The adult mouse dentate gyrus contains populations of committed progenitor cells that are distinct from subependymal zone neural stem cells

Stem Cells

Volumn 29, Issue 9, 2011, Pages 1448-1458

  Clarke, Laura ^a   Van Der Kooy, Derek ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Dentate gyrus; Multipotentiality; Neural stem cell; Self renewal; Subependymal zone

Indexed keywords

ANIMAL TISSUE; ARTICLE; BRAIN; CELL CULTURE; CELL POPULATION; CELL RENEWAL; COCULTURE; DENTATE GYRUS; EMBRYO; EMBRYONIC STEM CELL; FEMALE; HIPPOCAMPUS; IN VITRO STUDY; MOUSE; NEURAL STEM CELL; NONHUMAN; POSTNATAL GROWTH; STEM CELL; SUBVENTRICULAR ZONE;

ANIMALS; CALLITHRIX; CELL DIFFERENTIATION; CELL GROWTH PROCESSES; CELLS, CULTURED; DENTATE GYRUS; HEK293 CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; NEURAL STEM CELLS; NEUROGLIA; NEURONS;

MAMMALIA; MUS;

EID: 80051957728     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.692     Document Type: Article

References (58)

1. Doetsch F., Caillé I., Lim D.A. et al. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 1999;97:703-716. (Pubitemid 29278045)
2. Seri B., Garcia-Verdugo J.M., McEwen B.S. et al. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 2001;21:7135-7160.
3. Merkle F.T., Tramontin A.D., García-Verdugo J.M. et al. Radial glia give rise to adult neural stem cells in the subventricular zone. Proc Natl Acad Sci USA 2004;101:17528-17532. (Pubitemid 39657437)
4. Van Praag H., Schinder A.F., Christie B.R. et al. Functional neurogenesis in the adult hippocampus. Nature 2002;415:1030-1034. (Pubitemid 34193451)
5. Van Praag H., Kempermann G., Gage F.H. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 1999;2:266-270. (Pubitemid 30491298)
6. Gould E., Beylin A., Tanapat P. et al. Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 1999;2:260-265. (Pubitemid 30491297)
7. Shingo T., Gregg C., Enwere E. et al. Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin. Science 2003;299:117-120. (Pubitemid 36042416)
8. Rochefort C., Gheusi G., Vincent J.D. et al. Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J Neurosci 2002;22:2679-2689. (Pubitemid 37465817)
9. Brown J., Cooper-Kuhn C.M., Kempermann G. et al. Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur J Neurosci 2003;17:2042-2046. (Pubitemid 36713965)
10. Mak G.K., Enwere E.K., Gregg C. et al. Male pheromone-stimulated neurogenesis in the adult female brain: Possible role in mating behavior. Nat Neurosci 2007;10:1003-1011. (Pubitemid 47185196)
11. Reynolds B.A., Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992;255:1707-1710.
12. Morshead C.M., Reynolds B.A., Craig C.G. et al. Neural stem cells in the adult mammalian forebrain: A relatively quiescent subpopulation of subependymal cells. Neuron 1994;13:1071-1082. (Pubitemid 24372126)
13. Seaberg R.M., Van der Kooy D. Adult rodent neurogenic regions: The ventricular subependyma contains neural stem cells, but the dentate gyrus contains restricted progenitors. J Neurosci 2002;22:1784-1793. (Pubitemid 35386296)
14. Bull N.D., Bartlett P.F. The adult mouse hippocampal progenitor is neurogenic but not a stem cell. J Neurosci 2005;25:10815-10821. (Pubitemid 41692611)
15. Bonaguidi M.A., Peng C.Y., McGuire T. et al. Noggin expands neural stem cells in the adult hippocampus. J Neurosci 2008;28:9194-9204.
16. Walker T.L., White A., Black D.M. et al. Latent stem and progenitor cells in the hippocampus are activated by neural excitation. J Neurosci 2008;28:5240-5247.
17. Tramontin A.D., García-Verdugo J.M., Lim D.A. et al. Postnatal development of radial glia and the ventricular zone (VZ): A continuum of the neural stem cell compartment. Cereb Cortex 2003;13:580-587. (Pubitemid 36613164)
