The Adult Ventricular-Subventricular Zone (V-SVZ) and Olfactory Bulb (OB) Neurogenesis.

A large population of neural stem/precursor cells (NSCs) persists in the ventricular-subventricular zone (V-SVZ) located in the walls of the lateral brain ventricles. V-SVZ NSCs produce large numbers of neuroblasts that migrate a long distance into the olfactory bulb (OB) where they differentiate into local circuit interneurons. Here, we review a broad range of discoveries that have emerged from studies of postnatal V-SVZ neurogenesis: the identification of NSCs as a subpopulation of astroglial cells, the neurogenic lineage, new mechanisms of neuronal migration, and molecular regulators of precursor cell proliferation and migration. It has also become evident that V-SVZ NSCs are regionally heterogeneous, with NSCs located in different regions of the ventricle wall generating distinct OB interneuron subtypes. Insights into the developmental origins and molecular mechanisms that underlie the regional specification of V-SVZ NSCs have also begun to emerge. Other recent studies have revealed new cell-intrinsic molecular mechanisms that enable lifelong neurogenesis in the V-SVZ. Finally, we discuss intriguing differences between the rodent V-SVZ and the corresponding human brain region. The rapidly expanding cellular and molecular knowledge of V-SVZ NSC biology provides key insights into postnatal neural development, the origin of brain tumors, and may inform the development regenerative therapies from cultured and endogenous human neural precursors.

[1]  A. Álvarez-Buylla,et al.  Embryonic Origin of Postnatal Neural Stem Cells , 2015, Cell.

[2]  A. Kriegstein,et al.  The long noncoding RNA Pnky regulates neuronal differentiation of embryonic and postnatal neural stem cells. , 2015, Cell stem cell.

[3]  K. Nakayama,et al.  Slowly dividing neural progenitors are an embryonic origin of adult neural stem cells , 2015, Nature Neuroscience.

[4]  Giorgia Quadrato,et al.  Direct cell-cell contact with the vascular niche maintains quiescent neural stem cells , 2014, Nature Cell Biology.

[5]  D. Lim,et al.  Activation of neuronal gene expression by the JMJD3 demethylase is required for postnatal and adult brain neurogenesis. , 2014, Cell reports.

[6]  Dashi Qi,et al.  Human and Monkey Striatal Interneurons Are Derived from the Medial Ganglionic Eminence But Not from the Adult Subventricular Zone , 2014, The Journal of Neuroscience.

[7]  A. Álvarez-Buylla,et al.  Primary cilia are required in a unique subpopulation of neural progenitors , 2014, Proceedings of the National Academy of Sciences.

[8]  A. Pérez-Villalba,et al.  Endothelial NT-3 Delivered by Vasculature and CSF Promotes Quiescence of Subependymal Neural Stem Cells through Nitric Oxide Induction , 2014, Neuron.

[9]  Patricia Paez-Gonzalez,et al.  Identification of distinct ChAT+ neurons and activity-dependent control of postnatal SVZ neurogenesis , 2014, Nature Neuroscience.

[10]  Mercedes F. Paredes,et al.  Distinct and separable roles for EZH2 in neurogenic astroglia , 2014, eLife.

[11]  S. Morrison,et al.  Prospective identification of functionally distinct stem cells and neurosphere-initiating cells in adult mouse forebrain , 2014, eLife.

[12]  Erika Pastrana,et al.  Prospective Identification and Purification of Quiescent Adult Neural Stem Cells from Their In Vivo Niche , 2014, Neuron.

[13]  Arnold Kriegstein,et al.  Axonal control of the adult neural stem cell niche. , 2014, Cell stem cell.

[14]  Samuel Bernard,et al.  Neurogenesis in the Striatum of the Adult Human Brain , 2014, Cell.

[15]  A. Álvarez-Buylla,et al.  Adult neural stem cells in distinct microdomains generate previously unknown interneuron types , 2013, Nature Neuroscience.

[16]  David E. Leib,et al.  Evf2 (Dlx6as) lncRNA regulates ultraconserved enhancer methylation and the differential transcriptional control of adjacent genes , 2013, Development.

[17]  P. Ingham,et al.  Structure and function of the Smoothened extracellular domain in vertebrate Hedgehog signaling , 2013, eLife.

[18]  G. Crabtree,et al.  The BAF complex interacts with Pax6 in adult neural progenitors to establish a neurogenic cross-regulatory transcriptional network. , 2013, Cell stem cell.

[19]  S. Foti,et al.  HDAC inhibitors dysregulate neural stem cell activity in the postnatal mouse brain , 2013, International Journal of Developmental Neuroscience.

[20]  A. Álvarez-Buylla,et al.  Lineage progression from stem cells to new neurons in the adult brain ventricular-subventricular zone , 2013, Cell cycle.

[21]  Felipe Ortega,et al.  Oligodendrogliogenic and neurogenic adult subependymal zone neural stem cells constitute distinct lineages and exhibit differential responsiveness to Wnt signalling , 2013, Nature Cell Biology.

[22]  Jun S. Song,et al.  Integration of genome-wide approaches identifies lncRNAs of adult neural stem cells and their progeny in vivo. , 2013, Cell stem cell.

[23]  Khadar Abdi,et al.  Protective astrogenesis from the SVZ niche after injury is controlled by Notch modulator Thbs4 , 2013, Nature.

[24]  F. Gage,et al.  Paired Related Homeobox Protein 1 is a Regulator of Stemness in Adult Neural Stem/Progenitor Cells , 2013, The Journal of Neuroscience.

[25]  K. Hochedlinger,et al.  The sox family of transcription factors: versatile regulators of stem and progenitor cell fate. , 2013, Cell stem cell.

[26]  M. R. Costa,et al.  Primary culture and live imaging of adult neural stem cells and their progeny. , 2013, Methods in molecular biology.

