The Novel Roles of Glial Cells Revisited: The Contribution of Radial Glia and Astrocytes to Neurogenesis

Current Topics in Developmental Biology

Volumn 69, Issue , 2005, Pages 67-99

  Mori, Tetsuji ^a   Buffo, Annalisa ^a   Götz, Magdalena ^a  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; ASTROCYTE; GLIA; HUMAN; METABOLISM; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY; REVIEW;

ANIMALS; ASTROCYTES; HUMANS; NEUROGENESIS; NEUROGLIA;

EID: 29144469234     PISSN: 00702153     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0070-2153(05)69004-7     Document Type: Review

References (143)

1. Aaku-Saraste E., Hellwig A., and Huttner W.B. Loss of occludin and functional tight junctions, but not ZO-1, during neural tube closure-Remodeling of the neuroepithelium prior to neurogenesis. Dev. Biol. 180 (1996) 664-679
2. Aguirre A.A., Chittajallu R., Belachew S., and Gallo V. NG2-expressing cells in the subventricular zone are type C-like cells and contribute to interneuron generation in the postnatal hippocampus. J. Cell Biol. 165 (2004) 575-589
3. Akimoto J., Itoh H., Miwa T., and Ikeda K. Immunohistochemical study of glutamine synthetase expression in early glial development. Brain Res. Dev. Brain Res. 72 (1993) 9-14
4. Alvarez-Buylla A., Garcia-Verdugo J.M., and Tramontin A.D. A unified hypothesis on the lineage of neural stem cells. Nat. Rev. Neurosci. 2 (2001) 287-293
5. Anthony T.E., Klein C., Fishell G., and Heintz N. Radial glia serve as neuronal progenitors in all regions of the central nervous system. Neuron 41 (2004) 881-890
6. Anton M., and Graham F.L. Site-specific recombination mediated by an adenovirus vector expressing the Cre recombinase protein: A molecular switch for control of gene expression. J. Virol. 69 (1995) 4600-4606
7. Arvidsson A., Collin T., Kirik D., Kokaia Z., and Lindvall O. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat. Med. 8 (2002) 963-970
8. Bachoo R.M., Kim R.S., Ligon K.L., Maher E.A., Brennan C., Billings N., Chan S., Li C., Rowitch D.H., Wong W.H., and De Pinho R.A. Molecular diversity of astrocytes with implications for neurological disorders. Proc. Natl. Acad. Sci. USA 101 (2004) 8384-8349.
9. Bedard A., and Parent A. Evidence of newly generated neurons in the human olfactory bulb. Brain Res. Dev. Brain Res. 151 (2004) 159-168
10. Belachew S., Chittajallu R., Aguirre A.A., Yuan X., Kirby M., Anderson S., and Gallo V. Postnatal NG2 proteoglycan-expressing progenitor cells are intrinsically multipotent and generate functional neurons. J. Cell Biol. 161 (2003) 169-186
11. Belluzzi O., Benedusi M., Ackman J., and Lo Turco J.J. Electrophysiological differentiation of new neurons in the olfactory bulb. J. Neurosci. 23 (2003) 10411-10418
12. Bennett M.V., Contreras J.E., Bukauskas F.F., and Saez J.C. New roles for astrocytes: Gap junction hemichannels have something to communicate. Trends Neurosci. 26 (2003) 610-617
13. Bentivoglio M., and Mazzarello P. The history of radial glia. Brain Res. Bull. 49 (1999) 305-315
14. Bibel M., Richter J., Schrenk K., Tucker K.L., Staiger V., Korte M., Goetz M., and Barde Y.A. Differentiation of mouse embryonic stem cells into a defined neuronal lineage. Nat. Neurosci. 7 (2004) 1003-1009
15. Braun N., Sevigny J., Mishra S.K., Robson S.C., Barth S.W., Gerstberger R., Hammer K., and Zimmermann H. Expression of the ecto-ATPase NTPDase2 in the germinal zones of the developing and adult rat brain. Eur. J. Neurosci. 17 (2003) 1355-1364
16. Cameron R.S., and Rakic P. Glial cell lineage in the cerebral cortex: A review and synthesis. Glia 4 (1991) 124-137
17. Cao Q., Benton R.L., and Whittemore S.R. Stem cell repair of central nervous system injury. J. Neurosci. Res. 68 (2002) 501-510
18. Carleton A., Petreanu L.T., Lansford R., Alvarez-Buylla A., and Lledo P.M. Becoming a new neuron in the adult olfactory bulb. Nat. Neurosci. 6 (2003) 507-518
