A niche for adult neural stem cells

Current Opinion in Genetics and Development

Volumn 13, Issue 5, 2003, Pages 543-550

  Doetsch, Fiona ^a  

^a HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN; CELL DIFFERENTIATION; CELL INTERACTION; CELL RENEWAL; CHROMATIN; EXTRACELLULAR MATRIX; GENE CONTROL; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SOMATIC CELL; STEM CELL;

MAMMALIA;

EID: 0141785164     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.gde.2003.08.012     Document Type: Review

References (59)

1. Temple S. The development of neural stem cells. Nature. 414:2001;112-117.
2. Doetsch F., Scharff C. Challenges for brain repair: insights from adult neurogenesis in birds and mammals. Brain Behav Evol. 58:2001;306-322.
3. Spradling A., Drummond-Barbosa D., Kai T. Stem cells find their niche. Nature. 414:2001;98-104.
4. Nait-Oumesmar B., Decker L., Lachapelle F., Avellana-Adalid V., Bachelin C., Van Evercooren A.B. Progenitor cells of the adult mouse subventricular zone proliferate, migrate and differentiate into oligodendrocytes after demyelination. Eur J Neurosci. 11:1999;4357-4366.
5. Doetsch F., Garcia-Verdugo J.M., Alvarez-Buylla A. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci. 17:1997;5046-5061.
6. Doetsch F., Garcia-Verdugo J.M., Alvarez-Buylla A. Regeneration of a germinal layer in the adult mammalian brain. Proc Natl Acad Sci USA. 96:1999;11619-11624.
7. Mercier F., Kitasako J.T., Hatton G.I. Anatomy of the brain neurogenic zones revisited: fractones and the fibroblast/macrophage network. J Comp Neurol. 451:2002;170-188 Basal lamina are important components of stem cell niches. This paper describes the presence of a specialized basal lamina in the SVZ based on immunostaining for laminin at the light microscope and on ultrastructural analysis. The basal lamina contacts all SVZ cell types and may play an important role in cell tethering and ligand binding and regulation.
8. Doetsch F., Caille I., Lim D.A., García-Verdugo J.M., Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell. 97:1999;703-716.
9. Palmer T.D., Willhoite A.R., Gage F.H. Vascular niche for adult hippocampal neurogenesis. J Comp Neurol. 425:2000;479-494.
10. Seri B., Garcia-Verdugo J.M., McEwen B.S., Alvarez-Buylla A. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci. 21:2001;7153-7160.
11. Lim D.A., Alvarez-Buylla A. Interaction between astrocytes and adult subventricular zone precursors stimulates neurogenesis. Proc Natl Acad Sci USA. 96:1999;7526-7531.
12. Song H., Stevens C.F., Gage F.H. Astroglia induce neurogenesis from adult neural stem cells. Nature. 417:2002;39-44.
13. Capela A., Temple S. LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as non-ependymal. Neuron. 35:2002;865-875 This paper shows that the cell-surface carbohydrate LeX/SSEA-1, expressed by pluripotent stem cells, is also expressed in adult germinal regions. LeX is likely an important player in the stem cell niche, regulating the accessibility and influence of ligands. It is the first cell-surface marker identified that encompasses all neurosphere-forming cells in the adult SVZ. The authors also show that ependymal cells are LeX negative and purified ependymal cells do not make neurospheres.
14. Laywell E.D., Rakic P., Kukekov V.G., Holland E.C., Steindler D.A. Identification of a multipotent astrocytic stem cell in the immature and adult mouse brain. Proc Natl Acad Sci USA. 97:2000;13883-13888.
15. Chiasson B.J., Tropepe V., Morshead C.M., van der Kooy D. Adult mammalian forebrain ependymal and subependymal cells demonstrate proliferative potential, but only subependymal cells have neural stem cell characteristics. J Neurosci. 19:1999;4462-4471.
16. Doetsch F., Petreanu L., Caille I., Garcia-Verdugo J.M., Alvarez-Buylla A. EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron. 36:2002;1021-1034 In this paper, we used a combination of approaches to show that the transit-amplifying C cells are the majority of EGF responsive cells both in vivo and in vitro. C cells express the EGF-R and selective killing of C cells in mice expressing herpes simplex virus thymidine kinase under the Dlx2 promoter results in a dramatic reduction in the in vivo proliferative response to EGF and loss of ∼70% of neurospheres in vitro. FACS (fluorescence activated cell sorting) purified C cells are self-renewing and multipotent, revealing that stem cell potential is not only restricted to the primary stem cells.
17. Johansson C.B., Momma S., Clarke D.L., Risling M., Lendahl U., Frisen J. Identification of a neural stem cell in the adult mammalian central nervous system. Cell. 96:1999;25-34.