[27]  G. Kusek,et al.  VCAM1 is essential to maintain the structure of the SVZ niche and acts as an environmental sensor to regulate SVZ lineage progression. , 2012, Cell stem cell.

[28]  A. Álvarez-Buylla,et al.  Adult neural stem cells bridge their niche. , 2012, Cell stem cell.

[29]  Howard Y. Chang,et al.  Genome regulation by long noncoding RNAs. , 2012, Annual review of biochemistry.

[30]  D. Bernardo,et al.  Id proteins synchronize stemness and anchorage to the niche of neural stem cells , 2012, Nature Cell Biology.

[31]  R. Lovell-Badge,et al.  Betacellulin promotes cell proliferation in the neural stem cell niche and stimulates neurogenesis , 2012, Proceedings of the National Academy of Sciences.

[32]  H. Monyer,et al.  Diazepam binding inhibitor promotes progenitor proliferation in the postnatal SVZ by reducing GABA signaling. , 2012, Cell stem cell.

[33]  E. Lai,et al.  Ars2 maintains neural stem cell identity via direct transcriptional activation of Sox2 , 2011, Nature.

[34]  F. Gage,et al.  SRY-box-containing Gene 2 Regulation of Nuclear Receptor Tailless (Tlx) Transcription in Adult Neural Stem Cells* , 2011, The Journal of Biological Chemistry.

[35]  Maria K. Lehtinen,et al.  Neurogenesis at the brain-cerebrospinal fluid interface. , 2011, Annual review of cell and developmental biology.

[36]  Eugene Bolotin,et al.  The noncoding RNA Mistral activates Hoxa6 and Hoxa7 expression and stem cell differentiation by recruiting MLL1 to chromatin. , 2011, Molecular cell.

[37]  Cole Trapnell,et al.  Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. , 2011, Genes & development.

[38]  Mitchel S. Berger,et al.  Corridors of Migrating Neurons in Human Brain and Their Decline during Infancy , 2011, Nature.

[39]  Rebecca A. Ihrie,et al.  Persistent Sonic Hedgehog Signaling in Adult Brain Determines Neural Stem Cell Positional Identity , 2011, Neuron.

[40]  J. García-Verdugo,et al.  Ank3-Dependent SVZ Niche Assembly Is Required for the Continued Production of New Neurons , 2011, Neuron.

[41]  S. Weiss,et al.  PDGFRα Expression Distinguishes GFAP-Expressing Neural Stem Cells from PDGF-Responsive Neural Precursors in the Adult Periventricular Area , 2011, The Journal of Neuroscience.

[42]  Rebecca A. Ihrie,et al.  Lake-Front Property: A Unique Germinal Niche by the Lateral Ventricles of the Adult Brain , 2011, Neuron.

[43]  Pasko Rakic,et al.  Not(ch) just development: Notch signalling in the adult brain , 2011, Nature Reviews Neuroscience.

[44]  Howard Y. Chang,et al.  A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression , 2011, Nature.

[45]  P. Ernfors,et al.  Cell cycle restriction by histone H2AX limits proliferation of adult neural stem cells , 2011, Proceedings of the National Academy of Sciences.

[46]  Maria K. Lehtinen,et al.  The Cerebrospinal Fluid Provides a Proliferative Niche for Neural Progenitor Cells , 2011, Neuron.

[47]  Ryan A. Flynn,et al.  A unique chromatin signature uncovers early developmental enhancers in humans , 2011, Nature.

[48]  M. Doughty,et al.  Histone deacetylase inhibitors SAHA and sodium butyrate block G1-to-S cell cycle progression in neurosphere formation by adult subventricular cells , 2011, BMC Neuroscience.

[49]  J. Frisén,et al.  EphB signaling controls lineage plasticity of adult neural stem cell niche cells. , 2010, Cell stem cell.

[50]  Magdalena Götz,et al.  In vivo fate mapping and expression analysis reveals molecular hallmarks of prospectively isolated adult neural stem cells. , 2010, Cell stem cell.

[51]  B. Roysam,et al.  Adult SVZ lineage cells home to and leave the vascular niche via differential responses to SDF1/CXCR4 signaling. , 2010, Cell stem cell.

[52]  Yongsoo Kim,et al.  Dopamine stimulation of postnatal murine subventricular zone neurogenesis via the D3 receptor , 2010, Journal of neurochemistry.

[53]  Hideyuki Okano,et al.  New Neurons Clear the Path of Astrocytic Processes for Their Rapid Migration in the Adult Brain , 2010, Neuron.

[54]  Yi Zhang,et al.  Dnmt3a-Dependent Nonpromoter DNA Methylation Facilitates Transcription of Neurogenic Genes , 2010, Science.

[55]  V. Gallo,et al.  Notch and EGFR pathway interaction regulates neural stem cell number and self-renewal , 2010, Nature.

[56]  M. Götz,et al.  LRP2 in ependymal cells regulates BMP signaling in the adult neurogenic niche , 2010, Journal of Cell Science.

[57]  A. Álvarez-Buylla,et al.  The Subventricular Zone En-face: Wholemount Staining and Ependymal Flow , 2010, Journal of visualized experiments : JoVE.

[58]  W. Wurst,et al.  The specific role of histone deacetylase 2 in adult neurogenesis. , 2010, Neuron glia biology.

[59]  M. K. Cooper,et al.  Transventricular delivery of Sonic hedgehog is essential to cerebellar ventricular zone development , 2010, Proceedings of the National Academy of Sciences.

[60]  P. Jin,et al.  Cross talk between microRNA and epigenetic regulation in adult neurogenesis , 2010, The Journal of cell biology.

[61]  K. Mori,et al.  Essential Roles of Notch Signaling in Maintenance of Neural Stem Cells in Developing and Adult Brains , 2010, The Journal of Neuroscience.

[62]  Julie A. Law,et al.  Establishing, maintaining and modifying DNA methylation patterns in plants and animals , 2010, Nature Reviews Genetics.

