Neurogenesis is enhanced by stroke in multiple new stem cell niches along the ventricular system at sites of high BBB permeability

Neurobiology of Disease

Volumn 74, Issue , 2015, Pages 229-239

  Lin, Ruihe ^a   Cai, Jingli ^a   Nathan, Cody ^a   Wei, Xiaotao ^a   Schleidt, Stephanie ^a   Rosenwasser, Robert ^a   Iacovitti, Lorraine ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Blood brain barrier; CVO; Neural stem cell; Neurogenesis; Stroke

Indexed keywords

BROXURIDINE; DOUBLECORTIN; FIBROBLAST GROWTH FACTOR 2; GLIAL FIBRILLARY ACIDIC PROTEIN; NESTIN; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; TRANSCRIPTION FACTOR SOX2; FLUORESCEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN FOURTH VENTRICLE; BRAIN ISCHEMIA; BRAIN THIRD VENTRICLE; BRAIN VENTRICLE; CELL PROLIFERATION; CEREBROVASCULAR ACCIDENT; CIRCUMVENTRICULAR ORGAN; CONTROLLED STUDY; MALE; NERVE CELL DIFFERENTIATION; NERVE REGENERATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PROTEIN EXPRESSION; RAT; STEM CELL NICHE; TISSUE REPAIR; UPREGULATION; ANIMAL; CEREBRAL ARTERY DISEASE; DISEASE COURSE; DISEASE MODEL; METABOLISM; NERVE CELL; OLIGODENDROGLIA; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT; TIME;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN ISCHEMIA; CELL PROLIFERATION; CEREBRAL VENTRICLES; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FLUORESCEIN; INFARCTION, MIDDLE CEREBRAL ARTERY; MALE; NEURAL STEM CELLS; NEUROGENESIS; NEURONS; OLIGODENDROGLIA; RATS, SPRAGUE-DAWLEY; STEM CELL NICHE; STROKE; TIME FACTORS;

EID: 84919830696     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2014.11.016     Document Type: Article

References (63)

1. Abo-Ramadan U., Durukan A., Pitkonen M., Marinkovic I., Tatlisumak E., Pedrono E., Soinne L., Strbian D., Tatlisumak T. Post-ischemic leakiness of the blood-brain barrier: a quantitative and systematic assessment by Patlak plots. Exp. Neurol. 2009, 219:328-333. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/19520075 [Accessed May 27, 2014]).
2. Alvarez-Buylla A., Lim D.A. For the long run: maintaining germinal niches in the adult brain. Neuron 2004, 41:683-686. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/15003168 [Accessed June 28, 2014]).
3. Barkho B.Z., Song H., Aimone J.B., Smrt R.D., Kuwabara T., Nakashima K., Gage F.H., Zhao X. Identification of astrocyte-expressed factors that modulate neural stem/progenitor cell differentiation. Stem Cells Dev. 2006, 15:407-421. (Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2777811&tool=pmcentrez&rendertype=abstract [Accessed June 1, 2014]).
4. Barnabé-Heider F., Göritz C., Sabelström H., Takebayashi H., Pfrieger F.W., Meletis K., Frisén J. Origin of new glial cells in intact and injured adult spinal cord. Cell Stem Cell 2010, 7:470-482. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/20887953 [Accessed May 30, 2014]).
5. Bauer S., Hay M., Amilhon B., Jean A., Moyse E. In vivo neurogenesis in the dorsal vagal complex of the adult rat brainstem. Neuroscience 2005, 130:75-90. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/15561426 [Accessed June 14, 2014]).
6. Bennett L., Yang M., Enikolopov G., Iacovitti L. Circumventricular organs: a novel site of neural stem cells in the adult brain. Mol. Cell. Neurosci. 2009, 41:337-347. (Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2697272&tool=pmcentrez&rendertype=abstract [Accessed June 4, 2014]).
7. Bennett L.B., Cai J., Enikolopov G., Iacovitti L. Heterotopically transplanted CVO neural stem cells generate neurons and migrate with SVZ cells in the adult mouse brain. Neurosci. Lett. 2010, 475:1-6. (Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2876723&tool=pmcentrez&rendertype=abstract [Accessed September 19, 2012]).
