Neural stem cell niches in the adult mammalian brain

Home/2015, Vol. 3, No. 2/Neural stem cell niches in the adult mammalian brain

Cell and Organ Transplantology. 2015; 3(2): 190-194.
DOI: 10.22494/COT.V3I2.13

Neural stem cell niches in the adult mammalian brain

Tsupykov O. M.
Bogomoletz Institute of Physiology NAS of Ukraine, Кyiv, Ukraine
State Institute of Genetic and Regenerative Medicine NAMS of Ukraine, Kyiv, Ukraine

Abstract
Stem cells of the central nervous system have received a great deal of attention in neurobiology in the last decade.  It has been shown that neurogenesis occurs in the postnatal period in specialized niches of the adult mammalian brain. The niche is a key regulator of stem cell behavior. Recent data underscore the complexity and heterogeneity of the different components of the niche, and the presence of local signaling microdomain. The review is devoted to recent views on the structural organization of neurogenic niches and regulatory factors involved at different stages of neurogenesis in the postnatal period. Understanding of stem cells behavior in the niches can serve as a basis for determination of these cells function in the adult brain.

Keywords: neural progenitors, neurovascular niche, subventricular zone, subgranular zone

Full Text PDF

1. Aguirre A, Rubio ME, Gallo V. Notch and EGFR pathway interaction regulates neural stem cell number and self-renewal. Nature. 2010; 467(7313):323–327.
https://doi.org/10.1038/nature09347
PMid:20844536 PMCid:PMC2941915
2. Altman J. Are new neurons formed in the brains of adult mammals? Science. 1962; 135(3509):1127–1128.
https://doi.org/10.1126/science.135.3509.1127
PMid:13860748
3. Alvarez-Buylla A, Garcia-Verdugo JM, Tramontin AD. A unified hypothesis on the lineage of neural stem cells. Nat. Rev. Neurosci. 2001; 2:287–293.
https://doi.org/10.1038/35067582
PMid:11283751
4. Anthony TE, Klein C, Fishell G, et al. Radial glia serve as neuronal progenitors in all regions of the central nervous system. Neuron. 2004; 41:881–890.
https://doi.org/10.1016/S0896-6273(04)00140-0
5. Brandt MD, Jessberger S, Steiner B, et al. Transient calretinin expression defines early postmitotic step of neuronal differentiation in adult hippocampal neurogenesis of mice. Mol Cell Neurosci. 2003; 24:603–613.
https://doi.org/10.1016/S1044-7431(03)00207-0
6. Brown J, Cooper-Kuhn CM, Kempermann G, et al. Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur. J. Neurosci. 2003; 17(10):2042–2046.
https://doi.org/10.1046/j.1460-9568.2003.02647.x
PMid:12786970
7. Capilla-Gonzalez V, Lavell E, Qui-ones-Hinojosa A, et al. Regulation of subventricular zone-derived cells migration in the adult brain. Adv. Exp. Med. Biol. 2015; 853:1–21.
https://doi.org/10.1007/978-3-319-16537-0_1
PMid:25895704
8. Costa V, Lugert S, Jagasia R. Role of adult hippocampal neurogenesis in cognition in physiology and disease: pharmacological targets and biomarkers. Handb. Exp. Pharmacol. 2015; 228:99–155.
https://doi.org/10.1007/978-3-319-16522-6_4
PMid:25977081
9. Cunningham LA, Candelario K, Li L. Roles for HIF-1α in neural stem cell function and the regenerative response to stroke. Behav. Brain Res. 2012; 227:410–417.
https://doi.org/10.1016/j.bbr.2011.08.002
PMid:21871501 PMCid:PMC4559269
10. Decimo I, Bifari F, Krampera M, et al. Neural stem cell niches in health and diseases. Curr. Pharm. Des. 2012; 18(13):1755–1783.
https://doi.org/10.2174/138161212799859611
PMid:22394166 PMCid:PMC3343380
