Paper - WANFANG MED ONLINE

You Position: Home > Paper

Spatiotemporal microRNA profile in peripheral nerve regeneration: miR-138 targets vimentin and inhibits Schwann cell migration and proliferation

( views:12, downloads:0 )

Author:: No author available

Journal Title:: Neural Regeneration Research

Issue:: 7

DOI:: 10.4103/1673-5374.235073

Key Word:: non-coding RNA;neural regeneration;nerve guide;sciatic nerve transection;peripheral nerve injury;wound healing;Gene Ontology processes;Kyoto Encyclopedia of Genes and Genomes pathways;microarray;luciferase assay

Abstract： While the peripheral nervous system has regenerative ability,restoration of sufficient function remains a challenge.Vimentin has been shown to be localized in axonal growth fronts and associated with nerve regeneration,including myelination,neuroplasticity,kinase signaling in nerve axoplasm,and cell migration;however,the mechanisms regulating its expression within Schwann cell (SC) remain unexplored.The aim of this study was to profile the spatial and temporal expression profile of microRNA (miRNA) in a regenerating rat sciatic nerve after transection,and explore the potential role of miR-138-5p targeting vimentin in SC proliferation and migration.A rat sciatic nerve transection model,utilizing a polyethylene nerve guide,was used to investigate miRNA expression at 7,14,30,60,and 90 days during nerve regeneration.Relative levels of miRNA expression were determined using microarray analysis and subsequently validated with quantitative real-time polymerase chain reaction.In vitro assays were conducted with cultured Schwann cells transfected with miRNA mimics and assessed for migratory and proliferative potential.The top seven dysregulated miRNAs reported in this study have been implicated in cell migration elsewhere,and GO and KEGG analyses predicted activities essential to wound healing.Transfection of one of these,miRNA-138-5p,into SCs reduced cell migration and proliferation.miR-138-5p has been shown to directly target vimentin in cancer cells,and the luciferase assay performed here in rat Schwann cells confirmed it.These results detail a role of miR-138-5p in rat peripheral nerve regeneration and expand on reports of it as an important regulator in the peripheral nervous system.

