Primitive neural stem cells in the adult mammalian brain give rise to GFAP-expressing neural stem cells

Stem Cell Reports

Volumn 2, Issue 6, 2014, Pages 810-824

  Sachewsky, Nadia ^a   Leeder, Rachel ^a   Xu, Wenjun ^a   Rose, Keeley L ^a   Yu, Fenggang ^a   Van Der Kooy, Derek ^a   Morshead, Cindi M ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

EMBRYONIC FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR; GLIAL FIBRILLARY ACIDIC PROTEIN; LEUKEMIA INHIBITORY FACTOR; OCTAMER TRANSCRIPTION FACTOR 4; UNCLASSIFIED DRUG; GLIAL FIBRILLARY ASTROCYTIC PROTEIN, MOUSE; NERVE PROTEIN; POU5F1 PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ARTICLE; ASTROCYTE; BLASTOCYST; CELL POPULATION; CELL RENEWAL; CEREBROVASCULAR ACCIDENT; COLONY FORMATION; COLONY FORMING CELL; CONTROLLED STUDY; EMBRYO DEVELOPMENT; FOREBRAIN; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; INNER CELL MASS; MOUSE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; OLIGODENDROGLIA; PHENOTYPE; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SCANNING ELECTRON MICROSCOPY; SUBVENTRICULAR ZONE; SURVIVAL TIME; ANIMAL TISSUE; CELL PROLIFERATION; EMBRYO; LATERAL BRAIN VENTRICLE; MULTIPOTENT STEM CELL; PLURIPOTENT STEM CELL; ANIMAL; BRAIN; CYTOLOGY; METABOLISM;

ANIMALS; BRAIN; MICE; NERVE TISSUE PROTEINS; NEURAL STEM CELLS; NEURONS; OCTAMER TRANSCRIPTION FACTOR-3;

EID: 84902299428     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2014.04.008     Document Type: Article

References (34)

