A star is born: New insights into the mechanism of astrogenesis

Cellular and Molecular Life Sciences

Volumn 71, Issue 3, 2014, Pages 433-447

  Kanski, Regina ^a   Van Strien, Miriam E ^a   Van Tijn, Paula ^a,b   Hol, Elly M ^a,c  

^a NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^b HUBRECHT INSTITUTE   (Netherlands)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Astrocyte differentiation; Development; GFAP; Neural stem cell; Notch signaling

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DNA METHYLTRANSFERASE 1; JANUS KINASE; NOTCH RECEPTOR; REPRESSOR ELEMENT 1 SILENCING TRANSCRIPTION FACTOR; STAT PROTEIN; STAT3 PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ASTROCYTE; ASTROGENESIS; BINDING SITE; CELL DIFFERENTIATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; EPIGENETICS; GENE EXPRESSION; GLIA CELL; HUMAN; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PROTEIN FUNCTION; PROTEIN METHYLATION; PROTEIN SYNTHESIS INHIBITION; REGULATOR GENE; REVIEW; SIGNAL TRANSDUCTION;

ASTROCYTES; BRAIN; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLIAL FIBRILLARY ACIDIC PROTEIN; HUMANS; JANUS KINASES; MODELS, BIOLOGICAL; NEURAL STEM CELLS; NEUROGENESIS; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION;

EID: 84892781337     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-013-1435-9     Document Type: Review

References (110)

1. Sofroniew MV, Vinters HV (2010) Astrocytes: biology and pathology. Acta Neuropathol 119:7-35. doi: 10.1007/s00401-009-0619-8
2. Ullian EM, Sapperstein SK, Christopherson KS, Barres BA (2001) Control of synapse number by glia. Science 291:657-661. doi: 10.1126/science.291.5504.657 (Pubitemid 32150425)
3. Eroglu C, Barres BA (2010) Regulation of synaptic connectivity by glia. Nature 468:223-231. doi: 10.1038/nature09612
4. Freeman MR (2010) Specification and morphogenesis of astrocytes. Science 330:774-778. doi: 10.1126/science.1190928
5. Derouet D, Rousseau F, Alfonsi F et al (2004) Neuropoietin, a new IL-6-related cytokine signaling through the ciliary neurotrophic factor receptor. Proc Natl Acad Sci USA 101:4827-4832. doi: 10.1073/pnas.0306178101 (Pubitemid 38469162)
6. Uemura A, Takizawa T, Ochiai W et al (2002) Cardiotrophin-like cytokine induces astrocyte differentiation of fetal neuroepithelial cells via activation of STAT3. Cytokine 18:1-7 (Pubitemid 34762072)
7. Cheng P-Y, Lin Y-P, Chen Y-L et al (2011) Interplay between SIN3A and STAT3 mediates chromatin conformational changes and GFAP expression during cellular differentiation. PLoS One 6:e22018. doi: 10.1371/journal.pone.0022018
8. Sun Y, Nadal-Vicens M, Misono S et al (2001) Neurogenin promotes neurogenesis and inhibits glial differentiation by independent mechanisms. Cell 104:365-376 (Pubitemid 32206457)
9. He F, Ge W, Martinowich K et al (2005) A positive autoregulatory loop of Jak-STAT signaling controls the onset of astrogliogenesis. Nat Neurosci 8:616-625. doi: 10.1038/nn1440 (Pubitemid 40594203)
10. Nieto M, Schuurmans C, Britz O, Guillemot F (2001) Neural bHLH genes control the neuronal versus glial fate decision in cortical progenitors. Neuron 29:401-413 (Pubitemid 32206479)
11. Tomita K, Moriyoshi K, Nakanishi S et al (2000) Mammalian achaete-scute and atonal homologs regulate neuronal versus glial fate determination in the central nervous system. EMBO J 19:5460-5472. doi: 10.1093/emboj/19.20.5460