Reference

[1]Anjie Lu,Zufa Huang,Chaoyue Zhang,etc.Differential expression of microRNAs in dorsal root ganglia after sciatic nerve injury[J].2014,(10).
[2]Nan Jiang,Huaiqin Li,Yi Sun,etc.Differential gene expression in proximal and distal nerve segments of rats with sciatic nerve injury during Wallerian degeneration[J].2014,(12).
[3]Wang A,Shi F,Zhou X,etc.Downregulation of the Rho GTPase signaling pathway is involved in the microRNA-138-mediated inhibition of cell migration and invasion in tongue squamous cell carcinoma.[J].2010,127(3).
[4]Yahui, Liu,Wei, Zhang,Kai, Liu,etc.miR-138 suppresses cell proliferation and invasion by inhibiting SOX9 in hepatocellular carcinoma.[J].2016.
[5]Abe N,Cavalli V.Nerve injury signaling.[J].2008,18(3).
[6]Qian, Tianmei,Ding, Fei,Ding, Guohui,etc.miR-182 inhibits Schwann cell proliferation and migration by targeting FGF9 and NTM, respectively at an early stage following sciatic nerve injury[J].2012,40(20).
[7]Holway AH,Trantolo DJ,Rieger Christ KM,etc.Enhanced Peripheral Nerve Regeneration Elicited by Cell-Mediated Events Delivered via a Bioresorbable PLGA Guide.[J].2003,19(2).
[8]Park KH,Kim M,Roh JK,etc.Altered microRNA regulation in Huntington's disease models.[J].2011,227(1).
[9]Schneider, C.A.,Rasband, W.S.,Eliceiri, K.W..NIH Image to ImageJ: 25 years of image analysis[J].2012,9(7).
[10]Andrew D, Gaudet,Phillip G, Popovich,Matt S, Ramer.Wallerian degeneration: gaining perspective on inflammatory events after peripheral nerve injury.[J].2011,8.
[11].Exosomal cargo including microRNA regulates sensory neuron to macrophage communication after nerve trauma.[J].2017,8(1).
[12]Asa, Fex Svennigsen,Lars B, Dahlin.Repair of the Peripheral Nerve-Remyelination that Works.[J].2013,3(3).
[13]Akane, Hirotoshi,Saito, Fumiyo,Shiraki, Ayako,etc.Gene expression profile of brain regions reflecting aberrations in nervous system development targeting the process of neurite extension of rat offspring exposed developmentally to glycidol[J].2014,34(11).
[14]Aschrafi, A.,Kar, A.N.,Natera-Naranjo, O.,etc.MicroRNA-338 regulates the axonal expression of multiple nuclear-encoded mitochondrial mRNAs encoding subunits of the oxidative phosphorylation machinery[J].2012,69(23).
[15].Molecular mechanisms of epithelial-mesenchymal transition[J].2014,15(3).
[16]Gess, B.,Roehr, D.,Lange, E.,etc.Desmoplakin is involved in organization of an adhesion complex in peripheral nerve regeneration after injury[J].2015,264.
[17]Shen YW,Soares MB,Mayanil CS,etc.Folic acid remodels chromatin on Hes1 and Neurog2 promoters during caudal neural tube development.[J].2010,285(47).
[18]Monichan, Phay,Hak Hee, Kim,Soonmoon, Yoo.Dynamic Change and Target Prediction of Axon-Specific MicroRNAs in Regenerating Sciatic Nerve.[J].2015,10.
[19]Livak KJ,Schmittgen TD.Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method.[J].2001,25(4).
[20]Hedberg C,Martinez J,Drepper C,etc.A functional screen implicates microRNA-138-dependent regulation of the depalmitoylation enzyme APT1 in dendritic spine morphogenesis.[J].2009,11(6).
[21]S K, Lee,S W, Wolfe.Peripheral nerve injury and repair.[J].1900,8(4).
[22]Qiuyue, Yuan,Tingge, Sun,Feng, Ye,etc.MicroRNA-124-3p affects proliferation, migration and apoptosis of bladder cancer cells through targeting AURKA.[J].2017,19(1).
[23]Alexander, Berg,Johan, Zelano,Marcela, Pekna,etc.Axonal Regeneration after Sciatic Nerve Lesion Is Delayed but Complete in GFAP- and Vimentin-Deficient Mice.[J].2013,8(11).
[24]He,X.,Lu,Q.R.,Yu,Y.,etc.Unwrapping myelination by MicroRNAs[J].2012,18(1).
[25]V, Salonen,H, Aho,M, R?ytt,etc.Quantitation of Schwann cells and endoneurial fibroblast-like cells after experimental nerve trauma.[J].1988,75(4).
[26].Vimentin Intermediate Filaments Template Microtubule Networks to Enhance Persistence in Cell Polarity and Directed Migration[J].2016,(3).
[27]Dengbing Yao,Meiyuan Li,Dingding Shen,etc.Expression changes and bioinformatic analysis of Wallerian degeneration after sciatic nerve injury in rat[J].2013,(3).
[28]Tan, Yanjuan,Hu, Huaidong,Tan, Wuyuan,etc.MicroRNA-138 inhibits migration and invasion of non-small cell lung cancer cells by targeting LIMK1[J].2016,14(5 Pt.B).
[29]Liu,C.-M.,Wang,R.-Y.,Saijilafu,DepartmentofOrthopaedicSurgery,etc.MicroRNA-138 and SIRT1 form a mutual negative feedback loop to regulate mammalian axon regeneration[J].2013,27(13).
[30]Yao, Chun,Shi, Xiangxiang,Zhang, Zhanhu,etc.Hypoxia-Induced Upregulation of miR-132 Promotes Schwann Cell Migration After Sciatic Nerve Injury by Targeting PRKAG3[J].2016,53(8).
[31]Qian, Bao-Jiang,You, Ling,Shang, Fei-Fei,etc.Vimentin Regulates Neuroplasticity in Transected Spinal Cord Rats Associated with micRNA138[J].2015,51(2).
