Survivin is a prognostic indicator in glioblastoma and may be a target of microRNA‑218

Tong,Xuezhi; Yang,Pei; Wang,Kuanyu; Liu,Yanwei; Liu,Xiu; Shan,Xia; Huang,Ruoyu; Zhang,Ke'nan; Wang,Jiangfei

doi:10.3892/ol.2019.10335

Survivin is a prognostic indicator in glioblastoma and may be a target of microRNA‑218

Authors:
- Xuezhi Tong
- Pei Yang
- Kuanyu Wang
- Yanwei Liu
- Xiu Liu
- Xia Shan
- Ruoyu Huang
- Ke'nan Zhang
- Jiangfei Wang
View Affiliations

Affiliations: Department of Neurosurgery, Beijing Tiantan Hospital, Beijing 100050, P.R. China, Department of Neurosurgery, Beijing Neurosurgical Institute, Capital Medical University, Beijing 100050, P.R. China
Published online on: May 7, 2019 https://doi.org/10.3892/ol.2019.10335
Pages: 359-367

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Accumulating evidence has revealed that survivin expression is associated with a malignant phenotype and poor prognosis in glioma. Survivin is also a potential target of microRNA (miRNA/miR)‑218. The aim of the present study was to investigate the expression and function of survivin in glioblastoma, and to examine the association between survivin and miR‑218. For that purpose, survivin mRNA levels were analyzed in 144 frozen samples of glioblastoma using whole‑genome RNA sequencing. In vitro cell proliferation, migration, invasion and apoptosis assays were performed, and survivin expression was detected by western blotting. The results revealed that the mRNA expression levels of survivin were negatively and significantly associated with overall survival in glioblastoma. Further in vitro analyses suggested that miR‑218 may inhibit the expression of survivin. Expression of miR‑218 in the LN229 cell line was significantly lower than that in the immortalized human gliocyte HEB cell line. miR‑218 markedly inhibited tumor cell proliferation, migration and invasion capacities, and decreased apoptosis. miR‑218 also inhibited the expression of survivin. These results indicated that survivin may be a target of miR‑218 and could serve as a predictive biomarker.

