Methylation‑associated silencing of miR‑128 promotes the development of esophageal cancer by targeting COX‑2 in areas with a high incidence of esophageal cancer

Jin,Jing; Guo,Tiantian; Guo,Yongdong; Liu,Jianghui; Qu,Feng; He,Yutong

doi:10.3892/ijo.2018.4653

Methylation‑associated silencing of miR‑128 promotes the development of esophageal cancer by targeting COX‑2 in areas with a high incidence of esophageal cancer

Authors:
- Jing Jin
- Tiantian Guo
- Yongdong Guo
- Jianghui Liu
- Feng Qu
- Yutong He
View Affiliations

Affiliations: Cancer Institute, Fourth Hospital of Hebei Medical University, Shijiazhuang, Hebei 050011, P.R. China
Published online on: December 4, 2018 https://doi.org/10.3892/ijo.2018.4653
Pages: 644-654

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

Esophageal cancer is one of the most common cancer types in the world, with a widely varying incidence between different regions. Zinc deficiency (ZD) is very common in high‑risk areas for esophageal cancer. Dietary ZD is reported to be associated with esophageal squamous cell carcinoma (ESCC). In the current study, the effects of ZD on tumorigenesis and expression of inflammatory factors were investigated in mice. It was identified that a ZD diet advanced ESCC and increased the expression of cyclooxygenase‑2 (COX‑2) prior to the occurrence of ESCC in mice. ZD significantly enhanced DNA methyltransferase (DNMT) activity and increased the expression of DNMT1 and DNMT3B. Furthermore, the expression of miR‑128 was downregulated by methylation, and COX‑2, a direct target of miR‑128, was upregulated with the reduction in miR‑128. Upregulation of miR‑128 inhibited the cell cycle, proliferation and metastasis, and the expression of COX‑2, cyclin D1 and retinoblastoma protein (Rb). Furthermore, the relative expression level of miR‑128 was negatively associated with COX‑2 in ESCC tissues. Collectively, these findings indicate that methylation‑associated silencing of miR‑128 promotes the development of esophageal cancer through upregulation of the expression of cyclin D1 and Rb by targeting COX‑2 in ZD regions with a high incidence of esophageal cancer.

