Neurogenesis following stroke affecting the adult brain

Cold Spring Harbor Perspectives in Biology

Volumn 7, Issue 11, 2015, Pages

  Lindvall, Olle ^a   Kokaia, Zaal ^a  

^a LUND UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; BRAIN; CELL DEATH; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CEREBROVASCULAR ACCIDENT; HUMAN; MOUSE; NERVOUS SYSTEM DEVELOPMENT; PATHOLOGY; RAT;

ANIMALS; BRAIN; CELL DEATH; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; HUMANS; MICE; NEUROGENESIS; RATS; STROKE;

EID: 84946423581     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a019034     Document Type: Article

References (122)

1. Ahlenius H, Devaraju K, Monni E, Oki K, Wattananit S, Darsalia V, Iosif RE, Torper O, Wood JC, Braun S, et al. 2012. Adaptor protein LNK is a negative regulator of brain neural stem cell proliferation after stroke. J Neurosci 32: 5151–5164
2. Androutsellis-Theotokis A, Leker RR, Soldner F, Hoeppner DJ, Ravin R, Poser SW, Rueger MA, Bae SK, Kittappa R, McKay RD. 2006. Notch signalling regulates stem cell numbers in vitro and in vivo. Nature 442: 823–826
3. Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O. 2002. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 8: 963–970
4. Barkho BZ, Munoz AE, Li X, Li L, Cunningham LA, Zhao X. 2008. Endogenous matrix metalloproteinase (MMP)-3 and MMP-9 promote the differentiation and migration of adult neural progenitor cells in response to chemokines. Stem Cells 26: 3139–3149
5. Bernier PJ, Vinet J, Cossette M, Parent A. 2000. Characterization of the subventricular zone of the adult human brain: Evidence for the involvement of Bcl-2. Neurosci Res 37: 67–78
6. Bhardwaj RD, Curtis MA, Spalding KL, Buchholz BA, Fink D, Björk-Eriksson T, Nordborg C, Gage FH, Druid H, Eriksson PS, Frisén J. 2006. Neocortical neurogenesis in humans is restricted to development. Proc Natl Acad Sci 103: 12564–12568
7. Breunig JJ, Arellano JI, Macklis JD, Rakic P. 2007. Everything that glitters isn’t gold: Acritical reviewof postnatal neural precursor analyses. Cell Stem Cell 1: 612–627
8. Butovsky O, Ziv Y, Schwartz A, Landa G, Talpalar AE, Pluchino S, Martino G, Schwartz M. 2006. Microglia activated by IL-4 or IFN-g differentially induce neurogenesis and oligodendrogenesis fromadult stem/progenitor cells. Mol Cell Neurosci 31: 149–160
9. Butti E, Bacigaluppi M, Rossi S, Cambiaghi M, Bari M, Cebrian Silla A, Brambilla E, Musella A, De Ceglia R, Teneud L, et al. 2012. Subventricular zone neural progenitors protect striatal neurons from glutamatergic excitotoxicity. Brain 135: 3320–3335
10. Buza-Vidas N, Antonchuk J, Qian H, Mansson R, Luc S, Zandi S, Anderson K, Takaki S, Nygren JM, Jensen CT, Jacobsen SE. 2006. Cytokines regulate postnatal hematopoietic stem cell expansion: Opposing roles of thrombopoietin and LNK. Genes Dev 20: 2018–2023
11. Cacci E, Ajmone-Cat MA, Anelli T, Biagioni S, Minghetti L. 2008. In vitro neuronal and glial differentiation from embryonic or adult neural precursor cells are differently affected by chronic or acute activation of microglia. Glia 56: 412–425
12. Carlen M, Meletis K, Goritz C, Darsalia V, Evergren E, Tanigaki K, Amendola M, Barnabe-Heider F, Yeung MS, Naldini L, et al. 2009. Forebrain ependymal cells are Notch-dependent and generate neuroblasts and astrocytes after stroke. Nat Neurosci 12: 259–267
