Adult Neural Stem Cells from the Subventricular Zone Give Rise to Reactive Astrocytes in the Cortex after Stroke

Cell Stem Cell

Volumn 17, Issue 5, 2015, Pages 624-634

  Faiz, Maryam ^a   Sachewsky, Nadia ^b   Gascón, Sergio ^c,d   Bang, K W Annie ^a   Morshead, Cindi M ^b   Nagy, Andras ^a,b  

^a MOUNT SINAI HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF MUNICH   (Germany)

^d INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR MASH1; ASCL1 PROTEIN, MOUSE; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; ASTROCYTOSIS; BRAIN CORTEX; CELL DIFFERENTIATION; CELL MIGRATION; CELL SUBPOPULATION; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; MOUSE; NERVE CELL; NERVE REGENERATION; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CYTOLOGY; LATERAL BRAIN VENTRICLE; METABOLISM; PATHOLOGY; TRANSGENIC MOUSE;

ANIMALS; ASTROCYTES; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CEREBRAL CORTEX; LATERAL VENTRICLES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURAL STEM CELLS; NEURONS; STROKE;

EID: 84947813542     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2015.08.002     Document Type: Article

References (62)

1. A. Arvidsson, T. Collin, D. Kirik, Z. Kokaia, and O. Lindvall Neuronal replacement from endogenous precursors in the adult brain after stroke Nat. Med. 8 2002 963 970
2. S. Bauer, B.J. Kerr, and P.H. Patterson The neuropoietic cytokine family in development, plasticity, disease and injury Nat. Rev. Neurosci. 8 2007 221 232
3. E.J. Benner, D. Luciano, R. Jo, K. Abdi, P. Paez-Gonzalez, H. Sheng, D.S. Warner, C. Liu, C. Eroglu, and C.T. Kuo Protective astrogenesis from the SVZ niche after injury is controlled by Notch modulator Thbs4 Nature 497 2013 369 373
4. A. Buffo, I. Rite, P. Tripathi, A. Lepier, D. Colak, A.P. Horn, T. Mori, and M. Götz Origin and progeny of reactive gliosis: A source of multipotent cells in the injured brain Proc. Natl. Acad. Sci. USA 105 2008 3581 3586
5. J.E. Burda, and M.V. Sofroniew Reactive gliosis and the multicellular response to CNS damage and disease Neuron 81 2014 229 248
6. 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
7. 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
8. K.B. Casper, K. Jones, and K.D. McCarthy Characterization of astrocyte-specific conditional knockouts Genesis 45 2007 292 299
9. S. Chanda, C.E. Ang, J. Davila, C. Pak, M. Mall, Q.Y. Lee, H. Ahlenius, S.W. Jung, T.C. Südhof, and M. Wernig Generation of induced neuronal cells by the single reprogramming factor ASCL1 Stem Cell Reports 3 2014 282 296
10. S.R. Clarke, A.K. Shetty, J.L. Bradley, and D.A. Turner Reactive astrocytes express the embryonic intermediate neurofilament nestin Neuroreport 5 1994 1885 1888
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. S. Corti, M. Nizzardo, C. Simone, M. Falcone, C. Donadoni, S. Salani, F. Rizzo, M. Nardini, G. Riboldi, F. Magri, and et al. Direct reprogramming of human astrocytes into neural stem cells and neurons Exp. Cell Res. 318 2012 1528 1541
13. P. Dibajnia, and C.M. Morshead Role of neural precursor cells in promoting repair following stroke Acta Pharmacol. Sin. 34 2013 78 90
14. 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
15. A. Erlandsson, C.H. Lin, F. 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. L.C. Fuentealba, S.B. Rompani, J.I. Parraguez, K. Obernier, R. Romero, C.L. Cepko, and A. Alvarez-Buylla Embryonic origin of postnatal neural stem cells Cell 161 2015 1644 1655
17. Z. Guo, L. Zhang, Z. Wu, Y. Chen, F. Wang, and G. Chen In vivo direct reprogramming of reactive glial cells into functional neurons after brain injury and in an Alzheimer's disease model Cell Stem Cell 14 2014 188 202
18. C. Heinrich, R. Blum, S. Gascón, G. Masserdotti, P. Tripathi, R. Sánchez, S. Tiedt, T. Schroeder, M. Götz, and B. Berninger Directing astroglia from the cerebral cortex into subtype specific functional neurons PLoS Biol. 8 2010 e1000373
