2023
Neonatal loss of FGFR2 in astroglial cells affects locomotion, sociability, working memory, and glia-neuron interactions in mice
Stevens H, Scuderi S, Collica S, Tomasi S, Horvath T, Vaccarino F. Neonatal loss of FGFR2 in astroglial cells affects locomotion, sociability, working memory, and glia-neuron interactions in mice. Translational Psychiatry 2023, 13: 89. PMID: 36906620, PMCID: PMC10008554, DOI: 10.1038/s41398-023-02372-y.Peer-Reviewed Original ResearchConceptsFibroblast growth factor receptor 2Anxiety-like behaviorAttention deficit hyperactivity disorderAstroglial cellsGrowth factor receptor 2Reduced anxiety-like behaviorGlia-neuron interactionsAstroglial cell functionEarly postnatal periodFactor receptor 2Early postnatal lossPostnatal mouse brainWeeks of ageDeficit hyperactivity disorderGlial cellsGlutamine synthetase expressionBehavioral deficitsPostnatal periodReceptor 2Floxed miceHGFAP-CreMouse brainNeonatal lossPostnatal astrogliaPostnatal loss
2020
Antibodies From Children With PANDAS Bind Specifically to Striatal Cholinergic Interneurons and Alter Their Activity
Xu J, Liu RJ, Fahey S, Frick L, Leckman J, Vaccarino F, Duman RS, Williams K, Swedo S, Pittenger C. Antibodies From Children With PANDAS Bind Specifically to Striatal Cholinergic Interneurons and Alter Their Activity. American Journal Of Psychiatry 2020, 178: 48-64. PMID: 32539528, PMCID: PMC8573771, DOI: 10.1176/appi.ajp.2020.19070698.Peer-Reviewed Original ResearchConceptsStriatal cholinergic interneuronsCholinergic interneuronsMouse brain slicesObsessive-compulsive disorderControl subjectsBrain slicesPediatric autoimmune neuropsychiatric disordersIntravenous immunoglobulin treatmentAutoimmune neuropsychiatric disordersAcute mouse brain slicesParvalbumin-expressing GABAergic interneuronsPediatric obsessive-compulsive disorderBrain antigensImmunoglobulin treatmentBaseline serumStreptococcal infectionCritical cellular targetsSymptom improvementGABAergic interneuronsInduced autoimmunityIgG antibodiesMouse slicesIndependent cohortBehavioral pathologyNeuron types
2018
Fibroblast growth factor 2 is necessary for the antidepressant effects of fluoxetine
Simard S, Shail P, MacGregor J, Sayed M, Duman RS, Vaccarino FM, Salmaso N. Fibroblast growth factor 2 is necessary for the antidepressant effects of fluoxetine. PLOS ONE 2018, 13: e0204980. PMID: 30273396, PMCID: PMC6166983, DOI: 10.1371/journal.pone.0204980.Peer-Reviewed Original ResearchConceptsChronic variable stressSelective serotonin reuptake inhibitorsPost-mortem brainsGlucocorticoid receptorTherapeutic effectMood disordersAnxiety behaviorFgf2 knockout miceAnti-depressant effectsSerotonin reuptake inhibitorsEffects of fluoxetineTreatment of depressionHippocampal glucocorticoid receptorsAnti-depressant medicationWild-type miceEffect of CVSAnti-depressive agentsNovel therapeutic targetFGF2 geneFibroblast growth factor-2HPA changesAstroglial functionAntidepressant effectsAntidepressant medicationAntidepressant treatment
2016
Fibroblast Growth Factor 2 Modulates Hypothalamic Pituitary Axis Activity and Anxiety Behavior Through Glucocorticoid Receptors
Salmaso N, Stevens HE, McNeill J, ElSayed M, Ren Q, Maragnoli ME, Schwartz ML, Tomasi S, Sapolsky RM, Duman R, Vaccarino FM. Fibroblast Growth Factor 2 Modulates Hypothalamic Pituitary Axis Activity and Anxiety Behavior Through Glucocorticoid Receptors. Biological Psychiatry 2016, 80: 479-489. PMID: 27133954, PMCID: PMC8009045, DOI: 10.1016/j.biopsych.2016.02.026.Peer-Reviewed Original ResearchConceptsFibroblast growth factor-2Hippocampal glucocorticoid receptor expressionGlucocorticoid receptor expressionAdrenal axis activityKO miceAxis activityAnxiety behaviorReceptor expressionHypothalamic-pituitary axis activityReceptor KO miceFGF2 administrationWild-type miceGrowth factor 2Receptor subtypesTherapeutic effectNeuroendocrine studiesAdult miceGlucocorticoid receptorGR promoter regionsFGF2 levelsMeasures of anxietyMiceMotor behaviorFGF2 geneFactor 2