18. Tropepe V., Hitoshi S., Sirard C. et al. Direct neural fate specification from embryonic stem cells: A primitive mammalian neural stem cell stage acquired through a default mechanism. Neuron 2001;30:65-78. (Pubitemid 32441677)
19. Fedoroff S., Richardson A. Protocols for Neural Cell Culture. Totowa, NJ: Humana Press, 2001:362.
20. Lowenstein D.H., Arsenault L. The effects of growth factors on the survival and differentiation of cultured dentate gyrus neurons. J Neurosci 1996;16:1759-1769. (Pubitemid 26145953)
21. Foudi A., Hochedlinger K., Van Buren D. et al. Analysis of histone 2BGFP retention reveals slowly cycling hematopoietic stem cells. Nat Biotechnol 2009;27:84-90.
22. Gauthier A.S., Furstoss O., Araki T. et al. Control of CNS cell-fate decisions by SHP-2 and its dysregulation in Noonan syndrome. Neuron 2007;54:245-262. (Pubitemid 46562561)
23. Ding S., Wu X., Li G. et al. Efficient transposition of the piggyBac (PB) transposon in mammalian cells and mice. Cell 2005;122:473-483. (Pubitemid 41127147)
24. Mignone J.L., Kukekov V., Chiang A.S. et al. Neural stem and progenitor cells in nestin-GFP transgenic mice. J Comp Neurol 2004;469:311-324. (Pubitemid 38140640)
25. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001;25:402-408. (Pubitemid 34164012)
26. Seaberg R.M., Smukler S.R., Van der Kooy D. Intrinsic differences distinguish transiently neurogenic progenitors from neural stem cells in the early postnatal brain. Dev Biol 2005;278:71-85. (Pubitemid 40092850)
27. Davis A.A., Temple S. A self-renewing multipotential stem cell in embryonic rat cerebral cortex. Nature 1994;372:263-266. (Pubitemid 24352447)
28. Willaime-Morawek S., Seaberg R.M., Batista C. et al. Embryonic cortical neural stem cells migrate ventrally and persist as postnatal striatal stem cells. J Cell Biol 2006;175:159-168. (Pubitemid 44537207)
29. Seaberg R.M., Van der Kooy D. Stem and progenitor cells: The premature desertion of rigorous definitions. Trends Neurosci 2003;26:125-131. (Pubitemid 36183673)
30. Coles-Takabe B.L., Brain I., Purpura K.A. et al. Don't look: Growing clonal versus nonclonal neural stem cell colonies. Stem Cells 2008;26:2938-2944.
31. Morshead C.M., Craig C.G., Van der Kooy D. In vivo clonal analyses reveal the properties of endogenous neural stem cell proliferation in the adult mammalian forebrain. Development 1998;125:2251-2261. (Pubitemid 28336386)
32. Li G., Kataoka H., Coughlin S.R. et al. Identification of a transient subpial neurogenic zone in the developing dentate gyrus and its regulation by Cxcl12 and reelin signaling. Development 2009;136:327-335.
33. Altman J., Bayer S.A. Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods. J Comp Neurol 1990;301:365-381. (Pubitemid 20368500)
34. Navarro-Quiroga I., Hernandez-Valdes M., Lin S.L. et al. Postnatal cellular contributions of the hippocampus subventricular zone to the dentate gyrus, corpus callosum, fimbria, and cerebral cortex. J Comp Neurol 2006;497:833-845. (Pubitemid 43993446)
35. Lois C., Alvarez-Buylla A. Long-distance neuronal migration in the adult mammalian brain. Science 1994;264:1145-1148. (Pubitemid 24210676)
36. Marshall G.P., Laywell E.D., Zheng T. et al. In vitro-derived "neural stem cells" function as neural progenitors without the capacity for self-renewal. Stem Cells 2006;24:731-738. (Pubitemid 44464778)
37. Seidenfaden R., Desoeuvre A., Bosio A. et al. Glial conversion of SVZ-derived committed neuronal precursors after ectopic grafting into the adult brain. Mol Cell Neurosci 2006;32:187-198. (Pubitemid 43868107)
38. Palmer T.D., Takahashi J., Gage F.H. The adult rat hippocampus contains primordial neural stem cells. Mol Cell Neurosci 1997;8:389-404. (Pubitemid 127796477)