19. C. Heinrich, S. Gascón, G. Masserdotti, A. Lepier, R. Sanchez, T. Simon-Ebert, T. Schroeder, M. Götz, and B. Berninger Generation of subtype-specific neurons from postnatal astroglia of the mouse cerebral cortex Nat. Protoc. 6 2011 214 228
20. C. Heinrich, M. Bergami, S. Gascón, A. Lepier, F. Viganò, L. Dimou, B. Sutor, B. Berninger, and M. Götz Sox2-mediated conversion of NG2 glia into induced neurons in the injured adult cerebral cortex Stem Cell Reports 3 2014 1000 1014
21. R. Hua, and W. Walz Minocycline treatment prevents cavitation in rats after a cortical devascularizing lesion Brain Res. 1090 2006 172 181
22. H.B. Huttner, O. Bergmann, M. Salehpour, A. Rácz, J. Tatarishvili, E. Lindgren, T. Csonka, L. Csiba, T. Hortobágyi, G. Méhes, and et al. The age and genomic integrity of neurons after cortical stroke in humans Nat. Neurosci. 17 2014 801 803
23. I. Imayoshi, T. Ohtsuka, D. Metzger, P. Chambon, and R. Kageyama Temporal regulation of Cre recombinase activity in neural stem cells Genesis 44 2006 233 238
24. 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
25. H.J. Kim, E. McMillan, F. Han, and C.N. Svendsen Regionally specified human neural progenitor cells derived from the mesencephalon and forebrain undergo increased neurogenesis following overexpression of ASCL1 Stem Cells 27 2009 390 398
26. B. Kolb, C. Morshead, C. Gonzalez, M. Kim, C. Gregg, T. Shingo, and S. Weiss Growth factor-stimulated generation of new cortical tissue and functional recovery after stroke damage to the motor cortex of rats J. Cereb. Blood Flow Metab. 27 2007 983 997
27. D.C. Lagace, M.C. Whitman, M.A. Noonan, J.L. Ables, N.A. DeCarolis, A.A. Arguello, M.H. Donovan, S.J. Fischer, L.A. Farnbauch, R.D. Beech, and et al. Dynamic contribution of nestin-expressing stem cells to adult neurogenesis J. Neurosci. 27 2007 12623 12629
28. S.Y. Leong, and A.M. Turnley Regulation of adult neural precursor cell migration Neurochem. Int. 59 2011 382 393
29. C. Lois, and A. Alvarez-Buylla Long-distance neuronal migration in the adult mammalian brain Science 264 1994 1145 1148
30. L. Madisen, T.A. Zwingman, S.M. Sunkin, S.W. Oh, H.A. Zariwala, H. Gu, L.L. Ng, R.D. Palmiter, M.J. Hawrylycz, A.R. Jones, and et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain Nat. Neurosci. 13 2010 133 140
31. J.P. Magnusson, C. Göritz, J. Tatarishvili, D.O. Dias, E.M. Smith, O. Lindvall, Z. Kokaia, and J. Frisén A latent neurogenic program in astrocytes regulated by Notch signaling in the mouse Science 346 2014 237 241
32. S. Marro, Z.P. Pang, N. Yang, M.C. Tsai, K. Qu, H.Y. Chang, T.C. Südhof, and M. Wernig Direct lineage conversion of terminally differentiated hepatocytes to functional neurons Cell Stem Cell 9 2011 374 382
33. A.V. Molofsky, R. Krencik, E.M. Ullian, H.H. Tsai, B. Deneen, W.D. Richardson, B.A. Barres, and D.H. Rowitch Astrocytes and disease: a neurodevelopmental perspective Genes Dev. 26 2012 891 907
34. 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
35. 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
36. G. Nato, A. Caramello, S. Trova, V. Avataneo, C. Rolando, V. Taylor, A. Buffo, P. Peretto, and F. Luzzati Striatal astrocytes produce neuroblasts in an excitotoxic model of Huntington's disease Development 142 2015 840 845
37. W. Niu, T. Zang, Y. Zou, S. Fang, D.K. Smith, R. Bachoo, and C.L. Zhang In vivo reprogramming of astrocytes to neuroblasts in the adult brain Nat. Cell Biol. 15 2013 1164 1175
38. E. Pastrana, L.C. Cheng, and F. Doetsch Simultaneous prospective purification of adult subventricular zone neural stem cells and their progeny Proc. Natl. Acad. Sci. USA 106 2009 6387 6392
39. A. Petit, P. Pierret, A. Vallée, and G. Doucet Astrocytes from cerebral cortex or striatum attract adult host serotoninergic axons into intrastriatal ventral mesencephalic co-grafts J. Neurosci. 21 2001 7182 7193
40. J.C. Platel, V. Gordon, T. Heintz, and A. Bordey GFAP-GFP neural progenitors are antigenically homogeneous and anchored in their enclosed mosaic niche Glia 57 2009 66 78