13. Chen J, Zhang ZG, Li Y, Wang Y, Wang L, Jiang H, Zhang C, Lu M, Katakowski M, Feldkamp CS, Chopp M. 2003. Statins induce angiogenesis, neurogenesis, and synaptogenesis after stroke. Ann Neurol 53: 743–751
14. Chmielnicki E, Benraiss A, Economides AN, Goldman SA. 2004. Adenovirally expressed noggin and brain-derived neurotrophic factor cooperate to induce new medium spiny neurons from resident progenitor cells in the adult striatal ventricular zone. J Neurosci 24: 2133–2142
15. Collin T, Arvidsson A, Kokaia Z, Lindvall O. 2005. Quantitative analysis of the generation of different striatal neuronal subtypes in the adult brain following excitotoxic injury. Exp Neurol 195: 71–80
16. Curtis MA, Kam M, Nannmark U, Anderson MF, Axell MZ, Wikkelso C, Holtas S, van Roon-Mom WM, Bjork-Eriksson T, Nordborg C, et al. 2007. Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 315: 1243–1249
17. Darsalia V, Heldmann U, Lindvall O, Kokaia Z. 2005. Strokeinduced neurogenesis in aged brain. Stroke 36: 1790–1795
18. Delavaran H, Sjunnesson H, Arvidsson A, Lindvall O, Norrving B, van Westen D, Kokaia Z, Lindgren A. 2013. Proximity of brain infarcts to regions of endogenous neurogenesis and involvement of striatum in ischaemic stroke. Eur J Neurol 20: 473–479
19. Devaraju K, Barnabe-Heiderb F, Kokaia Z, Lindvall O. 2013. FoxJ1-expressing cells contribute to neurogenesis in forebrain of adult rats: Evidence from in vivo electroporation combined with piggyBac transposon. Exp Cell Res 319: 2790–2800
20. Diederich K, Frauenknecht K, Minnerup J, Schneider BK, Schmidt A, Altach E, Eggert V, Sommer CJ, Schabitz WR. 2012. Citicoline enhances neuroregenerative processes after experimental stroke in rats. Stroke 43: 1931–1940
21. Ekdahl CT, Claasen JH, Bonde S, Kokaia Z, Lindvall O. 2003. Inflammation is detrimental for neurogenesis in adult brain. Proc Natl Acad Sci 100: 13632–13637
22. Eriksson PS, Perfilieva E, Björk-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH. 1998. Neurogenesis in the adult human hippocampus. Nat Med 4: 1313–1317
23. Ernst A, Alkass K, Bernard S, Salehpour M, Perl S, Tisdale J, Possnert G, Druid H, Frisén J. 2014. Neurogenesis in the striatum of the adult human brain. Cell 156: 1072–1083
24. Gomez-Nicola D, Valle-Argos B, Pallas-Bazarra N, Nieto- Sampedro M. 2011. Interleukin-15 regulates proliferation and self-renewal of adult neural stem cells. Mol Biol Cell 22: 1960–1970
25. Gonzalez CL, Kolb B. 2003. A comparison of different models of stroke on behaviour and brain morphology. Eur J Neurosci 18: 1950–1962
26. Grade S, Weng YC, Snapyan M, Kriz J, Malva JO, Saghatelyan A. 2013. Brain-derived neurotrophic factor promotes vasculature-associated migration of neuronal precursors toward the ischemic striatum. PloS ONE 8: e55039
27. Gu W, Jiang W, Wester P. 1999. A photothrombotic ring stroke model in rats with sustained hypoperfusion followed by late spontaneous reperfusion in the region at risk. Exp Brain Res 125: 163–170
28. Gustafsson E, Andsberg G, Darsalia V, Mohapel P, Mandel RJ, Kirik D, Lindvall O, Kokaia Z. 2003. Anterograde delivery of brain-derived neurotrophic factor to striatum via nigral transduction of recombinant adeno-associated virus increases neuronal death but promotes neurogenic response following stroke. Eur J Neurosci 17: 2667–2678
