Neural stem cell heterogeneity through time and space in the ventricular-subventricular zone
Received date: 22 Apr 2016
Accepted date: 05 Jun 2016
Published date: 30 Aug 2016
Copyright
BACKGROUND: The origin and classification of neural stem cells (NSCs) has been a subject of intense investigation for the past two decades. Efforts to categorize NSCs based on their location, function and expression have established that these cells are a heterogeneous pool in both the embryonic and adult brain. The discovery and additional characterization of adult NSCs has introduced the possibility of using these cells as a source for neuronal and glial replacement following injury or disease. To understand how one could manipulate NSC developmental programs for therapeutic use, additional work is needed to elucidate how NSCs are programmed and how signals during development are interpreted to determine cell fate.
OBJECTIVE: This review describes the identification, classification and characterization of NSCs within the large neurogenic niche of the ventricular-subventricular zone (V-SVZ).
METHODS: A literature search was conducted using Pubmed including the keywords “ventricular-subventricular zone,” “neural stem cell,” “heterogeneity,” “identity” and/or “single cell” to find relevant manuscripts to include within the review. A special focus was placed on more recent findings using single-cell level analyses on neural stem cells within their niche(s).
RESULTS: This review discusses over 20 research articles detailing findings on V-SVZ NSC heterogeneity, over 25 articles describing fate determinants of NSCs, and focuses on 8 recent publications using distinct single-cell analyses of neural stem cells including flow cytometry and RNA-seq. Additionally, over 60 manuscripts highlighting the markers expressed on cells within the NSC lineage are included in a chart divided by cell type.
CONCLUSIONS: Investigation of NSC heterogeneity and fate decisions is ongoing. Thus far, much research has been conducted in mice however, findings in human and other mammalian species are also discussed here. Implications of NSC heterogeneity established in the embryo for the properties of NSCs in the adult brain are explored, including how these cells may be redirected after injury or genetic manipulation.
Gabrielle Rushing , Rebecca A. Ihrie . Neural stem cell heterogeneity through time and space in the ventricular-subventricular zone[J]. Frontiers in Biology, 2016 , 11(4) : 261 -284 . DOI: 10.1007/s11515-016-1407-1
| 1 |
Aguirre A, Rubio M E, Gallo V (2010). Notch and EGFR pathway interaction regulates neural stem cell number and self-renewal. Nature, 467(7313): 323–327
|
| 2 |
Ahn S, Joyner A L (2005). In vivo analysis of quiescent adult neural stem cells responding to Sonic hedgehog. Nature, 437(7060): 894–897
|
| 3 |
Altman J (1962). Autoradiographic study of degenerative and regenerative proliferation of neuroglia cells with tritiated thymidine. Exp Neurol, 5(4): 302–318
|
| 4 |
Altman J, Das G D (1965). Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol, 124(3): 319–335
|
| 5 |
Alvarez-Buylla A, García-Verdugo J M, Tramontin A D (2001). A unified hypothesis on the lineage of neural stem cells. Nat Rev Neurosci, 2(4): 287–293
|
| 6 |
Alvarez-Buylla A, Seri B, Doetsch F (2002). Identification of neural stem cells in the adult vertebrate brain. Brain Res Bull, 57(6): 751–758
|
| 7 |
Anthony T E, Klein C, Fishell G, Heintz N (2004). Radial glia serve as neuronal progenitors in all regions of the central nervous system. Neuron, 41(6): 881–890
|
| 8 |
Azim K, Zweifel S, Klaus F, Yoshikawa K, Amrein I, Raineteau O (2013). Early decline in progenitor diversity in the marmoset lateral ventricle. Cereb Cortex, 23(4): 922–931
|
| 9 |
Bannerman D M, Rawlins J N, McHugh S B, Deacon R M, Yee B K, Bast T, Zhang W N, Pothuizen H H, Feldon J (2004). Regional dissociations within the hippocampus—memory and anxiety. Neurosci Biobehav Rev, 28(3): 273–283
|
| 10 |
Barraud P, Thompson L, Kirik D, Björklund A, Parmar M (2005). Isolation and characterization of neural precursor cells from the Sox1-GFP reporter mouse. Eur J Neurosci, 22(7): 1555–1569
|
| 11 |
Beckervordersandforth R, Tripathi P, Ninkovic J, Bayam E, Lepier A, Stempfhuber B, Kirchhoff F, Hirrlinger J, Haslinger A, Lie D C, Beckers J, Yoder B, Irmler M, Götz M (2010). In vivo fate mapping and expression analysis reveals molecular hallmarks of prospectively isolated adult neural stem cells. Cell Stem Cell, 7(6): 744–758
|
| 12 |
Bendall S C, Davis K L, Amir A D, Tadmor M D, Simonds E F, Chen T J, Shenfeld D K, Nolan G P, Pe’er D (2014). Single-cell trajectory detection uncovers progression and regulatory coordination in human B cell development. Cell, 157(3): 714–725
|
| 13 |
Benner E J, Luciano D, Jo R, Abdi K, Paez-Gonzalez P, Sheng H, Warner D S, Liu C, Eroglu C, Kuo C T (2013). Protective astrogenesis from the SVZ niche after injury is controlled by Notch modulator Thbs4. Nature, 497(7449): 369–373
|
| 14 |
Bentivoglio M, Mazzarello P (1999). The history of radial glia. Brain Res Bull, 49(5): 305–315
|
| 15 |
Bergmann O, Liebl J, Bernard S, Alkass K, Yeung M S, Steier P, Kutschera W, Johnson L, Landén M, Druid H, Spalding K L, Frisén J (2012). The age of olfactory bulb neurons in humans. Neuron, 74(4): 634–639
|
| 16 |
Bernier P J, Bedard A, Vinet J, Levesque M, Parent A (2002). Newly generated neurons in the amygdala and adjoining cortex of adult primates. Proc Natl Acad Sci USA, 99(17): 11464–11469
|
| 17 |
Bhardwaj R D, Curtis M A, Spalding K L, Buchholz B A, Fink D, Björk-Eriksson T, Nordborg C, Gage F H, Druid H, Eriksson P S, Frisén J (2006). Neocortical neurogenesis in humans is restricted to development. Proc Natl Acad Sci USA, 103(33): 12564–12568
|
| 18 |
Bignami A, Dahl D (1974). Astrocyte-specific protein and radial glia in the cerebral cortex of newborn rat. Nature, 252(5478): 55–56
|
| 19 |
Bignami A, Eng L F, Dahl D, Uyeda C T (1972). Localization of the glial fibrillary acidic protein in astrocytes by immunofluorescence. Brain Res, 43(2): 429–435
|
| 20 |
Breton-Provencher V, Lemasson M, Peralta M R 3rd, Saghatelyan A (2009). Interneurons produced in adulthood are required for the normal functioning of the olfactory bulb network and for the execution of selected olfactory behaviors. J Neurosci, 29(48): 15245–15257
|
| 21 |
Briscoe J, Sussel L, Serup P, Hartigan-O’Connor D, Jessell T M, Rubenstein J L, Ericson J (1999). Homeobox gene Nkx2.2 and specification of neuronal identity by graded Sonic hedgehog signalling. Nature, 398(6728): 622–627
|
| 22 |
Brown K N, Chen S, Han Z, Lu C H, Tan X, Zhang X J, Ding L, Lopez-Cruz A, Saur D, Anderson S A, Huang K, Shi S H (2011). Clonal production and organization of inhibitory interneurons in the neocortex. Science, 334(6055): 480–486
|
| 23 |
Brus M, Meurisse M, Gheusi G, Keller M, Lledo P M, Lévy F (2013). Dynamics of olfactory and hippocampal neurogenesis in adult sheep. J Comp Neurol, 521(1): 169–188
|