2015
Imbalance of excitatory/inhibitory synaptic protein expression in iPSC-derived neurons from FOXG1+/− patients and in foxg1+/− mice
Patriarchi T, Amabile S, Frullanti E, Landucci E, Lo Rizzo C, Ariani F, Costa M, Olimpico F, W Hell J, M Vaccarino F, Renieri A, Meloni I. Imbalance of excitatory/inhibitory synaptic protein expression in iPSC-derived neurons from FOXG1+/− patients and in foxg1+/− mice. European Journal Of Human Genetics 2015, 24: 871-880. PMID: 26443267, PMCID: PMC4820038, DOI: 10.1038/ejhg.2015.216.Peer-Reviewed Original ResearchConceptsRett syndromeSynaptic markersInhibitory synapsesExcitatory/inhibitory balanceSynaptic protein expressionFetal mouse brainInhibitory synaptic markersPathogenesis of RTTExcitatory synaptic markersSevere neurodevelopmental disorderGlutamatergic markersInhibitory balanceAdult brainAdult micePrecise molecular mechanismsSynaptic differentiationPatientsMouse brainBrain synapsesPathological eventsNeuronsProtein expressionBrainGluD1Neurodevelopmental disordersAltered expression of neuropeptides in FoxG1-null heterozygous mutant mice
Frullanti E, Amabile S, Lolli MG, Bartolini A, Livide G, Landucci E, Mari F, Vaccarino FM, Ariani F, Massimino L, Renieri A, Meloni I. Altered expression of neuropeptides in FoxG1-null heterozygous mutant mice. European Journal Of Human Genetics 2015, 24: 252-257. PMID: 25966633, PMCID: PMC4717204, DOI: 10.1038/ejhg.2015.79.Peer-Reviewed Original ResearchConceptsBasal gangliaAdult brainParvalbumin-positive GABAergic interneuronsNeonatal brain developmentWild-type littermatesGroup of neuropeptidesHeterozygous mutant miceHippocampal neurogenesisImpaired social interactionCalcium-dependent signalingTotal brainGABAergic interneuronsNeuronal excitabilityControl of movementHippocampal neuronsArginine vasopressinBehavioral impairmentsWhole brainMammalian forebrainHeterozygous miceMutant miceFOXG1 geneBrain developmentBrainAltered expressionTargeted ablation of cholinergic interneurons in the dorsolateral striatum produces behavioral manifestations of Tourette syndrome
Xu M, Kobets A, Du JC, Lennington J, Li L, Banasr M, Duman RS, Vaccarino FM, DiLeone RJ, Pittenger C. Targeted ablation of cholinergic interneurons in the dorsolateral striatum produces behavioral manifestations of Tourette syndrome. Proceedings Of The National Academy Of Sciences Of The United States Of America 2015, 112: 893-898. PMID: 25561540, PMCID: PMC4311862, DOI: 10.1073/pnas.1419533112.Peer-Reviewed Original ResearchConceptsTourette syndromeCholinergic interneuronsDorsolateral striatumSensorimotor gatingD-amphetamine challengeLarge cholinergic interneuronsSpecific cell ablationInterneuron deficitsStriatal interneuronsAcute administrationGABAergic markersDopaminergic drugsAvailable treatmentsPostmortem studiesPrepulse inhibitionTic disordersSevere diseaseHuman putamenMotor coordinationInterneuronsTargeted ablationSevere endStriatumAcute stressGilles de
2014
Fgfr1 Inactivation in the Mouse Telencephalon Results in Impaired Maturation of Interneurons Expressing Parvalbumin