19. Chanas-Sacre G., Thiry M., Pirard S., Rogister B., Moonen G., Mbebi C., Verdiere-Sahuque M., and Leprince P. A 295-kDA intermediate filament-associated protein in radial glia and developing muscle cells in vivo and in vitro. Dev. Dyn. 219 (2000) 514-525
20. Chen J., Magavi S.S., and Macklis J.D. Neurogenesis of corticospinal motor neurons extending spinal projections in adult mice. Proc. Natl. Acad. Sci. USA 101 (2004) 16357-16362
21. Chmielnicki E., Benraiss A., Economides A.N., and Goldman S.A. Adenovirally expressed noggin and brain-derived neurotrophic factor cooperate to induce new medium spiny neurons from resident progenitor cells in the adult striatal ventricular zone. J. Neurosci. 24 (2004) 2133-2142
22. Choi B.H. Radial glia of developing human fetal spinal cord: Golgi, immunohistochemical and electron microscopic study. Brain Res. 227 (1981) 249-267
23. Craig C.G., Tropepe V., Morshead C.M., Reynolds B.A., Weiss S., and van der Kooy D. In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain. J. Neurosci. 16 (1996) 2649-2658
24. deAzevedo L.C., Fallet C., Moura-Neto V., Daumas-Duport C., Hedin-Pereira C., and Lent R. Cortical radial glial cells in human fetuses: Depth-correlated transformation into astrocytes. J. Neurobiol. 55 (2003) 288-298
25. Doetsch F., Garcia-Verdugo J.M., and 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
26. Doetsch F., Caille I., Lim D.A., Garcia-Verdugo J.M., and Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97 (1999) 703-716
27. Doetsch F., Garcia-Verdugo J.M., and Alvarez-Buylla A. Regeneration of a germinal layer in the adult mammalian brain. Proc. Natl. Acad. Sci. USA 96 (1999) 11619-11624
28. Doetsch F., Petreanu L., Caille I., Garcia-Verdugo J.M., and Alvarez-Buylla A. EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 36 (2002) 1021-1034
29. Eckenhoff M.F., and Rakic P. Radial organization of the hippocampal dentate gyrus: A Golgi, ultrastructural, and immunocytochemical analysis in the developing rhesus monkey. J. Comp. Neurol. 223 (1984) 1-21
30. Edwards M.A., Yamamoto M., and Caviness Jr. V.S. Organization of radial glia and related cells in the developing murine CNS. An analysis based upon a new monoclonal antibody marker. Neuroscience 36 (1990) 121-144
31. Eriksson P.S., Perfilieva E., Bjork-Eriksson T., Alborn A.M., Nordborg C., Peterson D.A., and Gage F.H. Neurogenesis in the adult human hippocampus. Nat. Med. 4 (1998) 1313-1317
32. Fallon J., Reid S., Kinyamu R., Opole I., Opole R., Baratta J., Korc M., Endo T.L., Duong A., Nguyen G., Karkehabadhi M., Twardzik D., Patel S., and Loughlin S. In vivo induction of massive proliferation, directed migration, and differentiation of neural cells in the adult mammalian brain. Proc. Natl. Acad. Sci. USA 97 (2000) 14686-14691
33. Fishell G., and Kriegstein A.R. Neurons from radial glia: The consequences of asymmetric inheritance. Curr. Opin. Neurobiol. 13 (2003) 34-41
34. Frederiksen K., and McKay R.D. Proliferation and differentiation of rat neuroepithelial precursor cells in vivo. J. Neurosci. 8 (1988) 1144-1151
35. Fricker-Gates R.A., Shin J.J., Tai C.C., Catapano L.A., and Macklis J.D. Late-stage immature neocortical neurons reconstruct interhemispheric connections and form synaptic contacts with increased efficiency in adult mouse cortex undergoing targeted neurodegeneration. J. Neurosci. 22 (2002) 4045-4056
36. Gabay L., Lowell S., Rubin L.L., and Anderson D.J. Deregulation of dorsoventral patterning by FGF confers trilineage differentiation capacity on CNS stem cells in vitro. Neuron 40 (2003) 485-499
37. Gadisseux J.F., and Evrard P. Glial-neuronal relationship in the developing central nervous system. A histochemical-electron microscope study of radial glial cell particulate glycogen in normal and reeler mice and the human fetus. Dev. Neurosci. 7 (1985) 12-32