| 24 |
Burns K A, Ayoub A E, Breunig J J, Adhami F, Weng W L, Colbert M C, Rakic P, Kuan C Y (2007). Nestin-CreER mice reveal DNA synthesis by nonapoptotic neurons following cerebral ischemia hypoxia. Cereb Cortex, 17(11): 2585–2592
|
| 25 |
Calaora V, Chazal G, Nielsen P J, Rougon G, Moreau H (1996). mCD24 expression in the developing mouse brain and in zones of secondary neurogenesis in the adult. Neuroscience, 73(2): 581–594
|
| 26 |
Calzolari F, Michel J, Baumgart E V, Theis F, Götz M, Ninkovic J (2015). Fast clonal expansion and limited neural stem cell self-renewal in the adult subependymal zone. Nat Neurosci, 18(4): 490–492
|
| 27 |
Cameron H A, McKay R D (2001). Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol, 435(4): 406–417
|
| 28 |
Cameron R S, Rakic P (1991). Glial cell lineage in the cerebral cortex: a review and synthesis. Glia, 4(2): 124–137
|
| 29 |
Campbell K (2003). Dorsal-ventral patterning in the mammalian telencephalon. Curr Opin Neurobiol, 13(1): 50–56
|
| 30 |
Capela A, Temple S (2002). LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron, 35(5): 865–875
|
| 31 |
Chanas-Sacré G, Thiry M, Pirard S, Rogister B, Moonen G, Mbebi C, Verdière-Sahuqué M, Leprince P (2000). A 295-kDA intermediate filament-associated protein in radial glia and developing muscle cells in vivo and in vitro. Dev Dyn, 219(4): 514–525
|
| 32 |
Chen X, Lepier A, Berninger B, Tolkovsky A M, Herbert J (2012). Cultured subventricular zone progenitor cells transduced with neurogenin-2 become mature glutamatergic neurons and integrate into the dentate gyrus. PLoS ONE, 7(2): e31547
|
| 33 |
Christian K M, Song H, Ming G L (2014). Functions and dysfunctions of adult hippocampal neurogenesis. Annu Rev Neurosci, 37(1): 243–262
|
| 34 |
Chuong C M, Edelman G M (1984). Alterations in neural cell adhesion molecules during development of different regions of the nervous system. J Neurosci, 4(9): 2354–2368
|
| 35 |
Codega P, Silva-Vargas V, Paul A, Maldonado-Soto A R, Deleo A M, Pastrana E, Doetsch F (2014). Prospective identification and purification of quiescent adult neural stem cells from their in vivo niche. Neuron, 82(3): 545–559
|
| 36 |
Corti S, Nizzardo M, Nardini M, Donadoni C, Locatelli F, Papadimitriou D, Salani S, Del Bo R, Ghezzi S, Strazzer S, Bresolin N, Comi G P (2007). Isolation and characterization of murine neural stem/progenitor cells based on Prominin-1 expression. Exp Neurol, 205(2): 547–562
|
| 37 |
Coskun V, Wu H, Blanchi B, Tsao S, Kim K, Zhao J, Biancotti J C, Hutnick L, Krueger R C Jr, Fan G, de Vellis J, Sun Y E (2008). CD133+ neural stem cells in the ependyma of mammalian postnatal forebrain. Proc Natl Acad Sci USA, 105(3): 1026–1031
|
| 38 |
Curtis M A, Kam M, Nannmark U, Anderson M F, Axell M Z, Wikkelso C, Holtås S, van Roon-Mom W M, Björk-Eriksson T, Nordborg C, Frisén J, Dragunow M, Faull R L, Eriksson P S (2007). Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science, 315(5816): 1243–1249
|
| 39 |
Dahl D, Rueger D C, Bignami A, Weber K, Osborn M (1981). Vimentin, the 57 000 molecular weight protein of fibroblast filaments, is the major cytoskeletal component in immature glia. Eur J Cell Biol, 24(2): 191–196
|
| 40 |
Davis A A, Temple S (1994). A self-renewing multipotential stem cell in embryonic rat cerebral cortex. Nature, 372(6503): 263–266
|
| 41 |
Dayer A G, Cleaver K M, Abouantoun T, Cameron H A (2005). New GABAergic interneurons in the adult neocortex and striatum are generated from different precursors. J Cell Biol, 168(3): 415–427
|
| 42 |
Daynac M, Morizur L, Kortulewski T, Gauthier L R, Ruat M, Mouthon M A, Boussin F D (2015). Cell Sorting of Neural Stem and Progenitor Cells from the Adult Mouse Subventricular Zone and Live-imaging of their Cell Cycle Dynamics. J Vis Exp, (103)
|
| 43 |
De Marchis S, Bovetti S, Carletti B, Hsieh Y C, Garzotto D, Peretto P, Fasolo A, Puche A C, Rossi F (2007). Generation of distinct types of periglomerular olfactory bulb interneurons during development and in adult mice: implication for intrinsic properties of the subventricular zone progenitor population. J Neurosci, 27(3): 657–664
|
| 44 |
Delgado R N, Lim D A (2015). Embryonic Nkx2.1-expressing neural precursor cells contribute to the regional heterogeneity of adult V-SVZ neural stem cells. Dev Biol, 407(2): 265–274
|
| 45 |
Deng W, Aimone J B, Gage F H (2010). New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat Rev Neurosci, 11(5): 339–350
|
| 46 |
Didier M, Harandi M, Aguera M, Bancel B, Tardy M, Fages C, Calas A, Stagaard M, Møllgård K, Belin M F (1986). Differential immunocytochemical staining for glial fibrillary acidic (GFA) protein, S-100 protein and glutamine synthetase in the rat subcommissural organ, nonspecialized ventricular ependyma and adjacent neuropil. Cell Tissue Res, 245(2): 343–351
|
| 47 |
Doetsch F (2003). The glial identity of neural stem cells. Nat Neurosci, 6(11): 1127–1134
|
| 48 |
Doetsch F, Alvarez-Buylla A (1996). Network of tangential pathways for neuronal migration in adult mammalian brain. Proc Natl Acad Sci USA, 93(25): 14895–14900
|
| 49 |
Doetsch F, Caillé I, Lim D A, García-Verdugo J M, Alvarez-Buylla A (1999a). Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell, 97(6): 703–716
|
| 50 |
Doetsch F, García-Verdugo J M, Alvarez-Buylla A (1997). Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci, 17(13): 5046–5061
|
| 51 |
Doetsch F, García-Verdugo J M, Alvarez-Buylla A (1999b). Regeneration of a germinal layer in the adult mammalian brain. Proc Natl Acad Sci USA, 96(20): 11619–11624
|
| 52 |
Doetsch F, Petreanu L, Caille I, Garcia-Verdugo J M, Alvarez-Buylla A (2002). EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron, 36(6): 1021–1034
|
| 53 |
Edwards M A, Yamamoto M, Caviness V S Jr (1990). Organization of radial glia and related cells in the developing murine CNS. An analysis based upon a new monoclonal antibody marker. Neuroscience, 36(1): 121–144
|
| 54 |
Egger V, Urban N N (2006). Dynamic connectivity in the mitral cell-granule cell microcircuit. Semin Cell Dev Biol, 17(4): 424–432
|
| 55 |
Ehninger D, Kempermann G (2003). Regional effects of wheel running and environmental enrichment on cell genesis and microglia proliferation in the adult murine neocortex. Cereb Cortex, 13(8): 845–851
|
| 56 |
Ellis P, Fagan B M, Magness S T, Hutton S, Taranova O, Hayashi S, McMahon A, Rao M, Pevny L (2004). SOX2, a persistent marker for multipotential neural stem cells derived from embryonic stem cells, the embryo or the adult. Dev Neurosci, 26(2-4): 148–165
|
| 57 |
Englund C, Fink A, Lau C, Pham D, Daza R A, Bulfone A, Kowalczyk T, Hevner R F (2005). Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J Neurosci, 25(1): 247–251
|
| 58 |
Enwere E, Shingo T, Gregg C, Fujikawa H, Ohta S, Weiss S (2004). Aging results in reduced epidermal growth factor receptor signaling, diminished olfactory neurogenesis, and deficits in fine olfactory discrimination. J Neurosci, 24(38): 8354–8365
|
| 59 |
