Abstract
In this chapter, heterogeneity is explored in the context of the ventricular–subventricular zone, the largest stem cell niche in the mammalian brain. This niche generates up to 10,000 new neurons daily in adult mice and extends over a large spatial area with dorso-ventral and medio-lateral subdivisions. The stem cells of the ventricular–subventricular zone can be subdivided by their anatomical position and transcriptional profile, and the stem cell lineage can also be further subdivided into stages of pre- and post-natal quiescence and activation. Beyond the stem cells proper, additional differences exist in their interactions with other cellular constituents of the niche, including neurons, vasculature, and cerebrospinal fluid. These variations in stem cell potential and local interactions are discussed, as well as unanswered questions within this system.
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References
Lois C, Garcia-Verdugo JM, Alvarez-Buylla A (1996) Chain migration of neuronal precursors. Science 271:978–981
Luskin MB (1993) Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11:173–189
Andreotti JP, Silva WN, Costa AC, Picoli CC, Bitencourt FCO, Coimbra-Campos LMC, Resende RR, Magno LAV, Romano-Silva MA, Mintz A, Birbrair A (2019) Neural stem cell niche heterogeneity. Semin Cell Dev Biol. https://doi.org/10.1016/j.semcdb.2019.01.005
Purves D (2012) Neuroscience. Sinauer Associates, Sunderland, MA
Anthony TE, Klein C, Fishell G, Heintz N (2004) Radial glia serve as neuronal progenitors in all regions of the central nervous system. Neuron 41:881–890
Kriegstein A, Alvarez-Buylla A (2009) The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 32:149–184
Noctor SC, Martinez-Cerdeno V, Kriegstein AR (2007) Neural stem and progenitor cells in cortical development. Novartis Found Symp 288:59–73. discussion 73–8, 96–8
Fentress JC, Stanfield BB, Cowan WM (1981) Observation on the development of the striatum in mice and rats. Anat Embryol 163:275–298
Pilz GA, Shitamukai A, Reillo I, Pacary E, Schwausch J, Stahl R, Ninkovic J, Snippert HJ, Clevers H, Godinho L, Guillemot F, Borrell V, Matsuzaki F, Gotz M (2013) Amplification of progenitors in the mammalian telencephalon includes a new radial glial cell type. Nat Commun 4:2125
Smart IH (1976) A pilot study of cell production by the ganglionic eminences of the developing mouse brain. J Anat 121:71–84
Ross ME (2011) Cell cycle regulation and interneuron production. Dev Neurobiol 71:2–9
Haubensak W, Attardo A, Denk W, Huttner WB (2004) Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc Natl Acad Sci U S A 101:3196–3201
Noctor SC, Martinez-Cerdeno V, Ivic L, Kriegstein AR (2004) Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 7:136–144
Noctor SC, Martinez-Cerdeno V, Kriegstein AR (2008) Distinct behaviors of neural stem and progenitor cells underlie cortical neurogenesis. J Comp Neurol 508:28–44
Fuentealba LC, Rompani SB, Parraguez JI, Obernier K, Romero R, Cepko CL, Alvarez-Buylla A (2015) Embryonic origin of postnatal neural stem cells. Cell 161:1644–1655
Merkle FT, Tramontin AD, Garcia-Verdugo JM, Alvarez-Buylla A (2004) Radial glia give rise to adult neural stem cells in the subventricular zone. Proc Natl Acad Sci U S A 101:17528–17532
Spassky N, Merkle FT, Flames N, Tramontin AD, Garcia-Verdugo JM, Alvarez-Buylla A (2005) Adult ependymal cells are postmitotic and are derived from radial glial cells during embryogenesis. J Neurosci 25:10–18
Tramontin AD, Garcia-Verdugo JM, Lim DA, Alvarez-Buylla A (2003) Postnatal development of radial glia and the ventricular zone (VZ): a continuum of the neural stem cell compartment. Cereb Cortex 13:580–587
Redmond SA, Figueres-Oñate M, Obernier K, Nascimento MA, Parraguez JI, López-Mascaraque L, Fuentealba LC, Alvarez-Buylla A (2019) Development of ependymal and postnatal neural stem cells and their origin from a common embryonic progenitor. Cell Rep 27(2):429–441.e3. https://doi.org/10.1016/j.celrep.2019.01.088
Ortiz-Álvarez G, Daclin M, Shihavuddin A, Lansade P, Fortoul A, Faucourt M, Clavreul S, Lalioti ME, Taraviras S, Hippenmeyer S, Livet J, Meunier A, Genovesio A, Spassky N (2019) Adult neural stem cells and multiciliated ependymal cells share a common lineage regulated by the geminin family members. Neuron 102(1):159–172.e7. https://doi.org/10.1016/j.neuron.2019.01.051
Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97:703–716
Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A (1999) Regeneration of a germinal layer in the adult mammalian brain. Proc Natl Acad Sci U S A 96:11619–11624
Fuentealba LC, Obernier K, Alvarez-Buylla A (2012) Adult neural stem cells bridge their niche. Cell Stem Cell 10:698–708
Kohwi M, Petryniak MA, Long JE, Ekker M, Obata K, Yanagawa Y, Rubenstein JL, Alvarez-Buylla A (2007) A subpopulation of olfactory bulb GABAergic interneurons is derived from Emx1- and Dlx5/6-expressing progenitors. J Neurosci 27:6878–6891
Ventura RE, Goldman JE (2007) Dorsal radial glia generate olfactory bulb interneurons in the postnatal murine brain. J Neurosci 27:4297–4302
Willaime-Morawek S, Seaberg RM, Batista C, Labbe E, Attisano L, Gorski JA, Jones KR, Kam A, Morshead CM, van der Kooy D (2006) Embryonic cortical neural stem cells migrate ventrally and persist as postnatal striatal stem cells. J Cell Biol 175:159–168
Willaime-Morawek S, van der Kooy D (2008) Cortex- and striatum-derived neural stem cells produce distinct progeny in the olfactory bulb and striatum. Eur J Neurosci 27:2354–2362
