Ependymal ciliary dysfunction and reactive astrocytosis in a reorganized subventricular zone after stroke

Cerebral Cortex

Volumn 23, Issue 3, 2013, Pages 647-659

  Young, Christopher C ^a   Van Der Harg, Judith M ^a   Lewis, Nicola J ^a   Brooks, Keith J ^b   Buchan, Alastair M ^b   Szele, Francis G ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

cerebrospinal fluid; ependymal cells; neurogenesis; planar cell polarity; reactive astrocytes; stroke; subventricular zone

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; ASTROCYTOSIS; CELL DIVISION; CELL POLARITY; CELL PROLIFERATION; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; EPENDYMA CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SUBVENTRICULAR ZONE;

EID: 84873621145     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhs049     Document Type: Article

References (72)

1. Altman J, Das GD. 1966. Autoradiographic and histological studies of postnatal neurogenesis. I. A longitudinal investigation of the kinetics, migration and transformation of cells incorporating tritiated thymidine in neonate rats, with special reference to postnatal neurogenesis in some brain regions. J Comp Neurol. 126:337-389.
2. Anton ES, Ghashghaei HT, Weber JL, McCann C, Fischer TM, Cheung ID, Gassmann M, Messing A, Klein R, Schwab MH, et al. 2004. Receptor tyrosine kinase ErbB4 modulates neuroblast migration and placement in the adult forebrain. Nat Neurosci. 7:1319-1328.
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. Attwell D, Buchan AM, Charpak S, Lauritzen M, Macvicar BA, Newman EA. 2010. Glial and neuronal control of brain blood flow. Nature. 468:232-243.
5. Barber PA, Hoyte L, Colbourne F, Buchan AM. 2004. Temperatureregulated model of focal ischemia in the mouse: a study with histopathological and behavioral outcomes. Stroke. 35:1720-1725.
6. Bolteus AJ, Bordey A. 2004. GABA release and uptake regulate neuronal precursor migration in the postnatal subventricular zone. J Neurosci. 24:7623-7631.
7. Buffo A, Rite I, Tripathi P, Lepier A, Colak D, Horn AP, Mori T, Gotz M. 2008. Origin and progeny of reactive gliosis: a source of multipotent cells in the injured brain. Proc Natl Acad Sci U S A. 105:3581-3586.
8. 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.
9. Comte I, Kim Y, Young CC, van der Harg JM, Hockberger P, Bolam PJ, Poirier F, Szele FG. 2011. Galectin-3 maintains cell motility from the subventricular zone to the olfactory bulb. J Cell Sci. 124:2438-2447.
10. Cooper O, Isacson O. 2004. Intrastriatal transforming growth factor alpha delivery to a model of Parkinson's disease induces proliferation and migration of endogenous adult neural progenitor cells without differentiation into dopaminergic neurons. J Neurosci. 24:8924-8931.
11. Del Bigio MR. 2010. Ependymal cells: biology and pathology. Acta Neuropathol. 119:55-73.
12. Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A. 1999. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell. 97:703-716.
13. Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A. 1997. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci. 17:5046-5061.
14. Doetsch F, Petreanu L, Caille I, Garcia-Verdugo JM, Alvarez-Buylla A. 2002. EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron. 36:1021-1034.
15. Endres M, Namura S, Shimizu-Sasamata M, Waeber C, Zhang L, Gomez-Isla T, Hyman BT, Moskowitz MA. 1998. Attenuation of delayed neuronal death after mild focal ischemia in mice by inhibition of the caspase family. J Cereb Blood Flow Metab. 18:238-247.
16. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn A-M, Nordborg C, Peterson DA, Gage FH. 1998. Neurogenesis in the adult human hippocampus. Nat Med. 4:1313-1317.
17. Ganat Y, Soni S, Chacon M, Schwartz ML, Vaccarino FM. 2002. Chronic hypoxia up-regulates fibroblast growth factor ligands in the perinatal brain and induces fibroblast growth factor-responsive radial glial cells in the sub-ependymal zone. Neuroscience. 112:977-991.
18. Garcia AD, Doan NB, Imura T, Bush TG, Sofroniew MV. 2004. GFAPexpressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat Neurosci. 7:1233-1241.
19. Gleason D, Fallon JH, Guerra M, Liu JC, Bryant PJ. 2008. Ependymal stem cells divide asymmetrically and transfer progeny into the subventricular zone when activated by injury. Neuroscience. 156:81-88.
20. Goings GE, Kozlowski DA, Szele FG. 2006. Differential activation of microglia in neurogenic versus non-neurogenic regions of the forebrain. Glia. 54:329-342.
21. Gotts JE, Chesselet MF. 2005. Vascular changes in the subventricular zone after distal cortical lesions. Exp Neurol. 194:139-150.
22. Gregg C, Weiss S. 2003. Generation of functional radial glial cells by embryonic and adult forebrain neural stem cells. J Neurosci. 23:11587-11601.
23. 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.
24. 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 U S A. 107:7993-7998.
25. Johanson C, Stopa E, McMillan P, Roth D, Funk J, Krinke G. 2011. The distributional nexus of choroid plexus to cerebrospinal fluid, ependyma and brain: toxicologic/pathologic phenomena, periventricular destabilization, and lesion spread. Toxicol Pathol. 39:186-212.
26. Johansson CB, Momma S, Clarke DL, Risling M, Lendahl U, Frisen J. 1999. Identification of a neural stem cell in the adult mammalian central nervous system. Cell. 96:25-34.
27. Kaneko N, Marin O, Koike M, Hirota Y, Uchiyama Y, Wu JY, Lu Q, Tessier-Lavigne M, Alvarez-Buylla A, Okano H, et al. 2010. New neurons clear the path of astrocytic processes for their rapid migration in the adult brain. Neuron. 67:213-223.
28. Kim Y, Wang WZ, Comte I, Pastrana E, Tran PB, Brown J, Miller RJ, Doetsch F, Molnar Z, Szele FG. 2010. Dopamine stimulation of postnatal murine subventricular zone neurogenesis via the D3 receptor. J Neurochem. 114:750-760.
29. 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.
30. Kokovay E, Goderie S, Wang Y, Lotz S, Lin G, Sun Y, Roysam B, Shen Q, Temple S. 2010. Adult SVZ lineage cells home to and leave the vascular niche via differential responses to SDF1/CXCR4 signaling. Cell Stem Cell. 7:163-173.
31. Kornack DR, Rakic P. 2001. The generation, migration, and differentiation of olfactory neurons in the adult primate brain. Proc Natl Acad Sci U S A. 98:4752-4757.
32. Lehtinen MK, Walsh CA. 2011. Neurogenesis at the brain-cerebrospinal fluid interface. Annu Rev Cell Dev Biol. 27:653-679.
33. Lewis PD. 1968. Mitotic activity in the primate subependymal layer and the genesis of gliomas. Nature. 217:974-975.
34. Li L, Harms KM, Ventura PB, Lagace DC, Eisch AJ, Cunningham LA. 2010. Focal cerebral ischemia induces a multilineage cytogenic response from adult subventricular zone that is predominantly gliogenic. Glia. 58:1610-1619.
