Generic placeholder image

CNS & Neurological Disorders - Drug Targets

Editor-in-Chief

ISSN (Print): 1871-5273
ISSN (Online): 1996-3181

Review Article

Causes and Consequences of MicroRNA Dysregulation Following Cerebral Ischemia-Reperfusion Injury

Author(s): Fatemeh Forouzanfar, Mana Shojapour, Samira Asgharzade* and Elham Amini

Volume 18, Issue 3, 2019

Page: [212 - 221] Pages: 10

DOI: 10.2174/1871527318666190204104629

Price: $65

Abstract

Stroke continues to be a major cause of death and disability worldwide. In this respect, the most important mechanisms underlying stroke pathophysiology are inflammatory pathways, oxidative stress, as well as apoptosis. Accordingly, miRNAs are considered as non-coding endogenous RNA molecules interacting with their target mRNAs to inhibit mRNA translation or reduce its transcription. Studies in this domain have similarly shown that miRNAs are strongly associated with coronary artery disease and correspondingly contributed to the brain ischemia molecular processes. To retrieve articles related to the study subject, i.e. the role of miRNAs involved in inflammatory pathways, oxidative stress, and apoptosis in stroke from the databases of Web of Science, PubMed (NLM), Open Access Journals, LISTA (EBSCO), and Google Scholar; keywords including cerebral ischemia, microRNA (miRNA), inflammatory pathway, oxidative stress, along with apoptosis were used. It was consequently inferred that, miRNAs could be employed as potential biomarkers for diagnosis and prognosis, as well as therapeutic goals of cerebral ischemia.

Keywords: MiRNAs, stroke, inflammatory pathways, oxidative stress, apoptosis, pathophysiology.

