Login Register Cart 0
Generic placeholder image

Current Neurovascular Research

Editor-in-Chief

ISSN (Print): 1567-2026
ISSN (Online): 1875-5739

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Research Article

Curcumin Prevents Brain Damage and Cognitive Dysfunction During Ischemic-reperfusion Through the Regulation of miR-7-5p

Author(s): Hui Xu, Beibei Nie, Lamei Liu, Chunhui Zhang*, Zhenxiang Zhang, Mengya Xu and Yongxia Mei

Volume 16, Issue 5, 2019

Page: [441 - 454] Pages: 14

DOI: 10.2174/1567202616666191029113633

Price: $65

Abstract

Objective: This study was to investigate the potential protective effects of curcumin in cerebral ischemia-reperfusion (CIR) and its regulation of miR-7.

Methods: Rats were occluded by middle cerebral artery occlusion (MCAO) for 1.5 h and reperfused for 2 h to establish a local CIR model. After 24 hours of model establishment, MCAO rats were given curcumin for 3 days by intragastric administration. PC12 cells were cultured for 6 h in oxygen-glucose deprivation medium and then reoxygenated for 24 h to establish an oxygenglucose deprivation/reoxygenation (OGD/R) model. The OGD/R model cells were treated with curcumin for 48 h.

Results: Curcumin inhibited the decrease of miR-7-5p expression and an increase of RelA p65 expression induced by CIR and ODG/R. RelA p65 was a target of miR-7-5p. MiR-7-5p antagonists were able to counteract the effect of curcumin on the expression of RelA p65 in ischemic brain tissue of MCAO rats and OGD/R model cells. Curcumin improved OGD/R-induced inhibition of cell activity, necrosis and apoptosis. Curcumin significantly reduced the levels of tumor necrosis factor (TNF)-α, interleukin (IL)-6, IL-1β, reactive oxygen species (ROS) and malondialdehyde (MDA) and increased the activity of superoxide dismutases (SOD) and catalase (CAT) in OGD/R-induced cells. Curcumin may inhibit OGD/R-induced cell damage by regulating miR-7-5p. Curcumin improved cerebral infarction, nerve damage and cognitive dysfunction in rats with CIR, which may be related to the regulation of miR-7-5p/RelA p65 axis.

Conclusion: Curcumin exerts cerebral protection by attenuating cell necrosis and apoptosis, inflammatory response and oxidative stress following CIR, which may be related to its regulation of the miR-7/RELA p65 axis.

Keywords: Cerebral ischemia-reperfusion, oxygen-glucose deprivation/reoxygenation model, curcumin, miR-7-5p/RelA p65 axis, middle cerebral artery occlusion, tumor necrosis factor.