View Figures

View References

1	Weller M, van den Bent M, Hopkins K, Tonn JC, Stupp R, Falini A, Cohen-Jonathan-Moyal E, Frappaz D, Henriksson R, Balana C, et al: EANO guideline for the diagnosis and treatment of anaplastic gliomas and glioblastoma. Lancet Oncol. 15:e395–e403. 2014. View Article : Google Scholar : PubMed/NCBI
2	Thakkar JP, Dolecek TA, Horbinski C, Ostrom QT, Lightner DD, Barnholtz-Sloan JS and Villano JL: Epidemiologic and molecular prognostic review of glioblastoma. Cancer Epidemiol Biomarkers Prev. 23:1985–1996. 2014. View Article : Google Scholar : PubMed/NCBI
3	Ostrom QT, Gittleman H, Stetson L, Virk SM and Barnholtz-Sloan JS: Epidemiology of gliomas. Cancer Treat Res. 163:1–14. 2015. View Article : Google Scholar : PubMed/NCBI
4	Omuro A and DeAngelis LM: Glioblastoma and other malignant gliomas: A clinical review. JAMA. 310:1842–1850. 2013. View Article : Google Scholar : PubMed/NCBI
5	Li N, Wang L, Tan G, Guo Z, Liu L, Yang M and He J: MicroRNA-218 inhibits proliferation and invasion in ovarian cancer by targeting Runx2. Oncotarget. 8:91530–91541. 2017.PubMed/NCBI
6	Shi D and Zhang Y, Lu R and Zhang Y: The long non-coding RNA MALAT1 interacted with miR-218 modulates choriocarcinoma growth by targeting Fbxw8. Biomed Pharmacother. 97:543–550. 2018. View Article : Google Scholar : PubMed/NCBI
7	Mohr AM and Mott JL: Overview of microRNA biology. Semin Liver Dis. 35:3–11. 2015. View Article : Google Scholar : PubMed/NCBI
8	Hammond SM: An overview of microRNAs. Adv Drug Deliv Rev. 87:3–14. 2015. View Article : Google Scholar : PubMed/NCBI
9	Chen P, Zhao Y and Li Y: MiR-218 inhibits migration and invasion of lung cancer cell by regulating Robo1 expression. Zhongguo Fei Ai Za Zhi. 20:452–458. 2017.(In Chinese). PubMed/NCBI
10	Bao ZS, Li MY, Wang JY, Zhang CB, Wang HJ, Yan W, Liu YW, Zhang W, Chen L and Jiang T: Prognostic value of a nine-gene signature in glioma patients based on mRNA expression profiling. CNS Neurosci Ther. 20:112–118. 2014. View Article : Google Scholar : PubMed/NCBI
11	Chen W, Yu Q, Chen B, Lu X and Li Q: The prognostic value of a seven-microRNA classifier as a novel biomarker for the prediction and detection of recurrence in glioma patients. Oncotarget. 7:53392–53413. 2016.PubMed/NCBI
12	Yang Y, Ding L, Hu Q, Xia J, Sun J, Wang X, Xiong H, Gurbani D, Li L, Liu Y and Liu A: MicroRNA-218 functions as a tumor suppressor in lung cancer by targeting IL-6/STAT3 and negatively correlates with poor prognosis. Mol Cancer. 16:1412017. View Article : Google Scholar : PubMed/NCBI
13	Cheng MW, Wang LL and Hu GY: Expression of microRNA-218 and its clinicopathological and prognostic significance in human glioma cases. Asian Pac J Cancer Prev. 16:1839–1843. 2015. View Article : Google Scholar : PubMed/NCBI
14	Mobahat M, Narendran A and Riabowol K: Survivin as a preferential target for cancer therapy. Int J Mol Sci. 15:2494–2516. 2014. View Article : Google Scholar : PubMed/NCBI
15	Jaskoll T, Chen H, Min Zhou Y, Wu D and Melnick M: Developmental expression of survivin during embryonic submandibular salivary gland development. BMC Dev Biol. 1:52001. View Article : Google Scholar : PubMed/NCBI
16	Conde M, Michen S, Wiedemuth R, Klink B, Schröck E, Schackert G and Temme A: Chromosomal instability induced by increased BIRC5/Survivin levels affects tumorigenicity of glioma cells. BMC Cancer. 17:8892017. View Article : Google Scholar : PubMed/NCBI
17	Sheng L, Wan B, Feng P, Sun J, Rigo F, Bennett CF, Akerman M, Krainer AR and Hua Y: Downregulation of Survivin contributes to cell-cycle arrest during postnatal cardiac development in a severe spinal muscular atrophy mouse model. Hum Mol Genet. 27:486–498. 2018. View Article : Google Scholar : PubMed/NCBI
18	Yoshikawa K, Shimada M, Higashijima J, Nakao T, Nishi M, Takasu C, Kashihara H, Eto S and Bando Y: Ki-67 and survivin as predictive factors for rectal cancer treated with preoperative chemoradiotherapy. Anticancer Res. 38:1735–1739. 2018.PubMed/NCBI
19	Li PL, Zhang X, Wang LL, Du LT, Yang YM, Li J and Wang CX: MicroRNA-218 is a prognostic indicator in colorectal cancer and enhances 5-fluorouracil-induced apoptosis by targeting BIRC5. Carcinogenesis. 36:1484–1493. 2015.PubMed/NCBI
20	Kogo R, How C, Chaudary N, Bruce J, Shi W, Hill RP, Zahedi P, Yip KW and Liu FF: The microRNA-218~Survivin axis regulates migration, invasion, and lymph node metastasis in cervical cancer. Oncotarget. 6:1090–1100. 2015. View Article : Google Scholar : PubMed/NCBI
21	Hu Y, Xu K and Yagüe E: miR-218 targets survivin and regulates resistance to chemotherapeutics in breast cancer. Breast Cancer Res Treat. 151:269–280. 2015. View Article : Google Scholar : PubMed/NCBI
22	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
