Inhibition of microRNA-181 reduces forebrain ischemia-induced neuronal loss

Journal of Cerebral Blood Flow and Metabolism

Volumn 33, Issue 12, 2013, Pages 1976-1982

  Moon, Jeong Mi ^a,b   Xu, Lijun ^a   Giffard, Rona G ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Chonnam National University Medical School   (South Korea)

Author keywords

Apoptosis; Astrocytes; Brain ischemia; Global ischemia; Glutamate; Hippocampus

Indexed keywords

ACTIN; ANTAGOMIR; CASPASE 3; CASPASE 7; MICRORNA; MICRORNA 181; PROTEIN BCL 2; UNCLASSIFIED DRUG; VESICULAR GLUTAMATE TRANSPORTER 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; ASTROCYTE; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CELL SURVIVAL; CONTROLLED STUDY; DENTATE GYRUS; DRUG INFUSION; FOREBRAIN; GENE EXPRESSION; HIPPOCAMPAL CA1 REGION; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT;

ANIMALS; APOPTOSIS; BRAIN; BRAIN ISCHEMIA; CELL LINE; CELLS, CULTURED; DOWN-REGULATION; EXCITATORY AMINO ACID TRANSPORTER 2; MALE; MICE; MICRORNAS; NEURONS; OLIGONUCLEOTIDES; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, SPRAGUE-DAWLEY; TRANSFECTION;

EID: 84889097694     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2013.157     Document Type: Article

References (41)