12. Takizawa T, Nakashima K, Namihira M et al (2001) DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain. Dev Cell 1:749-758 (Pubitemid 33586130)
13. Fan G, Martinowich K, Chin MH et al (2005) DNA methylation controls the timing of astrogliogenesis through regulation of JAK-STAT signaling. Development 132:3345-3356. doi: 10.1242/dev.01912 (Pubitemid 41246111)
14. Namihira M, Nakashima K, Taga T (2004) Developmental stage dependent regulation of DNA methylation and chromatin modification in a immature astrocyte specific gene promoter. FEBS Lett 572:184-188. doi: 10.1016/j.febslet.2004.07. 029 (Pubitemid 39092533)
15. Jones PL, Veenstra GJ, Wade PA et al (1998) Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat Genet 19:187-191. doi: 10.1038/561 (Pubitemid 28248804)
16. Icardi L, Mori R, Gesellchen V et al (2012) The Sin3a repressor complex is a master regulator of STAT transcriptional activity. Proc Natl Acad Sci USA 109:12058-12063. doi: 10.1073/pnas.1206458109
17. Cao F, Hata R, Zhu P et al (2006) Overexpression of SOCS3 inhibits astrogliogenesis and promotes maintenance of neural stem cells. J Neurochem 98:459-470. doi: 10.1111/j.1471-4159.2006.03890.x (Pubitemid 44133150)
18. Gu F, Hata R, Ma Y-J et al (2005) Suppression of Stat3 promotes neurogenesis in cultured neural stem cells. J Neurosci Res 81:163-171. doi: 10.1002/jnr.20561 (Pubitemid 41153329)
19. Cao F, Hata R, Zhu P et al (2010) Conditional deletion of Stat3 promotes neurogenesis and inhibits astrogliogenesis in neural stem cells. Biochem Biophys Res Commun 394:843-847. doi: 10.1016/j.bbrc.2010.03.092
20. Ménard C, Hein P, Paquin A et al (2002) An essential role for a MEK-C/EBP pathway during growth factor-regulated cortical neurogenesis. Neuron 36:597-610 (Pubitemid 35346754)
21. Neel BG, Gu H, Pao L (2003) The "Shp"ing news: SH2 domain-containing tyrosine phosphatases in cell signaling. Trends Biochem Sci 28:284-293. doi: 10.1016/S0968-0004(03)00091-4 (Pubitemid 36776291)
22. Gauthier AS, Furstoss O, Araki T et al (2007) Control of CNS cell-fate decisions by SHP-2 and its dysregulation in Noonan syndrome. Neuron 54:245-262. doi: 10.1016/j.neuron.2007.03.027 (Pubitemid 46562561)
23. Ernst M, Jenkins BJ (2004) Acquiring signalling specificity from the cytokine receptor gp130. Trends Genet 20:23-32. doi: 10.1016/j.tig.2003.11.003 (Pubitemid 38032817)
24. Pruitt K, Ulkü AS, Frantz K et al (2005) Ras-mediated loss of the pro-apoptotic response protein Par-4 is mediated by DNA hypermethylation through Raf-independent and Raf-dependent signaling cascades in epithelial cells. J Biol Chem 280:23363-23370. doi: 10.1074/jbc.M503083200 (Pubitemid 40853250)
25. Maisonpierre PC, Belluscio L, Friedman B et al (1990) NT-3, BDNF, and NGF in the developing rat nervous system: parallel as well as reciprocal patterns of expression. Neuron 5:501-509 (Pubitemid 20369586)
26. Barnabé-Heider F, Miller FD (2003) Endogenously produced neurotrophins regulate survival and differentiation of cortical progenitors via distinct signaling pathways. J Neurosci 23:5149-5160 (Pubitemid 36793243)
27. Tissir F, Goffinet AM (2003) Reelin and brain development. Nat Rev Neurosci 4:496-505. doi: 10.1038/nrn1113 (Pubitemid 37280170)