11. Decimo I, Bifari F, Rodriguez FJ, et al. Nestin- and doublecortin-positive cells reside in adult spinal cord meninges and participate in injury-induced parenchymal reaction. Stem Cells. 2011;29:2062–2076.
https://doi.org/10.1002/stem.766
PMid:22038821 PMCid:PMC3468739
12. Doetsch F. A niche for adult neural stem cells. Curr. Opin. Genet. Dev. 2003; 13:543–550.
https://doi.org/10.1016/j.gde.2003.08.012
PMid:14550422
13. Doetsch F. The glial identity of neural stem cells. Nat.Neurosci. 2003; 6:1127–1134.
https://doi.org/10.1038/nn1144
PMid:14583753
14. Eriksson PS, Perfilieva E, Björk-Eriksson T, et al. Neurogenesis in the adult human hippocampus. Nat. Med. 1998; 4(11):1313-1317.
https://doi.org/10.1038/3305
PMid:9809557
15. Faissner A, Reinhard J. The extracellular matrix compartment of neural stem and glial progenitor cells. Glia. 2015; 63(8):1330–1349.
https://doi.org/10.1002/glia.22839
PMid:25913849
16. Fuchs E, Tumbar T, Guasch G. Socializing with the neighbors: stem cells and their niche. Cell. 2004; 116:769–778.
https://doi.org/10.1016/S0092-8674(04)00255-7
17. Giachino C, Taylor V. Notching up neural stem cell homogeneity in homeostasis and disease. Front. Neurosci. 2014; 8:32.
https://doi.org/10.3389/fnins.2014.00032
PMid:24611040 PMCid:PMC3933793
18. Gil-Perotín S, Duran-Moreno M, Cebrián-Silla A, et al. Adult neural stem cells from the subventricular zone: a review of the neurosphere assay. Anat. Rec. (Hoboken). 2013; 296(9):1435–1452.
https://doi.org/10.1002/ar.22746
PMid:23904071
19. Goldman SA, Nottebohm F. Neuronal production, migration, and differentiation in vocal control nucleus of the adult female canary brain. Proc. Natl. Acad. Sci. USA. 1983; 80:2390–2394.
https://doi.org/10.1073/pnas.80.8.2390
20. Hirota Y, Sawada M, Huang SH, et al. Roles of Wnt signaling in the neurogenic niche of the adult mouse ventricular-subventricular zone. Neurochem. Res. 2015; Nov 16. [Epub ahead of print].
PMid:26572545
21. Jenny B, Kanemitsu M, Tsupykov O, et al. Fibroblast growth factor-2 overexpression in transplanted neural progenitors promotes perivascular cluster formation with a neurogenic potential. Stem Cells. 2009; 27(6):1309–1317.
https://doi.org/10.1002/stem.46
PMid:19489096
22. Jones KS, Connor B. Intrinsic regulation of adult subventricular zone neural progenitor cells and the effect of brain injury. Am. J. Stem Cells. 2011; 1(1):48–58.
PMid:23671797 PMCid:PMC3643385
23. Kaplan MS, Hinds JW. Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science. 1977; 197:1092–1094.
https://doi.org/10.1126/science.887941
24. Kempermann G, Song H, Gage FH. Neurogenesis in the adult hippocampus. Cold Spring Harb. Perspect. Med. 2015; 5(7):a018812.
https://doi.org/10.1101/cshperspect.a018812
PMid:26330519
25. Laywell ED, Rakic P, Kukekov VG, et al. Identification of a multipotent astrocytic stem cell in the immature and adult mouse brain. Proc. Natl Acad. Sci. USA. 2000; 97:13883–13888.
https://doi.org/10.1073/pnas.250471697
PMid:11095732 PMCid:PMC17670
26. Lee SW, Clemenson GD, Gage FH. New neurons in an aged brai. Behav. Brain Res. 2012; 227:497–507.
https://doi.org/10.1016/j.bbr.2011.10.009
PMid:22024433 PMCid:PMC3264739
27. Licht T, Keshet E. The vascular niche in adult neurogenesis. Mech. Dev. 2015; 138P1:56–62.
28. Lim DA, Alvarez-Buylla A. Adult neural stem cells stake their ground. Trends Neurosci. 2014; 37(10):563–571.
https://doi.org/10.1016/j.tins.2014.08.006
PMid:25223700 PMCid:PMC4203324
29. Lim DA, Tramontin AD, Trevejo JM, et al. Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron. 2000; 28(3):713–726.
