Identity crisis for adult periventricular neural stem cells: subventricular zone astrocytes, ependymal cells or both? (original) (raw)
Bonfanti, L. & Peretto, P. Radial glial origin of the adult neural stem cells in the subventricular zone. Prog. Neurobiol.83, 24–36 (2007). ArticleCASPubMed Google Scholar
Brazel, C. Y., Romanko, M. J., Rothstein, R. P. & Levison, S. W. Roles of the mammalian subventricular zone in brain development. Prog. Neurobiol.69, 49–69 (2003). ArticlePubMed Google Scholar
Allen, E. The cessation of mitosis in the central nervous system of the albino rat. J. Comp. Neurol.22, 547–568 (1912). Google Scholar
Altman, J. Autoradiographic and histological studies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. J. Comp. Neurol.137, 433–457 (1969). ArticleCASPubMed Google Scholar
Altman, J. Autoradiographic and histological studies of postnatal neurogenesis. 3. Dating the time of production and onset of differentiation of cerebellar microneurons in rats. J. Comp. Neurol.136, 269–293 (1969). ArticleCASPubMed Google Scholar
Kaplan, M. S. & Hinds, J. W. Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science197, 1092–1094 (1977). ArticleCASPubMed Google Scholar
Lewis, P. D. A quantitative study of cell proliferation in the subependymal layer of the adult rat brain. Exp. Neurol.20, 203–207 (1968). ArticleCASPubMed Google Scholar
Privat, A. & Leblond, C. P. The subependymal layer and neighboring region in the brain of the young rat. J. Comp. Neurol.146, 277–302 (1972). ArticleCASPubMed Google Scholar
Kaplan, M. S. Proliferation of subependymal cells in the adult primate CNS: differential uptake of DNA labelled precursors. J. Hirnforsch.24, 23–33 (1983). CASPubMed Google Scholar
Reynolds, B. A. & Weiss, S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science255, 1707–1710 (1992). ArticleCASPubMed Google Scholar
Morshead, C. M. & van der Kooy, D. Disguising adult neural stem cells. Curr. Opin. Neurobiol.14, 125–131 (2004). ArticleCASPubMed Google Scholar
Levison, S. W. & Goldman, J. E. Both oligodendrocytes and astrocytes develop from progenitors in the subventricular zone of postnatal rat forebrain. Neuron10, 201–212 (1993). ArticleCASPubMed Google Scholar
Lois, C. & Alvarez-Buylla, A. Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc. Natl Acad. Sci. USA90, 2074–2077 (1993). ArticleCASPubMedPubMed Central Google Scholar
Lois, C. & Alvarez-Buylla, A. Long-distance neuronal migration in the adult mammalian brain. Science264, 1145–1148 (1994). ArticleCASPubMed Google Scholar
Enwere, E. et al. Aging results in reduced epidermal growth factor receptor signaling, diminished olfactory neurogenesis, and deficits in fine olfactory discrimination. J. Neurosci.24, 8354–8365 (2004). ArticleCASPubMedPubMed Central Google Scholar
Gheusi, G. et al. Importance of newly generated neurons in the adult olfactory bulb for odor discrimination. Proc. Natl Acad. Sci. USA97, 1823–1828 (2000). ArticleCASPubMedPubMed Central Google Scholar
Rochefort, C., Gheusi, G., Vincent, J. D. & Lledo, P. M. Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J. Neurosci.22, 2679–2689 (2002). ArticleCASPubMedPubMed Central Google Scholar
Bedard, A. & Parent, A. Evidence of newly generated neurons in the human olfactory bulb. Brain Res. Dev. Brain Res.151, 159–168 (2004). ArticleCASPubMed Google Scholar