View Figures

View References

1	Ferlay JSI, Ervik M, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D and Bray F: GLOBOCAN 2012 v10, Cancer Incidence and Mortality Worldwide: IARC CancerBase 11 Lyon, France International Agency for Research on Cancer. 2013, http://globocan.iarc.fr. Accessed December 12, 2013.
2	He J and Chen W: Chinese cancer registry annual report. Press Mil Med Sci Beijing. 2012:160–161. 2012.
3	Anvari K, Sima HR, Seilanian Toussi M, Anvari A, Shahidsales S, Memar B, Aledavoud SA, Forghani MN, Abdollahi A and Ghaffarzadegan K: EGFR expression in patients with esophageal squamous cell carcinoma and its association with pathologic response to preoperative chemora-diotherapy: A study in Northeastern Iran. Arch Iran Med. 20:240–245. 2017.PubMed/NCBI
4	Zeng H, Zheng R, Guo Y, Zhang S, Zou X, Wang N, Zhang L, Tang J, Chen J, Wei K, et al: Cancer survival in China, 2003-2005: A population-based study. Int J Cancer. 136:1921–1930. 2015. View Article : Google Scholar
5	Hashemian M, Poustchi H, Abnet CC, Boffetta P, Dawsey SM, Brennan PJ, Pharoah P, Etemadi A, Kamangar F, Sharafkhah M, et al: Dietary intake of minerals and risk of esophageal squamous cell carcinoma: Results from the Golestan Cohort Study. Am J Clin Nutr. 102:102–108. 2015. View Article : Google Scholar : PubMed/NCBI
6	Abnet CC, Lai B, Qiao YL, Vogt S, Luo XM, Taylor PR, Dong ZW, Mark SD and Dawsey SM: Zinc concentration in esophageal biopsy specimens measured by X-ray fluorescence and esophageal cancer risk. J Natl Cancer Inst. 97:301–306. 2005. View Article : Google Scholar : PubMed/NCBI
7	Gaither LA and Eide DJ: Eukaryotic zinc transporters and their regulation. Biometals. 14:251–270. 2001. View Article : Google Scholar
8	Zou XN, Taylor PR, Mark SD, Chao A, Wang W, Dawsey SM, Wu YP, Qiao YL and Zheng SF: Seasonal variation of food consumption and selected nutrient intake in Linxian, a high risk area for esophageal cancer in China. Int J Vitam Nutr Res. 72:375–382. 2002. View Article : Google Scholar
9	He Y, Jin J, Wang L, Hu Y, Liang D, Yang H, Liu Y and Shan B: Evaluation of miR-21 and miR-375 as prognostic biomarkers in oesophageal cancer in high-risk areas in China. Clin Exp Metastasis. 34:73–84. 2017. View Article : Google Scholar :
10	Balkwill F and Mantovani A: Inflammation and cancer: back to Virchow? Lancet. 357:539–545. 2001. View Article : Google Scholar : PubMed/NCBI
11	Coussens LM and Werb Z: Inflammation and cancer. Nature. 420:860–867. 2002. View Article : Google Scholar : PubMed/NCBI
12	Taccioli C, Wan S-G, Liu C-G, Alder H, Volinia S, Farber JL, Croce CM and Fong LY: Zinc replenishment reverses overex-pression of the proinflammatory mediator S100A8 and esophageal preneoplasia in the rat. Gastroenterology. 136:953–966. 2009. View Article : Google Scholar
13	Taccioli, Chen H, Jiang Y, Liu XP, Huang K, Smalley KJ, Farber JL, Croce CM and Fong LY: Dietary zinc deficiency fuels esophageal cancer development by inducing a distinct inflammatory signature. Oncogene. 31:4550–4558. 2012. View Article : Google Scholar :
14	Jin J, Li Z, Liu J, Wu Y, Gao X and He Y: Knockdown of zinc transporter ZIP5 (SLC39A5) expression significantly inhibits human esophageal cancer progression. Oncol Rep. 34:1431–1439. 2015. View Article : Google Scholar : PubMed/NCBI
15	Zhao S, Jiang Y, Zhao J, Li H, Yin X, Wang Y, Xie Y, Chen X, Lu J, Dong Z, et al: Quercetin-3-methyl ether inhibits esophageal carcinogenesis by targeting the AKT/mTOR/p70S6K and MAPK pathways. Mol Carcinog. 57:1540–1552. 2018. View Article : Google Scholar : PubMed/NCBI
16	Cortés González R and Villaseñor Caloca R: Esophageal cancer. Rev Gastroenterol Mex. 62:149–159. 1997.In Spanish.
17	Ambros V: MicroRNA pathways in flies and worms: Growth, death, fat, stress, and timing. Cell. 113:673–676. 2003. View Article : Google Scholar : PubMed/NCBI
18	Bartel DP: MicroRNAs: Target recognition and regulatory functions. Cell. 136:215–233. 2009. View Article : Google Scholar : PubMed/NCBI
