Skip to main content

Regulatory Mechanisms Underlying the Neurogenesis-to-Gliogenesis Switch by Neural Stem Cells

  • Chapter
  • First Online:
Cortical Development

Abstract

During development of the vertebrate central nervous system (CNS), neural stem cells (NSCs) first generate neurons, followed by glia. This sequential production of specific cell types is advantageous for the organism, since glia play pivotal roles in the maintenance and function of neurons and also, under some conditions, in the inhibition of axonal growth. The latter may be related to the conservation of the newly established neuronal circuitry. The temporal regulation of stem cell differentiation is captivating, given that the loss of stem cell plasticity is often part of the standard mammalian aging process. The reduced plasticity of adult stem cells, including NSCs, directly affects the capacity of the metazoan to regenerate lost or damaged neural tissue and seems to have occurred over the course of evolution. Indeed, the injured adult mammalian brain is scarcely capable of regeneration, not only due to the limited number of adult NSCs but also because of their low neurogenic capacity, except for in certain restricted CNS regions. By contrast, some lower vertebrates (e.g., red-spotted newts) show high regenerative capacity in the brain, with the efficient induction of neurogenesis after injury. Therefore, addressing the regulatory mechanisms underlying the neurogenesis-to-gliogenesis switch by NSCs during development is critical to understanding the restricted plasticity of the adult mammalian CNS. Accordingly, this chapter will review the recent progress in the field of NSC biology, especially regarding the temporal regulation of neurogenesis and gliogenesis.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Altmann CR, Brivanlou AH (2001) Neural patterning in the vertebrate embryo. Int Rev Cytol 203:447–482. doi:10.1016/S0074-7696(01)03013-3

    PubMed  CAS  Google Scholar 

  • Asano H, Aonuma M, Sanosaka T, Kohyama J, Namihira M, Nakashima K (2009) Astrocyte differentiation of neural precursor cells is enhanced by retinoic acid through a change in epigenetic modification. Stem Cells 27:2744–2752. doi:10.1002/stem.176

    PubMed  CAS  Google Scholar 

  • Barnabe´-Heider F, Wasylnka JA, Fernandes KJ, Porsche C, Sendtner M, Kaplan DR, Miller FD (2005) Evidence that embryonic neurons regulate the onset of cortical gliogenesis via cardiotrophin-1. Neuron 48:253–265. doi:10.1016/j.neuron.2005.08.037

    PubMed  Google Scholar 

  • Bayer SA, Altman J (1991) Neocortical development. Raven, New York

    Google Scholar 

  • Bonaguidi MA, McGuire T, Hu M, Kan L, Samanta J, Kessler JA (2005) LIF and BMP signaling generate separate and discrete types of GFAP-expressing cells. Development 132:5503–5514. doi:10.1242/dev.02166

    PubMed  CAS  Google Scholar 

  • Bonaguidi MA, Wheeler MA, Shapiro JS, Stadel RP, Sun GJ, Ming GL, Song H (2011) In vivo clonal analysis reveals self-renewing and multipotent adult neural stem cell characteristics. Cell 145:1142–1155. doi:10.1016/j.cell.2011.05.024

    PubMed  CAS  Google Scholar 

  • Bultje RS, Castaneda-Castellanos DR, Jan LY, Jan YN, Kriegstein AR, Shi SH (2009) Mammalian Par3 regulates progenitor cell asymmetric division via notch signaling in the developing neocortex. Neuron 63:189–202. doi:10.1016/j.neuron.2009.07.004

    PubMed  CAS  Google Scholar 

  • Burrows RC, Wancio D, Levitt P, Lillien L (1997) Response diversity and the timing of progenitor cell maturation are regulated by developmental changes in EGFR expression in the cortex. Neuron 19:251–267. doi:10.1016/S0896-6273(00)80937-X

    PubMed  CAS  Google Scholar 

  • Cai L, Morrow EM, Cepko CL (2000) Misexpression of basic helix-loop-helix genes in the murine cerebral cortex affects cell fate choices and neuronal survival. Development 127:3021–3030

    PubMed  CAS  Google Scholar 

  • Cai J, Qi Y, Hu X, Tan M, Liu Z, Zhang J, Li Q, Sander M, Qiu M (2005) Generation of oligodendrocyte precursor cells from mouse dorsal spinal cord independent of Nkx6 regulation and Shh signaling. Neuron 45:41–53. doi:10.1016/j.neuron.2004.12.028

    PubMed  CAS  Google Scholar 

  • Cebolla B, Vallejo M (2006) Nuclear factor-I regulates glial fibrillary acidic protein gene expression in astrocytes differentiated from cortical precursor cells. J Neurochem 97:1057–1070. doi:10.1111/j.1471-4159.2006.03804.x

    PubMed  CAS  Google Scholar 

  • Chambers CB, Peng Y, Nguyen H, Gaiano N, Fishell G, Nye JS (2001) Spatiotemporal selectivity of response to Notch1 signals in mammalian forebrain precursors. Development 128:689–702

