Skip to main content

Advertisement

Log in

Neural stem cells and neuro/gliogenesis in the central nervous system: understanding the structural and functional plasticity of the developing, mature, and diseased brain

  • Review
  • Published:
The Journal of Physiological Sciences Aims and scope

Abstract

Neurons and glia in the central nervous system (CNS) originate from neural stem cells (NSCs). Knowledge of the mechanisms of neuro/gliogenesis from NSCs is fundamental to our understanding of how complex brain architecture and function develop. NSCs are present not only in the developing brain but also in the mature brain in adults. Adult neurogenesis likely provides remarkable plasticity to the mature brain. In addition, recent progress in basic research in mental disorders suggests an etiological link with impaired neuro/gliogenesis in particular brain regions. Here, we review the recent progress and discuss future directions in stem cell and neuro/gliogenesis biology by introducing several topics presented at a joint meeting of the Japanese Association of Anatomists and the Physiological Society of Japan in 2015. Collectively, these topics indicated that neuro/gliogenesis from NSCs is a common event occurring in many brain regions at various ages in animals. Given that significant structural and functional changes in cells and neural networks are accompanied by neuro/gliogenesis from NSCs and the integration of newly generated cells into the network, stem cell and neuro/gliogenesis biology provides a good platform from which to develop an integrated understanding of the structural and functional plasticity that underlies the development of the CNS, its remodeling in adulthood, and the recovery from diseases that affect it.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Taverna E, Götz M, Huttner WB (2014) The cell biology of neurogenesis: toward an understanding of the development and evolution of the neocortex. Annu Rev Cell Dev Biol 30:465–502

    Article  CAS  PubMed  Google Scholar 

  2. Altman J (2011) The discovery of adult mammalian neurogenesis. In: Seki T (ed) Neurogenesis in the adult brain, vol 1. Springer, Tokyo, pp 3–46

    Chapter  Google Scholar 

  3. Lepousez G, Nissant A, Lledo PM (2015) Adult neurogenesis and the future of the rejuvenating brain circuits. Neuron 86:387–401

    Article  CAS  PubMed  Google Scholar 

  4. Sandoe J, Eggan K (2013) Opportunities and challenges of pluripotent stem cell neurodegenerative disease models. Nat Neurosci 16:780–789

    Article  CAS  PubMed  Google Scholar 

  5. Kheirbek MA, Klemenhagen KC, Sahay A, Hen R (2012) Neurogenesis and generalization: a new approach to stratify and treat anxiety disorders. Nat Neurosci 15:1613–1620

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Kriegstein A, Alvarez-Buylla A (2009) The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 32:149–184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Fishell G, Kriegstein AR (2003) Neurons from radial glia: the consequences of asymmetric inheritance. Curr Opin Neurobiol 13:34–41

    Article  CAS  PubMed  Google Scholar 

  8. Imayoshi I, Kageyama R (2014) bHLH factors in self-renewal, multipotency, and fate choice of neural progenitor cells. Neuron 82:9–23

    Article  CAS  PubMed  Google Scholar 

  9. Imayoshi I, Kageyama R (2014) Oscillatory control of bHLH factors in neural progenitors. Trends Neurosci 37:531–538

    Article  CAS  PubMed  Google Scholar 

  10. Bertrand N, Castro DS, Guillemot F (2002) Proneural genes and the specification of neural cell types. Nat Rev Neurosci 3:517–530

    Article  CAS  PubMed  Google Scholar 

  11. Meijer DH, Kane MF, Mehta S, Liu H, Harrington E, Taylor CM, Rowitch DH (2012) Separated at birth? The functional and molecular divergence of OLIG1 and OLIG2. Nat Rev Neurosci 13:819–831

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Ross SE, Greenberg ME, Stiles CD (2003) Basic helix-loop-helix factors in cortical development. Neuron 39:13–25