29. Hoehn BD, Palmer TD, Steinberg GK. 2005. Neurogenesis in rats after focal cerebral ischemia is enhanced by indomethacin. Stroke 36: 2718–2724
30. Hou SW, Wang YQ, Xu M, Shen DH, Wang JJ, Huang F, Yu Z, Sun FY. 2008. Functional integration of newly generated neurons into striatum after cerebral ischemia in the adult rat brain. Stroke 39: 2837–2844
31. Huttner HB, et al. 2014. The age and genomic integrity of neurons after cortical stroke in humans. Nat Neurosci 17: 801–803
32. Iosif RE, Ahlenius H, Ekdahl CT, Darsalia V, Thored P, Jovinge S, Kokaia Z, Lindvall O. 2008. Suppression of stroke-induced progenitor proliferation in adult subventricular zone by tumor necrosis factor receptor 1. J Cereb Blood Flow Metab 28: 1574–1587
33. Jakubs K, Nanobashvili A, Bonde S, Ekdahl CT, Kokaia Z, Kokaia M, Lindvall O. 2006. Environment matters: Synaptic properties of neurons born in the epileptic adult brain develop to reduce excitability. Neuron 52: 1047–1059
34. Jakubs K, Bonde S, Iosif RE, Ekdahl CT, Kokaia Z, Kokaia M, Lindvall O. 2008. Inflammation regulates functional integration of neurons born in adult brain. J Neurosci 28: 12477–12488
35. Jiang W, Gu W, Brannstrom T, Rosqvist R, Wester P. 2001. Cortical neurogenesis in adult rats after transient middle cerebral artery occlusion. Stroke 32: 1201–1207
36. Jin K, Minami M, Lan JQ, Mao XO, Batteur S, Simon RP, Greenberg DA. 2001. Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat. ProcNatlAcad Sci 98: 4710–4715
37. Jin K, Sun Y, Xie L, Peel A, Mao XO, Batteur S, Greenberg DA. 2003. Directed migration of neuronal precursors into the ischemic cerebral cortex and striatum. Mol Cell Neurosci 24: 171–189
38. Jin K, Sun Y, Xie L, Childs J, Mao XO, Greenberg DA. 2004. Post-ischemic administration of heparin-binding epidermal growth factor-like growth factor (HB-EGF) reduces infarct size and modifies neurogenesis after focal cerebral ischemia in the rat. J Cereb Blood Flow Metab 24: 399–408
39. Jin K, Wang X, Xie L, Mao XO, Zhu W, Wang Y, Shen J, Mao Y, Banwait S, Greenberg DA. 2006. Evidence for strokeinduced neurogenesis in the human brain. ProcNatl Acad Sci 103: 13198–13202
40. Jin K, Wang X, Xie L, Mao XO, Greenberg DA. 2010. Transgenic ablation of doublecortin-expressing cells suppresses adult neurogenesis and worsens stroke outcome in mice. Proc Natl Acad Sci 107: 7993–7998
41. Jin K, Xie L, Mao X, Greenberg MB, Moore A, Peng B, Greenberg RB, Greenberg DA. 2011. Effect of human neural precursor cell transplantation on endogenous neurogenesis after focal cerebral ischemia in the rat. Brain Res 1374: 56–62
42. Kawada H, Takizawa S, Takanashi T, Morita Y, Fujita J, Fukuda K, Takagi S, Okano H, Ando K, Hotta T. 2006. Administration of hematopoietic cytokines in the subacute phase after cerebral infarction is effective for functional recovery facilitating proliferation of intrinsic neural stem/progenitor cells and transition of bone marrowderived neuronal cells. Circulation 113: 701–710
43. Keiner S, Witte OW, Redecker C. 2009. Immunocytochemical detection of newly generated neurons in the perilesional area of cortical infarcts after intraventricular application of brain-derived neurotrophic factor. J Neuropathol Exp Neurol 68: 83–93
44. Kobayashi T, Ahlenius H, Thored P, Kobayashi R, Kokaia Z, Lindvall O. 2006. Intracerebral infusion of glial cell linederived neurotrophic factor promotes striatal neurogenesis after stroke in adult rats. Stroke 37: 2361–2367
