Inhibitory effect of microRNA‑455‑5p on biological functions of esophageal squamous cell carcinoma Eca109 cells via Rab31

Liu,Ying; Tang,Yanping; Li,Ping

doi:10.3892/etm.2018.6820

Inhibitory effect of microRNA‑455‑5p on biological functions of esophageal squamous cell carcinoma Eca109 cells via Rab31

Authors:
- Ying Liu
- Yanping Tang
- Ping Li
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Affiliations: Second Department of Gastroenterology, Tianjin Integrated Traditional Chinese and Western Medicine Hospital, Tianjin Nankai Hospital, Tianjin 300100, P.R. China, College of Acupuncture and Massage, Tianjin University of Traditional Chinese Medicine, Tianjin 300193, P.R. China
Published online on: October 2, 2018 https://doi.org/10.3892/etm.2018.6820
Pages: 4959-4966
Copyright: © Liu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

The aim of the present study was to examine microRNA (miRNA or miR)‑455‑5p expression in esophageal squamous cell carcinoma (ESCC) at the tissue and cellular levels in order to elucidate its biological roles. A total of 60 patients with ESCC were enrolled in the present study and reverse transcription‑quantitative polymerase chain reaction was used to measure the expression of miR‑455‑5p. ESCC Eca109 cells were transfected with miR‑NC, miR‑455‑5p mimics or inhibitor and a Cell Counting Kit‑8 assay was used to assess proliferation. To investigate the migration and invasion abilities of Eca109 cells, Transwell and Matrigel assays were performed. Western blotting was employed to measure Rab31 protein expression, while a rescue assay was utilized to study the biological roles of miR‑455‑5p and Rab31 in Eca109 cells. To determine whether Rab31 is a direct target of miR‑455‑5p, a dual luciferase reporter assay was performed. The results revealed that miR‑455‑5p expression was decreased in ESCC tissues and was negatively correlated with metastasis and pathogenesis. In vitro overexpression of miR‑455‑5p inhibited the proliferation, migration and invasion of ESCC Eca109 cells. Furthermore, miR‑455‑5p regulated the expression of Rab31 protein in Eca109 cells. Rab31 overexpression promoted the proliferation, migration and invasion of Eca109 cells. Luciferase reporter assay results revealed that miR‑455‑5p is able to bind with the 3'‑untranslated region of Rab31 mRNA to regulate its expression. In summary, the results of the present study suggest that miR‑455‑5p expression is decreased in ESCC tissues and is miR‑455‑5p is negatively correlated with lymphatic metastasis and differentiation. As a tumor‑suppressor gene, miR‑455‑5p inhibits the proliferation, migration and invasion of ESCC Eca109 cells by suppressing the expression of Rab31.