    PubMed  CAS  Google Scholar 

  • Chandran S, Kato H, Gerreli D, Compston A, Svendsen CN, Allen ND (2003) FGF-dependent generation of oligodendrocytes by a hedgehog-independent pathway. Development 130:6599–6609. doi:10. 1242/dev.00871

    PubMed  CAS  Google Scholar 

  • Cheng LC, Pastrana E, Tavazoie M, Doetsch F (2009) miR-124 regulates adult neurogenesis in the subventricular zone stem cell niche. Nat Neurosci 12:399–408. doi:10.1038/nn.2294

    PubMed  CAS  Google Scholar 

  • Cichowski K, Jacks T (2001) NF1 tumor suppressor gene function: narrowing the GAP. Cell 104:593–604. doi:10.1016/S0092-8674(01)00245-8

    PubMed  CAS  Google Scholar 

  • Conti L, Cattaneo E (2010) Neural stem cell systems: physiological players or in vitro entities? Nat Rev Neurosci 11:176–187. doi:10.1038/nrn2761

    PubMed  CAS  Google Scholar 

  • Costa MR, Wen G, Lepier A, Schroeder T, Götz M (2008) Par-complex proteins promote proliferative progenitor divisions in the developing mouse cerebral cortex. Development 135:11–22. doi:10.1242/dev.009951

    PubMed  CAS  Google Scholar 

  • Costa MR, Bucholz O, Schroeder T, Götz M (2009) Late origin of glia-restricted progenitors in the developing mouse cerebral cortex. Cereb Cortex 19(Suppl 1):i135–i143. doi:10.1093/cercor/bhp046

    PubMed  Google Scholar 

  • Cundiff P, Liu L, Wang Y, Zou J, Pan YW, Abel G, Duan X, Ming GL, Englund C, Hevner R, Xia Z (2009) ERK5 MAP kinase regulates neurogenin1 during cortical neurogenesis. PLoS One 4:e5204. doi:10.1371/journal.pone.0005204

    PubMed  Google Scholar 

  • Delaunay D, Heydon K, Cumano A, Schwab MH, Thomas JL, Suter U, Nave KA, Zalc B, Spassky N (2008) Early neuronal and glial fate restriction of embryonic neural stem cells. J Neurosci 28:2551–2562. doi:10.1523/JNEUROSCI.5497-07.2008

    PubMed  CAS  Google Scholar 

  • Deneen B, Ho R, Lukaszewicz A, Hochstim CJ, Gronostajski RM, Anderson DJ (2006) The transcription factor NFIA controls the onset of gliogenesis in the developing spinal cord. Neuron 52:953–968. doi:10.1016/j.neuron.2006.11.019

    PubMed  CAS  Google Scholar 

  • Deverman BE, Patterson PH (2009) Cytokines and CNS development. Neuron 64:61–78. doi:10.1016/j.neuron.2009.09.002

    PubMed  CAS  Google Scholar 

  • Doetsch F, Caille I, Lim DA, García-Verdugo JM, Alvarez-Buylla A (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97:1–20. doi:10.1016/S0092-8674(00)80783-7

    Google Scholar 

  • Doetsch F, Petreanu L, Caille I, JM G ́ı-V, Alvarez-Buylla A (2002) EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 36:1021–1034. doi:10.1016/S0896-6273(02)01133-9

    PubMed  CAS  Google Scholar 

  • Dong Z, Yang N, Yeo SY, Chitnis A, Guo S (2012) Intralineage directional Notch signaling regulates self-renewal and differentiation of asymmetrically dividing radial glia. Neuron 74:65–78. doi:10.1016/j.neuron.2012.01.031

    PubMed  CAS  Google Scholar 

  • Drögemüller K, Helmuth U, Brunn A, Sakowicz-Burkiewicz M, Gutmann DH, Mueller W, Deckert M, Schlüter D (2008) Astrocyte gp130 expression is critical for the control of Toxoplasma encephalitis. J Immunol 181:2683–2693

    PubMed  Google Scholar 

  • Erlandsson A, Enarsson M, Forsberg-Nilsson K (2001) Immature neurons from CNS stem cells proliferate in response to platelet-derived growth factor. J Neurosci 21:3483–3491

    PubMed  CAS  Google Scholar 

  • Fan G, Martinowich K, Chin MH, He F, Fouse SD, Hutnick L, Hattori D, Ge W, Shen Y, Wu H, ten Hoeve J, Shuai K, Sun YE (2005) DNA methylation controls the timing of astrogliogenesis through regulation of JAK-STAT signaling. Development 132:3345–3356. doi:10.1242/dev.01912

    PubMed  CAS  Google Scholar 

  • Franco SJ, Gil-Sanz C, Martinez-Garay I, Espinosa A, Harkins-Perry SR, Ramos C, Müller U (2012) Fate-restricted neural progenitors in the mammalian cerebral cortex. Science 337:746–749. doi:10.1126/science.1223616