45. Kojima T, Hirota Y, Ema M, Takahashi S, Miyoshi I, Okano H, Sawamoto K. 2010. Subventricular zone-derived neural progenitor cells migrate along a blood vessel scaffold toward the post-stroke striatum. Stem Cells 28: 545–554
46. Kokaia Z, Martino G, Schwartz M, Lindvall O. 2012. Crosstalk between neural stem cells and immune cells: The key to better brain repair? Nat Neurosci 15: 1078–1087
47. Kolb B, Morshead C, Gonzalez C, Kim M, Gregg C, Shingo T, Weiss S. 2006. 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: 983–997
48. Kolb B, Morshead C, Gonzalez C, Kim M, Gregg C, Shingo T, Weiss S. 2007. 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: 983–997
49. Kreuzberg M, Kanov E, Timofeev O, Schwaninger M, Monyer H, Khodosevich K. 2010. Increased subventricular zone-derived cortical neurogenesis after ischemic lesion. Exp Neurol 226: 90–99
50. Lagace DC. 2012. Does the endogenous neurogenic response alter behavioral recovery following stroke? Behav Brain Res 227: 426–432
51. Lee SR, Kim HY, Rogowska J, Zhao BQ, Bhide P, Parent JM, Lo EH. 2006. Involvement of matrix metalloproteinase in neuroblast cell migration from the subventricular zone after stroke. J Neurosci 26: 3491–3495
52. Leifer D, Kowall NW. 1993. Immunohistochemical patterns of selective cellular vulnerability in human cerebral ischemia. J Neurol Sci 119: 217–228
53. Leker RR, Soldner F, Velasco I, Gavin DK, Androutsellis-Theotokis A, McKay RD. 2007. Long-lasting regeneration after ischemia in the cerebral cortex. Stroke 38: 153–161
54. Liu Z, Fan Y, Won SJ, Neumann M, Hu D, Zhou L, Weinstein PR, Liu J. 2007. Chronic treatment with minocycline preserves adult new neurons and reduces functional impairment after focal cerebral ischemia. Stroke 38: 146–152
55. Liu F, You Y, Li X, Ma T, Nie Y, Wei B, Li T, Lin H, Yang Z. 2009. Brain injury does not alter the intrinsic differentiation potential of adult neuroblasts. J Neurosci 29: 5075–5087
56. Liu K, Liu Y, Mo W, Qiu R, Wang X, Wu JY, He R. 2011. MiR- 124 regulates early neurogenesis in the optic vesicle and forebrain, targeting NeuroD1. Nucleic Acids Res 39: 2869–2879
57. Liu XS, Chopp M, Wang XL, Zhang L, Hozeska-Solgot A, Tang T, Kassis H, Zhang RL, Chen C, Xu J, Zhang ZG. 2013. MicroRNA-17-92 cluster mediates the proliferation and survival of neural progenitor cells after stroke. J Biol Chem 288: 12478–12488
58. Louissaint A Jr, Rao S, Leventhal C, Goldman SA. 2002. Coordinated interaction of neurogenesis and angiogenesis in the adult songbird brain. Neuron 34: 945–960
59. Love S, Plaha P, Patel NK, Hotton GR, Brooks DJ, Gill SS. 2005. Glial cell line-derived neurotrophic factor induces neuronal sprouting in human brain. Nat Med 11: 703–704
60. Macas J, Nern C, Plate KH, Momma S. 2006. Increased generation of neuronal progenitors after ischemic injury in the aged adult human forebrain. JNeurosci 26: 13114–13119
61. Magnusson JP, Göritz C, Tatarishvili J, Dias DO, Smith EMK, Lindvall O, Kokaia Z, Frisén J. 2014. A latent neurogenic program in astrocytes regulated by Notch signaling in the mouse. Science 346: 237–241
62. Marti-Fabregas J, Romaguera-Ros M, Gomez-Pinedo U, Martinez-Ramirez S, Jimenez-Xarrie E, Marin R, Marti- Vilalta JL, Garcia-Verdugo JM. 2010. Proliferation in the human ipsilateral subventricular zone after ischemic stroke. Neurology 74: 357–365