    Article  CAS  PubMed  Google Scholar 

  13. Wilkinson G, Dennis D, Schuurmans C (2013) Proneural genes in neocortical development. Neuroscience 253:256–273

    Article  CAS  PubMed  Google Scholar 

  14. Shimojo H, Ohtsuka T, Kageyama R (2008) Oscillations in notch signaling regulate maintenance of neural progenitors. Neuron 58:52–64

    Article  CAS  PubMed  Google Scholar 

  15. Imayoshi I, Isomura A, Harima Y, Kawaguchi K, Kori H, Miyachi H, Kageyama R (2013) Oscillatory control of factors determining multipotency and fate in mouse neural progenitors. Science 342:1203–1208

    Article  CAS  PubMed  Google Scholar 

  16. Li G, Pleasure SJ (2014) The development of hippocampal cellular assemblies. Wiley Interdiscip Rev Dev Biol 3:165–177

    Article  CAS  PubMed  Google Scholar 

  17. Urban N, Guillemot F (2014) Neurogenesis in the embryonic and adult brain: same regulators, different roles. Front Cell Neurosci 8:396

    Article  PubMed  PubMed Central  Google Scholar 

  18. Seki T (2011) From embryonic to adult neurogenesis in the dentate gyrus. In: Seki T et al (eds) Neurogenesis in the adult brain, vol 1. Springer, Tokyo, pp 193–216

    Chapter  Google Scholar 

  19. Seki T, Sato T, Toda K, Osumi N, Imura T, Shioda S (2014) Distinctive population of Gfap-expressing neural progenitors arising around the dentate notch migrate and form the granule cell layer in the developing hippocampus. J Comp Neurol 522:261–283

    Article  CAS  PubMed  Google Scholar 

  20. Li G, Kataoka H, Coughlin SR, Pleasure SJ (2009) Identification of a transient subpial neurogenic zone in the developing dentate gyrus and its regulation by Cxcl12 and reelin signaling. Development 136:327–335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Rickmann M, Amaral DG, Cowan WM (1987) Organization of radial glial cells during the development of the rat dentate gyrus. J Comp Neurol 264:449–479

    Article  CAS  PubMed  Google Scholar 

  22. Altman J, Bayer SA (1990) Mosaic organization of the hippocampal neuroepithelium and the multiple germinal sources of dentate granule cells. J Comp Neurol 301:325–342

    Article  CAS  PubMed  Google Scholar 

  23. Sievers J, Hartmann D, Pehlemann FW, Berry M (1992) Development of astroglial cells in the proliferative matrices, the granule cell layer, and the hippocampal fissure of the hamster dentate gyrus. J Comp Neurol 320:1–32

    Article  CAS  PubMed  Google Scholar 

  24. Yuasa S (2001) Development of astrocytes in the mouse hippocampus as tracked by tenascin-C gene expression. Arch Histol Cytol 64:149–158

    Article  CAS  PubMed  Google Scholar 

  25. Kaslin J, Ganz J, Brand M (2008) Proliferation, neurogenesis and regeneration in the non-mammalian vertebrate brain. Philos Trans R Soc B 363:101–122

    Article  Google Scholar 

  26. Bayer SA, Altman J (1991) Neocortical development. Raven Press, Johannesburg

    Google Scholar 

  27. Doetsch F, Caillé I, Lim DA, García-Verdugo JM, Alvarez-Buylla A (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97:703–716

    Article  CAS  PubMed  Google Scholar 

  28. Rakic P (2004) Neuroscience: immigration denied. Nature 427:685–686

    Article  CAS  PubMed  Google Scholar 

  29. Magavi SS, Leavitt BR, Macklis JD (2000) Induction of neurogenesis in the neocortex of adult mice. Nature 405:951–955

    Article  CAS  PubMed  Google Scholar 

  30. Costa MR, Kessaris N, Richardson WD, Gotz M, Hedin-Pereira C (2007) The marginal zone/layer I as a novel niche for neurogenesis and gliogenesis in developing cerebral cortex. J Neurosci 27:11376–11388