    PubMed  CAS  Google Scholar 

  • Gabay L, Lowell S, Rubin LL, Anderson DJ (2003) Deregulation of dorsoventral patterning by FGF confers trilineage differentiation capacity on CNS stem cells in vitro. Neuron 40:485–499. doi:10.1016/S0896-6273(03)00637-8)

    PubMed  CAS  Google Scholar 

  • Ge W, Martinowich K, Wu X, He F, Miyamoto A, Fan G, Weinmaster G, Sun YE (2002) Notch signaling promotes astrogliogenesis via direct CSL-mediated glial gene activation. J Neurosci Res 69:848–860. doi:10.1002/jnr.10364

    PubMed  CAS  Google Scholar 

  • 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. doi:10.1016/j.brainresrev.2011.01.001

    PubMed  CAS  Google Scholar 

  • 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. doi:10.1002/stem.119

    PubMed  CAS  Google Scholar 

  • Grandbarbe L, Bouissac J, Rand M, Hrabe de Angelis M, Artavanis-Tsakonas S, Mohier E (2003) Delta-Notch signaling controls the generation of neurons/glia from neural stem cells in a stepwise process. Development 130:1391–1402. doi:10.1242/dev.00374

    PubMed  CAS  Google Scholar 

  • Gregg C, Weiss S (2005) CNTF/LIF/gp130 receptor complex signaling maintains a VZ precursor differentiation gradient in the developing ventral forebrain. Development 132:565–578. doi:10.1242/dev.01592

    PubMed  CAS  Google Scholar 

  • Gritti A, Parati EA, Cova L, Frolichsthal P, Galli R, Wanke E, Faravelli L, Morassutti DJ, Roisen F, Nickel DD, Vescovi AL (1996) Multipotential stem-like cells from the adult mouse brain proliferate and self-renew in response to basic fibroblast growth factor. J Neurosci 16:1091–1100

    PubMed  CAS  Google Scholar 

  • 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. doi:10.1016/S0896-6273(00)80193-2

    PubMed  CAS  Google Scholar 

  • Groszer M, Erickson R, Scripture-Adams DD, Lesche R, Trumpp A, Zack JA, Kornblum HI, Liu X, Wu H (2001) Negative regulation of neural stem/progenitor cell proliferation by the Pten tumor suppressor gene in vivo. Science 294:2186–2189. doi:10.1126/science.1065518

    PubMed  CAS  Google Scholar 

  • Groszer M, Erickson R, Scripture-Adams DD, Dougherty JD, Le Belle J, Zack JA, Geschwind DH, Liu X, Kornblum HI, Wu H (2006) PTEN negatively regulates neural stem cell self-renewal by modulating G0-G1 cell cycle entry. Proc Natl Acad Sci U S A 103:111–116. doi:10.1073/pnas.0509939103

    PubMed  CAS  Google Scholar 

  • Guruharsha KG, Kankel MW, Artavanis-Tsakonas S (2012) The Notch signalling system: recent insights into the complexity of a conserved pathway. Nat Rev Genet 13:654–666. doi:10.1038/nrg3272

    PubMed  CAS  Google Scholar 

  • Hartline DK (2011) The evolutionary origins of glia. Glia 59:1215–1236. doi:10.1002/glia.21149

    PubMed  Google Scholar 

  • He F, Weihong G, Martinowich K, Becker-Catania S, Coskun V, Zhu W, Wu H, Castro D, Guillemot F, Fan G, de Vellis J, Sun YE (2005) A positive autoregulatory loop of Jak-STAT signaling controls the onset of astrogliogenesis. Nat Neurosci 8:616–625. doi:10.1038/nn1440

    PubMed  CAS  Google Scholar 

  • Hegedus B, Dasgupta B, Shin JE, Emnett RJ, Hart-Mahon EK, Elghazi L, Bernal-Mizrachi E, Gutmann DH (2007) Neurofibromatosis-1 regulates neuronal and glial cell differentiation from neuroglial progenitors in vivo by both cAMP- and Ras-dependent mechanisms. Cell Stem Cell 1:443–457. doi:10.1016/j.stem.2007.07.008

    PubMed  CAS  Google Scholar 

  • Heinrich PC, Behrmann I, Haan S, Hermanns HM, Müller-Newen G, Schaper F (2003) Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem J 374:1–20. doi:10.1042/BJ20030407

    PubMed  CAS  Google Scholar 

  • Hermanson O, Jepsen K, Rosenfeld MG (2002) N-CoR controls differentiation of neural stem cells into astrocytes. Nature 419:934–939. doi:10.1038/nature01156

    PubMed  CAS  Google Scholar 

  • Hirabayashi Y, Itoh Y, Tabata H, Nakajima K, Akiyama T, Masuyama N, Gotoh Y (2004) The Wnt/beta-catenin pathway directs neuronal differentiation of cortical neural precursor cells. Development 131:2791–2801. doi:10.1242/dev.01165