1. Kirino T, Tamura A, Sano K. Delayed neuronal death in the rat hippocampus following transient forebrain ischemia. Acta Neuropathol 1984; 64: 139-147. (Pubitemid 14096059)
2. Zola-Morgan S, Squire L, Amaral D. Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus. J Neurosci 1986; 6: 2950-2967. (Pubitemid 16026076)
3. Rempel-Clower NL, Zola SM, Squire LR, Amaral DG. Three cases of enduring memory impairment after bilateral damage limited to the hippocampal formation. J Neurosci 1996; 16: 5233-5255. (Pubitemid 26269682)
4. Bernard SA, Gray TW, Buist MD, Jones BM, Silvester W, Gutteridge G et al. Treatment of comatose survivors of out-of-hospital cardiac arrest with induced hypothermia. N Engl J Med 2002; 346: 557-563. (Pubitemid 34438816)
5. THACAS. Mild therapeutic hypothermia to improve the neurologic outcome after cardiac arrest. N Engl J Med 2002; 346: 549-556.
6. Padosch SA, Böttiger BW. Neuronal apoptosis following cerebral ischaemia: pathophysiology and possible therapeutic implications. Curr Opin Anesthesiol 2003; 16: 439-445. (Pubitemid 37297278)
7. Petito CK, Feldmann E, Pulsinelli WA, Plum F. Delayed hippocampal damage in humans following cardiorespiratory arrest. Neurology 1987; 37: 1281.
8. Teschendorf P, Padosch SA, Spöhr F, Albertsmeier M, Schneider A, Vogel P et al. Time course of caspase activation in selectively vulnerable brain areas following global cerebral ischemia due to cardiac arrest in rats. Neurosci Lett 2008; 448: 194-199.
9. Jeyaseelan K, Lim KY, Armugam A. MicroRNA expression in the blood and brain of rats subjected to transient focal ischemia by middle cerebral artery occlusion. Stroke 2008; 39: 959-966. (Pubitemid 351619577)
10. Dharap A, Bowen K, Place R, Li L-C, Vemuganti R. Transient focal ischemia induces extensive temporal changes in rat cerebral MicroRNAome. J Cereb Blood Flow Metab 2009; 29: 675-687.
11. Liu D-Z, Tian Y, Ander BP, Xu H, Stamova BS, Zhan X et al. Brain and blood microRNA expression profiling of ischemic stroke, intracerebral hemorrhage, and kainate seizures. J Cereb Blood Flow Metab 2010; 30: 92-101.
12. Shi G, Liu Y, Liu T, Yan W, Liu X, Wang Y et al. Upregulated miR-29b promotes neuronal cell death by inhibiting Bcl2L2 after ischemic brain injury. Exp Brain Res 2012; 216: 225-230.
13. Yin K-J, Deng Z, Huang H, Hamblin M, Xie C, Zhang J et al. miR-497 regulates neuronal death in mouse brain after transient focal cerebral ischemia. Neurobiol Dis 2010; 38: 17-26.
14. Ouyang Y-B, Lu Y, Yue S, Xu L-J, Xiong X-X, White RE et al. miR-181 regulates GRP78 and influences outcome from cerebral ischemia in vitro and in vivo. Neurobiol Dis 2012; 45: 555-563.
15. Chen C-Z, Li L, Lodish HF, Bartel DP. MicroRNAs modulate hematopoietic lineage differentiation. Science 2004; 303: 83-86. (Pubitemid 38055775)
16. Miska E, Alvarez Saavedra E, Townsend M, Yoshii A, Sestan N, Rakic P et al. Microarray analysis of microRNA expression in the developing mammalian brain. Genome Biol 2004; 5: R68.
17. Saba R, Störchel PH, Aksoy-Aksel A, Kepura F, Lippi G, Plant TD et al. Dopamineregulated microRNA MiR-181a controls GluA2 surface expression in hippocampal neurons. Mol Cell Biol 2012; 32: 619-632.
18. Ouyang Y-B, Lu Y, Yue S, Giffard RG. miR-181 targets multiple Bcl-2 family members and influences apoptosis and mitochondrial function in astrocytes. Mitochondrion 2012; 12: 213-219.
19. Dugan L, Bruno V, Amagasu S, Giffard R. Glia modulate the response of murine cortical neurons to excitotoxicity: glia exacerbate AMPA neurotoxicity. J Neurosci 1995; 15: 4545-4555.
20. Xu L, Koumenis IL, Tilly JL, Giffard RG. Overexpression of bcl-xL protects astrocytes from glucose deprivation and is associated with higher glutathione, ferritin, and iron levels. Anesthesiology 1999; 91: 1036.
21. Xu L, Emery JF, Ouyang Y-B, Voloboueva LA, Giffard RG. Astrocyte targeted overexpression of Hsp72 or SOD2 reduces neuronal vulnerability to forebrain ischemia. Glia 2010; 58: 1042-1049.
22. Ouyang Y-B, Voloboueva LA, Xu L-J, Giffard RG. Selective dysfunction of hippocampal CA1 astrocytes contributes to delayed neuronal damage after transient forebrain ischemia. J Neurosci 2007; 27: 4253-4260. (Pubitemid 46640722)
23. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2ΔΔDCT method. Methods 2001; 25: 402-408. (Pubitemid 34164012)
24. Linnik MD, Zahos P, Geschwind MD, Federoff HJ. Expression of bcl-2 from a defective herpes simplex virus-1 vector limits neuronal death in focal cerebral ischemia. Stroke 1995; 26: 1670-1675.
25. Zhao H, Yenari MA, Cheng D, Barreto-Chang OL, Sapolsky RM, Steinberg GK. Bcl-2 Transfection via herpes simplex virus blocks apoptosis-inducing factor translocation after focal ischemia in the rat. J Cereb Blood Flow Metab 2004; 24: 681-692. (Pubitemid 38725373)
26. Martinou J-C, Dubois-Dauphin M, Staple JK, Rodriguez I, Frankowski H, Missotten M et al. Overexpression of BCL-2 in transgenic mice protects neurons from naturally occurring cell death and experimental ischemia. Neuron 1994; 13: 1017-1030. (Pubitemid 24347313)
27. Xu L, Lee JE, Giffard RG. Overexpression of bcl-2, bcl-xL or hsp70 in murine cortical astrocytes reduces injury of co-cultured neurons. Neurosci Lett 1999; 277: 193-197.
28. Hutchison ER, Kawamoto EM, Taub DD, Lal A, Abdelmohsen K, Zhang Y et al. Evidence for miR-181 involvement in neuroinflammatory responses of astrocytes. Glia 2013; 61: 1018-1028.
29. Chen G, Zhu W, Shi D, Lv L, Zhang C, Liu P et al. MicroRNA-181a sensitizes human malignant glioma U87MG cells to radiation by targeting Bcl-2. Oncol Rep 2010; 23: 997-1003.
30. Su SF, Chang YW, Andreu-Vieyra C, Fang JY, Yang Z, Han B et al. miR-30d, miR-181a and miR-199a-5p cooperatively suppress the endoplasmic reticulum chaperone and signaling regulator GRP78 in cancer. Oncogene 2012.
31. Yuan Y, Wang JY, Xu LY, Cai R, Chen Z, Luo BY. MicroRNA expression changes in the hippocampi of rats subjected to global ischemia. J Clin Neurosci 2010; 17: 774-778.
32. Zhang W, Wang B, Zhou S, Qiu Y. The effect of ischemic post-conditioning on hippocampal cell apoptosis following global brain ischemia in rats. J Clin Neurosci 2012; 19: 570-573.
33. Hamby M, Sofroniew M. Reactive astrocytes as therapeutic targets for CNS disorders. Neurotherapeutics 2010; 7: 494-506.
34. Raghavendra Rao VL, Muralikrishna Rao A, Dogan A, Bowen KK, Hatcher J, Rothstein JD et al. Glial glutamate transporter GLT-1 down-regulation precedes delayed neuronal death in gerbil hippocampus following transient global cerebral ischemia. Neurochem Int 2000; 36: 531-537. (Pubitemid 30101565)
35. Liu Z, Huo W, Sun W, Lv M, Li F, Su Z. A sequential impairment of cortical astrocytes and GABAergic neurons during ischemia is improved by mGluR(1,5) activation. Neurol Sci 2013; 34: 1189-1195.
36. Kim DS, Kwak SE, Kim JE, Jung JY, Won MH, Choi SY et al. Transient ischaemia affects plasma membrane glutamate transporter, not vesicular glutamate transporter, expressions in the gerbil hippocampus. Anat Histol Embryol 2006; 35: 265-270.
37. Kettenmann H, Ransom BR (eds). Neuroglia. Oxford University Press: New York, NY, USA, 2012.
38. Nedergaard M, Ransom B, Goldman SA. New roles for astrocytes: redefining the functional architecture of the brain. Trends Neurosci 2003; 26: 523-530. (Pubitemid 37176906)
39. Takano T, Oberheim N, Cotrina ML, Nedergaard M. Astrocytes and ischemic injury. Stroke 2009; 40: S8-S12.
40. Zhang M, Li W-B, Geng J-X, Li Q-J, Sun X-C, Xian X-H et al. The upregulation of glial glutamate transporter-1 participates in the induction of brain ischemic tolerance in rats. J Cereb Blood Flow Metab 2007; 27: 1352-1368. (Pubitemid 46985352)
41. Zhang M, Li W-B, Liu Y-X, Liang C-J, Liu L-Z, Cui X et al. High expression of GLT-1 in hippocampal CA3 and dentate gyrus subfields contributes to their inherent resistance to ischemia in rats. Neurochem Int 2011; 59: 1019-1028.