19	Fong LY, Taccioli C, Jing R, Smalley KJ, Alder H, Jiang Y, Fadda P, Farber JL and Croce CM: MicroRNA dysregulation and esophageal cancer development depend on the extent of zinc dietary deficiency. Oncotarget. 7:10723–10738. 2016. View Article : Google Scholar : PubMed/NCBI
20	Alder H, Taccioli C, Chen H, Jiang Y, Smalley KJ, Fadda P, Ozer HG, Huebner K, Farber JL, Croce CM, et al: Dysregulation of miR-31 and miR-21 induced by zinc deficiency promotes esophageal cancer. Carcinogenesis. 33:1736–1744. 2012. View Article : Google Scholar : PubMed/NCBI
21	Fong LY, Taccioli C, Jing R, Smalley KJ, Alder H, Jiang Y, Fadda P, Farber JL and Croce CM: MicroRNA dysregulation and esophageal cancer development depend on the extent of zinc dietary deficiency. Oncotarget. 7:10723–1038. 2016. View Article : Google Scholar : PubMed/NCBI
22	Grosser T, Yu Y and Fitzgerald GA: Emotion recollected in tranquility: Lessons learned from the COX-2 saga. Annu Rev Med. 61:17–33. 2010. View Article : Google Scholar : PubMed/NCBI
23	Lin Y and Wu Z: MicroRNA-128 inhibits proliferation and invasion of glioma cells by targeting COX-2. Gene. 658:63–69. 2018. View Article : Google Scholar : PubMed/NCBI
24	Yao Q, Gu A, Wang Z and Xue Y: MicroRNA-144 functions as a tumor suppressor in gastric cancer by targeting cyclooxy-genase-2. Exp Ther Med. 15:3088–3095. 2018.PubMed/NCBI
25	Cornett AL and Lutz CS: Regulation of COX-2 expression by miR-146a in lung cancer cells. RNA. 20:1419–1430. 2014. View Article : Google Scholar : PubMed/NCBI
26	Espinosa-Parrilla Y, Muñoz X, Bonet C, Garcia N, Venceslá A, Yiannakouris N, Naccarati A, Sieri S, Panico S, Huerta JM, et al: Genetic association of gastric cancer with miRNA clusters including the cancer-related genes MIR29, MIR25, MIR93 and MIR106: Results from the EPIC-EURGAST study. Int J Cancer. 135:2065–2076. 2014. View Article : Google Scholar : PubMed/NCBI
27	Yu WW, Jiang H, Zhang CT and Peng Y: The SNAIL/miR-128 axis regulated growth, invasion, metastasis, and epithelial-to-mesen-chymal transition of gastric cancer. Oncotarget. 8:39280–39295. 2017.PubMed/NCBI
28	Takahashi Y, Iwaya T, Sawada G, Kurashige J, Matsumura T, Uchi R, Ueo H, Takano Y, Eguchi H, Sudo T, et al: Up-regulation of NEK2 by microRNA-128 methylation is associated with poor prognosis in colorectal cancer. Ann Surg Oncol. 21:205–212. 2014. View Article : Google Scholar
29	Feng Z, Xia Y, Gao T, Xu F 1, Lei Q 1, Peng C 2, Yang Y 3, Xue Q 1, Hu X 1, Wang Q, et al: The antipsychotic agent trifluoperazine hydrochloride suppresses triple-negative breast cancer tumor growth and brain metastasis by inducing G0/G1 arrest and apoptosis. Cell Death Dis. 9:10062018. View Article : Google Scholar : PubMed/NCBI
30	Zhuang ZH, Tsao SW, Deng W, Wang JD, Xia HH, He H, Feng HC, Wang LD, Gu Q, Lam SK, et al: Early upregulation of cyclooxygenase-2 in human papillomavirus type 16 and telom-erase-induced immortalization of human esophageal epithelial cells. J Gastroenterol Hepatol. 23:1613–1620. 2008. View Article : Google Scholar : PubMed/NCBI
31	Liu B, Wen JK, Li BH, Fang XM, Wang JJ, Zhang YP, Shi CJ, Zhang DQ and Han M: Celecoxib and acetylbritannilactone interact synergistically to suppress breast cancer cell growth via COX-2-dependent and -independent mechanisms. Cell Death Dis. 28:e1852011. View Article : Google Scholar
32	Yoshida A, Fujiwara T, Uotani K, Morita T, Kiyono M, Yokoo S, Hasei J, Nakata E, Kunisada T and Ozaki T: Clinical and functional significance of intracellular and extracellular microRNA-25-3p in osteosarcoma. Acta Med Okayama. 72:165–174. 2018.PubMed/NCBI
33	Komatsu S, Ichikawa D, Takeshita H, Tsujiura M, Morimura R, Nagata H, Kosuga T, Iitaka D, Konishi H, Shiozaki A, et al: Circulating microRNAs in plasma of patients with oesophageal squamous cell carcinoma. Br J Cancer. 105:104–111. 2011. View Article : Google Scholar : PubMed/NCBI
34	Komatsu S, Ichikawa D, Kawaguchi T, Miyamae M, Okajima W, Ohashi T, Imamura T, Kiuchi J, Konishi H, Shiozaki A, et al: Circulating miR-21 as an independent predictive biomarker for chemoresistance in esophageal squamous cell carcinoma. Am J Cancer Res. 6:1511–1523. 2016.PubMed/NCBI