Cortical spreading depression shifts cell fate determination of progenitor cells in the adult cortex

Journal of Cerebral Blood Flow and Metabolism

Volumn 32, Issue 10, 2012, Pages 1879-1887

  Tamura, Yasuhisa ^a   Eguchi, Asami ^a   Jin, Guanghua ^a   Sami, Mustafa M ^a   Kataoka, Yosky ^a  

^a RIKEN   (Japan)

Author keywords

astrocyte; brain recovery; glial cells; neural stem cells; spreading depression

Indexed keywords

BROXURIDINE; POTASSIUM CHLORIDE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; ASTROGENESIS; CELL FATE; CELL PROLIFERATION; CELLULAR PARAMETERS; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; MALE; NONHUMAN; OLIGODENDROGENESIS; OLIGODENDROGLIA; PRIORITY JOURNAL; RAT; SPREADING CORTICAL DEPRESSION; STEM CELL; STIMULUS RESPONSE;

ANIMALS; ANTIGENS; ASTROCYTES; BROMODEOXYURIDINE; CELL COUNT; CELL PROLIFERATION; CEREBRAL CORTEX; CORTICAL SPREADING DEPRESSION; IMMUNOHISTOCHEMISTRY; MALE; NEURAL STEM CELLS; OLIGODENDROGLIA; PROTEOGLYCANS; RATS; RATS, WISTAR; STEM CELLS;

EID: 84867090947     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2012.98     Document Type: Article

References (40)