    PubMed  CAS  Google Scholar 

  • Hirabayashi Y, Suzki N, Tsuboi M, Endo TA, Toyoda T, Shinga J, Koseki H, Vidal M, Gotoh Y (2009) Polycomb limits the neurogenic competence of neural precursor cells to promote astrogenic fate transition. Neuron 63:600–613. doi:10.1016/j.neuron.2009.08.021

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Imura T, Nakano I, Kornblum HI, Sofroniew MV (2006) Phenotypic and functional heterogeneity of GFAP-expressing cells in vitro: differential expression of LeX/CD15 by GFAP-expressing multipotent neural stem cells and non-neurogenic astrocytes. Glia 53:277–293. doi:10.1002/glia.20281

    PubMed  Google Scholar 

  • Israsena N, Hu M, Fu W, Kan L, Kessler JA (2004) The presence of FGF2 signaling determines whether beta-catenin exerts effects on proliferation or neuronal differentiation of neural stem cells. Dev Biol 268:220–231. doi:10.1016/j.ydbio.2003.12.024

    PubMed  CAS  Google Scholar 

  • Iwasaki Y, Hosoya T, Takebayashi H, Ogawa Y, Hotta Y, Ikenaka K (2003) The potential to induce glial differentiation is conserved between Drosophila and mammalian glial cells missing genes. Development 130:6027–6035. doi:10.1242/dev.00822

    PubMed  CAS  Google Scholar 

  • Jacobson M (1991) Developmental neurobiology. Plenum, New York

    Google Scholar 

  • Jones BW (2001) Glial cell development in the Drosophila embryo. Bioessays 23:877–887. doi:10.1002/bies.1129

    PubMed  CAS  Google Scholar 

  • Jung S, Park RH, Kim S, Jeon YJ, Ham DS, Jung MY, Kim SS, Lee YD, Park CH, Suh-Kim H (2010) Id proteins facilitate self-renewal and proliferation of neural stem cells. Stem Cells Dev 19:831–841. doi:10.1089/scd.2009.0093

    PubMed  CAS  Google Scholar 

  • Kageyama R, Ohtsuka T, Kobayashi T (2008) Roles of Hes genes in neural development. Dev Growth Differ 50(Suppl 1):S97–S103. doi:10.1111/j.1440-169X.2008.00993.x

    PubMed  CAS  Google Scholar 

  • Kang P, Lee HK, Glasgow SM, Finley M, Donti T, Gaber ZB, Graham BH, Foster AE, Novitch BG, Gronostajski RM, Deneen B (2012) Sox9 and NFIA coordinate a transcriptional regulatory cascade during the initiation of gliogenesis. Neuron 74:79–94. doi:10.1016/j.neuron.2012.01.024

    PubMed  CAS  Google Scholar 

  • Kawaguchi A, Ikawa T, Kasukawa T, Ueda HR, Kurimoto K, Saitou M, Matsuzaki F (2008) Single-cell gene profiling defines differential progenitor subclasses in mammalian neurogenesis. Development 135:3113–3124. doi:10.1242/dev.022616

    PubMed  CAS  Google Scholar 

  • Kessaris N, Jamen F, Rubin L, Richardson WD (2004) Cooperation between sonic hedgehog and fibroblast growth factor/MAPK signalling pathways in neocortical precursors. Development 131:1289–1298. doi:10.1242/dev.01027

    PubMed  CAS  Google Scholar 

  • Kessaris N, Pringle N, Richardson WD (2008) Specification of CNS glia from neural stem cells in the embryonic neuroepithelium. Philos Trans R Soc Lond B Biol Sci 363:71–85. doi:10.1098/rstb.2006.2013

    PubMed  CAS  Google Scholar 

  • Kim H, Shin J, Kim S, Poling J, Park HC, Appel B (2008) Notch-regulated oligodendrocyte specification from radial glia in the spinal cord of zebrafish embryos. Dev Dyn 237:2081–2089. doi:10.1002/dvdy.21620

    PubMed  Google Scholar 

  • Kishi Y, Fujii Y, Hirabayashi Y, Gotoh Y (2012) HMGA regulates the global chromatin state and neurogenic potential in neocortical precursor cells. Nat Neurosci 15:1127–1133. doi:10.1038/nn.3165

    PubMed  CAS  Google Scholar 

  • Kohyama J, Sanosaka T, Tokunaga A, Takatsuka E, Tsujimura K, Okano H, Nakashima K (2010) BMP-induced REST regulates the establishment and maintenance of astrocytic identity. J Cell Biol 189:159–170. doi:10.1083/jcb.200908048

    PubMed  CAS  Google Scholar 

  • Kondo T, Raff M (2000) Oligodendrocyte precursor cells reprogrammed to become multipotential CNS stem cells. Science 289:1754–1757. doi:10.1126/science.289.5485.1754

