Downregulation of microRNA‑155 by preoperative administration of valproic acid prevents postoperative seizures by upregulating SCN1A

Zhang,Zhijie; Wang,Zhenzhong; Zhang,Bo; Liu,Yan

doi:10.3892/mmr.2017.8004

Downregulation of microRNA‑155 by preoperative administration of valproic acid prevents postoperative seizures by upregulating SCN1A

Authors:
- Zhijie Zhang
- Zhenzhong Wang
- Bo Zhang
- Yan Liu
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Affiliations: Department of Neurosurgery, The Affiliated Yangming Hospital of Ningbo University, Ningbo, Zhejiang 315100, P.R. China, Department of Neurosurgery, Ningbo Yinzhou District No. 2 Hospital, Ningbo, Zhejiang 315100, P.R. China
Published online on: November 7, 2017 https://doi.org/10.3892/mmr.2017.8004
Pages: 1375-1381

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Abstract

The risk of seizure is increased following brain surgery such as cranioplasty. Patients with seizures that are treated with valproic acid (VPA) may have a decreased risk of further seizures. To verify microRNA (miR)‑155 as a potential biomarker for the occurrence of seizures, reverse transcription quantitative polymerase chain reaction (RT‑qPCR) was used. Computational analysis and luciferase reporter assay was performed to identify the putative target of miR‑155. RT‑qPCR and western blot analyses were used to determine the expression level of miR‑155, sodium voltage‑gated channel α subunit 1 (SCN1A) mRNA and protein. RT‑qPCR analysis indicated that miR‑155 levels in patients who experienced seizures increased 2.45‑fold compared with patient who did not experience seizures, indicating miR‑155 may be a potential biomarker for the occurrence of seizures. SCN1A was identified as a target gene of miR‑155; the luciferase reporter assay revealed a negative regulatory relationship between miR‑155 and SCN1A. The expression of SCN1A mRNA of patients receiving VPA was higher compared with the control group patients. Furthermore, the expression levels of SCN1A mRNA and protein were reduced or elevated following transfection with miR‑155 mimics or inhibitors, respectively, compared with the scramble control. Furthermore, a concentration‑dependent effect of miR‑155 on the expression of SCN1A was observed. In conclusion, miR‑155 may be associated with the risk of seizure and SCN1A may be a target gene of miR‑155. Downregulation of microRNA‑155 by preoperative administration of VPA may prevent postoperative seizure by upregulating the expression of SCN1A.

