Loss of miR-29b following acute ischemic stroke contributes to neural cell death and infarct size

Journal of Cerebral Blood Flow and Metabolism

Volumn 33, Issue 8, 2013, Pages 1197-1206

  Khanna, Savita ^a   Rink, Cameron ^a   Ghoorkhanian, Reza ^a   Gnyawali, Surya ^a   Heigel, Mallory ^a   Wijesinghe, Dayanjan S ^b,c   Chalfant, Charles E ^b,c,d   Chan, Yuk Cheung ^a   Banerjee, Jaideep ^a   Huang, Yue ^a   Roy, Sashwati ^a   Sen, Chandan K ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^d VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

12 lipoxygenase; arachidonic acid; brain; microRNA; stroke

Indexed keywords

ALPHA TOCOTRIENOL; ARACHIDONATE 12 LIPOXYGENASE; ARACHIDONIC ACID; GLUTATHIONE; ICOSANOID; MICRORNA; MICRORNA 29B; MICRORNA 29C; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARACHIDONIC ACID METABOLISM; ARTICLE; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; BRAIN NERVE CELL; CELL FUNCTION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVITY; IN VIVO STUDY; KNOCKOUT MOUSE; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NERVE CELL NECROSIS; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIMARY SOMATOSENSORY CORTEX; PRIORITY JOURNAL;

ANIMALS; ANTIOXIDANTS; ARACHIDONATE 12-LIPOXYGENASE; BLOTTING, WESTERN; BRAIN ISCHEMIA; CELL DEATH; CELL SURVIVAL; CELLS, CULTURED; CEREBRAL INFARCTION; EICOSANOIDS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GLUTATHIONE; MAGNETIC RESONANCE IMAGING; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, INBRED C57BL; MICRORNAS; NEURONS; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; REAL-TIME POLYMERASE CHAIN REACTION; RNA; RNA, SMALL INTERFERING; STROKE; TOCOTRIENOLS; TRANSFECTION;

EID: 84881142515     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2013.68     Document Type: Article

References (43)