« Previous Next »
[1]
Chen CM, Wu CT, Yang TH, Liu SH, Yang FY. Preventive effect of low intensity pulsed ultrasound against experimental cerebral ischemia/reperfusion injury via apoptosis reduction and brain-derived neurotrophic factor induction. Sci Rep 2018; 8(1): 5568.
[http://dx.doi.org/10.1038/s41598-018-23929-8] [PMID: 29615782]
[2]
Tsuda T. Curcumin as a functional food-derived factor: Degradation products, metabolites, bioactivity, and future perspectives. Food Funct 2018; 9(2): 705-14.
[http://dx.doi.org/10.1039/C7FO01242J] [PMID: 29206254]
[3]
Wu J, Li Q, Wang X, et al. Neuroprotection by curcumin in ischemic brain injury involves the Akt/Nrf2 pathway. PLoS One 2013; 8(3) e59843
[http://dx.doi.org/10.1371/journal.pone.0059843] [PMID: 23555802]
[4]
Bhat A, Mahalakshmi AM, Ray B, et al. Benefits of curcumin in brain disorders. Biofactors 2019; 45(5): 666-89. [https://www.ncbi.nlm.nih.gov/pubmed/31185140
[PMID: 31185140]
[5]
Alli-Oluwafuyi AM, Luis PB, Nakashima F, et al. Curcumin induces secretion of glucagon-like peptide-1 through an oxidation-dependent mechanism. Biochimie 2019; 165: 250-7. [https://www.sciencedirect.com/science/article/abs/pii/S0300908419302457
[6]
Zhao J, Zhao Y, Zheng W, Lu Y, Feng G, Yu S. Neuroprotective effect of curcumin on transient focal cerebral ischemia in rats. Brain Res 2008; 1229: 224-32.
[http://dx.doi.org/10.1016/j.brainres.2008.06.117] [PMID: 18640105]
[7]
Zhao J, Yu S, Zheng W, et al. Curcumin improves outcomes and attenuates focal cerebral ischemic injury via antiapoptotic mechanisms in rats. Neurochem Res 2010; 35(3): 374-9.
[http://dx.doi.org/10.1007/s11064-009-0065-y] [PMID: 19774461]
[8]
Jiang J, Wang W, Sun YJ, Hu M, Li F, Zhu DY. Neuroprotective effect of curcumin on focal cerebral ischemic rats by preventing blood-brain barrier damage. Eur J Pharmacol 2007; 561(1-3): 54-62.
[http://dx.doi.org/10.1016/j.ejphar.2006.12.028] [PMID: 17303117]
[9]
Yao X, Wang Y, Zhang D. microRNA-21 Confers neuroprotection against cerebral ischemia-reperfusion injury and alleviates blood-brain barrier disruption in rats via the MAPK signaling pathway. J Mol Neurosci 2018; 65: 43-53.
[10]
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: 774-8.
[http://dx.doi.org/10.1016/j.jocn.2009.10.009]
[11]
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(3): 959-66.
[http://dx.doi.org/10.1161/STROKEAHA.107.500736] [PMID: 18258830]
[12]
Saini S, Arora S, Majid S, et al. Curcumin modulates microRNA-203-mediated regulation of the Src-Akt axis in bladder cancer. Cancer Prev Res (Phila) 2011; 4(10): 1698-709.
[http://dx.doi.org/10.1158/1940-6207.CAPR-11-0267] [PMID: 21836020]
[13]
Ma F, Liu F, Ding L, et al. Anti-inflammatory effects of curcumin are associated with down regulating microRNA-155 in LPS-treated macrophages and mice. Pharm Biol 2017; 55(1): 1263-73.
[http://dx.doi.org/10.1080/13880209.2017.1297838] [PMID: 28264607]
[14]
Howell JC, Chun E, Farrell AN, et al. Global microRNA expression profiling: Curcumin (diferuloylmethane) alters oxidative stress-responsive microRNAs in human ARPE-19 cells. Mol Vis 2013; 19: 544-60.
[PMID: 23559849]
[15]
Longa EZ, Weinstein PR, Carlson S, Cummins R. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 1989; 20(1): 84-91.
[http://dx.doi.org/10.1161/01.STR.20.1.84] [PMID: 2643202]
[16]