18. Lim D.A., Tramontin A.D., Trevejo J.M., Herrera D.G., Garcia-Verdugo J.M., Alvarez-Buylla A. Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron. 28:2000;713-726.
19. Stumm R.K., Rummel J., Junker V., Culmsee C., Pfeiffer M., Krieglstein J., Hollt V., Schulz S. A dual role for the SDF-1/CXCR4 chemokine receptor system in adult brain: isoform-selective regulation of SDF-1 expression modulates CXCR4-dependent neuronal plasticity and cerebral leukocyte recruitment after focal ischemia. J Neurosci. 22:2002;5865-5878.
20. Lu M., Grove E.A., Miller R.J. Abnormal development of the hippocampal dentate gyrus in mice lacking the CXCR4 chemokine receptor. Proc Natl Acad Sci USA. 99:2002;7090-7095.
21. Klein R.S., Rubin J.B., Gibson H.D., DeHaan E.N., Alvarez-Hernandez X., Segal R.A., Luster A.D. SDF-1 alpha induces chemotaxis and enhances Sonic hedgehog-induced proliferation of cerebellar granule cells. Development. 128:2001;1971-1981.
22. Lu Q., Sun E.E., Klein R.S., Flanagan J.G. Ephrin-B reverse signaling is mediated by a novel PDZ-RGS protein and selectively inhibits G protein-coupled chemoattraction. Cell. 105:2001;69-79.
23. Conover J.C., Doetsch F., Garcia-Verdugo J.M., Gale N.W., Yancopoulos G.D., Alvarez-Buylla A. Disruption of Eph/ephrin signaling affects migration and proliferation in the adult subventricular zone. Nat Neurosci. 3:2000;1091-1097.
24. Lai K., Kaspar B.K., Gage F.H., Schaffer D.V. Sonic hedgehog regulates adult neural progenitor proliferation in vitro and in vivo. Nat Neurosci. 6:2003;21-27.
25. Perez-Moreno M., Jamora C., Fuchs E. Sticky business: orchestrating cellular signals at adherens junctions. Cell. 112:2003;535-548.
26. Reya T., Duncan A.W., Ailles L., Domen J., Scherer D.C., Willert K., Hintz L., Nusse R., Weissman I.L. A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature. 423:2003;409-414.
27. Lobo M.V., Alonso F.J., Redondo C., Lopez-Toledano M.A., Caso E., Herranz A.S., Paino C.L., Reimers D., Bazan E. Cellular characterization of epidermal growth factor-expanded free-floating neurospheres. J Histochem Cytochem. 51:2003;89-103.
28. Chenn A., Walsh C.A. Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science. 297:2002;365-369 Overexpression of constitutively active β-catenin in neuroepithelial precursors results in the expansion of the precursor pool due to increased cell cycle re-entry, perhaps as a result of switching to symmetric division, and is accompanied by the appearance of sulci and gyri-like folds in the brain.
29. Lambert J.D., Nagy L.M. Asymmetric inheritance of centrosomally localized mRNAs during embryonic cleavages. Nature. 420:2002;682-686.
30. Morshead C.M., Reynolds B.A., Craig C.G., McBurney M.W., Staines W.A., Morassutti D., Weiss S., Van der Kooy D. Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron. 13:1994;1071-1082.
31. Jin K., Zhu Y., Sun Y., Mao X.O., Xie L., Greenberg D.A. Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc Natl Acad Sci USA. 99:2002;11946-11950.
32. Shingo T., Gregg C., Enwere E., Fujikawa H., Hassam R., Geary C., Cross J.C., Weiss S. Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin. Science. 299:2003;117-120.
33. Peterson D.A. Stem cells in brain plasticity and repair. Curr Opin Pharmacol. 2:2002;34-42.
34. Doetsch F., Garcia-Verdugo J.M., Caille I., Alvarez-Buylla A., Chao M.V., Casaccia-Bonnefil P. Lack of the cell cycle inhibitor p27Kip1 results in selective increase of transit amplifying cells for adult neurogenesis. J Neurosci. 22:2002;2246-2254.
35. Coskun V., Luskin M.B. The expression pattern of the cell cycle inhibitor p19(Ink4d) by progenitor cells of the rat embryonic telencephalon and neonatal anterior subventricular zone. J Neurosci. 21:2001;3092-3103.
36. Chojnacki A., Shimazaki T., Gregg C., Weinmaster G., Weiss S. Glycoprotein 130 signaling regulates Notch1 expression and activation in the self-renewal of mammalian forebrain neural stem cells. J Neurosci. 23:2003;1730-1741.
37. Nakamura Y., Sakakibara S., Miyata T., Ogawa M., Shimazaki T., Weiss S., Kageyama R., Okano H. The bHLH gene hes1 as a repressor of the neuronal commitment of CNS stem cells. J Neurosci. 20:2000;283-293.
38. Galli R., Fiocco R., De Filippis L., Muzio L., Gritti A., Mercurio S., Broccoli V., Pellegrini M., Mallamaci A., Vescovi A.L. Emx2 regulates the proliferation of stem cells of the adult mammalian central nervous system. Development. 129:2002;1633-1644.