Young KM, Fogarty M, Kessaris N, Richardson WD (2007) Subventricular zone stem cells are heterogeneous with respect to their embryonic origins and neurogenic fates in the adult olfactory bulb. J Neurosci 27:8286–8296
Brown KN, Chen S, Han Z, Lu CH, Tan X, Zhang XJ, Ding L, Lopez-Cruz A, Saur D, Anderson SA, Huang K, Shi SH (2011) Clonal production and organization of inhibitory interneurons in the neocortex. Science 334:480–486
Ciceri G, Dehorter N, Sols I, Huang ZJ, Maravall M, Marin O (2013) Lineage-specific laminar organization of cortical GABAergic interneurons. Nat Neurosci 16:1199–1210
Harwell CC, Fuentealba LC, Gonzalez-Cerrillo A, Parker PR, Gertz CC, Mazzola E, Garcia MT, Alvarez-Buylla A, Cepko CL, Kriegstein AR (2015) Wide dispersion and diversity of clonally related inhibitory interneurons. Neuron 87:999–1007
Mayer C, Jaglin XH, Cobbs LV, Bandler RC, Streicher C, Cepko CL, Hippenmeyer S, Fishell G (2015) Clonally related forebrain interneurons disperse broadly across both functional areas and structural boundaries. Neuron 87:989–998
Turrero Garcia M, Harwell CC (2017) Radial glia in the ventral telencephalon. FEBS Lett 591:3942–3959
Frantz GD, Mcconnell SK (1996) Restriction of late cerebral cortical progenitors to an upper-layer fate. Neuron 17:55–61
Molyneaux BJ, Arlotta P, Menezes JR, Macklis JD (2007) Neuronal subtype specification in the cerebral cortex. Nat Rev Neurosci 8:427–437
Hartfuss E, Galli R, Heins N, Gotz M (2001) Characterization of CNS precursor subtypes and radial glia. Dev Biol 229:15–30
Doetsch F (2003) The glial identity of neural stem cells. Nat Neurosci 6:1127–1134
Kriegstein AR, Gotz M (2003) Radial glia diversity: a matter of cell fate. Glia 43:37–43
Feng L, Hatten ME, Heintz N (1994) Brain lipid-binding protein (BLBP): a novel signaling system in the developing mammalian CNS. Neuron 12:895–908
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 17:9212–9219
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 289:74–88
Schmechel DE, Rakic P (1979) A Golgi study of radial glial cells in developing monkey telencephalon: morphogenesis and transformation into astrocytes. Anat Embryol 156:115–152
Schmechel DE, Rakic P (1979) Arrested proliferation of radial glial cells during midgestation in rhesus monkey. Nature 277:303–305
Garcia AD, Doan NB, Imura T, Bush TG, Sofroniew MV (2004) GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat Neurosci 7:1233–1241
Imura T, Kornblum HI, Sofroniew MV (2003) The predominant neural stem cell isolated from postnatal and adult forebrain but not early embryonic forebrain expresses GFAP. J Neurosci 23:2824–2832
Morshead CM, Garcia AD, Sofroniew MV, 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 18:76–84
Chaker Z, Codega P, Doetsch F (2016) A mosaic world: puzzles revealed by adult neural stem cell heterogeneity. Wiley Interdiscip Rev Dev Biol 5:640–658
Mirzadeh Z, Merkle FT, Soriano-Navarro M, Garcia-Verdugo JM, 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 3:265–278
Lim DA, Alvarez-Buylla A (2016) The adult ventricular-subventricular zone (V-SVZ) and olfactory bulb (OB) neurogenesis. Cold Spring Harb Perspect Biol 8:pii: a018820
Rushing G, Ihrie RA (2016) Neural stem cell heterogeneity through time and space in the ventricular-subventricular zone. Front Biol 11:261–284
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 U S A 110:E1045–E1054
Obernier K, Cebrian-Silla A, Thomson M, Parraguez JI, Anderson R, Guinto C, Rodas Rodriguez J, Garcia-Verdugo JM, Alvarez-Buylla A (2018) Adult neurogenesis is sustained by symmetric self-renewal and differentiation. Cell Stem Cell 22:221–234.e8
Azim k, Fiorelli r, Zweifel s, Hurtado-Chong a, Yoshikawa k, Slomianka l, Raineteau O (2012) 3-dimensional examination of the adult mouse subventricular zone reveals lineage-specific microdomains. PLoS One 7:e49087
Brill MS, Snapyan M, Wohlfrom H, Ninkovic J, Jawerka M, Mastick GS, Ashery-Padan R, Saghatelyan A, Berninger B, Gotz M (2008) A dlx2- and pax6-dependent transcriptional code for periglomerular neuron specification in the adult olfactory bulb. J Neurosci 28:6439–6452
de Marchis S, Bovetti S, Carletti B, Hsieh YC, Garzotto D, Peretto P, Fasolo A, Puche AC, 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 27:657–664
Delgado RN, Lim DA (2015) Embryonic Nkx2.1-expressing neural precursor cells contribute to the regional heterogeneity of adult V-SVZ neural stem cells. Dev Biol 407:265–274
Fernandez ME, Croce S, Boutin C, Cremer H, Raineteau O (2011) Targeted electroporation of defined lateral ventricular walls: a novel and rapid method to study fate specification during postnatal forebrain neurogenesis. Neural Dev 6:13
Ihrie RA, Shah JK, Harwell CC, Levine JH, Guinto CD, Lezameta M, Kriegstein AR, Alvarez-Buylla A (2011) Persistent sonic hedgehog signaling in adult brain determines neural stem cell positional identity. Neuron 71:250–262
Lopez-Juarez A, Howard J, Ullom K, Howard L, Grande A, Pardo A, Waclaw R, Sun YY, Yang D, Kuan CY, Campbell K, Nakafuku M (2013) Gsx2 controls region-specific activation of neural stem cells and injury-induced neurogenesis in the adult subventricular zone. Genes Dev 27:1272–1287
Merkle FT, Fuentealba LC, Sanders TA, Magno L, Kessaris N, Alvarez-Buylla A (2014) Adult neural stem cells in distinct microdomains generate previously unknown interneuron types. Nat Neurosci 17:207–214
Merkle FT, Mirzadeh Z, Alvarez-Buylla A (2007) Mosaic organization of neural stem cells in the adult brain. Science 317:381–384
Winpenny E, Lebel-Potter M, Fernandez ME, Brill MS, Gotz M, Guillemot F, Raineteau O (2011) Sequential generation of olfactory bulb glutamatergic neurons by Neurog2-expressing precursor cells. Neural Dev 6:12
