Prospective isolation of functionally distinct radial glial subtypes-Lineage and transcriptome analysis

Molecular and Cellular Neuroscience

Volumn 38, Issue 1, 2008, Pages 15-42

  Pinto, Luisa ^a   Mader, Michael T ^a   Irmler, Martin ^a   Gentilini, Marco ^b   Santoni, Federico ^c   Drechsel, Daniela ^a   Blum, Robert ^e   Stahl, Ronny ^e   Bulfone, Alessandro ^b   Malatesta, Paolo ^d   Beckers, Johannes ^a   Götz, Magdalena ^a,e  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b BIOFLAG   (Italy)

^c CENTER FOR ADVANCED STUDIES   (Italy)

^d UNIVERSITY OF GENOA   (Italy)

^e UNIVERSITY OF MUNICH   (Germany)

Author keywords

Basal precursors; Cerebral cortex; Development; Gliogenesis; Lineage; Neurogenesis; Oligodendrogenesis; Pax6; Radial glia; Transcriptome

Indexed keywords

EOMESODERMIN; TRANSCRIPTOME;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CELL DIFFERENTIATION; CELL FATE; CELL ISOLATION; CELL LINEAGE; CELL TYPE; CLONE; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; GLIA CELL; IMMUNOCYTOCHEMISTRY; MICROARRAY ANALYSIS; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROGENY; RAT; RNA ISOLATION; STEM CELL; TRANSCRIPTOMICS;

ANIMALS; CELL LINEAGE; CELL SEPARATION; CELLS, CULTURED; CEREBRAL CORTEX; GENE EXPRESSION PROFILING; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEUROGLIA; RATS; RATS, WISTAR;

EID: 43049119575     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2008.01.012     Document Type: Article

References (119)