63. Merkle FT, Mirzadeh Z, Alvarez-Buylla A. 2007. Mosaic organization of neural stem cells in the adult brain. Science 317: 381–384
64. Mine Y, Tatarishvili J, Oki K, Monni E, Kokaia Z, Lindvall O. 2013. Grafted human neural stem cells enhance several steps of endogenous neurogenesis and improve behavioral recovery after middle cerebral artery occlusion in rats. Neurobiol Dis 52: 191–203
65. Minger SL, Ekonomou A, Carta EM, Chinoy A, Perry RH, Ballard CG. 2007. Endogenous neurogenesis in the human brain following cerebral infarction. Regenerative Med 2: 69–74
66. Monje ML, Toda H, Palmer TD. 2003. Inflammatory blockade restores adult hippocampal neurogenesis. Science 302: 1760–1765
67. Nakayama D, Matsuyama T, Ishibashi-Ueda H, Nakagomi T, Kasahara Y, Hirose H, Kikuchi-Taura A, Stern DM, Mori H, Taguchi A. 2010. Injury-induced neural stem/ progenitor cells in post-stroke human cerebral cortex. Eur J Neurosci 31: 90–98
68. Nyfeler Y, Kirch RD, Mantei N, Leone DP, Radtke F, Suter U, Taylor V. 2005. Jagged1 signals in the postnatal subventricular zone are required for neural stem cell self-renewal. EMBO J 24: 3504–3515
69. Ohab JJ, Fleming S, Blesch A, Carmichael ST. 2006. A neurovascular niche for neurogenesis after stroke. J Neurosci 26: 13007–13016
70. Ohira K, Furuta T, Hioki H, Nakamura KC, Kuramoto E, Tanaka Y, Funatsu N, Shimizu K, Oishi T, Hayashi M, et al. 2010. Ischemia-induced neurogenesis of neocortical layer 1 progenitor cells. Nat Neurosci 13: 173–179
71. Osman AM, Porritt MJ, Nilsson M, Kuhn HG. 2011. Longterm stimulation of neural progenitor cell migration after cortical ischemia in mice. Stroke 42: 3559–3565
72. Parent JM, Vexler ZS, Gong C, Derugin N, Ferriero DM. 2002. Rat forebrain neurogenesis and striatal neuron replacement after focal stroke. Ann Neurol 52: 802–813
73. Plane JM, Whitney JT, Schallert T, Parent JM. 2008. Retinoic acid and environmental enrichment alter subventricular zone and striatal neurogenesis after stroke. Exp Neurol 214: 125–134
74. Robin AM, Zhang ZG, Wang L, Zhang RL, Katakowski M, Zhang L, Wang Y, Zhang C, Chopp M. 2005. Stromal cellderived factor 1a mediates neural progenitor cell motility after focal cerebral ischemia. J Cereb Blood Flow Metab 26: 125–134
75. Robin AM, Zhang ZG, Wang L, Zhang RL, Katakowski M, Zhang L, Wang Y, Zhang C, Chopp M. 2006. Stromal cellderived factor 1a mediates neural progenitor cell motility after focal cerebral ischemia. J Cereb Blood Flow Metab 26: 125–134
76. Saha B, Peron S, Murray K, Jaber M, Gaillard A. 2013. Cortical lesion stimulates adult subventricular zone neural progenitor cell proliferation and migration to the site of injury. Stem Cell Res 11: 965–977
77. Saino O, Taguchi A, Nakagomi T, Nakano-Doi A, Kashiwamura S, Doe N, Nakagomi N, Soma T, Yoshikawa H, Stern DM, et al. 2010. Immunodeficiency reduces neural stem/progenitor cell apoptosis and enhances neurogenesis in the cerebral cortex after stroke. J Neurosci Res 88: 2385–2397
78. Sanai N, Tramontin AD, Quinones-Hinojosa A, Barbaro NM, Gupta N, Kunwar S, Lawton MT, McDermott MW, Parsa AT, Manuel-Garcia Verdugo J, Berger MS, Alvarez-Buylla A. 2004. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427: 740–744