Smith KM, Maragnoli ME, Phull PM, Tran KM, Choubey L, Vaccarino FM. Fgfr1 Inactivation in the Mouse Telencephalon Results in Impaired Maturation of Interneurons Expressing Parvalbumin. PLOS ONE 2014, 9: e103696. PMID: 25116473, PMCID: PMC4130531, DOI: 10.1371/journal.pone.0103696.Peer-Reviewed Original ResearchConceptsGanglionic eminenceSoma sizeCortical interneuronsAstrocytes of miceCortex of adultCortical GABAergic neuronsParvalbumin-positive cortical interneuronsRadial glial cellsSmaller soma sizeMedial ganglionic eminenceFibroblast growth factorDeficient astrocytesLocomotor hyperactivityGABAergic cellsGABAergic neuronsInterneuron maturationGlial cellsCortical astrocytesPostnatal periodAdult CNSPostnatal brainInterneuron markersInterneuronsImmunopositive interneuronsAstrocytesLeptin signaling in astrocytes regulates hypothalamic neuronal circuits and feeding
Kim JG, Suyama S, Koch M, Jin S, Argente-Arizon P, Argente J, Liu ZW, Zimmer MR, Jeong JK, Szigeti-Buck K, Gao Y, Garcia-Caceres C, Yi CX, Salmaso N, Vaccarino FM, Chowen J, Diano S, Dietrich MO, Tschöp MH, Horvath TL. Leptin signaling in astrocytes regulates hypothalamic neuronal circuits and feeding. Nature Neuroscience 2014, 17: 908-910. PMID: 24880214, PMCID: PMC4113214, DOI: 10.1038/nn.3725.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsAstrocytesCell CountEatingExcitatory Postsynaptic PotentialsGlial Fibrillary Acidic ProteinHypothalamusImmunohistochemistryIn Situ HybridizationLeptinMaleMelanocortinsMiceMice, KnockoutMicroscopy, ElectronNerve NetNeuronsPrimary Cell CulturePro-OpiomelanocortinPulmonary Gas ExchangeReal-Time Polymerase Chain ReactionRNA, MessengerSignal Transduction
2013
Hypoxia-Induced Developmental Delays of Inhibitory Interneurons Are Reversed by Environmental Enrichment in the Postnatal Mouse Forebrain
Komitova M, Xenos D, Salmaso N, Tran KM, Brand T, Schwartz ML, Ment L, Vaccarino FM. Hypoxia-Induced Developmental Delays of Inhibitory Interneurons Are Reversed by Environmental Enrichment in the Postnatal Mouse Forebrain. Journal Of Neuroscience 2013, 33: 13375-13387. PMID: 23946395, PMCID: PMC3742925, DOI: 10.1523/jneurosci.5286-12.2013.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsCell Adhesion Molecules, NeuronalCerebral CortexChromatography, High Pressure LiquidDisease Models, AnimalExtracellular Matrix ProteinsGene Knock-In TechniquesHousing, AnimalHypoxiaImmunohistochemistryInterneuronsMiceMice, Inbred C57BLMice, TransgenicNerve Tissue ProteinsParvalbuminsProsencephalonReelin ProteinSerine EndopeptidasesSomatostatinConceptsCortical interneuronsNormoxic controlsMarker expressionPostnatal cortical developmentVasoactive intestinal peptidePostnatal day 3Central nervous systemTotal GABA contentImpact of hypoxicPostnatal mouse forebrainEnvironmental enrichmentIntestinal peptideGABAergic interneuronsFrontal neocortexInhibitory interneuronsCortical developmentMouse modelReelin expressionInterneuron numbersNervous systemDay 3Cognitive impairmentInterneuronsHousing miceRLN expressionCortical Gyrification Induced by Fibroblast Growth Factor 2 in the Mouse Brain
Rash BG, Tomasi S, Lim HD, Suh CY, Vaccarino FM. Cortical Gyrification Induced by Fibroblast Growth Factor 2 in the Mouse Brain. Journal Of Neuroscience 2013, 33: 10802-10814. PMID: 23804101, PMCID: PMC3693057, DOI: 10.1523/jneurosci.3621-12.2013.