Colak D, Mori T, Brill MS, Pfeifer A, Falk S, Deng C, Monteiro R, Mummery C, Sommer L, Gotz M (2008) Adult neurogenesis requires Smad4-mediated bone morphogenic protein signaling in stem cells. J Neurosci 28:434–446
Zhuo L, Sun B, Zhang CL, Fine A, Chiu SY, Messing A (1997) Live astrocytes visualized by green fluorescent protein in transgenic mice. Dev Biol 187:36–42
Codega P, Silva-Vargas V, Paul A, Maldonado-Soto AR, Deleo AM, Pastrana E, Doetsch F (2014) Prospective identification and purification of quiescent adult neural stem cells from their in vivo niche. Neuron 82:545–559
Silva-Vargas V, Maldonado-Soto AR, Mizrak D, Codega P, Doetsch F (2016) Age-dependent niche signals from the choroid plexus regulate adult neural stem cells. Cell Stem Cell 19:643–652
Petrik D, Myoga MH, Grade S, Gerkau NJ, Pusch M, Rose CR, Grothe B, Gotz M (2018) Epithelial sodium channel regulates adult neural stem cell proliferation in a flow-dependent manner. Cell Stem Cell 22:865–878.e8
Tavazoie M, Van der Veken L, Silva-Vargas V, Louissaint M, Colonna L, Zaidi B, Garcia-Verdugo JM, Doetsch F (2008) A specialized vascular niche for adult neural stem cells. Cell Stem Cell 3:279–288
Shen Q, Goderie SK, 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 304:1338–1340
Shen Q, Wang Y, Kokovay E, Lin G, Chuang SM, Goderie SK, 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 3:289–300
Tong CK, Chen J, Cebrian-Silla A, Mirzadeh Z, Obernier K, Guinto CD, Tecott LH, Garcia-Verdugo JM, Kriegstein A, Alvarez-Buylla A (2014) Axonal control of the adult neural stem cell niche. Cell Stem Cell 14:500–511
Hoglinger GU, Rizk P, Muriel MP, Duyckaerts C, Oertel WH, Caille I, Hirsch EC (2004) Dopamine depletion impairs precursor cell proliferation in Parkinson disease. Nat Neurosci 7:726–735
Arias-Carrion O, Ortega-Robles E, de Celis-Alonso B, Palasz A, Mendez-Rojas M, Salas-Pacheco J, Murillo-Rodriguez E (2018) Depletion of hypocretin/orexin neurons increases cell proliferation in the adult subventricular zone. CNS Neurol Disord Drug Targets 17:106–112
Paez-Gonzalez P, Abdi K, Luciano D, Liu Y, Soriano-Navarro M, Rawlins E, Bennett V, Garcia-Verdugo JM, Kuo CT (2011) Ank3-dependent SVZ niche assembly is required for the continued production of new neurons. Neuron 71:61–75
Paul A, Chaker Z, Doetsch F (2017) Hypothalamic regulation of regionally distinct adult neural stem cells and neurogenesis. Science 356:1383–1386
Daynac M, Chicheportiche A, Pineda JR, Gauthier LR, Boussin FD, Mouthon MA (2013) Quiescent neural stem cells exit dormancy upon alteration of GABAAR signaling following radiation damage. Stem Cell Res 11:516–528
Fernando RN, Eleuteri B, Abdelhady S, Nussenzweig A, Andang M, Ernfors P (2011) Cell cycle restriction by histone H2AX limits proliferation of adult neural stem cells. Proc Natl Acad Sci U S A 108:5837–5842
Liu X, Wang Q, Haydar TF, Bordey A (2005) Nonsynaptic GABA signaling in postnatal subventricular zone controls proliferation of GFAP-expressing progenitors. Nat Neurosci 8:1179–1187
Nguyen L, Malgrange B, Breuskin I, Bettendorff L, Moonen G, Belachew S, Rigo JM (2003) Autocrine/paracrine activation of the GABA(A) receptor inhibits the proliferation of neurogenic polysialylated neural cell adhesion molecule-positive (PSA-NCAM+) precursor cells from postnatal striatum. J Neurosci 23:3278–3294
Wang DD, Krueger DD, Bordey A (2003) GABA depolarizes neuronal progenitors of the postnatal subventricular zone via GABAA receptor activation. J Physiol 550:785–800
Aguirre A, Rubio ME, Gallo V (2010) Notch and EGFR pathway interaction regulates neural stem cell number and self-renewal. Nature 467:323–327
Alunni A, Krecsmarik M, Bosco A, Galant S, Pan L, Moens CB, Bally-Cuif L (2013) Notch3 signaling gates cell cycle entry and limits neural stem cell amplification in the adult pallium. Development 140:3335–3347
Androutsellis-Theotokis A, Leker RR, Soldner F, Hoeppner DJ, Ravin R, Poser SW, Rueger MA, Bae SK, Kittappa R, Mckay RD (2006) Notch signalling regulates stem cell numbers in vitro and in vivo. Nature 442:823–826
Basak O, Giachino C, Fiorini E, Macdonald HR, Taylor V (2012) Neurogenic subventricular zone stem/progenitor cells are Notch1-dependent in their active but not quiescent state. J Neurosci 32:5654–5666
Nyfeler Y, Kirch RD, Mantei N, Leone DP, Radtke F, Suter U, Taylor V (2005) Jagged1 signals in the postnatal subventricular zone are required for neural stem cell self-renewal. EMBO J 24:3504–3515
Kawai H, Kawaguchi D, Kuebrich BD, Kitamoto T, Yamaguchi M, Gotoh Y, Furutachi S (2017) Area-specific regulation of quiescent neural stem cells by Notch3 in the adult mouse subependymal zone. J Neurosci 37:11867–11880
Lois C, Alvarez-Buylla A (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264:1145–1148
Sawamoto K, Wichterle H, Gonzalez-Perez O, Cholfin JA, Yamada M, Spassky N, Murcia NS, Garcia-Verdugo JM, Marin O, Rubenstein JL, Tessier-Lavigne M, Okano H, Alvarez-Buylla A (2006) New neurons follow the flow of cerebrospinal fluid in the adult brain. Science 311:629–632
Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A (1997) Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci 17:5046–5061
Garcia-Verdugo JM, Doetsch F, Wichterle H, Lim DA, Alvarez-Buylla A (1998) Architecture and cell types of the adult subventricular zone: in search of the stem cells. J Neurobiol 36:234–248
Alvarez-Buylla A, Garcia-Verdugo JM (2002) Neurogenesis in adult subventricular zone. J Neurosci 22:629–634
Doetsch F, Alvarez-Buylla A (1996) Network of tangential pathways for neuronal migration in adult mammalian brain. Proc Natl Acad Sci U S A 93:14895–14900