23	Ishiyama M, Miyazono Y, Sasamoto K, Ohkura Y and Ueno K: A highly water-soluble disulfonated tetrazolium salt as a chromogenic indicator for NADH as well as cell viability. Talanta. 44:1299–1305. 1997. View Article : Google Scholar : PubMed/NCBI
24	Sun Y, Zhang Y and Chi P: Pirfenidone suppresses TGF-β1-induced human intestinal fibroblasts activities by regulating proliferation and apoptosis via the inhibition of the Smad and PI3K/AKT signaling pathway. Mol Med Rep. 18:3907–3913. 2018.PubMed/NCBI
25	Dai Z, Wu J, Chen F, Cheng Q, Zhang M, Wang Y, Guo Y and Song T: CXCL5 promotes the proliferation and migration of glioma cells in autocrine- and paracrine-dependent manners. Oncol Rep. 36:3303–3310. 2016. View Article : Google Scholar : PubMed/NCBI
26	Zhang T, Shao Y, Chu TY, Huang HS, Liou YL, Li Q and Zhou H: MiR-135a and MRP1 play pivotal roles in the selective lethality of phenethyl isothiocyanate to malignant glioma cells. Am J Cancer Res. 6:957–972. 2016.PubMed/NCBI
27	Lechler P, Renkawitz T, Campean V, Balakrishnan S, Tingart M, Grifka J and Schaumburger J: The antiapoptotic gene survivin is highly expressed in human chondrosarcoma and promotes drug resistance in chondrosarcoma cells in vitro. BMC Cancer. 11:1202011. View Article : Google Scholar : PubMed/NCBI
28	Zhao G, Wang Q, Gu Q, Qiang W, Wei JJ, Dong P, Watari H, Li W and Yue J: Lentiviral CRISPR/Cas9 nickase vector mediated BIRC5 editing inhibits epithelial to mesenchymal transition in ovarian cancer cells. Oncotarget. 8:94666–94680. 2017.PubMed/NCBI
29	Slattery ML, Mullany LE, Sakoda LC, Wolff RK, Samowitz WS and Herrick JS: Dysregulated genes and miRNAs in the apoptosis pathway in colorectal cancer patients. Apoptosis. 23:237–250. 2018. View Article : Google Scholar : PubMed/NCBI
30	Jingjing L, Wangyue W, Qiaoqiao X and Jietong Y: MiR-218 increases sensitivity to cisplatin in esophageal cancer cells via targeting survivin expression. Open Med (Wars). 11:31–35. 2016.PubMed/NCBI
31	Zarogoulidis P, Petanidis S, Kioseoglou E, Domvri K, Anestakis D and Zarogoulidis K: MiR-205 and miR-218 expression is associated with carboplatin chemoresistance and regulation of apoptosis via Mcl-1 and Survivin in lung cancer cells. Cell Signal. 27:1576–1588. 2015. View Article : Google Scholar : PubMed/NCBI
32	Zheng HC: The molecular mechanisms of chemoresistance in cancers. Oncotarget. 8:59950–59964. 2017.PubMed/NCBI
33	Tu Y, Gao X, Li G, Fu H, Cui D, Liu H, Jin W and Zhang Y: MicroRNA-218 inhibits glioma invasion, migration, proliferation, and cancer stem-like cell self-renewal by targeting the polycomb group gene Bmi1. Cancer Res. 73:6046–6055. 2013. View Article : Google Scholar : PubMed/NCBI
34	Gu JJ, Gao GZ and Zhang SM: miR-218 inhibits the migration and invasion of glioma U87 cells through the Slit2-Robo1 pathway. Oncol Lett. 9:1561–1566. 2015. View Article : Google Scholar : PubMed/NCBI
35	Xia H, Yan Y, Hu M, Wang Y, Wang Y, Dai Y, Chen J, Di G, Chen X and Jiang X: MiR-218 sensitizes glioma cells to apoptosis and inhibits tumorigenicity by regulating ECOP-mediated suppression of NF-κB activity. Neuro Oncol. 15:413–422. 2013. View Article : Google Scholar : PubMed/NCBI
36	Xu J, Xu W and Zhu J: Propofol suppresses proliferation and invasion of glioma cells by upregulating microRNA-218 expression. Mol Med Rep. 12:4815–4820. 2015. View Article : Google Scholar : PubMed/NCBI
37	Gao X and Jin W: The emerging role of tumor-suppressive microRNA-218 in targeting glioblastoma stemness. Cancer Lett. 353:25–31. 2014. View Article : Google Scholar : PubMed/NCBI
38	Alajez NM, Lenarduzzi M, Ito E, Hui AB, Shi W, Bruce J, Yue S, Huang SH, Xu W, Waldron J, et al: MiR-218 suppresses nasopharyngeal cancer progression through downregulation of survivin and the SLIT2-ROBO1 pathway. Cancer Res. 71:2381–2391. 2011. View Article : Google Scholar : PubMed/NCBI
39	Yang X, Zhang C, Guo T, Feng Y, Liu Q, Chen Y and Zhang Q: Reduced expression of microRNA206 regulates cell proliferation via cyclinD2 in gliomas. Mol Med Rep. 11:3295–3300. 2015. View Article : Google Scholar : PubMed/NCBI
40	Wang H, Wang Y, Bao Z, Zhang C, Liu Y, Cai J and Jiang C: Hypomethylated Rab27b is a progression-associated prognostic biomarker of glioma regulating MMP-9 to promote invasion. Oncol Rep. 34:1503–1509. 2015. View Article : Google Scholar : PubMed/NCBI
41	Liu Y, Tang K, Yan W, Wang Y, You G, Kang C, Jiang T and Zhang W: Identifying Ki-67 specific miRNA-mRNA interactions in malignant astrocytomas. Neurosci Lett. 546:36–41. 2013. View Article : Google Scholar : PubMed/NCBI
42	Zhou GS, Song LJ and Yang B: Isoliquiritigenin inhibits proliferation and induces apoptosis of U87 human glioma cells in vitro. Mol Med Rep. 7:531–536. 2013. View Article : Google Scholar : PubMed/NCBI