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsAntimetabolitesAxonsBrain ChemistryBromodeoxyuridineCell CountCerebral CortexCerebral VentriclesDensitometryDependovirusDNA, ComplementaryFemaleFibroblast Growth Factor 2Green Fluorescent ProteinsImmunohistochemistryIn Situ HybridizationLymphoid Enhancer-Binding Factor 1MiceNeocortexPregnancyReal-Time Polymerase Chain ReactionRNAWnt3A ProteinConceptsVentricular zoneIntermediate neuronal progenitorsSubventricular zoneCortical gyrificationCortical primordiumRegion-specific actionsFibroblast growth factor-2ER81 expressionGrowth factor 2Ventricular injectionCortical layer structureBasal radial gliaCortical gyriRadial gliaMouse brainCortical hemEmbryonic day 11.5Neuronal progenitorsGyrus formationLEF1 expressionGyrificationNeurogenesisLissencephalic speciesFactor 2Impaired growth
2012
Oligodendrocyte Regeneration after Neonatal Hypoxia Requires FoxO1-Mediated p27Kip1 Expression
Jablonska B, Scafidi J, Aguirre A, Vaccarino F, Nguyen V, Borok E, Horvath TL, Rowitch DH, Gallo V. Oligodendrocyte Regeneration after Neonatal Hypoxia Requires FoxO1-Mediated p27Kip1 Expression. Journal Of Neuroscience 2012, 32: 14775-14793. PMID: 23077062, PMCID: PMC3517297, DOI: 10.1523/jneurosci.2060-12.2012.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsAnimals, NewbornCell DifferentiationCells, CulturedCyclin-Dependent Kinase Inhibitor p27Forkhead Box Protein O1Forkhead Transcription FactorsGene Expression Regulation, DevelopmentalHumansHypoxia, BrainInfantInfant, NewbornMiceMice, 129 StrainMice, Inbred C57BLMice, KnockoutMice, TransgenicNerve RegenerationOligodendrogliaConceptsDiffuse white matter injuryNeonatal hypoxiaOligodendrocyte regenerationOligodendrocyte progenitor cell proliferationWhite matter injuryWhite matter lesionsPermanent neurodevelopmental disabilityCritical developmental time windowWhite matter developmentOverexpression of FoxO1Preterm infantsProgenitor cell proliferationDevelopmental time windowMatter lesionsOligodendrocyte deathAbnormal myelinationNeurodevelopmental disabilitiesMouse modelBiphasic effectP27Kip1 expressionNull miceOligodendrogenesisHypoxiaOligodendrocyte differentiationOligodendrocyte developmentPrenatal stress delays inhibitory neuron progenitor migration in the developing neocortex
Stevens HE, Su T, Yanagawa Y, Vaccarino FM. Prenatal stress delays inhibitory neuron progenitor migration in the developing neocortex. Psychoneuroendocrinology 2012, 38: 509-521. PMID: 22910687, PMCID: PMC3532962, DOI: 10.1016/j.psyneuen.2012.07.011.Peer-Reviewed Original ResearchEnvironmental Enrichment Increases the GFAP+ Stem Cell Pool and Reverses Hypoxia-Induced Cognitive Deficits in Juvenile Mice
Salmaso N, Silbereis J, Komitova M, Mitchell P, Chapman K, Ment LR, Schwartz ML, Vaccarino FM. Environmental Enrichment Increases the GFAP+ Stem Cell Pool and Reverses Hypoxia-Induced Cognitive Deficits in Juvenile Mice. Journal Of Neuroscience 2012, 32: 8930-8939. PMID: 22745493, PMCID: PMC3399175, DOI: 10.1523/jneurosci.1398-12.2012.Peer-Reviewed Original ResearchMeSH KeywordsAnalysis of VarianceAnimalsAnimals, NewbornBromodeoxyuridineCell CountCell DifferentiationCognition DisordersDeoxyuridineDisease Models, AnimalEnvironmentEstrogen AntagonistsFemaleGene Expression Regulation, DevelopmentalGlial Fibrillary Acidic ProteinGreen Fluorescent ProteinsHumansHypoxiaIdoxuridineKi-67 AntigenMaleMaze LearningMiceMice, Inbred C57BLMice, TransgenicNerve Tissue ProteinsNeurogenesisNeurogliaReceptors, EstrogenStem CellsTamoxifenConceptsHypoxic injuryBrain injuryAstroglial cellsChronic hypoxic injuryDevelopmental brain injuryLow birth weightCell poolEnvironmental enrichmentAdult brain injuryAbnormal lung developmentStem cell poolPerinatal hypoxic injuryFate-mapping modelsSocio-demographic factorsNeurobiological recoveryHippocampal neurogenesisVLBW cohortPremature childrenBirth weightCardiovascular abnormalitiesJuvenile miceAnimal modelsLung developmentInjuryCognitive deficitsLearning and Memory Depend on Fibroblast Growth Factor Receptor 2 Functioning in Hippocampus
