miR‑584‑5p regulates migration and invasion in non‑small cell lung cancer cell lines through regulation of MMP‑14

Guo,Tianmin; Zheng,Chenzhao; Wang,Zhigang; Zheng,Xifu

doi:10.3892/mmr.2019.9813

miR‑584‑5p regulates migration and invasion in non‑small cell lung cancer cell lines through regulation of MMP‑14

Authors:
- Tianmin Guo
- Chenzhao Zheng
- Zhigang Wang
- Xifu Zheng
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Affiliations: Department of Oncology, Shouguang People's Hospital, Shouguang, Shandong 262700, P.R. China, Department of Thoracic Surgery, Weifang Hospital of Traditional Chinese Medicine, Weifang, Shandong 261041, P.R. China, Cancer Center, Weifang Hospital of Traditional Chinese Medicine, Weifang, Shandong 261041, P.R. China, Department of Medical Oncology, Weifang Second People's Hospital, Weifang, Shandong 261041, P.R. China
Published online on: January 3, 2019 https://doi.org/10.3892/mmr.2019.9813
Pages: 1747-1752

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Abstract

An increasing number of studies have demonstrated that microRNAs (miRNAs/miRs) are involved in cancer progression. In 2010, an estimated 1,500,000 patients suffered mortality from lung cancer (LC) worldwide, and ~80% of LC patients were diagnosed with non‑small‑cell lung cancer (NSCLC). miR‑584‑5p was reported to be a potential biomarker in the diagnosis of LC; in addition, miR‑584 was recently observed to suppress the progression of thyroid carcinoma, glioma and gastric cancer. However, the specific function of miR‑584‑5p in NSCLC remains unclear. In the present study, miR‑584‑5p was decreased in the tumor tissues of NSCLC patients. Furthermore, miR‑584‑5p markedly inhibited the migration and invasion of NSCLC cells. The direct regulatory association between miR‑584‑5p and matrix metalloproteinase (MMP)‑14 was verified by a luciferase reporter gene assay. Furthermore, the results indicated that miR‑584‑5p inhibited the expression of MMP‑14 at the protein and mRNA levels. miR‑584‑5p also inhibited the expression of MMP‑4 and Slug, which are involved in tumor invasion and metastasis. Taken together, these results indicated that the miR‑584‑5p/MMP‑14 axis may serve as an anticancer target in the treatment of NSCLC patients.

