Down-regulation of miRNA-30a alleviates cerebral ischemic injury through enhancing Beclin 1-mediated autophagy

Neurochemical Research

Volumn 39, Issue 7, 2014, Pages 1279-1291

  Wang, Peng ^a,b   Liang, Jia ^b   Li, Yun ^a   Li, Jiefei ^a   Yang, Xuan ^a   Zhang, Xinxin ^a   Han, Song ^a   Li, Shujuan ^c   Li, Junfa ^a  

^a BEIJING INSTITUTE FOR BRAIN DISORDERS   (China)

^b JINZHOU MEDICAL UNIVERSITY   (China)

^c CAPITAL MEDICAL UNIVERSITY   (China)

Author keywords

Autophagy; Beclin 1; Ischemic stroke; Microtubule associated protein 1 light chain 3 (LC3); miRNA 30a; Oxygen glucose deprivation (OGD)

Indexed keywords

BECLIN 1; MICRORNA; MICRORNA 30A; MICROTUBULE ASSOCIATED PROTEIN 1; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; APOPTOSIS REGULATORY PROTEIN; BECN1 PROTEIN, MOUSE; MIRN30D MICRORNA, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; BRAIN CELL; BRAIN CELL CULTURE; BRAIN CORTEX; BRAIN HYPOXIA; CONTROLLED STUDY; DOWN REGULATION; GLUCOSE BRAIN LEVEL; HYPERTENSION; HYPOXIC ISCHEMIC ENCEPHALOPATHY; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NONHUMAN; PRIORITY JOURNAL; REOXYGENATION; UPREGULATION; ANIMAL; BIOSYNTHESIS; BRAIN ISCHEMIA; C57BL MOUSE; CELL CULTURE; METABOLISM; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; BRAIN ISCHEMIA; CELL LINE, TUMOR; CELLS, CULTURED; DOWN-REGULATION; MALE; MICE; MICE, INBRED C57BL; MICRORNAS;

EID: 84904541192     PISSN: 03643190     EISSN: 15736903     Source Type: Journal    
DOI: 10.1007/s11064-014-1310-6     Document Type: Article

References (48)