39. Shimazaki T., Shingo T., Weiss S. The ciliary neurotrophic factor/leukemia inhibitory factor/gp130 receptor complex operates in the maintenance of mammalian forebrain neural stem cells. J Neurosci. 21:2001;7642-7653.
40. Groszer M., Erickson R., Scripture-Adams D.D., Lesche R., Trumpp A., Zack J.A., Kornblum H.I., Liu X., Wu H. Negative regulation of neural stem/progenitor cell proliferation by the Pten tumor suppressor gene in vivo. Science. 294:2001;2186-2189.
41. Nakatomi H., Kuriu T., Okabe S., Yamamoto S., Hatano O., Kawahara N., Tamura A., Kirino T., Nakafuku M. Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell. 110:2002;429-441 Infusion of bFGF and EGF after ischemia stimulates the regeneration of pyramidal neurons in the hippocampus. This is accompanied by some recovery of lost brain function in spatial cognitive tasks, as assayed by the Morris water maze. The functional recovery of a damaged non-neurogenic brain region after stimulation of endogenous progenitors highlights the potential for brain repair.
42. Louissaint A. Jr., Rao S., Leventhal C., Goldman S.A. Coordinated interaction of neurogenesis and angiogenesis in the adult songbird brain. Neuron. 34:2002;945-960.
43. Monje M.L., Mizumatsu S., Fike J.R., Palmer T.D. Irradiation induces neural precursor-cell dysfunction. Nat Med. 8:2002;955-962.
44. Heissig B., Hattori K., Dias S., Friedrich M., Ferris B., Hackett N.R., Crystal R.G., Besmer P., Lyden D., Moore M.A.et al. Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell. 109:2002;625-637.
45. Bergers G., Brekken R., McMahon G., Vu T.H., Itoh T., Tamaki K., Tanzawa K., Thorpe P., Itohara S., Werb Z.et al. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol. 2:2000;737-744.
46. Gates M.A., Thomas L.B., Howard E.M., Laywell E.D., Sajin B., Faissner A., Gotz B., Silver J., Steindler D.A. Cell and molecular analysis of the developing and adult mouse subventricular zone of the cerebral hemispheres. J Comp Neurol. 361:1995;249-266.
47. Jankovski A., Sotelo C. Subventricular zone-olfactory bulb migratory pathway in the adult mouse: cellular composition and specificity as determined by heterochronic and heterotopic transplantation. J Comp Neurol. 371:1996;376-396.
48. Jacques T.S., Relvas J.B., Nishimura S., Pytela R., Edwards G.M., Streuli C.H., ffrench-Constant C. neural precursor cell chain migration and division are regulated through different B1 integrins. Development. 125:1998;3167-3177.
49. Murase S., Horwitz A.F. Deleted in colorectal carcinoma and differentially expressed integrins mediate the directional migration of neural precursors in the rostral migratory stream. J Neurosci. 22:2002;3568-3579.
50. Bernfield M., Gotte M., Park P.W., Reizes O., Fitzgerald M.L., Lincecum J., Zako M. Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem. 68:1999;729-777.
51. Isshiki T., Pearson B., Holbrook S., Doe C.Q. Drosophila neuroblasts sequentially express transcription factors which specify the temporal identity of their neuronal progeny. Cell. 106:2001;511-521.
52. Bertrand N., Castro D.S., Guillemot F. Proneural genes and the specification of neural cell types. Nat Rev Neurosci. 3:2002;517-530.
53. Fisher A.G., Merkenschlager M. Gene silencing, cell fate and nuclear organisation. Curr Opin Genet Dev. 12:2002;193-197.
54. Takizawa T., Nakashima K., Namihira M., Ochiai W., Uemura A., Yanagisawa M., Fujita N., Nakao M., Taga T. DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain. Dev Cell. 1:2001;749-758 This paper highlights the importance of the epigenetic state of a cell in regulating its responsiveness to extrinsic signals. DNA methylation of a STAT3 binding element in the GFAP promoter of embryonic neuroepithelial cells inhibits their differentiation into astrocytes by preventing STAT3 binding and transcriptional activation. Forced demethylation results in the precocious acquisition of responsiveness to gliogenic signals.
55. ••].
56. ••] demonstrate the coordinate regulation of genes via repression. REST and Co-REST bind to RE-1 sites as a complex with HDACs. Contiguous genes, without RE-1 sites, are simultaneously silenced by the recruitment and spreading of silencing machinery along adjacent chromatin.
57. Ramalho-Santos M., Yoon S., Matsuzaki Y., Mulligan R.C., Melton D.A. "Stemness": transcriptional profiling of embryonic and adult stem cells. Science. 298:2002;597-600.
58. Lessard J., Sauvageau G. Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature. 423:2003;255-260.
59. Park I.K., Qian D., Kiel M., Becker M.W., Pihalja M., Weissman I.L., Morrison S.J., Clarke M.F. Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature. 423:2003;302-305.