Ignatova, T. N. et al. Human cortical glial tumors contain neural stem-like cells expressing astroglial and neuronal markers in vitro. Glia39, 193–206 (2002). ArticlePubMed Google Scholar
Singh, S. K., Clarke, I. D., Hide, T. & Dirks, P. B. Cancer stem cells in nervous system tumors. Oncogene23, 7267–7273 (2004). ArticleCAS Google Scholar
Tramontin, A. D., Garcia-Verdugo, J. M., Lim, D. A. & Alvarez-Buylla, A. Postnatal development of radial glia and the ventricular zone (VZ): a continuum of the neural stem cell compartment. Cereb. Cortex13, 580–587 (2003). ArticlePubMed Google Scholar
Merkle, F. T., Tramontin, A. D., Garcia-Verdugo, J. M. & Alvarez-Buylla, A. Radial glia give rise to adult neural stem cells in the subventricular zone. Proc. Natl Acad. Sci. USA101, 17528–17532 (2004). ArticleCASPubMedPubMed Central Google Scholar
Garcia-Verdugo, J. M. et al. The proliferative ventricular zone in adult vertebrates: a comparative study using reptiles, birds, and mammals. Brain Res. Bull.57, 765–775 (2002). ArticlePubMed Google Scholar
Weiss, S. et al. Is there a neural stem cell in the mammalian forebrain? Trends Neurosci.19, 387–393 (1996). ArticleCASPubMed Google Scholar
Alvarez-Buylla, A., Garcia-Verdugo, J. M. & Tramontin, A. D. A unified hypothesis on the lineage of neural stem cells. Nature Rev. Neurosci.2, 287–293 (2001). ArticleCAS Google Scholar
Alvarez-Buylla, A. & Lim, D. A. For the long run: maintaining germinal niches in the adult brain. Neuron41, 683–686 (2004). ArticleCASPubMed Google Scholar
Wognum, A. W., Eaves, A. C. & Thomas, T. E. Identification and isolation of hematopoietic stem cells. Arch. Med. Res.34, 461–475 (2003). ArticleCASPubMed Google Scholar
Temple, S. Division and differentiation of isolated CNS blast cells in microculture. Nature340, 471–473 (1989). ArticleCASPubMed Google Scholar
Jensen, J. B. & Parmar, M. Strengths and limitations of the neurosphere culture system. Mol. Neurobiol.34, 153–161 (2006). ArticleCASPubMed Google Scholar
Chaichana, K., Zamora-Berridi, G., Camara-Quintana, J. & Quinones-Hinojosa, A. Neurosphere assays: growth factors and hormone differences in tumor and nontumor studies. Stem Cells24, 2851–2857 (2006). ArticleCASPubMed Google Scholar
Reynolds, B. A. & Rietze, R. L. Neural stem cells and neurospheres—re-evaluating the relationship. Nature Methods2, 333–336 (2005). ArticleCASPubMed Google Scholar
Marshall, G. P., Reynolds, B. A. & Laywell, E. D. Using the neurosphere assay to quantify neural stem cells in vivo. Curr. Pharm. Biotechnol.8, 141–145 (2007). ArticleCASPubMed Google Scholar
Singec, I. et al. Defining the actual sensitivity and specificity of the neurosphere assay in stem cell biology. Nature Methods3, 801–806 (2006). ArticleCASPubMed Google Scholar
Parker, M. A. et al. Expression profile of an operationally-defined neural stem cell clone. Exp. Neurol.194, 320–332 (2005). ArticleCASPubMed Google Scholar
Navarro-Galve, B. & Martinez-Serrano, A. “Is there any need to argue...” about the nature and genetic signature of in vitro neural stem cells? Exp. Neurol.199, 20–25 (2006). ArticleCASPubMed Google Scholar
Morshead, C. M. et al. Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron13, 1071–1082 (1994). ArticleCASPubMed Google Scholar
