Reactive astrocytes as neural stem or progenitor cells: In vivo lineage, In vitro potential, and Genome-wide expression analysis

GLIA

Volumn 63, Issue 8, 2015, Pages 1452-1468

  Götz, Magdalena ^a,b,c   Sirko, Swetlana ^a,b   Beckers, Johannes ^b,d,e   Irmler, Martin ^b  

^a UNIVERSITY OF MUNICH   (Germany)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

^c LMU ^*  (Germany)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^e GERMAN CENTER FOR DIABETES RESEARCH DZD   (Germany)

Author keywords

Brain injury; Lineage; Potential; Radial glial cells; Self renewal; Transcriptome

Indexed keywords

ASTROCYTE; BRAIN REGION; CELL EXPANSION; CELL LINEAGE; CELL RENEWAL; CENTRAL NERVOUS SYSTEM; EMBRYO DEVELOPMENT; EPENDYMA CELL; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC ASSOCIATION; GLIA CELL; HUMAN; HYPOXIC ISCHEMIC ENCEPHALOPATHY; IN VITRO STUDY; IN VIVO STUDY; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEURAL STEM CELL TRANSPLANTATION; NEUROEPITHELIUM CELL; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROGENY; REACTIVE ASTROCYTE; REVIEW; STEM CELL CULTURE; STEM CELL NICHE; ANIMAL; EMBRYOLOGY; NERVE CELL; PHYSIOLOGY;

ANIMALS; ASTROCYTES; CENTRAL NERVOUS SYSTEM; HUMANS; NEURAL STEM CELLS; NEURONS;

EID: 84930865559     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22850     Document Type: Review

References (163)

1. Amat JA, Ishiguro H, Nakamura K, Norton WT. 1996. Phenotypic diversity and kinetics of proliferating microglia and astrocytes following cortical stab wounds. Glia 16:368-382.
2. Anderson SA, Kaznowski CE, Horn C, Rubenstein JL, McConnell SK. 2002. Distinct origins of neocortical projection neurons and interneurons in vivo. Cereb Cortex 12:702-709.
3. Arendt T. 2012. Cell cycle activation and aneuploid neurons in Alzheimer's disease. Mol Neurobiol 46:125-135.
4. Babu H, Cheung G, Kettenmann H, Palmer TD, Kempermann G. 2007. Enriched monolayer precursor cell cultures from micro-dissected adult mouse dentate gyrus yield functional granule cell-like neurons. PLoS One 2:e388.
5. Bardehle S, Krüger M, Buggenthin F, Schwausch J, Ninkovic J, Clevers H, Snippert HJ, Theis FJ, Meyer-Luehmann M, Bechmann I, Dimou L, Götz M. 2013. Live imaging of astrocyte responses to acute injury reveals selective juxtavascular proliferation. Nat Neurosci 16:580-586.
6. Barnabé-Heider F, Göritz C, Sabelström H, Takebayashi H, Pfrieger FW, Meletis K, Frisén J. 2010. Origin of new glial cells in intact and injured adult spinal cord. Cell Stem Cell 7:470-482.
7. Barry DS, McDermott KW. 2005. Differentiation of radial glia from radial precursor cells and transformation into astrocytes in the developing rat spinal cord. Glia 50:187-197.
8. Battiste J, Helms AW, Kim EJ, Savage TK, Lagace DC, Mandyam CD, Eisch AJ, Miyoshi G, Johnson JE. 2007. Ascl1 defines sequentially generated lineage-restricted neuronal and oligodendrocyte precursor cells in the spinal cord. Development 134:285-293.
9. Beckervordersandforth R, Tripathi P, Ninkovic J, Bayam E, Lepier A, Stempfhuber B, Kirchhoff F, Hirrlinger J, Haslinger A, Lie DC, Beckers J, Yoder B, Irmler M, Götz M. 2010. In vivo fate mapping and expression analysis reveals molecular hallmarks of prospectively isolated adult neural stem cells. Cell Stem Cell 7:744-758.
10. Benner EJ, Luciano D, Jo R, Abdi K, Paez-Gonzalez P, Sheng H, Warner DS, Liu C, Eroglu C, Kuo CT. 2013. Protective astrogenesis from the SVZ niche after injury is controlled by Notch modulator Thbs4. Nature 497:369-373.
11. Bi B, Salmaso N, Komitova M, Simonini MV, Silbereis J, Cheng E, Kim J, Luft S, Ment LR, Horvath TL, Schwartz ML, Vaccarino FM. 2011. Cortical glial fibrillary acidic protein-positive cells generate neurons after perinatal hypoxic injury. J Neurosci 31:9205-9021.
12. Bonaguidi MA, Wheeler MA, Shapiro JS, Stadel RP, Sun GJ, Ming GL, Song H. 2011. In vivo clonal analysis reveals self-renewing and multipotent adult neural stem cell characteristics. Cell 145:1142-1155.