    PubMed  CAS  Google Scholar 

  • Kriegstein A, Alvarez-Buylla A (2009) The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 32:149–184. doi:10.1146/annurev.neuro.051508.135600

    PubMed  CAS  Google Scholar 

  • Levitt P, Rakic P (1980) Immunoperoxidase localization of glial fibrillary acidic protein in radial glial cells and astrocytes of the developing rhesus monkey brain. J Comp Neurol 193:815–840

    PubMed  CAS  Google Scholar 

  • Levitt P, Cooper ML, 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 1:27–39

    PubMed  CAS  Google Scholar 

  • Levitt P, Cooper ML, Rakic P (1983) Early divergence and changing proportions of neuronal and glial precursor cells in the primate cerebral ventricular zone. Dev Biol 96:472–484. doi:10.1016/0012-1606(83)90184-7

    PubMed  CAS  Google Scholar 

  • Li W, Cogswell CA, LoTurco JJ (1998) Neuronal differentiation of precursors in the neocortical ventricular zone is triggered by BMP. J Neurosci 18:8562–8853

    Google Scholar 

  • Li X, Newbern JM, Wu Y, Morgan-Smith M, Zhong J, Charron J, Snider WD (2012) MEK is a key regulator of gliogenesis in the developing brain. Neuron 75:1035–1050. doi:10.1016/j.neuron.2012.08.031

    PubMed  CAS  Google Scholar 

  • Liu L, Cundiff P, Abel G, Wang Y, Faigle R, Sakagami H, Xu M, Xia Z (2006) Extracellular signal-regulated kinase (ERK) 5 is necessary and sufficient to specify cortical neuronal fate. Proc Natl Acad Sci U S A 103:9697–9702. doi:10.1073/pnas.0603373103

    PubMed  CAS  Google Scholar 

  • Loeffler M, Potten CS (1997) Stem cells and cellular pedigrees - a conceptual introduction. In: Potten CS (ed) Stem cells. Academic, Cambridge, pp 1–27

    Google Scholar 

  • Louis SA, Rietze RL, Deleyrolle L, Wagey RE, Thomas TE, Eaves AC, Reynolds BA (2008) Enumeration of neural stem and progenitor cells in the neural colony-forming cell assay. Stem Cells 26:988–996. doi:10.1634/stemcells.2007-0867

    PubMed  Google Scholar 

  • Mao H, Lv Z, Ho MS (2012) Gcm proteins function in the developing nervous system. Dev Biol 370:63–70. doi:10.1016/j.ydbio.2012.07.018

    PubMed  CAS  Google Scholar 

  • Mason S, Piper M, Gronostajski RM, Richards LJ (2008) Nuclear factor one transcription factors in CNS development. Mol Neurobiol 39:10–23. doi:10.1007/s12035-008-8048-6

    PubMed  Google Scholar 

  • McCarthy M, Turnbull DH, Walsh CA, Fishell G (2001) Telencephalic neural progenitors appear to be restricted to regional and glial fates before the onset of neurogenesis. J Neurosci 21:6772–6781

    PubMed  CAS  Google Scholar 

  • Mehler MF, Mabie PC, Zhu G, Gokhan S, Kessler JA (2000) Developmental changes in progenitor cell responsiveness to bone morphogenetic proteins differentially modulate progressive CNS lineage fate. Dev Neurosci 22:74–85. doi:10.1159/000017429

    PubMed  CAS  Google Scholar 

  • Mekki-Dauriac S, Agius E, Kan P, Cochard P (2002) Bone morphogenetic proteins negatively control oligodendrocyte precursor specification in the chick spinal cord. Development 129:5117–5130

    PubMed  CAS  Google Scholar 

  • Ménard C, Hein P, Paquin A, Savelson A, Yang XM, Lederfein D, Barnabé-Heider F, Mir AA, Sterneck E, Peterson AC, Johnson PF, Vinson C, Miller FD (2002) An essential role for a MEK-C/EBP pathway during growth factor-regulated cortical neurogenesis. Neuron 36:597–610. doi:10.1016/S0896-6273(02)01026-7

    PubMed  Google Scholar 

  • 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. doi:10.1523/JNEUROSCI.1299-06.2006

    PubMed  CAS  Google Scholar 

  • Miller FD, Gauthier AS (2007) Timing is everything: making neurons versus glia in the developing cortex. Neuron 54:357–369. doi:10.1016/j.neuron.2007.04.019

    PubMed  CAS  Google Scholar 

  • Ming GL, Song H (2011) Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 70:687–702. doi:10.1016/j.neuron.2011.05.001

    PubMed  CAS  Google Scholar 

  • Molne M, Studer L, Tabar V, Ting YT, Eiden MV, McKay RD (2000) Early cortical precursors do not undergo LIF-mediated astrocytic differentiation. J Neurosci Res 59:301–311. doi:10.1002/(SICI)1097-4547(20000201)59:3<301::AID-JNR3>3.0.CO;2-H