Cooper-Kuhn, C. M. & Kuhn, H. G. Is it all DNA repair? Methodological considerations for detecting neurogenesis in the adult brain. Brain Res. Dev. Brain Res.134, 13–21 (2002). ArticleCASPubMed Google Scholar
Luo, J., Shook, B. A., Daniels, S. B. & Conover, J. C. Subventricular zone-mediated ependyma repair in the adult mammalian brain. J. Neurosci.28, 3804–3813 (2008). ArticleCASPubMedPubMed Central Google Scholar
Maslov, A. Y., Barone, T. A., Plunkett, R. J. & Pruitt, S. C. Neural stem cell detection, characterization, and age-related changes in the subventricular zone of mice. J. Neurosci.24, 1726–1733 (2004). ArticleCASPubMedPubMed Central Google Scholar
Rando, T. A. The immortal strand hypothesis: segregation and reconstruction. Cell129, 1239–1243 (2007). ArticleCASPubMed Google Scholar
Potten, C. S., Hume, W. J., Reid, P. & Cairns, J. The segregation of DNA in epithelial stem cells. Cell15, 899–906 (1978). ArticleCASPubMed Google Scholar
Potten, C. S., Owen, G. & Booth, D. Intestinal stem cells protect their genome by selective segregation of template DNA strands. J. Cell Sci.115, 2381–2388 (2002). ArticleCASPubMed Google Scholar
Karpowicz, P. et al. Support for the immortal strand hypothesis: neural stem cells partition DNA asymmetrically in vitro. J. Cell Biol.170, 721–732 (2005). ArticleCASPubMedPubMed Central Google Scholar
Kuhn, H. G. & Peterson D. A. in Adult Neurogenesis (eds Gage, F. H., Kempermann, G. & Song, H.) 25–47 (Cold Spring Harbor Laboratory Press, 2008). Google Scholar
Doetsch, F., Caille, I., Lim, D. A., Garcia-Verdugo, J. M. & Alvarez-Buylla, A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell97, 703–716 (1999). ArticleCASPubMed Google Scholar
Johansson, C. B. et al. Identification of a neural stem cell in the adult mammalian central nervous system. Cell96, 25–34 (1999). ArticleCASPubMed Google Scholar
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. Development125, 2251–2261 (1998). ArticleCASPubMed Google Scholar
Colak, D. et al. Adult neurogenesis requires Smad4-mediated bone morphogenic protein signaling in stem cells. J. Neurosci.28, 434–446 (2008). ArticleCASPubMedPubMed Central Google Scholar
Ackman, J. B., Siddiqi, F., Walikonis, R. S. & LoTurco, J. J. Fusion of microglia with pyramidal neurons after retroviral infection. J. Neurosci.26, 11413–11422 (2006). ArticleCASPubMedPubMed Central Google Scholar
Gilyarov, A. V. Nestin in central nervous system cells. Neurosci. Behav. Physiol.38, 165–169 (2008). ArticleCASPubMed Google Scholar
Sakakibara, S. et al. Mouse-Musashi-1, a neural RNA-binding protein highly enriched in the mammalian CNS stem cell. Dev. Biol.176, 230–242 (1996). ArticleCASPubMed Google Scholar
Sakakibara, S., Nakamura, Y., Satoh, H. & Okano, H. RNA-binding protein Musashi2: developmentally regulated expression in neural precursor cells and subpopulations of neurons in mammalian CNS. J. Neurosci.21, 8091–8107 (2001). ArticleCASPubMedPubMed Central Google Scholar
Episkopou, V. SOX2 functions in adult neural stem cells. Trends Neurosci.28, 219–221 (2005). ArticleCASPubMed Google Scholar
Graham, V., Khudyakov, J., Ellis, P. & Pevny, L. SOX2 functions to maintain neural progenitor identity. Neuron39, 749–765 (2003). ArticleCASPubMed Google Scholar
Pevny, L. & Placzek, M. SOX genes and neural progenitor identity. Curr. Opin. Neurobiol.15, 7–13 (2005). ArticleCASPubMed Google Scholar