[63]  Guoqiang Sun,et al.  MicroRNA let-7b regulates neural stem cell proliferation and differentiation by targeting nuclear receptor TLX signaling , 2010, Proceedings of the National Academy of Sciences.

[64]  G. Crabtree,et al.  Chromatin remodelling during development , 2010, Nature.

[65]  池田 麻記子 Expression and proliferation-promoting role of diversin in the neuronally committed precursor cells migrating in the adult mouse brain , 2010 .

[66]  A. Bosio,et al.  NeuroD1 induces terminal neuronal differentiation in olfactory neurogenesis , 2009, Proceedings of the National Academy of Sciences.

[67]  I. Fariñas,et al.  Vascular niche factor PEDF modulates Notch-dependent stemness in the adult subependymal zone , 2009, Nature Neuroscience.

[68]  R. Benezra,et al.  High levels of Id1 expression define B1 type adult neural stem cells. , 2009, Cell Stem Cell.

[69]  M. Frotscher,et al.  Adult generation of glutamatergic olfactory bulb interneurons , 2009, Nature Neuroscience.

[70]  K. Nave,et al.  Neurod1 is essential for the survival and maturation of adult-born neurons , 2009, Nature Neuroscience.

[71]  J. Disterhoft,et al.  Balanced gene regulation by an embryonic brain ncRNA is critical for adult hippocampal GABA circuitry. , 2009, Nature neuroscience.

[72]  G. Crabtree,et al.  MicroRNA-mediated switching of chromatin-remodelling complexes in neural development , 2009, Nature.

[73]  J. Rinn,et al.  Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression , 2009, Proceedings of the National Academy of Sciences.

[74]  Arnold Kriegstein,et al.  The glial nature of embryonic and adult neural stem cells. , 2009, Annual review of neuroscience.

[75]  J. Dalley,et al.  Dopamine-induced proliferation of adult neural precursor cells in the mammalian subventricular zone is mediated through EGF , 2009, Proceedings of the National Academy of Sciences.

[76]  E. Olson,et al.  Histone deacetylases 1 and 2 control the progression of neural precursors to neurons during brain development , 2009, Proceedings of the National Academy of Sciences.

[77]  Raphael Kopan,et al.  The Canonical Notch Signaling Pathway: Unfolding the Activation Mechanism , 2009, Cell.

[78]  Dafydd G. Thomas,et al.  Bmi-1 over-expression in neural stem/progenitor cells increases proliferation and neurogenesis in culture but has little effect on these functions in vivo. , 2009, Developmental biology.

[79]  Erika Pastrana,et al.  Simultaneous prospective purification of adult subventricular zone neural stem cells and their progeny , 2009, Proceedings of the National Academy of Sciences.

[80]  J. García-Verdugo,et al.  Chromatin remodelling factor Mll1 is essential for neurogenesis from postnatal neural stem cells , 2009, Nature.

[81]  Erika Pastrana,et al.  miR-124 regulates adult neurogenesis in the SVZ stem cell niche , 2009, Nature Neuroscience.

[82]  Guoqiang Sun,et al.  A feedback regulatory loop involving microRNA-9 and nuclear receptor TLX in neural stem cell fate determination , 2009, Nature Structural &Molecular Biology.

[83]  John T. Dimos,et al.  Bmi-1 cooperates with Foxg1 to maintain neural stem cell self-renewal in the forebrain. , 2009, Genes & development.

[84]  P. Mehlen,et al.  EphrinB3 is an anti-apoptotic ligand that inhibits the dependence receptor functions of EphA4 receptors during adult neurogenesis. , 2009, Biochimica et biophysica acta.

[85]  P. Brundin,et al.  Involvement of Ngn2, Tbr and NeuroD proteins during postnatal olfactory bulb neurogenesis , 2009, The European journal of neuroscience.

[86]  J. García-Verdugo,et al.  Brain-Derived Neurotrophic Factor Signaling Does Not Stimulate Subventricular Zone Neurogenesis in Adult Mice and Rats , 2008, The Journal of Neuroscience.

[87]  M. Grubb,et al.  Turning Astrocytes from the Rostral Migratory Stream into Neurons: A Role for the Olfactory Sensory Organ , 2008, The Journal of Neuroscience.

[88]  Sean J. Morrison,et al.  Hmga2 Promotes Neural Stem Cell Self-Renewal in Young but Not Old Mice by Reducing p16Ink4a and p19Arf Expression , 2008, Cell.

[89]  J. García-Verdugo,et al.  A specialized vascular niche for adult neural stem cells. , 2008, Cell stem cell.

[90]  J. García-Verdugo,et al.  Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. , 2008, Cell stem cell.

[91]  B. Roysam,et al.  Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions. , 2008, Cell stem cell.

[92]  J. MacDonald,et al.  Histone deacetylases 1 and 2 are expressed at distinct stages of neuro‐glial development , 2008, Developmental dynamics : an official publication of the American Association of Anatomists.

[93]  Claudia Petritsch,et al.  miR-124 and miR-137 inhibit proliferation of glioblastoma multiforme cells and induce differentiation of brain tumor stem cells , 2008 .

[94]  G. Fishell,et al.  The Distinct Temporal Origins of Olfactory Bulb Interneuron Subtypes , 2008, The Journal of Neuroscience.

[95]  G. Fan,et al.  CD133+ neural stem cells in the ependyma of mammalian postnatal forebrain , 2008, Proceedings of the National Academy of Sciences.

[96]  C. Mummery,et al.  Adult Neurogenesis Requires Smad4-Mediated Bone Morphogenic Protein Signaling in Stem Cells , 2008, The Journal of Neuroscience.

[97]  安達 一英 {beta}-catenin signaling promotes proliferation of progenitor cells in the adult mouse subventricular zone , 2008 .