1. Abramova N., Charniga C., Goderie S.K., and Temple S. Stage-specific changes in gene expression in acutely isolated mouse CNS progenitor cells. Dev. Biol. 283 (2005) 269-281
2. 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
3. Auman H.J., Nottoli T., Lakiza O., Winger Q., Donaldson S., and Williams T. Transcription factor AP-2gamma is essential in the extra-embryonic lineages for early postimplantation development. Development (Cambridge, England) 129 (2002) 2733-2747
4. Baker K.M., Wei G., Schaffner A.E., and Ostrowski M.C. Ets-2 and components of mammalian SWI/SNF form a repressor complex that negatively regulates the BRCA1 promoter. J. Biol. Chem. 278 (2003) 17876-17884
5. Baldi P., and Long A.D. A Bayesian framework for the analysis of microarray expression data: regularized t-test and statistical inferences of gene changes. Bioinformatics 17 (2001) 509-519
6. Bartkowska K., Paquin A., Gauthier A.S., Kaplan D.R., and Miller F.D. Trk signaling regulates neural precursor cell proliferation and differentiation during cortical development. Development 134 (2007) 4369-4380
7. Benjamini Y., and Hochberg Y. Multiple hypotheses testing with weights. Scand. J. Statist. 24 (1997) 407-418
8. Bentivoglio M., and Mazzarello P. The history of radial glia. Brain Res. Bull. 49 (1999) 305-315
9. Berninger B., Costa M.R., Koch U., Schroeder T., Sutor B., Grothe B., and Gotz M. Functional properties of neurons derived from in vitro reprogrammed postnatal astroglia. J. Neurosci. 27 (2007) 8654-8664
10. Berninger B., Guillemot F., and Gotz M. Directing neurotransmitter identity of neurones derived from expanded adult neural stem cells. Eur. J. Neurosci. 25 (2007) 2581-2590
11. Bolstad B.M., Irizarry R.A., Astrand M., and Speed T.P. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19 (2003) 185-193
12. Buffo A., Vosko M.R., Erturk D., Hamann G.F., Jucker M., Rowitch D., and Gotz M. Expression pattern of the transcription factor Olig2 in response to brain injuries: implications for neuronal repair. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 18183-18188
13. Cameron R.S., and Rakic P. Glial cell lineage in the cerebral cortex: a review and synthesis. Glia 4 (1991) 124-137
14. Cappello S., Attardo A., Wu X., Iwasato T., Itohara S., Wilsch-Brauninger M., Eilken H.M., Rieger M.A., Schroeder T.T., Huttner W.B., Brakebusch C., and Gotz M. The Rho-GTPase Cdc42 regulates neural progenitor fate at the apical surface. Nat. Neurosci. 9 (2006) 1099-1107
15. Caviness Jr. V.S., Goto T., Tarui T., Takahashi T., Bhide P.G., and Nowakowski R.S. Cell output, cell cycle duration and neuronal specification: a model of integrated mechanisms of the neocortical proliferative process. Cereb. Cortex 13 (2003) 592-598
16. Chapouton P., Schuurmans C., Guillemot F., and Gotz M. The transcription factor neurogenin 2 restricts cell migration from the cortex to the striatum. Development 128 (2001) 5149-5159
17. Chenn A., and Walsh C.A. Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 297 (2002) 365-369
18. Chiang D.Y., Brown P.O., and Eisen M.B. Visualizing associations between genome sequences and gene expression data using genome-mean expression profiles. Bioinformatics 17 Suppl. 1 (2001) S49-S55
19. Cleveland W.S. Lowess: a program for smoothing scatterplots by robust locally weighted regression. Am. Statistician 35 (1981) 54
20. Costa M.R., Wen G., Lepier A., Schroeder T., and Gotz M. Par-complex proteins promote proliferative progenitor divisions in the developing mouse cerebral cortex. Development 135 (2008) 11-22
21. Dehay C., and Kennedy H. Cell-cycle control and cortical development. Nat. Rev. Neurosci. 8 (2007) 438-450
22. den Hollander A.I., Ghiani M., de Kok Y.J., Wijnholds J., Ballabio A., Cremers F.P., and Broccoli V. Isolation of Crb1, a mouse homologue of Drosophila crumbs, and analysis of its expression pattern in eye and brain. Mech. Dev. 110 (2002) 203-207
23. Easterday M.C., Dougherty J.D., Jackson R.L., Ou J., Nakano I., Paucar A.A., Roobini B., Dianati M., Irvin D.K., Weissman I.L., Terskikh A.V., Geschwind D.H., and Kornblum H.I. Neural progenitor genes. Germinal zone expression and analysis of genetic overlap in stem cell populations. Dev. Biol. 264 (2003) 309-322
24. Englund C., Fink A., Lau C., Pham D., Daza R.A., Bulfone A., Kowalczyk T., and Hevner R.F. Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J. Neurosci. 25 (2005) 247-251