Ericson J, Briscoe J, Rashbass P, van Heyningen V, Jessell T M (1997a). Graded sonic hedgehog signaling and the specification of cell fate in the ventral neural tube. Cold Spring Harb Symp Quant Biol, 62(1): 451–466
|
| 60 |
Ericson J, Rashbass P, Schedl A, Brenner-Morton S, Kawakami A, van Heyningen V, Jessell T M, Briscoe J (1997b). Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling. Cell, 90(1): 169–180
|
| 61 |
Eriksson P S, Perfilieva E, Björk-Eriksson T, Alborn A M, Nordborg C, Peterson D A, Gage F H (1998). Neurogenesis in the adult human hippocampus. Nat Med, 4(11): 1313–1317
|
| 62 |
Ernst A, Alkass K, Bernard S, Salehpour M, Perl S, Tisdale J, Possnert G, Druid H, Frisén J (2014). Neurogenesis in the striatum of the adult human brain. Cell, 156(5): 1072–1083
|
| 63 |
Fan G, Martinowich K, Chin M H, He F, Fouse S D, Hutnick L, Hattori D, Ge W, Shen Y, Wu H, ten Hoeve J, Shuai K, Sun Y E (2005). DNA methylation controls the timing of astrogliogenesis through regulation of JAK-STAT signaling. Development, 132(15): 3345–3356
|
| 64 |
Fanselow M S, Dong H W (2010). Are the dorsal and ventral hippocampus functionally distinct structures? Neuron, 65(1): 7–19
|
| 65 |
Feliciano D M, Bordey A (2013). Newborn cortical neurons: only for neonates? Trends Neurosci, 36(1): 51–61
|
| 66 |
Feng L, Hatten M E, Heintz N (1994). Brain lipid-binding protein (BLBP): a novel signaling system in the developing mammalian CNS. Neuron, 12(4): 895–908
|
| 67 |
Ferri A L, Cavallaro M, Braida D, Di Cristofano A, Canta A, Vezzani A, Ottolenghi S, Pandolfi P P, Sala M, DeBiasi S, Nicolis S K (2004). Sox2 deficiency causes neurodegeneration and impaired neurogenesis in the adult mouse brain. Development, 131(15): 3805–3819
|
| 68 |
Florio M, Albert M, Taverna E, Namba T, Brandl H, Lewitus E, Haffner C, Sykes A, Wong F K, Peters J, Guhr E, Klemroth S, Prüfer K, Kelso J, Naumann R, Nüsslein I, Dahl A, Lachmann R, Pääbo S, Huttner W B (2015). Human-specific gene ARHGAP11B promotes basal progenitor amplification and neocortex expansion. Science, 347(6229): 1465–1470
|
| 69 |
Frantz G D, McConnell S K (1996). Restriction of late cerebral cortical progenitors to an upper-layer fate. Neuron, 17(1): 55–61
|
| 70 |
Fuccillo M, Joyner A L, Fishell G (2006). Morphogen to mitogen: the multiple roles of hedgehog signalling in vertebrate neural development. Nat Rev Neurosci, 7(10): 772–783
|
| 71 |
Fuentealba L C, Obernier K, Alvarez-Buylla A (2012). Adult neural stem cells bridge their niche. Cell Stem Cell, 10(6): 698–708
|
| 72 |
Fuentealba L C, Rompani S B, Parraguez J I, Obernier K, Romero R, Cepko C L, Alvarez-Buylla A (2015). Embryonic Origin of Postnatal Neural Stem Cells. Cell, 161(7): 1644–1655
|
| 73 |
Gage F H (2002). Neurogenesis in the adult brain. J Neurosci, 22(3): 612–613
|
| 74 |
Galileo D S, Gray G E, Owens G C, Majors J, Sanes J R (1990). Neurons and glia arise from a common progenitor in chicken optic tectum: demonstration with two retroviruses and cell type-specific antibodies. Proc Natl Acad Sci USA, 87(1): 458–462
|
| 75 |
Garcia A D, Doan N B, Imura T, Bush T G, Sofroniew M V (2004). GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat Neurosci, 7(11): 1233–1241
|
| 76 |
Garner C C, Brugg B, Matus A (1988). A 70-kilodalton microtubule-associated protein (MAP2c), related to MAP2. J Neurochem, 50(2): 609–615
|
| 77 |
Giachino C, Basak O, Lugert S, Knuckles P, Obernier K, Fiorelli R, Frank S, Raineteau O, Alvarez-Buylla A, Taylor V (2014). Molecular diversity subdivides the adult forebrain neural stem cell population. Stem Cells, 32(1): 70–84
|
| 78 |
Gil-Perotín S, Alvarez-Buylla A, García-Verdugo J M (2009). Identification and characterization of neural progenitor cells in the adult mammalian brain. Adv Anat Embryol Cell Biol, 203: 1–101, ix (ix.)
|
| 79 |
Gleeson J G, Lin P T, Flanagan L A, Walsh C A (1999). Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron, 23(2): 257–271
|
| 80 |
Goldman S A, Nottebohm F (1983). Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain. Proc Natl Acad Sci USA, 80(8): 2390–2394
|
| 81 |
Golds E E, Braun P E (1976). Organization of membrane proteins in the intact myelin sheath. Pyridoxal phosphate and salicylaldehyde as probes of myelin structure. J Biol Chem, 251(15): 4729–4735
|
| 82 |
Gonzales-Roybal G, Lim D A (2013). Chromatin-based epigenetics of adult subventricular zone neural stem cells. Front Genet, 4: 194
|
| 83 |
Gonzalez-Perez O, Alvarez-Buylla A (2011). Oligodendrogenesis in the subventricular zone and the role of epidermal growth factor. Brain Res Brain Res Rev, 67(1-2): 147–156
|
| 84 |
Gonzalez-Perez O, Quiñones-Hinojosa A (2010). Dose-dependent effect of EGF on migration and differentiation of adult subventricular zone astrocytes. Glia, 58(8): 975–983
|
| 85 |
Götz M, Stoykova A, Gruss P (1998). Pax6 controls radial glia differentiation in the cerebral cortex. Neuron, 21(5): 1031–1044
|
| 86 |
Gould E, Vail N, Wagers M, Gross C G (2001). Adult-generated hippocampal and neocortical neurons in macaques have a transient existence. Proc Natl Acad Sci USA, 98(19): 10910–10917
|
| 87 |
Guerrero-Cázares H, Gonzalez-Perez O, Soriano-Navarro M, Zamora-Berridi G, García-Verdugo J M, Quinoñes-Hinojosa A (2011). Cytoarchitecture of the lateral ganglionic eminence and rostral extension of the lateral ventricle in the human fetal brain. J Comp Neurol, 519(6): 1165–1180
|
| 88 |
Guillemot F (2005). Cellular and molecular control of neurogenesis in the mammalian telencephalon. Curr Opin Cell Biol, 17(6): 639–647
|
| 89 |
Hack M A, Saghatelyan A, de Chevigny A, Pfeifer A, Ashery-Padan R, Lledo P M, Götz M (2005). Neuronal fate determinants of adult olfactory bulb neurogenesis. Nat Neurosci, 8(7): 865–872
|
| 90 |
Hall A, Giese N A, Richardson W D (1996). Spinal cord oligodendrocytes develop from ventrally derived progenitor cells that express PDGF alpha-receptors. Development, 122(12): 4085–4094
|
| 91 |
Hansen D V, Lui J H, Parker P R, Kriegstein A R (2010). Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature, 464(7288): 554–561
|
| 92 |
Hart I K, Richardson W D, Heldin C H, Westermark B, Raff M C (1989). PDGF receptors on cells of the oligodendrocyte-type-2 astrocyte (O-2A) cell lineage. Development, 105(3): 595–603
|
| 93 |
Hartfuss E, Galli R, Heins N, Götz M (2001). Characterization of CNS precursor subtypes and radial glia. Dev Biol, 229(1): 15–30
|
| 94 |
Harwell C C, Fuentealba L C, Gonzalez-Cerrillo A, Parker P R, Gertz C C, Mazzola E, Garcia M T, Alvarez-Buylla A, Cepko C L, Kriegstein A R (2015). Wide Dispersion and Diversity of Clonally Related Inhibitory Interneurons. Neuron, 87(5): 999–1007
|
| 95 |
Haubensak W, Attardo A, Denk W, Huttner W B (2004). Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc Natl Acad Sci USA, 101(9): 3196–3201
|
| 96 |
He F, Ge W, Martinowich K, Becker-Catania S, Coskun V, Zhu W, Wu H, Castro D, Guillemot F, Fan G, de Vellis J, Sun Y E (2005). A positive autoregulatory loop of Jak-STAT signaling controls the onset of astrogliogenesis. Nat Neurosci, 8(5): 616–625