[98]  J. Reiter,et al.  The primary cilium at the crossroads of mammalian hedgehog signaling. , 2008, Current topics in developmental biology.

[99]  A. Álvarez-Buylla,et al.  The heterogeneity of adult neural stem cells and the emerging complexity of their niche. , 2008, Cold Spring Harbor symposia on quantitative biology.

[100]  H. Okano,et al.  β‐Catenin Signaling Promotes Proliferation of Progenitor Cells in the Adult Mouse Subventricular Zone , 2007, Stem cells.

[101]  T. Swigut,et al.  H3K27 Demethylases, at Long Last , 2007, Cell.

[102]  Guoqiang Sun,et al.  Orphan nuclear receptor TLX recruits histone deacetylases to repress transcription and regulate neural stem cell proliferation , 2007, Proceedings of the National Academy of Sciences.

[103]  G. Natoli,et al.  The Histone H3 Lysine-27 Demethylase Jmjd3 Links Inflammation to Inhibition of Polycomb-Mediated Gene Silencing , 2007, Cell.

[104]  Arturo Alvarez-Buylla,et al.  Mosaic Organization of Neural Stem Cells in the Adult Brain , 2007, Science.

[105]  K. Campbell,et al.  Molecular identity of olfactory bulb interneurons: transcriptional codes of periglomerular neuron subtypes , 2007, Journal of Molecular Histology.

[106]  Y. Jan,et al.  Numb and Numbl are required for maintenance of cadherin-based adhesion and polarity of neural progenitors , 2007, Nature Neuroscience.

[107]  M. Ekker,et al.  A Subpopulation of Olfactory Bulb GABAergic Interneurons Is Derived from Emx1- and Dlx5/6-Expressing Progenitors , 2007, The Journal of Neuroscience.

[108]  M. T. Shipley,et al.  Quantitative analysis of neuronal diversity in the mouse olfactory bulb , 2007, The Journal of comparative neurology.

[109]  R. Ventura,et al.  Dorsal Radial Glia Generate Olfactory Bulb Interneurons in the Postnatal Murine Brain , 2007, The Journal of Neuroscience.

[110]  T. Kouzarides Chromatin Modifications and Their Function , 2007, Cell.

[111]  I. Blumcke,et al.  Histone deacetylase inhibitors increase neuronal differentiation in adult forebrain precursor cells , 2007, Experimental Brain Research.

[112]  Y. Jan,et al.  Postnatal Deletion of Numb/Numblike Reveals Repair and Remodeling Capacity in the Subventricular Neurogenic Niche , 2006, Cell.

[113]  D. Steindler,et al.  Microglia instruct subventricular zone neurogenesis , 2006, Glia.

[114]  S. Bauer,et al.  Leukemia Inhibitory Factor Promotes Neural Stem Cell Self-Renewal in the Adult Brain , 2006, The Journal of Neuroscience.

[115]  A. Bernad,et al.  Generation of GABAergic and dopaminergic interneurons from endogenous embryonic olfactory bulb precursor cells , 2006, Development.

[116]  S. Morrison,et al.  Increasing p16INK4a expression decreases forebrain progenitors and neurogenesis during ageing , 2006, Nature.

[117]  Oscar Gonzalez-Perez,et al.  Origin of Oligodendrocytes in the Subventricular Zone of the Adult Brain , 2006, The Journal of Neuroscience.

[118]  S. Vandenberg,et al.  PDGFRα-Positive B Cells Are Neural Stem Cells in the Adult SVZ that Form Glioma-like Growths in Response to Increased PDGF Signaling , 2006, Neuron.

[119]  A. Bosio,et al.  Glial conversion of SVZ-derived committed neuronal precursors after ectopic grafting into the adult brain , 2006, Molecular and Cellular Neuroscience.

[120]  D. Liebl,et al.  EphrinB3 regulates cell proliferation and survival in adult neurogenesis , 2006, Molecular and Cellular Neuroscience.

[121]  M. Katoh,et al.  Notch ligand, JAG1, is evolutionarily conserved target of canonical WNT signaling pathway in progenitor cells. , 2006, International journal of molecular medicine.

[122]  I. Fariñas,et al.  Pigment epithelium–derived factor is a niche signal for neural stem cell renewal , 2006, Nature Neuroscience.

[123]  Matthew S. Grubb,et al.  Adult neurogenesis and functional plasticity in neuronal circuits , 2006, Nature Reviews Neuroscience.

[124]  S. Potter,et al.  The Zinc Finger Transcription Factor Sp8 Regulates the Generation and Diversity of Olfactory Bulb Interneurons , 2006, Neuron.

[125]  Hideyuki Okano,et al.  New Neurons Follow the Flow of Cerebrospinal Fluid in the Adult Brain , 2006, Science.

[126]  E. Bongarzone,et al.  Notch Signaling in Astrocytes and Neuroblasts of the Adult Subventricular Zone in Health and after Cortical Injury , 2006, Developmental Neuroscience.

[127]  M. Sofroniew,et al.  Phenotypic and functional heterogeneity of GFAP‐expressing cells in vitro: Differential expression of LeX/CD15 by GFAP‐expressing multipotent neural stem cells and non‐neurogenic astrocytes , 2006, Glia.

[128]  Felix Naef,et al.  In vivo transcriptional profile analysis reveals RNA splicing and chromatin remodeling as prominent processes for adult neurogenesis , 2006, Molecular and Cellular Neuroscience.

[129]  Nader Sanai,et al.  Cellular composition and cytoarchitecture of the adult human subventricular zone: A niche of neural stem cells , 2006, The Journal of comparative neurology.

[130]  J. H. Kim,et al.  Increase in Proliferation and Differentiation of Neural Progenitor Cells Isolated from Postnatal and Adult Mice Brain by Wnt-3a and Wnt-5a , 2006, Molecular and Cellular Biochemistry.

[131]  M. Bonaguidi,et al.  LIF and BMP signaling generate separate and discrete types of GFAP-expressing cells , 2005, Development.