Falcao AM, Palha JA, Ferreira AC, Marques F, Sousa N, Sousa JC (2012) Topographical analysis of the subependymal zone neurogenic niche. PLoS One 7:e38647
Kelsch W, Mosley CP, Lin CW, Lois C (2007) Distinct mammalian precursors are committed to generate neurons with defined dendritic projection patterns. PLoS Biol 5:e300
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 17:329–340
Dulken BW, Leeman DS, Boutet SC, Hebestreit K, Brunet A (2017) Single-cell transcriptomic analysis defines heterogeneity and transcriptional dynamics in the adult neural stem cell lineage. Cell Rep 18(3):777–790. https://doi.org/10.1016/j.celrep.2016.12.060
Mizrak D, Levitin HM, Delgado AC, Crotet V, Yuan J, Chaker Z, Silva-Vargas V, Sims PA, Doetsch F (2019) Single-cell analysis of regional differences in adult V-SVZ neural stem cell lineages. Cell Rep 26(2):394–406.e5. https://doi.org/10.1016/j.celrep.2018.12.044
Sussel L, Marin O, Kimura S, Rubenstein JL (1999) Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal molecular respecification within the basal telencephalon: evidence for a transformation of the pallidum into the striatum. Development 126:3359–3370
Delgado RN, Lu C, Lim DA (2016) Maintenance of neural stem cell regional identity in culture. Neurogenesis 3:e1187321
Furutachi S, Miya H, Watanabe T, Kawai H, Yamasaki N, Harada Y, Imayoshi I, Nelson M, Nakayama KI, Hirabayashi Y, Gotoh Y (2015) Slowly dividing neural progenitors are an embryonic origin of adult neural stem cells. Nat Neurosci 18:657–665
Lepousez G, Valley MT, Lledo PM (2013) The impact of adult neurogenesis on olfactory bulb circuits and computations. Annu Rev Physiol 75:339–363
Sakamoto M, Ieki N, Miyoshi G, Mochimaru D, Miyachi H, Imura T, Yamaguchi M, Fishell G, Mori K, Kageyama R, Imayoshi I (2014) Continuous postnatal neurogenesis contributes to formation of the olfactory bulb neural circuits and flexible olfactory associative learning. J Neurosci 34:5788–5799
Sakamoto M, Kageyama R, Imayoshi I (2014) The functional significance of newly born neurons integrated into olfactory bulb circuits. Front Neurosci 8:121
Egger V, Urban NN (2006) Dynamic connectivity in the mitral cell-granule cell microcircuit. Semin Cell Dev Biol 17:424–432
Isaacson JS, Strowbridge BW (1998) Olfactory reciprocal synapses: dendritic signaling in the CNS. Neuron 20:749–761
Yokoi M, Mori K, Nakanishi S (1995) Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb. Proc Natl Acad Sci U S A 92:3371–3375
Price JL, Powell TP (1970) The mitral and short axon cells of the olfactory bulb. J Cell Sci 7:631–651
Kosaka K, Aika Y, Toida K, Heizmann CW, Hunziker W, Jacobowitz DM, Nagatsu I, Streit P, Visser TJ, Kosaka T (1995) Chemically defined neuron groups and their subpopulations in the glomerular layer of the rat main olfactory bulb. Neurosci Res 23:73–88
Lledo PM, Merkle FT, Alvarez-Buylla A (2008) Origin and function of olfactory bulb interneuron diversity. Trends Neurosci 31:392–400
Calzolari F, Michel J, Baumgart EV, Theis F, Gotz M, Ninkovic J (2015) Fast clonal expansion and limited neural stem cell self-renewal in the adult subependymal zone. Nat Neurosci 18:490–492
Miyoshi G, Hjerling-Leffler J, Karayannis T, Sousa VH, Butt SJ, Battiste J, Johnson JE, Machold RP, Fishell G (2010) Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. J Neurosci 30:1582–1594
Nery S, Fishell G, Corbin JG (2002) The caudal ganglionic eminence is a source of distinct cortical and subcortical cell populations. Nat Neurosci 5:1279–1287
Wonders CP, Anderson SA (2006) The origin and specification of cortical interneurons. Nat Rev Neurosci 7:687–696
Brill MS, Ninkovic J, Winpenny E, Hodge RD, Ozen I, Yang R, Lepier A, Gascon S, Erdelyi F, Szabo G, Parras C, Guillemot F, Frotscher M, Berninger B, Hevner RF, Raineteau O, Gotz M (2009) Adult generation of glutamatergic olfactory bulb interneurons. Nat Neurosci 12:1524–1533
Gage FH (2000) Mammalian neural stem cells. Science 287:1433–1438
Hack MA, Saghatelyan A, De Chevigny A, Pfeifer A, Ashery-Padan R, Lledo PM, Gotz M (2005) Neuronal fate determinants of adult olfactory bulb neurogenesis. Nat Neurosci 8:865–872
Kohwi M, Osumi N, Rubenstein JL, Alvarez-Buylla A (2005) Pax6 is required for making specific subpopulations of granule and periglomerular neurons in the olfactory bulb. J Neurosci 25:6997–7003
Azim K, Fischer B, Hurtado-Chong A, Draganova K, Cantu C, Zemke M, Sommer L, Butt A, Raineteau O (2014) Persistent Wnt/beta-catenin signaling determines dorsalization of the postnatal subventricular zone and neural stem cell specification into oligodendrocytes and glutamatergic neurons. Stem Cells 32:1301–1312
Gonzalez-Perez O, Alvarez-Buylla A (2011) Oligodendrogenesis in the subventricular zone and the role of epidermal growth factor. Brain Res Rev 67:147–156
Gonzalez-Perez O, Quinones-Hinojosa A (2010) Dose-dependent effect of EGF on migration and differentiation of adult subventricular zone astrocytes. Glia 58:975–983
Gonzalez-Perez O, Romero-Rodriguez R, Soriano-Navarro M, Garcia-Verdugo JM, Alvarez-Buylla A (2009) Epidermal growth factor induces the progeny of subventricular zone type B cells to migrate and differentiate into oligodendrocytes. Stem Cells 27:2032–2043
Menn B, Garcia-Verdugo JM, Yaschine C, Gonzalez-Perez O, Rowitch D, Alvarez-Buylla A (2006) Origin of oligodendrocytes in the subventricular zone of the adult brain. J Neurosci 26:7907–7918
Ortega F, Gascon S, Masserdotti G, Deshpande A, Simon C, Fischer J, Dimou L, Chichung Lie D, Schroeder T, Berninger B (2013) Oligodendrogliogenic and neurogenic adult subependymal zone neural stem cells constitute distinct lineages and exhibit differential responsiveness to Wnt signalling. Nat Cell Biol 15:602–613