38. Gage F.H. Stem cells of the central nervous system. Curr. Opin. Neurobiol. 8 (1998) 671-676
39. Gage F.H. Neurogenesis in the adult brain. J. Neurosci. 22 (2002) 612-613
40. Gaiano N., Nye J.S., and Fishell G. Radial glial identity is promoted by Notch1 signaling in the murine forebrain. Neuron 26 (2000) 395-404
41. Ganat Y., Soni S., Chacon M., Schwartz M.L., and Vaccarino F.M. Chronic hypoxia up-regulates fibroblast growth factor ligands in the perinatal brain and induces fibroblast growth factor-responsive radial glial cells in the sub-ependymal zone. Neuroscience 112 (2002) 977-991
42. Gangemi R.M., Daga A., Marubbi D., Rosatto N., Capra M.C., and Corte G. Emx2 in adult neural precursor cells. Mech Dev. 109 (2001) 323-329
43. Garcia-Verdugo J.M., Ferron S., Flames N., Collado L., Desfilis E., and Font E. The proliferative ventricular zone in adult vertebrates: A comparative study using reptiles, birds, and mammals. Brain Res. Bull. 57 (2002) 765-775
44. Gates M.A., Thomas L.B., Howard E.M., Laywell E.D., Sajin B., Faissner A., Götz B., Silver J., and 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
45. Götz M. Glial cells generate neurons-master control within CNS regions: Developmental perspectives on neural stem cells. Neuroscientist 9 (2003) 379-397
46. Götz M., Stoykova A., and Gruss P. Pax6 controls radial glia differentiation in the cerebral cortex. Neuron 21 (1998) 1031-1044
47. Götz M., Hartfuss E., and Malatesta P. Radial glial cells as neuronal precursors: A new perspective on the correlation of morphology and lineage restriction in the developing cerebral cortex of mice. Brain Res. Bull. 57 (2002) 777-788
48. Grove E.A., Williams B.P., Li D.Q., Hajihosseini M., Friedrich A., and Price J. Multiple restricted lineages in the embryonic rat cerebral cortex. Development 117 (1993) 553-561
49. Hack M.A., Sugimori M., Lundberg C., Nakafuku M., and Götz M. Regionalization and fate specification in neurospheres: The role of Olig2 and Pax6. Mol. Cell Neurosci. 25 (2004) 664-678
50. Hajihosseini M.K., and Dickson C. A subset of fibroblast growth factors (Fgfs) promote survival, but Fgf-8b specifically promotes astroglial differentiation of rat cortical precursor cells. Mol. Cell Neurosci. 14 (1999) 468-485
51. Harkany T., Andang M., Kingma H.J., Gorcs T.J., Holmgren C.D., Zilberter Y., and Ernfors P. Region-specific generation of functional neurons from naive embryonic stem cells in adult brain. J. Neurochem. 88 (2004) 1229-1239
52. Hartfuss E., Galli R., Heins N., and Götz M. Characterization of CNS precursor subtypes and radial glia. Dev. Biol. 229 (2001) 15-30
53. Hartfuss E., Forster E., Bock H.H., Hack M.A., Leprince P., Luque J.M., Herz J., Frotscher M., and Götz M. Reelin signaling directly affects radial glia morphology and biochemical maturation. Development 130 (2003) 4597-4609
54. Hatakeyama J., Bessho Y., Katoh K., Ookawara S., Fujioka M., Guillemot F., and Kageyama R. Hes genes regulate size, shape and histogenesis of the nervous system by control of the timing of neural stem cell differentiation. Development 131 (2004) 5539-5550
55. Haubensak W., Attardo A., Denk W., and Huttner W.B. Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: A major site of neurogenesis. Proc. Natl. Acad. Sci. USA 101 (2004) 3196-3201
56. Haubst N., Berger J., Radjendirane V., Graw J., Favor J., Saunders G.F., Stoykova A., and Götz M. Molecular dissection of Pax6 function: The specific roles of the paired domain and homeodomain in brain development. Development 131 (2004) 6131-6140
57. Heins N., Malatesta P., Cecconi F., Nakafuku M., Tucker K.L., Hack M.A., Chapouton P., Barde Y.A., and Götz M. Glial cells generate neurons: The role of the transcription factor Pax6. Nat. Neurosci. 5 (2002) 308-315