Graphical Abstract
[1]
Khoshnam SE, Winlow W, Farzaneh M. The interplay of micrornas in the inflammatory mechanisms following ischemic stroke. J Neuropathol Exp Neurol 2017; 76(7): 548-61.
[2]
Forouzanfar F, Hosseinzadeh H, Ebrahimzadeh Bideskan A, Sadeghnia HR. Aqueous and ethanolic extracts of Boswellia serrata protect against focal cerebral ischemia and reperfusion injury in rats. Phytother Res 2016; 30(12): 1954-67.
[3]
Beal CC. Gender and stroke symptoms: a review of the current literature. J Neurosci Nurs 2010; 42(2): 80-7.
[4]
Ghazavi H, Hoseini SJ, Ebrahimzadeh-Bideskan A, et al. Fibroblast growth factor type 1 [FGF1]-overexpressed adipose-derived mesenchaymal stem cells [AD-MSCFGF1] induce neuroprotection and functional recovery in a rat stroke model. Stem Cell Rev 2017; 13(5): 670-85.
[5]
Eltzschig HK, Eckle T. Ischemia and reperfusion—from mechanism to translation. Nat Med 2011; 17(11): 1391-401.
[6]
Sadeghnia HR, Shaterzadeh H, Forouzanfar F, Hosseinzadeh H. Neuroprotective effect of safranal, an active ingredient of Crocus sativus, in a rat model of transient cerebral ischemia. Folia Neuropathol 2017; 55(3): 206-13.
[7]
Zhao L, Zhou XY, Zhou XG, Cheng R, Li Y, Qiu J. Role of miRNA-210 in hypoxic-ischemic brain edema in neonatal rats. Zhongguo Dang Dai Er Ke Za Zhi 2016; 18(8): 770-4.
[8]
Zhu F, Liu JL, Li JP, Xiao F, Zhang ZX, Zhang L. MicroRNA-124 [miR-124] regulates Ku70 expression and is correlated with neuronal death induced by ischemia/reperfusion. J Mol Neurosci 2014; 52(1): 148-55.
[9]
Xiao S, Ma Y, Zhu H, Sun H, Yin Y, Feng G. miRNA functional synergistic network analysis of mice with ischemic stroke. Neurol Sci 2015; 36(1): 143-8.
[10]
Zhu R, Liu X, Zhu Y, He Z. MiRNAs: potential diagnostic and therapeutic targets for cerebral ischaemia. Neurol Res 2016; 38(1): 86-92.
[11]
Ouyang YB, Stary CM, Yang GY, Giffard R. microRNAs: innovative targets for cerebral ischemia and stroke. Curr Drug Targets 2013; 14(1): 90-101.
[12]
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.
[13]
Zeng L, Liu J, Wang Y, Wang L, Weng S, Tang Y, et al. MicroRNA-210 as a novel blood biomarker in acute cerebral ischemia. Front Biosci 2011; 3: 1265-72.
[14]
Ekdahl C, Kokaia Z, Lindvall O. Brain inflammation and adult neurogenesis: the dual role of microglia. Neuroscience 2009; 158(3): 1021-9.
[15]
Lucas SM, Rothwell NJ, Gibson RM. The role of inflammation in CNS injury and disease. Br J Pharmacol 2006; 147(Suppl. 1): S232-40.
[16]
Bigham A, Shadkhast M, Hassanpour H, Lakzian A, Khalegi M, Asgharzade S. Nitric oxide metabolite levels during the ectopic osteoinduction in rats. Comp Clin Pathol 2009; 18(4): 377-81.
[17]
Shichita T, Sugiyama Y, Ooboshi H, et al. Pivotal role of cerebral interleukin-17–producing γδT cells in the delayed phase of ischemic brain injury. Nat Med 2009; 15(8): 946-50.
[18]
Lakhan SE, Kirchgessner A, Hofer M. Inflammatory mechanisms in ischemic stroke: therapeutic approaches. J Leukoc Biol 2009; 17(7): 97.
[19]
Barone FC, Feuerstein GZ. Inflammatory mediators and stroke: new opportunities for novel therapeutics. J Cereb Blood Flow Metab 1999; 19(8): 819-34.
[20]
Ferrarese C, Mascarucci P, Zoia C, et al. Increased cytokine release from peripheral blood cells after acute stroke. J Cereb Blood Flow Metab 1999; 19(9): 1004-9.
[21]
Zhu Y, Yang G-Y, Ahlemeyer B, et al. Transforming growth factor-β1 increases bad phosphorylation and protects neurons against damage. J Neurosci 2002; 22(10): 3898-909.
[22]
Caso JR, Moro MA, Lorenzo P, Lizasoain I, Leza JC. Involvement of IL-1β in acute stress-induced worsening of cerebral ischaemia in rats. Eur Neuropsychopharmacol 2007; 17(9): 600-7.
[23]
Kim JS, Gautam SC, Chopp M, et al. Expression of monocyte chemoattractant protein-1 and macrophage inflammatory protein-1 after focal cerebral ischemia in the rat. J Neuroimmunol 1995; 56(2): 127-34.
[24]
Kumai Y, Ooboshi H, Takada J, et al. Anti—monocyte chemoattractant protein-1 gene therapy protects against focal brain ischemia in hypertensive rats. J Cereb Blood Flow Metab 2004; 24(12): 1359-68.
[25]
