MicroRNA‑181 inhibits glioblastoma cell growth by directly targeting CCL8

Zhai,Fengyu; Chen,Xinfeng; He,Qianyi; Zhang,Heng; Hu,Yongqiang; Wang,Dan; Liu,Shasha; Zhang,Yi

doi:10.3892/ol.2019.10480

MicroRNA‑181 inhibits glioblastoma cell growth by directly targeting CCL8

Authors:
- Fengyu Zhai
- Xinfeng Chen
- Qianyi He
- Heng Zhang
- Yongqiang Hu
- Dan Wang
- Shasha Liu
- Yi Zhang
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Affiliations: Biotherapy Center, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan 450052, P.R. China, Department of Neurology, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan 450052, P.R. China, Department of Radiotherapy, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan 450052, P.R. China, Department of Radiotherapy, Puyang Oil Field General Hospital, Puyang, Henan 457000, P.R. China
Published online on: June 14, 2019 https://doi.org/10.3892/ol.2019.10480
Pages: 1922-1930
Copyright: © Zhai et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

MicroRNAs (miRNAs/miRs), including miR‑181, are closely linked to the development and progression of glioblastoma. However, the function of miR‑181 in glioblastoma has not been fully clarified. The aim of the present study was to investigate the role of miR‑181 in glioblastoma. miR‑181 was revealed to be downregulated in glioblastoma tissues and cell lines, and associated with poor prognosis in patients with glioblastoma. Overexpression of miR‑181 inhibited glioblastoma cell proliferation, invasion and migration, arrested glioblastoma cell cycle in the G1 phase and induced glioblastoma cell apoptosis. miR‑181 was demonstrated to decrease expression of C‑C motif chemokine ligand 8 (CCL8) by directly interacting with its 3'‑untranslated region. Overexpression of CCL8 inversely reversed the proliferation, invasion and migration‑promoting effects of miR‑181 in glioblastoma cells. Furthermore, CCL8 was upregulated in glioblastoma tissues and was negatively correlated with miR‑181 expression. These results indicate that miR‑181 is a potential molecular biomarker or therapeutic target in the clinical management of glioblastoma.