[132]  K. Jin,et al.  From angiogenesis to neuropathology , 2005, Nature.

[133]  M. Yukawa,et al.  Autocrine activation of EGF receptor promotes oscillation of glutamate‐induced calcium increase in astrocytes cultured in rat cerebral cortex , 2005, Journal of neurochemistry.

[134]  A. Joyner,et al.  In vivo analysis of quiescent adult neural stem cells responding to Sonic hedgehog , 2005, Nature.

[135]  Robert D. Kirch,et al.  Jagged1 signals in the postnatal subventricular zone are required for neural stem cell self‐renewal , 2005, The EMBO journal.

[136]  S. Mcconnell,et al.  Cytoskeletal coordination during neuronal migration. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[137]  A. Bordey,et al.  Nonsynaptic GABA signaling in postnatal subventricular zone controls proliferation of GFAP-expressing progenitors , 2005, Nature Neuroscience.

[138]  J. Goldman,et al.  Olig2 Directs Astrocyte and Oligodendrocyte Formation in Postnatal Subventricular Zone Cells , 2005, The Journal of Neuroscience.

[139]  J. Rubenstein,et al.  Pax6 Is Required for Making Specific Subpopulations of Granule and Periglomerular Neurons in the Olfactory Bulb , 2005, The Journal of Neuroscience.

[140]  M. Götz,et al.  Neuronal fate determinants of adult olfactory bulb neurogenesis , 2005, Nature Neuroscience.

[141]  Michelle Y. Cheng,et al.  Dependence of Olfactory Bulb Neurogenesis on Prokineticin 2 Signaling , 2005, Science.

[142]  S. Morrison,et al.  Bmi-1 promotes neural stem cell self-renewal and neural development but not mouse growth and survival by repressing the p16Ink4a and p19Arf senescence pathways. , 2005, Genes & development.

[143]  Ryoichiro Kageyama,et al.  Roles of bHLH genes in neural stem cell differentiation. , 2005, Experimental cell research.

[144]  L. Sommer,et al.  Wnt signaling: multiple functions in neural development , 2005, Cellular and Molecular Life Sciences CMLS.

[145]  K. Senti,et al.  Ephrin-A2 reverse signaling negatively regulates neural progenitor proliferation and neurogenesis. , 2005, Genes & development.

[146]  Alan Carleton,et al.  Sonic hedgehog controls stem cell behavior in the postnatal and adult brain , 2005, Development.

[147]  T. Kosaka,et al.  Structural organization of the glomerulus in the main olfactory bulb. , 2005, Chemical senses.

[148]  J. García-Verdugo,et al.  Radial glia give rise to adult neural stem cells in the subventricular zone. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[149]  R. Galli,et al.  Defective Postnatal Neurogenesis and Disorganization of the Rostral Migratory Stream in Absence of the Vax1 Homeobox Gene , 2004, The Journal of Neuroscience.

[150]  Ryoichiro Kageyama,et al.  Hes genes regulate size, shape and histogenesis of the nervous system by control of the timing of neural stem cell differentiation , 2004, Development.

[151]  François Guillemot,et al.  Mash1 specifies neurons and oligodendrocytes in the postnatal brain , 2004, The EMBO journal.

[152]  A. Bordey,et al.  GABA Release and Uptake Regulate Neuronal Precursor Migration in the Postnatal Subventricular Zone , 2004, The Journal of Neuroscience.

[153]  Pier Paolo Pandolfi,et al.  Sox2 deficiency causes neurodegeneration and impaired neurogenesis in the adult mouse brain , 2004, Development.

[154]  Charles Duyckaerts,et al.  Dopamine depletion impairs precursor cell proliferation in Parkinson disease , 2004, Nature Neuroscience.

[155]  T. Shimogori,et al.  Members of the Wnt, Fz, and Frp gene families expressed in postnatal mouse cerebral cortex , 2004, The Journal of comparative neurology.

[156]  Sally Temple,et al.  Endothelial Cells Stimulate Self-Renewal and Expand Neurogenesis of Neural Stem Cells , 2004, Science.

[157]  Armen Saghatelyan,et al.  Tenascin-R mediates activity-dependent recruitment of neuroblasts in the adult mouse forebrain , 2004, Nature Neuroscience.

[158]  G. Fishell,et al.  Radial Glia Serve as Neuronal Progenitors in All Regions of the Central Nervous System , 2004, Neuron.

[159]  E. Fuchs,et al.  Socializing with the Neighbors Stem Cells and Their Niche , 2004, Cell.

[160]  A. Álvarez-Buylla,et al.  For the Long Run Maintaining Germinal Niches in the Adult Brain , 2004, Neuron.

[161]  A. Benraiss,et al.  Adenovirally Expressed Noggin and Brain-Derived Neurotrophic Factor Cooperate to Induce New Medium Spiny Neurons from Resident Progenitor Cells in the Adult Striatal Ventricular Zone , 2004, The Journal of Neuroscience.

[162]  F. Vaccarino,et al.  Fibroblast Growth Factor 2 Is Required for Maintaining the Neural Stem Cell Pool in the Mouse Brain Subventricular Zone , 2004, Developmental Neuroscience.

[163]  Mahendra Rao,et al.  SOX2, a Persistent Marker for Multipotential Neural Stem Cells Derived from Embryonic Stem Cells, the Embryo or the Adult , 2004, Developmental Neuroscience.

[164]  M. Héry,et al.  Serotonin-Induced Increases in Adult Cell Proliferation and Neurogenesis are Mediated Through Different and Common 5-HT Receptor Subtypes in the Dentate Gyrus and the Subventricular Zone , 2004, Neuropsychopharmacology.

[165]  Mitchel S. Berger,et al.  Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration , 2004, Nature.