58. Hunter K.E., and Hatten M.E. Radial glial cell transformation to astrocytes is bidirectional: Regulation by a diffusible factor in embryonic forebrain. Proc. Natl. Acad. Sci. USA 92 (1995) 2061-2205
59. Huttner W.B., and Brand M. Asymmetric division and polarity of neuroepithelial cells. Curr. Opin. Neurobiol. 7 (1997) 29-39
60. Kimelberg H.K. The problem of astrocyte identity. Neurochem. Int. 45 (2004) 191-202
61. Kondo T., and Raff M. Oligodendrocyte precursor cells reprogrammed to become multipotential CNS stem cells. Science 289 (2000) 1754-1757
62. Laywell E.D., Rakic P., Kukekov V.G., Holland E.C., and 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
63. Leavitt B.R., Hernit-Grant C.S., and Macklis J.D. Mature astrocytes transform into transitional radial glia within adult mouse neocortex that supports directed migration of transplanted immature neurons. Exp. Neurol. 157 (1999) 43-57
64. Levitt P., and 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 (1980) 815-840
65. Li H., Babiarz J., Woodbury J., Kane-Goldsmith N., and Grumet M. Spatiotemporal heterogeneity of CNS radial glial cells and their transition to restricted precursors. Dev. Biol. 271 (2004) 225-238
66. Li Y., and Raisman G. Long axon growth from embryonic neurons transplanted into myelinated tracts of the adult rat spinal cord. Brain Res. 629 (1993) 115-127
67. Lillien L. Neural development: Instructions for neural diversity. Curr. Biol. 7 (1997) R168-R171
68. Lim D.A., Tramontin A.D., Trevejo J.M., Herrera D.G., Garcia-Verdugo J.M., and Alvarez-Buylla A. Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron 28 (2000) 713-726
69. Liu S., Wang J., Zhu D., Fu Y., Lukowiak K., and Lu Y.M. Generation of functional inhibitory neurons in the adult rat hippocampus. J. Neurosci. 23 (2003) 732-736
70. Lo Turco J.J., and Kriegstein A.R. Clusters of coupled neuroblasts in embryonic neocortex. Science 252 (1991) 563-566
71. Lobe C.G., Koop K.E., Kreppner W., Lomeli H., Gertsenstein M., and Nagy A. Z/AP, a double reporter for cre-mediated recombination. Dev. Biol. 208 (1999) 281-292
72. Luskin M.B., Pearlman A.L., and Sanes J.R. Cell lineage in the cerebral cortex of the mouse studied in vivo and in vitro with a recombinant retrovirus. Neuron 1 (1988) 635-647
73. Macklis J.D. Transplanted neocortical neurons migrate selectively into regions of neuronal degeneration produced by chromophore-targeted laser photolysis. J. Neurosci. 13 (1993) 3848-3863
74. Magavi S.S., Leavitt B.R., and Macklis J.D. Induction of neurogenesis in the neocortex of adult mice. Nature 405 (2000) 951-955
75. Malatesta P., Hartfuss E., and Götz M. Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 127 (2000) 5253-5263
76. Malatesta P., Hack M.A., Hartfuss E., Kettenmann H., Klinkert W., Kirchhoff F., and Götz M. Neuronal or glial progeny: Regional differences in radial glia fate. Neuron 37 (2003) 751-764
77. Marin-Padilla M. Prenatal development of fibrous (white matter), protoplasmic (gray matter), and layer I astrocytes in the human cerebral cortex: A Golgi study. J. Comp. Neurol. 357 (1995) 554-572
78. Marshall C.A., Suzuki S.O., and Goldman J.E. Gliogenic and neurogenic progenitors of the subventricular zone: Who are they, where did they come from, and where are they going?. Glia 43 (2003) 52-61
79. McCarthy M., Turnbull D.H., Walsh C.A., and Fishell G. Telencephalic neural progenitors appear to be restricted to regional and glial fates before the onset of neurogenesis. J. Neurosci. 21 (2001) 6772-6781
80. McKay R. Stem cells in the central nervous system. Science 276 (1997) 66-71
81. McKay R.D. Stem cell biology and neurodegenerative disease. Philos. Trans. R Soc. Lond. B Biol. Sci. 359 (2004) 851-856
82. Mehler M.F., Mabie P.C., Zhang D., and Kessler J.A. Bone morphogenetic proteins in the nervous system. Trends Neurosci. 20 (1997) 309-317
