High expression of lncRNA PVT1 promotes invasion by inducing epithelial‑to-mesenchymal transition in esophageal cancer

Zheng,Xiangxiang; Hu,Haibo; Li,Shiting

doi:10.3892/ol.2016.5026

High expression of lncRNA PVT1 promotes invasion by inducing epithelial‑to-mesenchymal transition in esophageal cancer

Authors:
- Xiangxiang Zheng
- Haibo Hu
- Shiting Li
View Affiliations

Affiliations: Department of Cardiothoracic Surgery, Huai'an First People's Hospital, Nanjing Medical University, Huai'an, Jiangsu 223300, P.R. China, Department of Cardiothoracic Surgery, The Affiliated Huai'an Hospital of Xuzhou Medical College, Huai'an, Jiangsu 223300, P.R. China
Published online on: August 16, 2016 https://doi.org/10.3892/ol.2016.5026
Pages: 2357-2362
Copyright: © Zheng et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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

The long non-coding RNA (lncRNA) plasmacytoma variant translocation 1 (PVT1) has been identified as an oncogene in numerous diseases, and aberrant lncRNA PVT1 expression has been associated with the development of cancer. However, the underlying mechanism by which lncRNA PVT1 affects cell invasion in esophageal cancer has been not demonstrated. In the current study, the expression of lncRNA PVT1 was found to be increased in esophageal cancer specimens (n=77) by reverse transcription‑quantitative polymerase chain reaction, and was correlated with tumor stage (P=0.009) and metastasis (P<0.001). In vitro, by using transwell assay, upregulation of lncRNA PVT1 promoted the invasion of TE‑1 esophageal cancer cells; while downregulation of lncRNA PVT1 inhibited Eca‑109 cell invasion. In addition, western blot analysis indicated that upregulation of lncRNA PVT1 may induce epithelial‑to‑mesenchymal transition (EMT) by regulating the expression levels of EMT markers (E‑cadherin, N‑cadherin and vimentin). In conclusion, lncRNA PVT1 is able to regulate the invasion of esophageal cancer cells by inducing EMT.