13. Borrell V, Götz M. 2014. Role of radial glial cells in cerebral cortex folding. Curr Opin Neurobiol 27:39-46.
14. Brill MS, Ninkovic J, Winpenny E, Hodge RD, Ozen I, Yang R, Lepier A, Gascón S, Erdelyi F, Szabo G, Parras C, Guillemot F, Frotscher M, Berninger B, Hevner RF, Raineteau O, Götz M. 2009. Adult generation of glutamatergic olfactory bulb interneurons. Nat Neurosci 12:1524-1533.
15. Brilli E, Reitano E, Conti L, Conforti P, Gulino R, Consalez GG, Cesana E, Smith A, Rossi F, Cattaneo E. 2013. Neural stem cells engrafted in the adult brain fuse with endogenous neurons. Stem Cells Dev 22:538-547.
16. Bruni JE. 1998. Ependymal development, proliferation, and functions: A review. Microsc Res Tech 41:2-13.
17. Buffo A, Rite I, Tripathi P, Lepier A, Colak D, Horn AP, Mori T, Götz M. 2008. Origin and progeny of reactive gliosis: A source of multipotent cells in the injured brain. Proc Natl Acad Sci USA 105:3581-3586
18. Busch K, Klapproth K, Barile M, Flossdorf M, Holland-Letz T, Schlenner SM, Reth M, Höfer T, Rodewald HR. 2015. Fundamental properties of unperturbed haematopoiesis from stem cells in vivo. Nature 518:542-546.
19. Cahoy JD, Emery B, Kaushal A, Foo LC, Zamanian JL, Christopherson KS, Xing Y, Lubischer JL, Krieg PA, Krupenko SA, Thompson WJ, Barres BA. 2008. A transcriptome database for astrocytes, neurons, and oligodendrocytes: A new resource for understanding brain development andfunction. J Neurosci 28:264-278.
20. Calzolari F, Michel J, Baumgart EV, Theis F, Götz M, Ninkovic J. 2015. Fast clonal expansion and limited neural stem cell self-renewal in the adult subependymal zone. Nat Neurosci 18:490-492.
21. Caputi A, Melzer S, Michael M, Monyer H. 2013. The long and short of GABAergic neurons. Curr Opin Neurobiol 23:179-186.
22. Carlén M, Meletis K, Göritz C, Darsalia V, Evergren E, Tanigaki K, Amendola M, Barnabé-Heider F, Yeung MS, Naldini L, Honjo T, Kokaia Z, Shupliakov O, Cassidy RM, Lindvall O, Frisén J. 2009. Forebrain ependymal cells are Notch-dependent and generate neuroblasts and astrocytes after stroke. Nat Neurosci 12:259-267.
23. Chen X, Lepier A, Berninger B, Tolkovsky AM, Herbert J. 2012. Cultured subventricular zone progenitor cells transduced with neurogenin-2 become mature glutamatergic neurons and integrate into the dentate gyrus. PLoS One 7:e31547.
24. Clapes T, Robin C. 2012. Embryonic development of hematopoietic stem cells: Implications for clinical use. Regen Med 7:349-368.
25. Codega P, Silva-Vargas V, Paul A, Maldonado-Soto AR, Deleo AM, Pastrana E, Doetsch F. 2014. Prospective identification and purification of quiescent adult neural stem cells from their in vivo niche. Neuron 82:545-559.
26. Costa MR, Ortega F, Brill MS, Beckervordersandforth R, Petrone C, Schroeder T, Götz M, Berninger B. 2011. Continuous live imaging of adult neural stem cell division and lineage progression in vitro. Development 138:1057-1068.
27. Curtis MA, Eriksson PS, Faull RL. 2007. Progenitor cells and adult neurogenesis in neurodegenerative diseases and injuries of the basal ganglia. Clin Exp Pharmacol Physiol 34:528-532.
28. De Juan Romero C, Borrell V. 2015. Co-evolution of radial glial cells and the cerebral cortex. Glia (this issue).
29. Desai AR, McConnell SK. 2000. Progressive restriction in fate potential by neural progenitors during cerebral cortical development. Development 127:2863-2872.
30. Dimou L, Gallo V. 2015. NG2-glia and their functions in the central nervous system. Glia (this issue).
31. Dimou L, Götz M. 2014. Glial cells as progenitors and stem cells: New roles in the healthy and diseased brain. Physiol Rev 94:709-737.
32. Dimou L, Simon C, Kirchhoff F, Takebayashi H, Götz M. 2008. Progeny of Olig2-expressing progenitors in the gray and white matter of the adult mouse cerebral cortex. J Neurosci 28:10434-10442.
33. Encinas JM, Michurina TV, Peunova N, Park JH, Tordo J, Peterson DA, Fishell G, Koulakov A, Enikolopov G. 2011. Division-coupled astrocytic differentiation and age-related depletion of neural stem cells in the adult hippocampus. Cell Stem Cell 8:566-579.