25. Fan G., Martinowich K., Chin M.H., He F., Fouse S.D., Hutnick L., Hattori D., Ge W., Shen Y., Wu H., ten Hoeve J., Shuai K., and Sun Y.E. DNA methylation controls the timing of astrogliogenesis through regulation of JAK-STAT signaling. Development 132 (2005) 3345-3356
26. Fjose A., Nornes S., Weber U., and Mlodzik M. Functional conservation of vertebrate seven-up related genes in neurogenesis and eye development. EMBO J. 12 (1993) 1403-1414
27. Fode C., Ma Q., Casarosa S., Ang S.L., Anderson D.J., and Guillemot F. A role for neural determination genes in specifying the dorsoventral identity of telencephalic neurons. Genes Dev. 14 (2000) 67-80
28. 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
29. Gal J.S., Morozov Y.M., Ayoub A.E., Chatterjee M., Rakic P., and Haydar T.F. Molecular and morphological heterogeneity of neural precursors in the mouse neocortical proliferative zones. J. Neurosci. 26 (2006) 1045-1056
30. Gao F.B., Kohwi M., Brenman J.E., Jan L.Y., and Jan Y.N. Control of dendritic field formation in Drosophila: the roles of flamingo and competition between homologous neurons. Neuron 28 (2000) 91-101
31. Gauchat D., Escriva H., Miljkovic-Licina M., Chera S., Langlois M.C., Begue A., Laudet V., and Galliot B. The orphan COUP-TF nuclear receptors are markers for neurogenesis from cnidarians to vertebrates. Dev. Biol. 275 (2004) 104-123
32. Gentilini M., and Santoni F. FlagTrap, a bioinformatic pipeline to identify membrane proteins. CRS4 Technical Report 10 (2006)
33. Geschwind D.H., Ou J., Easterday M.C., Dougherty J.D., Jackson R.L., Chen Z., Antoine H., Terskikh A., Weissman I.L., Nelson S.F., and Kornblum H.I. A genetic analysis of neural progenitor differentiation. Neuron 29 (2001) 325-339
34. Götz M., and Huttner W.B. The cell biology of neurogenesis. Nat. Rev. Mol. Cell Biol. 6 (2005) 777-788
35. Götz M., Stoykova A., and Gruss P. Pax6 controls radial glia differentiation in the cerebral cortex. Neuron 21 (1998) 1031-1044
36. 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
37. Hack M.A., Saghatelyan A., de Chevigny A., Pfeifer A., Ashery-Padan R., Lledo P.M., and Gotz M. Neuronal fate determinants of adult olfactory bulb neurogenesis. Nat. Neurosci. 8 (2005) 865-872
38. Hartfuss E., Forster E., Bock H.H., Hack M.A., Leprince P., Luque J.M., Herz J., Frotscher M., and Gotz M. Reelin signaling directly affects radial glia morphology and biochemical maturation. Development 130 (2003) 4597-4609
39. 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. U. S. A. 101 (2004) 3196-3201
40. Haubst N., Berger J., Radjendirane V., Graw J., Favor J., Saunders G.F., Stoykova A., and Gotz M. Molecular dissection of Pax6 function: the specific roles of the paired domain and homeodomain in brain development. Development (Cambridge, England) 131 (2004) 6131-6140
41. Haubst N., Favor J., and Götz M. The role of Pax6 in the nervous system during development and in adulthood - master control regulator or modular function?. In: Thiel G. (Ed). Development, Brain Function and Disease (2005), Wiley-VCH
42. Heins N., Cremisi F., Malatesta P., Gangemi R.M., Corte G., Price J., Goudreau G., Gruss P., and Gotz M. Emx2 promotes symmetric cell divisions and a multipotential fate in precursors from the cerebral cortex. Mol. Cell. Neurosci. 18 (2001) 485-502
43. Heins N., Malatesta P., Cecconi F., Nakafuku M., Tucker K.L., Hack M.A., Chapouton P., Barde Y.A., and Gotz M. Glial cells generate neurons: the role of the transcription factor Pax6. Nat. Neurosci. 5 (2002) 308-315
44. Holm P.C., Mader M.T., Haubst N., Wizenmann A., Sigvardsson M., and Gotz M. Loss- and gain-of-function analyses reveal targets of Pax6 in the developing mouse telencephalon. Mol. Cell. Neurosci. 34 (2007) 99-119
45. Imai F., Hirai S., Akimoto K., Koyama H., Miyata T., Ogawa M., Noguchi S., Sasaoka T., Noda T., and Ohno S. Inactivation of aPKClambda results in the loss of adherens junctions in neuroepithelial cells without affecting neurogenesis in mouse neocortex. Development 133 (2006) 1735-1744
46. Jung C.G., Kim H.J., Kawaguchi M., Khanna K.K., Hida H., Asai K., Nishino H., and Miura Y. Homeotic factor ATBF1 induces the cell cycle arrest associated with neuronal differentiation. Development 132 (2005) 5137-5145