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1	Lozano R, Naghavi M, Foreman K, Lim S, Shibuya K, Aboyans V, Abraham J, Adair T, Aggarwal R, Ahn SY, et al: Global and regioal mortality from 235 causes of death for 20 age groups in 1990 and 2010: A systematic analysis for the Global burden of disease study 2010. Lancet. 380:2095–2128. 2012. View Article : Google Scholar : PubMed/NCBI
2	Xue C, Hu Z, Jiang W, Zhao Y, Xu F, Huang Y, Zhao H, Wu J, Zhang Y, Zhao L, et al: National survey of the medical treatment status for non-small cell lung cancer (NSCLC) in China. Lung Cancer. 77:371–375. 2012. View Article : Google Scholar : PubMed/NCBI
3	Wang Y, Gu J, Roth JA, Hildebrandt MA, Lippman SM, Ye Y, Minna JD and Wu X: Pathway-based serum microRNA profiling and survival in patients with advanced stage non-small cell lung cancer. Cancer Res. 73:4801–4809. 2013. View Article : Google Scholar : PubMed/NCBI
4	Oak CH, Wilson D, Lee HJ, Lim HJ and Park EK: Potential molecular approaches for the early diagnosis of lung cancer (review). Mol Med Rep. 6:931–936. 2012. View Article : Google Scholar : PubMed/NCBI
5	Yang Q, Xu E, Dai J, Liu B, Han Z, Wu J, Zhang S, Peng B, Zhang Y and Jiang Y: A novel long noncoding RNA AK001796 acts as an oncogene and is involved in cell growth inhibition by resveratrol in lung cancer. Toxicol Appl Pharmacol. 285:79–88. 2015. View Article : Google Scholar : PubMed/NCBI
6	Jemal A, Bray F, Center MM, Ferlay J, Ward E and Forman D: Global cancer statistics. CA Cancer J Clin. 61:69–90. 2011. View Article : Google Scholar : PubMed/NCBI
7	Kesanakurti D, Maddirela DR, Chittivelu S, Rao JS and Chetty C: Suppression of tumor cell invasiveness and in vivo tumor growth by microRNA-874 in non-small cell lung cancer. Biochem Biophys Res Commun. 434:627–633. 2013. View Article : Google Scholar : PubMed/NCBI
8	Cho S, Park TI, Lee EB and Son SA: Poor prognostic factors in surgically resected stage I non-small cell lung cancer: Histopathologic and immunohistochemical analysis. Korean J Thorac Cardiovasc Surg. 45:101–109. 2012. View Article : Google Scholar : PubMed/NCBI
9	Valencia-Sanchez MA, Liu J, Hannon GJ and Parker R: Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev. 20:515–524. 2006. View Article : Google Scholar : PubMed/NCBI
10	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
11	Garzon R, Marcucci G and Croce CM: Targeting microRNAs in cancer: Rationale, strategies and challenges. Nat Rev Drug Discov. 9:775–789. 2010. View Article : Google Scholar : PubMed/NCBI
12	Esquela-Kerscher A, Trang P, Wiggins JF, Patrawala L, Cheng A, Ford L, Weidhaas JB, Brown D, Bader AG and Slack FJ: The let-7 microRNA reduces tumor growth in mouse models of lung cancer. Cell Cycle. 7:759–764. 2008. View Article : Google Scholar : PubMed/NCBI
13	Xiang J, Wu Y, Li DS, Wang ZY, Shen Q, Sun TQ, Guan Q and Wang YJ: miR-584 suppresses invasion and cell migration of thyroid carcinoma by regulating the target oncogene ROCK1. Oncol Res Treat. 38:436–440. 2015. View Article : Google Scholar : PubMed/NCBI
14	Xue H, Guo X, Han X, Yan S, Zhang J, Xu S, Li T, Guo X, Zhang P, Gao X, et al: MicroRNA-584-3p, a novel tumor suppressor and prognostic marker, reduces the migration and invasion of human glioma cells by targeting hypoxia-induced ROCK1. Oncotarget. 7:4785–4805. 2016. View Article : Google Scholar : PubMed/NCBI
15	Li Q, Li Z, Wei S, Wang W, Chen Z, Zhang L, Chen L, Li B, Sun G, Xu J, et al: Overexpression of miR-584-5p inhibits proliferation and induces apoptosis by targeting WW domain-containing E3 ubiquitin protein ligase 1 in gastric cancer. J Exp Clin Cancer Res. 36:592017. View Article : Google Scholar : PubMed/NCBI
16	Zhou X, Wen W, Shan X, Zhu W, Xu J, Guo R, Cheng W, Wang F, Qi LW, Chen Y, et al: A six-microRNA panel in plasma was identified as a potential biomarker for lung adenocarcinoma diagnosis. Oncotarget. 8:6513–6525. 2017.PubMed/NCBI
17	Dweep H, Sticht C, Pandey P and Gretz N: miRWalk-database: Prediction of possible miRNA binding sites by ‘walking’ the genes of three genomes. J Biomed Inform. 44:839–847. 2011. View Article : Google Scholar : PubMed/NCBI
18	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