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1	Lin D, Ma L, Ye T, Pan Y, Shao L, Song Z, Jiang S, Chen H and Xiang J: Results of neoadjuvant therapy followed by esophagectomy for patients with locally advanced thoracic esophageal squamous cell carcinoma. J Thorac Dis. 9:318–326. 2017. View Article : Google Scholar : PubMed/NCBI
2	Mao Y, Han Y and Shi W: The expression of aplysia ras homolog I (ARHI) and its inhibitory effect on cell biological behavior in esophageal squamous cell carcinoma. Onco Targets Ther. 10:1217–1226. 2017. View Article : Google Scholar : PubMed/NCBI
3	Cong L and Hu L: The value of the combination of hemoglobin, albumin, lymphocyte and platelet in predicting platinum-based chemoradiotherapy response in male patients with esophageal squamous cell carcinoma. Int Immunopharmacol. 46:75–79. 2017. View Article : Google Scholar : PubMed/NCBI
4	He Z, Li G, Tang L and Li Y: SIX1 overexpression predicts poor prognosis and induces radioresistance through AKT signaling in esophageal squamous cell carcinoma. Onco Targets Ther. 10:1071–1079. 2017. View Article : Google Scholar : PubMed/NCBI
5	Qiu B, Li J, Wang B, Wang Z, Liang Y, Cai P, Chen Z, Liu M, Fu J, Yang H and Liu H: Adjuvant therapy for a microscopically incomplete resection margin after an esophagectomy for esophageal squamous cell carcinoma. J Cancer. 8:249–257. 2017. View Article : Google Scholar : PubMed/NCBI
6	Morimoto H, Yano T, Yoda Y, Oono Y, Ikematsu H, Hayashi R, Ohtsu A and Kaneko K: Clinical impact of surveillance for head and neck cancer in patients with esophageal squamous cell carcinoma. World J Gastroenterol. 23:1051–1058. 2017. View Article : Google Scholar : PubMed/NCBI
7	Zhao Y, Ma K, Yang S, Zhang X, Wang F, Zhang X, Liu H and Fan Q: MicroRNA-125a-5p enhances the sensitivity of esophageal squamous cell carcinoma cells to cisplatin by suppressing the activation of the STAT3 signaling pathway. Int J Oncol. 53:644–658. 2018.PubMed/NCBI
8	Sugase T, Takahashi T, Serada S, Nakatsuka R, Fujimoto M, Ohkawara T, Hara H, Nishigaki T, Tanaka K, Miyazaki Y, et al: Suppressor of cytokine signaling-1 gene therapy induces potent antitumor effect in patient-derived esophageal squamous cell carcinoma xenograft mice. Int J Cancer. 140:2608–2621. 2017. View Article : Google Scholar : PubMed/NCBI
9	Xue L, Nan J, Dong L, Zhang C, Li H, Na R, He H and Wang Y: Upregulated miR-483-5p expression as a prognostic biomarker for esophageal squamous cell carcinoma. Cancer Biomark. 19:193–197. 2017. View Article : Google Scholar : PubMed/NCBI
10	Xie R, Wu SN, Gao CC, Yang XZ, Wang HG, Zhang JL, Yan W and Ma TH: MicroRNA-30d inhibits the migration and invasion of human esophageal squamous cell carcinoma cells via the post-transcriptional regulation of enhancer of zeste homolog 2. Oncol Rep. 37:1682–1690. 2017. View Article : Google Scholar : PubMed/NCBI
11	Shi Q, Wang Y, Mu Y, Wang X and Fan Q: miR-433-3p inhibits proliferation and invasion of esophageal squamous cell carcinoma by targeting GRB2. Cell Physiol Biochem. 46:2187–2196. 2018. View Article : Google Scholar : PubMed/NCBI
12	Li SP, Su HX, Zhao D and Guan QL: Plasma miRNA-506 as a prognostic biomarker for esophageal squamous cell carcinoma. Med Sci Monit. 22:2195–2201. 2016. View Article : Google Scholar : PubMed/NCBI
13	Wang C, Li Q, Liu F, Chen X, Nesa EU, Guan S, Liu B, Han L, Tan B, Wang D, et al: Serum miR-1297: A promising diagnostic biomarker in esophageal squamous cell carcinoma. Biomarkers. 21:517–522. 2016. View Article : Google Scholar : PubMed/NCBI
14	Guan S, Wang C, Chen X, Liu B, Tan B, Liu F, Wang D, Han L, Wang L, Huang X, et al: miR-613: A novel diagnostic and prognostic biomarker for patients with esophageal squamous cell carcinoma. Tumour Biol. 37:4383–4391. 2016. View Article : Google Scholar : PubMed/NCBI
15	Xu H, Yao Y, Meng F, Qian X, Jiang X, Li X, Gao Z and Gao L: Predictive value of serum miR-10b, miR-29c, and miR-205 as promising biomarkers in esophageal squamous cell carcinoma screening. Medicine (Baltimore). 94:e15582015. View Article : Google Scholar : PubMed/NCBI
16	Chen W, Chen L, Zhang Z, Meng F, Huang G, Sheng P, Zhang Z and Liao W: MicroRNA-455-3p modulates cartilage development and degeneration through modification of histone H3 acetylation. Biochim Biophys Acta. 1863:2881–2891. 2016. View Article : Google Scholar : PubMed/NCBI
17	Yao S, Tang B, Li G, Fan R and Cao F: miR-455 inhibits neuronal cell death by targeting TRAF3 in cerebral ischemic stroke. Neuropsychiatr Dis Treat. 12:3083–3092. 2016. View Article : Google Scholar : PubMed/NCBI