8. Carlén M., Meletis K., Göritz C., Darsalia V., Evergren E., Tanigaki K., Amendola M., Barnabé-Heider F., Yeung M.S.Y., Naldini L., Honjo T., Kokaia Z., Shupliakov O., Cassidy R.M., Lindvall O., Frisén J. Forebrain ependymal cells are Notch-dependent and generate neuroblasts and astrocytes after stroke. Nat. Neurosci. 2009, 12:259-267. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/19234458 [Accessed May 30, 2014]).
9. Charrier C., Coronas V., Fombonne J., Roger M., Jean A., Krantic S., Moyse E. Characterization of neural stem cells in the dorsal vagal complex of adult rat by in vivo proliferation labeling and in vitro neurosphere assay. Neuroscience 2006, 138:5-16. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/16338085 [Accessed June 14, 2014]).
10. Chen S.-D., Lin T.-K., Yang D.-I., Lee S.-Y., Shaw F.-Z., Liou C.-W., Chuang Y.-C. The role of sestrin 2 on transient global ischemia-induced hippocampal neuronal injury. Program No. 337.05. Neuroscience 2013 Abstracts 2013, Society for Neuroscience, San Diego, CA, (Online).
11. Chiasson B.J., Tropepe V., Morshead C.M., van der Kooy D. Adult mammalian forebrain ependymal and subependymal cells demonstrate proliferative potential, but only subependymal cells have neural stem cell characteristics. J. Neurosci. 1999, 19:4462-4471. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/10341247 [Accessed June 18, 2014]).
12. Chouaf-Lakhdar L., Fèvre-Montange M., Brisson C., Strazielle N., Gamrani H., Didier-Bazès M. Proliferative activity and nestin expression in periventricular cells of the adult rat brain. Neuroreport 2003, 14:633-636. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/12657901 [Accessed June 28, 2014]).
13. Doetsch F. A niche for adult neural stem cells. Curr. Opin. Genet. Dev. 2003, 13:543-550. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/14550422 [Accessed June 23, 2014]).
14. Doetsch F. The glial identity of neural stem cells. Nat. Neurosci. 2003, 6:1127-1134. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/14583753 [Accessed May 29, 2014]).
15. Doetsch F., Caillé I., Lim D.A., García-Verdugo J.M., Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 1999, 97:703-716. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/10380923 [Accessed June 2, 2014]).
16. Doetsch F., García-Verdugo J.M., Alvarez-Buylla A. Regeneration of a germinal layer in the adult mammalian brain. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:11619-11624. (Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=18083&tool=pmcentrez&rendertype=abstract [Accessed May 27, 2014]).
17. Engelhardt B., Liebner S. Novel insights into the development and maintenance of the blood-brain barrier. Cell Tissue Res. 2014, 355:687-699. (Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3972432&tool=pmcentrez&rendertype=abstract [Accessed May 28, 2014]).
18. Fabis M.J., Phares T.W., Kean R.B., Koprowski H., Hooper D.C. Blood-brain barrier changes and cell invasion differ between therapeutic immune clearance of neurotrophic virus and CNS autoimmunity. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:15511-15516. (Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2563072&tool=pmcentrez&rendertype=abstract [Accessed June 28, 2014]).
19. Gelderblom M., Leypoldt F., Steinbach K., Behrens D., Choe C.-U., Siler D.A., Arumugam T.V., Orthey E., Gerloff C., Tolosa E., Magnus T. Temporal and spatial dynamics of cerebral immune cell accumulation in stroke. Stroke 2009, 40:1849-1857. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/19265055 [Accessed November 3, 2014]).
20. Goldmacher G.V., Nasser R., Lee D.Y., Yigit S., Rosenwasser R., Iacovitti L. Tracking transplanted bone marrow stem cells and their effects in the rat MCAO stroke model. PLoS One 2013, 8:e60049. (Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3612030&tool=pmcentrez&rendertype=abstract [Accessed June 28, 2014]).
21. Grønberg N.V., Johansen F.F., Kristiansen U., Hasseldam H. Leukocyte infiltration in experimental stroke. J. Neuroinflammation 2013, 10:115. (Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3852747&tool=pmcentrez&rendertype=abstract [Accessed November 3, 2014]).