39. Encinas J.M., Vaahtokari A., Enikolopov G. Fluoxetine targets early progenitor cells in the adult brain. Proc Natl Acad Sci USA 2006;103:8233-8238. (Pubitemid 43801081)
40. Luskin M.B., Pearlman A.L., Sanes J.R. Cell lineage in the cerebral cortex of the mouse studied in vivo and in vitro with a recombinant retrovirus. Neuron 1988;1:635-647.
41. Luskin M.B. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 1993;11:173-189. (Pubitemid 23222544)
42. Krushel L.A., Johnston J.G., Fishell G. et al. Spatially localized neuronal cell lineages in the developing mammalian forebrain. Neuroscience 1993;53:1035-1047. (Pubitemid 23126099)
43. Mione M.C., Cavanagh J.F., Harris B. et al. Cell fate specification and symmetrical/asymmetrical divisions in the developing cerebral cortex. J Neurosci 1997;17:2018-2029.
44. McCarthy M., Turnbull D.H., Walsh C.A. et al. Telencephalic neural progenitors appear to be restricted to regional and glial fates before the onset of neurogenesis. J Neurosci 2001;21:6772-6781. (Pubitemid 32781120)
45. Wu S., Wu Y., Capecchi M.R. Motoneurons and oligodendrocytes are sequentially generated from neural stem cells but do not appear to share common lineage-restricted progenitors in vivo. Development 2006;133:581-590.
46. Battiste J., Helms A.W., Kim E.J. et al. Ascl1 defines sequentially generated lineage-restricted neuronal and oligodendrocyte precursor cells in the spinal cord. Development 2007;134:285-293.
47. Delaunay D., Heydon K., Cumano A. et al. Early neuronal and glial fate restriction of embryonic neural stem cells. J Neurosci 2008;28:2551-2562. (Pubitemid 351348193)
48. Suh H., Consiglio A., Ray J. et al. In vivo fate analysis reveals the multipotent and self-renewal capacities of Sox2+ neural stem cells in the adult hippocampus. Cell Stem Cell 2007;1:515-528. (Pubitemid 350056408)
49. Bonaguidi M.A., Wheeler M.A., Shapiro J.S. et al. In vivo clonal analysis reveals self-renewing and multipotent adult neural stem cell characteristics. Cell 2011;145:1142-1155.
50. Walsh C., Cepko C.L. Clonal dispersion in proliferative layers of developing cerebral cortex. Nature 1993;362:632-635. (Pubitemid 23109271)
51. Babu H., Cheung G., Kettenmann H. et al. Enriched monolayer precursor cell cultures from micro-dissected adult mouse dentate gyrus yield functional granule cell-like neurons. PLoS One 2007;2:e388.
52. Ahmed S., Reynolds B.A., Weiss S. BDNF enhances the differentiation but not the survival of CNS stem cell-derived neuronal precursors. J Neurosci 1995;15:5765.
53. Hitoshi S., Alexson T., Tropepe V. et al. Notch pathway molecules are essential for the maintenance, but not the generation, of mammalian neural stem cells. Genes Dev 2002;16:846-858. (Pubitemid 34280108)
54. Alexson T.O., Hitoshi S., Coles B.L. et al. Notch signaling is required to maintain all neural stem cell populations - irrespective of spatial or temporal niche. Dev Neurosci 2006;28:34-48.
55. Imayoshi I., Sakamoto M., Yamaguchi M. et al. Essential roles of Notch signaling in maintenance of neural stem cells in developing and adult brains. J Neurosci 2010;30:3489-3498.
56. Ables J.L., Decarolis N.A., Johnson M.A. et al. Notch1 is required for maintenance of the reservoir of adult hippocampal stem cells. J Neurosci 2010;30:10484-10492.
57. Basak O., Taylor V. Identification of self-replicating multipotent progenitors in the embryonic nervous system by high Notch activity and Hes5 expression. Eur J Neurosci 2007;25:1006-1022.
58. Jhaveri D.J., Mackay E.W., Hamlin A.S. et al. Norepinephrine directly activates adult hippocampal precursors via beta3-adrenergic receptors. J Neurosci 2010;30:2795-2806.