Uyeda, C. T., Eng, L. F. & Bignami, A. Immunological study of the glial fibrillary acidic protein. Brain Res.37, 81–89 (1972). ArticleCASPubMed Google Scholar
Bignami, A. & Dahl, D. Astrocyte-specific protein and neuroglial differentiation. An immunofluorescence study with antibodies to the glial fibrillary acidic protein. J. Comp. Neurol.153, 27–38 (1974). ArticleCASPubMed Google Scholar
Yanagisawa, M. & Yu, R. K. The expression and functions of glycoconjugates in neural stem cells. Glycobiology17, 57R–74R (2007). ArticleCASPubMed Google Scholar
Capela, A. & Temple, S. LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron35, 865–875 (2002). ArticlePubMed Google Scholar
Corti, S. et al. Isolation and characterization of murine neural stem/progenitor cells based on Prominin-1 expression. Exp. Neurol.205, 547–562 (2007). ArticleCASPubMed Google Scholar
Coskun, V. et al. CD133+ neural stem cells in the ependyma of mammalian postnatal forebrain. Proc. Natl Acad. Sci. USA105, 1026–1031 (2008). ArticleCASPubMedPubMed Central Google Scholar
Zhuo, L. et al. Live astrocytes visualized by green fluorescent protein in transgenic mice. Dev. Biol.187, 36–42 (1997). ArticleCASPubMed Google Scholar
Mirzadeh, Z., Merkle, F. T., Soriano-Navarro, M., Garcia-Verdugo, J. M. & Alvarez-Buylla, A. Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell3, 265–278 (2008). ArticleCASPubMedPubMed Central Google Scholar
Garcia, A. D., Doan, N. B., Imura, T., Bush, T. G. & Sofroniew, M. V. GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nature Neurosci.7, 1233–1241 (2004). ArticleCASPubMed Google Scholar
Soriano, P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nature Genet.21, 70–71 (1999). ArticleCASPubMed Google Scholar
Novak, A., Guo, C., Yang, W., Nagy, A. & Lobe, C. G. Z/EG, a double reporter mouse line that expresses enhanced green fluorescent protein upon Cre-mediated excision. Genesis28, 147–155 (2000). ArticleCASPubMed Google Scholar
Sauer, B. Site-specific recombination: developments and applications. Curr. Opin. Biotechnol.5, 521–527 (1994). ArticleCASPubMed Google Scholar
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. Neuron36, 1021–1034 (2002). ArticleCASPubMed Google Scholar
Morshead, C. M., Garcia, A. D., Sofroniew, M. V. & van Der Kooy, D. 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 (2003). ArticlePubMed Google Scholar
Imura, T., Kornblum, H. I. & Sofroniew, M. V. The predominant neural stem cell isolated from postnatal and adult forebrain but not early embryonic forebrain expresses GFAP. J. Neurosci.23, 2824–2832 (2003). ArticleCASPubMedPubMed Central Google Scholar
Garcia-Verdugo, J. M., Doetsch, F., Wichterle, H., Lim, D. A. & Alvarez-Buylla, A. Architecture and cell types of the adult subventricular zone: in search of the stem cells. J. Neurobiol.36, 234–248 (1998). ArticleCASPubMed Google Scholar
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, 5046–5061 (1997). ArticleCASPubMedPubMed Central Google Scholar
Shen, Q. et al. Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions. Cell Stem Cell3, 289–300 (2008). ArticleCASPubMedPubMed Central Google Scholar
Fuchs, E., Tumbar, T. & Guasch, G. Socializing with the neighbors: stem cells and their niche. Cell116, 769–778 (2004). ArticleCASPubMed Google Scholar
Lim, D. A., Huang, Y. C. & Alvarez-Buylla, A. The adult neural stem cell niche: lessons for future neural cell replacement strategies. Neurosurg. Clin. N. Am.18, 81–92, ix (2007). ArticlePubMed Google Scholar