1. Kriegel AJ, Liu Y, Fang Y, Ding X, Liang M. The miR-29 family: genomics, cell biology, and relevance to renal and cardiovascular injury. Physiol Genomics 2012; 44: 237-244.
2. Hebert SS, Horre K, Nicolai L, Papadopoulou AS, Mandemakers W, Silahtaroglu AN et al. Loss of microRNA cluster miR-29a/b-1 in sporadic Alzheimer's disease correlates with increased BACE1/beta-secretase expression. Proc Natl Acad Sci USA 2008; 105: 6415-6420.
3. Kole AJ, Swahari V, Hammond SM, Deshmukh M. miR-29b is activated during neuronal maturation and targets BH3-only genes to restrict apoptosis. Genes Dev 2011; 25: 125-130.
4. Adibhatla RM, Hatcher JF, Dempsey RJ. Effects of citicoline on phospholipid and glutathione levels in transient cerebral ischemia. Stroke 2001; 32: 2376-2381.
5. de Bilbao F, Arsenijevic D, Moll T, Garcia-Gabay I, Vallet P, Langhans W et al. In vivo over-expression of interleukin-10 increases resistance to focal brain ischemia in mice. J Neurochem 2009; 110: 12-22.
6. Yoshida S, Inoh S, Asano T, Sano K, Kubota M, Shimazaki H et al. Effect of transient ischemia on free fatty-acids and phospholipids in the gerbil brain-lipid-peroxidation as a possible cause of post-ischemic injury. J Neurosurg 1980; 53: 323-331.
7. Khanna S, Roy S, Slivka A, Craft TK, Chaki S, Rink C et al. Neuroprotective properties of the natural vitamin E alpha-tocotrienol. Stroke 2005; 36: 2258-2264.
8. Jin G, Arai K, Murata Y, Wang S, Stins MF, Lo EH et al. Protecting against cerebrovascular injury: contributions of 12/15-lipoxygenase to edema formation after transient focal ischemia. Stroke 2008; 39: 2538-2543.
9. Khanna S, Parinandi NL, Kotha SR, Roy S, Rink C, Bibus D et al. Nanomolar vitamin E alpha-tocotrienol inhibits glutamate-induced activation of phospholipase A2 and causes neuroprotection. J Neurochem 2010; 112: 1249-1260.
10. Khanna S, Park HA, Sen CK, Golakoti T, Sengupta K, Venkateswarlu S et al. Neuroprotective and antiinflammatory properties of a novel demethylated curcuminoid. Antioxid Redox Signal 2009; 11: 449-468.
11. Khanna S, Roy S, Park HA, Sen CK. Regulation of c-Src activity in glutamateinduced neurodegeneration. J Biol Chem 2007; 282: 23482-23490.
12. Khanna S, Roy S, Ryu H, Bahadduri P, Swaan PW, Ratan RR et al. Molecular basis of vitamin E action: tocotrienol modulates 12-lipoxygenase, a key mediator of glutamate-induced neurodegeneration. J Biol Chem 2003; 278: 43508-43515.
13. Park HA, Khanna S, Rink C, Gnyawali S, Roy S, Sen CK. Glutathione disulfide induces neural cell death via a 12-lipoxygenase pathway. Cell Death Differ 2009; 16: 1167-1179.
14. Sen CK, Khanna S, Roy S, Packer L. Molecular basis of vitamin E action. Tocotrienol potently inhibits glutamate-induced pp60(c-Src) kinase activation and death of HT4 neuronal cells. J Biol Chem 2000; 275: 13049-13055.
15. Tirosh O, Sen CK, Roy S, Kobayashi MS, Packer L. Neuroprotective effects of alphalipoic acid and its positively charged amide analogue. Free Radic Biol Med 1999; 26: 1418-1426.
16. Tirosh O, Sen CK, Roy S, Packer L. Cellular and mitochondrial changes in glutamate-induced HT4 neuronal cell death. Neuroscience 2000; 97: 531-541.
17. Park HA, Kubicki N, Gnyawali S, Chan YC, Roy S, Khanna S et al. Natural vitamin E alpha-tocotrienol protects against ischemic stroke by induction of multidrug resistance-associated protein 1. Stroke 2011; 42: 2308-2314.
18. Han D, Sen CK, Roy S, Kobayashi MS, Tritschler HJ, Packer L. Protection against glutamate-induced cytotoxicity in C6 glial cells by thiol antioxidants. Am J Physiol 1997; 273: R1771-R1778.
19. Chan YC, Khanna S, Roy S, Sen CK. miR-200b targets Ets-1 and is down-regulated by hypoxia to induce angiogenic response of endothelial cells. J Biol Chem 2011; 286: 2047-2056.
20. Khanna S, Roy S, Parinandi NL, Maurer M, Sen CK. Characterization of the potent neuroprotective properties of the natural vitamin E alpha-tocotrienol. J Neurochem 2006; 98: 1474-1486.
21. Roy S, Khanna S, Hussain SR, Biswas S, Azad A, Rink C et al. MicroRNA expression in response to murine myocardial infarction: miR-21 regulates fibroblast metalloprotease-2 via phosphatase and tensin homologue. Cardiovasc Res 2009; 82: 21-29.
22. Jamaluddin MS, Wang X, Wang H, Rafael C, Yao Q, Chen C. Eotaxin increases monolayer permeability of human coronary artery endothelial cells. Arterioscler Thromb Vasc Biol 2009; 29: 2146-2152.