Stevens HE, Jiang GY, Schwartz ML, Vaccarino FM. Learning and Memory Depend on Fibroblast Growth Factor Receptor 2 Functioning in Hippocampus. Biological Psychiatry 2012, 71: 1090-1098. PMID: 22541947, PMCID: PMC3371339, DOI: 10.1016/j.biopsych.2012.03.013.Peer-Reviewed Original ResearchConceptsFGF receptor 2Fibroblast growth factorDentate gyrusReceptor 2Embryonic knockoutWater maze probe trialGrowth factor receptor 2Reference memoryFactor receptor 2Spatial reference memoryNeural stem cellsFibroblast growth factor receptor 2Immature neuronsCortical neuronsHippocampal volumeInducible knockout miceParvalbumin interneuronsShort-term learningGranule cellsKnockout miceSeparate cellular componentsHippocampusLong-term reference memoryAdult spatial memoryGrowth factorImpaired motor coordination and disrupted cerebellar architecture in Fgfr1 and Fgfr2 double knockout mice
Smith K, Williamson TL, Schwartz ML, Vaccarino FM. Impaired motor coordination and disrupted cerebellar architecture in Fgfr1 and Fgfr2 double knockout mice. Brain Research 2012, 1460: 12-24. PMID: 22578469, PMCID: PMC3361544, DOI: 10.1016/j.brainres.2012.04.002.Peer-Reviewed Original ResearchConceptsFibroblast growth factor receptorHuman GFAP promoterInner granule cell layerDKO miceGranule cell numberGranule cell progenitorsRadial glial stem cellsMidline glial structuresImpaired motor coordinationCerebellar sizeGranule cell layerDouble knockout miceGlial precursor cellsGlial stem cellsCell numberGranule neuron precursorsGrowth factor receptorGABA interneuronsGranule cell migrationCerebral cortexExternal granular layerMolecular layerMotor coordinationGranule cellsKnockout mice
2011
FGF Signaling Expands Embryonic Cortical Surface Area by Regulating Notch-Dependent Neurogenesis
Rash BG, Lim HD, Breunig JJ, Vaccarino FM. FGF Signaling Expands Embryonic Cortical Surface Area by Regulating Notch-Dependent Neurogenesis. Journal Of Neuroscience 2011, 31: 15604-15617. PMID: 22031906, PMCID: PMC3235689, DOI: 10.1523/jneurosci.4439-11.2011.Peer-Reviewed Original ResearchMeSH KeywordsAge FactorsAnalysis of VarianceAnimalsBrainBromodeoxyuridineCaspase 3Cell CountCell DifferentiationCells, CulturedCerebral CortexDNA-Binding ProteinsElectroporationEmbryo, MammalianEye ProteinsFatty Acid-Binding Protein 7Fatty Acid-Binding ProteinsFibroblast Growth FactorsGene Expression Regulation, DevelopmentalGreen Fluorescent ProteinsHomeodomain ProteinsKi-67 AntigenMiceMice, TransgenicMutationNerve Tissue ProteinsNeurogenesisNeuronsPaired Box Transcription FactorsPAX6 Transcription FactorReceptors, Fibroblast Growth FactorReceptors, NotchRepressor ProteinsSignal TransductionStem CellsT-Box Domain ProteinsTranscription FactorsConceptsCortical neurogenesisCortical surface area expansionCortical surface expansionCortical surface areaGrowth factor receptorEmbryonic day 12.5Fibroblast growth factor receptorFGFR mutantsNormal miceCortical layer structureCortical developmentNeurogenic stagesDominant negative FGFRLoss of functionRadial progenitorsNeurogenesisNotch pathway genesSevere deficitsFactor receptorDay 12.5Notch pathwayMiceSimultaneous activationGreater proportionFGFR activityCortical Glial Fibrillary Acidic Protein-Positive Cells Generate Neurons after Perinatal Hypoxic Injury