28. Kwon I-S, Cho S-K, Kim M-J et al (2009) Expression of Disabled 1 suppresses astroglial differentiation in neural stem cells. Mol Cell Neurosci 40:50-61. doi: 10.1016/j.mcn.2008.08.012
29. Zhao S, Chai X, Frotscher M (2007) Balance between neurogenesis and gliogenesis in the adult hippocampus: role for Reelin. Dev Neurosci 29:84-90. doi: 10.1159/000096213 (Pubitemid 44934964)
30. Piao C-S, Li B, Zhang L-J, Zhao L-R (2012) Stem cell factor and granulocyte colony-stimulating factor promote neuronal lineage commitment of neural stem cells. Differentiation 83:17-25. doi: 10.1016/j.diff.2011.08.006
31. Wang L, Zhang ZG, Zhang RL et al (2006) Neurogenin 1 mediates erythropoietin enhanced differentiation of adult neural progenitor cells. J Cereb Blood Flow Metab 26:556-564. doi: 10.1038/sj.jcbfm.9600215
32. Alnaeeli M, Wang L, Piknova B et al (2012) Erythropoietin in brain development and beyond. Anat Res Int 2012:953264. doi: 10.1155/2012/953264
33. Sardi SP, Murtie J, Koirala S et al (2006) Presenilin-dependent ErbB4 nuclear signaling regulates the timing of astrogenesis in the developing brain. Cell 127:185-197. doi: 10.1016/j.cell.2006.07.037 (Pubitemid 44466644)
34. Fox IJ, Kornblum HI (2005) Developmental profile of ErbB receptors in murine central nervous system: implications for functional interactions. J Neurosci Res 79:584-597. doi: 10.1002/jnr.20381 (Pubitemid 40476437)
35. Mei L, Xiong W-C (2008) Neuregulin 1 in neural development, synaptic plasticity and schizophrenia. Nat Rev Neurosci 9:437-452. doi: 10.1038/nrn2392 (Pubitemid 351704944)
36. Kouzarides T (2007) Chromatin modifications and their function. Cell 128:693-705. doi: 10.1016/j.cell.2007.02.005 (Pubitemid 46273577)
37. Hirabayashi Y, Suzki N, Tsuboi M et al (2009) Polycomb limits the neurogenic competence of neural precursor cells to promote astrogenic fate transition. Neuron 63:600-613. doi: 10.1016/j.neuron.2009.08.021
38. Schwartz YB, Pirrotta V (2007) Polycomb silencing mechanisms and the management of genomic programmes. Nat Rev Genet 8:9-22. doi: 10.1038/nrg1981 (Pubitemid 46006046)
39. Yuan Z-L, Guan Y-J, Chatterjee D, Chin YE (2005) Stat3 dimerization regulated by reversible acetylation of a single lysine residue. Science 307:269-273. doi: 10.1126/science.1105166 (Pubitemid 40116244)
40. Wilczynska KM, Singh SK, Adams B et al (2009) Nuclear factor I isoforms regulate gene expression during the differentiation of human neural progenitors to astrocytes. Stem Cells 27:1173-1181. doi: 10.1002/stem.35
41. Cebolla B, Vallejo M (2006) Nuclear factor-I regulates glial fibrillary acidic protein gene expression in astrocytes differentiated from cortical precursor cells. J Neurochem 97:1057-1070. doi: 10.1111/j.1471-4159.2006.03804.x
42. Namihira M, Kohyama J, Semi K et al (2009) Committed neuronal precursors confer astrocytic potential on residual neural precursor cells. Dev Cell 16:245-255. doi: 10.1016/j.devcel.2008.12.014
43. Das Neves L, Duchala CS, Tolentino-Silva F et al (1999) Disruption of the murine nuclear factor I-A gene (Nfia) results in perinatal lethality, hydrocephalus, and agenesis of the corpus callosum. Proc Natl Acad Sci USA 96:11946-11951 (Pubitemid 29502838)
44. Steele-Perkins G, Plachez C, Butz KG et al (2005) The transcription factor gene Nfib is essential for both lung maturation and brain development. Mol Cell Biol 25:685-698. doi: 10.1128/MCB.25.2.685-698.2005 (Pubitemid 40096589)