    Article  CAS  PubMed  Google Scholar 

  31. Ohira K, Furuta T, Hioki H, Nakamura KC, Kuramoto E, Tanaka Y, Funatsu N, Shimizu K, Oishi T, Hayashi M, Miyakawa T, Kaneko T, Nakamura S (2010) Ischemia-induced neurogenesis of neocortical layer 1 progenitor cells. Nat Neurosci 13:173–179

    Article  CAS  PubMed  Google Scholar 

  32. Nakagomi T, Molnar Z, Taguchi A, Nakano-Doi A, Lu S, Kasahara Y, Nakagomi N, Matsuyama T (2012) Leptomeningeal-derived doublecortin-expressing cells in poststroke brain. Stem Cells Dev 21:2350–2354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Ninomiya S, Esumi S, Ohta K, Fukuda T, Ito T, Imayoshi I, Kageyama R, Ikeda T, Itohara S, Tamamaki N (2013) Amygdala kindling induces nestin expression in the leptomeninges of the neocortex. Neurosci Res 75:121–129

    Article  CAS  PubMed  Google Scholar 

  34. Imayoshi I, Sakamoto M, Ohtsuka T, Takao K, Miyakawa T, Yamaguchi M, Mori K, Ikeda T, Itohara S, Kageyama R (2008) Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat Neurosci 11:1153–1161

    Article  CAS  PubMed  Google Scholar 

  35. Yamaguchi M, Mori K (2005) Critical period for sensory experience-dependent survival of newly generated granule cells in the adult mouse olfactory bulb. Proc Natl Acad Sci USA 102:9697–9702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Diekelmann S, Born J (2010) The memory function of sleep. Nat Rev Neurosci 11:114–126

    Article  CAS  PubMed  Google Scholar 

  37. Yokoyama TK, Mochimaru D, Murata K, Manabe H, Kobayakawa K, Kobayakawa R, Sakano H, Mori K, Yamaguchi M (2011) Elimination of adult-born neurons in the olfactory bulb is promoted during the postprandial period. Neuron 71:883–897

    Article  CAS  PubMed  Google Scholar 

  38. Manabe H, Kusumoto-Yoshida I, Ota M, Mori K (2011) Olfactory cortex generates synchronized top-down inputs to the olfactory bulb during slow-wave sleep. J Neurosci 31:8123–8133

    Article  CAS  PubMed  Google Scholar 

  39. Komano-Inoue S, Manabe H, Ota M, Kusumoto-Yoshida I, Yokoyama TK, Mori K, Yamaguchi M (2014) Top-down inputs from the olfactory cortex in the postprandial period promote elimination of granule cells in the olfactory bulb. Eur J Neurosci 40:2724–2733

    Article  PubMed  Google Scholar 

  40. Komano-Inoue S, Murata K, Mori K, Yamaguchi M (2015) Rapid induction of granule cell elimination in the olfactory bulb by noxious stimulation in mice. Neurosci Lett 598:6–11

    Article  CAS  PubMed  Google Scholar 

  41. Yamaguchi M, Manabe H, Murata K, Mori K (2013) Reorganization of neuronal circuits of the central olfactory system during postprandial sleep. Front Neural Circuits 7:132

    Article  PubMed  PubMed Central  Google Scholar 

  42. Drevets WC, Bogers W, Raichle ME (2002) Functional anatomical correlates of antidepressant drug treatment assessed using PET measures of regional glucose metabolism. Eur Neuropsychopharmacol 12:527–544

    Article  CAS  PubMed  Google Scholar 

  43. Frodl T, Meisenzahl EM, Zetzsche T, Born C, Groll C, Jager M, Leinsinger G, Bottlender R, Hahn K, Moller HJ (2002) Hippocampal changes in patients with a first episode of major depression. Am J Psychiatry 159:1112–1118

    Article  PubMed  Google Scholar 

  44. Chang CC, Yu SC, McQuoid DR, Messer DF, Taylor WD, Singh K, Boyd BD, Krishnan RR, MacFall JR, Steffens DC, Payne ME (2011) Reduction of dorsolateral prefrontal cortex gray matter in late-life depression. Psychiatry Res 193:1–6