1. Ayata C, Shin HK, Salomone S, Ozdemir-Gursoy Y, Boas DA, Dunn AK, Moskowitz MA (2004) Pronounced hypoperfusion during spreading depression in mouse cortex. J Cereb Blood Flow Metab 24: 1172-82 (Pubitemid 39332157)
2. Bonaguidi MA, McGuire T, Hu M, Kan L, Samanta J, Kessler JA (2005) LIF and BMP signaling generate separate and discrete types of GFAP-expressing cells. Development 132: 5503-14 (Pubitemid 43125877)
3. Bushong EA, Martone ME, Ellisman MH (2004) Maturation of astrocyte morphology and the establishment of astrocyte domains during postnatal hippocampal development. Int J Dev Neurosci 22: 73-86 (Pubitemid 38264165)
4. Canals S, Larrosa B, Pintor J, Mena MA, Herreras O (2008) Metabolic challenge to glia activates an adenosinemediated safety mechanism that promotes neuronal survival by delaying the onset of spreading depression waves. J Cereb Blood Flow Metab 28: 1835-44
5. Cassiani-Ingoni R, Coksaygan T, Xue H, Reichert-Scrivner SA, Wiendl H, Rao MS, Magnus T (2006) Cytoplasmic translocation of Olig2 in adult glial progenitors marks the generation of reactive astrocytes following autoimmune inflammation. Exp Neurol 201: 349-58 (Pubitemid 44344228)
6. Cui Y, Kataoka Y, Li QH, Yokoyama C, Yamagata A, Mochizuki-Oda N, Watanabe J, Yamada H, Watanabe Y (2003) Targeted tissue oxidation in the cerebral cortex induces local prolonged depolarization and cortical spreading depression in the rat brain. Biochem Biophys Res Commun 300: 631-6 (Pubitemid 36268882)
7. Dawson MR, Levine JM, Reynolds R (2000) NG2-expressing cells in the central nervous system: are they oligodendroglial progenitors? J Neurosci Res 61: 471-9
8. Dawson MR, Polito A, Levine JM, Reynolds R (2003) NG2-expressing glial progenitor cells: an abundant and widespread population of cycling cells in the adult rat CNS. Mol Cell Neurosci 24: 476-88 (Pubitemid 37311310)
9. Dayer AG, Cleaver KM, Abouantoun T, Cameron HA (2005) New GABAergic interneurons in the adult neocortex and striatum are generated from different precursors. J Cell Biol 168: 415-27 (Pubitemid 40205064)
10. Dimou L, Simon C, Kirchhoff F, Takebayashi H, Gotz M (2008) Progeny of Olig2-expressing progenitors in the gray and white matter of the adult mouse cerebral cortex. J Neurosci 28: 10434-42
11. Fabricius M, Akgoren N, Lauritzen M (1995) Argininenitric oxide pathway and cerebrovascular regulation in cortical spreading depression. Am J Physiol 269: H23-9
12. Fabricius M, Fuhr S, Bhatia R, Boutelle M, Hashemi P, Strong AJ, Lauritzen M (2006) Cortical spreading depression and peri-infarct depolarization in acutely injured human cerebral cortex. Brain 129: 778-90 (Pubitemid 43278239)
13. Gomes WA, Mehler MF, Kessler JA (2003) Transgenic overexpression of BMP4 increases astroglial and decreases oligodendroglial lineage commitment. Dev Biol 255: 164-77 (Pubitemid 36287148)
14. Grinspan JB, Edell E, Carpio DF, Beesley JS, Lavy L, Pleasure D, Golden JA (2000) Stage-specific effects of bone morphogenetic proteins on the oligodendrocyte lineage. J Neurobiol 43: 1-17 (Pubitemid 30191176)
15. Guo F, Ma J, McCauley E, Bannerman P, Pleasure D (2009) Early postnatal proteolipid promoter-expressing progenitors produce multilineage cells in vivo. J Neurosci 29: 7256-70
16. Hampton DW, Rhodes KE, Zhao C, Franklin RJ, Fawcett JW (2004) The responses of oligodendrocyte precursor cells, astrocytes and microglia to a cortical stab injury, in the brain. Neuroscience 127: 813-20 (Pubitemid 39099547)
17. James MF, Smith JM, Boniface SJ, Huang CL, Leslie RA (2001) Cortical spreading depression and migraine: new insights from imaging? Trends Neurosci 24: 266-71 (Pubitemid 32304468)
18. Kataoka Y, Tamura Y, Takamori Y, Cui Y, Yamada H (2006) Perineuronal germinal cells in the rat cerebral cortex. Med Mol Morphol 39: 28-32 (Pubitemid 44306508)
19. Komitova M, Zhu X, Serwanski DR, Nishiyama A (2009) NG2 cells are distinct from neurogenic cells in the postnatal mouse subventricular zone. J Comp Neurol 512: 702-16
20. Larrosa B, Pastor J, Lopez-Aguado L, Herreras O (2006) A role for glutamate and glia in the fast network oscillations preceding spreading depression. Neuroscience 141: 1057-68 (Pubitemid 44066647)
21. Lian XY, Stringer JL (2004a) Astrocytes contribute to regulation of extracellular calcium and potassium in the rat cerebral cortex during spreading depression. Brain Res 1012: 177-84 (Pubitemid 38648913)