|
| 97 |
Herholz K, Schopphoff H, Schmidt M, Mielke R, Eschner W, Scheidhauer K, Schicha H, Heiss W D, Ebmeier K (2002). Direct comparison of spatially normalized PET and SPECT scans in Alzheimer's disease. J Nucl Med, 43(1): 21–26
|
| 98 |
Herrera D G, Garcia-Verdugo J M, Alvarez-Buylla A (1999). Adult-derived neural precursors transplanted into multiple regions in the adult brain. Ann Neurol, 46(6): 867–877
|
| 99 |
Hevner R F (2006). From radial glia to pyramidal-projection neuron: transcription factor cascades in cerebral cortex development. Mol Neurobiol, 33(1): 33–50
|
| 100 |
Hevner R F, Hodge R D, Daza R A, Englund C (2006). Transcription factors in glutamatergic neurogenesis: conserved programs in neocortex, cerebellum, and adult hippocampus. Neurosci Res, 55(3): 223–233
|
| 101 |
His W (1904). Die Entwickelung des menschlichen Gehirns wahrend der esten Monte.Leipzig: Hirzel
|
| 102 |
Hochstim C, Deneen B, Lukaszewicz A, Zhou Q, Anderson D J (2008). Identification of positionally distinct astrocyte subtypes whose identities are specified by a homeodomain code. Cell, 133(3): 510–522
|
| 103 |
Hockfield S, McKay R D (1985). Identification of major cell classes in the developing mammalian nervous system. J Neurosci, 5(12): 3310–3328
|
| 104 |
Huang L, DeVries G J, Bittman E L (1998). Photoperiod regulates neuronal bromodeoxyuridine labeling in the brain of a seasonally breeding mammal. J Neurobiol, 36(3): 410–420
|
| 105 |
Ihrie R A, Shah J K, Harwell C C, Levine J H, Guinto C D, Lezameta M, Kriegstein A R, Alvarez-Buylla A (2011). Persistent sonic hedgehog signaling in adult brain determines neural stem cell positional identity. Neuron, 71(2): 250–262
|
| 106 |
Ihrie R A, Alvarez-Buylla A (2009). Neural Stem Cells Disguised as Astrocytes. In: Astrocytes in (Patho)Physiology of the Nervous System, Parpura V, Haydon P G (Eds.). (Springer US), pp. 27–47
|
| 107 |
Imayoshi I, Isomura A, Harima Y, Kawaguchi K, Kori H, Miyachi H, Fujiwara T, Ishidate F, Kageyama R (2013). Oscillatory control of factors determining multipotency and fate in mouse neural progenitors. Science, 342(6163): 1203–1208
|
| 108 |
Imayoshi I, Sakamoto M, Kageyama R (2011). Genetic methods to identify and manipulate newly born neurons in the adult brain. Front Neurosci, 5: 64
|
| 109 |
Imayoshi I, Sakamoto M, Yamaguchi M, Mori K, Kageyama R (2010). Essential roles of Notch signaling in maintenance of neural stem cells in developing and adult brains. J Neurosci, 30(9): 3489–3498
|
| 110 |
Imura T, Kornblum H I, Sofroniew M V (2003). The predominant neural stem cell isolated from postnatal and adult forebrain but not early embryonic forebrain expresses GFAP. J Neurosci, 23(7): 2824–2832
|
| 111 |
Inta D, Alfonso J, von Engelhardt J, Kreuzberg M M, Meyer A H, van Hooft J A, Monyer H (2008). Neurogenesis and widespread forebrain migration of distinct GABAergic neurons from the postnatal subventricular zone. Proc Natl Acad Sci USA, 105(52): 20994–20999
|
| 112 |
Irvin D K, Nakano I, Paucar A, Kornblum H I (2004). Patterns of Jagged1, Jagged2, Delta-like 1 and Delta-like 3 expression during late embryonic and postnatal brain development suggest multiple functional roles in progenitors and differentiated cells. J Neurosci Res, 75(3): 330–343
|
| 113 |
Isaacson J S, Strowbridge B W (1998). Olfactory reciprocal synapses: dendritic signaling in the CNS. Neuron, 20(4): 749–761
|
| 114 |
Jackson E L, Alvarez-Buylla A (2008). Characterization of adult neural stem cells and their relation to brain tumors. Cells Tissues Organs, 188(1-2): 212–224
|
| 115 |
Johe K K, Hazel T G, Muller T, Dugich-Djordjevic M M, McKay R D (1996). Single factors direct the differentiation of stem cells from the fetal and adult central nervous system. Genes Dev, 10(24): 3129–3140
|
| 116 |
Kaplan M S, Hinds J W (1977). Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science, 197(4308): 1092–1094
|
| 117 |
Kawaguchi A, Miyata T, Sawamoto K, Takashita N, Murayama A, Akamatsu W, Ogawa M, Okabe M, Tano Y, Goldman S A, Okano H (2001). Nestin-EGFP transgenic mice: visualization of the self-renewal and multipotency of CNS stem cells. Mol Cell Neurosci, 17(2): 259–273
|
| 118 |
Kirino T, Brightman M W, Oertel W H, Schmechel D E, Marangos P J (1983). Neuron-specific enolase as an index of neuronal regeneration and reinnervation. J Neurosci, 3(5): 915–923
|
| 119 |
Kirschenbaum B, Doetsch F, Lois C, Alvarez-Buylla A (1999). Adult subventricular zone neuronal precursors continue to proliferate and migrate in the absence of the olfactory bulb. J Neurosci, 19(6): 2171–2180
|
| 120 |
Kohwi M, Osumi N, Rubenstein J L, Alvarez-Buylla A (2005). Pax6 is required for making specific subpopulations of granule and periglomerular neurons in the olfactory bulb. J Neurosci, 25(30): 6997–7003
|
| 121 |
Kohwi M, Petryniak M A, Long J E, Ekker M, Obata K, Yanagawa Y, Rubenstein J L, Alvarez-Buylla A (2007). A subpopulation of olfactory bulb GABAergic interneurons is derived from Emx1- and Dlx5/6-expressing progenitors. J Neurosci, 27(26): 6878–6891
|
| 122 |
Kokovay E, Goderie S, Wang Y, Lotz S, Lin G, Sun Y, Roysam B, Shen Q, Temple S (2010). Adult SVZ lineage cells home to and leave the vascular niche via differential responses to SDF1/CXCR4 signaling. Cell Stem Cell, 7(2): 163–173
|
| 123 |
Kokovay E, Wang Y, Kusek G, Wurster R, Lederman P, Lowry N, Shen Q, Temple S (2012). VCAM1 is essential to maintain the structure of the SVZ niche and acts as an environmental sensor to regulate SVZ lineage progression. Cell Stem Cell, 11(2): 220–230
|
| 124 |
Kopan R, Ilagan M X G (2009). The canonical Notch signaling pathway: unfolding the activation mechanism. Cell, 137(2): 216–233
|
| 125 |
Kornack D R, Rakic P (2001a). Cell proliferation without neurogenesis in adult primate neocortex. Science, 294(5549): 2127–2130
|
| 126 |
Kornack D R, Rakic P (2001b). The generation, migration, and differentiation of olfactory neurons in the adult primate brain. Proc Natl Acad Sci USA, 98(8): 4752–4757
|
| 127 |
Kosaka K, Aika Y, Toida K, Heizmann C W, Hunziker W, Jacobowitz D M, Nagatsu I, Streit P, Visser T J, Kosaka T (1995). Chemically defined neuron groups and their subpopulations in the glomerular layer of the rat main olfactory bulb. Neurosci Res, 23(1): 73–88
|
| 128 |
Kosaka K, Kosaka T (2005). synaptic organization of the glomerulus in the main olfactory bulb: compartments of the glomerulus and heterogeneity of the periglomerular cells. Anat Sci Int, 80(2): 80–90
|
| 129 |
Kriegstein A, Alvarez-Buylla A (2009). The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci, 32(1): 149–184
|
| 130 |
Kriegstein A R, Götz M (2003). Radial glia diversity: a matter of cell fate. Glia, 43(1): 37–43
|
| 131 |
Laywell E D, Rakic P, Kukekov V G, Holland E C, Steindler D A (2000). Identification of a multipotent astrocytic stem cell in the immature and adult mouse brain. Proc Natl Acad Sci USA, 97(25): 13883–13888
|
| 132 |