34. Ernst A, Alkass K, Bernard S, Salehpour M, Perl S, Tisdale J, Possnert G, Druid HJ. 2014. Neurogenesis in the striatum of the adult human brain. Cell 156:1072-1083.
35. Etxeberria A, Mangin JM, Aguirre A, Gallo V. 2010. Adult-born SVZ progenitors receive transient synapses during remyelination in corpus callosum. Nat Neurosci 13:287-289.
36. Fischer J, Beckervordersandforth R, Tripathi P, Steiner-Mezzadri A, Ninkovic J, Götz M. 2011. Prospective isolation of adult neural stem cells from the mouse subependymal zone. Nat Protoc 6:1981-1989.
37. Frantz GD, McConnell SK. 1996. Restriction of late cerebral cortical progenitors to an upper-layer fate. Neuron 17:55-61.
38. Furutachi S, Miya H, Watanabe T, Kawai H, Yamasaki N, Harada Y, Imayoshi I, Nelson M, Nakayama KI, Hirabayashi Y, Gotoh Y. 2015. Slowly dividing neural progenitors are an embryonic origin of adult neural stem cells. Nat Neurosci doi: 10.1038/nn.3989.
39. Gabay L, Lowell S, Rubin LL, Anderson DJ. 2003. Deregulation of dorsoventral patterning by FGF confers trilineage differentiation capacity on CNS stem cells in vitro. Neuron 40:485-499.
40. Gage FH, Kempermann G, Palmer TD, Peterson DA, Ray J. 1998. Multipotent progenitor cells in the adult dentate gyrus. J Neurobiol 36:249-266.
41. Gage FH, Ray J, Fisher LJ. 1995. Isolation, characterization, and use of stem cells from the CNS. Annu Rev Neurosci 18:159-192.
42. Ganat YM, Silbereis J, Cave C, Ngu H, Anderson GM, Ohkubo Y, Ment LR, Vaccarino FM. 2006. Early postnatal astroglial cells produce multilineage precursors and neural stem cells in vivo. J Neurosci 26:8609-8621.
43. Gao P, Postiglione MP, Krieger TG, Hernandez L, Wang C, Han Z, Streicher C, Papusheva E, Insolera R, Chugh K, Kodish O, Huang K, Simons BD, Luo L, Hippenmeyer S, Shi SH. 2014. Deterministic progenitor behavior and unitary production of neurons in the neocortex. Cell 159:775-788.
44. García-Marqués J, López-Mascaraque L. 2013. Clonal identity determines astrocyte cortical heterogeneity. Cereb Cortex 23:1463-1472.
45. Ge WP, Miyawaki A, Gage FH, Jan YN, Jan LY. 2012. Local generation of glia is a major astrocyte source in postnatal cortex. Nature 484:376-380.
46. Götz M. 2013. Radial glial cells. In: Helmut K, Bruce R R, editors. Neuroglia, 3rd ed. New York: Oxford University Press. pp 50-61.
47. Götz M, Huttner WB. 2005. The cell biology of neurogenesis. Nat Rev Mol Cell Biol 6:777-788.
48. Götz M, Sirko S. 2013. Potential of glial cells. In: Stewart Sell, editor. Stem cells handbook, 2nd ed. New York: Springer. pp 347-361.
49. Grande A, Sumiyoshi K, López-Juárez A, Howard J, Sakthivel B, Aronow B, Campbell K, Nakafuku M. 2013. Environmental impact on direct neuronal reprogramming in vivo in the adult brain. Nat Commun 4:2373.
50. Grégoire CA, Goldenstein BL, Floriddia EM, Barnabé-Heider F, Fernandes KJL. 2015. Endogenous neural stem cell responses to stroke and spinal cord injury. Glia (this issue).
51. Greig LC, Woodworth MB, Galazo MJ, Padmanabhan H, Macklis JD. 2013. Molecular logic of neocortical projection neuron specification, development and diversity. Nat Rev Neurosci 14:755-769.
52. Grove EA, Williams BP, Li DQ, Hajihosseini M, Friedrich A, Price J. 1993. Multiple restricted lineages in the embryonic rat cerebral cortex. Development 117:553-561.
53. Guérout N, Li X, Barnabé-Heider F. 2014. Cell fate control in the developing central nervous system. Exp Cell Res 321:77-83.
54. Haan N, Goodman T, Najdi-Samiei A, Stratford CM, Rice R, El Agha E, Bellusci S, Hajihosseini MK. 2013. Fgf10-expressing tanycytes add new neurons to the appetite/energy-balance regulating centers of the postnatal and adult hypothalamus. J Neurosci 33:6170-6180.
55. Hack MA, Sugimori M, Lundberg C, Nakafuku M, Götz M. 2004 Regionalization and fate specification in neurospheres: The role of Olig2 and Pax6. Mol Cell Neurosci 25:664-678.
56. Hartfuss E, Galli R, Heins N, Götz M. 2001. Characterization of CNS precursor subtypes and radial glia. Dev Biol 229:15-30.