Sohn J, Orosco L, Guo F, Chung SH, 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 35:3756–3763
Tong CK, Fuentealba LC, Shah JK, Lindquist RA, Ihrie RA, Guinto CD, Rodas-Rodriguez JL, 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 Reports 5:461–470
Bai CB, Auerbach W, Lee JS, Stephen D, Joyner AL (2002) Gli2, but not Gli1, is required for initial Shh signaling and ectopic activation of the Shh pathway. Development 129:4753–4761
Fuccillo M, Rallu M, Mcmahon AP, Fishell G (2004) Temporal requirement for hedgehog signaling in ventral telencephalic patterning. Development 131:5031–5040
Machold R, Hayashi S, Rutlin M, Muzumdar MD, Nery S, Corbin JG, Gritli-Linde A, Dellovade T, Porter JA, Rubin LL, Dudek H, Mcmahon AP, Fishell G (2003) Sonic hedgehog is required for progenitor cell maintenance in telencephalic stem cell niches. Neuron 39:937–950
Palma V, Lim DA, Dahmane N, Sanchez P, Brionne TC, Herzberg CD, Gitton Y, Carleton A, Alvarez-Buylla A, Ruiz i Altaba A (2005) Sonic hedgehog controls stem cell behavior in the postnatal and adult brain. Development 132:335–344
Petrova R, Garcia AD, Joyner AL (2013) Titration of GLI3 repressor activity by sonic hedgehog signaling is critical for maintaining multiple adult neural stem cell and astrocyte functions. J Neurosci 33:17490–17505
Samanta J, Grund EM, Silva HM, Lafaille JJ, Fishell G, Salzer JL (2015) Inhibition of Gli1 mobilizes endogenous neural stem cells for remyelination. Nature 526(7573):448–452. https://doi.org/10.1038/nature14957
Curtis MA, Kam M, Nannmark U, Anderson MF, Axell MZ, Wikkelso C, Holtas S, van Roon-Mom WM, Bjork-Eriksson T, Nordborg C, Frisen J, Dragunow M, Faull RL, Eriksson PS (2007) Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 315:1243–1249
Sanai N, Tramontin AD, Quinones-Hinojosa A, Barbaro NM, Gupta N, Kunwar S, Lawton MT, Mcdermott MW, Parsa AT, Manuel-Garcia Verdugo J, Berger MS, Alvarez-Buylla A (2004) Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427:740–744
Florio M, Albert M, Taverna E, Namba T, Brandl H, Lewitus E, Haffner C, Sykes A, Wong FK, Peters J, Guhr E, Klemroth S, Prufer K, Kelso J, Naumann R, Nusslein I, Dahl A, Lachmann R, Paabo S, Huttner WB (2015) Human-specific gene ARHGAP11B promotes basal progenitor amplification and neocortex expansion. Science 347:1465–1470
Guerrero-Cazares H, Gonzalez-Perez O, Soriano-Navarro M, Zamora-Berridi G, Garcia-Verdugo JM, Quinones-Hinojosa A (2011) Cytoarchitecture of the lateral ganglionic eminence and rostral extension of the lateral ventricle in the human fetal brain. J Comp Neurol 519:1165–1180
Hansen DV, Lui JH, Flandin P, Yoshikawa K, Rubenstein JL, Alvarez-Buylla A, Kriegstein AR (2013) Non-epithelial stem cells and cortical interneuron production in the human ganglionic eminences. Nat Neurosci 16:1576–1587
Quinones-Hinojosa A, Sanai N, Soriano-Navarro M, Gonzalez-Perez O, Mirzadeh Z, Gil-Perotin S, Romero-Rodriguez R, Berger MS, Garcia-Verdugo JM, Alvarez-Buylla A (2006) Cellular composition and cytoarchitecture of the adult human subventricular zone: a niche of neural stem cells. J Comp Neurol 494:415–434
Sanai N, Berger MS, Garcia-Verdugo JM, Alvarez-Buylla A (2007) Comment on “Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension”. Science 318:393. author reply 393
Sanai N, Nguyen T, Ihrie RA, Mirzadeh Z, Tsai HH, Wong M, Gupta N, Berger MS, Huang E, Garcia-Verdugo JM, Rowitch DH, Alvarez-Buylla A (2011) Corridors of migrating neurons in the human brain and their decline during infancy. Nature 478:382–386
Wang C, Liu F, Liu YY, Zhao CH, 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 21:1534–1550
Zecevic N (2004) Specific characteristic of radial glia in the human fetal telencephalon. Glia 48:27–35
Zecevic N, Chen Y, Filipovic R (2005) Contributions of cortical subventricular zone to the development of the human cerebral cortex. J Comp Neurol 491:109–122
Hansen DV, Lui JH, Parker PR, Kriegstein AR (2010) Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature 464:554–561
Flandin P, Kimura S, Rubenstein JL (2010) The progenitor zone of the ventral medial ganglionic eminence requires Nkx2-1 to generate most of the globus pallidus but few neocortical interneurons. J Neurosci 30:2812–2823
Marin O, Anderson SA, Rubenstein JL (2000) Origin and molecular specification of striatal interneurons. J Neurosci 20:6063–6076
Nobrega-Pereira S, Kessaris N, Du T, Kimura S, Anderson SA, Marin O (2008) Postmitotic Nkx2-1 controls the migration of telencephalic interneurons by direct repression of guidance receptors. Neuron 59:733–745
Wichterle H, Turnbull DH, Nery S, Fishell G, Alvarez-Buylla A (2001) In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain. Development 128:3759–3771
Nowakowski TJ, Bhaduri A, Pollen AA, Alvarado B, Mostajo-Radji MA, Di Lullo E, Haeussler M, Sandoval-Espinosa C, Liu SJ, Velmeshev D, Ounadjela JR, Shuga J, Wang X, Lim DA, West JA, Leyrat AA, Kent WJ, Kriegstein AR (2017) Spatiotemporal gene expression trajectories reveal developmental hierarchies of the human cortex. Science 358:1318–1323
Bignami A, Dahl D (1974) Astrocyte-specific protein and radial glia in the cerebral cortex of newborn rat. Nature 252:55–56
Cameron RS, Rakic P (1991) Glial cell lineage in the cerebral cortex: a review and synthesis. Glia 4:124–137
Dahl D, Rueger DC, 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 24:191–196
