene expression to precursors of adult generated periglomerular neurons. The Journal Of Comparative Neurology 2004, 475: 128-141. PMID: 15176089, DOI: 10.1002/cne.20179.Peer-Reviewed Original ResearchConceptsPG neuronsSubventricular zoneGranule cellsOlfactory bulbMajor neurogenic regionsAdult-generated neuronsSVZ precursor cellsTetracycline transactivatorRostral migratory streamOlfactory bulb interneuronsTransgene expressionPeriglomerular neuronsPeriglomerular cellsNestin promoterTyrosine hydroxylaseAdult brainInterneuronal populationsBulb interneuronsNeurogenic regionsMigratory streamNeuronal precursorsNeuronsUnique subsetPromoter/enhancerPrecursor cells
2002
Asymmetric Numb distribution is critical for asymmetric cell division of mouse cerebral cortical stem cells and neuroblasts.
Shen Q, Zhong W, Jan YN, Temple S. Asymmetric Numb distribution is critical for asymmetric cell division of mouse cerebral cortical stem cells and neuroblasts. Development 2002, 129: 4843-53. PMID: 12361975, DOI: 10.1242/dev.129.20.4843.Peer-Reviewed Original ResearchConceptsAsymmetric cell divisionCell divisionMouse cortical developmentCell fateStem cellsProgenitor cellsDiverse cell fatesNeural cell fateMouse cortical neurogenesisNext cell divisionEmbryonic mouse cortexDrosophila neurogenesisProgenitor marker nestinAsymmetric segregationLineage treesNumb proteinCortical stem cellsMouse homologueNotch activityWild typeNumbNeuronal differentiationNeuronal cellsCortical neurogenesisCortical developmentProgenitor cell maintenance requires numb and numblike during mouse neurogenesis
Petersen PH, Zou K, Hwang JK, Jan YN, Zhong W. Progenitor cell maintenance requires numb and numblike during mouse neurogenesis. Nature 2002, 419: 929-934. PMID: 12410312, DOI: 10.1038/nature01124.Peer-Reviewed Original ResearchConceptsMouse NumbNeural progenitor cellsMolecular mechanismsProgenitor cellsProgenitor cell maintenanceMammalian nervous systemOnset of neurogenesisConserved homologuesMutant embryosCourse of neurogenesisCell maintenanceMouse neurogenesisNeuronal fateNumbDividing cellsNeural cellsEarly neuronsNervous systemCritical roleProgenitorsCellsNeurogenesisDrosophilaTemporal patternsEmbryogenesis
2000
Mouse numb is an essential gene involved in cortical neurogenesis
Zhong W, Jiang M, Schonemann M, Meneses J, Pedersen R, Jan L, Jan Y. Mouse numb is an essential gene involved in cortical neurogenesis. Proceedings Of The National Academy Of Sciences Of The United States Of America 2000, 97: 6844-6849. PMID: 10841580, PMCID: PMC18761, DOI: 10.1073/pnas.97.12.6844.Peer-Reviewed Original ResearchConceptsEssential genesDaughter cellsProgenitor cellsCranial neural tube closureFunction mutant allelesApical daughter cellMembrane-associated proteinsProgenitor cell fateCortical neurogenesisNeural tube closureEmbryonic day 11.5Neural progenitor cellsCortical progenitor cellsNumb functionsCell fateApical cell membraneNumb geneSevere defectsTube closureMutant allelesNeural developmentDay 11.5Cell membraneGenesMammalian neocortex
1999
DLX‐1, DLX‐2, and DLX‐5 expression define distinct stages of basal forebrain differentiation