41. J. Pollak, M.S. Wilken, Y. Ueki, K.E. Cox, J.M. Sullivan, R.J. Taylor, E.M. Levine, and T.A. Reh ASCL1 reprograms mouse Muller glia into neurogenic retinal progenitors Development 140 2013 2619 2631
42. A. Popp, N. Jaenisch, O.W. Witte, and C. Frahm Identification of ischemic regions in a rat model of stroke PLoS ONE 4 2009 e4764
43. C.S. Potten, and M. Loeffler Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt Development 110 1990 1001 1020
44. S. Robel, B. Berninger, and M. Götz The stem cell potential of glia: lessons from reactive gliosis Nat. Rev. Neurosci. 12 2011 88 104
45. R. Seidenfaden, A. Desoeuvre, A. Bosio, I. Virard, and H. Cremer Glial conversion of SVZ-derived committed neuronal precursors after ectopic grafting into the adult brain Mol. Cell. Neurosci. 32 2006 187 198
46. I.S. Shimada, M.D. LeComte, J.C. Granger, N.J. Quinlan, and J.L. Spees Self-renewal and differentiation of reactive astrocyte-derived neural stem/progenitor cells isolated from the cortical peri-infarct area after stroke J. Neurosci. 32 2012 7926 7940
47. S. Sirko, G. Behrendt, P.A. Johansson, P. Tripathi, M. Costa, S. Bek, C. Heinrich, S. Tiedt, D. Colak, M. Dichgans, and et al. Reactive glia in the injured brain acquire stem cell properties in response to sonic hedgehog. [corrected] Cell Stem Cell 12 2013 426 439
48. S. Srinivas, T. Watanabe, C.S. Lin, C.M. William, Y. Tanabe, T.M. Jessell, and F. Costantini Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus BMC Dev. Biol. 1 2001 4
49. Z. Su, W. Niu, M.L. Liu, Y. Zou, and C.L. Zhang In vivo conversion of astrocytes to neurons in the injured adult spinal cord Nat. Commun. 5 2014 3338
50. M.Y. Sun, M.J. Yetman, T.C. Lee, Y. Chen, and J.L. Jankowsky Specificity and efficiency of reporter expression in adult neural progenitors vary substantially among nestin-CreER(T2) lines J. Comp. Neurol. 522 2014 1191 1208
51. M. Synowitz, J. Kiwit, H. Kettenmann, and R. Glass Tumor Young Investigator Award: tropism and antitumorigenic effect of endogenous neural precursors for gliomas Clin. Neurosurg. 53 2006 336 344
52. O. Torper, U. Pfisterer, D.A. Wolf, M. Pereira, S. Lau, J. Jakobsson, A. Björklund, S. Grealish, and M. Parmar Generation of induced neurons via direct conversion in vivo Proc. Natl. Acad. Sci. USA 110 2013 7038 7043
53. V. Tropepe, C.G. Craig, C.M. Morshead, and D. van der Kooy Transforming growth factor-alpha null and senescent mice show decreased neural progenitor cell proliferation in the forebrain subependyma J. Neurosci. 17 1997 7850 7859
54. S.F. Tzeng, and J.P. Wu Responses of microglia and neural progenitors to mechanical brain injury Neuroreport 10 1999 2287 2292
55. T. Vierbuchen, A. Ostermeier, Z.P. Pang, Y. Kokubu, T.C. Südhof, and M. Wernig Direct conversion of fibroblasts to functional neurons by defined factors Nature 463 2010 1035 1041
56. I.B. Wanner, M.A. Anderson, B. Song, J. Levine, A. Fernandez, Z. Gray-Thompson, Y. Ao, and M.V. Sofroniew Glial scar borders are formed by newly proliferated, elongated astrocytes that interact to corral inflammatory and fibrotic cells via STAT3-dependent mechanisms after spinal cord injury J. Neurosci. 33 2013 12870 12886
57. K. Woltjen, I.P. Michael, P. Mohseni, R. Desai, M. Mileikovsky, R. Hämäläinen, R. Cowling, W. Wang, P. Liu, M. Gertsenstein, and et al. piggyBac transposition reprograms fibroblasts to induced pluripotent stem cells Nature 458 2009 766 770
58. L. Xu, R.M. Sapolsky, and R.G. Giffard Differential sensitivity of murine astrocytes and neurons from different brain regions to injury Exp. Neurol. 169 2001 416 424
59. Y. Yang, H. Higashimori, and L. Morel Developmental maturation of astrocytes and pathogenesis of neurodevelopmental disorders J. Neurodev. Disord. 5 2013 22
60. 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
61. X. Zhu, D.E. Bergles, and A. Nishiyama NG2 cells generate both oligodendrocytes and gray matter astrocytes Development 135 2008 145 157
62. L. Zhuo, B. Sun, C.L. Zhang, A. Fine, S.Y. Chiu, and A. Messing Live astrocytes visualized by green fluorescent protein in transgenic mice Dev. Biol. 187 1997 36 42