Edwards MA, Yamamoto M, Caviness VS, JR. (1990) Organization of radial glia and related cells in the developing murine CNS. An analysis based upon a new monoclonal antibody marker. Neuroscience 36:121–144
Pixley SK, De Vellis J (1984) Transition between immature radial glia and mature astrocytes studied with a monoclonal antibody to vimentin. Brain Res 317:201–209
Schnitzer J, Schachner M (1981) Characterization of isolated mouse cerebellar cell populations in vitro. J Neuroimmunol 1:457–470
Ihrie RA, Alvarez-Buylla A (2009) Neural stem cells disguised as astrocytes. In: Parpura V, Haydon PG (eds) Astrocytes in (patho)physiology of the nervous system. Springer Science+Business Media
Paredes MF, Sorrells SF, Garcia-Verdugo JM, Alvarez-Buylla A (2016) Brain size and limits to adult neurogenesis. J Comp Neurol 524:646–664
Mirzaa GM, Campbell CD, Solovieff N, Goold C, Jansen LA, Menon S, Timms AE, Conti V, Biag JD, Adams C, Boyle EA, Collins S, Ishak G, Poliachik S, Girisha KM, Yeung KS, Chung BHY, Rahikkala E, Gunter SA, Mcdaniel SS, Macmurdo CF, Bernstein JA, Martin B, Leary R, Mahan S, Liu S, Weaver M, Doerschner M, Jhangiani S, Muzny DM, Boerwinkle E, Gibbs RA, Lupski JR, Shendure J, Saneto RP, Novotny EJ, Wilson CJ, Sellers WR, Morrissey M, Hevner RF, Ojemann JG, Guerrini R, Murphy LO, Winckler W, Dobyns WB (2016) Association of MTOR mutations with developmental brain disorders, including megalencephaly, focal cortical dysplasia, and pigmentary mosaicism. JAMA Neurol 73:836–845
Chau KF, Shannon ML, Fame RM, Fonseca E, Mullan H, Johnson MB, Sendamarai AK, Springel MW, Laurent B, Lehtinen MK (2018) Downregulation of ribosome biogenesis during early forebrain development. elife 7:e36998
Khajuria RK, Munschauer M, Ulirsch JC, Fiorini C, Ludwig LS, Mcfarland SK, Abdulhay NJ, Specht H, Keshishian H, Mani DR, Jovanovic M, Ellis SR, Fulco CP, Engreitz JM, Schutz S, Lian J, Gripp KW, Weinberg OK, Pinkus GS, Gehrke L, Regev A, Lander ES, Gazda HT, Lee WY, Panse VG, Carr SA, Sankaran VG (2018) Ribosome levels selectively regulate translation and lineage commitment in human hematopoiesis. Cell 173:90–103.e19
Sanchez CG, Teixeira FK, Czech B, Preall JB, Zamparini AL, Seifert JR, Malone CD, Hannon GJ, Lehmann R (2016) Regulation of ribosome biogenesis and protein synthesis controls germline stem cell differentiation. Cell Stem Cell 18:276–290
Paliouras GN, Hamilton LK, Aumont A, Joppe SE, Barnabe-Heider F, Fernandes KJ (2012) Mammalian target of rapamycin signaling is a key regulator of the transit-amplifying progenitor pool in the adult and aging forebrain. J Neurosci 32:15012–15026
Miyata T, Kawaguchi A, Okano H, Ogawa M (2001) Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 31:727–741
Magnani D, Hasenpusch-Theil K, Jacobs EC, Campagnoni AT, Price DJ, Theil T (2010) The Gli3 hypomorphic mutation Pdn causes selective impairment in the growth, patterning, and axon guidance capability of the lateral ganglionic eminence. J Neurosci 30:13883–13894
Bhide PG (1996) Cell cycle kinetics in the embryonic mouse corpus striatum. J Comp Neurol 374:506–522
Calegari F, Haubensak W, Haffner C, Huttner WB (2005) Selective lengthening of the cell cycle in the neurogenic subpopulation of neural progenitor cells during mouse brain development. J Neurosci 25:6533–6538
Martin-Ibanez R, Pardo M, Giralt A, Miguez A, Guardia I, Marion-Poll L, Herranz C, Esgleas M, Garcia-Diaz Barriga G, Edel MJ, Vicario-Abejon C, Alberch J, Girault JA, Chan S, Kastner P, Canals JM (2017) Helios expression coordinates the development of a subset of striatopallidal medium spiny neurons. Development 144:1566–1577
Pilaz LJ, Mcmahon JJ, Miller EE, Lennox AL, Suzuki A, Salmon E, Silver DL (2016) Prolonged mitosis of neural progenitors alters cell fate in the developing brain. Neuron 89:83–99
Pilaz LJ, Patti D, Marcy G, Ollier E, Pfister S, Douglas RJ, Betizeau M, Gautier E, Cortay V, Doerflinger N, Kennedy H, Dehay C (2009) Forced G1-phase reduction alters mode of division, neuron number, and laminar phenotype in the cerebral cortex. Proc Natl Acad Sci U S A 106:21924–21929
Bjornsson CS, Apostolopoulou M, Tian Y, Temple S (2015) It takes a village: constructing the neurogenic niche. Dev Cell 32:435–446
Bond AM, Ming GL, Song H (2015) Adult mammalian neural stem cells and neurogenesis: five decades later. Cell Stem Cell 17:385–395
Silva-Vargas V, Crouch EE, Doetsch F (2013) Adult neural stem cells and their niche: a dynamic duo during homeostasis, regeneration, and aging. Curr Opin Neurobiol 23:935–942
Lehtinen MK, Zappaterra MW, Chen X, Yang YJ, Hill AD, Lun M, Maynard T, Gonzalez D, Kim S, Ye P, D’ercole A, Wong E, Lamantia A, Walsh C (2011) The cerebrospinal fluid provides a proliferative niche for neural progenitor cells. Neuron 69:893–905
Zappaterra MD, Lisgo SN, Lindsay S, Gygi SP, Walsh CA, Ballif BA (2007) A comparative proteomic analysis of human and rat embryonic cerebrospinal fluid. J Proteome Res 6:3537–3548
Alonso MI, Lamus F, Carnicero E, Moro JA, de la Mano A, Fernandez JMF, Desmond ME, Gato A (2017) Embryonic cerebrospinal fluid increases neurogenic activity in the brain ventricular-subventricular zone of adult mice. Front Neuroanat 11:124
Hoch RV, Rubenstein JL, Pleasure S (2009) Genes and signaling events that establish regional patterning of the mammalian forebrain. Semin Cell Dev Biol 20:378–386
Ulloa F, Briscoe J (2007) Morphogens and the control of cell proliferation and patterning in the spinal cord. Cell Cycle 6:2640–2649
Tong CK, Han YG, Shah JK, Obernier K, Guinto CD, Alvarez-Buylla A (2014) Primary cilia are required in a unique subpopulation of neural progenitors. Proc Natl Acad Sci USA 111(34):12438–12443. https://doi.org/10.1073/pnas.1321425111