View Figures

View References

1	Shigaki H, Baba Y, Watanabe M, Murata A, Ishimoto T, Iwatsuki M, Iwagami S, Nosho K and Baba H: PIK3CA mutation is associated with a favorable prognosis among patients with curatively resected esophageal squamous cell carcinoma. Clin Cancer Res. 19:2451–2459. 2013. View Article : Google Scholar : PubMed/NCBI
2	Chen Y, Tong Y, Yang C, Gan Y, Sun H, Bi H, Cao S, Yin X and Lu Z: Consumption of hot beverages and foods and the risk of esophageal cancer: A meta-analysis of observational studies. BMC Cancer. 15:4492015. View Article : Google Scholar : PubMed/NCBI
3	Liao Y, Xue Y, Zhang L, Feng X, Liu W and Zhang G: Higher heat shock factor 1 expression in tumor stroma predicts poor prognosis in esophageal squamous cell carcinoma patients. J Transl Med. 13:3382015. View Article : Google Scholar : PubMed/NCBI
4	Koshy M, Esiashvilli N, Landry JC, Thomas CR Jr and Matthews RH: Multiple management modalities in esophageal cancer: Combined modality management approaches. Oncologist. 9:147–159. 2004. View Article : Google Scholar : PubMed/NCBI
5	Mercer TR, Dinger ME and Mattick JS: Long non-coding RNAs: Insights into functions. Nat Rev Genet. 10:155–159. 2009. View Article : Google Scholar : PubMed/NCBI
6	Shi Y, Li J, Liu Y, Ding J, Fan Y, Tian Y, Wang L, Lian Y, Wang K and Shu Y: The long noncoding RNA SPRY4-IT1 increases the proliferation of human breast cancer cells by upregulating ZNF703 expression. Mol Cancer. 14:512015. View Article : Google Scholar : PubMed/NCBI
7	Han L, Zhang EB, Yin DD, Kong R, Xu TP, Chen WM, Xia R, Shu YQ and De W: Low expression of long noncoding RNA PANDAR predicts a poor prognosis of non-small cell lung cancer and affects cell apoptosis by regulating Bcl-2. Cell Death Dis. 6:e16652015. View Article : Google Scholar : PubMed/NCBI
8	Hu L, Wu Y, Tan D, Meng H, Wang K, Bai Y and Yang K: Up-regulation of long noncoding RNA MALAT1 contributes to proliferation and metastasis in esophageal squamous cell carcinoma. J Exp Clin Cancer Res. 34:72015. View Article : Google Scholar : PubMed/NCBI
9	Huang C, Yu W, Wang Q, Cui H, Wang Y, Zhang L, Han F and Huang T: Increased expression of the lncRNA PVT1 is associated with poor prognosis in pancreatic cancer patients. Minerva Med. 106:143–149. 2015.PubMed/NCBI
10	Yang YR, Zang SZ, Zhong CL, Li YX, Zhao SS and Feng XJ: Increased expression of the lncRNA PVT1 promotes tumorigenesis in non-small cell lung cancer. Int J Clin Exp Pathol. 7:6929–6935. 2014.PubMed/NCBI
11	Ding J, Li D, Gong M, Wang J, Huang X, Wu T and Wang C: Expression and clinical significance of the long non-coding RNA PVT1 in human gastric cancer. Onco Targets Ther. 7:1625–1630. 2014. View Article : Google Scholar : PubMed/NCBI
12	Liu SG, Qin XG, Zhao BS, Qi B, Yao WJ, Wang TY, Li HC and Wu XN: Differential expression of miRNAs in esophageal cancer tissue. Oncol Lett. 5:1639–1642. 2013.PubMed/NCBI
13	Liu J, Ruan B, You N, Huang Q, Liu W, Dang Z, Xu W, Zhou T, Ji R, Cao Y, et al: Downregulation of miR-200a induces EMT phenotypes and CSC-like signatures through targeting the β-catenin pathway in hepatic oval cells. PLoS One. 8:e794092013. View Article : Google Scholar : PubMed/NCBI
14	Han Y, Ye J, Wu D, Wu P, Chen Z, Chen J, Gao S and Huang J: LEIGC long non-coding RNA acts as a tumor suppressor in gastric carcinoma by inhibiting the epithelial-to-mesenchymal transition. BMC Cancer. 14:9322014. View Article : Google Scholar : PubMed/NCBI
15	Dong H, Xie L, Tang C, Chen S, Liu Q, Zhang Q, Zheng W, Zheng Z and Zhang H: Snail1 correlates with patient outcomes in E-cadherin-preserved gastroesophageal junction adenocarcinoma. Clin Transl Oncol. 16:783–791. 2014. View Article : Google Scholar : PubMed/NCBI
16	Liu Y, Li H, Feng J, Cui X, Huang W, Li Y, Su F, Liu Q, Zhu J, Lv X, et al: Lin28 induces epithelial-to-mesenchymal transition and stemness via downregulation of let-7a in breast cancer cells. PLoS One. 8:e830832013. View Article : Google Scholar : PubMed/NCBI