[166]  C. Estrada,et al.  Nitric Oxide Is a Physiological Inhibitor of Neurogenesis in the Adult Mouse Subventricular Zone and Olfactory Bulb , 2004, The Journal of Neuroscience.

[167]  L. Stensaas,et al.  Light microscopy of glial cells in turtles and birds , 2004, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

[168]  J. Sotelo,et al.  Electron microscope study on the development of ciliary components of the neural epithelium of the chick embryo , 2004, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

[169]  F. Gage,et al.  Expression and function of orphan nuclear receptor TLX in adult neural stem cells , 2004, Nature.

[170]  M. Raff Adult stem cell plasticity: fact or artifact? , 2003, Annual review of cell and developmental biology.

[171]  J. Loturco,et al.  Electrophysiological Differentiation of New Neurons in the Olfactory Bulb , 2003, The Journal of Neuroscience.

[172]  J. Nichols,et al.  BMP Induction of Id Proteins Suppresses Differentiation and Sustains Embryonic Stem Cell Self-Renewal in Collaboration with STAT3 , 2003, Cell.

[173]  S. Morrison,et al.  Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation , 2003, Nature.

[174]  J. Emsley,et al.  Endogenous and exogenous ciliary neurotrophic factor enhances forebrain neurogenesis in adult mice , 2003, Experimental Neurology.

[175]  J. Emsley,et al.  α6β1 integrin directs migration of neuronal precursors in adult mouse forebrain , 2003, Experimental Neurology.

[176]  V. Palma,et al.  The emergent design of the neural tube: prepattern, SHH morphogen and GLI code. , 2003, Current opinion in genetics & development.

[177]  G. Fishell,et al.  Sonic Hedgehog Is Required for Progenitor Cell Maintenance in Telencephalic Stem Cell Niches , 2003, Neuron.

[178]  Andrew P. McMahon,et al.  Sonic Hedgehog Is Required for Progenitor Cell Maintenance in Telencephalic Stem Cell Niches , 2003, Neuron.

[179]  Jane E. Johnson Numb and Numblike control cell number during vertebrate neurogenesis , 2003, Trends in Neurosciences.

[180]  A. Benraiss,et al.  Nitric oxide negatively regulates mammalian adult neurogenesis , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[181]  Y. Rao,et al.  Neuronal Migration from the Forebrain to the Olfactory Bulb Requires a New Attractant Persistent in the Olfactory Bulb , 2003, The Journal of Neuroscience.

[182]  Alan Carleton,et al.  Becoming a new neuron in the adult olfactory bulb , 2003, Nature Neuroscience.

[183]  K. Jin,et al.  Cerebral neurogenesis is induced by intranasal administration of growth factors , 2003, Annals of neurology.

[184]  S. Weiss,et al.  Glycoprotein 130 Signaling Regulates Notch1Expression and Activation in the Self-Renewal of Mammalian Forebrain Neural Stem Cells , 2003, The Journal of Neuroscience.

[185]  L. Parada,et al.  mRNA expression of ephrins and Eph receptor tyrosine kinases in the neonatal and adult mouse central nervous system , 2003, Journal of neuroscience research.

[186]  Arturo Alvarez-Buylla,et al.  EGF Converts Transit-Amplifying Neurogenic Precursors in the Adult Brain into Multipotent Stem Cells , 2002, Neuron.

[187]  A. Joyner,et al.  Gli2, but not Gli1, is required for initial Shh signaling and ectopic activation of the Shh pathway. , 2002, Development.

[188]  K. Loulier,et al.  Reelin is a detachment signal in tangential chain-migration during postnatal neurogenesis , 2002, Nature Neuroscience.

[189]  A. Fasolo,et al.  BMP mRNA and protein expression in the developing mouse olfactory system , 2002, The Journal of comparative neurology.

[190]  G. I. Hatton,et al.  Anatomy of the brain neurogenic zones revisited: Fractones and the fibroblast/macrophage network , 2002, The Journal of comparative neurology.

[191]  Anne Baron-Van Evercooren,et al.  Experimental autoimmune encephalomyelitis mobilizes neural progenitors from the subventricular zone to undergo oligodendrogenesis in adult mice , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[192]  M. Luskin,et al.  Intrinsic and extrinsic regulation of the proliferation and differentiation of cells in the rodent rostral migratory stream , 2002, Journal of neuroscience research.

[193]  S. Temple,et al.  LeX/ssea-1 Is Expressed by Adult Mouse CNS Stem Cells, Identifying Them as Nonependymal , 2002, Neuron.

[194]  K. Jin,et al.  Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[195]  Arturo Alvarez-Buylla,et al.  Maturation and Death of Adult-Born Olfactory Bulb Granule Neurons: Role of Olfaction , 2002, The Journal of Neuroscience.

[196]  M. Klagsbrun,et al.  Heparin-Binding Epidermal Growth Factor-Like Growth Factor: Hypoxia-Inducible Expression In Vitro and Stimulation of Neurogenesis In Vitro and In Vivo , 2002, The Journal of Neuroscience.

[197]  Steven A. Goldman,et al.  Coordinated Interaction of Neurogenesis and Angiogenesis in the Adult Songbird Brain , 2002, Neuron.

[198]  U. Suter,et al.  Notch1 and its ligands Delta-like and Jagged are expressed and active in distinct cell populations in the postnatal mouse brain , 2002, Mechanisms of Development.

[199]  Magdalena Götz,et al.  Radial glia: multi-purpose cells for vertebrate brain development , 2002, Trends in Neurosciences.

[200]  A. Horwitz,et al.  Deleted in Colorectal Carcinoma and Differentially Expressed Integrins Mediate the Directional Migration of Neural Precursors in the Rostral Migratory Stream , 2002, The Journal of Neuroscience.

[201]  R. Galli,et al.  Emx2 regulates the proliferation of stem cells of the adult mammalian central nervous system. , 2002, Development.