Conover, J. C. & Notti, R. Q. The neural stem cell niche. Cell Tissue Res.331, 211–224 (2008). ArticlePubMed Google Scholar
Nyfeler, Y. et al. Jagged1 signals in the postnatal subventricular zone are required for neural stem cell self-renewal. EMBO J.24, 3504–3515 (2005). ArticleCASPubMedPubMed Central Google Scholar
Jiao, J. & Chen, D. F. Induction of neurogenesis in nonconventional neurogenic regions of the adult central nervous system by niche astrocyte-produced signals. Stem Cells26, 1221–1230 (2008). ArticleCASPubMedPubMed Central Google Scholar
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, 4462–4471 (1999). ArticleCASPubMedPubMed Central Google Scholar
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. USA97, 13883–13888 (2000). ArticleCASPubMedPubMed Central Google Scholar
Rietze, R. L. et al. Purification of a pluripotent neural stem cell from the adult mouse brain. Nature412, 736–739 (2001). ArticleCASPubMed Google Scholar
Weigmann, A., Corbeil, D., Hellwig, A. & Huttner, W. B. Prominin, a novel microvilli-specific polytopic membrane protein of the apical surface of epithelial cells, is targeted to plasmalemmal protrusions of non-epithelial cells. Proc. Natl Acad. Sci. USA94, 12425–12430 (1997). ArticleCASPubMedPubMed Central Google Scholar
Spassky, N. et al. Adult ependymal cells are postmitotic and are derived from radial glial cells during embryogenesis. J. Neurosci.25, 10–18 (2005). ArticleCASPubMedPubMed Central Google Scholar
Imamoto, K., Paterson, J. A. & Leblond, C. P. Radioautographic investigation of gliogenesis in the corpus callosum of young rats. I. Sequential changes in oligodendrocytes. J. Comp. Neurol.180, 115–128, 132–7 (1978). ArticleCASPubMed Google Scholar
Kraus-Ruppert, R., Laissue, J., Burki, H. & Odartchenko, N. Kinetic studies on glial, Schwann and capsular cells labelled with 3H thymidine in cerebrospinal tissue of young mice. J. Neurol. Sci.26, 555–563 (1975). ArticleCASPubMed Google Scholar
Chauhan, A. N. & Lewis, P. D. A quantitative study of cell proliferation in ependyma and choroid plexus in the postnatal rat brain. Neuropathol. Appl. Neurobiol.5, 303–309 (1979). ArticleCASPubMed Google Scholar
Altman, J. Autoradiographic investigation of cell proliferation in the brains of rats and cats. Anat. Rec.145, 573–591 (1963). ArticleCASPubMed Google Scholar
Korr, H. Proliferation of different cell types in the brain. Adv. Anat. Embryol. Cell Biol.61, 1–72 (1980). ArticleCASPubMed Google Scholar
Bryans, W. A. Mitotic activity in the brain of the adult rat. Anat. Rec.133, 65–71 (1959). Article Google Scholar
Smart, I. The subependymal layer of the mouse brain and its cell production as shown by radioautography after thymidine-H3 injection. J. Comp. Neurol.116, 325–338 (1961). Article Google Scholar
Mori, T. et al. Inducible gene deletion in astroglia and radial glia - a valuable tool for functional and lineage analysis. Glia54, 21–34 (2006). ArticlePubMed Google Scholar
Metzger, D. & Chambon, P. Site- and time-specific gene targeting in the mouse. Methods24, 71–80 (2001). ArticleCASPubMed Google Scholar
Doetsch, F., Garcia-Verdugo, J. M. & Alvarez-Buylla, A. Regeneration of a germinal layer in the adult mammalian brain. Proc. Natl Acad. Sci. USA96, 11619–11624 (1999). ArticleCASPubMedPubMed Central Google Scholar