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1	Vengoji R, Macha MA, Batra SK and Shonka NA: Natural products: A hope for glioblastoma patients. Oncotarget. 9:22194–22219. 2018. View Article : Google Scholar : PubMed/NCBI
2	Ouanouki A, Lamy S and Annabi B: Periostin, a signal transduction intermediate in TGF-β-induced EMT in U-87MG human glioblastoma cells, and its inhibition by anthocyanidins. Oncotarget. 9:22023–22037. 2018. View Article : Google Scholar : PubMed/NCBI
3	Liu J, Wang WM, Zhang XL, Du QH, Li HG and Zhang Y: Effect of downregulated lncRNA NBAT1 on the biological behavior of glioblastoma cells. Eur Rev Med Pharmacol Sci. 22:2715–2722. 2018.PubMed/NCBI
4	Jayachandran A, Jonathan GE, Patel B and Prabhu K: Primary spinal cord glioblastoma metastasizing to the cerebellum: A missed entity. Neurol India. 66:854–857. 2018. View Article : Google Scholar : PubMed/NCBI
5	Huang L, Boling W and Zhang JH: Hyperbaric oxygen therapy as adjunctive strategy in treatment of glioblastoma multiforme. Med Gas Res. 8:24–28. 2018. View Article : Google Scholar : PubMed/NCBI
6	Paulmurugan R, Afjei R, Sekar TV, Babikir HA and Massoud TF: A protein folding molecular imaging biosensor monitors the effects of drugs that restore mutant p53 structure and its downstream function in glioblastoma cells. Oncotarget. 9:21495–21511. 2018. View Article : Google Scholar : PubMed/NCBI
7	Tanaka H, Yamaguchi T, Hachiya K, Miwa K, Shinoda J, Hayashi M, Ogawa S, Nishibori H, Goshima S and Matsuo M: ¹¹C-methionine positron emission tomography for target delineation of recurrent glioblastoma in re-irradiation planning. Rep Pract Oncol Radiother. 23:215–219. 2018. View Article : Google Scholar : PubMed/NCBI
8	Puchalski RB, Shah N, Miller J, Dalley R, Nomura SR, Yoon JG, Smith KA, Lankerovich M, Bertagnolli D, Bickley K, et al: An anatomic transcriptional atlas of human glioblastoma. Science. 360:660–663. 2018. View Article : Google Scholar : PubMed/NCBI
9	Schulze M, Hutterer M, Sabo A, Hoja S, Lorenz J, Rothhammer-Hampl T, Herold-Mende C, Floßbach L, Monoranu C and Riemenschneider MJ: Chronophin regulates active vitamin B6 levels and transcriptomic features of glioblastoma cell lines cultured under non-adherent, serum-free conditions. BMC Cancer. 18:5242018. View Article : Google Scholar : PubMed/NCBI
10	Di Sebastiano AR, Deweyert A, Benoit S, Iredale E, Xu H, De Oliveira C, Wong E, Schmid S and Hebb MO: Preclinical outcomes of intratumoral modulation therapy for glioblastoma. Sci Rep. 8:73012018. View Article : Google Scholar : PubMed/NCBI
11	Wang X, Sun S, Tong X, Ma Q, Di H, Fu T, Sun Z, Cai Y, Fan W, Wu Q, et al: MiRNA-154-5p inhibits cell proliferation and metastasis by targeting PIWIL1 in glioblastoma. Brain Res. 1676:69–76. 2017. View Article : Google Scholar : PubMed/NCBI
12	Hinske LC, Heyn J, Hübner M, Rink J, Hirschberger S and Kreth S: Intronic miRNA-641 controls its host Gene's pathway PI3K/AKT and this relationship is dysfunctional in glioblastoma multiforme. Biochem Biophys Res Commun. 489:477–483. 2017. View Article : Google Scholar : PubMed/NCBI
13	Zhang X, Zhang X, Hu S, Zheng M, Zhang J, Zhao J, Zhang X, Yan B, Jia L, Zhao J, et al: Identification of miRNA-7 by genome-wide analysis as a critical sensitizer for TRAIL-induced apoptosis in glioblastoma cells. Nucleic Acids Res. 45:5930–5944. 2017. View Article : Google Scholar : PubMed/NCBI
14	Li LY, Xiao J, Liu Q and Xia K: Parecoxib inhibits glioblastoma cell proliferation, migration and invasion by upregulating miRNA-29c. Biol Open. 6:311–316. 2017. View Article : Google Scholar : PubMed/NCBI
15	Bing ZT, Yang GH, Xiong J, Guo L and Yang L: Identify signature regulatory network for glioblastoma prognosis by integrative mRNA and miRNA co-expression analysis. IET Syst Biol. 10:244–251. 2016. View Article : Google Scholar : PubMed/NCBI