35. Li L, Lundkvist A, Andersson D, Wilhelmsson U, Nagai N, Pardo AC, Nodin C, Stahlberg A, Aprico K, Larsson K, et al. 2008. Protective role of reactive astrocytes in brain ischemia. J Cereb Blood Flow Metab. 28:468-481.
36. Lim DA, Tramontin AD, Trevejo JM, Herrera DG, Garc?a-Verdugo JM, Alvarez-Buylla A. 2000. Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron. 28:713-726.
37. Lin TN, He YY, Wu G, Khan M, Hsu CY. 1993. Effect of brain edema on infarct volume in a focal cerebral ischemia model in rats. Stroke. 24:117-121.
38. Lois C, Alvarez-Buylla A. 1993. Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc Natl Acad Sci U S A. 90:2074-2077.
39. Lu YB, Iandiev I, Hollborn M, Korber N, Ulbricht E, Hirrlinger PG, Pannicke T, Wei EQ, Bringmann A, Wolburg H, et al. 2011. Reactive glial cells: increased stiffness correlates with increased intermediate filament expression. Faseb J. 25:624-631.
40. Luo J, Shook BA, Daniels SB, Conover JC. 2008. Subventricular zonemediated ependyma repair in the adult mammalian brain. J Neurosci. 28:3804-3813.
41. Macas J, Nern C, Plate KH, Momma S. 2006. Increased generation of neuronal progenitors after ischemic injury in the aged adult human forebrain. J Neurosci. 26:13114-13119.
42. Martinez-Molina N, Kim Y, Hockberger P, Szele FG. 2011. Rostral migratory stream neuroblasts turn and change directions in stereotypic patterns. Cell Adh Migr. 5:83-95.
43. McDermott KW, Lantos PL. 1990. Cell proliferation in the subependymal layer of the postnatal marmoset, Callithrix jacchus. Brain Res Dev Brain Res. 57:269-277.
44. 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 U S A. 101:17528-17532.
45. Mirzadeh Z, Doetsch F, Sawamoto K, Wichterle H, Alvarez-Buylla A. 2010. The subventricular zone en-face: wholemount staining and ependymal flow. J Vis Exp. doi: 10.3791/1938.
46. Mirzadeh Z, Han YG, Soriano-Navarro M, Garcia-Verdugo JM, Alvarez-Buylla A. 2010. Cilia organize ependymal planar polarity. J Neurosci. 30:2600-2610.
47. Mirzadeh Z, Merkle FT, Soriano-Navarro M, Garcia-Verdugo JM, Alvarez-Buylla A. 2008. Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell. 3:265-278.
48. Nam SC, Kim Y, Dryanovski D, Walker A, Goings G, Woolfrey K, Kang SS, Chu C, Chenn A, Erdelyi F, et al. 2007. Dynamic features of postnatal subventricular zone cell motility: a two-photon time-lapse study. J Comp Neurol. 505:190-208.
49. Nie K, Molnar Z, Szele FG. 2010. Proliferation but not migration is associated with blood vessels during development of the rostral migratory stream. Dev Neurosci. 32:163-172.
50. Nomura T, Goritz C, Catchpole T, Henkemeyer M, Frisen J. 2010. EphB signaling controls lineage plasticity of adult neural stem cell niche cells. Cell Stem Cell. 7:730-743.
51. Ohab JJ, Fleming S, Blesch A, Carmichael ST. 2006. A neurovascular niche for neurogenesis after stroke. J Neurosci. 26:13007-13016.
52. Ortinski PI, Dong J, Mungenast A, Yue C, Takano H, Watson DJ, Haydon PG, Coulter DA. 2010. Selective induction of astrocytic gliosis generates deficits in neuronal inhibition. Nat Neurosci. 13:584-591.
53. Parent JM, Valentin VV, Lowenstein DH. 2002. Prolonged seizures increase proliferating neuroblasts in the adult rat subventricular zone-olfactory bulb pathway. J Neurosci. 22:3174-3188.
54. Pekny M, Johansson CB, Eliasson C, Stakeberg J, Wallen A, Perlmann T, Lendahl U, Betsholtz C, Berthold CH, Frisen J. 1999. Abnormal reaction to central nervous system injury in mice lacking glial fibrillary acidic protein and vimentin. J Cell Biol. 145:503-514.