83. Merkle F.T., Tramontin A.D., Garcia-Verdugo J.M., and Alvarez-Buylla A. Radial glia give rise to adult neural stem cells in the subventricular zone. Proc. Natl. Acad. Sci. USA 101 (2004) 17528-17532
84. Misson J.P., Edwards M.A., Yamamoto M., and Caviness Jr. V.S. Identification of radial glial cells within the developing murine central nervous system: Studies based upon a new immunohistochemical marker. Brain Res. Dev. Brain Res. 44 (1988) 95-108
85. Misson J.P., Edwards M.A., Yamamoto M., and Caviness Jr. V.S. Mitotic cycling of radial glial cells of the fetal murine cerebral wall: A combined autoradiographic and immunohistochemical study. Brain Res. 466 (1988) 183-190
86. Miyake T., and Kitamura T. Glutamine synthetase immunoreactivity in two types of mouse brain glial cells. Brain Res. 586 (1992) 53-60
87. Miyata T., Kawaguchi A., Okano H., and Ogawa M. Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 31 (2001) 727-741
88. Miyata T., Kawaguchi A., Saito K., Kawano M., Muto T., and Ogawa M. Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells. Development 131 (2004) 3133-3145
89. Mollgard K., Balslev Y., Lauritzen B., and Saunders N.R. Cell junctions and membrane specializations in the ventricular zone (germinal matrix) of the developing sheep brain: A CSF-brain barrier. J. Neurocytol. 16 (1987) 433-444
90. Morest D.K. A study of neurogenesis in the forebrain of opossum pouch young. Z. Anat. Entwicklungsgesch 130 (1970) 265-305
91. Morest D.K., and Silver J. Precursors of neurons, neuroglia, and ependymal cells in the CNS: What are they? Where are they from? How do they get where they are going?. Glia 43 (2003) 6-18
92. Morshead C.M., Garcia A.D., Sofroniew M.V., and 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 (2003) 76-84
93. Nadarajah B., Brunstrom J.E., Grutzendler J., Wong R.O., and Pearlman A.L. Two modes of radial migration in early development of the cerebral cortex. Nat. Neurosci. 4 (2001) 143-150
94. Nakatomi H., Kuriu T., Okabe S., Yamamoto S., Hatano O., Kawahara N., Tamura A., Kirino T., and Nakafuku M. Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 110 (2002) 429-441
95. Naujoks-Manteuffel C., and Roth G. Astroglial cells in a salamander brain (Salamandra salamandra) as compared to mammals: A glial fibrillary acidic protein immunohistochemistry study. Brain Res. 487 (1989) 397-401
96. Noctor S.C., Flint A.C., Weissman T.A., Dammerman R.S., and Kriegstein A.R. Neurons derived from radial glial cells establish radial units in neocortex. Nature 409 (2001) 714-720
97. Noctor S.C., Flint A.C., Weissman T.A., Wong W.S., Clinton B.K., and Kriegstein A.R. Dividing precursor cells of the embryonic cortical ventricular zone have morphological and molecular characteristics of radial glia. J. Neurosci. 22 (2002) 3161-3173
98. Noctor S.C., Martinez-Cerdeno V., Ivic L., and Kriegstein A.R. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat. Neurosci. 7 (2004) 136-144
99. Nunes M.C., Roy N.S., Keyoung H.M., Goodman R.R., McKhann II G., Jiang L., Kang J., Nedergaard M., and Goldman S.A. Identification and isolation of multipotential neural progenitor cells from the subcortical white matter of the adult human brain. Nat. Med. 9 (2003) 439-447
100. Owada Y., Yoshimoto T., and Kondo H. Spatio-temporally differential expression of genes for three members of fatty acid binding proteins in developing and mature rat brains. J. Chem NeuroaNat. 12 (1996) 113-122
101. Palmer T.D., Ray J., and Gage F.H. FGF-2-responsive neuronal progenitors reside in proliferative and quiescent regions of the adult rodent brain. Mol. Cell Neurosci. 6 (1995) 474-486
102. Palmer T.D., Markakis E.A., Willhoite A.R., Safar F., and Gage F.H. Fibroblast growth factor-2 activates a latent neurogenic program in neural stem cells from diverse regions of the adult CNS. J. Neurosci. 19 (1999) 8487-8497