Lazarini F, Mouthon M A, Gheusi G, de Chaumont F, Olivo-Marin J C, Lamarque S, Abrous D N, Boussin F D, Lledo P M (2009). Cellular and behavioral effects of cranial irradiation of the subventricular zone in adult mice. PLoS ONE, 4(9): e7017
|
| 133 |
Lehtinen M K, Zappaterra M W, Chen X, Yang Y J, Hill A D, Lun M, Maynard T, Gonzalez D, Kim S, Ye P, D’Ercole A J, Wong E T, LaMantia A S, Walsh C A (2011). The cerebrospinal fluid provides a proliferative niche for neural progenitor cells. Neuron, 69(5): 893–905
|
| 134 |
Lendahl U, Zimmerman L B, McKay R D (1990). CNS stem cells express a new class of intermediate filament protein. Cell, 60(4): 585–595
|
| 135 |
Lepousez G, Valley M T, Lledo P M (2013). The impact of adult neurogenesis on olfactory bulb circuits and computations. Annu Rev Physiol, 75(1): 339–363
|
| 136 |
Levine J H, Simonds E F, Bendall S C, Davis K L, Amir A D, Tadmor M D, Litvin O, Fienberg H G, Jager A, Zunder E R, Finck R, Gedman A L, Radtke I, Downing J R, Pe’er D, Nolan G P (2015). Data-Driven Phenotypic Dissection of AML Reveals Progenitor-like Cells that Correlate with Prognosis. Cell, 162(1): 184–197
|
| 137 |
LeVine S M, Goldman J E (1988a). Embryonic divergence of oligodendrocyte and astrocyte lineages in developing rat cerebrum. J Neurosci, 8(11): 3992–4006
|
| 138 |
LeVine S M, Goldman J E (1988b). Ultrastructural characteristics of GD3 ganglioside-positive immature glia in rat forebrain white matter. J Comp Neurol, 277(3): 456–464
|
| 139 |
Levitt P, Cooper M L, Rakic P (1981). Coexistence of neuronal and glial precursor cells in the cerebral ventricular zone of the fetal monkey: an ultrastructural immunoperoxidase analysis. J Neurosci, 1(1): 27–39
|
| 140 |
Li G, Fang L, Fernández G, Pleasure S J (2013). The ventral hippocampus is the embryonic origin for adult neural stem cells in the dentate gyrus. Neuron, 78(4): 658–672
|
| 141 |
Li L, Clevers H (2010). Coexistence of quiescent and active adult stem cells in mammals. Science, 327(5965): 542–545
|
| 142 |
Li X, Sun C, Lin C, Ma T, Madhavan M C, Campbell K, Yang Z (2011). The transcription factor Sp8 is required for the production of parvalbumin-expressing interneurons in the olfactory bulb. J Neurosci, 31(23): 8450–8455
|
| 143 |
Lim D A, Alvarez-Buylla A (1999). Interaction between astrocytes and adult subventricular zone precursors stimulates neurogenesis. Proc Natl Acad Sci USA, 96(13): 7526–7531
|
| 144 |
Lim D A, Alvarez-Buylla A (2016). The Adult Ventricular-Subventricular Zone (V-SVZ) and Olfactory Bulb (OB) Neurogenesis. Cold Spring Harb Perspect Biol, 8(5): 8
|
| 145 |
Lim D A, Huang Y C, Swigut T, Mirick A L, Garcia-Verdugo J M, Wysocka J, Ernst P, Alvarez-Buylla A (2009). Chromatin remodelling factor Mll1 is essential for neurogenesis from postnatal neural stem cells. Nature, 458(7237): 529–533
|
| 146 |
Liu F, You Y, Li X, Ma T, Nie Y, Wei B, Li T, Lin H, Yang Z (2009). Brain injury does not alter the intrinsic differentiation potential of adult neuroblasts. J Neurosci, 29(16): 5075–5087
|
| 147 |
Liu Y, Han S S, Wu Y, Tuohy T M, Xue H, Cai J, Back S A, Sherman L S, Fischer I, Rao M S (2004). CD44 expression identifies astrocyte-restricted precursor cells. Dev Biol, 276(1): 31–46
|
| 148 |
Livneh Y, Adam Y, Mizrahi A (2014). Odor processing by adult-born neurons. Neuron, 81(5): 1097–1110
|
| 149 |
Lledo P M, Alonso M, Grubb M S (2006). Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci, 7(3): 179–193
|
| 150 |
Llorens-Bobadilla E, Zhao S, Baser A, Saiz-Castro G, Zwadlo K, Martin-Villalba A (2015). Single-Cell Transcriptomics Reveals a Population of Dormant Neural Stem Cells that Become Activated upon Brain Injury. Cell Stem Cell, 17(3): 329–340
|
| 151 |
Lois C, Alvarez-Buylla A (1993). Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc Natl Acad Sci USA, 90(5): 2074–2077
|
| 152 |
Lois C, García-Verdugo J M, Alvarez-Buylla A (1996). Chain migration of neuronal precursors. Science, 271(5251): 978–981
|
| 153 |
Long J E, Garel S, Alvarez-Dolado M, Yoshikawa K, Osumi N, Alvarez-Buylla A, Rubenstein J L (2007). Dlx-dependent and-independent regulation of olfactory bulb interneuron differentiation. J Neurosci, 27(12): 3230–3243
|
| 154 |
Longe O, Senior C, Rippon G (2009). The lateral and ventromedial prefrontal cortex work as a dynamic integrated system: evidence from FMRI connectivity analysis. J Cogn Neurosci, 21(1): 141–154
|
| 155 |
Low V F, Faull R L, Bennet L, Gunn A J, Curtis M A (2013). Neurogenesis and progenitor cell distribution in the subgranular zone and subventricular zone of the adult sheep brain. Neuroscience, 244: 173–187
|
| 156 |
Luo J, Daniels S B, Lennington J B, Notti R Q, Conover J C (2006). The aging neurogenic subventricular zone. Aging Cell, 5(2): 139–152
|
| 157 |
Luo Y, Coskun V, Liang A, Yu J, Cheng L, Ge W, Shi Z, Zhang K, Li C, Cui Y, Lin H, Luo D, Wang J, Lin C, Dai Z, Zhu H, Zhang J, Liu J, Liu H, deVellis J, Horvath S, Sun Y E, Li S (2015). Single-cell transcriptome analyses reveal signals to activate dormant neural stem cells. Cell, 161(5): 1175–1186
|
| 158 |
Luzzati F, Peretto P, Aimar P, Ponti G, Fasolo A, Bonfanti L (2003). Glia-independent chains of neuroblasts through the subcortical parenchyma of the adult rabbit brain. Proc Natl Acad Sci USA, 100(22): 13036–13041
|
| 159 |
Marzesco A M, Janich P, Wilsch-Bräuninger M, Dubreuil V, Langenfeld K, Corbeil D, Huttner W B (2005). Release of extracellular membrane particles carrying the stem cell marker prominin-1 (CD133) from neural progenitors and other epithelial cells. J Cell Sci, 118(Pt 13): 2849–2858
|
| 160 |
Maslov A Y, Barone T A, Plunkett R J, Pruitt S C (2004). Neural stem cell detection, characterization, and age-related changes in the subventricular zone of mice. J Neurosci, 24(7): 1726–1733
|
| 161 |
Maurice A (2007). Response to Comment on “Human Neuroblasts Migrate to the Olfactory Bulb via a Lateral Ventricular Extension”. Science, 318(5849): 393c
|
| 162 |
Mayer C, Jaglin X H, Cobbs L V, Bandler R C, Streicher C, Cepko C L, Hippenmeyer S, Fishell G (2015). Clonally Related Forebrain Interneurons Disperse Broadly across Both Functional Areas and Structural Boundaries. Neuron, 87(5): 989–998
|
| 163 |
McCarthy M, Turnbull D H, Walsh C A, Fishell G (2001). Telencephalic neural progenitors appear to be restricted to regional and glial fates before the onset of neurogenesis. J Neurosci, 21(17): 6772–6781
|
| 164 |
McDermott K W, Lantos P L (1989). The distribution of glial fibrillary acidic protein and vimentin in postnatal marmoset (Callithrix jacchus) brain. Brain Res Dev Brain Res, 45(2): 169–177
|
| 165 |
McDermott K W, Lantos P L (1990). Cell proliferation in the subependymal layer of the postnatal marmoset, Callithrix jacchus. Brain Res Dev Brain Res, 57(2): 269–277
|
| 166 |
McMahon A P, Ingham P W, Tabin C J (2003). Developmental roles and clinical significance of hedgehog signaling. Curr Top Dev Biol, 53: 1–114
|
| 167 |