17	Bao YX, Cao Q, Yang Y, Mao R, Xiao L, Zhang H, Zhao HR and Wen H: Expression and prognostic significance of Golgiglycoprotein73 (GP73) with epithelial-mesenchymal transition (EMT) related molecules in hepatocellular carcinoma (HCC). Diagn Pathol. 8:1972013. 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	Iguchi T, Uchi R, Nambara S, Saito T, Komatsu H, Hirata H, Ueda M, Sakimura S, Takano Y, Kurashige J, et al: A long noncoding RNA, lncRNA-ATB, is involved in the progression and prognosis of colorectal cancer. Anticancer Res. 35:1385–1388. 2015.PubMed/NCBI
20	Wang CM, Wu QQ, Li SQ, Chen FJ, Tuo L, Xie HW, Tong YS, Ji L, Zhou GZ, Cao G, et al: Upregulation of the long non-coding RNA PlncRNA-1 promotes esophageal squamous carcinoma cell proliferation and correlates with advanced clinical stage. Dig Dis Sci. 59:591–597. 2014. View Article : Google Scholar : PubMed/NCBI
21	Ge XS, Ma HJ, Zheng XH, Ruan HL, Liao XY, Xue WQ, Chen YB, Zhang Y and Jia WH: HOTAIR, a prognostic factor in esophageal squamous cell carcinoma, inhibits WIF-1 expression and activates Wnt pathway. Cancer Sci. 104:1675–1682. 2013. View Article : Google Scholar : PubMed/NCBI
22	Li W, Zheng J, Deng J, You Y, Wu H, Li N, Lu J and Zhou Y: Increased levels of the long intergenic non-protein coding RNA POU3F3 promote DNA methylation in esophageal squamous cell carcinoma cells. Gastroenterology. 146:1714–1726. 2014. View Article : Google Scholar : PubMed/NCBI
23	Xie HW, Wu QQ, Zhu B, Chen FJ, Ji L, Li SQ, Wang CM, Tong YS, Tuo L, Wu M, et al: Long noncoding RNA SPRY4-IT1 is upregulated in esophageal squamous cell carcinoma and associated with poor prognosis. Tumour Biol. 35:7743–7754. 2014. View Article : Google Scholar : PubMed/NCBI
24	Pan F, Yao J, Chen Y, Zhou C, Geng P, Mao H and Fang X: A novel long non-coding RNA FOXCUT and mRNA FOXC1 pair promote progression and predict poor prognosis in esophageal squamous cell carcinoma. Int J Clin Exp Pathol. 7:2838–2849. 2014.PubMed/NCBI
25	Kitamura K, Seike M, Okano T, Matsuda K, Miyanaga A, Mizutani H, Noro R, Minegishi Y, Kubota K and Gemma A: MiR-134/487b/655 cluster regulates TGF-β-induced epithelial-mesenchymal transition and drug resistance to gefitinib by targeting MAGI2 in lung adenocarcinoma cells. Mol Cancer Ther. 13:444–453. 2014. View Article : Google Scholar : PubMed/NCBI
26	Guo S, Xu X, Tang Y, Zhang C, Li J, Ouyang Y, Ju J, Bie P and Wang H: miR-15a inhibits cell proliferation and epithelial to mesenchymal transition in pancreatic ductal adenocarcinoma by down-regulating Bmi-1 expression. Cancer Lett. 344:40–46. 2014. View Article : Google Scholar : PubMed/NCBI
27	Yamada S, Fuchs BC, Fujii T, Shimoyama Y, Sugimoto H, Nomoto S, Takeda S, Tanabe KK, Kodera Y and Nakao A: Epithelial-to-mesenchymal transition predicts prognosis of pancreatic cancer. Surgery. 154:946–954. 2013. View Article : Google Scholar : PubMed/NCBI
28	Li SP, Xu HX, Yu Y, He JD, Wang Z, Xu YJ, Wang CY, Zhang HM, Zhang RX, Zhang JJ, et al: LncRNA HULC enhances epithelial-mesenchymal transition to promote tumorigenesis and metastasis of hepatocellular carcinoma via the miR-200a-3p/ZEB1 signaling pathway. Oncotarget. 7:2016.(Epub ahead of print) doi: 10.18632/oncotarget.9883.
29	Wang Y, Liu Z, Yao B, Dou C, Xu M, Xue Y, Ding L, Jia Y, Zhang H, Li Q, et al: Long non-coding RNA TUSC7 acts a molecular sponge for miR-10a and suppresses EMT in hepatocellular carcinoma. Tumour Biol. 2016.(Epub ahead of print).
30	Sun R, Qin C, Jiang B, Fang S, Pan X, Peng L, Liu Z, Li W, Li Y and Li G.: Down-regulation of MALAT1 inhibits cervical cancer cell invasion and metastasis by inhibition of epithelial-mesenchymal transition. Mol Biosyst. 12:952–962. 2016. View Article : Google Scholar : PubMed/NCBI
31	Vitalone MJ, Naesens M, Sigdel T, Li L, Hseih S and Sarwal MM: The dual role of epithelial-to-mesenchymal transition in chronic allograft injury in pediatric renal transplantation. Transplantation. 92:787–795. 2011. View Article : Google Scholar : PubMed/NCBI
32	López-Novoa JM and Nieto MA: Inflammation and EMT: An alliance towards organ fibrosis and cancer progression. EMBO Mol Med. 1:303–314. 2009. View Article : Google Scholar : PubMed/NCBI
33	Mucsi I and Rosivall L: Epithelial-mesenchymal transition in renal tubular cells in the pathogenesis of progressive tubulo-interstitial fibrosis. Acta Physiol Hung. 94:117–131. 2007. View Article : Google Scholar : PubMed/NCBI