1. Marsh JD, Keyrouz SG (2010) Stroke prevention and treatment. J Am Coll Cardiol 56:683-691
2. Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136:215-233
3. Fasanaro P, Greco S, Ivan M, Capogrossi MC, Martelli F (2010) microRNA: emerging therapeutic targets in acute ischemic diseases. Pharmacol Ther 125:92-104
4. Huang Y, Shen XJ, Zou Q, Zhao QL (2010) Biological functions of microRNAs. Bioorg Khim 36:747-752
5. Zhao Y, Srivastava D (2007) A developmental view of microRNA function. Trends Biochem Sci 32:189-197 (Pubitemid 46603281)
6. Frankel LB, Wen J, Lees M, Hoyer-Hansen M, Farkas T, Krogh A, Jaattela M, Lund AH (2011) microRNA-101 is a potent inhibitor of autophagy. EMBO J 30:4628-4641
7. Chang Y, Yan W, He X, Zhang L, Li C, Huang H, Nace G, Geller DA, Lin J, Tsung A (2012) miR-375 inhibits autophagy and reduces viability of hepatocellular carcinoma cells under hypoxic conditions. Gastroenterology 143:177-187
8. Korkmaz G, Le SC, Tekirdag KA, Agami R, Gozuacik D (2012) miR-376b controls starvation and mTOR inhibition-related autophagy by targeting ATG4C and BECN1. Autophagy 8:165-176
9. Kovaleva V, Mora R, Park YJ, Plass C, Chiramel AI, Bartenschlager R, Dohner H, Stilgenbauer S, Pscherer A, Lichter P, Seiffert M (2012) miRNA-130a targets ATG2B and DICER1 to inhibit autophagy and trigger killing of chronic lymphocytic leukemia cells. Cancer Res 72:1763-1772
10. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19:5720-5728
11. Cao Y, Klionsky DJ (2007) Physiological functions of Atg6/Beclin 1: a unique autophagy-related protein. Cell Res 17:839-849 (Pubitemid 47585112)
12. Wang J (2008) Beclin 1 bridges autophagy, apoptosis and differentiation. Autophagy 4:947-948
13. Rink C, Khanna S (2011) MicroRNA in ischemic stroke etiology and pathology. Physiol Genomics 43:521-528
14. Kosik KS (2006) The neuronal microRNA system. Nat Rev Neurosci 7:911-920
15. Dharap A, Bowen K, Place R, Li LC, Vemuganti R (2009) Transient focal ischemia induces extensive temporal changes in rat cerebral microRNAome. J Cereb Blood Flow Metab 29:675-687
16. Tan JR, Koo YX, Kaur P, Liu F, Armugam A, Wong PT, Jeyaseelan K (2011) microRNAs in stroke pathogenesis. Curr Mol Med 11:76-92
17. Liu C, Peng Z, Zhang N, Yu L, Han S, Li D, Li J (2012) Identification of differentially expressed microRNAs and their PKCisoform specific gene network prediction during hypoxic preconditioning and focal cerebral ischemia of mice. J Neurochem 120:830-841
18. Zhu H, Wu H, Liu X, Li B, Chen Y, Ren X, Liu CG, Yang JM (2009) Regulation of autophagy by a beclin 1-targeted microRNA, miR-30a, in cancer cells. Autophagy 5:816-823
19. Zou Z, Wu L, Ding H, Wang Y, Zhang Y, Chen X, Chen X, Zhang CY, Zhang Q, Zen K (2012) MicroRNA-30a sensitizes tumor cells to cis-platinum via suppressing beclin 1-mediated autophagy. J Biol Chem 287:4148-4156
20. Yu Y, Yang L, Zhao M, Zhu S, Kang R, Vernon P, Tang D, Cao L (2012) Targeting microRNA-30a-mediated autophagy enhances imatinib activity against human chronic myeloid leukemia cells. Leukemia 26:1752-1760
21. Pan W, Zhong Y, Cheng C, Liu B, Wang L, Li A, Xiong L, Liu S (2013) MiR-30-regulated autophagy mediates angiotensin II-induced myocardial hypertrophy. PLoS ONE 8:e53950
22. Yin X, Peng C, Ning W, Li C, Ren Z, Zhang J, Gao H, Zhao K (2013) miR-30a downregulation aggravates pressure overload-induced cardiomyocyte hypertrophy. Mol Cell Biochem 379:1-6
23. Bu X, Zhang N, Yang X, Liu Y, Du J, Liang J, Xu Q, Li J (2011) Proteomic analysis of cPKCbetaII-interacting proteins involved in HPC-induced neuroprotection against cerebral ischemia of mice. J Neurochem 117:346-356
24. Feng S, Li D, Li Y, Yang X, Han S, Li J (2013) Insight into hypoxic preconditioning and ischemic injury through determination of nPKCepsilon-interacting proteins in mouse brain. Neurochem Int 63:69-79
25. Zhang N, Yin Y, Han S, Jiang J, Yang W, Bu X, Li J (2011) Hypoxic preconditioning induced neuroprotection against cerebral ischemic injuries and its cPKCgamma-mediated molecular mechanism. Neurochem Int 58:684-692
26. Rodriguez R, Santiago-Mejia J, Gomez C, San-Juan ER (2005) A simplified procedure for the quantitative measurement of neurological deficits after forebrain ischemia in mice. J Neurosci Methods 147:22-28 (Pubitemid 41058665)
27. Zhou L, Li F, Xu HB, Luo CX, Wu HY, Zhu MM, Lu W, Ji X, Zhou QG, Zhu DY (2010) Treatment of cerebral ischemia by disrupting ischemia-induced interaction of nNOS with PSD-95. Nat Med 16:1439-1443