    PubMed  CAS  Google Scholar 

  • 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. doi:10.1046/j.1460-9568.2003.02727.x

    PubMed  Google Scholar 

  • Mueller TD, Nickel J (2012) Promiscuity and specificity in BMP receptor activation. FEBS Lett 586:1846–1859. doi:10.1016/j.febslet.2012.02.043

    PubMed  CAS  Google Scholar 

  • Munji RN, Choe Y, Li G, Siegenthaler JA, Pleasure SJ (2011) Wnt signaling regulates neuronal differentiation of cortical intermediate progenitors. J Neurosci 31:1676–1687. doi:10.1523/JNEUROSCI.5404-10.2011

    PubMed  CAS  Google Scholar 

  • Nagao M, Campbell K, Burns K, Kuan CY, Trumpp A, Nakafuku M (2008) Coordinated control of self-renewal and differentiation of neural stem cells by Myc and the p19ARF-p53 pathway. J Cell Biol 183:1243–1257. doi:10.1083/jcb.200807130

    PubMed  CAS  Google Scholar 

  • Naka H, Nakamura S, Shimazaki T, Okano H (2008) Requirement for COUP-TFI and II in the temporal specification of neural stem cells in CNS development. Nat Neurosci 11:1014–1023. doi:10.1038/nn.2168

    PubMed  CAS  Google Scholar 

  • Nakashima K, Yanagisawa M, Arakawa H, Kimura N, Hisatsune T, Kawabata M, Miyazono K, Taga T (1999) Synergistic signaling in fetal brain by STAT3-Smad1 complex bridged by p300. Science 284:479–482. doi:10.1126/science.284.5413.479

    PubMed  CAS  Google Scholar 

  • Namihira M, Kohyama J, Semi K, Sanosaka T, Deneen B, Taga T, Nakashima K (2009) Committed neuronal precursors confer astrocytic potential on residual neural precursor cells. Dev Cell 16:245–255. doi:10.1016/j.devcel.2008.12.014

    PubMed  CAS  Google Scholar 

  • Nishino J, Kim I, Chada K, Morrison SJ (2008) Hmga2 promotes neural stem cell self-renewal in young, but not old, mice by reducing p16Ink4a and p19Arf expression. Cell 135:227–239. doi:10.1016/j.cell.2008.09.017

    PubMed  CAS  Google Scholar 

  • Noctor SC, Martinez-Cerdeno V, Ivic L, Kriegstein AR (2008) Distinct behaviors of neural stem and progenitor cells underlie cortical neurogenesis. J Comp Neurol 508:28–44. doi:10.1002/cne.21669

    PubMed  Google Scholar 

  • O’Leary DD, Nakagawa Y (2002) Patterning centers, regulatory genes and extrinsic mechanisms controlling a realization of the neocortex. Curr Opin Neurobiol 12:14–25. doi:10.1016/S0959-4388(02)00285-4

    PubMed  Google Scholar 

  • Palma V, Ruiz i Altaba A (2004) Hedgehog-GLI signaling regulates the behavior of cells with stem cell properties in the developing neocortex. Development 131:337–345. doi:10.1242/dev.00930

    PubMed  CAS  Google Scholar 

  • Paschaki M, Lin SC, Wong RL, Finnell RH, Dollé P, Niederreither K (2012) Retinoic acid-dependent signaling pathways and lineage events in the developing mouse spinal cord. PLoS One 7:e32447. doi:10.1371/journal.pone.0032447

    PubMed  CAS  Google Scholar 

  • Qian X, Goderie SK, Shen Q, Stern JH, Temple S (1998) Intrinsic programs of patterned cell lineages in isolated vertebrate CNS ventricular zone cells. Development 125:3143–3152

    PubMed  CAS  Google Scholar 

  • Qian X, Shen Q, Goderie SK, He W, Capela A, Davis AA, Temple S (2000) Timing of CNS cell generation: a programmed sequence of neuron and glial cell production from isolated murine cortical stem cells. Neuron 28:69–80. doi:10.1016/S0896-6273(00)00086-6

    PubMed  CAS  Google Scholar 

  • Represa A, Shimazaki T, Simmonds M, Weiss S (2001) EGF-responsive neural stem cells are a transient population in the developing mouse spinal cord. Eur J Neurosci 14:452–462. doi:10.1046/j.0953-816x.2001.01660.x

    PubMed  CAS  Google Scholar 

  • Reynolds BA, Weiss S (1992) Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255:1707–1710. doi:10.1126/science.1553558

    PubMed  CAS  Google Scholar 

  • Reynolds BA, Tetzlaff W, Weiss S (1992) A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J Neurosci 12:4565–4574

    PubMed  CAS  Google Scholar 

  • Riobo NA, Haines GM, Emerson CP Jr (2006) Protein kinase C-delta and mitogen-activated protein/extracellular signal-regulated kinase-1 control GLI activation in hedgehog signaling. Cancer Res 66:839–845. doi:10.1158/0008-5472.CAN-05-2539