47. Kessaris N., Fogarty M., Iannarelli P., Grist M., Wegner M., and Richardson W.D. Competing waves of oligodendrocytes in the forebrain and postnatal elimination of an embryonic lineage. Nat. Neurosci. 9 (2006) 173-179
48. Key G., Kubbutat M.H., and Gerdes J. Assessment of cell proliferation by means of an enzyme-linked immunosorbent assay based on the detection of the Ki-67 protein. J. Immunol. Methods 177 (1994) 113-117
49. Lagenaur C., and Schachner M. Monoclonal antibody (M2) to glial and neuronal cell surfaces. J. Supramol. Struct. Cell. Biochem. 15 (1981) 335-346
50. Lee M.K., Tuttle J.B., Rebhun L.I., Cleveland D.W., and Frankfurter A. The expression and posttranslational modification of a neuron-specific beta-tubulin isotype during chick embryogenesis. Cell. Motil. Cytoskelet. 17 (1990) 118-132
51. Li C., and Hung Wong W. Model-based analysis of oligonucleotide arrays: model validation, design issues and standard error application. Genome Biol. 2 (2001) (RESEARCH0032)
52. Liepelt U., Kindler-Rohrborn A., Lennartz K., Reinhardt-Maelicke S., and Rajewsky M.F. Differentiation potential of a monoclonal antibody-defined neural progenitor cell population isolated from prenatal rat brain by fluorescence-activated cell sorting. Brain Res. Dev. Brain Res. 51 (1990) 267-278
53. Lin X., Shah S., and Bulleit R.F. The expression of MEF2 genes is implicated in CNS neuronal differentiation. Brain Res. Mol. Brain Res. 42 (1996) 307-316
54. Lindsell C.E., Boulter J., diSibio G., Gossler A., and Weinmaster G. Expression patterns of Jagged, Delta1, Notch1, Notch2, and Notch3 genes identify ligand-receptor pairs that may function in neural development. Mol. Cell. Neurosci. 8 (1996) 14-27
55. Lu X.P., Salbert G., and Pfahl M. An evolutionary conserved COUP-TF binding element in a neural-specific gene and COUP-TF expression patterns support a major role for COUP-TF in neural development. Mol. Endocrinol. 8 (1994) 1774-1788
56. Lu Q.R., Sun T., Zhu Z., Ma N., Garcia M., Stiles C.D., and Rowitch D.H. Common developmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection. Cell 109 (2002) 75-86
57. Luskin M.B., Parnavelas J.G., and Barfield J.A. Neurons, astrocytes, and oligodendrocytes of the rat cerebral cortex originate from separate progenitor cells: an ultrastructural analysis of clonally related cells. J. Neurosci. 13 (1993) 1730-1750
58. Lyons G.E., Micales B.K., Schwarz J., Martin J.F., and Olson E.N. Expression of mef2 genes in the mouse central nervous system suggests a role in neuronal maturation. J. Neurosci. 15 (1995) 5727-5738
59. Malatesta P., Hartfuss E., and Gotz M. Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 127 (2000) 5253-5263
60. Malatesta P., Hack M.A., Hartfuss E., Kettenmann H., Klinkert W., Kirchhoff F., and Gotz M. Neuronal or glial progeny: regional differences in radial glia fate. Neuron 37 (2003) 751-764
61. Maric D., and Barker J.L. Neural stem cells redefined: a FACS perspective. Mol. Neurobiol. 30 (2004) 49-76
62. Mason H.A., Rakowiecki S.M., Gridley T., and Fishell G. Loss of Notch activity in the developing central nervous system leads to increased cell death. Dev. Neurosci. 28 (2006) 49-57
63. Matsumoto S., Banine F., Struve J., Xing R., Adams C., Liu Y., Metzger D., Chambon P., Rao M.S., and Sherman L.S. Brg1 is required for murine neural stem cell maintenance and gliogenesis. Dev. Biol. 289 (2006) 372-383
64. Mattar P., Britz O., Johannes C., Nieto M., Ma L., Rebeyka A., Klenin N., Polleux F., Guillemot F., and Schuurmans C. A screen for downstream effectors of Neurogenin2 in the embryonic neocortex. Dev. Biol. 273 (2004) 373-389
65. 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
66. Mirnics K., and Pevsner J. Progress in the use of microarray technology to study the neurobiology of disease. Nat. Neurosci. 7 (2004) 434-439
67. Miyata T. Asymmetric cell division during brain morphogenesis. Prog. Mol. Subcell. Biol 45 (2007) 121-142
68. Miyata T., Kawaguchi A., Okano H., and Ogawa M. Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 31 (2001) 727-741
69. 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
70. Mizuguchi R., Sugimori M., Takebayashi H., Kosako H., Nagao M., Yoshida S., Nabeshima Y., Shimamura K., and Nakafuku M. Combinatorial roles of olig2 and neurogenin2 in the coordinated induction of pan-neuronal and subtype-specific properties of motoneurons. Neuron 31 (2001) 757-771