https://doi.org/10.1016/S0896-6273(00)00148-3
30. Lin R, Iacovitti L. Classic and novel stem cell niches in brain homeostasis and repair. Brain Res. 2015: S0006-8993(15)00325-X.
31. Lin R, Cai J, Nathan C, et al. Neurogenesis is enhanced by stroke in multiple new stem cell niches along the ventricular system at sites of high BBB permeability. Neurobiol. Dis. 2015; 74:229–239.
https://doi.org/10.1016/j.nbd.2014.11.016
PMid:25484283
32. Mariano ED, Teixeira MJ, Marie SK, et al. Adult stem cells in neural repair: Current options, limitations and perspectives. World J. Stem Cells. 2015; 7(2):477–482.
https://doi.org/10.4252/wjsc.v7.i2.477
PMid:25815131 PMCid:PMC4369503
33. Massirer KB, Carromeu C, Griesi-Oliveira K, et al. Maintenance and differentiation of neural stem cells. Wiley Interdiscip Rev. Syst. Biol. Med. 2011; 3(1):107–114.
https://doi.org/10.1002/wsbm.100
PMid:21061307
34. Mercier F, Kitasako JT, Hatton GI. Anatomy of the brain neurogenic zones revisited: fractones and the fibroblast/macrophage network. J. Comp. Neurol. 2002; 451:170–188.
https://doi.org/10.1002/cne.10342
PMid:12209835
35. Merkle FT, Tramontin AD, Garcia-Verdugo JM, et al. Radial glia give rise to adult neural stem cells in the subventricular zone. Proc. Natl. Acad. Sci. USA. 2004; 101:17528–17532.
https://doi.org/10.1073/pnas.0407893101
PMid:15574494 PMCid:PMC536036
36. Montalbán-Loro R, Domingo-Muelas A, Bizy A, et al. Epigenetic regulation of stemness maintenance in the neurogenic niches. World J. Stem Cells. 2015; 7(4):700–710.
https://doi.org/10.4252/wjsc.v7.i4.700
PMid:26029342 PMCid:PMC4444611
37. Nait-Oumesmar B, Decker L, Lachapelle F, et al. Progenitor cells of the adult mouse subventricular zone proliferate, migrate and differentiate into oligodendrocytes after demyelination. Eur. J. Neurosci. 1999; 11:4357–4366.
https://doi.org/10.1046/j.1460-9568.1999.00873.x
PMid:10594662
38. Nam H, Lee KH, Nam DH, et al. Adult human neural stem cell therapeutics: Current developmental status and prospect. World J. Stem Cells. 2015; 7(1):126–136.
https://doi.org/10.4252/wjsc.v7.i1.126
PMid:25621112 PMCid:PMC4300923
39. Ottone C, Krusche B, Whitby A, et al. Direct cell-cell contact with the vascular niche maintains quiescent neural stem cells. Nature Cell Biol. 2014; 16:1045–1056.
https://doi.org/10.1038/ncb3045
PMid:25283993 PMCid:PMC4298702
40. Park K, Nam Y, Choi Y. An agarose gel-based neurosphere culture system leads to enrichment of neuronal lineage cells in vitro. In Vitro Cell Dev. Biol. Anim. 2015; 51(5):455–462.
https://doi.org/10.1007/s11626-014-9855-x
PMid:25539864
41. Platel JC, Bordey A. The multifaceted subventricular zone astrocyte: From a metabolic and pro-neurogenic role to acting as a neural stem cell. Neuroscience. 2015. pii: S0306-4522(15)00981-1.
42. Plumpe T, Ehninger D, Steiner B, et al. Variability of doublecortin-associated dendrite maturation in adult hippocampal neurogenesis is independent of the regulation of precursor cell proliferation. BMC Neurosci. 2006; 7:77.
https://doi.org/10.1186/1471-2202-7-77
PMid:17105671 PMCid:PMC1657022
43. Putnam AJ. The instructive role of the vasculature in stem cell niches. Biomat. Sci. 2014; 2:1562–1573.
https://doi.org/10.1039/C4BM00200H
PMid:25530848 PMCid:PMC4267578
44. Rakic P. Limits of neurogenesis in primates. Science. 1985; 227(4690):1054-1056.
https://doi.org/10.1126/science.3975601
PMid:3975601
45. Ramasamy S, Narayanan G, Sankaran S, et al. Neural stem cell survival factors. Arch. Biochem. Biophys. 2013; 534(1-2):71–87.