[202]  L. Astic,et al.  Expression of netrin-1 and netrin-1 receptor, DCC, in the rat olfactory nerve pathway during development and axonal regeneration , 2002, Neuroscience.

[203]  Gord Fishell,et al.  The role of notch in promoting glial and neural stem cell fates. , 2002, Annual review of neuroscience.

[204]  G. Corfas,et al.  Extracellular Signals That Regulate the Tangential Migration of Olfactory Bulb Neuronal Precursors: Inducers, Inhibitors, and Repellents , 2001, The Journal of Neuroscience.

[205]  M. Nakafuku,et al.  Combinatorial Roles of Olig2 and Neurogenin2 in the Coordinated Induction of Pan-Neuronal and Subtype-Specific Properties of Motoneurons , 2001, Neuron.

[206]  T. Jessell,et al.  Coordinate Regulation of Motor Neuron Subtype Identity and Pan-Neuronal Properties by the bHLH Repressor Olig2 , 2001, Neuron.

[207]  Stanley J. Wiegand,et al.  Infusion of Brain-Derived Neurotrophic Factor into the Lateral Ventricle of the Adult Rat Leads to New Neurons in the Parenchyma of the Striatum, Septum, Thalamus, and Hypothalamus , 2001, The Journal of Neuroscience.

[208]  R. McKay,et al.  Sequential actions of BMP receptors control neural precursor cell production and fate. , 2001, Genes & development.

[209]  C. Allis,et al.  Translating the Histone Code , 2001, Science.

[210]  T. Ohtsuka,et al.  Roles of the Basic Helix-Loop-Helix Genes Hes1 and Hes5 in Expansion of Neural Stem Cells of the Developing Brain* , 2001, The Journal of Biological Chemistry.

[211]  C. Hedin-Pereira,et al.  The 9-O-acetyl GD3 gangliosides are expressed by migrating chains of subventricular zone neurons in vitro. , 2001, Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas.

[212]  D. Anderson,et al.  Stem Cells and Pattern Formation in the Nervous System The Possible versus the Actual , 2001, Neuron.

[213]  G. Fishell,et al.  Spatiotemporal selectivity of response to Notch1 signals in mammalian forebrain precursors. , 2001, Development.

[214]  M. Greenberg,et al.  Neurogenin Promotes Neurogenesis and Inhibits Glial Differentiation by Independent Mechanisms , 2001, Cell.

[215]  T. Weissman,et al.  Neurons derived from radial glial cells establish radial units in neocortex , 2001, Nature.

[216]  J. García-Verdugo,et al.  Noggin Antagonizes BMP Signaling to Create a Niche for Adult Neurogenesis , 2000, Neuron.

[217]  J. García-Verdugo,et al.  Disruption of Eph/ephrin signaling affects migration and proliferation in the adult subventricular zone , 2000, Nature Neuroscience.

[218]  T. Palmer,et al.  Vascular niche for adult hippocampal neurogenesis , 2000, The Journal of comparative neurology.

[219]  B. McEwen,et al.  Widespread expression of rat collapsin response‐mediated protein 4 in the telencephalon and other areas of the adult rat central nervous system , 2000, The Journal of comparative neurology.

[220]  Gord Fishell,et al.  Radial Glial Identity Is Promoted by Notch1 Signaling in the Murine Forebrain , 2000, Neuron.

[221]  F M Watt,et al.  Out of Eden: stem cells and their niches. , 2000, Science.

[222]  G. Rougon,et al.  Consequences of Neural Cell Adhesion Molecule Deficiency on Cell Migration in the Rostral Migratory Stream of the Mouse , 2000, The Journal of Neuroscience.

[223]  J. García-Verdugo,et al.  Adult‐derived neural precursors transplanted into multiple regions in the adult brain , 1999, Annals of neurology.

[224]  L. Decker,et al.  Progenitor cells of the adult mouse subventricular zone proliferate, migrate and differentiate into oligodendrocytes after demyelination , 1999, The European journal of neuroscience.

[225]  A. Otte,et al.  Transcriptional repression mediated by the human polycomb-group protein EED involves histone deacetylation , 1999, Nature Genetics.

[226]  J. García-Verdugo,et al.  Regeneration of a germinal layer in the adult mammalian brain. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[227]  M. Mehler,et al.  Multiple Roles of Bone Morphogenetic Protein Signaling in the Regulation of Cortical Cell Number and Phenotype , 1999, The Journal of Neuroscience.

[228]  Huaiyu Hu,et al.  Chemorepulsion of Neuronal Migration by Slit2 in the Developing Mammalian Forebrain , 1999, Neuron.

[229]  Sophie Dupuis,et al.  Directional guidance of neuronal migration in the olfactory system by the protein Slit , 1999, Nature.

[230]  Daniel A. Lim,et al.  Subventricular Zone Astrocytes Are Neural Stem Cells in the Adult Mammalian Brain , 1999, Cell.

[231]  S. Rafii,et al.  Endothelial Trophic Support of Neuronal Production and Recruitment from the Adult Mammalian Subependyma , 1999, Molecular and Cellular Neuroscience.

[232]  S. Mcconnell,et al.  Doublecortin Is a Developmentally Regulated, Microtubule-Associated Protein Expressed in Migrating and Differentiating Neurons , 1999, Neuron.

[233]  T. Ohtsuka,et al.  Hes1 and Hes5 as Notch effectors in mammalian neuronal differentiation , 1999, The EMBO journal.

[234]  A. Daszuta,et al.  Depletion in serotonin decreases neurogenesis in the dentate gyrus and the subventricular zone of adult rats , 1999, Neuroscience.

[235]  Y. Rao,et al.  Vertebrate Slit, a Secreted Ligand for the Transmembrane Protein Roundabout, Is a Repellent for Olfactory Bulb Axons , 1999, Cell.