103. Parras C.M., Galli R., Britz O., Soares S., Galichet C., Battiste J., Johnson J.E., Nakafuku M., Vescovi A., and Guillemot F. Mash1 specifies neurons and oligodendrocytes in the postnatal brain. EMBO J. 23 (2004) 4495-4505
104. Pixley S.K., and de Vellis J. Transition between immature radial glia and mature astrocytes studied with a monoclonal antibody to vimentin. Brain Res. 317 (1984) 201-209
105. Plachta N., Bibel M., Tucker K.L., and Barde Y.A. Developmental potential of defined neural progenitors derived from mouse embryonic stem cells. Development 131 (2004) 5449-5456
106. Price J., and Thurlow L. Cell lineage in the rat cerebral cortex: A study using retroviral-mediated gene transfer. Development 104 (1988) 473-482
107. Qian X., Goderie S.K., Shen Q., Stern J.H., and Temple S. Intrinsic programs of patterned cell lineages in isolated vertebrate CNS ventricular zone cells. Development 125 (1998) 3143-3152
108. Qian X., Shen Q., Goderie S.K., He W., Capela A., Davis A.A., and Temple S. Timing of CNS cell generation: A programmed sequence of neuron and glial cell production from isolated murine cortical stem cells. Neuron 28 (2000) 69-80
109. Rakic P. Specification of cerebral cortical areas. Science 241 (1988) 170-176
110. Rakic P. Elusive radial glial cells: Historical and evolutionary perspective. Glia 43 (2003) 19-32
111. Reynolds B.A., and Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255 (1992) 1707-1710
112. Reynolds B.A., and Weiss S. Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev. Biol. 175 (1996) 1-13
113. Sanai N., Tramontin A.D., Quinones-Hinojosa A., Barbaro N.M., Gupta N., Kunwar S., Lawton M.T., McDermott M.W., Parsa A.T., Manuel-Garcia Verdugo J., Berger M.S., and Alvarez-Buylla A. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427 (2004) 740-744
114. Sancho-Tello M., Valles S., Montoliu C., Renau-Piqueras J., and Guerri C. Developmental pattern of GFAP and vimentin gene expression in rat brain and in radial glial cultures. Glia 15 (1995) 157-166
115. Schmid R.S., McGrath B., Berechid B.E., Boyles B., Marchionni M., Sestan N., and Anton E.S. Neuregulin 1-erbB2 signaling is required for the establishment of radial glia and their transformation into astrocytes in cerebral cortex. Proc. Natl. Acad. Sci. USA 100 (2003) 4251-4256
116. Schnitzer J., Franke W.W., and Schachner M. Immunocytochemical demonstration of vimentin in astrocytes and ependymal cells of developing and adult mouse nervous system. J. Cell Biol. 90 (1981) 435-447
117. Seaberg R.M., and van der Kooy D. Adult rodent neurogenic regions: The ventricular subependyma contains neural stem cells, but the dentate gyrus contains restricted progenitors. J. Neurosci. 22 (2002) 1784-1793
118. Seri B., Garcia-Verdugo J.M., McEwen B.S., and Alvarez-Buylla A. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J. Neurosci. 21 (2001) 7153-7160
119. Seri B., Garcia-Verdugo J.M., Collado-Morente L., McEwen B.S., and Alvarez-Buylla A. Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J. Comp. Neurol. 478 (2004) 359
120. Shin J.J., Fricker-Gates R.A., Perez F.A., Leavitt B.R., Zurakowski D., and Macklis J.D. Transplanted neuroblasts differentiate appropriately into projection neurons with correct neurotransmitter and receptor phenotype in neocortex undergoing targeted projection neuron degeneration. J. Neurosci. 20 (2000) 7404-7416
121. Shoukimas G.M., and Hinds J.W. The development of the cerebral cortex in the embryonic mouse: An electron microscopic serial section analysis. J. Comp. Neurol. 179 (1978) 795-830
122. Smart I.H. A pilot study of cell production by the ganglionic eminences of the developing mouse brain. J. Anat. 121 (1976) 71-84