22. Lian XY, Stringer JL (2004b) Inhibition of aconitase in astrocytes increases the sensitivity to chemical convulsants. Epilepsy Res 60: 41-52 (Pubitemid 38981760)
23. Lian XY, Stringer JL (2004c) Energy failure in astrocytes increases the vulnerability of neurons to spreading depression. Eur J Neurosci 19: 2446-54 (Pubitemid 38621842)
24. Magnus T, Coksaygan T, Korn T, Xue H, Arumugam TV, Mughal MR, Eckley DM, Tang SC, Detolla L, Rao MS, Cassiani-Ingoni R, Mattson MP (2007) Evidence that nucleocytoplasmic Olig2 translocation mediates braininjury-induced differentiation of glial precursors to astrocytes. J Neurosci Res 85: 2126-37 (Pubitemid 47172144)
25. Nakanishi M, Niidome T, Matsuda S, Akaike A, Kihara T, Sugimoto H (2007) Microglia-derived interleukin-6 and leukaemia inhibitory factor promote astrocytic differentiation of neural stem/progenitor cells. Eur J Neurosci 25: 649-58
26. Nedergaard M, Hansen AJ (1993) Characterization of cortical depolarizations evoked in focal cerebral ischemia. J Cereb Blood Flow Metab 13: 568-74 (Pubitemid 23187499)
27. Rivers LE, Young KM, Rizzi M, Jamen F, Psachoulia K, Wade A, Kessaris N, Richardson WD (2008) PDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice. Nat Neurosci 11: 1392-401
28. See J, Zhang X, Eraydin N, Mun SB, Mamontov P, Golden JA, Grinspan JB (2004) Oligodendrocyte maturation is inhibited by bone morphogenetic protein. Mol Cell Neurosci 26: 481-92 (Pubitemid 38969946)
29. Strong AJ, Fabricius M, Boutelle MG, Hibbins SJ, Hopwood SE, Jones R, Parkin MC, Lauritzen M (2002) Spreading and synchronous depressions of cortical activity in acutely injured human brain. Stroke 33: 2738-43 (Pubitemid 35462836)
30. Tamura Y, Kataoka Y, Cui Y, Takamori Y, Watanabe Y, Yamada H (2007a) Multi-directional differentiation of doublecortin-and NG2-immunopositive progenitor cells in the adult rat neocortex in vivo. Eur J Neurosci 25: 3489-98 (Pubitemid 47020456)
31. Tamura Y, Kataoka Y, Cui Y, Takamori Y, Watanabe Y, Yamada H (2007b) Intracellular translocation of glutathione S-transferase pi during oligodendrocyte differentiation in adult rat cerebral cortex in vivo. Neuroscience 148: 535-40 (Pubitemid 47362505)
32. Tamura Y, Kataoka Y, Cui Y, Yamada H (2004) Cellular proliferation in the cerebral cortex following neural excitation in rats. Neurosci Res 50: 129-33 (Pubitemid 39024309)
33. Tatsumi K, Takebayashi H, Manabe T, Tanaka KF, Makinodan M, Yamauchi T, Makinodan E, Matsuyoshi H, Okuda H, Ikenaka K, Wanaka A (2008) Genetic fate mapping of Olig2 progenitors in the injured adult cerebral cortex reveals preferential differentiation into astrocytes. J Neurosci Res 86: 3494-502
34. Tripathi RB, Rivers LE, Young KM, Jamen F, Richardson WD (2010) NG2 glia generate new oligodendrocytes but few astrocytes in a murine experimental autoimmune encephalomyelitis model of demyelinating disease. J Neurosci 30: 16383-90
35. White BD, Nathe RJ, Maris DO, Nguyen NK, Goodson JM, Moon RT, Horner PJ (2010) Beta-catenin signaling increases in proliferating NG2+ progenitors and astro-cytes during post-traumatic gliogenesis in the adult brain. Stem Cells 28: 297-307
36. Willoughby JO, Mackenzie L, Broberg M, Thoren AE, Medvedev A, Sims NR, Nilsson M (2003) Fluorocitratemediated astroglial dysfunction causes seizures. J Neurosci Res 74: 160-6 (Pubitemid 37176679)
37. Xiong ZQ, Stringer JL (1999) Astrocytic regulation of the recovery of extracellular potassium after seizures in vivo. Eur J Neurosci 11: 1677-84 (Pubitemid 29192243)
38. Yanamoto H, Miyamoto S, Tohnai N, Nagata I, Xue JH, Nakano Y, Nakajo Y, Kikuchi H (2005) Induced spreading depression activates persistent neurogenesis in the subventricular zone, generating cells with markers for divided and early committed neurons in the caudate putamen and cortex. Stroke 36: 1544-50 (Pubitemid 40967527)
39. Zhao JW, Raha-Chowdhury R, Fawcett JW, Watts C (2009) Astrocytes and oligodendrocytes can be generated from NG2+ progenitors after acute brain injury: intracellular localization of oligodendrocyte transcription factor 2 is associated with their fate choice. Eur J Neurosci 29: 1853-69
40. Zhu X, Bergles DE, Nishiyama A (2008) NG2 cells generate both oligodendrocytes and gray matter astrocytes. Development 135: 145-57 (Pubitemid 351201488)