19	Roberto GM, Delsin LEA, Vieira GM, Silva MO, Hakime RG, Gava NF, Engel EE, Scrideli CA, Tone LG and Brassesco MS: ROCK1-predictedmicroRNAs dysregulation contributes to tumor progression in ewing sarcoma. Pathol Oncol Res. 21–Dec;2017.(Epub ahead of print). View Article : Google Scholar
20	Cipolla GA, Park JK, de Oliveira LA, Lobo-Alves SC, de Almeida RC, Farias TD, Lemos Dde S, Malheiros D, Lavker RM and Petzl-Erler ML: A 3′UTR polymorphism marks differential KLRG1 mRNA levels through disruption of a miR-584-5p binding site and associates with pemphigus foliaceus susceptibility. Biochim Biophys Acta 1859. 1306–1313. 2016.
21	Chun TH, Sabeh F, Ota I, Murphy H, McDonagh KT, Holmbeck K, Birkedal-Hansen H, Allen ED and Weiss SJ: MT1-MMP-dependent neovessel formation within the confines of the three-dimensional extracellular matrix. J Cell Biol. 167:757–767. 2004. View Article : Google Scholar : PubMed/NCBI
22	Sabeh F, Ota I, Holmbeck K, Birkedal-Hansen H, Soloway P, Balbin M, Lopez-Otin C, Shapiro S, Inada M, Krane S, et al: Tumor cell traffic through the extracellular matrix is controlled by the membrane-anchored collagenase MT1-MMP. J Cell Biol. 167:769–781. 2004. View Article : Google Scholar : PubMed/NCBI
23	Tolde O, Rösel D, Mierke CT, Panková D, Folk P, Vesely P and Brábek J: Neoplastic progression of the human breast cancer cell line G3S1 is associated with elevation of cytoskeletal dynamics and upregulation of MT1-MMP. Int J Oncol. 36:833–839. 2010.PubMed/NCBI
24	Wang YZ, Wu KP, Wu AB, Yang ZC, Li JM, Mo YL, Xu M, Wu B and Yang ZX: MMP-14 overexpression correlates with poor prognosis in non-small cell lung cancer. Tumor Biol. 35:9815–9821. 2014. View Article : Google Scholar
25	Zhou H, Wu A, Fu W, Lv Z and Zhang Z: Significance of semaphorin-3A and MMP-14 protein expression in non-small cell lung cancer. Oncol Lett. 7:1395–1400. 2014. View Article : Google Scholar : PubMed/NCBI
26	Xiang X, Mei H, Qu H, Zhao X, Li D, Song H, Jiao W, Pu J, Huang K, Zheng L and Tong Q: miRNA-584-5p exerts tumor suppressive functions in human neuroblastoma through repressing transcription of matrix metalloproteinase 14. Biochim Biophys Acta 1852. 1743–1754. 2015.
27	Fils-Aimé N, Dai M, Guo J, El-Mousawi M, Kahramangil B, Neel JC and Lebrun JJ: MicroRNA-584 and the protein phosphatase and actin regulator 1 (PHACTR1), a new signaling route through which transforming growth factor-β mediates the migration and actin dynamics of breast cancer cells. J Biol Chem. 288:11807–11823. 2013. View Article : Google Scholar : PubMed/NCBI
28	Ueno K, Hirata H, Shahryari V, Chen Y, Zaman MS, Singh K, Tabatabai ZL, Hinoda Y and Dahiya R: Tumour suppressor microRNA-584 directly targets oncogene Rock-1 and decreases invasion ability in human clear cell renal cell carcinoma. Br J Cancer. 104:308–315. 2011. View Article : Google Scholar : PubMed/NCBI
29	Wang L, Yuan J, Tu Y, Mao X, He S, Fu G, Zong J and Zhang Y: Co-expression of MMP-14 and MMP-19 predicts poor survival in human glioma. Clin Transl Oncol. 15:139–145. 2013. View Article : Google Scholar : PubMed/NCBI
30	Xie H, Xue YX, Liu LB, Wang P, Liu YH and Ying HQ: Expressions of matrix metalloproteinase-7 and matrix metalloproteinase-14 associated with the activation of extracellular signal-regulated kinase1/2 in human brain gliomas of different pathological grades. Med Oncol. 28 Suppl 1:S433–S438. 2011. View Article : Google Scholar : PubMed/NCBI
31	Jemal A, Siegel R, Ward E, Murray T, Xu J, Smigal C and Thun MJ: Cancer statistics, 2006. CA Cancer J Clin. 56:106–130. 2006. View Article : Google Scholar : PubMed/NCBI
32	Kraljevic Pavelic S, Sedic M, Bosnjak H, Spaventi S and Pavelic K: Metastasis: New perspectives on an old problem. Mol Cancer. 10:222011. View Article : Google Scholar : PubMed/NCBI
33	Sohn EJ, Jung DB, Lee H, Han I, Lee J, Lee H and Kim SH: CNOT2 promotes proliferation and angiogenesis via VEGF signaling in MDA-MB-231 breast cancer cells. Cancer Lett. 412:88–98. 2018. View Article : Google Scholar : PubMed/NCBI
34	Shao S and Zhao X, Zhang X, Luo M, Zuo X, Huang S, Wang Y, Gu S and Zhao X: Notch1 signaling regulates the epithelial-mesenchymal transition and invasion of breast cancer in a Slug-dependent manner. Mol Cancer. 14:282015. View Article : Google Scholar : PubMed/NCBI