71. Mizutani K., Yoon K., Dang L., Tokunaga A., and Gaiano N. Differential Notch signalling distinguishes neural stem cells from intermediate progenitors. Nature 449 (2007) 351-355
72. Muhlfriedel S., Kirsch F., Gruss P., Chowdhury K., and Stoykova A. Novel genes differentially expressed in cortical regions during late neurogenesis. Eur. J. Neurosci. 26 (2007) 33-50
73. Mukouyama Y.S., Deneen B., Lukaszewicz A., Novitch B.G., Wichterle H., Jessell T.M., and Anderson D.J. Olig2+ neuroepithelial motoneuron progenitors are not multipotent stem cells in vivo. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 1551-1556
74. Nieto M., Schuurmans C., Britz O., and Guillemot F. Neural bHLH genes control the neuronal versus glial fate decision in cortical progenitors. Neuron 29 (2001) 401-413
75. Nieto M., Monuki E.S., Tang H., Imitola J., Haubst N., Khoury S.J., Cunningham J., Gotz M., and Walsh C.A. Expression of Cux-1 and Cux-2 in the subventricular zone and upper layers II-IV of the cerebral cortex. J. Comp. Neurol. 479 (2004) 168-180
76. Nikoletopoulou V., Plachta N.D., Allen N., Pinto L., Götz M., and Barde Y.A. Neurotrophin receptor-mediated death of misspecified neurons generated from embryonic stem cells lacking Pax6. Cell Stem Cells 1 (2007) 529-540
77. 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
78. 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
79. Nolte C., Matyash M., Pivneva T., Schipke C.G., Ohlemeyer C., Hanisch U.K., Kirchhoff F., and Kettenmann H. GFAP promoter-controlled EGFP-expressing transgenic mice: a tool to visualize astrocytes and astrogliosis in living brain tissue. Glia 33 (2001) 72-86
80. Ohba H., Chiyoda T., Endo E., Yano M., Hayakawa Y., Sakaguchi M., Darnell R.B., Okano H.J., and Okano H. Sox21 is a repressor of neuronal differentiation and is antagonized by YB-1. Neurosci. Lett. 358 (2004) 157-160
81. Olenik C., Aktories K., and Meyer D.K. Differential expression of the small GTP-binding proteins RhoA, RhoB, Cdc42u and Cdc42b in developing rat neocortex. Brain Res. 70 (1999) 9-17
82. Paul Horton K.-J.P., Takeshi O., and Kenta Nakai. Protein subcellular localization prediction with WoLF PSORT. Proceedings of the 4th Annual Asia Pacific Bioinformatics Conference APBC06, Taipei, Taiwan (2006) 39-48
83. Petryniak M.A., Potter G.B., Rowitch D.H., and Rubenstein J.L. Dlx1 and Dlx2 control neuronal versus oligodendroglial cell fate acquisition in the developing forebrain. Neuron 55 (2007) 417-433
84. Pinto L., and Gotz M. Radial glial cell heterogeneity-the source of diverse progeny in the CNS. Prog. Neurobiol. 83 (2007) 2-23
85. 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
86. Ramalho-Santos M., Yoon S., Matsuzaki Y., Mulligan R.C., and Melton D.A. "Stemness": transcriptional profiling of embryonic and adult stem cells. Science 298 (2002) 597-600
87. Rao M.S., and Mayer-Proschel M. Glial-restricted precursors are derived from multipotent neuroepithelial stem cells. Dev. Biol. 188 (1997) 48-63
88. Reinhardt-Maelicke S., Cleeves V., Kindler-Rohrborn A., and Rajewsky M.F. Differential recognition of a set of O-acetylated gangliosides by monoclonal antibodies RB13-2, D1.1, and JONES during rat brain development. Brain Res. Dev. Brain Res. 51 (1990) 279-282
89. Russ A.P., Wattler S., Colledge W.H., Aparicio S.A., Carlton M.B., Pearce J.J., Barton S.C., Surani M.A., Ryan K., Nehls M.C., Wilson V., and Evans M.J. Eomesodermin is required for mouse trophoblast development and mesoderm formation. Nature 404 (2000) 95-99
90. Schreiber J., Enderich J., Sock E., Schmidt C., Richter-Landsberg C., and Wegner M. Redundancy of class III POU proteins in the oligodendrocyte lineage. J. Biol. Chem. 272 (1997) 32286-32293
91. Schuurmans C., Armant O., Nieto M., Stenman J.M., Britz O., Klenin N., Brown C., Langevin L.M., Seibt J., Tang H., Cunningham J.M., Dyck R., Walsh C., Campbell K., Polleux F., and Guillemot F. Sequential phases of cortical specification involve Neurogenin-dependent and -independent pathways. EMBO J. 23 (2004) 2892-2902
92. Shen Q., Wang Y., Dimos J.T., Fasano C.A., Phoenix T.N., Lemischka I.R., Ivanova N.B., Stifani S., Morrisey E.E., and Temple S. The timing of cortical neurogenesis is encoded within lineages of individual progenitor cells. Nat. Neurosci. 9 (2006) 743-751
93. Sif S., Stukenberg P.T., Kirschner M.W., and Kingston R.E. Mitotic inactivation of a human SWI/SNF chromatin remodeling complex. Genes Dev. 12 (1998) 2842-2851