57. Hochstim C, Deneen B, Lukaszewicz A, Zhou Q, Anderson DJ. 2008. Identification of positionally distinct astrocyte subtypes whose identities are specified by a homeodomain code. Cell 133:510-522.
58. Hsu YC, Li L, Fuchs E. 2014. Emerging interactions between skin stem cells and their niches. Nat Med 20:847-856.
59. Ihrie RA, Shah JK, Harwell CC, Levine JH, Guinto CD, Lezameta M, Kriegstein AR, Alvarez-Buylla A. 2011. Persistent sonic hedgehog signaling in adult brain determines neural stem cell positional identity. Neuron 71:250-262.
60. Imayoshi I, Kageyama R. 2014. Oscillatory control of bHLH factors in neural progenitors. Trends Neurosci 37:531-538.
61. Inta D, Alfonso J, von Engelhardt J, Kreuzberg MM, Meyer AH, van Hooft JA, Monyer H. 2008. Neurogenesis and widespread forebrain migration of distinct GABAergic neurons from the postnatal subventricular zone. Proc Natl Acad Sci USA 105:20994-20999.
62. Jacquet BV, Salinas-Mondragon R, Liang H, Therit B, Buie JD, Dykstra M, Campbell K, Ostrowski LE, Brody SL, Ghashghaei HT. 2009. FoxJ1-dependent gene expression is required for differentiation of radial glia into ependymal cells and a subset of astrocytes in the postnatal brain. Development 136:4021-4031.
63. Jiménez AJ, Domínguez-Pinos MD, Guerra MM, Fernández-Llebrez P, Pérez-Fígares JM. 2014. Structure and function of the ependymal barrier and diseases associated with ependyma disruption. Tissue Barriers 2:e28426.
64. Kang W, Balordi F, Su N, Chen L, Fishell G, Hébert JM. 2014. Astrocyte activation is suppressed in both normal and injured brain by FGF signaling. Proc Natl Acad Sci USA 111:E2987-E2995.
65. Kazanis I, Lathia J, Moss L, ffrench-Constant C. 2008. The neural stem cell microenvironment. In: The Stem CellStemBook [Internet]. Cambridge (MA): Harvard Stem Cell Institute. Doi: 10.3824/stembook.1.15.1 http://www.stembook.org/node/490.
66. Kondo T, Raff M. 2000. Oligodendrocyte precursor cells reprogrammed to become multipotential CNS stem cells. Science 289:1754-1757.
67. Kriegstein A, Alvarez-Buylla A. 2009. The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 32:149-184.
68. Ledford H. 2008. Disputed definitions. Nature 455:1023-1028.
69. Le Magueresse C, Alfonso J, Khodosevich K, Arroyo Martín AA, Bark C, Monyer H. 2011. "Small axonless neurons": Postnatally generated neocortical interneurons with delayed functional maturation. J Neurosci 31:16731-16747.
70. Leone DP, Srinivasan K, Chen B, Alcamo E, McConnell SK. 2008. The determination of projection neuron identity in the developing cerebral cortex. Curr Opin Neurobiol 18:28-35.
71. Levison SW, Goldman JE. 1993. Both oligodendrocytes and astrocytes develop from progenitors in the subventricular zone of postnatal rat forebrain. Neuron 10:201-212.
72. Levison SW, Goldman JE. 1997. Multipotential and lineage restricted precursors coexist in the mammalian perinatal subventricular zone. J Neurosci Res 48:83-94.
73. Li H, de Faria JP, Andrew P, Nitarska J, Richardson WD. 2011. Phosphorylation regulates OLIG2 cofactor choice and the motor neuron-oligodendrocyte fate switch. Neuron 69:918-929.
74. Lin G, Goldman JE. 2009. An FGF-responsive astrocyte precursor isolated from the neonatal forebrain. Glia 57:592-603.
75. Lledo PM, Merkle FT, Alvarez-Buylla A. 2008. Origin and function of olfactory bulb interneuron diversity. Trends Neurosci 31:392-400.
76. Lodato S, Shetty AS, Arlotta P. 2015. Cerebral cortex assembly: Generating and reprogramming projection neuron diversity. Trends Neurosci 38:117-125.
77. Luskin MB. 1993. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11:173-189.
78. Luzzati F, De Marchis S, Fasolo A, Peretto P. 2006. Neurogenesis in the caudate nucleus of the adult rabbit. J Neurosci 26:609-621.
79. Magnusson JP, Göritz C, Tatarishvili J, Dias DO, Smith EM, Lindvall O, Kokaia Z, Frisén J. 2014. A latent neurogenic program in astrocytes regulated by Notch signaling in the mouse. Science 346:237-241.
80. Malatesta P, Hack MA, Hartfuss E, Kettenmann H, Klinkert W, Kirchhoff F, Götz M. 2003. Neuronal or glial progeny: Regional differences in radial glia fate. Neuron 37:751-764.