    Article  PubMed  PubMed Central  Google Scholar 

  45. Cotter D, Mackay D, Chana G, Beasley C, Landau S, Everall IP (2002) Reduced neuronal size and glial cell density in area 9 of the dorsolateral prefrontal cortex in subjects with major depressive disorder. Cereb Cortex 12:386–394

    Article  PubMed  Google Scholar 

  46. Uranova NA, Vostrikov VM, Orlovskaya DD, Rachmanova VI (2004) Oligodendroglial density in the prefrontal cortex in schizophrenia and mood disorders: a study from the Stanley Neuropathology Consortium. Schizophr Res 67:269–275

    Article  PubMed  Google Scholar 

  47. Vostricov V, Uranova N (2011) Age-related increase in the number of oligodendrocytes is dysregulated in schizophrenita and mood disorders. Schizophr Res Treat 2011:174689

    Google Scholar 

  48. Hayashi Y, Kikuchi NN, Hisanaga SI, Tatebayashi Y (2011) A novel, rapid, cell-counting method for unfixed frozen brains comprehensively quantifies at least four neural cell populations. Mol Psychiatry 16:1155

    Article  CAS  PubMed  Google Scholar 

  49. Hayashi Y, Kikuchi NN, Yu X, Ishimoto K, Hisanaga SI, Tatebayashi Y (2011) A novel, rapid, quantitative cell-counting method reveals oligodendroglial reduction in the frontopolar cortex in major depressive disorder. Mol Psychiatry 16:1156–1158

    Article  Google Scholar 

  50. Malberg J, Eisch AJ, Nestler EJ, Duman RS (2000) Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci 20:9104–9110

    CAS  PubMed  Google Scholar 

  51. Hitoshi S, Maruta N, Higashi M, Kumer A, Kato N, Ikenaka K (2007) Antidepressant drugs reverse the loss of adult neural stem cells following chronic stress. J Neurosci Res 85:3574–3585

    Article  CAS  PubMed  Google Scholar 

  52. Kornack DR, Rakic P (1999) Continuation of neurogenesis in the hippocampus of adult macaque monkey. Proc Natl Acad Sci USA 96:5768–5773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Rivers LE, Young KM, Rizzi M, Jamen F, Psachoulia K, Wade A, Kessaris N, Richardson W (2008) PDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice. Nat Neurosci 11:1392–1401

    Article  CAS  PubMed  Google Scholar 

  55. Livine JM, Raynolds R, Fawcett JW (2001) The oligodendrocyte precursor cell in health and disease. Trends Neurosci 24:39–47

    Article  Google Scholar 

  56. Kikuchi NN, Hayashi Y, Yu XJ, Tatebayashi Y (2013) Depression and alzheimer’s disease: novel postmortem barin studies reveal a possible common mechanism. J Alzheimers Dis 37:611–621

    Google Scholar 

  57. Elsayed M, Banasr M, Duric V, Fournier NM, Licznerski P, Duman R (2012) Antidepressant effects of fibroblast growth factor-2 in behavioral and cellular models of depression. Biol Psychiatry 72:258–265

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Chetty S, Friedman AR, Lahn KT, Kirby ED, Mirescu C, Guo F, Krupik D, Nicholas A, Geraghty AC, Krishnamurthy A, Tsai MK, Covarrubias D, Wong AT, Francis DD, Sapolskey RM, Palmer TD, Pleasure D, Kaufe D (2014) Stress and glucocorticoids promote oligodendrogenesis in the adult hippocampus. Mol Psychiatry 19:1275–1283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Masahiro Yamaguchi or Tatsunori Seki.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yamaguchi, M., Seki, T., Imayoshi, I. et al. Neural stem cells and neuro/gliogenesis in the central nervous system: understanding the structural and functional plasticity of the developing, mature, and diseased brain. J Physiol Sci 66, 197–206 (2016). https://doi.org/10.1007/s12576-015-0421-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12576-015-0421-4

Keywords

Navigation