45. Shu T, Butz KG, Plachez C et al (2003) Abnormal development of forebrain midline glia and commissural projections in Nfia knock-out mice. J Neurosci 23:203-212 (Pubitemid 36050420)
46. Song M-R, Ghosh A (2004) FGF2-induced chromatin remodeling regulates CNTF-mediated gene expression and astrocyte differentiation. Nat Neurosci 7:229-235. doi: 10.1038/nn1192 (Pubitemid 38280446)
47. Irmady K, Zechel S, Unsicker K (2011) Fibroblast growth factor 2 regulates astrocyte differentiation in a region-specific manner in the hindbrain. Glia 59:708-719. doi: 10.1002/glia.21141
48. Nishioka K, Rice JC, Sarma K et al (2002) PR-Set7 is a nucleosome-specific methyltransferase that modifies lysine 20 of histone H4 and is associated with silent chromatin. Mol Cell 9:1201-1213 (Pubitemid 34722300)
49. Haskell GT, LaMantia A-S (2005) Retinoic acid signaling identifies a distinct precursor population in the developing and adult forebrain. J Neurosci 25:7636-7647. doi: 10.1523/JNEUROSCI.0485-05.2005 (Pubitemid 41170620)
50. Mizee MR, Wooldrik D, Lakeman KAM et al (2013) Retinoic acid induces blood-brain barrier development. J Neurosci 33:1660-1671. doi: 10.1523/JNEUROSCI.1338-12.2013
51. Rossant J, Zirngibl R, Cado D et al (1991) Expression of a retinoic acid response element-hsplacZ transgene defines specific domains of transcriptional activity during mouse embryogenesis. Genes Dev 5:1333-1344 (Pubitemid 21906042)
52. Jepsen K, Solum D, Zhou T et al (2007) SMRT-mediated repression of an H3K27 demethylase in progression from neural stem cell to neuron. Nature 450:415-419. doi: 10.1038/nature06270 (Pubitemid 350126746)
53. Asano H, Aonuma M, Sanosaka T et al (2009) Astrocyte differentiation of neural precursor cells is enhanced by retinoic acid through a change in epigenetic modification. Stem Cells 27:2744-2752. doi: 10.1002/stem.176
54. Malatesta P, Hartfuss E, Gotz M (2000) Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 127:5253-5263 (Pubitemid 32049182)
55. Guruharsha KG, Kankel MW, Artavanis-Tsakonas S (2012) The Notch signalling system: recent insights into the complexity of a conserved pathway. Nat Rev Genet 13:654-666. doi: 10.1038/nrg3272
56. Kopan R, Ilagan MXG (2009) The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 137:216-233. doi: 10.1016/j.cell.2009. 03.045
57. Yoshimatsu T, Kawaguchi D, Oishi K et al (2006) Non-cell-autonomous action of STAT3 in maintenance of neural precursor cells in the mouse neocortex. Development 133:2553-2563. doi: 10.1242/dev.02419 (Pubitemid 44123404)
58. Kamakura S, Oishi K, Yoshimatsu T et al (2004) Hes binding to STAT3 mediates crosstalk between Notch and JAK-STAT signalling. Nat Cell Biol 6:547-554. doi: 10.1038/ncb1138 (Pubitemid 38786598)
59. Piper M, Barry G, Hawkins J et al (2010) NFIA controls telencephalic progenitor cell differentiation through repression of the Notch effector Hes1. J Neurosci 30:9127-9139. doi: 10.1523/JNEUROSCI.6167-09.2010
60. Monuki ES, Porter FD, Walsh CA (2001) Patterning of the dorsal telencephalon and cerebral cortex by a roof plate-Lhx2 pathway. Neuron 32:591-604 (Pubitemid 33145194)
61. Subramanian L, Sarkar A, Shetty AS et al (2011) Transcription factor Lhx2 is necessary and sufficient to suppress astrogliogenesis and promote neurogenesis in the developing hippocampus. Proc Natl Acad Sci USA 108:E265-E274. doi: 10.1073/pnas.1101109108
