Abstract
Objectives
Esophageal cancer is one of the malignant tumor with poor survival. The 5-year survival rate of esophageal cancer patients remains poor due to limited therapeutic options and the development of drug-resistance. Recent evidence suggests that long non-coding RNAs (lncRNAs) are involved in occurrence and development of tumor, however, the molecular mechanisms of lncRNA taurine-upregulated gene 1 (TUG1) in esophageal cancer remain unknown.
Results
TUG1 was overexpressed in esophageal cancer tissues and cells. The knockdown of TUG1 repressed proliferation and invasion, while promoted apoptosis of esophageal cancer cells by negatively regulating miR-1294 expression. Furthermore, PLK1 was a target mRNA of miR-1294 in esophageal cancer cells. Therefore, the effects of PLK1 silencing on proliferation, apoptosis, and invasion of esophageal cancer cells could be overturned by silencing miR-1294. Additionally, TUG1 silencing inhibited growth of tumor cells in vivo.
Conclusions
TUG1 was found as oncogenic gene in esophageal cancer. Mechanically, TUG1 attributed to esophageal cancer process by regulating miR-1294/ PLK1 axis.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Cai XP, Chen LD, Song HB, Zhang CX, Yuan ZW, Xiang ZX (2016) PLK1 promotes epithelial–mesenchymal transition and metastasis of gastric carcinoma cells. Am J Transl Res 8:4172–4183
Cao YY et al (2018) Plumbagin inhibits the proliferation and survival of esophageal cancer cells by blocking STAT3-PLK1-AKT signaling. Cell Death Dis 9:17. https://doi.org/10.1038/s41419-017-0068-6
Chen S, Wang M, Yang H et al (2017) LncRNA TUG1 sponges microRNA-9 to promote neurons apoptosis by up-regulated Bcl2l11 under ischemia. Biochem Biophys Res Commun 485(1):167–173. https://doi.org/10.1016/j.bbrc.2017.02.043
Dong Z et al (2017) Aberrant methylation-mediated silencing of lncRNA MEG3 functions as a ceRNA in esophageal cancer. Mol Cancer Res 15:800–810. https://doi.org/10.1158/1541-7786.MCR-16-0385
Feng YB et al (2009) Overexpression of PLK1 is associated with poor survival by inhibiting apoptosis via enhancement of survivin level in esophageal squamous cell carcinoma. Int J Cancer 124:578–588. https://doi.org/10.1002/ijc.23990
Guo TY, Xu HY, Chen WJ, Wu MX, Dai X (2018) Downregulation of miR-1294 associates with prognosis and tumor progression in epithelial ovarian cancer. Eur Rev Med Pharmacol Sci 22(22):7646–7652. https://doi.org/10.26355/eurrev_201811_16381
Hu Y et al (2017) Upregulation of long noncoding RNA TUG1 promotes cervical cancer cell proliferation and migration. Cancer Med 6:471–482. https://doi.org/10.1002/cam4.994
Ilson DH (2008) Esophageal cancer chemotherapy: recent advances. Gastrointest Cancer Res 2:85–92 (PMID: 19259300)
Ishigaki M et al (2016) Diagnosis of early-stage esophageal cancer by Raman spectroscopy and chemometric techniques. Analyst 141:1027–1033. https://doi.org/10.1039/C5AN01323B
Iyer RS, Nicol SM, Quinlan PR, Thompson AM, Meek DW, Fuller-Pace FV (2014) The RNA helicase/transcriptional co-regulator, p68 (DDX5), stimulates expression of oncogenic protein kinase, Polo-like kinase-1 (PLK1), and is associated with elevated PLK1 levels in human breast cancers. Cell Cycle 13:1413–1423. https://doi.org/10.4161/cc.28415
Jiang L, Wang W, Li G et al (2016) High TUG1 expression is associated with chemotherapy resistance and poor prognosis in esophageal squamous cell carcinoma. Cancer Chemother Pharmacol 78(2):333–339. https://doi.org/10.1007/s00280-016-3066-y
Jiao C et al (2016) lncRNA-UCA1 enhances cell proliferation through functioning as a ceRNA of Sox4 in esophageal cancer. Oncol Rep 36:2960–2966. https://doi.org/10.3892/or.2016.5121
Lei H, Gao Y, Xu X (2017) LncRNA TUG1 influences papillary thyroid cancer cell proliferation, migration and EMT formation through targeting miR-145. Acta Biochim Biophys Sinica (Shanghai) 49(7):588–597. https://doi.org/10.1093/abbs/gmx047
Li J, Zhang M, An G, Ma Q (2016) LncRNA TUG1 acts as a tumor suppressor in human glioma by promoting cell apoptosis. Exp Biol Med (Maywood) 241:644–649. https://doi.org/10.1177/1535370215622708
Li Z, Shen J, Chan MTV, Wu WKK (2016) TUG1: a pivotal oncogenic long non-coding RNA of human cancers. Cell Prolif 49:471–475. https://doi.org/10.1111/cpr.12269
Liu K, Li L, Rusidanmu A, Wang Y, Lv X (2015) Down-regulation of miR-1294 is related to dismal prognosis of patients with esophageal squamous cell carcinoma through elevating C-MYC expression. Cell Physiol Biochem 36:100–110. https://doi.org/10.1159/000374056
Liu Z, Sun Q, Wang X (2017) PLK1, a potential target for cancer therapy. Transl Oncol 10(1):22–32. https://doi.org/10.1016/j.tranon.2016.10.003