Brawer, J. R. The fine structure of the ependymal tanycytes at the level of the arcuate nucleus. J. Comp. Neurol.145, 25–41 (1972). ArticleCASPubMed Google Scholar
Millhouse, O. E. Light and electron microscopic studies of the ventricular wall. Z. Zellforsch. Mikrosk. Anat.127, 149–174 (1972). ArticleCAS Google Scholar
Bruni, J. E. Ependymal development, proliferation, and functions: a review. Microsc. Res. Tech.41, 2–13 (1998). ArticleCASPubMed Google Scholar
Coates, P. W. & Davis, S. L. Tanycytes in long-term ovariectomized ewes treated with estrogen exhibit ultrastructural features associated with increased cellular activity. Anat. Rec.203, 179–187 (1982). ArticleCASPubMed Google Scholar
de Vitry, F., Picart, R., Jacque, C. & Tixier-Vidal, A. Glial fibrillary acidic protein. A cellular marker of tanycytes in the mouse hypothalamus. Dev. Neurosci.4, 457–460 (1981). ArticleCASPubMed Google Scholar
Jeffrey, M., Wells, G. A. & Bridges, A. W. An immunohistochemical study of the topography and cellular localization of three neural proteins in the sheep nervous system. J. Comp. Pathol.103, 23–35 (1990). ArticleCASPubMed Google Scholar
Alvarez-Buylla, A., Buskirk, D. R. & Nottebohm, F. Monoclonal antibody reveals radial glia in adult avian brain. J. Comp. Neurol.264, 159–170 (1987). ArticleCASPubMed Google Scholar
Gotz, M. & Huttner, W. B. The cell biology of neurogenesis. Nature Rev. Mol. Cell Biol.6, 777–788 (2005). ArticleCAS Google Scholar
Alvarez-Buylla, A., Garcia-Verdugo, J. M., Mateo, A. S. & Merchant-Larios, H. Primary neural precursors and intermitotic nuclear migration in the ventricular zone of adult canaries. J. Neurosci.18, 1020–1037 (1998). ArticleCASPubMedPubMed Central Google Scholar
Del Bene, F., Wehman, A. M., Link, B. A. & Baier, H. Regulation of neurogenesis by interkinetic nuclear migration through an apical-basal notch gradient. Cell134, 1055–1065 (2008). ArticleCASPubMedPubMed Central Google Scholar
Tsai, J. W., Chen, Y., Kriegstein, A. R. & Vallee, R. B. LIS1 RNA interference blocks neural stem cell division, morphogenesis, and motility at multiple stages. J. Cell Biol.170, 935–945 (2005). ArticleCASPubMedPubMed Central Google Scholar
Willaime-Morawek, S. & van der Kooy, D. Cortex- and striatum- derived neural stem cells produce distinct progeny in the olfactory bulb and striatum. Eur. J. Neurosci.27, 2354–2362 (2008). ArticlePubMed Google Scholar
Merkle, F. T., Mirzadeh, Z. & Alvarez-Buylla, A. Mosaic organization of neural stem cells in the adult brain. Science317, 381–384 (2007). ArticleCASPubMed Google Scholar
Kohwi, M. et al. A subpopulation of olfactory bulb GABAergic interneurons is derived from _Emx1_- and _Dlx5/6_-expressing progenitors. J. Neurosci.27, 6878–6891 (2007). ArticleCASPubMedPubMed Central Google Scholar
Hack, M. A. et al. Neuronal fate determinants of adult olfactory bulb neurogenesis. Nature Neurosci.8, 865–872 (2005). ArticleCASPubMed Google Scholar
Willaime-Morawek, S. et al. Embryonic cortical neural stem cells migrate ventrally and persist as postnatal striatal stem cells. J. Cell Biol.175, 159–168 (2006). ArticleCASPubMedPubMed Central Google Scholar
Young, K. M., Fogarty, M., Kessaris, N. & Richardson, W. D. Subventricular zone stem cells are heterogeneous with respect to their embryonic origins and neurogenic fates in the adult olfactory bulb. J. Neurosci.27, 8286–8296 (2007). ArticleCASPubMedPubMed Central Google Scholar