Menn B, Garcia-Verdugo J M, Yaschine C, Gonzalez-Perez O, Rowitch D, Alvarez-Buylla A (2006). Origin of oligodendrocytes in the subventricular zone of the adult brain. J Neurosci, 26(30): 7907–7918
|
| 168 |
Merkle F T, Fuentealba L C, Sanders T A, Magno L, Kessaris N, Alvarez-Buylla A (2014). Adult neural stem cells in distinct microdomains generate previously unknown interneuron types. Nat Neurosci, 17(2): 207–214
|
| 169 |
Merkle F T, Mirzadeh Z, Alvarez-Buylla A (2007). Mosaic organization of neural stem cells in the adult brain. Science, 317(5836): 381–384
|
| 170 |
Merkle F T, Tramontin A D, García-Verdugo J M, Alvarez-Buylla A (2004). Radial glia give rise to adult neural stem cells in the subventricular zone. Proc Natl Acad Sci USA, 101(50): 17528–17532
|
| 171 |
Mich J K, Signer R A, Nakada D, Pineda A, Burgess R J, Vue T Y, Johnson J E, Morrison S J (2014). Prospective identification of functionally distinct stem cells and neurosphere-initiating cells in adult mouse forebrain. eLife, 3: e02669
|
| 172 |
Milosevic A, Noctor S C, Martinez-Cerdeno V, Kriegstein A R, Goldman J E (2008). Progenitors from the postnatal forebrain subventricular zone differentiate into cerebellar-like interneurons and cerebellar-specific astrocytes upon transplantation. Mol Cell Neurosci, 39(3): 324–334
|
| 173 |
Mirzadeh Z, Merkle F T, Soriano-Navarro M, Garcia-Verdugo J M, Alvarez-Buylla A (2008). Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell, 3(3): 265–278
|
| 174 |
Misson J P, Edwards M A, Yamamoto M, Caviness V S Jr (1988). Identification of radial glial cells within the developing murine central nervous system: studies based upon a new immunohistochemical marker. Brain Res Dev Brain Res, 44(1): 95–108
|
| 175 |
Molofsky A V, Slutsky S G, Joseph N M, He S, Pardal R, Krishnamurthy J, Sharpless N E, Morrison S J (2006). Increasing p16INK4a expression decreases forebrain progenitors and neurogenesis during ageing. Nature, 443(7110): 448–452
|
| 176 |
Molyneaux B J, Arlotta P, Menezes J R, Macklis J D (2007). Neuronal subtype specification in the cerebral cortex. Nat Rev Neurosci, 8(6): 427–437
|
| 177 |
Moreno M M, Linster C, Escanilla O, Sacquet J, Didier A, Mandairon N (2009). Olfactory perceptual learning requires adult neurogenesis. Proc Natl Acad Sci USA, 106(42): 17980–17985
|
| 178 |
Mori T, Buffo A, Götz M (2005). The novel roles of glial cells revisited: the contribution of radial glia and astrocytes to neurogenesis. Curr Top Dev Biol, 69: 67–99
|
| 179 |
Morshead C M, Garcia A D, Sofroniew M V, van Der Kooy D (2003). The ablation of glial fibrillary acidic protein-positive cells from the adult central nervous system results in the loss of forebrain neural stem cells but not retinal stem cells. Eur J Neurosci, 18(1): 76–84
|
| 180 |
Morshead C M, Reynolds B A, Craig C G, McBurney M W, Staines W A, Morassutti D, Weiss S, van der Kooy D (1994). Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron, 13(5): 1071–1082
|
| 181 |
Mullen R J, Buck C R, Smith A M (1992). NeuN, a neuronal specific nuclear protein in vertebrates. Development, 116(1): 201–211
|
| 182 |
Nedelec J, Pierres M, Moreau H, Barbet J, Naquet P, Faivre-Sarrailh C, Rougon G (1992). Isolation and characterization of a novel glycosyl-phosphatidylinositol-anchored glycoconjugate expressed by developing neurons. Eur J Biochem, 203(3): 433–442
|
| 183 |
Nishiyama A, Lin X H, Giese N, Heldin C H, Stallcup W B (1996). Co-localization of NG2 proteoglycan and PDGF alpha-receptor on O2A progenitor cells in the developing rat brain. J Neurosci Res, 43(3): 299–314
|
| 184 |
Nissant A, Bardy C, Katagiri H, Murray K, Lledo P M (2009). Adult neurogenesis promotes synaptic plasticity in the olfactory bulb. Nat Neurosci, 12(6): 728–730
|
| 185 |
Niu W, Zang T, Zou Y, Fang S, Smith D K, Bachoo R, Zhang C L (2013). In vivo reprogramming of astrocytes to neuroblasts in the adult brain. Nat Cell Biol, 15(10): 1164–1175
|
| 186 |
Noctor S C, Flint A C, Weissman T A, Wong W S, Clinton B K, Kriegstein A R (2002). Dividing precursor cells of the embryonic cortical ventricular zone have morphological and molecular characteristics of radial glia. J Neurosci, 22(8): 3161–3173
|
| 187 |
Noctor S C, Martínez-Cerdeño V, Ivic L, Kriegstein A R (2004). Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci, 7(2): 136–144
|
| 188 |
Noctor S C, Martinez-Cerdeno, V, Kriegstein A R (2007). Neural stem and progenitor cells in cortical development. Novartis Found Symp, 288: 59–73; discussion 73–58, 96–58
|
| 189 |
Noctor S C, Martínez-Cerdeño V, Kriegstein A R (2008). Distinct behaviors of neural stem and progenitor cells underlie cortical neurogenesis. J Comp Neurol, 508(1): 28–44
|
| 190 |
Omlin F X, Webster H D, Palkovits C G, Cohen S R (1982). Immunocytochemical localization of basic protein in major dense line regions of central and peripheral myelin. J Cell Biol, 95(1): 242–248
|
| 191 |
Ong W Y, Levine J M (1999). A light and electron microscopic study of NG2 chondroitin sulfate proteoglycan-positive oligodendrocyte precursor cells in the normal and kainate-lesioned rat hippocampus. Neuroscience, 92(1): 83–95
|
| 192 |
Paez-Gonzalez P, Abdi K, Luciano D, Liu Y, Soriano-Navarro M, Rawlins E, Bennett V, Garcia-Verdugo J M, Kuo C T (2011). Ank3-dependent SVZ niche assembly is required for the continued production of new neurons. Neuron, 71(1): 61–75
|
| 193 |
Paredes M F, Sorrells S F, Garcia-Verdugo J M, Alvarez-Buylla A (2016). Brain size and limits to adult neurogenesis. J Comp Neurol, 524(3): 646–664
|
| 194 |
Parras C M, Galli R, Britz O, Soares S, Galichet C, Battiste J, Johnson J E, Nakafuku M, Vescovi A, Guillemot F (2004). Mash1 specifies neurons and oligodendrocytes in the postnatal brain. EMBO J, 23(22): 4495–4505
|
| 195 |
Pastrana E, Cheng L C, Doetsch F (2009). Simultaneous prospective purification of adult subventricular zone neural stem cells and their progeny. Proc Natl Acad Sci USA, 106(15): 6387–6392
|
| 196 |
Pencea V, Bingaman K D, Freedman L J, Luskin M B (2001). Neurogenesis in the subventricular zone and rostral migratory stream of the neonatal and adult primate forebrain. Exp Neurol, 172(1): 1–16
|
| 197 |
Peretto P, Merighi A, Fasolo A, Bonfanti L (1997). Glial tubes in the rostral migratory stream of the adult rat. Brain Res Bull, 42(1): 9–21
|
| 198 |
Pérez-Martín M, Cifuentes M, Grondona J M, Bermúdez-Silva F J, Arrabal P M, Pérez-Fígares J M, Jiménez A J, García-Segura L M, Férnandez-Llebrez P, Fernandez-Llebrez P, the P. Fernández-Llebrez (2003). Neurogenesis in explants from the walls of the lateral ventricle of adult bovine brain: role of endogenous IGF-1 as a survival factor. Eur J Neurosci, 17(2): 205–211
|
| 199 |
Petreanu L, Alvarez-Buylla A (2002). Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J Neurosci, 22(14): 6106–6113
|
| 200 |
Picard-Riera N, Decker L, Delarasse C, Goude K, Nait-Oumesmar B, Liblau R, Pham-Dinh D, Baron-Van Evercooren A (2002). Experimental autoimmune encephalomyelitis mobilizes neural progenitors from the subventricular zone to undergo oligodendrogenesis in adult mice. Proc Natl Acad Sci USA, 99(20): 13211–13216