79. Sanai N, Nguyen T, Ihrie RA, Mirzadeh Z, Tsai HH, Wong M, Gupta N, Berger MS, Huang E, Garcia-Verdugo JM, Rowitch DH, Alvarez-Buylla A. 2011. Corridors of migrating neurons in the human brain and their decline during infancy. Nature 478: 382–386
80. Schneider A, Kruger C, Steigleder T, Weber D, Pitzer C, Laage R, Aronowski J, Maurer MH, Gassler N, Mier W, Hasselblatt M, Kollmar R, Schwab S, Sommer C, Bach A, Kuhn HG, Schabitz WR. 2005. The hematopoietic factor G-CSF is a neuronal ligand that counteracts programmed cell death and drives neurogenesis. J Clin Invest 115: 2083–2098
81. Shang J, Deguchi K, Ohta Y, Liu N, Zhang X, Tian F, Yamashita T, Ikeda Y, Matsuura T, Funakoshi H, et al. 2011. Strong neurogenesis, angiogenesis, synaptogenesis, and antifibrosis of hepatocyte growth factor in rats brain after transient middle cerebral artery occlusion. J Neurosci Res 89: 86–95
82. Spalding KL, Bergmann O, Alkass K, Bernard S, Salehpour M, Huttner HB, Bostrom E, Westerlund I, Vial C, Buchholz BA, et al. 2013. Dynamics of hippocampal neurogenesis in adult humans. Cell 153: 1219–1227
83. Stump G, Durrer A, Klein AL, Lutolf S, Suter U, Taylor V. 2002. Notch1 and its ligands Delta-like and Jagged are expressed and active in distinct cell populations in the postnatal mouse brain. Mech Dev 114: 153–159
84. Sun Y, Jin K, Xie L, Childs J, Mao XO, Logvinova A, Greenberg DA. 2003. VEGF-induced neuroprotection, neurogenesis, and angiogenesis after focal cerebral ischemia. J Clin Invest 111: 1843–1851
85. Sun X, Zhang QW, Xu M, Guo JJ, Shen SW, Wang YQ, Sun FY. 2012. New striatal neurons form projections to substantia nigra in adult rat brain after stroke. Neurobiol Dis 45: 601–609
86. Taguchi A, Soma T, Tanaka H, Kanda T, Nishimura H, Yoshikawa H, Tsukamoto Y, Iso H, Fujimori Y, Stern DM, Naritomi H, Matsuyama T. 2004. Administration of CD34þ cells after stroke enhances neurogenesis via angiogenesis in a mouse model. J Clin Invest 114: 330–338
87. Takaki S, Sauer K, Iritani BM, Chien S, Ebihara Y, Tsuji K, Takatsu K, Perlmutter RM. 2000. Control of B cell production by the adaptor protein lnk. Definition of a conserved family of signal-modulating proteins. Immunity 13: 599–609
88. Takata M, Nakagomi T, Kashiwamura S, Nakano-Doi A, Saino O, Nakagomi N, Okamura H, Mimura O, Taguchi A, Matsuyama T. 2012. Glucocorticoid-induced TNF receptor- triggered T cells are key modulators for survival/ death of neural stem/progenitor cells induced by ischemic stroke. Cell Death Differ 19: 756–767
89. Tanaka Y, Tanaka R, Liu M, Hattori N, Urabe T. 2010. Cilostazol attenuates ischemic brain injury and enhances neurogenesis in the subventricular zone of adult mice after transient focal cerebral ischemia. Neuroscience 171: 1367–1376
90. Teramoto T, Qiu J, Plumier JC, Moskowitz MA. 2003. EGF amplifies the replacement of parvalbumin-expressing striatal interneurons after ischemia. J Clin Invest 111: 1125–1132
91. Thored P, Arvidsson A, Cacci E, Ahlenius H, Kallur T, Darsalia V, Ekdahl CT, Kokaia Z, Lindvall O. 2006. Persistent production of neurons from adult brain stem cells during recovery after stroke. Stem Cells 24: 739–747
92. Thored P, Wood J, Arvidsson A, Cammenga J, Kokaia Z, Lindvall O. 2007. Long-term neuroblast migration along blood vessels in an area with transient angiogenesis and increased vascularization after stroke. Stroke 38: 3032–3039