    PubMed  CAS  Google Scholar 

  • Samanta J, Kessler JA (2004) Interactions between ID and OLIG proteins mediate the inhibitory effects of BMP4 on oligodendroglial differentiation. Development 131:4131–4142. doi:10.1242/dev.01273

    PubMed  CAS  Google Scholar 

  • Sanosaka T, Namihira M, Asano H, Kohyama J, Aisaki K, Igarashi K, Kanno J, Nakashima K (2008) Identification of genes that restrict astrocyte differentiation of midgestational neural precursor cells. Neuroscience 155:780–788. doi:10.1016/j.neuroscience.2008.06.039

    PubMed  CAS  Google Scholar 

  • Sardi SP, Murtie J, Koirala S, Patten BA, Corfas G (2006) Presenilin-dependent ErbB4 nuclear signaling regulates the timing of astrogenesis in the developing brain. Cell 127:185–197. doi:10.1016/j.cell.2006.07.037

    PubMed  CAS  Google Scholar 

  • Sauer FC (1935) Mitosis in the neural tube. J Comp Neurol 62:377–405

    Google Scholar 

  • Schaper A (1897) The earliest differentiation in the central nervous system of vertebrates. Science 5:430–431

    Google Scholar 

  • Schmid RS, McGrath B, Berechid BE, Boyles B, Marchionni M, Sestan N, Anton ES (2003) Neuregulin 1-erbB2 signaling is required for the establishment of radial glia and their transformation into astrocytes in cerebral cortex. Proc Natl Acad Sci U S A 100:4251–4256. doi:10.1073/pnas.0630496100

    PubMed  CAS  Google Scholar 

  • Schwamborn JC, Berezikov E, Knoblich JA (2009) The TRIM-NHL protein TRIM32 activates microRNAs and prevents self-renewal in mouse neural progenitors. Cell 136:913–925. doi:10.1016/j.cell.2008.12.024

    PubMed  CAS  Google Scholar 

  • Scott CE, Wynn SL, Sesay A, Cruz C, Cheung M, Gomez Gaviro MV, Booth S, Gao B, Cheah KSE, Lovell-Badge R, Briscoe J (2010) SOX9 induces and maintains neural stem cells. Nat Neurosci 13:1181–1189. doi:10.1038/nn.2646

    PubMed  CAS  Google Scholar 

  • Shen Q, Zhong W, Jan YN, Temple S (2002) Asymmetric Numb distribution is critical for asymmetric cell division of mouse cerebral cortical stem cells and neuroblasts. Development 129:4843–4853

    PubMed  CAS  Google Scholar 

  • Shen Q, Wang Y, Dimos JT, Fasano CA, Phoenix TN, Lemischka IR, Ivanova NB, Stifani S, Morrisey EE, Temple S (2006) The timing of cortical neurogenesis is encoded within lineages of individual progenitor cells. Nat Neurosci 9:743–751. doi:10.1038/nn1694

    PubMed  CAS  Google Scholar 

  • Siegenthaler JA, Ashique AM, Zarbalis K, Patterson KP, Hecht JH, Kane MA, Folias AE, Choe Y, May SR, Kume T, Napoli JL, Peterson AS, Pleasure SJ (2009) Retinoic acid from the meninges regulates cortical neuron generation. Cell 139:597–609. doi:10.1016/j.cell.2009.10.004

    PubMed  CAS  Google Scholar 

  • Song MR, Ghosh A (2004) FGF2-induced chromatin remodeling regulates CNTF-mediated gene expression and astrocyte differentiation. Nat Neurosci 7:229–235. doi:10.1038/nn1192

    PubMed  Google Scholar 

  • Soula C, Foulquier F, Duprat AM, Cochard P (1993) Lineage analysis of early neural plate cells: cells with purely neuronal fate coexist with bipotential neuroglial progenitors. Dev Biol 159:196–207. doi:10.1006/dbio.1993.1233

    PubMed  CAS  Google Scholar 

  • Soustelle L, Trousse F, Jacques C, Ceron J, Cochard P, Soula C, Giangrande A (2007) Neurogenic role of Gcm transcription factors is conserved in chicken spinal cord. Development 134:625–634. doi:10.1242/dev.02750

    PubMed  CAS  Google Scholar 

  • Stolt CC, Lommes P, Sock E, Chaboissier MC, Schedl A, Wegner M (2003) The Sox9 transcription factor determines glial fate choice in the developing spinal cord. Genes Dev 17:1677–1689. doi:10.1101/gad.259003

    PubMed  CAS  Google Scholar 

  • Sun Y, Nadal-Vicens M, Misono S, Lin MZ, Zubiaga A, Hua X, Fan G, Greenberg ME (2001) Neurogenin promotes neurogenesis and inhibits glial differentiation by independent mechanisms. Cell 104:365–376. doi:10.1016/S0092-8674(01)00224-0