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1	Lee L, Ker J, Quah BL, Chou N, Choy D and Yeo TT: A retrospective analysis and review of an institution's experience with the complications of cranioplasty. Br J Neurosurg. 27:629–635. 2013. View Article : Google Scholar : PubMed/NCBI
2	Pechmann A, Anastasopoulos C, Korinthenberg R, van Velthoven-Wurster V and Kirschner J: Decompressive craniectomy after severe traumatic brain injury in children: Complications and outcome. Neuropediatrics. 46:5–12. 2015. View Article : Google Scholar : PubMed/NCBI
3	Ronen GM, Buckley D, Penney S and Streiner DL: Long-term prognosis in children with neonatal seizures: A population-based study. Neurology. 69:1816–1822. 2007. View Article : Google Scholar : PubMed/NCBI
4	Mizrahi EM: Neonatal seizures: Problems in diagnosis and classification. Epilepsia. 28 Suppl 1:S46–S55. 1987. View Article : Google Scholar : PubMed/NCBI
5	Sankar R and Painter MJ: Neonatal seizures: After all these years we still love what doesn't work. Neurology. 64:776–777. 2005. View Article : Google Scholar : PubMed/NCBI
6	Hunsberger JG, Fessler EB, Wang Z, Elkahloun AG and Chuang DM: Post-insult valproic acid-regulated microRNAs: Potential targets for cerebral ischemia. Am J Transl Res. 4:316–332. 2012.PubMed/NCBI
7	Filip A: MiRNA-new mechanisms of gene expression control. Postepy Biochem. 53:413–419. 2007.(In Polish). PubMed/NCBI
8	Chen K and Rajewsky N: The evolution of gene regulation by transcription factors and microRNAs. Nat Rev Genet. 8:93–103. 2007. View Article : Google Scholar : PubMed/NCBI
9	Esquela-Kerscher A and Slack FJ: Oncomirs-microRNAs with a role in cancer. Nat Rev Cancer. 6:259–269. 2006. View Article : Google Scholar : PubMed/NCBI
10	Guarnieri DJ and DiLeone RJ: MicroRNAs: A new class of gene regulators. Ann Med. 40:197–208. 2008. View Article : Google Scholar : PubMed/NCBI
11	Gauthier BR and Wollheim CB: MicroRNAs: ‘Ribo-regulators’ of glucose homeostasis. Nat Med. 12:36–38. 2006. View Article : Google Scholar : PubMed/NCBI
12	Bi Y, Liu G and Yang R: MicroRNAs: Novel regulators during the immune response. J Cell Physiol. 218:467–472. 2009. View Article : Google Scholar : PubMed/NCBI
13	Hatfield S and Ruohola-Baker H: microRNA and stem cell function. Cell Tissue Res. 331:57–66. 2008. View Article : Google Scholar : PubMed/NCBI
14	Matsubara H, Takeuchi T, Nishikawa E, Yanagisawa K, Hayashita Y, Ebi H, Yamada H, Suzuki M, Nagino M, Nimura Y, et al: Apoptosis induction by antisense oligonucleotides against miR-17-5p and miR-20a in lung cancers overexpressing miR-17-92. Oncogene. 26:6099–6105. 2007. View Article : Google Scholar : PubMed/NCBI
15	Beveridge NJ, Tooney PA, Carroll AP, Gardiner E, Bowden N, Scott RJ, Tran N, Dedova I and Cairns MJ: Dysregulation of miRNA 181b in the temporal cortex in schizophrenia. Hum Mol Genet. 17:1156–1168. 2008. View Article : Google Scholar : PubMed/NCBI
16	Kuhn DE, Nuovo GJ, Martin MM, Malana GE, Pleister AP, Jiang J, Schmittgen TD, Terry AV Jr, Gardiner K, Head E, et al: Human chromosome 21-derived miRNAs are overexpressed in down syndrome brains and hearts. Biochem Biophys Res Commun. 370:473–477. 2008. View Article : Google Scholar : PubMed/NCBI
17	Nicoloso MS and Calin GA: MicroRNA involvement in brain tumors: From bench to bedside. Brain Pathol. 18:122–129. 2008. View Article : Google Scholar : PubMed/NCBI
18	Zhou R, Yuan P, Wang Y, Hunsberger JG, Elkahloun A, Wei Y, Damschroder-Williams P, Du J, Chen G and Manji HK: Evidence for selective microRNAs and their effectors as common long-term targets for the actions of mood stabilizers. Neuropsychopharmacology. 34:1395–1405. 2009. View Article : Google Scholar : PubMed/NCBI
19	Goh WW, Oikawa H, Sng JC, Sergot M and Wong L: The role of miRNAs in complex formation and control. Bioinformatics. 28:453–456. 2012. View Article : Google Scholar : PubMed/NCBI
20	Wang L, Wu G, Qin X, Ma Q, Zhou Y, Liu S and Tan Y: Expression of Nodal on bronchial epithelial cells influenced by lung microbes through DNA methylation modulates the differentiation of T-Helper cells. Cell Physiol Biochem. 37:2012–2022. 2015. View Article : Google Scholar : PubMed/NCBI
21	Meyer FB: Calcium, neuronal hyperexcitability and ischemic injury. Brain Res Brain Res Rev. 14:227–243. 1989. View Article : Google Scholar : PubMed/NCBI
22	Cranley MR, Craner M and McGilloway E: Antiepileptic prophylaxis following severe traumatic brain injury within a military cohort. J R Army Med Corps. 162:109–114. 2016. View Article : Google Scholar : PubMed/NCBI
23	Klimek M and Dammers R: Antiepileptic drug therapy in the perioperative course of neurosurgical patients. Curr Opin Anaesthesiol. 23:564–567. 2010. View Article : Google Scholar : PubMed/NCBI
24	Creutzfeldt CJ, Tirschwell DL, Kim LJ, Schubert GB, Longstreth WT Jr and Becker KJ: Seizures after decompressive hemicraniectomy for ischaemic stroke. J Neurol Neurosurg Psychiatry. 85:721–725. 2014. View Article : Google Scholar : PubMed/NCBI
25	Krause-Titz UR, Warneke N, Freitag-Wolf S, Barth H and Mehdorn HM: Factors influencing the outcome (GOS) in reconstructive cranioplasty. Neurosurg Rev. 39:133–139. 2016. View Article : Google Scholar : PubMed/NCBI
26	Hesdorffer DC, Benn EK, Cascino GD and Hauser WA: Is a first acute symptomatic seizure epilepsy? Mortality and risk for recurrent seizure. Epilepsia. 50:1102–1108. 2009. View Article : Google Scholar : PubMed/NCBI
27	Martina M, Vida I and Jonas P: Distal initiation and active propagation of action potentials in interneuron dendrites. Science. 287:295–300. 2000. View Article : Google Scholar : PubMed/NCBI
28	Escayg A, MacDonald BT, Meisler MH, Baulac S, Huberfeld G, An-Gourfinkel I, Brice A, LeGuern E, Moulard B, Chaigne D, et al: Mutations of SCN1A, encoding a neuronal sodium channel, in two families with GEFS+2. Nat Genet. 24:343–345. 2000. View Article : Google Scholar : PubMed/NCBI
29	Liu DZ, Tian Y, Ander BP, Xu H, Stamova BS, Zhan X, Turner RJ, Jickling G and Sharp FR: Brain and blood microRNA expression profiling of ischemic stroke, intracerebral hemorrhage, and kainate seizures. J Cereb Blood Flow Metab. 30:92–101. 2010. View Article : Google Scholar : PubMed/NCBI
30	Ashhab MU, Omran A, Kong H, Gan N, He F, Peng J and Yin F: Expressions of tumor necrosis factor alpha and microRNA-155 in immature rat model of status epilepticus and children with mesial temporal lobe epilepsy. J Mol Neurosci. 51:950–958. 2013. View Article : Google Scholar : PubMed/NCBI
31	Cai Z, Li S, Li S, Song F, Zhang Z, Qi G, Li T, Qiu J, Wan J, Sui H and Guo H: Antagonist targeting microRNA-155 protects against lithium-pilocarpine-induced status epilepticus in C57BL/6 mice by activating brain-derived neurotrophic factor. Front Pharmacol. 7:1292016. View Article : Google Scholar : PubMed/NCBI