62. Brancaccio M, Pivetta C, Granzotto M et al (2010) Emx2 and Foxg1 inhibit gliogenesis and promote neuronogenesis. Stem Cells 28:1206-1218. doi: 10.1002/stem.443
63. Gangemi RMR, Daga A, Muzio L et al (2006) Effects of Emx2 inactivation on the gene expression profile of neural precursors. Eur J Neurosci 23:325-334. doi: 10.1111/j.1460-9568.2005.04559.x
64. Stolt CC, Lommes P, Sock E et al (2003) The Sox9 transcription factor determines glial fate choice in the developing spinal cord. Genes Dev 17:1677-1689. doi: 10.1101/gad.259003 (Pubitemid 36828793)
65. Kang P, Lee HK, Glasgow SM et al (2012) Sox9 and NFIA coordinate a transcriptional regulatory cascade during the initiation of gliogenesis. Neuron 74:79-94. doi: 10.1016/j.neuron.2012.01.024
66. Welcker M, Clurman BE (2008) FBW7 ubiquitin ligase: a tumour suppressor at the crossroads of cell division, growth and differentiation. Nat Rev Cancer 8:83-93. doi: 10.1038/nrc2290 (Pubitemid 351161321)
67. Hoeck JD, Jandke A, Blake SM et al (2010) Fbw7 controls neural stem cell differentiation and progenitor apoptosis via Notch and c-Jun. Nat Neurosci 13:1365-1372. doi: 10.1038/nn.2644
68. Matsumoto A, Onoyama I, Sunabori T et al (2011) Fbxw7-dependent degradation of Notch is required for control of "stemness" and neuronal-glial differentiation in neural stem cells. J Biol Chem 286:13754-13764. doi: 10.1074/jbc.M110.194936
69. Moore KA, Hollien J (2012) The unfolded protein response in secretory cell function. Annu Rev Genet 46:165-183. doi: 10.1146/annurev-genet-110711- 155644
70. Saito A, Kanemoto S, Kawasaki N et al (2012) Unfolded protein response, activated by OASIS family transcription factors, promotes astrocyte differentiation. Nat Commun 3:967. doi: 10.1038/ncomms1971
71. Barnabé-Heider F, Wasylnka JA, Fernandes KJL et al (2005) Evidence that embryonic neurons regulate the onset of cortical gliogenesis via cardiotrophin-1. Neuron 48:253-265. doi: 10.1016/j.neuron.2005.08.037 (Pubitemid 41476359)
72. Bugga L, Gadient RA, Kwan K et al (1998) Analysis of neuronal and glial phenotypes in brains of mice deficient in leukemia inhibitory factor. J Neurobiol 36:509-524 (Pubitemid 28402557)
73. Miller FD, Gauthier AS (2007) Timing is everything: making neurons versus glia in the developing cortex. Neuron 54:357-369. doi: 10.1016/j.neuron.2007. 04.019 (Pubitemid 46659814)
74. Bonni A, Sun Y, Nadal-Vicens M et al (1997) Regulation of gliogenesis in the central nervous system by the JAK-STAT signaling pathway. Science 278:477-483 (Pubitemid 27454434)
75. Stahl N, Yancopoulos GD (1994) The tripartite CNTF receptor complex: activation and signaling involves components shared with other cytokines. J Neurobiol 25:1454-1466. doi: 10.1002/neu.480251111 (Pubitemid 24325068)
76. Nakashima K, Yanagisawa M, Arakawa H, Taga T (1999) Astrocyte differentiation mediated by LIF in cooperation with BMP2. FEBS Lett 457:43-46 (Pubitemid 29388176)
77. Bonaguidi MA, McGuire T, Hu M et al (2005) LIF and BMP signaling generate separate and discrete types of GFAP-expressing cells. Development 132:5503-5514. doi: 10.1242/dev.02166 (Pubitemid 43125877)
78. Gross RE, Mehler MF, Mabie PC et al (1996) Bone morphogenetic proteins promote astroglial lineage commitment by mammalian subventricular zone progenitor cells. Neuron 17:595-606 (Pubitemid 26365340)