22. Gross P.M., Weindl A. Peering through the windows of the brain. J. Cereb. Blood Flow Metab. 1987, 7:663-672. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/2891718 [Accessed June 28, 2014]).
23. Hawkins B.T., Egleton R.D. Fluorescence imaging of blood-brain barrier disruption. J. Neurosci. Methods 2006, 151:262-267. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/16181683 [Accessed May 24, 2014]).
24. Huang B., Krafft P.R., Ma Q., Rolland W.B., Caner B., Lekic T., Manaenko A., Le M., Tang J., Zhang J.H. Fibroblast growth factors preserve blood-brain barrier integrity through RhoA inhibition after intracerebral hemorrhage in mice. Neurobiol. Dis. 2012, 46:204-214. (Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3299916&tool=pmcentrez&rendertype=abstract [Accessed November 3, 2014]).
25. Iosif R.E., Ahlenius H., Ekdahl C.T., Darsalia V., Thored P., Jovinge S., Kokaia Z., Lindvall O. Suppression of stroke-induced progenitor proliferation in adult subventricular zone by tumor necrosis factor receptor 1. J. Cereb. Blood Flow Metab. 2008, 28:1574-1587. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/18493257 [Accessed June 20, 2014]).
26. Itokazu Y., Kitada M., Dezawa M., Mizoguchi A., Matsumoto N., Shimizu A., Ide C. Choroid plexus ependymal cells host neural progenitor cells in the rat. Glia 2006, 53:32-42. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/16158416 [Accessed June 28, 2014]).
27. Johnson A.K., Gross P.M. Sensory circumventricular organs and brain homeostatic pathways. FASEB J. 1993, 7:678-686. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/8500693 [Accessed May 26, 2014]).
28. Joly J.-S., Osório J., Alunni A., Auger H., Kano S., Rétaux S. Windows of the brain: towards a developmental biology of circumventricular and other neurohemal organs. Semin. Cell Dev. Biol. 2007, 18:512-524. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/17631396 [Accessed June 28, 2014]).
29. Kokaia Z., Martino G., Schwartz M., Lindvall O. Cross-talk between neural stem cells and immune cells: the key to better brain repair?. Nat. Neurosci. 2012, 15:1078-1087. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/22837038 [Accessed June 6, 2014]).
30. Kovács Z., Ikezaki K., Samoto K., Inamura T., Fukui M. VEGF and flt. Expression time kinetics in rat brain infarct. Stroke 1996, 27:1865-1872. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/8841346 discussion 1872-3 [Accessed June 28, 2014]).
31. Lee J.-Y., Kim Y.-J., Kim T.-Y., Koh J.-Y., Kim Y.-H. Essential role for zinc-triggered p75NTR activation in preconditioning neuroprotection. J. Neurosci. 2008, 28:10919-10927. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/18945899 [Accessed June 28, 2014]).
32. Lee D.A., Bedont J.L., Pak T., Wang H., Song J., Miranda-Angulo A., Takiar V., Charubhumi V., Balordi F., Takebayashi H., Aja S., Ford E., Fishell G., Blackshaw S. Tanycytes of the hypothalamic median eminence form a diet-responsive neurogenic niche. Nat. Neurosci. 2012, 15:700-702. (Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3380241&tool=pmcentrez&rendertype=abstract [Accessed May 23, 2014]).
33. Li P., Mao L., Zhou G., Leak R.K., Sun B.-L., Chen J., Hu X. Adoptive regulatory T-cell therapy preserves systemic immune homeostasis after cerebral ischemia. Stroke 2013, 44:3509-3515. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/24092548 [Accessed June 28, 2014]).
34. Lie D.C., Song H., Colamarino S.A., Ming G., Gage F.H. Neurogenesis in the adult brain: new strategies for central nervous system diseases. Annu. Rev. Pharmacol. Toxicol. 2004, 44:399-421. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/14744252 [Accessed June 2, 2014]).