Eisenstat D, Liu J, Mione M, Zhong W, Yu G, Anderson S, Ghattas I, Puelles L, Rubenstein J. DLX‐1, DLX‐2, and DLX‐5 expression define distinct stages of basal forebrain differentiation. The Journal Of Comparative Neurology 1999, 414: 217-237. PMID: 10516593, DOI: 10.1002/(sici)1096-9861(19991115)414:2<217::aid-cne6>3.0.co;2-i.Peer-Reviewed Original ResearchMeSH Keywords3T3 CellsAnimalsAntibody SpecificityBasal GangliaCell DifferentiationCell NucleusCerebral VentriclesCytoplasmGene Expression Regulation, DevelopmentalHomeodomain ProteinsIn Situ HybridizationIsomerismMiceMitosisMutagenesisNeuronsProsencephalonRecombinant ProteinsRNA, MessengerS PhaseTranscription FactorsConceptsDlx-2Dlx-1Dlx-5Dlx genesDlx-5 expressionEmbryonic day 10.5Ventricular zoneDlx proteinsDlx familyM phase cellsCraniofacial morphogenesisHomeobox genesSingle mutantsDaughter cellsDay 10.5GenesForebrain differentiationProteinSame cellsMouse forebrainMild phenotypeCellsDifferentiationExpressionDistinct stages
1997
Differential expression of mammalian Numb, Numblike and Notch1 suggests distinct roles during mouse cortical neurogenesis
Zhong W, Jiang M, Weinmaster G, Jan L, Jan Y. Differential expression of mammalian Numb, Numblike and Notch1 suggests distinct roles during mouse cortical neurogenesis. Development 1997, 124: 1887-1897. PMID: 9169836, DOI: 10.1242/dev.124.10.1887.Peer-Reviewed Original ResearchMeSH KeywordsAmino Acid SequenceAnimalsBase SequenceCerebral CortexCloning, MolecularCytoplasmDrosophilaDrosophila ProteinsGene Expression Regulation, DevelopmentalGenesIntracellular Signaling Peptides and ProteinsJuvenile HormonesMembrane ProteinsMiceModels, NeurologicalMolecular Sequence DataMorphogenesisMutationNerve Tissue ProteinsNervous SystemNeuronsOrgan SpecificityReceptor, Notch1Receptors, Cell SurfaceRecombinant Fusion ProteinsRNA, MessengerSequence Homology, Amino AcidStem CellsTranscription FactorsConceptsDaughter cellsNeural precursorsMammalian cortical neurogenesisAsymmetric cell divisionSignificant sequence similarityMouse cortical neurogenesisCortical neurogenesisEmbryonic nervous systemFunction mutant embryosCell-cell interactionsCell-intrinsic mechanismsMammalian NumbMouse NumbNumb lossProgenitor cell proliferationDrosophila neurogenesisMammalian genesMutant embryosCell-extrinsic mechanismsSequence similarityCell divisionDifferential segregationNumblikePostmitotic neuronsNumb
1996
Asymmetric Localization of a Mammalian Numb Homolog during Mouse Cortical Neurogenesis
Zhong W, Feder J, Jiang M, Jan L, Jan Y. Asymmetric Localization of a Mammalian Numb Homolog during Mouse Cortical Neurogenesis. Neuron 1996, 17: 43-53. PMID: 8755477, DOI: 10.1016/s0896-6273(00)80279-2.Peer-Reviewed Original ResearchMeSH KeywordsAmino Acid SequenceAnimalsCell DivisionCell MembraneCerebral CortexDrosophilaDrosophila ProteinsEmbryo, MammalianEmbryo, NonmammalianEmbryonic and Fetal DevelopmentJuvenile HormonesMembrane ProteinsMiceMolecular Sequence DataMutationNeuronsRatsReceptors, Cell SurfaceReceptors, NotchSequence Homology, Amino AcidTissue DistributionConceptsMouse cortical neurogenesisDaughter cellsAsymmetric cell divisionCortical neurogenesisCell-cell interactionsDrosophila neurogenesisMammalian homologMutant phenotypeMouse Notch1Drosophila embryosDistinct fatesDrosophila NumbAsymmetric divisionAsymmetric localizationCell divisionDifferential segregationMolecular mechanismsNeural progenitorsNumbNeural precursorsApical membraneHomologNeurogenesisInvertebratesVertebrates