    PubMed  CAS  Google Scholar 

  • Takahashi T, Nowakowski RS, Caviness VS Jr (1993) Cell cycle parameters and patterns of nuclear movement in the neocortical proliferative zone of the fetal mouse. J Neurosci 13:820–833

    PubMed  CAS  Google Scholar 

  • Takahashi T, Nowakowski RS, Caviness VS Jr (1995) Early ontogeny of the secondary proliferative population of the embryonic murine cerebral wall. J Neurosc 15:6058–6068

    Google Scholar 

  • Takizawa T, Nakashima K, Namihira M, Ochiai W, Uemura A, Yanagisawa M, Fujita N, Nakao M, Taga T (2001) DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain. Dev Cell 1:749–758. doi:10.1016/S1534-5807(01)00101-0

    PubMed  CAS  Google Scholar 

  • Tanigaki K, Nogaki F, Takahashi J, Tashiro K, Kurooka H, Honjo T (2001) Notch1 and Notch3 instructively restrict bFGF responsive multipotent neural progenitor cells to an astroglial fate. Neuron 29:45–55. doi:10.1016/S0896-6273(01)00179-9

    PubMed  CAS  Google Scholar 

  • Temple S (2001) The development of neural stem cells. Nature 414:112–117. doi:10.1038/35102174

    PubMed  CAS  Google Scholar 

  • Tropepe V, Sibilia M, Ciruna BG, Rossant J, Wagner EF, van der Kooy D (1999) Distinct neural stem cells proliferate in response to EGF and FGF in the developing mouse telencephalon. Dev Biol 208:166–188. doi:10.1006/dbio.1998.9192

    PubMed  CAS  Google Scholar 

  • Tsunekawa Y, Britto JM, Takahashi M, Polleux F, Tan SS, Osumi N (2012) Cyclin D2 in the basal process of neural progenitors is linked to non-equivalent cell fates. EMBO J 31:1879–1892. doi:10.1038/emboj.2012.43

    PubMed  CAS  Google Scholar 

  • Vallejo M (2009) PACAP signaling to DREAM: a cAMP-dependent pathway that regulates cortical astrogliogenesis. Mol Neurobiol 39:90–100. doi:10.1007/s12035-009-8055-2

    PubMed  CAS  Google Scholar 

  • Vallstedt A, Klos JM, Ericson J (2005) Multiple dorsoventral origins of oligodendrocyte generation in the spinal cord and hindbrain. Neuron 45:55–67. doi:10.1016/j.neuron.2004.12.026

    PubMed  CAS  Google Scholar 

  • Wang Y, Kim E, Wang X, Novitch BG, Yoshikawa K, Chang LS, Zhu Y (2012) ERK inhibition rescues defects in fate specification of Nf1-deficient neural progenitors and brain abnormalities. Cell 150:816–830. doi:10.1016/j.cell.2012.06.034

    PubMed  CAS  Google Scholar 

  • Wohl CA, Weiss S (1998) Retinoic acid enhances neuronal proliferation and astroglial differentiation in cultures of CNS stem cell-derived precursors. J Neurobiol 37:281–290. doi:10.1002/(SICI)1097-4695(19981105)37:2<281::AID-NEU7>3.0.CO;2-J

    PubMed  CAS  Google Scholar 

  • Wu Y, Liu Y, Levine EM, Rao MS (2003) Hes1 but not Hes5 regulates an astrocyte versus oligodendrocyte fate choice in glial restricted precursors. Dev Dyn 226:675–689. doi:10.1002/dvdy.10278

    PubMed  CAS  Google Scholar 

  • Yoon K, Gaiano N (2005) Notch signaling in the mammalian central nervous system: insights from mouse mutants. Nat Neurosci 8:709–715. doi:10.1038/nn1475

    Google Scholar 

  • Yoshimatsu T, Kawaguchi D, Oishi K, Takeda K, Akira S, Masuyama N, Gotoh Y (2006) Non-cell-autonomous action of STAT3 in maintenance of neural precursor cells in the mouse neocortex. Development 133:2553–2563. doi:10.1242/dev.02419

    PubMed  CAS  Google Scholar 

  • Yung SY, Gokhan S, Jurcsak J, Molero AE, Abrajano JJ, Mehler MF (2002) Differential modulation of BMP signaling promotes the elaboration of cerebral cortical GABAergic neurons or oligodendrocytes from a common sonic hedgehog-responsive ventral forebrain progenitor species. Proc Natl Acad Sci U S A 99:16273–16278. doi:10.1073/pnas.232586699

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Takuya Shimazaki .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer Japan

About this chapter

Cite this chapter

Shimazaki, T. (2013). Regulatory Mechanisms Underlying the Neurogenesis-to-Gliogenesis Switch by Neural Stem Cells. In: Kageyama, R., Yamamori, T. (eds) Cortical Development. Springer, Tokyo. https://doi.org/10.1007/978-4-431-54496-8_4

Download citation

Publish with us

Policies and ethics