MicroRNA-93 Downregulation Ameliorates Cerebral Ischemic Injury Through the Nrf2/HO-1 Defense Pathway

Moskowitz MA, Lo EH, Iadecola C (2010) The science of stroke: mechanisms in search of treatments. Neuron 67:181–198

Jung JE, Kim GS, Chen H, Maier CM, Narasimhan P, Song YS, Niizuma K, Katsu M, Okami N, Yoshioka H, Sakata H, Goeders CE, Chan PH (2010) Reperfusion and neurovascular dysfunction in stroke: from basic mechanisms to potential strategies for neuroprotection. Mol Neurobiol 41:172–179

Nguyen T, Nioi P, Pickett CB (2009) The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress. J Biol Chem 284:13291–13295

Keum YS, Choi BY (2014) Molecular and chemical regulation of the Keap1-Nrf2 signaling pathway. Molecules 19:10074–10089

Shah ZA, Li RC, Ahmad AS, Kensler TW, Yamamoto M, Biswal S, Dore S (2010) The flavanol (−)-epicatechin prevents stroke damage through the Nrf2/HO1 pathway. J Cereb Blood Flow Metab 30:1951–1961

Ding Y, Chen M, Wang M, Wang M, Zhang T, Park J, Zhu Y, Guo C, Jia Y, Li Y, Wen A (2014) Neuroprotection by acetyl-11-keto-beta-Boswellic acid, in ischemic brain injury involves the Nrf2/HO-1 defense pathway. Sci Rep 4:7002

Alfieri A, Srivastava S, Siow RC, Cash D, Modo M, Duchen MR, Fraser PA, Williams SC, Mann GE (2013) Sulforaphane preconditioning of the Nrf2/HO-1 defense pathway protects the cerebral vasculature against blood–brain barrier disruption and neurological deficits in stroke. Free Radic Biol Med 65:1012–1022

Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136:215–233

Fasanaro P, Greco S, Ivan M, Capogrossi MC, Martelli F (2010) microRNA: emerging therapeutic targets in acute ischemic diseases. Pharmacol Ther 125:92–104

Huang Y, Shen XJ, Zou Q, Zhao QL (2010) Biological functions of microRNAs. Bioorg Khim 36:747–752

Zhao Y, Srivastava D (2007) A developmental view of microRNA function. Trends Biochem Sci 32:189–197

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

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

Rink C, Khanna S (2011) MicroRNA in ischemic stroke etiology and pathology. Physiol Genomics 43:521–528

Zhang JF, Shi LL, Zhang L, Zhao ZH, Liang F, Xu X, Zhao LY, Yang PB, Zhang JS, Tian YF (2016) MicroRNA-25 negatively regulates cerebral ischemia/reperfusion injury-induced cell apoptosis through Fas/FasL pathway. J Mol Neurosci. doi: 10.1007/s12031-016-0712-0

Fabbri E, Borgatti M, Montagner G, Bianchi N, Finotti A, Lampronti I, Bezzerri V, Dechecchi MC, Cabrini G, Gambari R (2014) Expression of microRNA-93 and Interleukin-8 during Pseudomonas aeruginosa-mediated induction of proinflammatory responses. Am J Respir Cell Mol Biol 50:1144–1155

Singh B, Ronghe AM, Chatterjee A, Bhat NK, Bhat HK (2013) MicroRNA-93 regulates NRF2 expression and is associated with breast carcinogenesis. Carcinogenesis 34:1165–1172

Rouse M, Rao R, Nagarkatti M, Nagarkatti PS (2014) 3,3′-Diindolylmethane ameliorates experimental autoimmune encephalomyelitis by promoting cell cycle arrest and apoptosis in activated T cells through microRNA signaling pathways. J Pharmacol Exp Ther 350:341–352

Han RQ, Ouyang YB, Xu L, Agrawal R, Patterson AJ, Giffard RG (2009) Postischemic brain injury is attenuated in mice lacking the beta2-adrenergic receptor. Anesth Analg 108:280–287