[32]Kolokythas A,Wang Y,Dai Y,etc.MicroRNA-138 suppresses epithelial-mesenchymal transition in squamous cell carcinoma cell lines.[J].2011,440(1 Pt.1).
[33]Tomita K,Fujiwara T,Hata Y,etc.Effects of the in vivo predegenerated nerve graft on early Schwann cell migration: quantitative analysis using S100-GFP mice.[J].2009,461(1).
[34]Qian T,Yu B,Gu X,etc.Early changes of microRNAs expression in the dorsal root ganglia following rat sciatic nerve transection.[J].2011,494(2).
[35]Li, Jiefang,Wang, Qinrong,Wen, Ruiling,etc.MiR-138 inhibits cell proliferation and reverses epithelial-mesenchymal transition in non-small cell lung cancer cells by targeting GIT1 and SEMA4C[J].2015,19(12).
[36]Pallari HM,Eriksson JE,Ivaska J,etc.Novel functions of vimentin in cell adhesion, migration, and signaling[J].2007,313(10).
[37]Waller A..Experiments on the Section of the Glossopharyngeal and Hypoglossal Nerves of the Frog, and Observations of the Alterations Produced Thereby in the Structure of Their Primitive Fibres[J].1850.
[38]Liu, Chunxi,Wang, Zhiyu,Wang, Yi,etc.miR-338 suppresses the growth and metastasis of OSCC cells by targeting NRP1[J].2015,398(1).
[39]Zhang, Jun,Mao, Jun,Feng, Zhuo,etc.MicroRNA-138 modulates metastasis and EMT in breast cancer cells by targeting vimentin[J].2016,77.
[40]Satelli, A.,Li, S..Vimentin in cancer and its potential as a molecular target for cancer therapy[J].2011,68(18).
[41]Bhavana V, Chapman,Abigail I, Wald,Parvez, Akhtar,etc.MicroRNA-363 targets myosin 1B to reduce cellular migration in head and neck cancer.[J].2015,15.
[42]Zhou, Songlin,Zhang, Shibo,Wang, Yaxian,etc.miR-21 and miR-222 inhibit apoptosis of adult dorsal root ganglion neurons by repressing TIMP3 following sciatic nerve injury[J].2015,586.
[43]Chang,I.A.,Kim,M.H.,Park,S.-K.,etc.Vimentin phosphorylation by Cdc2 in Schwann cell controls axon growth via β1-integrin activation[J].2012,26(6).
[44]Zhao, Guoliang,Han, Chuangye,Zhang, Zhi,etc.Increased expression of microRNA-31-5p inhibits cell proliferation, migration, and invasion via regulating Sp1 transcription factor in HepG2 hepatocellular carcinoma cell line[J].2017,490(2).
[45]Li, Yan,Rui, Cao,YuanBo, Liu,etc.MiR-21-5p Links Epithelial-Mesenchymal Transition Phenotype with Stem-Like Cell Signatures via AKT Signaling in Keloid Keratinocytes.[J].2016.
[46]Michael, Costigan,Katia, Befort,Laurie, Karchewski,etc.Replicate high-density rat genome oligonucleotide microarrays reveal hundreds of regulated genes in the dorsal root ganglion after peripheral nerve injury.[J].2002,3.
[47]Raivich,G.,Patodia,S..Downstream effector molecules in successful peripheral nerve regeneration[J].2012,349(1).
[48]Xianglai, Xu,Shiqi, Li,Yiwei, Lin,etc.MicroRNA-124-3p inhibits cell migration and invasion in bladder cancer cells by targeting ROCK1.[J].2013,11.
[49]Jie, Ying,Xuechun, Yu,Chaojian, Ma,etc.MicroRNA-363-3p is downregulated in hepatocellular carcinoma and inhibits tumorigenesis by directly targeting specificity protein 1.[J].2017,16(2).
[50]Archana N, Iyer,Ana?s, Bellon,Marie-Laure, Baudet.microRNAs in axon guidance.[J].2014,8.
[51]Yi, Sheng,Wang, Shanshan,Zhao, Qing,etc.miR-sc3, a Novel MicroRNA, Promotes Schwann Cell Proliferation and Migration by Targeting Astn1[J].2016,25(5).
[52]Jiang-Tao, Chen,Kun-Hou, Yao,Long, Hua,etc.miR-338-3p inhibits the proliferation and migration of gastric cancer cells by targeting ADAM17.[J].2015,8(9).
[53]Eran Perlson,Shlomit Hanz,Keren Ben-Yaakov,etc.Vimentin-Dependent Spatial Translocation of an Activated MAP Kinase in Injured Nerve[J].2005,45(5).
[54]T M, Brushart.Motor axons preferentially reinnervate motor pathways.[J].1993,13(6).
[55]Terenghi G.Peripheral nerve regeneration and neurotrophic factors.[J].1999,194(Pt.1).
[56]Jialei Yang,Xiufen Zhang,Xiangjie Chen,etc.Exosome Mediated Delivery of miR-124 Promotes Neurogenesis after Ischemia[J].2017,7.
[57].Non-coding RNAs as Emerging Regulators of Neural Injury Responses and Regeneration[J].2016,32(3).
[58]Li,M.,Zhang,P.,Guo,W.,etc.Protein expression profiling during wallerian degeneration after rat sciatic nerve injury[J].2014,50(1).
[59]Cai, Shang-Dang,Chen, Jian-She,Xi, Zuo-Wu,etc.MicroRNA-144 inhibits migration and proliferation in rectal cancer by downregulating ROCK-1[J].2015,12(5 Pt.B).
[60]Taveggia,C.,Previtali,S.C.,Triolo,D.,etc.Vimentin regulates peripheral nerve myelination[J].2012,139(7).
[61]T. KISLIOUK,N. MEIRI.Mir-138 Promotes the Migration of Cultured Chicken Embryonic Hypothalamic Cells by Targeting Reelin[J].2013,238.
[62]Chang LW,Nagarajan R,Viader A,etc.MicroRNAs modulate Schwann cell response to nerve injury by reinforcing transcriptional silencing of dedifferentiation-related genes.[J].2011,31(48).