93. Thored P, Heldmann U, Gomes-Leal W, Gisler R, Darsalia V, Taneera J, Nygren JM, Jacobsen SE, Ekdahl CT, Kokaia Z, Lindvall O. 2009. Long-term accumulation of microglia with proneurogenic phenotype concomitant with persistent neurogenesis in adult subventricular zone after stroke. Glia 57: 835–849
94. Tsai PT, Ohab JJ, Kertesz N, Groszer M, Matter C, Gao J, Liu X, Wu H, Carmichael ST. 2006. A critical role of erythropoietin receptor in neurogenesis and post-stroke recovery. J Neurosci 26: 1269–1274
95. Walton NM, Sutter BM, Laywell ED, Levkoff LH, Kearns SM, Marshall GP 2nd, Scheffler B, Steindler DA. 2006. Microglia instruct subventricular zone neurogenesis. Glia 54: 815–825
96. Wang L, Zhang Z, Zhang R, Hafner MS, Wong HK, Jiao Z, Chopp M. 2004. Erythropoietin up-regulates SOCS2 in neuronal progenitor cells derived from SVZ of adult rat. Neuroreport 15: 1225–1229
97. Wang H, Ward N, Boswell M, Katz DM. 2006. Secretion of brain-derived neurotrophic factor from brain microvascular endothelial cells. Eur J Neurosci 23: 1665–1670
98. Wang Y, Jin K, Mao XO, Xie L, Banwait S, Marti HH, Greenberg DA. 2007. VEGF-overexpressing transgenic mice show enhanced post-ischemic neurogenesis and neuromigration. J Neurosci Res 85: 740–747
99. Wang L, Chopp M, Zhang RL, Zhang L, Letourneau Y, Feng YF, Jiang A, Morris DC, Zhang ZG. 2009a. The Notch pathway mediates expansion of a progenitor pool and neuronal differentiation in adult neural progenitor cells after stroke. Neuroscience 158: 1356–1363
100. Wang X, Mao X, Xie L, Greenberg DA, Jin K. 2009b. Involvement of Notch1 signaling in neurogenesis in the subventricular zone of normal and ischemic rat brain in vivo. J Cereb Blood Flow Metab 29: 1644–1654
101. Wang X, Mao X, Xie L, Sun F, Greenberg DA, Jin K. 2012. Conditional depletion of neurogenesis inhibits long-term recovery after experimental stroke in mice. PloS ONE 7: e38932
102. Wolf SA, Steiner B, Wengner A, Lipp M, Kammertoens T, Kempermann G. 2009. Adaptive peripheral immune response increases proliferation of neural precursor cells in the adult hippocampus. FASEB J 23: 3121–3128
103. Wood JC, Jackson JS, Jakubs K, Chapman KZ, Ekdahl CT, Kokaia Z, Kokaia M, Lindvall O. 2011. Functional integration of new hippocampal neurons following insults to the adult brain is determined by characteristics of pathological environment. Exp Neurol 229: 484–493
104. Yamashita T, Ninomiya M, Hernandez Acosta P, Garcia-Verdugo JM, Sunabori T, Sakaguchi M, Adachi K, Kojima T, Hirota Y, Kawase T, et al. 2006. Subventricular zone-derived neuroblasts migrate and differentiate into mature neurons in the post-stroke adult striatum. J Neurosci 26: 6627–6636
105. Yan YP, Sailor KA, Lang BT, Park SW, Vemuganti R, Dempsey RJ. 2007.Monocyte chemoattractant protein-1 plays a critical role in neuroblast migration after focal cerebral ischemia. J Cereb Blood Flow Metab 27: 1213–1224
106. Yan YP, Lang BT, Vemuganti R, Dempsey RJ. 2009. Osteopontin is a mediator of the lateral migration of neuroblasts from the subventricular zone after focal cerebral ischemia. Neurochem Int 55: 826–832
107. Young CC, van der Harg JM, Lewis NJ, Brooks KJ, Buchan AM, Szele FG. 2013. Ependymal ciliary dysfunction and reactive astrocytosis in a reorganized subventricular zone after stroke. Cereb Cortex 23: 647–659
108. Zhang RL, Chopp M, Zhang ZG, Jiang Q, Ewing JR. 1997. A rat model of focal embolic cerebral ischemia. Brain Res 766: 83–92