Bi B, Salmaso N, Komitova M, Simonini MV, Silbereis J, Cheng E, Kim J, Luft S, Ment LR, Horvath TL, Schwartz ML, Vaccarino FM. Cortical Glial Fibrillary Acidic Protein-Positive Cells Generate Neurons after Perinatal Hypoxic Injury. Journal Of Neuroscience 2011, 31: 9205-9221. PMID: 21697371, PMCID: PMC3142780, DOI: 10.1523/jneurosci.0518-11.2011.Peer-Reviewed Original ResearchConceptsGlial fibrillary acidic protein-positive cellsCortical excitatory neuronsProtein-positive cellsPerinatal hypoxic injuryPostnatal hypoxiaGenetic fate mappingCortical astrogliaPremature childrenHypoxic injuryBrain injuryNew neuronsPreterm childrenNeurogenic nicheCognitive recoveryExcitatory neuronsGenerate neuronsNeuronal fateNeuronsHypoxiaCortical parenchymaInjuryParenchymaFate mappingCellsChildren
2010
Pyramidal Neurons Are Generated from Oligodendroglial Progenitor Cells in Adult Piriform Cortex
Guo F, Maeda Y, Ma J, Xu J, Horiuchi M, Miers L, Vaccarino F, Pleasure D. Pyramidal Neurons Are Generated from Oligodendroglial Progenitor Cells in Adult Piriform Cortex. Journal Of Neuroscience 2010, 30: 12036-12049. PMID: 20826667, PMCID: PMC2940828, DOI: 10.1523/jneurosci.1360-10.2010.Peer-Reviewed Original ResearchMeSH KeywordsAdult Stem CellsAnimalsAntigensAntineoplastic Agents, HormonalBromodeoxyuridineCell CountCell DifferentiationCerebral CortexDoublecortin Domain ProteinsDrug Administration ScheduleEye ProteinsGene Expression RegulationGreen Fluorescent ProteinsHomeodomain ProteinsMiceMice, Inbred C57BLMice, TransgenicMicrotubule-Associated ProteinsMyelin Proteolipid ProteinNerve Tissue ProteinsNeuronsNeuropeptidesOligodendrogliaPaired Box Transcription FactorsPAX6 Transcription FactorProteoglycansPyramidal CellsReceptor, Platelet-Derived Growth Factor alphaReceptors, N-Methyl-D-AspartateRepressor ProteinsSOXB1 Transcription FactorsTamoxifenTime FactorsConceptsOligodendroglial progenitor cellsPyramidal glutamatergic neuronsPiriform cortexAdult piriform cortexGlutamatergic neuronsCortical glutamatergic neuronsProgenitor cellsNeural stem cell markersCortical neuronal networksStem cell markersTranscription factor characteristicImmature neuronsCerebral cortexPyramidal neuronsCell markersCortexNeuronsCre-loxP recombination systemNeuronal networksLines of evidenceMarkersLow levelsCellsPrevious studiesDoublecortinAstroglial cells in the external granular layer are precursors of cerebellar granule neurons in neonates
Silbereis J, Heintz T, Taylor MM, Ganat Y, Ment LR, Bordey A, Vaccarino F. Astroglial cells in the external granular layer are precursors of cerebellar granule neurons in neonates. Molecular And Cellular Neuroscience 2010, 44: 362-373. PMID: 20470892, PMCID: PMC2900521, DOI: 10.1016/j.mcn.2010.05.001.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsAnimals, NewbornAstrocytesBasic Helix-Loop-Helix Transcription FactorsBeta-GalactosidaseCell LineageCerebellumGenes, ReporterGlial Fibrillary Acidic ProteinGreen Fluorescent ProteinsIntegrasesMiceMice, Inbred C57BLMice, TransgenicNeurogenesisNeuronsPromoter Regions, GeneticStem CellsTime FactorsConceptsExternal granule cell layerGranule cell precursorsInternal granule cell layerGranule cell layerGranule cellsRhombic lipAstroglial cellsProtein expression profilesGlial fibrillary acidic protein promoterCerebellar granule cell precursorsHuman glial fibrillary acidic protein promoterEmbryonic rhombic lipInducible Cre recombinaseNeuronal progenitor cellsReporter proteinFirst postnatal weekNeural stem cell markersLate embryogenesisCellular plasticityImmature granule cellsEarly postnatal developmentCell layerReporter geneCerebellar granule neuronsStem cell markers