Pan Z, Mao W, Bao Y, Zhang M, Su X, Xu X (2016) The long noncoding RNA CASC9 regulates migration and invasion in esophageal cancer. Cancer Med 5:2442–2447. https://doi.org/10.1002/cam4.770
Pennathur A, Gibson MK, Jobe BA, Luketich JD (2013) Oesophageal carcinoma. Lancet 381:400–412. https://doi.org/10.1016/S0140-6736(12)60643-6
Rupaimoole R, Slack FJ (2017) MicroRNA therapeutics: towards a new era for the management of cancer and other diseases. Nat Rev Drug Discov 16(3):203–222. https://doi.org/10.1038/nrd.2016.246
Shi YX, Ye BL, Hu BR, Ruan XJ (2018) Expression of miR-1294 is downregulated and predicts a poor prognosis in gastric cancer. Eur Rev Med Pharmacol Sci 22(17):5525–5530. https://doi.org/10.26355/eurrev_201809_15813
Shimada H et al (2003) Treatment response and prognosis of patients after recurrence of esophageal cancer. Surgery 133:24–31. https://doi.org/10.1067/msy.2003.31
Takahashi T et al (2003) Polo-like kinase 1 (PLK1) is overexpressed in primary colorectal cancers. Cancer Sci 94:148–152. https://doi.org/10.1111/j.1349-7006.2003.tb01411.x
Takai N, Hamanaka R, Yoshimatsu J, Miyakawa I (2005) Polo-like kinases (Plks) and cancer. Oncogene 24:287–291. https://doi.org/10.1038/sj.onc.1208272
Vishnoi A, Rani S (2017) MiRNA biogenesis and regulation of diseases: an overview. Methods Mol Biol 1509:1–10. https://doi.org/10.1007/978-1-4939-6524-3_1
Wang L et al (2016) Long non-coding RNA TUG1 promotes colorectal cancer metastasis via EMT pathway. Oncotarget 7:51713–51719. https://doi.org/10.18632/oncotarget.10563
Xiao HJ, Ji Q, Yang L, Li RT, Zhang C, Hou JM (2018) In vivo and in vitro effects of microRNA-124 on human gastric cancer by targeting JAG1 through the Notch signaling pathway. J Cell Biochem 119:2520–2534. https://doi.org/10.1002/jcb.26413
Xu Y et al (2015) Upregulation of the long noncoding RNA TUG1 promotes proliferation and migration of esophageal squamous cell carcinoma. Tumor Biol 36:1643–1651. https://doi.org/10.1007/s13277-014-2763-6
Xu C, Guo Y, Liu H, Chen G, Yan Y, Liu T (2018) TUG1 confers cisplatin resistance in esophageal squamous cell carcinoma by epigenetically suppressing PDCD4 expression via EZH2. Cell Biosci 8:61. https://doi.org/10.1186/s13578-018-0260-0
Yang B, Tang X, Wang Z, Sun D, Wei X, Ding Y (2018) TUG1 promotes prostate cancer progression by acting as a ceRNA of miR-26a. Biosci Rep 38(5):BSR20180677. https://doi.org/10.1042/BSR20180677
Yin DD et al (2015) Downregulation of lncRNA TUG1 affects apoptosis and insulin secretion in mouse pancreatic beta cells. Cell Physiol Biochem 35:1892–1904. https://doi.org/10.1159/000373999
Yu C, Li L, Xie F et al (2018) LncRNA TUG1 sponges miR-204-5p to promote osteoblast differentiation through upregulating Runx2 in aortic valve calcification. Cardiovasc Res 114(1):168–179. https://doi.org/10.1093/cvr/cvx180
Zhang X et al (2015) Elevated expression of CCAT2 is associated with poor prognosis in esophageal squamous cell carcinoma. J Surg Oncol 111:834–839. https://doi.org/10.1002/jso.23888
Zhang Z et al (2019) Hsa_circ_0004370 promotes esophageal cancer progression through miR-1294/LASP1 pathway. Biosci Rep 39:BSR20182377. https://doi.org/10.1042/BSR20182377
Zhang Q, Geng PL, Yin P, Wang XL, Jia JP, Yao J (2013) Down-regulation of long non-coding RNA TUG1 inhibits osteosarcoma cell proliferation and promotes apoptosis. Asian Pac J Cancer Prev 14:2311–2315. https://doi.org/10.7314/apjcp.2013.14.4.2311
Zhang D, Sun G, Zhang H, Tian J, Li Y (2017) Long non-coding RNA ANRIL indicates a poor prognosis of cervical cancer and promotes carcinogenesis via PI3K/Akt pathways. Biomed Pharmacother 85:511–516. https://doi.org/10.1016/j.biopha.2016.11.058
Zhang HY, Yang W, Zheng FS, Wang YB, Lu JB (2017) Long non-coding RNA SNHG1 regulates zinc finger E-box binding homeobox 1 expression by interacting with TAp63 and promotes cell metastasis and invasion in Lung squamous cell carcinoma. Biomed Pharmacother 90:650–658. https://doi.org/10.1016/j.biopha.2017.03.104
Zheng X, Hu H, Li S (2016) High expression of lncRNA PVT1 promotes invasion by inducing epithelial-to-mesenchymal transition in esophageal cancer. Oncol Lett 12:2357–2362. https://doi.org/10.3892/ol.2016.5026
Funding
Not applicable.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflict of interest to declare.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Zong, M., Feng, W., Wan, L. et al. LncRNA TUG1 promotes esophageal cancer development through regulating PLK1 expression by sponging miR-1294. Biotechnol Lett 42, 2537–2549 (2020). https://doi.org/10.1007/s10529-020-02984-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10529-020-02984-0