94. Simone C. SWI/SNF: the crossroads where extracellular signaling pathways meet chromatin. J. Cell. Physiol. 207 (2006) 309-314
95. Skerjanc I.S., and Wilton S. Myocyte enhancer factor 2C upregulates MASH-1 expression and induces neurogenesis in P19 cells. FEBS Lett. 472 (2000) 53-56
96. Stoykova A., Treichel D., Hallonet M., and Gruss P. Pax6 modulates the dorsoventral patterning of the mammalian telencephalon. J. Neurosci. 20 (2000) 8042-8050
97. Strathmann F.G., Wang X., and Mayer-Proschel M. Identification of two novel glial-restricted cell populations in the embryonic telencephalon arising from unique origins. BMC Dev. Biol. 7 (2007) 33
98. Stuart J.M., Segal E., Koller D., and Kim S.K. A gene-coexpression network for global discovery of conserved genetic modules. Science 302 (2003) 249-255
99. Sugimori M., Nagao M., Bertrand N., Parras C.M., Guillemot F., and Nakafuku M. Combinatorial actions of patterning and HLH transcription factors in the spatiotemporal control of neurogenesis and gliogenesis in the developing spinal cord. Development 134 (2007) 1617-1629
100. Sun Y., Nadal-Vicens M., Misono S., Lin M.Z., Zubiaga A., Hua X., Fan G., and Greenberg M.E. Neurogenin promotes neurogenesis and inhibits glial differentiation by independent mechanisms. Cell 104 (2001) 365-376
101. Suzuki A., and Ohno S. The PAR-aPKC system: lessons in polarity. J. Cell Sci. 119 (2006) 979-987
102. Takeichi M. The cadherin superfamily in neuronal connections and interactions. Nat. Rev. Neurosci. 8 (2007) 11-20
103. 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
104. Tarabykin V., Stoykova A., Usman N., and Gruss P. Cortical upper layer neurons derive from the subventricular zone as indicated by Svet1 gene expression. Development 128 (2001) 1983-1993
105. Tokunaga A., Kohyama J., Yoshida T., Nakao K., Sawamoto K., and Okano H. Mapping spatio-temporal activation of Notch signaling during neurogenesis and gliogenesis in the developing mouse brain. J. Neurochem. 90 (2004) 142-154
106. 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
107. Tripodi M., Filosa A., Armentano M., and Studer M. The COUP-TF nuclear receptors regulate cell migration in the mammalian basal forebrain. Development 131 (2004) 6119-6129
108. Walsh C. Cell lineage and regional specification in the mammalian neocortex. Perspect Dev. Neurobiol. 1 (1993) 75-80
109. Weigmann A., Corbeil D., Hellwig A., and 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. U. S. A. 94 (1997) 12425-12430
110. Werling U., and Schorle H. Transcription factor gene AP-2 gamma essential for early murine development. Mol. Cell. Biol. 22 (2002) 3149-3156
111. Williams B.P., and Price J. Evidence for multiple precursor cell-types in the embryonic rat cerebral cortex. Neuron 14 (1995) 1181-1188
112. Williams B.P., Read J., and Price J. The generation of neurons and oligodendrocytes from a common precursor cell. Neuron 7 (1991) 685-693
113. Wu S.X., Goebbels S., Nakamura K., Nakamura K., Kometani K., Minato N., Kaneko T., Nave K.A., and Tamamaki N. Pyramidal neurons of upper cortical layers generated by NEX-positive progenitor cells in the subventricular zone. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 17172-17177
114. Wurmbach E., Gonzalez-Maeso J., Yuen T., Ebersole B.J., Mastaitis J.W., Mobbs C.V., and Sealfon S.C. Validated genomic approach to study differentially expressed genes in complex tissues. Neurochem. Res. 27 (2002) 1027-1033
115. Yoon K., and Gaiano N. Notch signaling in the mammalian central nervous system: insights from mouse mutants. Nat. Neurosci. 8 (2005) 709-715
116. Young K.M., Merson T.D., Sotthibundhu A., Coulson E.J., and Bartlett P.F. p75 neurotrophin receptor expression defines a population of BDNF-responsive neurogenic precursor cells. J. Neurosci. 27 (2007) 5146-5155
117. Yue T., Xian K., Hurlock E., Xin M., Kernie S.G., Parada L.F., and Lu Q.R. A critical role for dorsal progenitors in cortical myelination. J. Neurosci. 26 (2006) 1275-1280
118. Zhou Q., and Anderson D.J. The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 109 (2002) 61-73
119. Zimmer C., Tiveron M.C., Bodmer R., and Cremer H. Dynamics of Cux2 expression suggests that an early pool of SVZ precursors is fated to become upper cortical layer neurons. Cereb. Cortex 14 (2004) 1408-1420