55. Pham M, Helluy X, Braeuninger S, Jakob P, Stoll G, Kleinschnitz C, Bendszus M. 2010. Outcome of experimental stroke in C57Bl/6 and Sv/129 mice assessed by multimodal ultra-high field MRI. Exp Transl Stroke Med. 2:6.
56. Reynolds BA, Weiss S. 1992. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science. 255:1707-1710.
57. Sanai N, Nguyen T, Ihrie RA, Mirzadeh Z, Tsai HH, Wong M, Gupta N, Berger MS, Huang E, Garcia-Verdugo JM, et al. 2011. Corridors of migrating neurons in the human brain and their decline during infancy. Nature. 478:382-386.
58. Sawamoto K, Wichterle H, Gonzalez-Perez O, Cholfin JA, Yamada M, Spassky N, Murcia NS, Garcia-Verdugo JM, Marin O, Rubenstein JLR, et al. 2006. New neurons follow the flow of cerebrospinal fluid in the adult brain. Science. 311:629-632.
59. Shen Q, Goderie SK, Jin L, Karanth N, Sun Y, Abramova N, Vincent P, Pumiglia K, Temple S. 2004. Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science. 304:1338-1340.
60. Shen Q, Wang Y, Kokovay E, Lin G, Chuang SM, Goderie SK, Roysam B, Temple S. 2008. Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions. Cell Stem Cell. 3:289-300.
61. Snapyan M, Lemasson M, Brill MS, Blais M, Massouh M, Ninkovic J, Gravel C, Berthod F, Gotz M, Barker PA, et al. 2009. Vasculature guides migrating neuronal precursors in the adult mammalian forebrain via brain-derived neurotrophic factor signaling. J Neurosci. 29:4172-4188.
62. Spassky N, Merkle FT, Flames N, Tramontin AD, Garcia-Verdugo JM, Alvarez-Buylla A. 2005. Adult ependymal cells are postmitotic and are derived from radial glial cells during embryogenesis. J Neurosci. 25:10-18.
63. Szele FG, Chesselet MF. 1996. Cortical lesions induce an increase in cell number and PSA-N-CAM expression in the subventricular zone of adult rats. J Comp Neurol. 368:439-454.
64. Tavazoie M, Van der Veken L, Silva-Vargas V, Louissaint M, Colonna L, Zaidi B, Garcia-Verdugo JM, Doetsch F. 2008. A specialized vascular niche for adult neural stem cells. Cell Stem Cell. 3:279-288.
65. Thomas LB, Gates MA, Steindler DA. 1996. Young neurons from the adult subependymal zone proliferate and migrate along an astrocyte, extracellular matrix-rich pathway. Glia. 17:1-14.
66. 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.
67. Weller RO, Mitchell J, Griffin RL, Gardner MJ. 1978. The effects of hydrocephalus upon the developing brain. Histological and quantitative studies of the ependyma and subependyma in hydrocephalic rats. J Neurol Sci. 36:383-402.
68. White BD, Nathe RJ, Maris DO, Nguyen NK, Goodson JM, Moon RT, Horner PJ. 2009. Beta-catenin signaling increases in proliferating NG2+ progenitors and astrocytes during posttraumatic gliogenesis in the adult brain. Stem Cells. 28:297-307.
69. Wilhelmsson U, Li L, Pekna M, Berthold CH, Blom S, Eliasson C, Renner O, Bushong E, Ellisman M, Morgan TE, et al. 2004. Absence of glial fibrillary acidic protein and vimentin prevents hypertrophy of astrocytic processes and improves post-traumatic regeneration. J Neurosci. 24:5016-5021.
70. Young CC, Brooks KJ, Buchan AM, Szele FG. 2010. Cellular and molecular determinants of stroke-induced changes in subventricular zone cell migration. Antioxid Redox Signal. 14:1877-1888.
71. 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.
72. Zhang RL, Zhang ZG, Wang Y, LeTourneau Y, Liu XS, Zhang X, Gregg SR, Wang L, Chopp M. 2007. 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.