|
| 201 |
Pilaz L J, McMahon J J, Miller E E, Lennox A L, Suzuki A, Salmon E, Silver D L (2016). Prolonged Mitosis of Neural Progenitors Alters Cell Fate in the Developing Brain. Neuron, 89(1): 83–99
|
| 202 |
Pinto L, Mader M T, Irmler M, Gentilini M, Santoni F, Drechsel D, Blum R, Stahl R, Bulfone A, Malatesta P, Beckers J, Götz M (2008). Prospective isolation of functionally distinct radial glial subtypes—lineage and transcriptome analysis. Mol Cell Neurosci, 38(1): 15–42
|
| 203 |
Pixley S K, de Vellis J (1984). Transition between immature radial glia and mature astrocytes studied with a monoclonal antibody to vimentin. Brain Res, 317(2): 201–209
|
| 204 |
Poduslo J F, Braun P E (1975). Topographical arrangement of membrane proteins in the intact myelin sheath. Lactoperoxidase incorproation of iodine into myelin surface proteins. J Biol Chem, 250(3): 1099–1105
|
| 205 |
Ponti G, Obernier K, Guinto C, Jose L, Bonfanti L, Alvarez-Buylla A (2013). Cell cycle and lineage progression of neural progenitors in the ventricular-subventricular zones of adult mice. Proc Natl Acad Sci USA, 110(11): E1045–E1054
|
| 206 |
Price J L, Powell T P (1970). The mitral and short axon cells of the olfactory bulb. J Cell Sci, 7(3): 631–651
|
| 207 |
Pringle N P, Mudhar H S, Collarini E J, Richardson W D (1992). PDGF receptors in the rat CNS: during late neurogenesis, PDGF alpha-receptor expression appears to be restricted to glial cells of the oligodendrocyte lineage. Development, 115(2): 535–551
|
| 208 |
Puelles L, Rubenstein J L (2003). Forebrain gene expression domains and the evolving prosomeric model. Trends Neurosci, 26(9): 469–476
|
| 209 |
Purves D (2012). Neuroscience, 5th edn (Sunderland, Mass.: Sinauer Associates)
|
| 210 |
Qian X, Goderie S K, Shen Q, Stern J H, Temple S (1998). Intrinsic programs of patterned cell lineages in isolated vertebrate CNS ventricular zone cells. Development, 125(16): 3143–3152
|
| 211 |
Quarles R H, Trapp B D (1984). Localization of myelin-associated glycoprotein. J Neurochem, 43(6): 1773–1777
|
| 212 |
Rakic P (1988). Specification of cerebral cortical areas. Science, 241(4862): 170–176
|
| 213 |
Rakic P (2006). A century of progress in corticoneurogenesis: from silver impregnation to genetic engineering. Cereb Cortex, 16(Suppl 1): i3–i17
|
| 214 |
Ramalho-Santos M, Yoon S, Matsuzaki Y, Mulligan R C, Melton D A (2002). “Stemness”: transcriptional profiling of embryonic and adult stem cells. Science, 298(5593): 597–600
|
| 215 |
Ramos A D, Andersen R E, Liu S J, Nowakowski T J, Hong S J, Gertz C C, Salinas R D, Zarabi H, Kriegstein A R, Lim D A (2015). The long noncoding RNA Pnky regulates neuronal differentiation of embryonic and postnatal neural stem cells. Cell Stem Cell, 16(4): 439–447
|
| 216 |
Reid C B, Liang I, Walsh C (1995). Systematic widespread clonal organization in cerebral cortex. Neuron, 15(2): 299–310
|
| 217 |
Reynolds B A, Weiss S (1992). Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science, 255(5052): 1707–1710
|
| 218 |
Roccio M, Schmitter D, Knobloch M, Okawa Y, Sage D, Lutolf M P (2013). Predicting stem cell fate changes by differential cell cycle progression patterns. Development, 140(2): 459–470
|
| 219 |
Rochefort C, Gheusi G, Vincent J D, Lledo P M (2002). Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J Neurosci, 22(7): 2679–2689
|
| 220 |
Rodríguez-Pérez L M, Pérez-Martín M, Jiménez A J, Fernández-Llebrez P (2003). Immunocytochemical characterisation of the wall of the bovine lateral ventricle. Cell Tissue Res, 314(3): 325–335
|
| 221 |
Rougon G, Alterman L A, Dennis K, Guo X J, Kinnon C (1991). The murine heat-stable antigen: a differentiation antigen expressed in both the hematolymphoid and neural cell lineages. Eur J Immunol, 21(6): 1397–1402
|
| 222 |
Sakamoto M, Ieki N, Miyoshi G, Mochimaru D, Miyachi H, Imura T, Yamaguchi M, Fishell G, Mori K, Kageyama R, Imayoshi I (2014a). Continuous postnatal neurogenesis contributes to formation of the olfactory bulb neural circuits and flexible olfactory associative learning. J Neurosci, 34(17): 5788–5799
|
| 223 |
Sakamoto M, Kageyama R, Imayoshi I (2014b). The functional significance of newly born neurons integrated into olfactory bulb circuits. Front Neurosci, 8: 121
|
| 224 |
Samanta J, Grund E M, Silva H M, Lafaille J J, Fishell G, Salzer J L (2015). Inhibition of Gli1 mobilizes endogenous neural stem cells for remyelination. Nature, 526(7573): 448–452
|
| 225 |
Sanai N, Berger M S, Garcia-Verdugo J M, Alvarez-Buylla A (2007). Comment on “Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension”. Science, 318(5849): 393, author reply 393
|
| 226 |
Sanai N, Nguyen T, Ihrie R A, Mirzadeh Z, Tsai H H, Wong M, Gupta N, Berger M S, Huang E, Garcia-Verdugo J M, Rowitch D H, Alvarez-Buylla A (2011). Corridors of migrating neurons in the human brain and their decline during infancy. Nature, 478(7369): 382–386
|
| 227 |
Sanai N, Tramontin A D, Quiñones-Hinojosa A, Barbaro N M, Gupta N, Kunwar S, Lawton M T, McDermott M W, Parsa A T, Manuel-García Verdugo J, Berger M S, Alvarez-Buylla A (2004). Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature, 427(6976): 740–744
|
| 228 |
Sawamoto K, Hirota Y, Alfaro-Cervello C, Soriano-Navarro M, He X, Hayakawa-Yano Y, Yamada M, Hikishima K, Tabata H, Iwanami A, Nakajima K, Toyama Y, Itoh T, Alvarez-Buylla A, Garcia-Verdugo J M, Okano H (2011). Cellular composition and organization of the subventricular zone and rostral migratory stream in the adult and neonatal common marmoset brain. J Comp Neurol, 519(4): 690–713
|
| 229 |
Sawamoto K, Wichterle H, Gonzalez-Perez O, Cholfin J A, Yamada M, Spassky N, Murcia N S, Garcia-Verdugo J M, Marin O, Rubenstein J L, Tessier-Lavigne M, Okano H, Alvarez-Buylla A (2006). New neurons follow the flow of cerebrospinal fluid in the adult brain. Science, 311(5761): 629–632
|
| 230 |
Schmechel D E, Marangos P J (1983). Neuron specific enolase as a marker or differentiation in neurons and neuroendocine cells. In: McKelvey J, Ba J, ed. Current Methods in Cellular Neurobiology. New York: John Wiley & Sons. pp 1–62
|
| 231 |
Schmechel D E, Rakic P (1979). A Golgi study of radial glial cells in developing monkey telencephalon: morphogenesis and transformation into astrocytes. Anat Embryol (Berl), 156(2): 115–152
|
| 232 |
Schnitzer J, Schachner M (1981). Characterization of isolated mouse cerebellar cell populations in vitro. J Neuroimmunol, 1(4): 457–470
|
| 233 |
Shen Q, Goderie S K, Jin L, Karanth N, Sun Y, Abramova N, Vincent P, Pumiglia K, Temple S (2004). Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science, 304(5675): 1338–1340
|
| 234 |
Shen Q, Wang Y, Kokovay E, Lin G, Chuang S M, Goderie S K, Roysam B, Temple S (2008). Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions. Cell Stem Cell, 3(3): 289–300
|
| 235 |