81. Malatesta P, Hartfuss E, Götz M. 2000. Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 127:5253-5263.
82. Marshall CA, Novitch BG, Goldman JE. 2005. Olig2 directs astrocyte and oligodendrocyte formation in postnatal subventricular zone cells. J Neurosci 25:7289-7298.
83. Marshall CA, Suzuki SO, Goldman JE. 2003. Gliogenic and neurogenic progenitors of the subventricular zone: Who are they, where did they come from, and where are they going? Glia 43:52-61.
84. Martín-López E, García-Marques J, Núñez-Llaves R, López-Mascaraque L. 2013. Clonal astrocytic response to cortical injury. PLoS One 8:e74039.
85. Martynoga B, Mateo JL, Zhou B, Andersen J, Achimastou A, Urbán N, van den Berg D, Georgopoulou D, Hadjur S, Wittbrodt J, Ettwiller L, Piper M, Gronostajski RM, Guillemot F. 2013. Epigenomic enhancer annotation reveals a key role for NFIX in neural stem cell quiescence. Genes Dev 27:1769-1786.
86. McDermott KW, Barry DS, McMahon SS. 2005. Role of radial glia in cytogenesis, patterning and boundary formation in the developing spinal cord. J Anat 207:241-250.
87. Meletis K, Barnabé-Heider F, Carlén M, Evergren E, Tomilin N, Shupliakov O, Frisén J. 2008. Spinal cord injury reveals multilineage differentiation of ependymal cells. PLoS Biol 6:e182.
88. Merkle FT, Fuentealba LC, Sanders TA, Magno L, Kessaris N, Alvarez-Buylla A. 2014. Adult neural stem cells in distinct microdomains generate previously unknown interneuron types. Nat Neurosci 17:207-214.
89. Merkle FT, Mirzadeh Z, Alvarez-Buylla A. 2007. Mosaic organization of neural stem cells in the adult brain. Science 317:381-384.
90. Merkle FT, Tramontin AD, Garcia-Verdugo JM, Alvarez-Buylla A. 2004. Radial glia give rise to adult neural stem cells in the subventricular zone. Proc Natl Acad Sci USA 101:17528-17532.
91. Mich JK, Signer RA, Nakada D, Pineda A, Burgess RJ, Vue TY, Johnson JE, Morrison SJ. 2014. Prospective identification of functionally distinct stem cells and neurosphere-initiating cells in adult mouse forebrain. Elife 3:e02669.
92. Molofsky AV, Deneen B. 2015. Astrocyte development: A guide for the perplexed. Glia (this issue).
93. Molofsky AV, Kelley KW, Tsai HH, Redmond SA, Chang SM, Madireddy L, Chan JR, Baranzini SE, Ullian EM, Rowitch DH. 2014. Astrocyte-encoded positional cues maintain sensorimotor circuit integrity. Nature 509:189-194.
94. Mukouyama YS, Deneen B, Lukaszewicz A, Novitch BG, Wichterle H, Jessell TM, Anderson DJ. 2006. Olig2+ neuroepithelial motoneuron progenitors are not multipotent stem cells in vivo. Proc Natl Acad Sci USA 103:1551-1556.
95. Nagy A, Gócza E, Diaz EM, Prideaux VR, Iványi E, Markkula M, Rossant J. 1990. Embryonic stem cells alone are able to support fetal development in the mouse. Development 110:815-821.
96. Nakatomi H, Kuriu T, Okabe S, Yamamoto S, Hatano O, Kawahara N, Tamura A, Kirino T, Nakafuku M. 2002. Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 110:429-441.
97. Neumeister B, Grabosch A, Basak O, Kemler R, Taylor V. 2009. Neural progenitors of the postnatal and adult mouse forebrain retain the ability to self-replicate, form neurospheres, and undergo multipotent differentiation in vivo. Stem Cells 27:714-723.
98. Ninkovic J, Götz M. 2014. A time and place for understanding neural stem cell specification. Dev Cell 30:114-115.
99. Ninkovic J, Götz M. 2015. How to make neurons-thoughts on the molecular logic of neurogenesis in the central nervous system. Cell Tissue Res 359:5-16.
100. Ninkovic J, Mori T, Götz M. 2007. Distinct modes of neuron addition in adult mouse neurogenesis. J Neurosci 27:10906-10911.
101. Ninkovic J, Steiner-Mezzadri A, Jawerka M, Akinci U, Masserdotti G, Petricca S, Fischer J, von Holst A, Beckers J, Lie CD, Petrik D, Miller E, Tang J, Wu J, Lefebvre V, Demmers J, Eisch A, Metzger D, Crabtree G, Irmler M, Poot R, Götz M. 2013. The BAF complex interacts with Pax6 in adult neural progenitors to establish a neurogenic cross-regulatory transcriptional network. Cell Stem Cell 13:403-418.
102. Nishiyama A, Komitova M, Suzuki R, Zhu X. 2009. Polydendrocytes (NG2 cells): Multifunctional cells with lineage plasticity. Nature Rev Neurosci 10:9-22.