Yilmaz G, Granger DN. Cell adhesion molecules and ischemic stroke. Neurol Res 2008; 30(8): 783-93.
[26]
Zhang R, Chopp M, Zhang Z, Jiang N, Powers C. The expression of P-and E-selectins in three models of middle cerebral artery occlusion. Brain Res 1998; 785(2): 207-14.
[27]
Montaner J, Alvarez-Sabín J, Molina C, et al. Matrix metalloproteinase expression after human cardioembolic stroke: temporal profile and relation to neurological impairment. Stroke 2001; 32(8): 1759-66.
[28]
Asahi M, Wang X, Mori T, et al. Effects of matrix metalloproteinase-9 gene knock-out on the proteolysis of blood–brain barrier and white matter components after cerebral ischemia. J Neurosci 2001; 21(19): 7724-32.
[29]
Park K-P, Rosell A, Foerch C, et al. Plasma and brain matrix metalloproteinase-9 after acute focal cerebral ischemia in rats. Stroke 2009; 40(8): 2836-42.
[30]
Bronisz A, Godlewski J, Wallace JA, et al. Reprogramming of the tumour microenvironment by stromal PTEN-regulated miR-320. Nat Cell Biol 2011; 14(2): 159-67.
[31]
Philippe L, Alsaleh G, Suffert G, et al. TLR2 expression is regulated by microRNA miR-19 in rheumatoid fibroblast-like synoviocytes. J Immunol 2012; 188(1): 454-61.
[32]
Iyer A, Zurolo E, Prabowo A, et al. MicroRNA-146a: a key regulator of astrocyte-mediated inflammatory response. PLoS One 2012; 7(9): e44789.
[33]
Khoshnam SE, Winlow W, Farzaneh M. The interplay of MicroRNAs in the inflammatory mechanisms following ischemic stroke. J Neuropathol Exp Neurol 2017; 76(7): 548-61.
[34]
Wang Z-k. Liu F-f, Wang Y, Jiang X-m, Yu X-f. Let-7a gene knockdown protects against cerebral ischemia/reperfusion injury. Neural Regen Res 2016; 11(2): 262.
[35]
Ponomarev ED, Veremeyko T, Barteneva N, Krichevsky AM, Weiner HL. MicroRNA-124 promotes microglia quiescence and suppresses EAE by deactivating macrophages via the C/EBP-α–PU. 1 pathway. Nat Med 2011; 17(1): 64-70.
[36]
Cardoso AL, Guedes JR, Pereira de Almeida L, Pedroso de Lima MC. miR‐155 modulates microglia‐mediated immune response by down‐regulating SOCS‐1 and promoting cytokine and nitric oxide production. Immunology 2012; 135(1): 73-88.
[37]
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.
[38]
Wang X, Chen S, Ni J, Cheng J, Jia J, Zhen X. miRNA-3473b contributes to neuroinflammation following cerebral ischemia. Cell Death Dis 2018; 9(1): 11.
[39]
Liu Y, Zhang J, Han R, Liu H, Sun D, Liu X. Downregulation of serum brain specific microRNA is associated with inflammation and infarct volume in acute ischemic stroke. J Clin Neurosci 2015; 22(2): 291-5.
[40]
Zhang L, Li YJ, Wu XY, Hong Z, Wei WS. Micro RNA‐181c negatively regulates the inflammatory response in oxygen‐glucose‐deprived microglia by targeting Toll‐like receptor 4. J Neurochem 2015; 132(6): 713-23.
[41]
Fredman G, Li Y, Dalli J, Chiang N, Serhan CN. Self-limited versus delayed resolution of acute inflammation: temporal regulation of pro-resolving mediators and microRNA. Sci Rep 2012; 2: 639.
[42]
Recchiuti A, Krishnamoorthy S, Fredman G, Chiang N, Serhan CN. MicroRNAs in resolution of acute inflammation: identification of novel resolvin D1-miRNA circuits. FASEB J 2011; 25(2): 544-60.
[43]
Forouzanfar F, Afkhami Goli A, Asadpour E, Ghorbani A, Sadeghnia HR. Protective effect of Punica granatum L. against serum/glucose deprivation-induced PC12 cells injury. Evid Based Complement Alternat Med 2013; 13: 716-30.
[44]
Chen H, Yoshioka H, Kim GS, et al. Oxidative stress in ischemic brain damage: mechanisms of cell death and potential molecular targets for neuroprotection. Antioxid Redox Signal 2011; 14(8): 1505-17.
[45]
Asgharzade S, Rabiei Z, Rafieian-Kopaei M. Effects of Matricaria chamomilla extract on motor coordination impairment induced by scopolamine in rats. Asian Pac J Trop Biomed 2015; 5(10): 829-33.
[46]
Magenta A, Cencioni C, Fasanaro P, et al. miR-200c is upregulated by oxidative stress and induces endothelial cell apoptosis and senescence via ZEB1 inhibition. Cell Death Differ 2011; 18(10): 1628-39.
[47]
Varga ZV, Kupai K, Szűcs G, et al. MicroRNA-25-dependent up-regulation of NADPH oxidase 4 [NOX4] mediates hypercholesterolemia-induced oxidative/nitrative stress and subsequent dysfunction in the heart. J Mol Cell Cardiol 2013; 62: 111-21.