Kippin TE, Kapur S, Van Der Kooy D (2005) Dopamine specifically inhibits forebrain neural stem cell proliferation, suggesting a novel effect of antipsychotic drugs. J Neurosci 25:5815–5823
Romero-Grimaldi C, Moreno-Lopez B, Estrada C (2008) Age-dependent effect of nitric oxide on subventricular zone and olfactory bulb neural precursor proliferation. J Comp Neurol 506:339–346
Culver JC, Vadakkan TJ, Dickinson ME (2013) A specialized microvascular domain in the mouse neural stem cell niche. PLoS One 8:e53546
Kazanis I, Lathia JD, Vadakkan TJ, Raborn E, Wan R, Mughal MR, Eckley DM, Sasaki T, Patton B, Mattson MP, Hirschi KK, Dickinson ME, Ffrench-Constant C (2010) Quiescence and activation of stem and precursor cell populations in the subependymal zone of the mammalian brain are associated with distinct cellular and extracellular matrix signals. J Neurosci 30:9771–9781
Baker KL, Daniels SB, Lennington JB, Lardaro T, Czap A, Notti RQ, Cooper O, Isacson O, Frasca S Jr, Conover JC (2006) Neuroblast protuberances in the subventricular zone of the regenerative MRL/MpJ mouse. J Comp Neurol 498:747–761
Ottone C, Krusche B, Whitby A, Clements M, Quadrato G, Pitulescu ME, Adams RH, Parrinello S (2014) Direct cell-cell contact with the vascular niche maintains quiescent neural stem cells. Nat Cell Biol 16:1045–1056
Weinstein BM (2005) Vessels and nerves: marching to the same tune. Cell 120:299–302
Morizur L, Chicheportiche A, Gauthier LR, Daynac M, Boussin FD, Mouthon MA (2018) Distinct molecular signatures of quiescent and activated adult neural stem cells reveal specific interactions with their microenvironment. Stem Cell Reports 11(2):565–577
Douet V, Arikawa-Hirasawa E, Mercier F (2012) Fractone-heparan sulfates mediate BMP-7 inhibition of cell proliferation in the adult subventricular zone. Neurosci Lett 528:120–125
Douet V, Kerever A, Arikawa-Hirasawa E, Mercier F (2013) Fractone-heparan sulphates mediate FGF-2 stimulation of cell proliferation in the adult subventricular zone. Cell Prolif 46:137–145
Kerever A, Schnack J, Vellinga D, Ichikawa N, Moon C, Arikawa-Hirasawa E, Efird JT, Mercier F (2007) Novel extracellular matrix structures in the neural stem cell niche capture the neurogenic factor fibroblast growth factor 2 from the extracellular milieu. Stem Cells 25:2146–2157
Mercier F (2016) Fractones: extracellular matrix niche controlling stem cell fate and growth factor activity in the brain in health and disease. Cell Mol Life Sci 73:4661–4674
Mercier F, Arikawa-Hirasawa E (2012) Heparan sulfate niche for cell proliferation in the adult brain. Neurosci Lett 510:67–72
Mercier F, Douet V (2014) Bone morphogenetic protein-4 inhibits adult neurogenesis and is regulated by fractone-associated heparan sulfates in the subventricular zone. J Chem Neuroanat 57–58:54–61
Alfonso J, Le Magueresse C, Zuccotti A, Khodosevich K, Monyer H (2012) Diazepam binding inhibitor promotes progenitor proliferation in the postnatal SVZ by reducing GABA signaling. Cell Stem Cell 10:76–87
Holmberg J, Armulik A, Senti KA, Edoff K, Spalding K, Momma S, Cassidy R, Flanagan JG, Frisen J (2005) Ephrin-A2 reverse signaling negatively regulates neural progenitor proliferation and neurogenesis. Genes Dev 19:462–471
Todd KL, Baker KL, Eastman MB, Kolling FW, Trausch AG, Nelson CE, Conover JC (2017) EphA4 regulates neuroblast and astrocyte organization in a neurogenic niche. J Neurosci 37:3331–3341
Wu W, Wong K, Chen J, Jiang Z, Dupuis S, Wu JY, Rao Y (1999) Directional guidance of neuronal migration in the olfactory system by the protein slit. Nature 400:331–336
Herrera DG, Garcia-Verdugo JM, Alvarez-Buylla A (1999) Adult-derived neural precursors transplanted into multiple regions in the adult brain. Ann Neurol 46:867–877
Imamura T, Uesaka M, Nakashima K (2014) Epigenetic setting and reprogramming for neural cell fate determination and differentiation. Philos Trans R Soc Lond Ser B Biol Sci 369:pii: 20130511
Gross RE, Mehler MF, Mabie PC, Zang Z, Santschi L, Kessler JA (1996) Bone morphogenetic proteins promote astroglial lineage commitment by mammalian subventricular zone progenitor cells. Neuron 17:595–606
Li W, Cogswell CA, Loturco JJ (1998) Neuronal differentiation of precursors in the neocortical ventricular zone is triggered by BMP. J Neurosci 18:8853–8862
Mabie PC, Mehler MF, Kessler JA (1999) Multiple roles of bone morphogenetic protein signaling in the regulation of cortical cell number and phenotype. J Neurosci 19:7077–7088
Lim DA, Tramontin AD, Trevejo JM, Herrera DG, Garcia-Verdugo JM, Alvarez-Buylla A (2000) Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron 28:713–726
Panchision DM, Pickel JM, Studer L, Lee SH, Turner PA, Hazel TG, Mckay RD (2001) Sequential actions of BMP receptors control neural precursor cell production and fate. Genes Dev 15:2094–2110
Moyon S, Huynh JL, Dutta D, Zhang F, Ma D, Yoo S, Lawrence R, Wegner M, John GR, Emery B, Lubetzki C, Franklin RJM, Fan G, Zhu J, Dupree JL, Casaccia P (2016) Functional characterization of DNA methylation in the oligodendrocyte lineage. Cell Rep 15:748–760
Wu H, Coskun V, Tao J, Xie W, Ge W, Yoshikawa K, Li E, Zhang Y, Sun YE (2010) Dnmt3a-Dependent Nonpromoter Dna Methylation facilitates transcription of neurogenic genes. Science 329:444–448
Hwang WW, Salinas RD, Siu JJ, Kelley KW, Delgado RN, Paredes MF, Alvarez-Buylla A, Oldham MC, Lim DA (2014) Distinct and separable roles for EZH2 in neurogenic astroglia. elife 3:e02439
Lim DA, Huang YC, Swigut T, Mirick AL, Garcia-Verdugo JM, Wysocka J, Ernst P, Alvarez-Buylla A (2009) Chromatin remodelling factor Mll1 is essential for neurogenesis from postnatal neural stem cells. Nature 458:529–533