16	Hu HQ, Sun LG and Guo WJ: Decreased miRNA-146a in glioblastoma multiforme and regulation of cell proliferation and apoptosis by target Notch1. Int J Biol Markers. 31:e270–e275. 2016. View Article : Google Scholar : PubMed/NCBI
17	Liu W, Li P, Xu Q and Wang C: Regulation of miR-181 on chemotherapy-resistant cervical cancer cells. Int J Clin Experimental Pathol. 9:4560–4565. 2016.
18	Zhou WY, Chen JC, Jiao TT, Hui N and Qi X: MicroRNA-181 targets Yin Yang 1 expression and inhibits cervical cancer progression. Mol Med Rep. 11:4541–4546. 2015. View Article : Google Scholar : PubMed/NCBI
19	Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 25:402–408. 2001. View Article : Google Scholar : PubMed/NCBI
20	Wang X, Xin Z, Xu Y and Ma J: Upregulated miRNA-622 inhibited cell proliferation, motility, and invasion via repressing Kirsten rat sarcoma in glioblastoma. Tumour Biol. 37:5963–5970. 2016. View Article : Google Scholar : PubMed/NCBI
21	Bo LJ, Wei B, Li ZH, Wang ZF, Gao Z and Miao Z: Bioinformatics analysis of miRNA expression profile between primary and recurrent glioblastoma. Eur Rev Med Pharmacol Sci. 19:3579–3586. 2015.PubMed/NCBI
22	Kouri FM, Ritner C and Stegh AH: miRNA-182 and the regulation of the glioblastoma phenotype-toward miRNA-based precision therapeutics. Cell Cycle. 14:3794–3800. 2015. View Article : Google Scholar : PubMed/NCBI
23	LeBlanc VC and Morin P: Exploring miRNA-associated signatures with diagnostic relevance in glioblastoma multiforme and breast cancer patients. J Clin Med. 4:1612–1630. 2015. View Article : Google Scholar : PubMed/NCBI
24	Wu SL, Fu X, Huang J, Jia TT, Zong FY, Mu SR, Zhu H, Yan Y, Qiu S, Wu Q, et al: Genome-wide analysis of YB-1-RNA interactions reveals a novel role of YB-1 in miRNA processing in glioblastoma multiforme. Nucleic Acids Res. 43:8516–8528. 2015. View Article : Google Scholar : PubMed/NCBI
25	Das S, Kohr M, Dunkerly-Eyring B, Lee DI, Bedja D, Kent OA, Leung AK, Henao-Mejia J, Flavell RA and Steenbergen C: Divergent effects of miR-181 family members on myocardial function through protective cytosolic and detrimental mitochondrial microRNA targets. J Am Heart Assoc. 6(pii): e0046942017.PubMed/NCBI
26	Strotbek M, Schmid S, Sànchezgonzàlez I, Boerries M, Busch H and Olayioye MA: miR-181 elevates Akt signaling by co-targeting PHLPP2 and INPP4B phosphatases in luminal breast cancer. Int J Cancer. 140:2310–2320. 2017. View Article : Google Scholar : PubMed/NCBI
27	Liu J, Xing Y and Rong L: miR-181 regulates cisplatin-resistant non-small cell lung cancer via downregulation of autophagy through the PTEN/PI3K/AKT pathway. Oncol Rep. 39:1631–1639. 2018.PubMed/NCBI
28	Su R, Lin HS, Zhang XH, Yin XL, Ning HM, Liu B, Zhai PF, Gong JN, Shen C, Song L, et al: MiR-181 family: Regulators of myeloid differentiation and acute myeloid leukemia as well as potential therapeutic targets. Oncogene. 34:3226–3239. 2015. View Article : Google Scholar : PubMed/NCBI
29	Ge B, Li J, Wei Z, Sun T, Song Y and Khan NU: Functional expression of CCL8 and its interaction with chemokine receptor CCR3. BMC Immunol. 18:542017. View Article : Google Scholar : PubMed/NCBI
30	Lee JU, Cheong HS, Shim EY, Bae DJ, Chang HS, Uh ST, Kim YH, Park JS, Lee B, Shin HD and Park CS: Gene profile of fibroblasts identify relation of CCL8 with idiopathic pulmonary fibrosis. Respir Res. 18:32017. View Article : Google Scholar : PubMed/NCBI
31	Halvorsen EC, Hamilton MJ, Young A, Wadsworth BJ, LePard NE, Lee HN, Firmino N, Collier JL and Bennewith KL: Maraviroc decreases CCL8-mediated migration of CCR5(+) regulatory T cells and reduces metastatic tumor growth in the lungs. Oncoimmunology. 5:e11503982016. View Article : Google Scholar : PubMed/NCBI