103. Noctor SC, Martínez-Cerdeño V, Ivic L, Kriegstein AR. 2004. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 7:136-144.
104. Nolte C, Matyash M, Pivneva T, Schipke CG, Ohlemeyer C, Hanisch UK, Kirchhoff F, Kettenmann H. 2001. GFAP promoter-controlled EGFP-expressing transgenic mice: A tool to visualize astrocytes and astrogliosis in living brain tissue. Glia 33:72-86.
105. Norton WT, Aquino DA, Hozumi I, Chiu FC, Brosnan CF. 1992. Quantitative aspects of reactive gliosis: A review. Neurochem Res 17:877-885.
106. Ohori Y, Yamamoto S, Nagao M, Sugimori M, Yamamoto N, Nakamura K, Nakafuku M. 2006. Growth factor treatment and genetic manipulation stimulate neurogenesis and oligodendrogenesis by endogenous neural progenitors in the injured adult spinal cord. J Neurosci 26:11948-11960.
107. Orre M, Kamphuis W, Osborn LM, Melief J, Kooijman L, Huitinga I, Klooster J, Bossers K, Hol EM. 2014. Acute isolation and transcriptome characterization of cortical astrocytes and microglia from young and aged mice. Neurobiol Aging 35:1-14.
108. Ortega F, Gascón S, Masserdotti G, Deshpande A, Simon C, Fischer J, Dimou L, Chichung Lie D, Schroeder T, Berninger B. 2013. Oligodendrogliogenic and neurogenic adult subependymal zone neural stem cells constitute distinct lineages and exhibit differential responsiveness to Wnt ignaling. Nat Cell Biol 15:602-613.
109. Paez-Gonzalez P, Abdi K, Luciano D, Liu Y, Soriano-Navarro M, Rawlins E, Bennett V, Garcia-Verdugo JM, Kuo CT. 2011. Ank3-dependent SVZ niche assembly is required for the continued production of new neurons. Neuron 71:61-75.
110. Palmer TD, Markakis EA, Willhoite AR, Safar F, Gage FH. 1999. Fibroblast growth factor-2 activates a latent neurogenic program in neural stem cells from diverse regions of the adult CNS. J Neurosci 19:8487-8497.
111. Pekny M, Johansson CB, Eliasson C, Stakeberg J, Wallén A, Perlmann T, Lendahl U, Betsholtz C, Berthold CH, Frisén J. 1999. Abnormal reaction to central nervous system injury in mice lacking glial fibrillary acidic protein and vimentin. J Cell Biol 145:503-514.
112. Pekny M, Pekna M. 2014. Astrocyte reactivity and reactive astrogliosis: Costs and benefits. Physiol Rev 94:1077-1098.
113. Pilz GA, Shitamukai A, Reillo I, Pacary E, Schwausch J, Stahl R, Ninkovic J, Snippert HJ, Clevers H, Godinho L, Guillemot F, Borrell V, Matsuzaki F, Götz M. 2013. Amplification of progenitors in the mammalian telencephalon includes a new radial glial cell type. Nat Commun 4:2125.
114. Pinto L, Drechsel D, Schmid MT, Ninkovic J, Irmler M, Brill MS, Restani L, Gianfranceschi L, Cerri C, Weber SN, Tarabykin V, Baer K, Guillemot F, Beckers J, Zecevic N, Dehay C, Caleo M, Schorle H, Götz M. 2009. AP2gamma regulates basal progenitor fate in a region- and layer-specific manner in the developing cortex. Nat Neurosci 12:1229-1237.
115. Pinto L, Mader MT, Irmler M, Gentilini M, Santoni F, Drechsel D, Blum R, Stahl R, Bulfone A, Malatesta P, Beckers J, Götz M. 2008. Prospective isolation of functionally distinct radial glial subtypes-lineage and transcriptome analysis. Mol Cell Neurosci 38:15-42.
116. Pollard SM, Conti L, Sun Y, Goffredo D, Smith A. 2006. Adherent neural stem (NS) cells from fetal and adult forebrain. Cereb Cortex 16 Suppl 1:i112-i120.
117. Pollard SM, Wallbank R, Tomlinson S, Grotewold L, Smith A. 2008. Fibroblast growth factor induces a neural stem cell phenotype in foetal forebrain progenitors and during embryonic stem cell differentiation. Mol Cell Neurosci 38:393-403.
118. Psachoulia K, Jamen F, Young KM, Richardson WD. 2009. Cell cycle dynamics of NG2 cells in the postnatal and ageing brain. Neuron Glia Biol 5:57-67
119. Qian X, Shen Q, Goderie SK, He W, Capela A, Davis AA, Temple S. 2000. Timing of CNS cell generation: A programmed sequence of neuron and glial cell production from isolated murine cortical stem cells. Neuron 28:69-80.
120. Reynolds BA, Weiss S. 1992. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255:1707-1710.
121. Reynolds R, Hardy R. 1997. Oligodendroglial progenitors labeled with the O4 antibody persist in the adult rat cerebral cortex in vivo. J Neurosci Res 47:455-470.