79. Li W, Cogswell CA, LoTurco JJ (1998) Neuronal differentiation of precursors in the neocortical ventricular zone is triggered by BMP. J Neurosci 18:8853-8862 (Pubitemid 28491750)
80. Nakashima K, Takizawa T, Ochiai W et al (2001) BMP2-mediated alteration in the developmental pathway of fetal mouse brain cells from neurogenesis to astrocytogenesis. Proc Natl Acad Sci USA 98:5868-5873. doi: 10.1073/pnas. 101109698 (Pubitemid 32435734)
81. Fukuda S, Taga T (2005) Cell fate determination regulated by a transcriptional signal network in the developing mouse brain. Anat Sci Int 80:12-18. doi: 10.1111/j.1447-073x.2005.00097.x (Pubitemid 40425962)
82. Ortega JA, Alcántara S (2010) BDNF/MAPK/ERK-induced BMP7 expression in the developing cerebral cortex induces premature radial glia differentiation and impairs neuronal migration. Cereb Cortex 20:2132-2144. doi: 10.1093/cercor/bhp275
83. Miller MW (2003) Expression of transforming growth factor-beta in developing rat cerebral cortex: effects of prenatal exposure to ethanol. J Comp Neurol 460:410-424. doi: 10.1002/cne.10658 (Pubitemid 36514618)
84. De Sampaio e Spohr TCL, Martinez R, da Silva EF et al (2002) Neuro-glia interaction effects on GFAP gene: a novel role for transforming growth factor-beta1. Eur J Neurosci 16:2059-2069 (Pubitemid 35454250)
85. Stipursky J, Gomes FCA (2007) TGF-beta1/SMAD signaling induces astrocyte fate commitment in vitro: implications for radial glia development. Glia 55:1023-1033. doi: 10.1002/glia.20522 (Pubitemid 47066742)
86. Stipursky J, Francis D, Gomes FCA (2012) Activation of MAPK/PI3 K/SMAD pathways by TGF-β(1) controls differentiation of radial glia into astrocytes in vitro. Dev Neurosci 34:68-81. doi: 10.1159/000338108
87. Yamaguchi K, Shirakabe K, Shibuya H et al (1995) Identification of a member of the MAPKKK family as a potential mediator of TGF-beta signal transduction. Science 270:2008-2011 (Pubitemid 26097194)
88. Vallejo M (2009) PACAP signaling to DREAM: a cAMP-dependent pathway that regulates cortical astrogliogenesis. Mol Neurobiol 39:90-100. doi: 10.1007/s12035-009-8055-2
89. Conaco C, Otto S, Han J-J, Mandel G (2006) Reciprocal actions of REST and a microRNA promote neuronal identity. Proc Natl Acad Sci USA 103:2422-2427. doi: 10.1073/pnas.0511041103 (Pubitemid 43271685)
90. Lunyak VV, Burgess R, Prefontaine GG et al (2002) Corepressor-dependent silencing of chromosomal regions encoding neuronal genes. Science 298:1747-1752. doi: 10.1126/science.1076469 (Pubitemid 35404110)
91. Abrajano JJ, Qureshi IA, Gokhan S et al (2009) Differential deployment of REST and CoREST promotes glial subtype specification and oligodendrocyte lineage maturation. PLoS One 4:e7665. doi: 10.1371/journal.pone.0007665
92. Kohyama J, Sanosaka T, Tokunaga A et al (2010) BMP-induced REST regulates the establishment and maintenance of astrocytic identity. J Cell Biol 189:159-170. doi: 10.1083/jcb.200908048
93. Huang Y, Myers SJ, Dingledine R (1999) Transcriptional repression by REST: recruitment of Sin3A and histone deacetylase to neuronal genes. Nat Neurosci 2:867-872. doi: 10.1038/13165 (Pubitemid 30602598)
94. Verwer RWH, Sluiter AA, Balesar RA et al (2007) Mature astrocytes in the adult human neocortex express the early neuronal marker doublecortin. Brain 130:3321-3335. doi: 10.1093/brain/awm264 (Pubitemid 350209078)