35. Lindvall O., Kokaia Z. Neurogenesis following stroke affecting the adult brain. Adult Neurogenesis 2008, 549-570. Cold Spring Harbor Laboratory Press, New York. F.H. Gage, G. Kempermann, H. Song (Eds.).
36. Migaud M., Batailler M., Segura S., Duittoz A., Franceschini I., Pillon D. Emerging new sites for adult neurogenesis in the mammalian brain: a comparative study between the hypothalamus and the classical neurogenic zones. Eur. J. Neurosci. 2010, 32:2042-2052. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/21143659 [Accessed June 28, 2014]).
37. Mignone J.L., Kukekov V., Chiang A.-S., Steindler D., Enikolopov G. Neural stem and progenitor cells in nestin-GFP transgenic mice. J. Comp. Neurol. 2004, 469:311-324. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/14730584 [Accessed May 24, 2014]).
38. Ming G.-L., Song H. Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 2011, 70:687-702. (Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3106107&tool=pmcentrez&rendertype=abstract [Accessed May 24, 2014]).
39. Moyse E., Bauer S., Charrier C., Coronas V., Krantic S., Jean A. Neurogenesis and neural stem cells in the dorsal vagal complex of adult rat brain: new vistas about autonomic regulations-a review. Auton. Neurosci. 2006, 126-127:50-58. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/16697711 [Accessed June 28, 2014]).
40. Murakami M., Nguyen L.T., Zhuang Z.W., Zhang Z.W., Moodie K.L., Carmeliet P., Stan R.V., Simons M. The FGF system has a key role in regulating vascular integrity. J. Clin. Invest. 2008, 118:3355-3366. (Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2528913&tool=pmcentrez&rendertype=abstract [Accessed November 3, 2014]).
41. Offner H., Subramanian S., Parker S.M., Afentoulis M.E., Vandenbark A.A., Hurn P.D. Experimental stroke induces massive, rapid activation of the peripheral immune system. J. Cereb. Blood Flow Metab. 2006, 26:654-665. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/16121126 [Accessed June 25, 2014]).
42. Pencea V., Bingaman K.D., Freedman L.J., Luskin M.B. Neurogenesis in the subventricular zone and rostral migratory stream of the neonatal and adult primate forebrain. Exp. Neurol. 2001, 172:1-16. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/11681836 [Accessed October 31, 2014]).
43. Rakic P. Limits of neurogenesis in primates. Science 1985, 227:1054-1056. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/3975601 [Accessed June 28, 2014]).
44. Rakic P. DNA synthesis and cell division in the adult primate brain. Ann. N. Y. Acad. Sci. 1985, 457:193-211. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/3913364 [Accessed June 28, 2014]).
45. Reynolds B.A., Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992, 255:1707-1710. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/1553558 [Accessed May 26, 2014]).
46. Robins S.C., Stewart I., McNay D.E., Taylor V., Giachino C., Goetz M., Ninkovic J., Briancon N., Maratos-Flier E., Flier J.S., Kokoeva M.V., Placzek M. α-Tanycytes of the adult hypothalamic third ventricle include distinct populations of FGF-responsive neural progenitors. Nat. Commun. 2013, 4:2049. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/23804023 [Accessed May 23, 2014]).
47. Sanin V., Heeß C., Kretzschmar H.A., Schüller U. Recruitment of neural precursor cells from circumventricular organs of patients with cerebral ischaemia. Neuropathol. Appl. Neurobiol. 2013, 39:510-518. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/22985410 [Accessed June 28, 2014]).
48. Shen Q., Goderie S.K., Jin L., Karanth N., Sun Y., Abramova N., Vincent P., Pumiglia K., Temple S. Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 2004, 304:1338-1340. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/15060285 [Accessed May 29, 2014]).
49. Shen Q., Wang Y., Kokovay E., Lin G., Chuang S.-M., Goderie S.K., Roysam B., Temple S. Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions. Cell Stem Cell 2008, 3:289-300. (Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2747473&tool=pmcentrez&rendertype=abstract [Accessed June 13, 2014]).
50. Slevin M., Krupinski J., Slowik A., Kumar P., Szczudlik A., Gaffney J. Serial measurement of vascular endothelial growth factor and transforming growth factor-beta1 in serum of patients with acute ischemic stroke. Stroke 2000, 31:1863-1870. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/10926948 [Accessed June 28, 2014]).