Kakita, A. & Goldman, J. E. Patterns and dynamics of SVZ cell migration in the postnatal forebrain: monitoring living progenitors in slice preparations. Neuron23, 461–472 (1999). ArticleCASPubMed Google Scholar
Halliday, A. L. & Cepko, C. L. Generation and migration of cells in the developing striatum. Neuron9, 15–26 (1992). ArticleCASPubMed Google Scholar
Noctor, S. C., Martinez-Cerdeno, V., Ivic, L. & Kriegstein, A. R. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nature Neurosci.7, 136–144 (2004). ArticleCASPubMed Google Scholar
Haubensak, W., Attardo, A., Denk, W. & Huttner, W. B. Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc. Natl Acad. Sci. USA101, 3196–3201 (2004). ArticleCASPubMedPubMed Central Google Scholar
Porteus, M. H. et al. DLX-2, MASH-1, and MAP-2 expression and bromodeoxyuridine incorporation define molecularly distinct cell populations in the embryonic mouse forebrain. J. Neurosci.14, 6370–6383 (1994). ArticleCASPubMedPubMed Central Google Scholar
Torii, M. et al. Transcription factors Mash-1 and Prox-1 delineate early steps in differentiation of neural stem cells in the developing central nervous system. Development126, 443–456 (1999). ArticleCASPubMed Google Scholar
Wu, S. X. et al. Pyramidal neurons of upper cortical layers generated by NEX-positive progenitor cells in the subventricular zone. Proc. Natl Acad. Sci. USA102, 17172–17177 (2005). ArticleCASPubMedPubMed Central Google Scholar
Staugaitis, S. M., Zerlin, M., Hawkes, R., Levine, J. M. & Goldman, J. E. Aldolase C/zebrin II expression in the neonatal rat forebrain reveals cellular heterogeneity within the subventricular zone and early astrocyte differentiation. J. Neurosci.21, 6195–6205 (2001). ArticleCASPubMedPubMed Central Google Scholar
Lledo, P. M., Merkle, F. T. & Alvarez-Buylla, A. Origin and function of olfactory bulb interneuron diversity. Trends Neurosci.31, 392–400 (2008). ArticleCASPubMedPubMed Central Google Scholar
Corbin, J. G., Gaiano, N., Machold, R. P., Langston, A. & Fishell, G. The Gsh2 homeodomain gene controls multiple aspects of telencephalic development. Development127, 5007–5020 (2000). ArticleCASPubMed Google Scholar
Toresson, H., Potter, S. S. & Campbell, K. Genetic control of dorsal-ventral identity in the telencephalon: opposing roles for Pax6 and Gsh2. Development127, 4361–4371 (2000). ArticleCASPubMed Google Scholar
Parmar, M., Sjoberg, A., Bjorklund, A. & Kokaia, Z. Phenotypic and molecular identity of cells in the adult subventricular zone: in vivo and after expansion in vitro. Mol. Cell Neurosci.24, 741–752 (2003). ArticleCASPubMed Google Scholar
Jessen, K. R. & Mirsky, R. Glial cells in the enteric nervous system contain glial fibrillary acidic protein. Nature286, 736–737 (1980). ArticleCASPubMed Google Scholar
Antanitus, D. S., Choi, B. H. & Lapham, L. W. The demonstration of glial fibrillary acidic protein in the cerebrum of the human fetus by indirect immunofluorescence. Brain Res.103, 613–616 (1976). ArticleCASPubMed Google Scholar
Levitt, P. & Rakic, P. 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 (1980). ArticleCASPubMed Google Scholar
Choi, B. H. & Lapham, L. W. Radial glia in the human fetal cerebrum: a combined Golgi, immunofluorescent and electron microscopic study. Brain Res.148, 295–311 (1978). ArticleCASPubMed Google Scholar