95. Laywell ED, Kearns SM, Zheng T et al (2005) Neuron-to-astrocyte transition: phenotypic fluidity and the formation of hybrid asterons in differentiating neurospheres. J Comp Neurol 493:321-333. doi: 10.1002/cne.20722 (Pubitemid 41677465)
96. Kamphuis W, Mamber C, Moeton M et al (2012) GFAP isoforms in adult mouse brain with a focus on neurogenic astrocytes and reactive astrogliosis in mouse models of Alzheimer disease. PLoS One 7:e42823. doi: 10.1371/journal.pone. 0042823
97. Doetsch F, Caillé I, Lim DA et al (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97:703-716. doi: 10.1016/S0092-8674(00)80783-7 (Pubitemid 29278045)
98. Calegari F, Huttner WB (2003) An inhibition of cyclin-dependent kinases that lengthens, but does not arrest, neuroepithelial cell cycle induces premature neurogenesis. J Cell Sci 116:4947-4955. doi: 10.1242/jcs.00825 (Pubitemid 38016701)
99. Tury A, Mairet-Coello G, DiCicco-Bloom E (2011) The cyclin-dependent kinase inhibitor p57Kip2 regulates cell cycle exit, differentiation, and migration of embryonic cerebral cortical precursors. Cereb Cortex 21:1840-1856. doi: 10.1093/cercor/bhq254
100. Andreu-Agullo C, Maurin T, Thompson CB, Lai EC (2012) Ars2 maintains neural stem-cell identity through direct transcriptional activation of Sox2. Nature 481:195-198. doi: 10.1038/nature10712
101. Zencak D, Lingbeek M, Kostic C et al (2005) Bmi1 loss produces an increase in astroglial cells and a decrease in neural stem cell population and proliferation. J Neurosci 25:5774-5783. doi: 10.1523/JNEUROSCI.3452-04.2005 (Pubitemid 40847890)
102. Rowitch DH, Kriegstein AR (2010) Developmental genetics of vertebrate glial - cell specification. Nature 468:214-222. doi: 10.1038/nature09611
103. Ge W-P, Miyawaki A, Gage FH et al (2012) Local generation of glia is a major astrocyte source in postnatal cortex. Nature 484:376-380. doi: 10.1038/nature10959
104. Martini S, Bernoth K, Main H et al (2013) A critical role for Sox9 in Notch-induced astrogliogenesis and stem cell maintenance. Stem Cells 31:741-751. doi: 10.1002/stem.1320
105. Krencik R, Weick JP, Liu Y et al (2011) Specification of transplantable astroglial subtypes from human pluripotent stem cells. Nat Biotechnol 29:528-534. doi: 10.1038/nbt.1877
106. Emdad L, D'Souza SL, Kothari HP et al (2012) Efficient differentiation of human embryonic and induced pluripotent stem cells into functional astrocytes. Stem Cells Dev 21:404-410. doi: 10.1089/scd.2010.0560
107. Shaltouki A, Peng J, Liu Q et al (2013) Efficient generation of astrocytes from human pluripotent stem cells in defined conditions. Stem Cells. doi: 10.1002/stem.1334
108. Ideguchi M, Shinoyama M, Gomi M et al (2008) Immune or inflammatory response by the host brain suppresses neuronal differentiation of transplanted ES cell-derived neural precursor cells. J Neurosci Res 86:1936-1943. doi: 10.1002/jnr.21652
109. Nakanishi M, Niidome T, Matsuda S et al (2007) Microglia-derived interleukin-6 and leukaemia inhibitory factor promote astrocytic differentiation of neural stem/progenitor cells. Eur J Neurosci 25:649-658. doi: 10.1111/j.1460-9568.2007.05309.x
110. Faijerson J, Tinsley RB, Apricó K et al (2006) Reactive astrogliosis induces astrocytic differentiation of adult neural stem/progenitor cells in vitro. J Neurosci Res 84:1415-1424. doi: 10.1002/jnr.21044 (Pubitemid 44683136)