122. Richards LJ, Kilpatrick TJ, Bartlett PF. 1992. De novo generation of neuronal cells from the adult mouse brain. Proc Natl Acad Sci USA 89:8591-8595.
123. Riquelme PA, Drapeau E, Doetsch F. 2008. Brain micro-ecologies: Neural stem cell niches in the adult mammalian brain. Philos Trans R Soc Lond B Biol Sci 363:123-137.
124. Robel S, Berninger B, Götz M. 2011. The stem cell potential of glia: Lessons from reactive gliosis. Nat Rev Neurosci 12:88-104.
125. Robins SC, Stewart I, McNay DE, Taylor V, Giachino C, Goetz M, Ninkovic J, Briancon N, Maratos-Flier E, Flier JS, Kokoeva MV, Placzek M. 2013. Α-Tanycytes of the adult hypothalamic third ventricle include distinct populations of FGF-responsive neural progenitors. Nat Commun 4:2049.
126. Rousso DL, Pearson CA, Gaber ZB, Miquelajauregui A, Li S, Portera-Cailliau C, Morrisey EE, Novitch BG. 2012. Foxp-mediated suppression of N-cadherin regulates neuroepithelial character and progenitor maintenance in the CNS. Neuron 74:314-330.
127. Rowitch DH, Kriegstein AR. 2010. Developmental genetics of vertebrate glial-cell specification. Nature 468:214-222.
128. Sabelström H, Stenudd M, Réu P, Dias DO, Elfineh M, Zdunek S, Damberg P, Göritz C, Frisén J. 2013. Resident neural stem cells restrict tissue damage and neuronal loss after spinal cord injury in mice. Science 342:637-640.
129. Sahara S, O'Leary DD. 2009. Fgf10 regulates transition period of cortical stem cell differentiation to radial glia controlling generation of neurons and basal progenitors. Neuron 63:48-62.
130. Seidenfaden R, Desoeuvre A, Bosio A, Virard I, Cremer H. 2006. Glial conversion of SVZ-derived committed neuronal precursors after ectopic grafting into the adult brain. Mol Cell Neurosci 32:187-198.
131. Shear DA, Tate MC, Archer DR, Hoffman SW, Hulce VD, Laplaca MC, Stein DG. 2004. Neural progenitor cell transplants promote long-term functional recovery after traumatic brain injury. Brain Res 1026:11-22.
132. Shihabuddin LS, Horner PJ, Ray J, Gage FH. 2000. Adult spinal cord stem cells generate neurons after transplantation in the adult dentate gyrus. J Neurosci 20:8727-8735.
133. Shimada IS, LeComte MD, Granger JC, Quinlan NJ, Spees JL. 2012. Self-renewal and differentiation of reactive astrocyte-derived neural stem/progenitor cells isolated from the cortical peri-infarct area after stroke. J Neurosci 32:7926-7940.
134. Shimojo H, Ohtsuka T, Kageyama R. 2011. Dynamic expression of notch signaling genes in neural stem/progenitor cells. Front Neurosci 5:78.
135. Simon C, Götz M, Dimou L. 2011. Progenitors in the adult cerebral cortex: Cell cycle properties and regulation by physiological stimuli and injury. Glia 59:869-881.
136. Sirko S, Behrendt G, Johansson PA, Tripathi P, Costa M, Bek S, Heinrich C, Tiedt S, Colak D, Dichgans M, Fischer IR, Plesnila N, Staufenbiel M, Haass C, Snapyan M, Saghatelyan A, Tsai LH, Fischer A, Grobe K, Dimou L, Götz M. 2013. Reactive glia in the injured brain acquire stem cell properties in response to sonic hedgehog. Cell Stem Cell 12:426-439.
137. Sirko S, Neitz A, Mittmann T, Horvat-Bröcker A, von Holst A, Eysel UT, Faissner A. 2009. Focal laser-lesions activate an endogenous population of neural stem/progenitor cells in the adult visual cortex. Brain 132:2252-2264.
138. Sirko S, von Holst A, Weber A, Wizenmann A, Theocharidis U, Götz M, Faissner A. 2010. Chondroitin sulfates are required for fibroblast growth factor-2-dependent proliferation and maintenance in neural stem cells and for epidermal growth factor-dependent migration of their progeny. Stem Cells 28:775-787.
139. Sofroniew MV. 2014. Multiple roles for astrocytes as effectors of cytokines and inflammatory mediators. Neuroscientist 20:160-172.
140. Southwell DG, Nicholas CR, Basbaum AI, Stryker MP, Kriegstein AR, Rubenstein JL, Alvarez-Buylla A. 2014. Interneurons from embryonic development to cell-based therapy. Science 344:1240622.
141. Stahl R, Walcher T, De Juan Romero C, Pilz GA, Cappello S, Irmler M, Sanz-Aquela JM, Beckers J, Blum R, Borrell V, Götz M. 2013. Trnp1 regulates expansion and folding of the mammalian cerebral cortex by control of radial glial fate. Cell 153:535-549.