Shibata T, Yamada K, Watanabe M, Ikenaka K, Wada K, Tanaka K, Inoue Y (1997). Glutamate transporter GLAST is expressed in the radial glia-astrocyte lineage of developing mouse spinal cord. J Neurosci, 17(23): 9212–9219
|
| 236 |
Shin J, Berg D A, Zhu Y, Shin J Y, Song J, Bonaguidi M A, Enikolopov G, Nauen D W, Christian K M, Ming G L, Song H (2015). Single-Cell RNA-Seq with Waterfall Reveals Molecular Cascades underlying Adult Neurogenesis. Cell Stem Cell, 17(3): 360–372
|
| 237 |
Sidman R L, Miale I L, Feder N (1959). Cell proliferation and migration in the primitive ependymal zone: an autoradiographic study of histogenesis in the nervous system. Exp Neurol, 1(4): 322–333
|
| 238 |
Sohn J, Orosco L, Guo F, Chung S H, Bannerman P, Mills Ko E, Zarbalis K, Deng W, Pleasure D (2015). The subventricular zone continues to generate corpus callosum and rostral migratory stream astroglia in normal adult mice. J Neurosci, 35(9): 3756–3763
|
| 239 |
Sommer I, Schachner M (1981). Monoclonal antibodies (O1 to O4) to oligodendrocyte cell surfaces: an immunocytological study in the central nervous system. Dev Biol, 83(2): 311–327
|
| 240 |
Spalding K L, Bergmann O, Alkass K, Bernard S, Salehpour M, Huttner H B, Boström E, Westerlund I, Vial C, Buchholz B A, Possnert G, Mash D C, Druid H, Frisén J (2013). Dynamics of hippocampal neurogenesis in adult humans. Cell, 153(6): 1219–1227
|
| 241 |
Spassky N, Merkle F T, Flames N, Tramontin A D, García-Verdugo J M, Alvarez-Buylla A (2005). Adult ependymal cells are postmitotic and are derived from radial glial cells during embryogenesis. J Neurosci, 25(1): 10–18
|
| 242 |
Stallcup W B, Beasley L (1987). Bipotential glial precursor cells of the optic nerve express the NG2 proteoglycan. J Neurosci, 7(9): 2737–2744
|
| 243 |
Stühmer T, Puelles L, Ekker M, Rubenstein J L (2002). Expression from a Dlx gene enhancer marks adult mouse cortical GABAergic neurons. Cereb Cortex, 12(1): 75–85
|
| 244 |
Sultan S, Mandairon N, Kermen F, Garcia S, Sacquet J, Didier A (2010). Learning-dependent neurogenesis in the olfactory bulb determines long-term olfactory memory. FASEB J, 24(7): 2355–2363. doi: 10.1096/fj.09-151456
|
| 245 |
Sunabori T, Tokunaga A, Nagai T, Sawamoto K, Okabe M, Miyawaki A, Matsuzaki Y, Miyata T, Okano H (2008). Cell-cycle-specific nestin expression coordinates with morphological changes in embryonic cortical neural progenitors. J Cell Sci, 121(Pt 8): 1204–1212
|
| 246 |
Szatkowska I, Szymańska O, Grabowska A (2004). The role of the human ventromedial prefrontal cortex in memory for contextual information. Neurosci Lett, 364(2): 71–75
|
| 247 |
Temple S (2001). The development of neural stem cells. Nature, 414(6859): 112–117
|
| 248 |
Tong C K, Fuentealba L C, Shah J K, Lindquist R A, Ihrie R A, Guinto C D, Rodas-Rodriguez J L, Alvarez-Buylla A (2015). A Dorsal SHH-Dependent Domain in the V-SVZ Produces Large Numbers of Oligodendroglial Lineage Cells in the Postnatal Brain. Stem Cell Rep, 5(4): 461–470
|
| 249 |
Uchida N, Buck D W, He D, Reitsma M J, Masek M, Phan T V, Tsukamoto A S, Gage F H, Weissman I L (2000). Direct isolation of human central nervous system stem cells. Proc Natl Acad Sci USA, 97(26): 14720–14725
|
| 250 |
Ullensvang K, Lehre K P, Storm-Mathisen J, Danbolt N C (1997). Differential developmental expression of the two rat brain glutamate transporter proteins GLAST and GLT. Eur J Neurosci, 9(8): 1646–1655
|
| 251 |
Ventura R E, Goldman J E (2007). Dorsal radial glia generate olfactory bulb interneurons in the postnatal murine brain. J Neurosci, 27(16): 4297–4302
|
| 252 |
Voigt T (1989). Development of glial cells in the cerebral wall of ferrets: direct tracing of their transformation from radial glia into astrocytes. J Comp Neurol, 289(1): 74–88
|
| 253 |
Waclaw R R, Allen Z J 2nd, Bell S M, Erdélyi F, Szabó G, Potter S S, Campbell K (2006). The zinc finger transcription factor Sp8 regulates the generation and diversity of olfactory bulb interneurons. Neuron, 49(4): 503–516
|
| 254 |
Walker A S, Goings G E, Kim Y, Miller R J, Chenn A, Szele F G (2010). Nestin reporter transgene labels multiple central nervous system precursor cells. Neural Plast, 2010: 894374
|
| 255 |
Walsh C, Cepko C L (1988). Clonally related cortical cells show several migration patterns. Science, 241(4871): 1342–1345
|
| 256 |
Walsh C, Cepko C L (1992). Widespread dispersion of neuronal clones across functional regions of the cerebral cortex. Science, 255(5043): 434–440
|
| 257 |
Walsh C, Cepko C L (1993). Clonal dispersion in proliferative layers of developing cerebral cortex. Nature, 362(6421): 632–635
|
| 258 |
Wang C, Liu F, Liu Y Y, Zhao C H, You Y, Wang L, Zhang J, Wei B, Ma T, Zhang Q, Zhang Y, Chen R, Song H, Yang Z (2011). Identification and characterization of neuroblasts in the subventricular zone and rostral migratory stream of the adult human brain. Cell Res, 21(11): 1534–1550
|
| 259 |
Wang D D, Bordey A (2008). The astrocyte odyssey. Prog Neurobiol, 86(4): 342–367
|
| 260 |
Ware M L, Tavazoie S F, Reid C B, Walsh C A (1999). Coexistence of widespread clones and large radial clones in early embryonic ferret cortex. Cereb Cortex, 9(6): 636–645
|
| 261 |
Weiss S, Dunne C, Hewson J, Wohl C, Wheatley M, Peterson A C, Reynolds B A (1996). Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J Neurosci, 16(23): 7599–7609
|
| 262 |
Wichterle H, Garcia-Verdugo J M, Herrera D G, Alvarez-Buylla A (1999). Young neurons from medial ganglionic eminence disperse in adult and embryonic brain. Nat Neurosci, 2(5): 461–466
|
| 263 |
Willaime-Morawek S, Seaberg R M, Batista C, Labbé E, Attisano L, Gorski J A, Jones K R, Kam A, Morshead C M, van der Kooy D (2006). Embryonic cortical neural stem cells migrate ventrally and persist as postnatal striatal stem cells. J Cell Biol, 175(1): 159–168
|
| 264 |
Young K M, Fogarty M, Kessaris N, Richardson W D (2007). Subventricular zone stem cells are heterogeneous with respect to their embryonic origins and neurogenic fates in the adult olfactory bulb. J Neurosci, 27(31): 8286–8296
|
| 265 |
Zappaterra M D, Lisgo S N, Lindsay S, Gygi S P, Walsh C A, Ballif B A (2007). A comparative proteomic analysis of human and rat embryonic cerebrospinal fluid. J Proteome Res, 6(9): 3537–3548
|
| 266 |
Zappone M V, Galli R, Catena R, Meani N, De Biasi S, Mattei E, Tiveron C, Vescovi A L, Lovell-Badge R, Ottolenghi S, Nicolis S K (2000). Sox2 regulatory sequences direct expression of a (beta)-geo transgene to telencephalic neural stem cells and precursors of the mouse embryo, revealing regionalization of gene expression in CNS stem cells. Development, 127(11): 2367–2382
|
| 267 |
Zecevic N (2004). Specific characteristic of radial glia in the human fetal telencephalon. Glia, 48(1): 27–35
|
| 268 |
Zecevic N, Chen Y, Filipovic R (2005). Contributions of cortical subventricular zone to the development of the human cerebral cortex. J Comp Neurol, 491(2): 109–122
|
| 269 |
Zhao C, Deng W, Gage F H (2008). Mechanisms and functional implications of adult neurogenesis. Cell, 132(4): 645–660
|
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