123. Smart I.H., Dehay C., Giroud P., Berland M., and Kennedy H. Unique morphological features of the proliferative zones and postmitotic compartments of the neural epithelium giving rise to striate and extrastriate cortex in the monkey. Cereb. Cortex 12 (2002) 37-53
124. Snyder E.Y., Yoon C., Flax J.D., and Macklis J.D. Multipotent neural precursors can differentiate toward replacement of neurons undergoing targeted apoptotic degeneration in adult mouse neocortex. Proc. Natl. Acad. Sci. USA 94 (1997) 11663-11668
125. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21 (1999) 70-71
126. Stenman J., Toresson H., and Campbell K. Identification of two distinct progenitor populations in the lateral ganglionic eminence: Implications for striatal and olfactory bulb neurogenesis. J. Neurosci. 23 (2003) 167-174
127. Tamamaki N., Nakamura K., Okamoto K., and Kaneko T. Radial glia is a progenitor of neocortical neurons in the developing cerebral cortex. Neurosci. Res. 41 (2001) 51-60
128. Theodosis D.T., Pierre K., Cadoret M.A., Allard M., Faissner A., and Poulain D.A. Expression of high levels of the extracellular matrix glycoprotein, tenascin-C, in the normal adult hypothalamoneurohypophysial system. J. Comp. Neurol. 379 (1997) 386-398
129. Toresson H., and Campbell K. A role for Gsh1 in the developing striatum and olfactory bulb of Gsh2 mutant mice. Development 128 (2001) 4769-4780
130. Toresson H., Potter S.S., and Campbell K. Genetic control of dorsal-ventral identity in the telencephalon: Opposing roles for Pax6 and Gsh2. Development 127 (2000) 4361-4371
131. Tramontin A.D., Garcia-Verdugo J.M., Lim D.A., and Alvarez-Buylla A. Postnatal development of radial glia and the ventricular zone (VZ): A continuum of the neural stem cell compartment. Cereb. Cortex 13 (2003) 580-587
132. Voigt T. Development of glial cells in the cerebral wall of ferrets: Direct tracing of their transformation from radial glia into astrocytes. J. Comp. Neurol. 289 (1989) 74-88
133. Walz W. Controversy surrounding the existence of discrete functional classes of astrocytes in adult gray matter. Glia 31 (2000) 95-103
134. Wang Y., Sheen V.L., and Macklis J.D. Cortical interneurons upregulate neurotrophins in vivo in response to targeted apoptotic degeneration of neighboring pyramidal neurons. Exp. Neurol. 154 (1998) 389-402
135. Weiss S., Dunne C., Hewson J., Wohl C., Wheatley M., Peterson A.C., and Reynolds B.A. Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J. Neurosci. 16 (1996) 7599-7609
136. Wictorin K., Brundin P., Gustavii B., Lindvall O., and Bjorklund A. Reformation of long axon pathways in adult rat central nervous system by human forebrain neuroblasts. Nature 347 (1990) 556-558
137. Wood H.B., and Episkopou V. Comparative expression of the mouse Sox1, Sox2 and Sox3 genes from pre-gastrulation to early somite stages. Mech Dev. 86 (1999) 197-201
138. Ying Q.L., Stavridis M., Griffiths D., Li M., and Smith A. Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat. Biotechnol. 21 (2003) 183-186
139. Young J.K., Baker J.H., and Muller T. Immunoreactivity for brain-fatty acid binding protein in gomori-positive astrocytes. Glia 16 (1996) 218-226
140. Zhuo L., Theis M., Alvarez-Maya I., Brenner M., Willecke K., and Messing A. hGFAP-cre transgenic mice for manipulation of glial and neuronal function in vivo. Genesis 31 (2001) 85-94
141. Zigova T., Pencea V., Wiegand S.J., and Luskin M.B. Intraventricular administration of BDNF increases the number of newly generated neurons in the adult olfactory bulb. Mol. Cell Neurosci. 11 (1998) 234-245
142. Zinyk D.L., Mercer E.H., Harris E., Anderson D.J., and Joyner A.L. Fate mapping of the mouse midbrain-hindbrain constriction using a site-specific recombination system. Curr. Biol. 8 (1998) 665-668
143. Zupanc G.K., and Clint S.C. Potential role of radial glia in adult neurogenesis of teleost fish. Glia 43 (2003) 77-86