Nicotine Upregulates MicroRNA-21 and Promotes TGF-β-dependent Epithelial-mesenchymal Transition of Esophageal Cancer Cells

Overview

Journal Tumour Biol

Publisher Sage Publications

Specialty Oncology

Date 2014 Apr 24

PMID 24756761

Citations 34

Authors

Yi Zhang

Tiecheng Pan

Xiaoxuan Zhong

Cai Cheng

Affiliations

Soon will be listed here.

Abstract

A consistent positive association between cigarette smoking and the human esophageal cancer has been confirmed all over the world. However, details in the association need to be more focused on and be identified. Recently, aberrantly expressed microRNAs (miRNAs) have been shown to be promising biomarkers for understanding the tumorigenesis of a wide array of human cancers, including the esophageal cancer, and the deregulation on the epithelial to mesenchymal transition (EMT) by miRNAs is involved in the tumorigenesis. In present study, we were going to identify the role of nicotine-induced miR-21 in the EMT of esophageal cells. We found that there was an overexpression of miR-21 in esophageal specimens, having an association with cigarette smoking, and the upregulation of miR-21 was also induced by nicotine in esophageal carcinoma cell line, EC9706. Moreover, the upregulated miR-21 by nicotine promoted EMT transforming growth factor beta (TGF-β) dependently. Thus, the present study reveals a novel oncogenic role of nicotine in human esophageal cancer.

Citing Articles

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References

Asangani I, Rasheed S, Nikolova D, Leupold J, Colburn N, Post S . MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene. 2007; 27(15):2128-36. DOI: 10.1038/sj.onc.1210856. View

Au W, Su D, Yuan J . Cigarette smoking in China: public health, science, and policy. Rev Environ Health. 2012; 27(1):43-9. DOI: 10.1515/reveh-2012-0003. View

Bartel D . MicroRNAs: target recognition and regulatory functions. Cell. 2009; 136(2):215-33. PMC: 3794896. DOI: 10.1016/j.cell.2009.01.002. View

Wei W, Yang J, Zhang S, Chen W, Qiao Y . [Analysis of the esophageal cancer mortality in 2004 - 2005 and its trends during last 30 years in China]. Zhonghua Yu Fang Yi Xue Za Zhi. 2010; 44(5):398-402. View

Han M, Wang Y, Liu M, Bi X, Bao J, Zeng N . MiR-21 regulates epithelial-mesenchymal transition phenotype and hypoxia-inducible factor-1α expression in third-sphere forming breast cancer stem cell-like cells. Cancer Sci. 2012; 103(6):1058-64. PMC: 7685092. DOI: 10.1111/j.1349-7006.2012.02281.x. View

Shin V, Jin H, Ng E, Sung J, Chu K, Cho C . Activation of 5-lipoxygenase is required for nicotine mediated epithelial-mesenchymal transition and tumor cell growth. Cancer Lett. 2010; 292(2):237-45. DOI: 10.1016/j.canlet.2009.12.011. View

Kimm H, Kim S, Jee S . The independent effects of cigarette smoking, alcohol consumption, and serum aspartate aminotransferase on the alanine aminotransferase ratio in korean men for the risk for esophageal cancer. Yonsei Med J. 2010; 51(3):310-7. PMC: 2852784. DOI: 10.3349/ymj.2010.51.3.310. View

Dische S, Saunders M, Lee M, Bennett M . Cigarette smoking and cancer of bladder and lung. Br Med J. 1976; 2(6045):1174-5. PMC: 1689550. DOI: 10.1136/bmj.2.6045.1174. View

Bhagat T, Zhou L, Sokol L, Kessel R, Caceres G, Gundabolu K . miR-21 mediates hematopoietic suppression in MDS by activating TGF-β signaling. Blood. 2013; 121(15):2875-81. PMC: 3624935. DOI: 10.1182/blood-2011-12-397067. View

10.

Pan X, Wang Z, Wang R . MicroRNA-21: a novel therapeutic target in human cancer. Cancer Biol Ther. 2010; 10(12):1224-32. DOI: 10.4161/cbt.10.12.14252. View

11.

Di Bernardini E, Campagnolo P, Margariti A, Zampetaki A, Karamariti E, Hu Y . Endothelial lineage differentiation from induced pluripotent stem cells is regulated by microRNA-21 and transforming growth factor β2 (TGF-β2) pathways. J Biol Chem. 2013; 289(6):3383-93. PMC: 3916541. DOI: 10.1074/jbc.M113.495531. View

12.

Al-Wadei M, Al-Wadei H, Schuller H . Effects of chronic nicotine on the autocrine regulation of pancreatic cancer cells and pancreatic duct epithelial cells by stimulatory and inhibitory neurotransmitters. Carcinogenesis. 2012; 33(9):1745-53. PMC: 3514900. DOI: 10.1093/carcin/bgs229. View

13.

Lee Y, Cohet C, Yang Y, Stayner L, Hashibe M, Straif K . Meta-analysis of epidemiologic studies on cigarette smoking and liver cancer. Int J Epidemiol. 2009; 38(6):1497-511. DOI: 10.1093/ije/dyp280. View

14.

Mani S, Guo W, Liao M, Eaton E, Ayyanan A, Zhou A . The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell. 2008; 133(4):704-15. PMC: 2728032. DOI: 10.1016/j.cell.2008.03.027. View

15.

Ishiguro S, Sasazuki S, Inoue M, Kurahashi N, Iwasaki M, Tsugane S . Effect of alcohol consumption, cigarette smoking and flushing response on esophageal cancer risk: a population-based cohort study (JPHC study). Cancer Lett. 2008; 275(2):240-6. DOI: 10.1016/j.canlet.2008.10.020. View

16.

Min S, Xiaoyan X, Fanghui P, Yamei W, Xiaoli Y, Feng W . The glioma-associated oncogene homolog 1 promotes epithelial--mesenchymal transition in human esophageal squamous cell cancer by inhibiting E-cadherin via Snail. Cancer Gene Ther. 2013; 20(7):379-85. DOI: 10.1038/cgt.2013.36. View

17.

Gao Y, McLaughlin J, Blot W, Ji B, Benichou J, Dai Q . Risk factors for esophageal cancer in Shanghai, China. I. Role of cigarette smoking and alcohol drinking. Int J Cancer. 1994; 58(2):192-6. DOI: 10.1002/ijc.2910580208. View

18.

Fuxe J, Karlsson M . TGF-β-induced epithelial-mesenchymal transition: a link between cancer and inflammation. Semin Cancer Biol. 2012; 22(5-6):455-61. DOI: 10.1016/j.semcancer.2012.05.004. View

19.

Zhang B, Zhang Z, Xia S, Xing C, Ci X, Li X . KLF5 activates microRNA 200 transcription to maintain epithelial characteristics and prevent induced epithelial-mesenchymal transition in epithelial cells. Mol Cell Biol. 2013; 33(24):4919-35. PMC: 3889554. DOI: 10.1128/MCB.00787-13. View

20.

Reinhart B, Slack F, Basson M, Pasquinelli A, Bettinger J, Rougvie A . The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature. 2000; 403(6772):901-6. DOI: 10.1038/35002607. View