[236]  C. Lois,et al.  Adult Subventricular Zone Neuronal Precursors Continue to Proliferate and Migrate in the Absence of the Olfactory Bulb , 1999, The Journal of Neuroscience.

[237]  Alain Chédotal,et al.  Slit2-Mediated Chemorepulsion and Collapse of Developing Forebrain Axons , 1999, Neuron.

[238]  R. Probstmeier,et al.  Tenascin-C inhibits beta1 integrin-dependent cell adhesion and neurite outgrowth on fibronectin by a disialoganglioside-mediated signaling mechanism. , 1999, Glycobiology.

[239]  C. Sotelo,et al.  Proliferation, migration and differentiation of neuronal progenitor cells in the adult mouse subventricular zone surgically separated from its olfactory bulb , 1998, The European journal of neuroscience.

[240]  Richard Axel,et al.  An Olfactory Sensory Map Develops in the Absence of Normal Projection Neurons or GABAergic Interneurons , 1998, Neuron.

[241]  F. Gage,et al.  Neurogenesis in the adult human hippocampus , 1998, Nature Medicine.

[242]  J. Loturco,et al.  Neuronal Differentiation of Precursors in the Neocortical Ventricular Zone Is Triggered by BMP , 1998, The Journal of Neuroscience.

[243]  C. ffrench-Constant,et al.  Neural precursor cell chain migration and division are regulated through different beta1 integrins. , 1998, Development.

[244]  J. García-Verdugo,et al.  Architecture and cell types of the adult subventricular zone: in search of the stem cells. , 1998, Journal of neurobiology.

[245]  Stanley J. Wiegand,et al.  Intraventricular Administration of BDNF Increases the Number of Newly Generated Neurons in the Adult Olfactory Bulb , 1998, Molecular and Cellular Neuroscience.

[246]  Yuh Nung Jan,et al.  Asymmetric cell division , 1998, Nature.

[247]  T. Kosaka,et al.  How simple is the organization of the olfactory glomerulus?: the heterogeneity of so-called periglomerular cells , 1998, Neuroscience Research.

[248]  J. García-Verdugo,et al.  Primary Neural Precursors and Intermitotic Nuclear Migration in the Ventricular Zone of Adult Canaries , 1998, The Journal of Neuroscience.

[249]  D. van der Kooy,et al.  Transforming Growth Factor-α Null and Senescent Mice Show Decreased Neural Progenitor Cell Proliferation in the Forebrain Subependyma , 1997, The Journal of Neuroscience.

[250]  J. García-Verdugo,et al.  Cellular Composition and Three-Dimensional Organization of the Subventricular Germinal Zone in the Adult Mammalian Brain , 1997, The Journal of Neuroscience.

[251]  S. Baylin,et al.  Conservation of the Drosophila lateral inhibition pathway in human lung cancer: a hairy-related protein (HES-1) directly represses achaete-scute homolog-1 expression. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[252]  Hynek Wichterle,et al.  Direct Evidence for Homotypic, Glia-Independent Neuronal Migration , 1997, Neuron.

[253]  A. Álvarez-Buylla,et al.  Network of tangential pathways for neuronal migration in adult mammalian brain. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[254]  F. Gage,et al.  Differentiation of adult hippocampus-derived progenitors into olfactory neurons in vivo , 1996, Nature.

[255]  M. Mehler,et al.  Bone Morphogenetic Proteins Promote Astroglial Lineage Commitment by Mammalian Subventricular Zone Progenitor Cells , 1996, Neuron.

[256]  J. Chen,et al.  Differential effects of the integrins alpha9beta1, alphavbeta3, and alphavbeta6 on cell proliferative responses to tenascin. Roles of the beta subunit extracellular and cytoplasmic domains. , 1996, The Journal of biological chemistry.

[257]  D. Steindler,et al.  Young neurons from the adult subependymal zone proliferate and migrate along an astrocyte, extracellular matrix‐rich pathway , 1996, Glia.

[258]  T. Magnuson,et al.  The Role of Polysialic Acid in Migration of Olfactory Bulb Interneuron Precursors in the Subventricular Zone , 1996, Neuron.

[259]  Arturo Alvarez-Buylla,et al.  Chain Migration of Neuronal Precursors , 1996, Science.

[260]  D. Jacobowitz,et al.  Chemically defined neuron groups and their subpopulations in the glomerular layer of the rat main olfactory bulb , 1995, Neuroscience Research.

[261]  M. Seike,et al.  The reeler gene-associated antigen on cajal-retzius neurons is a crucial molecule for laminar organization of cortical neurons , 1995, Neuron.

[262]  Brent A. Reynolds,et al.  Neural stem cells in the adult mammalian forebrain: A relatively quiescent subpopulation of subependymal cells , 1994, Neuron.

[263]  T. Magnuson,et al.  N-CAM mutation inhibits tangential neuronal migration and is phenocopied by enzymatic removal of polysialic acid , 1994, Neuron.

[264]  C. Lois,et al.  Long-distance neuronal migration in the adult mammalian brain. , 1994, Science.

[265]  J. Davie,et al.  Multiple functions of dynamic histone acetylation , 1994, Journal of cellular biochemistry.

[266]  K. Moriyoshi,et al.  Persistent expression of helix‐loop‐helix factor HES‐1 prevents mammalian neural differentiation in the central nervous system. , 1994, The EMBO journal.

[267]  K. Rajewsky,et al.  Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning , 1994, Nature.

[268]  T. Magnuson,et al.  Genetic deletion of a neural cell adhesion molecule variant (N-CAM-180) produces distinct defects in the central nervous system , 1993, Neuron.

[269]  R. Shigemoto,et al.  Two mammalian helix-loop-helix factors structurally related to Drosophila hairy and Enhancer of split. , 1992, Genes & development.

[270]  S. Weiss,et al.  Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. , 1992, Science.

[271]  R. Schofield The relationship between the spleen colony-forming cell and the haemopoietic stem cell. , 1978, Blood cells.