Zhao H, Wang J, Gao L, et al. MiRNA-424 protects against permanent focal cerebral ischemia injury in mice involving suppressing microglia activation. Stroke 2013; 44(6): 1706-13.
[http://dx.doi.org/10.1161/STROKEAHA.111.000504] [PMID: 23613494]
[17]
Zhang F, Chen J. Leptin protects hippocampal CA1 neurons against ischemic injury. J Neurochem 2008; 107(2): 578-87.
[http://dx.doi.org/10.1111/j.1471-4159.2008.05645.x] [PMID: 18752642]
[18]
Shi X, Liu HY, Li SP, Xu HB. Keratinocyte growth factor protects endometrial cells from oxygen glucose deprivation/re-oxygenation via activating Nrf2 signaling. Biochem Biophys Res Commun 2018; 501(1): 178-85.
[http://dx.doi.org/10.1016/j.bbrc.2018.04.208] [PMID: 29709474]
[19]
Ni S, Yu Y, Zhang Y, Wu W, Lai K, Yao K. Study of oxidative stress in human lens epithelial cells exposed to 1.8 GHz radiofrequency fields. PLoS One 2013; 8(8) e72370
[http://dx.doi.org/10.1371/journal.pone.0072370] [PMID: 23991100]
[20]
Vorhees CV, Williams MT. Morris water maze: Procedures for assessing spatial and related forms of learning and memory. Nat Protoc 2006; 1(2): 848-58.
[http://dx.doi.org/10.1038/nprot.2006.116] [PMID: 17406317]
[21]
le Feber J, Tzafi Pavlidou S, Erkamp N, van Putten MJ, Hofmeijer J. Progression of neuronal damage in an in vitro model of the ischemic penumbra. PLoS One 2016; 11(2) e0147231
[http://dx.doi.org/10.1371/journal.pone.0147231] [PMID: 26871437]
[22]
Wu X, Zhao J, Yu S, Chen Y, Wu J, Zhao Y. Sulforaphane protects primary cultures of cortical neurons against injury induced by oxygen-glucose deprivation/reoxygenation via antiapoptosis. Neurosci Bull 2012; 28(5): 509-16.
[http://dx.doi.org/10.1007/s12264-012-1273-z] [PMID: 23054633]
[23]
Korsmeyer SJ, Shutter JR, Veis DJ, Merry DE, Oltvai ZN. Bcl-2/Bax: A rheostat that regulates an anti-oxidant pathway and cell death. Semin Cancer Biol 1993; 4(6): 327-32.
[PMID: 8142617]
[24]
Wong CH, Crack PJ. Modulation of neuro-inflammation and vascular response by oxidative stress following cerebral ischemia-reperfusion injury. Curr Med Chem 2008; 15(1): 1-14.
[http://dx.doi.org/10.2174/092986708783330665] [PMID: 18220759]
[25]
Chen L, Liu T, Wang Q, Liu J. Anti-inflammatory effect of combined tetramethylpyrazine, resveratrol and curcumin in vivo. BMC Complement Altern Med 2017; 17(1): 233.
[http://dx.doi.org/10.1186/s12906-017-1739-7] [PMID: 28449676]
[26]
Thiyagarajan M, Sharma SS. Neuroprotective effect of curcumin in middle cerebral artery occlusion induced focal cerebral ischemia in rats. Life Sci 2004; 74(8): 969-85.
[http://dx.doi.org/10.1016/j.lfs.2003.06.042] [PMID: 14672754]
[27]
Yang J, Qi J, Xiu B, Yang B, Niu C, Yang H. Reactive oxygen species play a biphasic role in brain ischemia. J Invest Surg 2019; 32: 97-102.
[http://dx.doi.org/10.1080/08941939.2017.1376131]
[28]
Du C, Hu R, Csernansky CA, Hsu CY, Choi DW. Very delayed infarction after mild focal cerebral ischemia: A role for apoptosis? J Cereb Blood Flow Metab 1996; 16(2): 195-201.
[http://dx.doi.org/10.1097/00004647-199603000-00003] [PMID: 8594050]
[29]
Liu QS, Deng R, Li S, et al. Ellagic acid protects against neuron damage in ischemic stroke through regulating the ratio of Bcl-2/Bax expression. Appl Physiol Nutrition Metabol 2017; 42: 855-60.
[30]
Cao YJ, Shibata T, Rainov NG. Liposome-mediated transfer of the bcl-2 gene results in neuroprotection after in vivo transient focal cerebral ischemia in an animal model. Gene Ther 2002; 9(6): 415-9.