18	Wong N, Khwaja SS, Baker CM, Gay HA, Thorstad WL, Daly MD, Lewis JS Jr and Wang X: Prognostic microRNA signatures derived from the cancer genome atlas for head and neck squamous cell carcinomas. Cancer Med. 5:1619–1628. 2016. View Article : Google Scholar : PubMed/NCBI
19	Chai L, Kang XJ, Sun ZZ, Zeng MF, Yu SR, Ding Y, Liang JQ, Li TT and Zhao J: miR-497-5p, miR-195-5p and miR-455-3p function as tumor suppressors by targeting hTERT in melanoma A375 cells. Cancer Manag Res. 10:989–1003. 2018. View Article : Google Scholar : PubMed/NCBI
20	Zheng J, Lin Z, Zhang L and Chen H: MicroRNA-455-3p inhibits tumor cell proliferation and induces apoptosis in HCT116 human colon cancer cells. Med Sci Monit. 22:4431–4437. 2016. View Article : Google Scholar : PubMed/NCBI
21	Li Z, Meng Q, Pan A, Wu X, Cui J, Wang Y and Li L: MicroRNA-455-3p promotes invasion and migration in triple negative breast cancer by targeting tumor suppressor EI24. Oncotarget. 8:19455–19466. 2017.PubMed/NCBI
22	Chai J, Guo D, Ma W, Han D, Dong W, Guo H and Zhang Y: A feedback loop consisting of RUNX2/LncRNA-PVT1/miR-455 is involved in the progression of colorectal cancer. Am J Cancer Res. 8:538–550. 2018.PubMed/NCBI
23	Liu J, Zhang J, Li Y, Wang L, Sui B and Dai D: miR-455-5p acts as a novel tumor suppressor in gastric cancer by down-regulating RAB18. Gene. 592:308–315. 2016. View Article : Google Scholar : PubMed/NCBI
24	Cheng CM, Shiah SG, Huang CC, Hsiao JR and Chang JY: Up-regulation of miR-455-5p by the TGF-β-SMAD signalling axis promotes the proliferation of oral squamous cancer cells by targeting UBE2B. J Pathol. 240:38–49. 2016. View Article : Google Scholar : PubMed/NCBI
25	Kotzsch M, Kirchner T, Soelch S, Schäfer S, Friedrich K, Baretton G, Magdolen V and Luther T: Inverse association of rab31 and mucin-1 (CA15-3) antigen levels in estrogen receptor-positive (ER+) breast cancer tissues with clinicopathological parameters and patients' prognosis. Am J Cancer Res. 7:1959–1970. 2017.PubMed/NCBI
26	Pan Y, Zhang Y, Chen L, Liu Y, Feng Y and Yan J: The critical role of Rab31 in cell proliferation and apoptosis in cancer progression. Mol Neurobiol. 53:4431–4437. 2016. View Article : Google Scholar : PubMed/NCBI
27	Sui Y, Zheng X and Zhao D: Rab31 promoted hepatocellular carcinoma (HCC) progression via inhibition of cell apoptosis induced by PI3K/AKT/Bcl-2/BAX pathway. Tumour Biol. 36:8661–8670. 2015. View Article : Google Scholar : PubMed/NCBI
28	Wang J, Wu N, Zheng QF, Yan S, Lv C, Li SL and Yang Y: Evaluation of the 7th edition of the TNM classification in patients with resected esophageal squamous cell carcinoma. World J Gastroentero. 20:18397–18403. 2014. View Article : Google Scholar
29	Ke W, Zeng L, Hu Y, Chen S, Tian M and Hu Q: Detection of early-stage extrahepatic cholangiocarcinoma in patients with biliary strictures by soluble B7-H4 in the bile. Am J Cancer Res. 8:699–707. 2018.PubMed/NCBI
30	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
31	Zhang W, Hong R, Xue L, Ou Y, Liu X, Zhao Z, Xiao W, Dong D, Dong L and Fu M: Piccolo mediates EGFR signaling and acts as a prognostic biomarker in esophageal squamous cell carcinoma. Oncogene. 36:3890–3902. 2017. View Article : Google Scholar : PubMed/NCBI
32	Mei LL, Qiu YT, Zhang B and Shi ZZ: MicroRNAs in esophageal squamous cell carcinoma: Potential biomarkers and therapeutic targets. Cancer Biomark. 19:1–9. 2017. View Article : Google Scholar : PubMed/NCBI
33	Meng X, Chen X, Lu P, Ma W, Yue D, Song L and Fan Q: miR-202 promotes cell apoptosis in esophageal squamous cell carcinoma by targeting HSF2. Oncol Res. 25:215–223. 2017. View Article : Google Scholar : PubMed/NCBI
34	Yi J, Jin L, Chen J, Feng B, He Z, Chen L and Song H: miR-375 suppresses invasion and metastasis by direct targeting of SHOX2 in esophageal squamous cell carcinoma. Acta Biochim Biophys Sin (Shanghai). 49:159–169. 2017.PubMed/NCBI
35	Ren Y, Chen Y, Liang X, Lu Y, Pan W and Yang M: miRNA-638 promotes autophagy and malignant phenotypes of cancer cells via directly suppressing DACT3. Cancer Lett. 390:126–136. 2017. View Article : Google Scholar : PubMed/NCBI
36	Wang J, Wang Y, Sun D, Bu J, Ren F, Liu B, Zhang S, Xu Z, Pang S and Xu S: miR-455-5p promotes cell growth and invasion by targeting SOCO3 in non-small cell lung cancer. Oncotarget. 8:114956–114965. 2017.PubMed/NCBI
37	Grismayer B, Sölch S, Seubert B, Kirchner T, Schäfer S, Baretton G, Schmitt M, Luther T, Krüger A, Kotzsch M and Magdolen V: Rab31 expression levels modulate tumor-relevant characteristics of breast cancer cells. Mol Cancer. 11:622012. View Article : Google Scholar : PubMed/NCBI