109. Zhang R, Zhang L, Zhang Z, Wang Y, Lu M, Lapointe M, Chopp M. 2001. A nitric oxide donor induces neurogenesis and reduces functional deficits after stroke in rats. Ann Neurol 50: 602–611
110. Zhang R, Wang Y, Zhang L, Zhang Z, Tsang W, Lu M, Zhang L, Chopp M. 2002. Sildenafil (Viagra) induces neurogenesis and promotes functional recovery after stroke in rats. Stroke 33: 2675–2680
111. Zhang R, Zhang Z, Zhang C, Zhang L, Robin A, Wang Y, Lu M, Chopp M. 2004a. Stroke transiently increases subventricular zone cell division from asymmetric to symmetric and increases neuronal differentiation in the adult rat. J Neurosci 24: 5810–5815
112. Zhang R, Zhang Z, Wang L, Wang Y, Gousev A, Zhang L, Ho KL, Morshead C, Chopp M. 2004b. 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: 441–448
113. Zhang R, Xue YY, Lu SD, Wang Y, Zhang LM, Huang YL, Signore AP, Chen J, Sun FY. 2006a. Bcl-2 enhances neurogenesis and inhibits apoptosis of newborn neurons in adult rat brain following a transient middle cerebral artery occlusion. Neurobiol Dis 24: 345–356
114. Zhang RL, Zhang ZG, Lu M, Wang Y, Yang JJ, Chopp M. 2006b. Reduction of the cell cycle length by decreasing G1 phase and cell cycle reentry expand neuronal progenitor cells in the subventricular zone of adult rat after stroke. J Cereb Blood Flow Metab 26: 857–863
115. Zhang RL, Zhang ZG, Wang Y, LeTourneau Y, Liu XS, Zhang X, Gregg SR, Wang L, Chopp M. 2007a. Stroke induces ependymal cell transformation into radial glia in the subventricular zone of the adult rodent brain. J Cereb Blood Flow Metab 27: 1201–1212
116. Zhang RL, Letourneau Y, Gregg SR, Wang Y, Toh Y, Robin AM, Zhang ZG, Zhang Z, Chopp M. 2007b. Neuroblast division during migration toward the ischemic striatum: A study of dynamic migratory and proliferative characteristics of neuroblasts from the subventricular zone. J Neurosci 27: 3157–3162
117. Zhang RL, Chopp M, Gregg SR, Toh Y, Roberts C, LeTourneau Y, Buller B, Jia L, Davarani SPN, Zhang ZG. 2009. Patterns and dynamics of subventricular zone neuroblast migration in the ischemic striatum of the adult mouse. J Cereb Blood Flow Metab 29: 1240–1250
118. Zhang C, Chopp M, Cui Y, Wang L, Zhang R, Zhang L, Lu M, Szalad A, Doppler E, Hitzl M, Zhang ZG. 2010. Cerebrolysin enhances neurogenesis in the ischemic brain and improves functional outcome after stroke. J Neurosci Res 88: 3275–3281
119. Zhang P, Li J, Liu Y, Chen X, Lu H, Kang Q, Li W, Gao M. 2011.Human embryonic neural stem cell transplantation increases subventricular zone cell proliferation and promotes peri-infarct angiogenesis after focal cerebral ischemia. Neuropathology 31: 384–391
120. Zheng J, Zhang P, Li X, Lei S, Li W, He X, Zhang J, Wang N, Qi C, Chen X, et al. 2013. Post-stroke estradiol treatment enhances neurogenesis in the subventricular zone of rats after permanent focal cerebral ischemia. Neuroscience 231: 82–90
121. Ziv Y, Ron N, Butovsky O, Landa G, Sudai E, Greenberg N, Cohen H, Kipnis J, Schwartz M. 2006. Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood. Nat Neurosci 9: 268–275
122. Ziv Y, Finkelstein A, Geffen Y, Kipnis J, Smirnov I, Shpilman S, Vertkin I, Kimron M, Lange A, Hecht T, et al. 2007. A novel immune-based therapy for stroke induces neuroprotection and supports neurogenesis. Stroke 38: 774–782.