142. Suhonen JO, Peterson DA, Ray J, Gage FH. 1996. Differentiation of adult hippocampus-derived progenitors into olfactory neurons in vivo. Nature 383:624-627.
143. Sultan KT, Brown KN, Shi SH. 2013. Production and organization of neocortical interneurons. Front Cell Neurosci 7:221.
144. Suslov ON, Kukekov VG, Ignatova TN, Steindler DA. 2002. Neural stem cell heterogeneity demonstrated by molecular phenotyping of clonal neurospheres. Proc Natl Acad Sci USA 99:14506-14511.
145. Suzuki SO, Goldman JE. 2003. Multiple cell populations in the early postnatal subventricular zone take distinct migratory pathways: A dynamic study of glial and neuronal progenitor migration. J Neurosci 23:4240-4250.
146. Takebayashi H, Ikenaka K. 2015. Oligodendrocyte generation during mouse development. Glia (this issue).
147. Taverna E, Götz M, Huttner WB. 2014. The cell biology of neurogenesis: Toward an understanding of the development and evolution of the neocortex. Annu Rev Cell Dev Biol 30:465-502.
148. Than-Trong E, Bally-Cuif L. 2015. Radial glia and neural progenitors in the adult zebrafish central nervous system. Glia (this issue).
149. Tsai HH, Li H, Fuentealba LC, Molofsky AV, Taveira-Marques R, Zhuang H, Tenney A, Murnen AT, Fancy SP, Merkle F, Kessaris N, Alvarez-Buylla A, Richardson WD, Rowitch DH. 2012 Regional astrocyte allocation regulates CNS synaptogenesis and repair. Science 337:358-362.
150. Vergaño-Vera E, Díaz-Guerra E, Rodríguez-Traver E, Méndez-Gómez HR, Solís O, Pignatelli J, Pickel J, Lee SH, Moratalla R, Vicario-Abejón C. 2014. Nurr1 blocks the mitogenic effect of FGF-2 and EGF, inducing olfactory bulb neural stem cells to adopt dopaminergic and dopaminergic-GABAergic neuronal phenotypes. Dev Neurobiol. Doi: 10.1002/dneu.22251.
151. Vergaño-Vera E, Méndez-Gómez HR, Hurtado-Chong A, Cigudosa JC, Vicario-Abejón C. 2009. Fibroblast growth factor-2 increases the expression of neurogenic genes and promotes the migration and differentiation of neurons derived from transplanted neural stem/progenitor cells. Neuroscience 162:39-54.
152. Vicario-Abejón C, Yusta-Boyo MJ, Fernández-Moreno C, de Pablo F. 2003. Locally born olfactory bulb stem cells proliferate in response to insulin-related factors and require endogenous insulin-like growth factor-I for differentiation into neurons and glia. J Neurosci 23:895-906.
153. von Holst A, Sirko S, Faissner A. 2006 The unique 473HD-Chondroitinsulfate epitope is expressed by radial glia and involved in neural precursor cell proliferation. J Neurosci 26:4082-4094.
154. Weinandy F, Ninkovic J, Götz M. 2011. Restrictions in time and space-new insights into generation of specific neuronal subtypes in the adult mammalian brain. Eur J Neurosci 33:1045-1054.
155. Williams BP, Read J, Price J. 1991. The generation of neurons and oligodendrocytes from a common precursor cell. Neuron 7:685-693.
156. Wray J, Kalkan T, Smith AG. 2010. The ground state of pluripotency. Biochem Soc Trans 38:1027-1032.
157. Wu S, Wu Y, Capecchi MR. 2006. Motoneurons and oligodendrocytes are sequentially generated from neural stem cells but do not appear to share common lineage-restricted progenitors in vivo. Development 133:581-590.
158. Ying QL, Wray J, Nichols J, Batlle-Morera L, Doble B, Woodgett J, Cohen P, Smith A. 2008. The ground state of embryonic stem cell self-renewal. Nature 453:519-523.
159. Young KM, Fogarty M, Kessaris N, Richardson WD. 2007. 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.
160. Zamanian JL, Xu L, Foo LC, Nouri N, Zhou L, Giffard RG, Barres BA. 2012. Genomic analysis of reactive astrogliosis. J Neurosci 32:6391-6410.
161. Zerlin M, Milosevic A, Goldman JE. 2004. Glial progenitors of the neonatal subventricular zone differentiate asynchronously, leading to spatial dispersion of glial clones and to the persistence of immature glia in the adult mammalian CNS. Dev Biol 270:200-213.
162. Zhu X, Bergles DE, Nishiyama A. 2008. NG2 cells generate both oligodendrocytes and gray matter astrocytes. Development 135:145-157.
163. Zhu X, Hill RA, Dietrich D, Komitova M, Suzuki R, Nishiyama A. 2011. Age-dependent fate and lineage restriction of single NG2 cells. Development 138:745-753.