Schmechel, D. E. & Rakic, P. A Golgi study of radial glial cells in developing monkey telencephalon: morphogenesis and transformation into astrocytes. Anat. Embryol.156, 115–152 (1979). ArticleCAS Google Scholar
Bodega, G., Suarez, I., Rubio, M. & Fernandez, B. Ependyma: phylogenetic evolution of glial fibrillary acidic protein (GFAP) and vimentin expression in vertebrate spinal cord. Histochemistry102, 113–122 (1994). ArticleCASPubMed Google Scholar
Gould, S. J. & Howard, S. An immunohistochemical study of the germinal layer in the late gestation human fetal brain. Neuropathol. Appl. Neurobiol.13, 421–437 (1987). ArticleCASPubMed Google Scholar
Roessmann, U., Velasco, M. E., Sindely, S. D. & Gambetti, P. Glial fibrillary acidic protein (GFAP) in ependymal cells during development. An immunocytochemical study. Brain Res.200, 13–21 (1980). ArticleCASPubMed Google Scholar
Gould, S. J., Howard, S. & Papadaki, L. The development of ependyma in the human fetal brain: an immunohistological and electron microscopic study. Brain Res. Dev. Brain Res.55, 255–267 (1990). ArticleCASPubMed Google Scholar
Rafols, J. A. & Goshgarian, H. G. Spinal tanycytes in the adult rat: a correlative Golgi gold-toning study. Anat. Rec.211, 75–86 (1985). ArticleCASPubMed Google Scholar
Xu, Y. et al. Neurogenesis in the ependymal layer of the adult rat 3rd ventricle. Exp. Neurol.192, 251–264 (2005). ArticleCASPubMed Google Scholar
Messier, B., Leblond, C. P. & Smart, I. Presence of DNA synthesis and mitosis in the brain of young adult mice. Exp. Cell Res.14, 224–226 (1958). ArticleCASPubMed Google Scholar
Smart, I. & Leblond, C. P. Evidence for division and transformation of neuroglia cells in the mouse brain as derived from radioautography after injection of thymidine-H3. J. Comp. Neurol.116, 349–367 (1961). Article Google Scholar
Altman, J. Are new neurons formed in the brains of adult mammals? Science135, 1127–1128 (1962). ArticleCASPubMed Google Scholar
Altman, J. & Das, G. D. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J. Comp. Neurol.124, 319–335 (1965). ArticleCASPubMed Google Scholar
Altman, J. & Das, G. D. Post-natal origin of microneurones in the rat brain. Nature207, 953–956 (1965). ArticleCASPubMed Google Scholar
Richards, L. J., Kilpatrick, T. J. & Bartlett, P. F. De novo generation of neuronal cells from the adult mouse brain. Proc. Natl Acad. Sci. USA89, 8591–8595 (1992). ArticleCASPubMedPubMed Central Google Scholar
Corotto, F. S., Henegar, J. A. & Maruniak, J. A. Neurogenesis persists in the subependymal layer of the adult mouse brain. Neurosci. Lett.149, 111–114 (1993). ArticleCASPubMed Google Scholar
Luskin, M. B. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron11, 173–189 (1993). ArticleCASPubMed Google Scholar
Lois, C., Garcia-Verdugo, J. M. & Alvarez-Buylla, A. Chain migration of neuronal precursors. Science271, 978–981 (1996). ArticleCASPubMed Google Scholar
Craig, C. G. et al. In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain. J. Neurosci.16, 2649–2658 (1996). ArticleCASPubMedPubMed Central Google Scholar
Johansson, C. B., Svensson, M., Wallstedt, L., Janson, A. M. & Frisen, J. Neural stem cells in the adult human brain. Exp. Cell Res.253, 733–736 (1999). ArticleCASPubMed Google Scholar