23. Tang Y, Scheef EA, Wang S, Sorenson CM, Marcus CB, Jefcoate CR et al. CYP1B1 expression promotes the proangiogenic phenotype of endothelium through decreased intracellular oxidative stress and thrombospondin-2 expression. Blood 2009; 113: 744-754.
24. Hussain SR, Lucas DM, Johnson AJ, Lin TS, Bakaletz AP, Dang VX et al. Flavopiridol causes early mitochondrial damage in chronic lymphocytic leukemia cells with impaired oxygen consumption and mobilization of intracellular calcium. Blood 2008; 111: 3190-3199.
25. Tirosh O, Guo Q, Sen CK, Packer L. Mitochondrial control of inducible nitric oxide production in stimulated RAW 264.7 macrophages. Antioxid Redox Signal 2001; 3: 711-719.
26. Rink C, Gnyawali S, Peterson L, Khanna S. Oxygen-inducible glutamate oxaloacetate transaminase as protective switch transforming neurotoxic glutamate to metabolic fuel during acute ischemic stroke. Antioxid Redox Signal 2011; 14: 1777-1785.
27. Rink C, Roy S, Khan M, Ananth P, Kuppusamy P, Sen CK et al. Oxygen-sensitive outcomes and gene expression in acute ischemic stroke. J Cereb Blood Flow Metab 2010; 30: 1275-1287.
28. Loubinoux I, Volk A, Borredon J, Guirimand S, Tiffon B, Seylaz J et al. Spreading of vasogenic edema and cytotoxic edema assessed by quantitative diffusion and T2 magnetic resonance imaging. Stroke 1997; 28: 419-426, discussion 426-7.
29. Chan YC, Roy S, Khanna S, Sen CK. Downregulation of endothelial microRNA-200b supports cutaneous wound angiogenesis by desilencing GATA-binding protein 2 and vascular endothelial growth factor receptor 2. Arterioscler Thromb Vasc Biol 2012; 32: 1372-1382.
30. Rink C, Christoforidis G, Khanna S, Peterson L, Patel Y, Abduljalil A et al. Tocotrienol vitamin E protects against preclinical canine ischemic stroke by inducing arteriogenesis. J Cereb Blood Flow Metab 2011; 31: 2218-2230.
31. Higuchi Y, Yoshimoto T. Arachidonic acid converts the glutathione depletion-induced apoptosis to necrosis by promoting lipid peroxidation and reducing caspase-3 activity in rat glioma cells. Arch Biochem Biophys 2002; 400: 133-140.
32. Kwon KJ, Jung YS, Lee SH, Moon CH, Baik EJ. Arachidonic acid induces neuronal death through lipoxygenase and cytochrome P450 rather than cyclooxygenase. J Neurosci Res 2005; 81: 73-84.
33. Patel V, Rink C, Gordillo GM, Khanna S, Gnyawali U, Roy S et al. Oral tocotrienols are transported to human tissues and delay the progression of the model for endstage liver disease score in patients. J Nutr 2012; 142: 513-519.
34. Rink C, Khanna S. MicroRNA in ischemic stroke etiology and pathology. Physiol Genomics 2011; 43: 521-528.
35. Schmitt MJ, Margue C, Behrmann I, Kreis S. miRNA-29: A microRNA family with tumor-suppressing and immune-modulating properties. Curr Mol Med 2012; 13: 572-585.
36. Wang L, Zhou L, Jiang P, Lu L, Chen X, Lan H et al. Loss of miR-29 in myoblasts contributes to dystrophic muscle pathogenesis. Mol Ther 2012; 20: 1222-1233.
37. Wang XH, Hu Z, Klein JD, Zhang L, Fang F, Mitch WE. Decreased miR-29 suppresses myogenesis in CKD. J Am Soc Nephrol 2011; 22: 2068-2076.
38. Xiao J, Meng XM, Huang XR, Chung AC, Feng YL, Hui DS et al. miR-29 inhibits bleomycin-induced pulmonary fibrosis in mice. Mol Ther 2012; 20: 1251-1260.
39. Rink C, Khanna S. Significance of brain tissue oxygenation and the arachidonic acid cascade in stroke. Antioxid Redox Signal 2011; 14: 1889-1903.
40. Adibhatla RM, Hatcher JF. Lipid oxidation and peroxidation in CNS health and disease: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal 2010; 12: 125-169.
41. Canals S, Casarejos MJ, de Bernardo S, Rodriguez-Martin E, Mena MA. Nitric oxide triggers the toxicity due to glutathione depletion in midbrain cultures through 12-lipoxygenase. J Biol Chem 2003; 278: 21542-21549.
42. Gong PF, Cederbaum AI. Transcription factor Nrf2 protects HepG2 cells against CYP2E1 plus arachidonic acid-dependent toxicity. J Biol Chem 2006; 281: 14573-14579.
43. Pizzimenti S, Ferracin M, Sabbioni S, Toaldo C, Pettazzoni P, Dianzani MU et al. MicroRNA expression changes during human leukemic HL-60 cell differentiation induced by 4-hydroxynonenal, a product of lipid peroxidation. Free Radic Biol Med 2009; 46: 282-288.