[http://dx.doi.org/10.1038/sj.gt.3301676] [PMID: 11960318]
[31]
Zhao L, Gu Q, Xiang L, et al. Curcumin inhibits apoptosis by modulating Bax/Bcl-2 expression and alleviates oxidative stress in testes of streptozotocin-induced diabetic rats. Ther Clin Risk Manag 2017; 13: 1099-105.
[http://dx.doi.org/10.2147/TCRM.S141738] [PMID: 28894373]
[32]
Hou Y, Wang Y, He Q, et al. Nrf2 inhibits NLRP3 inflammasome activation through regulating Trx1/TXNIP complex in cerebral ischemia reperfusion injury. Behav Brain Res 2018; 336: 32-9.
[http://dx.doi.org/10.1016/j.bbr.2017.06.027] [PMID: 28851669]
[33]
Wu H, Tang C, Tai LW, et al. Flurbiprofen axetil attenuates cerebral ischemia/reperfusion injury by reducing inflammation in a rat model of transient global cerebral ischemia/reperfusion. Biosci Rep 2018; 38(4): 38.
[http://dx.doi.org/10.1042/BSR20171562] [PMID: 29540536]
[34]
Jin CY, Lee JD, Park C, Choi YH, Kim GY. Curcumin attenuates the release of pro-inflammatory cytokines in lipopolysaccharide-stimulated BV2 microglia. Acta Pharmacol Sin 2007; 28(10): 1645-51.
[http://dx.doi.org/10.1111/j.1745-7254.2007.00651.x] [PMID: 17883952]
[35]
Qiu Z, Yue S. Curcumin improves learning and memory function through decreasing hippocampal TNF-α and iNOS levels after subarachnoid hemorrhage in rats. Xibao Yu Fenzi Mianyixue Zazhi 2016; 32(3): 343-6.
[PMID: 26927554]
[36]
Vaibhav K, Shrivastava P, Tabassum R, et al. Delayed administration of zingerone mitigates the behavioral and histological alteration via repression of oxidative stress and intrinsic programmed cell death in focal transient ischemic rats. Pharmacol Biochem Behav 2013; 113: 53-62.
[http://dx.doi.org/10.1016/j.pbb.2013.10.008] [PMID: 24141173]
[37]
Sagara Y, Ishige K, Tsai C, Maher P. Tyrphostins protect neuronal cells from oxidative stress. J Biol Chem 2002; 277(39): 36204-15.
[http://dx.doi.org/10.1074/jbc.M203895200] [PMID: 12121989]
[38]
Lu CC, Yang JS, Huang AC, et al. Chrysophanol induces necrosis through the production of ROS and alteration of ATP levels in J5 human liver cancer cells. Mol Nutr Food Res 2010; 54(7): 967-76.
[http://dx.doi.org/10.1002/mnfr.200900265] [PMID: 20169580]
[39]
Bazmandegan G, Boroushaki MT, Shamsizadeh A, Ayoobi F, Hakimizadeh E, Allahtavakoli M. Brown propolis attenuates cerebral ischemia-induced oxidative damage via affecting antioxidant enzyme system in mice. Biomed Pharmacother 2017; 83: 503-10.
[http://dx.doi.org/10.1016/j.biopha.2016.11.057]
[40]
Tian F, Yuan C, Hu L, Shan S. MicroRNA-93 inhibits inflammatory responses and cell apoptosis after cerebral ischemia reperfusion by targeting interleukin-1 receptor-associated kinase 4. Exp Ther Med 2017; 14(4): 2903-10.
[http://dx.doi.org/10.3892/etm.2017.4874] [PMID: 28912849]
[41]
Webster RJ, Giles KM, Price KJ, Zhang PM, Mattick JS, Leedman PJ. Regulation of epidermal growth factor receptor signaling in human cancer cells by microRNA-7. J Biol Chem 2009; 284(9): 5731-41.
[http://dx.doi.org/10.1074/jbc.M804280200] [PMID: 19073608]
[42]
Li B, Li R, Zhang C, et al. MicroRNA-7a/b protects against cardiac myocyte injury in ischemia/reperfusion by targeting poly(ADP-ribose) polymerase. PLoS One 2014; 9(3) e90096
[http://dx.doi.org/10.1371/journal.pone.0090096] [PMID: 24594984]
[43]
Fang Y, Xue JL, Shen Q, Chen J, Tian L. MicroRNA-7 inhibits tumor growth and metastasis by targeting the phosphoinositide 3-kinase/Akt pathway in hepatocellular carcinoma. Hepatology 2012; 55(6): 1852-62.