Xiong X, Barreto GE, Xu L, Ouyang YB, Xie X, Giffard RG (2011) Increased brain injury and worsened neurological outcome in interleukin-4 knockout mice after transient focal cerebral ischemia. Stroke 42:2026–2032

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

Liu P, Zhao H, Wang R, Wang P, Tao Z, Gao L, Yan F, Liu X, Yu S, Ji X, Luo Y (2015) MicroRNA-424 protects against focal cerebral ischemia and reperfusion injury in mice by suppressing oxidative stress. Stroke 46:513–519

Wang P, Liang J, Li Y, Li J, Yang X, Zhang X, Han S, Li S, Li J (2014) Down-regulation of miRNA-30a alleviates cerebral is-chemic injury through enhancing beclin 1-mediated autophagy. Neurochem Res 39:1279–1291

Zhao H, Tao Z, Wang R, Liu P, Yan F, Li J, Zhang C, Ji X, Luo Y (2014) MicroRNA-23a-3p attenuates oxidative stress injury in a mouse model of focal cerebral ischemia-reperfusion. Brain Res 1592:65–72

Wang L, Wang Q, Li HL, Han LY (2013) Expression of MiR200a, miR93, metastasis-related gene RECK and MMP2/MMP9 in human cervical carcinoma–relationship with prognosis. Asian Pac J Cancer Prev 14:2113–2118

Kim BH, Hong SW, Kim A, Choi SH, Yoon SO (2013) Prognostic implications for high expression of oncogenic microRNAs in advanced gastric carcinoma. J Surg Oncol 107:505–510

Ohta K, Hoshino H, Wang J, Ono S, Iida Y, Hata K, Huang SK, Colquhoun S, Hoon DS (2015) MicroRNA-93 activates c-Met/PI3K/Akt pathway activity in hepatocellular carcinoma by directly inhibiting PTEN and CDKN1A. Oncotarget 6:3211–3224

Li G, Ren S, Su Z, Liu C, Deng T, Huang D, Tian Y, Qiu Y, Liu Y (2015) Increased expression of miR-93 is associated with poor prognosis in head and neck squamous cell carcinoma. Tumour Biol 36:3949–3956

Montanini L, Lasagna L, Barili V, Jonstrup SP, Murgia A, Pazzaglia L, Conti A, Novello C, Kjems J, Perris R, Benassi MS (2012) MicroRNA cloning and sequencing in osteosarcoma cell lines: differential role of miR-93. Cell Oncol (Dordr) 35: 29–41

Yang IP, Tsai HL, Hou MF, Chen KC, Tsai PC, Huang SW, Chou WW, Wang JY, Juo SH (2012) MicroRNA-93 inhibits tumor growth and early relapse of human colorectal cancer by affecting genes involved in the cell cycle. Carcinogenesis 33:1522–1530

Tang Q, Zou Z, Zou C, Zhang Q, Huang R, Guan X, Li Q, Han Z, Wang D, Wei H, Gao X, Wang X (2015) MicroRNA-93 suppress colorectal cancer development via Wnt/beta-catenin pathway downregulating. Tumour Biol 36:1701–1710

Tasoulis MK, Douzinas EE (2016) Hypoxemic reperfusion of ischemic states: an alternative approach for the attenuation of oxidative stress mediated reperfusion injury. J Biomed Sci 23:7

Halladin NL (2015) Oxidative and inflammatory biomarkers of ischemia and reperfusion injuries. Dan Med J 62:B5054

Manzanero S, Santro T, Arumugam TV (2013) Neuronal oxidative stress in acute ischemic stroke: sources and contribution to cell injury. Neurochem Int 62:712–718

Jiang S, Deng C, Lv J, Fan C, Hu W, Di S, Yan X, Ma Z, Liang Z, Yang Y (2016) Nrf2 Weaves an Elaborate Network of Neuroprotection Against Stroke. Mol Neurobiol. doi: 10.1007/s12035-016-9707-7

Alfieri A, Srivastava S, Siow RC, Modo M, Fraser PA, Mann GE (2011) Targeting the Nrf2-Keap1 antioxidant defence pathway for neurovascular protection in stroke. J Physiol 589:4125–4136