1. W. Akamatsu, B. DeVeale, H. Okano, A.J. Cooney, and D. van der Kooy Suppression of Oct4 by germ cell nuclear factor restricts pluripotency and promotes neural stem cell development in the early neural lineage J. Neurosci. 29 2009 2113 2124
2. L.R. Banner, N.N. Moayeri, and P.H. Patterson Leukemia inhibitory factor is expressed in astrocytes following cortical brain injury Exp. Neurol. 147 1997 1 9 (Pubitemid 27402437)
3. S. Bauer, and P.H. Patterson Leukemia inhibitory factor promotes neural stem cell self-renewal in the adult brain J. Neurosci. 26 2006 12089 12099 (Pubitemid 44772119)
4. S. Bauer, S. Rasika, J. Han, C. Mauduit, M. Raccurt, G. Morel, F. Jourdan, M. Benahmed, E. Moyse, and P.H. Patterson Leukemia inhibitory factor is a key signal for injury-induced neurogenesis in the adult mouse olfactory epithelium J. Neurosci. 23 2003 1792 1803 (Pubitemid 36314734)
5. T.G. Bush, T.C. Savidge, T.C. Freeman, H.J. Cox, E.A. Campbell, L. Mucke, M.H. Johnson, and M.V. Sofroniew Fulminant jejuno-ileitis following ablation of enteric glia in adult transgenic mice Cell 93 1998 189 201 (Pubitemid 28180853)
6. T.G. Bush, N. Puvanachandra, C.H. Horner, A. Polito, T. Ostenfeld, C.N. Svendsen, L. Mucke, M.H. Johnson, and M.V. Sofroniew Leukocyte infiltration, neuronal degeneration, and neurite outgrowth after ablation of scar-forming, reactive astrocytes in adult transgenic mice Neuron 23 1999 297 308 (Pubitemid 29315725)
7. A. Capela, and S. Temple LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal Neuron 35 2002 865 875
8. M. Carlén, K. Meletis, C. Göritz, V. Darsalia, E. Evergren, K. Tanigaki, M. Amendola, F. Barnabé-Heider, M.S. Yeung, and L. Naldini et al. Forebrain ependymal cells are Notch-dependent and generate neuroblasts and astrocytes after stroke Nat. Neurosci. 12 2009 259 267
9. B.J. Chiasson, V. Tropepe, C.M. Morshead, and D. van der Kooy Adult mammalian forebrain ependymal and subependymal cells demonstrate proliferative potential, but only subependymal cells have neural stem cell characteristics J. Neurosci. 19 1999 4462 4471 (Pubitemid 29241097)
10. A.K. Chojnacki, G.K. Mak, and S. Weiss Identity crisis for adult periventricular neural stem cells: subventricular zone astrocytes, ependymal cells or both? Nat. Rev. Neurosci. 10 2009 153 163
11. B.L. Coles-Takabe, I. Brain, K.A. Purpura, P. Karpowicz, P.W. Zandstra, C.M. Morshead, and D. van der Kooy Don't look: growing clonal versus nonclonal neural stem cell colonies Stem Cells 26 2008 2938 2944
12. F. Doetsch, I. Caillé, D.A. Lim, J.M. García-Verdugo, and A. Alvarez-Buylla Subventricular zone astrocytes are neural stem cells in the adult mammalian brain Cell 97 1999 703 716 (Pubitemid 29278045)
13. F. Doetsch, J.M. García-Verdugo, and A. Alvarez-Buylla Regeneration of a germinal layer in the adult mammalian brain Proc. Natl. Acad. Sci. USA 96 1999 11619 11624 (Pubitemid 29487430)
14. F. Doetsch, L. Petreanu, I. Caille, J.M. Garcia-Verdugo, and A. Alvarez-Buylla EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells Neuron 36 2002 1021 1034 (Pubitemid 36044505)
15. A. Erlandsson, C.H. Lin, F.G. Yu, and C.M. Morshead Immunosuppression promotes endogenous neural stem and progenitor cell migration and tissue regeneration after ischemic injury Exp. Neurol. 230 2011 48 57
16. A. Foudi, K. Hochedlinger, D. Van Buren, J.W. Schindler, R. Jaenisch, V. Carey, and H. Hock Analysis of histone 2B-GFP retention reveals slowly cycling hematopoietic stem cells Nat. Biotechnol. 27 2009 84 90
17. E. Fuchs The tortoise and the hair: slow-cycling cells in the stem cell race Cell 137 2009 811 819
18. A.D. Garcia, N.B. Doan, T. Imura, T.G. Bush, and M.V. Sofroniew GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain Nat. Neurosci. 7 2004 1233 1241 (Pubitemid 39426243)
19. D.E. Harrison, and C.M. Astle Loss of stem cell repopulating ability upon transplantation. Effects of donor age, cell number, and transplantation procedure J. Exp. Med. 156 1982 1767 1779 (Pubitemid 13167420)
20. D.E. Harrison, C.M. Astle, and J.A. Delaittre Loss of proliferative capacity in immunohemopoietic stem cells caused by serial transplantation rather than aging J. Exp. Med. 147 1978 1526 1531 (Pubitemid 8328688)
21. S. Hitoshi, R.M. Seaberg, C. Koscik, T. Alexson, S. Kusunoki, I. Kanazawa, S. Tsuji, and D. van der Kooy Primitive neural stem cells from the mammalian epiblast differentiate to definitive neural stem cells under the control of Notch signaling Genes Dev. 18 2004 1806 1811 (Pubitemid 39025091)
22. J. Hunt, A. Cheng, A. Hoyles, E. Jervis, and C.M. Morshead Cyclosporin A has direct effects on adult neural precursor cells J. Neurosci. 30 2010 2888 2896
23. T. Imura, H.I. Kornblum, and M.V. Sofroniew The predominant neural stem cell isolated from postnatal and adult forebrain but not early embryonic forebrain expresses GFAP J. Neurosci. 23 2003 2824 2832 (Pubitemid 36418618)
24. P. Karpowicz, T. Inoue, S. Runciman, B. Deveale, R. Seaberg, M. Gertsenstein, L. Byers, Y. Yamanaka, S. Tondat, and J. Slevin et al. Adhesion is prerequisite, but alone insufficient, to elicit stem cell pluripotency J. Neurosci. 27 2007 5437 5447 (Pubitemid 46790166)
25. Z. Mirzadeh, F.T. Merkle, M. Soriano-Navarro, J.M. Garcia-Verdugo, and A. Alvarez-Buylla Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain Cell Stem Cell 3 2008 265 278
26. Z. Mirzadeh, F. Doetsch, K. Sawamoto, H. Wichterle, and A. Alvarez-Buylla The subventricular zone en-face: wholemount staining and ependymal flow J. Vis. Exp. 6 2010 1938
27. C.M. Morshead, B.A. Reynolds, C.G. Craig, M.W. McBurney, W.A. Staines, D. Morassutti, S. Weiss, and D. van der Kooy Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells Neuron 13 1994 1071 1082 (Pubitemid 24372126)
28. C.M. Morshead, C.G. Craig, and D. van der Kooy In vivo clonal analyses reveal the properties of endogenous neural stem cell proliferation in the adult mammalian forebrain Development 125 1998 2251 2261 (Pubitemid 28336386)
29. C.M. Morshead, A.D. Garcia, M.V. Sofroniew, and D. van Der Kooy 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 (Pubitemid 36920847)
30. S. Suzuki, T. Yamashita, K. Tanaka, H. Hattori, K. Sawamoto, H. Okano, and N. Suzuki Activation of cytokine signaling through leukemia inhibitory factor receptor (LIFR)/gp130 attenuates ischemic brain injury in rats J. Cereb. Blood Flow Metab. 25 2005 685 693 (Pubitemid 40705604)
31. V. Tropepe, S. Hitoshi, C. Sirard, T.W. Mak, J. Rossant, and D. van der Kooy Direct neural fate specification from embryonic stem cells: a primitive mammalian neural stem cell stage acquired through a default mechanism Neuron 30 2001 65 78 (Pubitemid 32441677)
32. A. Wilson, E. Laurenti, G. Oser, R.C. van der Wath, W. Blanco-Bose, M. Jaworski, S. Offner, C.F. Dunant, L. Eshkind, and E. Bockamp et al. Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair Cell 135 2008 1118 1129
33. H.B. Wood, and V. Episkopou Comparative expression of the mouse Sox1, Sox2 and Sox3 genes from pre-gastrulation to early somite stages Mech. Dev. 86 1999 197 201 (Pubitemid 29371760)
34. R. Zhang, Z. Zhang, L. Wang, Y. Wang, A. Gousev, L. Zhang, K.L. Ho, C. Morshead, and M. Chopp Activated neural stem cells contribute to stroke-induced neurogenesis and neuroblast migration toward the infarct boundary in adult rats J. Cereb. Blood Flow Metab. 24 2004 441 448 (Pubitemid 38452235)