https://doi.org/10.1016/j.abb.2013.02.004
PMid:23470250
46. Reya T, Morrison SJ, Clarke MF, et al. Stem cells, cancer, and cancer stem cells. Nature. 2001; 414:105–111.
https://doi.org/10.1038/35102167
PMid:11689955
47. Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science. 1992; 255:1707–1710.
https://doi.org/10.1126/science.1553558
48. Robins SC, Stewart I, McNay DE, et al. α-Tanycytes of the adult hypothalamic third ventricle include distinct populations of FGF-responsive neural progenitors. Nat. Commun. 2013; 4:2049.
https://doi.org/10.1038/ncomms3049
PMid:23804023
49. Rueger MA, Schroeter M. In vivo imaging of endogenous neural stem cells in the adult brain. World J. Stem Cells. 2015; 7(1):75–83.
https://doi.org/10.4252/wjsc.v7.i1.75
PMid:25621107 PMCid:PMC4300938
50. Sanin V, Heeß C, Kretzschmar HA, Schuller U. Recruitment of neural precursor cells from circumventricular organs of patients with cerebral ischaemia. Neuropathol. Appl. Neurobiol. 2013; 39:510–518.
https://doi.org/10.1111/j.1365-2990.2012.01301.x
PMid:22985410
51. Scadden D.T. The stem-cell niche as an entity of action. Nature. 2006; 441(7097):1075–1079.
https://doi.org/10.1038/nature04957
PMid:16810242
52. Seaberg RM, van der Kooy DJ. Adult rodent neurogenic regions: the ventricular subependyma contains neural stem cells, but the dentate gyrus contains restricted progenitors. Neurosci. 2002; 22(5):1784–1793.
53. Steiner B, Kronenberg G, Jessberger S, et al. Differential regulation of gliogenesis in the context of adult hippocampal neurogenesis in mice. Glia. 2004; 46:41–52.
https://doi.org/10.1002/glia.10337
PMid:14999812
54. Sun YJ, Jin K, Childs JT, et al. Vascular endothelial growth factor-B (VEGFB) stimulates neurogenesis: Evidence from knockout mice and growth factor administration. Developmental Biology. 2006; 289(2):329–335.
https://doi.org/10.1016/j.ydbio.2005.10.016
PMid:16337622
55. Sütterlin P, Williams EJ, Chambers D, et al. The molecular basis of the cooperation between EGF, FGF and eCB receptors in the regulation of neural stem cell function. Mol. Cell. Neurosci. 2013; 52:20–30.
https://doi.org/10.1016/j.mcn.2012.10.006
PMid:23085403
56. Tao Y, Ma L, Liao Z, et al. Astroglial β-arrestin1-mediated nuclear signaling regulates the expansion of neural precursor cells in adult hippocampus. Sci. Rep. 2015; 5:15506.
https://doi.org/10.1038/srep15506
PMid:26500013 PMCid:PMC4620451
57. Tavazoie M, Van der Veken L, Silva-Vargas V, et al. A specialized vascular niche for adult neural stem cells. Cell Stem Cell. 2008; 3(3):279–288.
https://doi.org/10.1016/j.stem.2008.07.025
PMid:18786415
58. Tramontin AD, García-Verdugo JM, Lim DA, et al. Postnatal development of radial glia and the ventricular zone (VZ): a continuum of the neural stem cell compartment. Cereb. Cortex. 2003; 13(6):580–587.
https://doi.org/10.1093/cercor/13.6.580
59. Urbán N, Guillemot F. Neurogenesis in the embryonic and adult brain: same regulators, different roles. Front. Cell. Neurosci. 2014; 8:396.
https://doi.org/10.3389/fncel.2014.00396
PMid:25505873 PMCid:PMC4245909
60. Whitman MC, Greer CA. Adult neurogenesis and the olfactory system. Prog. Neurobiol. 2009; 89(2):162–175.
https://doi.org/10.1016/j.pneurobio.2009.07.003
PMid:19615423 PMCid:PMC2748178

Tsupykov OM. Neural stem cell niches in the adult mammalian brain. Cell and Organ Transplantology. 2015; 3(2):190-194. doi: 10.22494/COT.V3I2.13

 

Creative Commons License
Is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.