[http://dx.doi.org/10.1002/hep.25576] [PMID: 22234835]
[44]
Yin KJ, Deng Z, Huang H, et al. miR-497 regulates neuronal death in mouse brain after transient focal cerebral ischemia. Neurobiol Dis 2010; 38(1): 17-26.
[http://dx.doi.org/10.1016/j.nbd.2009.12.021] [PMID: 20053374]
[45]
Madrid LV, Wang CY, Guttridge DC, Schottelius AJ, Baldwin AS Jr, Mayo MW. Akt suppresses apoptosis by stimulating the transactivation potential of the RelA/p65 subunit of NF-kappaB. Mol Cell Biol 2000; 20(5): 1626-38.
[http://dx.doi.org/10.1128/MCB.20.5.1626-1638.2000] [PMID: 10669740]
[46]
Irving EA, Hadingham SJ, Roberts J, et al. Decreased nuclear factor-kappaB DNA binding activity following permanent focal cerebral ischaemia in the rat. Neurosci Lett 2000; 288(1): 45-8.
[http://dx.doi.org/10.1016/S0304-3940(00)01203-9] [PMID: 10869812]
[47]
Han HS, Karabiyikoglu M, Kelly S, Sobel RA, Yenari MA. Mild hypothermia inhibits nuclear factor-kappaB translocation in experimental stroke. J Cereb Blood Flow Metab 2003; 23(5): 589-98.
[http://dx.doi.org/10.1097/01.WCB.0000059566.39780.8D] [PMID: 12771574]
[48]
Nurmi A, Lindsberg PJ, Koistinaho M, et al. Nuclear factor-kappaB contributes to infarction after permanent focal ischemia. Stroke 2004; 35(4): 987-91.
[http://dx.doi.org/10.1161/01.STR.0000120732.45951.26] [PMID: 14988572]
[49]
Huang CY, Fujimura M, Noshita N, Chang YY, Chan PH. SOD1 down-regulates NF-kappaB and c-Myc expression in mice after transient focal cerebral ischemia. J Cereb Blood Flow Metab 2001; 21(2): 163-73.
[http://dx.doi.org/10.1097/00004647-200102000-00008] [PMID: 11176282]
[50]
Kairisalo M, Korhonen L, Blomgren K, Lindholm D. X-linked inhibitor of apoptosis protein increases mitochondrial antioxidants through NF-kappaB activation. Biochem Biophys Res Commun 2007; 364(1): 138-44.
[http://dx.doi.org/10.1016/j.bbrc.2007.09.115] [PMID: 17936246]
[51]
Ranjit S, Sinha N, Kodidela S, Kumar S. Benzo(a)pyrene in cigarette smoke enhances HIV-1 replication through NF-κB activation via CYP-mediated oxidative stress pathway. Sci Rep 2018; 8(1): 10394.
[http://dx.doi.org/10.1038/s41598-018-28500-z] [PMID: 29991690]
[52]
Xia Q, Li X, Zhou HJ, Zheng L, Shi J. S100A11 protects against neuronal cell apoptosis induced by cerebral ischemia via inhibiting the nuclear translocation of annexin A1. Cell Death Dis 2018; 9: 657.
[53]
Huang W, Zhou Z, Wan B, Chen G, Li J. Nuclear factor kB and inhibitor of kB: Acupuncture protection against acute focal cerebral ischemia in rodents. Altern Ther Health Med 2017; 23(3): 20-8.
[PMID: 28236616]
[54]
Zhao H, Chen Z, Xie LJ, Liu GF. Suppression of TLR4/NF-κB signaling pathway improves cerebral ischemia-reperfusion injury in rats. Mol Neurobiol 2018; 55(5): 4311-9.
[PMID: 28624894]
[55]
Yang CH, Yue J, Sims M, Pfeffer LM. The curcumin analog EF24 targets NF-κB and miRNA-21, and has potent anticancer activity in vitro and in vivo. PLoS One 2013; 8(8) e71130
[http://dx.doi.org/10.1371/journal.pone.0071130] [PMID: 23940701]
[56]
Cai J, Xu D, Bai X, et al. Curcumin mitigates cerebral vasospasm and early brain injury following subarachnoid hemorrhage via inhibiting cerebral inflammation. Brain Behav 2017; 7(9) e00790
[http://dx.doi.org/10.1002/brb3.790] [PMID: 28948084]

Rights & Permissions Print Cite
Article Metrics
36
3
© 2024 Bentham Science Publishers | Privacy Policy