28. Li J, Qu Y, Zu P, Han S, Gao G, Xu Q, Fang L (2006) Increased isoform-specific membrane translocation of conventional and novel protein kinase C in human neuroblastoma SH-SY5Y cells following prolonged hypoxia. Brain Res 1093:25-32 (Pubitemid 43946405)
29. Li J, Niu C, Han S, Zu P, Li H, Xu Q, Fang L (2005) Identification of protein kinase C isoforms involved in cerebral hypoxic preconditioning of mice. Brain Res 1060:62-72 (Pubitemid 41483590)
30. Bak M, Silahtaroglu A, Moller M, Christensen M, Rath MF, Skryabin B, Tommerup N, Kauppinen S (2008) MicroRNA expression in the adult mouse central nervous system. RNA 14:432-444 (Pubitemid 351397808)
31. Hebert SS, De SB (2009) Alterations of the microRNA network cause neurodegenerative disease. Trends Neurosci 32:199-206
32. Liu DZ, Tian Y, Ander BP, Xu H, Stamova BS, Zhan X, Turner RJ, Jickling G, Sharp FR (2010) Brain and blood microRNA expression profiling of ischemic stroke, intracerebral hemorrhage, and kainate seizures. J Cereb Blood Flow Metab 30:92-101
33. Teplyuk NM, Mollenhauer B, Gabriely G, Giese A, Kim E, Smolsky M, Kim RY, Saria MG, Pastorino S, Kesari S, Krichevsky AM (2012) MicroRNAs in cerebrospinal fluid identify glioblastoma and metastatic brain cancers and reflect disease activity. Neuro Oncol 14:689-700
34. Zhong M, Bian Z, Wu Z (2013) miR-30a suppresses cell migration and invasion through downregulation of PIK3CD in colorectal carcinoma. Cell Physiol Biochem 31:209-218
35. Kumarswamy R, Mudduluru G, Ceppi P, Muppala S, Kozlowski M, Niklinski J, Papotti M, Allgayer H (2012) MicroRNA-30a inhibits epithelial-to-mesenchymal transition by targeting Snai1 and is downregulated in non-small cell lung cancer. Int J Cancer 130:2044-2053
36. Cheng CW, Wang HW, Chang CW, Chu HW, Chen CY, Yu JC, Chao JI, Liu HF, Ding SL, Shen CY (2012) MicroRNA-30a inhibits cell migration and invasion by downregulating vimentin expression and is a potential prognostic marker in breast cancer. Breast Cancer Res Treat 134:1081-1093
37. Mellios N, Huang HS, Grigorenko A, Rogaev E, Akbarian S (2008) A set of differentially expressed miRNAs, including miR-30a-5p, act as post-transcriptional inhibitors of BDNF in prefrontal cortex. Hum Mol Genet 17:3030-3042
38. Croce N, Gelfo F, Ciotti MT, Federici G, Caltagirone C, Bernardini S, Angelucci F (2013) NPY modulates miR-30a-5p and BDNF in opposite direction in an in vitro model of Alzheimer disease: a possible role in neuroprotection? Mol Cell Biochem 376:189-195
39. Long G, Wang F, Duan Q, Yang S, Chen F, Gong W, Yang X, Wang Y, Chen C, Wang DW (2012) Circulating miR-30a, miR-195 and let-7b associated with acute myocardial infarction. PLoS ONE 7:e50926
40. Zheng YQ, Liu JX, Li XZ, Xu L, Xu YG (2009) RNA interference-mediated downregulation of Beclin1 attenuates cerebral ischemic injury in rats. Acta Pharmacol Sin 30:919-927
41. Shi R, Weng J, Zhao L, Li XM, Gao TM, Kong J (2012) Excessive autophagy contributes to neuron death in cerebral ischemia. CNS Neurosci Ther 18:250-260
42. Wen YD, Sheng R, Zhang LS, Han R, Zhang X, Zhang XD, Han F, Fukunaga K, Qin ZH (2008) Neuronal injury in rat model of permanent focal cerebral ischemia is associated with activation of autophagic and lysosomal pathways. Autophagy 4:762-769
43. Papadakis M, Hadley G, Xilouri M, Hoyte LC, Nagel S, McMenamin MM, Tsaknakis G, Watt SM, Drakesmith CW, Chen R, Wood MJ, Zhao Z, Kessler B, Vekrellis K, Buchan AM (2013) Tsc1 (hamartin) confers neuroprotection against ischemia by inducing autophagy. Nat Med 19:351-357
44. Carloni S, Buonocore G, Balduini W (2008) Protective role of autophagy in neonatal hypoxia-ischemia induced brain injury. Neurobiol Dis 32:329-339
45. Wang P, Guan YF, Du H, Zhai QW, Su DF, Miao CY (2012) Induction of autophagy contributes to the neuroprotection of nicotinamide phosphoribosyltransferase in cerebral ischemia. Autophagy 8:77-87
46. Mizushima N, Yoshimori T, Levine B (2010) Methods in mammalian autophagy research. Cell 140:313-326
47. Tanida I (2011) Autophagosome formation and molecular mechanism of autophagy. Antioxid Redox Signal 14:2201-2214
48. Ge W, Ren J (2012) mTOR-STAT3-notch signalling contributes to ALDH2-induced protection against cardiac contractile dysfunction and autophagy under alcoholism. J Cell Mol Med 16:616-626