[48]
Zhao H, Tao Z, Wang R, Liu P, Yan F, Li J, et al. MicroRNA-23a-3p attenuates oxidative stress injury in a mouse model of focal cerebral ischemia-reperfusion. Brain Res 2014; 1592: 65-72.
[49]
Hengartner MO. The biochemistry of apoptosis. Nature 2000; 407(6805): 770-6.
[50]
Hu Y, Deng H, Xu S, Zhang J. MicroRNAs regulate mitochondrial function in cerebral ischemia-reperfusion injury. Int J Mol Sci 2015; 16(10): 24895-17.
[51]
Niizuma K, Endo H, Nito C, Myer DJ, Chan PH. Potential role of PUMA in delayed death of hippocampal CA1 neurons after transient global cerebral ischemia. Stroke 2009; 40(2): 618-25.
[52]
Doyle KP, Simon RP, Stenzel-Poore MP. Mechanisms of ischemic brain damage. Neuropharmacology 2008; 55(3): 310-8.
[53]
4Trapp T, Korhonen L, Besselmann M, Martinez R, Mercer EA, Lindholm D. Transgenic mice overexpressing XIAP in neurons show better outcome after transient cerebral ischemia. Mol Cell Neurosci 2003; 23(2): 302-13.
[54]
Su W, Hopkins S, Nesser NK, et al. The p53 transcription factor modulates microglia behavior through microRNA-dependent regulation of c-Maf. J Immunol 2014; 192(1): 358-66.
[55]
Zhang C, Zhang J, Zhang A, et al. PUMA is a novel target of miR-221/222 in human epithelial cancers. Int J Oncol 2010; 37(6): 1621-6.
[56]
Huang W, Liu X, Cao J, Meng F, Li M, Chen B, et al. miR-134 regulates ischemia/reperfusion injury-induced neuronal cell death by regulating CREB signaling. J Mol Neurosci 2015; 55(4): 821-9.
[57]
Siegel C, Li J, Liu F, Benashski SE, McCullough LD. miR-23a regulation of X-linked inhibitor of apoptosis [XIAP] contributes to sex differences in the response to cerebral ischemia. Proc Natl Acad Sci USA 2011; 108(28): 11662-7.
[58]
Ni J, Wang X, Chen S, et al. MicroRNA let-7c-5p protects against cerebral ischemia injury via mechanisms involving the inhibition of microglia activation. Brain Behav Immun 2015; 49: 75-85.
[59]
Sun X, Ren Z, Pan Y, Zhang C. Antihypoxic effect of miR-24 in SH-SY5Y cells under hypoxia via downregulating expression of neurocan. Biochem Biophys Res Commun 2016; 477(4): 692-9.
[60]
Zhou X, Su S, Li S, et al. MicroRNA-146a down-regulation correlates with neuroprotection and targets pro-apoptotic genes in cerebral ischemic injury in vitro. Brain Res 2016; 1648: 136-43.
[61]
Zhang JF, Shi LL, Zhang L, et al. MicroRNA-25 negatively regulates cerebral ischemia/reperfusion injury-induced cell apoptosis through fas/fasl pathway. J Mol Neurosci 2016; 58(4): 507-16.
[62]
Caballero-Garrido E, Pena-Philippides JC, Lordkipanidze T, et al. In Vivo Inhibition of miR-155 promotes recovery after experimental mouse stroke. J Neurosci 2015; 35(36): 12446-64.
[63]
Chen F, Du Y, Esposito E, et al. Effects of focal cerebral ischemia on exosomal versus serum miR126. Transl Stroke Res 2015; 6(6): 478-84.
[64]
Chen SH, Sun H, Zhang YM, Xu H, Yang Y, Wang FM. Effects of acupuncture at Baihui [GV 20] and Zusanli [ST 36] on peripheral serum expression of MicroRNA 124, laminin and integrin beta1 in rats with cerebral ischemia reperfusion injury. Chin J Integr Med 2016; 22(1): 49-55.
[65]
Chi W, Meng F, Li Y, et al. Downregulation of miRNA-134 protects neural cells against ischemic injury in N2A cells and mouse brain with ischemic stroke by targeting HSPA12B. Neuroscience 2014; 277: 111-22.
[66]
Cui H, Yang L. Analysis of microRNA expression detected by microarray of the cerebral cortex after hypoxic-ischemic brain injury. J Craniofac Surg 2013; 24(6): 2147-52.
[67]
Dharap A, Bowen K, Place R, Li LC, Vemuganti R. Transient focal ischemia induces extensive temporal changes in rat cerebral microRNAome. J Cereb Blood Flow Metab 2009; 29(4): 675-87.
[68]
Dhiraj DK, Chrysanthou E, Mallucci GR, Bushell M. miRNAs-19b, -29b-2* and -339-5p show an early and sustained up-regulation in ischemic models of stroke. PLoS One 2013; 8(12): e83717.
[69]
Ding X, Sun B, Huang J, et al. The role of miR-182 in regulating pineal CLOCK expression after hypoxia-ischemia brain injury in neonatal rats. Neurosci Lett 2015; 591: 75-80.