Baizabal JM, Mistry M, Garcia MT, Gomez N, Olukoya O, Tran D, Johnson MB, Walsh CA, Harwell CC (2018) The epigenetic state of PRDM16-regulated enhancers in radial glia controls cortical neuron position. Neuron 99:239–241
Lim DA, Alvarez-Buylla A (2014) Adult neural stem cells stake their ground. Trends Neurosci 37:563–571
de Chevigny A, Core N, Follert P, Gaudin M, Barbry P, Beclin C, Cremer H (2012) miR-7a regulation of Pax6 controls spatial origin of forebrain dopaminergic neurons. Nat Neurosci 15:1120–1126
Cabili MN, Trapnell C, Goff L, Koziol M, Tazon-Vega B, Regev A, Rinn JL (2011) Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev 25:1915–1927
Ramos AD, Diaz A, Nellore A, Delgado RN, Park KY, Gonzales-Roybal G, Oldham MC, Song JS, Lim DA (2013) Integration of genome-wide approaches identifies lncRNAs of adult neural stem cells and their progeny in vivo. Cell Stem Cell 12:616–628
Ramos AD, Andersen RE, Liu SJ, Nowakowski TJ, Hong SJ, Gertz CC, Salinas RD, Zarabi H, Kriegstein AR, Lim DA (2015) The long noncoding RNA pnky regulates neuronal differentiation of embryonic and postnatal neural stem cells. Cell Stem Cell 16:439–447
Blanpain C, Lowry WE, Geoghegan A, Polak L, Fuchs E (2004) Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche. Cell 118:635–648
Cheung TH, Rando TA (2013) Molecular regulation of stem cell quiescence. Nat Rev Mol Cell Biol 14:329–340
Forsberg EC, Passegue E, Prohaska SS, Wagers AJ, Koeva M, Stuart JM, Weissman IL (2010) Molecular signatures of quiescent, mobilized and leukemia-initiating hematopoietic stem cells. PLoS One 5:e8785
Fukada S, Uezumi A, Ikemoto M, Masuda S, Segawa M, Tanimura N, Yamamoto H, Miyagoe-Suzuki Y, Takeda S (2007) Molecular signature of quiescent satellite cells in adult skeletal muscle. Stem Cells 25:2448–2459
Ivanova NB, Dimos JT, Schaniel C, Hackney JA, Moore KA, Lemischka IR (2002) A stem cell molecular signature. Science 298:601–604
Pallafacchina G, Francois S, Regnault B, Czarny B, Dive V, Cumano A, Montarras D, Buckingham M (2010) An adult tissue-specific stem cell in its niche: a gene profiling analysis of in vivo quiescent and activated muscle satellite cells. Stem Cell Res 4:77–91
Powell AE, Wang Y, Li Y, Poulin EJ, Means AL, Washington MK, Higginbotham JN, Juchheim A, Prasad N, Levy SE, Guo Y, Shyr Y, Aronow BJ, Haigis KM, Franklin JL, Coffey RJ (2012) The pan-ErbB negative regulator Lrig1 is an intestinal stem cell marker that functions as a tumor suppressor. Cell 149:146–158
Venezia TA, Merchant AA, Ramos CA, Whitehouse NL, Young AS, Shaw CA, Goodell MA (2004) Molecular signatures of proliferation and quiescence in hematopoietic stem cells. PLoS Biol 2:e301
Rushing GV, Brockman AA, Bollig MK, Leelatian N, Mobley BC, Irish JM, Ess KC, Fu C, Ihrie RA (2019) Location-dependent maintenance of intrinsic susceptibility to mTORC1-driven tumorigenesis. Life Sci Alliance 2(2):e201800218. https://doi.org/10.26508/lsa.201800218
Ahlenius H, Visan V, Kokaia M, Lindvall O, Kokaia Z (2009) Neural stem and progenitor cells retain their potential for proliferation and differentiation into functional neurons despite lower number in aged brain. J Neurosci 29:4408–4419
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 24:8354–8365
Jin K, Sun Y, Xie L, Batteur S, Mao XO, Smelick C, Logvinova A, Greenberg DA (2003) Neurogenesis and aging: FGF-2 and HB-EGF restore neurogenesis in hippocampus and subventricular zone of aged mice. Aging Cell 2:175–183
Luo J, Daniels SB, Lennington JB, Notti RQ, Conover JC (2006) The aging neurogenic subventricular zone. Aging Cell 5:139–152
Maslov AY, Barone TA, Plunkett RJ, Pruitt SC (2004) Neural stem cell detection, characterization, and age-related changes in the subventricular zone of mice. J Neurosci 24:1726–1733
Tropepe V, Craig CG, Morshead CM, van der Kooy D (1997) Transforming growth factor-alpha null and senescent mice show decreased neural progenitor cell proliferation in the forebrain subependyma. J Neurosci 17:7850–7859
Shook BA, Manz DH, Peters JJ, Kang S, Conover JC (2012) Spatiotemporal changes to the subventricular zone stem cell pool through aging. J Neurosci 32:6947–6956
Capela A, Temple S (2002) LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron 35:865–875
Conover JC, Shook BA (2011) Aging of the subventricular zone neural stem cell niche. Aging Dis 2:49–63
Apostolopoulou M, Kiehl TR, Winter M, Cardenas de la Hoz E, Boles NC, Bjornsson CS, Zuloaga KL, Goderie SK, Wang Y, Cohen AR, Temple S (2017) Non-monotonic changes in progenitor cell behavior and gene expression during aging of the adult V-SVZ neural stem cell niche. Stem Cell Reports 9:1931–1947
Daynac M, Morizur L, Kortulewski T, Gauthier LR, Ruat M, Mouthon MA, Boussin FD (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. https://doi.org/10.3791/53247
Leeman DS, Hebestreit K, Ruetz T, Webb AE, Mckay A, Pollina EA, Dulken BW, Zhao X, Yeo RW, Ho TT, Mahmoudi S, Devarajan K, Passegue E, Rando TA, Frydman J, Brunet A (2018) Lysosome activation clears aggregates and enhances quiescent neural stem cell activation during aging. Science 359:1277–1283
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Rushing, G.V., Bollig, M.K., Ihrie, R.A. (2019). Heterogeneity of Neural Stem Cells in the Ventricular–Subventricular Zone. In: Birbrair, A. (eds) Stem Cells Heterogeneity in Different Organs. Advances in Experimental Medicine and Biology, vol 1169. Springer, Cham. https://doi.org/10.1007/978-3-030-24108-7_1
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