51. Spassky N., Merkle F.T., Flames N., Tramontin A.D., García-Verdugo J.M., Alvarez-Buylla A. Adult ependymal cells are postmitotic and are derived from radial glial cells during embryogenesis. J. Neurosci. 2005, 25:10-18. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/15634762 [Accessed June 28, 2014]).
52. Sundholm-Peters N.L., Yang H.K.C., Goings G.E., Walker A.S., Szele F.G. Radial glia-like cells at the base of the lateral ventricles in adult mice. J. Neurocytol. 2004, 33:153-164. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/15173638 [Accessed June 28, 2014]).
53. Tavazoie M., Van der Veken L., Silva-Vargas V., Louissaint M., Colonna L., Zaidi B., Garcia-Verdugo J.M., Doetsch F. A specialized vascular niche for adult neural stem cells. Cell Stem Cell 2008, 3:279-288. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/18786415 [Accessed May 29, 2014]).
54. Temple S. The development of neural stem cells. Nature 2001, 414:112-117. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/11689956 [Accessed May 30, 2014]).
55. Thored P., Arvidsson A., Cacci E., Ahlenius H., Kallur T., Darsalia V., Ekdahl C.T., Kokaia Z., Lindvall O. Persistent production of neurons from adult brain stem cells during recovery after stroke. Stem Cells 2006, 24:739-747. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/16210404 [Accessed May 29, 2014]).
56. Wang C., Zhang M., Sun C., Cai Y., You Y., Huang L., Liu F. Sustained increase in adult neurogenesis in the rat hippocampal dentate gyrus after transient brain ischemia. Neurosci. Lett. 2011, 488:70-75. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/21056620 [Accessed June 28, 2014]).
57. Wei X., Lin R., Cai J., Schleidt S., Rosenwasser R., Iacovitti L. Enhanced neurogenesis in adult circumventricular organs following transient focal ischemic stroke in rat. Program No. 608.12. Neuroscience 2013 Abstracts 2013, Society for Neuroscience, San Diego, CA, (Online).
58. Weiss S., Dunne C., Hewson J., Wohl C., Wheatley M., Peterson A.C., Reynolds B.A. Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J. Neurosci. 1996, 16:7599-7609. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/8922416 [Accessed May 26, 2014]).
59. Xu Y., Tamamaki N., Noda T., Kimura K., Itokazu Y., Matsumoto N., Dezawa M., Ide C. Neurogenesis in the ependymal layer of the adult rat 3rd ventricle. Exp. Neurol. 2005, 192:251-264. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/15755543 [Accessed June 4, 2014]).
60. Yang M., Wei X., Li J., Heine L.A., Rosenwasser R., Iacovitti L. Changes in host blood factors and brain glia accompanying the functional recovery after systemic administration of bone marrow stem cells in ischemic stroke rats. Cell Transplant. 2010, 19:1073-1084. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/20412636 [Accessed June 13, 2014]).
61. Zhang Z.G., Zhang L., Jiang Q., Zhang R., Davies K., Powers C., Bruggen N.v., Chopp M. VEGF enhances angiogenesis and promotes blood-brain barrier leakage in the ischemic brain. J. Clin. Invest. 2000, 106:829-838. (Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=517814&tool=pmcentrez&rendertype=abstract [Accessed June 28, 2014]).
62. Zhang R.L., Zhang Z.G., Zhang L., Chopp M. Proliferation and differentiation of progenitor cells in the cortex and the subventricular zone in the adult rat after focal cerebral ischemia. Neuroscience 2001, 105:33-41. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/11483298 [Accessed June 28, 2014]).
63. Zhang R.L., Zhang Z.G., Wang Y., LeTourneau Y., Liu X.S., Zhang X., Gregg S.R., Wang L., Chopp M. Stroke induces ependymal cell transformation into radial glia in the subventricular zone of the adult rodent brain. J. Cereb. Blood Flow Metab. 2007, 27:1201-1212. (Available at: http://www.ncbi.nlm.nih.gov/pubmed/17200679 [Accessed June 28, 2014]).