[70]
Garberg HT, Huun MU, Baumbusch LO, Asegg-Atneosen M, Solberg R, Saugstad OD. Temporal profile of circulating micrornas after global hypoxia-ischemia in newborn piglets. Neonatology 2017; 111(2): 133-9.
[71]
Gubern C, Camos S, Ballesteros I, et al. miRNA expression is modulated over time after focal ischaemia: up-regulation of miR-347 promotes neuronal apoptosis. FEBS J 2013; 280(23): 6233-46.
[72]
Gusar VA, Timofeeva AV, Zhanin IS, Shram SI, Pinelis VG. Estimation of time-dependent microRNA expression patterns in brain tissue, leukocytes, and blood plasma of rats under photochemically induced focal cerebral ischemia. Mol Biol 2017; 51(4): 683-95.
[73]
Han X, Ding X, Xu LX, Liu MH, Feng X. Expression profiles of miRNA-182 and Clock mRNA in the pineal gland of neonatal rats with hypoxic-ischemic brain damage. Zhongguo Dang Dai Er Ke Za Zhi 2016; 18(3): 270-6.
[74]
Herzog R, Zendedel A, Lammerding L, Beyer C, Slowik A. Impact of 17beta-estradiol and progesterone on inflammatory and apoptotic microRNA expression after ischemia in a rat model. J Steroid Biochem Mol Biol 2017; 167: 126-34.
[75]
Huang S, Lv Z, Guo Y, et al. Identification of Blood Let-7e-5p as a Biomarker for Ischemic Stroke. PLoS One 2016; 11(10): e0163951.
[76]
Huang W, Liu X, Cao J, et al. miR-134 regulates ischemia/reperfusion injury-induced neuronal cell death by regulating CREB signaling. J Mol Neurosci 2015; 55(4): 821-9.
[77]
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.
[78]
Lee ST, Chu K, Jung KH, et al. MicroRNAs induced during ischemic preconditioning. Stroke 2010; 41(8): 1646-51.
[79]
Li P, Teng F, Gao F, Zhang M, Wu J, Zhang C. Identification of circulating microRNAs as potential biomarkers for detecting acute ischemic stroke. Cell Mol Neurobiol 2015; 353: 433-47.
[80]
Li SH, Su SY, Liu JL. Differential regulation of microRNAs in patients with ischemic stroke. Curr Neurovasc Res 2015; 12(3): 214-21.
[81]
Liang TY, Lou JY. Increased expression of mir-34a-5p and clinical association in acute ischemic stroke patients and in a rat model. Med Sci Monit 2016; 22: 2950-5.
[82]
Liang Y, Xu J, Wang Y, et al. Inhibition of MiRNA-125b decreases cerebral ischemia/reperfusion injury by targeting CK2alpha/ NADPH oxidase signaling. Cell Physiol Biochem 2018; 45(5): 1818-26.
[83]
Liu FJ, Lim KY, Kaur P, et al. microRNAs involved in regulating spontaneous recovery in embolic stroke model. PLoS One 2013; 8(6): e66393.
[84]
Liu XS, Chopp M, Zhang RL, et al. MicroRNA profiling in subventricular zone after stroke: MiR-124a regulates proliferation of neural progenitor cells through Notch signaling pathway. PLoS One 2011; 6(8): e23461.
[85]
Ma Q, Zhao H, Tao Z, et al. MicroRNA-181c Exacerbates Brain Injury in Acute Ischemic Stroke. Aging Dis 2016; 7(6): 705-14.
[86]
Miao W, Bao TH, Han JH, et al. Neuroprotection induced by post-conditioning following ischemia/reperfusion in mice is associated with altered microRNA expression. Mol Med Rep 2016; 14(3): 2582-8.
[87]
Murphy SJ, Lusardi TA, Phillips JI, Saugstad JA. Sex differences in microRNA expression during development in rat cortex. Neurochem Int 2014; 77: 24-32.
[88]
Siegel C, Li J, Liu F, Benashski SE, McCullough LD. miR-23a regulation of X-linked inhibitor of apoptosis [XIAP] contributes to sex differences in the response to cerebral ischemia. Proc Natl Acad Sci USA 2011; 108(28): 11662-7.
[89]
Sorensen SS, Nygaard AB, Nielsen MY, Jensen K, Christensen T. miRNA expression profiles in cerebrospinal fluid and blood of patients with acute ischemic stroke. Transl Stroke Res 2014; 5(6): 711-8.
[90]
Tao J, Liu W, Shang G, et al. MiR-207/352 regulates lysosomal-associated membrane proteins and enzymes following ischemic stroke. Neuroscience 2015; 305: 1-14.
[91]
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.
[92]
Wang P, Zhang N, Liang J, Li J, Han S, Li J. Micro-RNA-30a regulates ischemia-induced cell death by targeting heat shock protein HSPA5 in primary cultured cortical neurons and mouse brain after stroke. J Neurosci Res 2015; 93(11): 1756-68.

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy