microRNA-217 inhibits tumor progression and metastasis by downregulating EZH2 and predicts favorable prognosis in gastric cancer

Oncotarget

Volumn 6, Issue 13, 2015, Pages 10868-10879

  Chen, Dong Liang ^a   Zhang, Dong Sheng ^a   Lu, Yun Xin ^a   Chen, Le Zong ^a   Zeng, Zhao Lei ^a   He, Ming Ming ^a   Wang, Feng Hua ^a   Li, Yu Hong ^a   Zhang, Hui Zhong ^a   Pelicano, Helene ^b   Zhang, Wei ^b   Xu, Rui Hua ^a  

^a SUN YAT SEN UNIVERSITY CANCER CENTER   (China)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

EZH2; Gastric cancer; Metastasis; microRNA; microRNA 217

Indexed keywords

MICRORNA; MICRORNA 217; TRANSCRIPTION FACTOR EZH2; UNCLASSIFIED DRUG; EZH2 PROTEIN, HUMAN; MIRN217 MICRORNA, HUMAN; POLYCOMB REPRESSIVE COMPLEX 2;

ADULT; ARTICLE; CANCER GROWTH; CANCER INHIBITION; CANCER PROGNOSIS; CANCER SURVIVAL; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE ASSOCIATION; DOWN REGULATION; FEMALE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MAJOR CLINICAL STUDY; MALE; METASTASIS; OVERALL SURVIVAL; PHENOTYPE; STOMACH CANCER; UPREGULATION; ANIMAL; BAGG ALBINO MOUSE; CELL MOTION; GENETIC TRANSFECTION; GENETICS; KAPLAN MEIER METHOD; METABOLISM; MIDDLE AGED; MORTALITY; NUDE MOUSE; PATHOLOGY; PROGNOSIS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; STOMACH NEOPLASMS; TIME FACTOR; TUMOR CELL LINE; TUMOR INVASION;

ANIMALS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; DOWN-REGULATION; ENHANCER OF ZESTE HOMOLOG 2 PROTEIN; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; KAPLAN-MEIER ESTIMATE; MALE; MICE, INBRED BALB C; MICE, NUDE; MICRORNAS; MIDDLE AGED; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; POLYCOMB REPRESSIVE COMPLEX 2; PROGNOSIS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; STOMACH NEOPLASMS; TIME FACTORS; TRANSFECTION;

EID: 84929645859     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3451     Document Type: Article

References (39)

1. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010 CA Cancer J Clin. 2010; 60:277-300.
2. Kamangar F, Dores GM, Anderson WF. Patterns of cancer incidence, mortality, and prevalence across five continents:defining priorities to reduce cancer disparities in different geographic regions of the world. J Clin Oncol. 2006; 24:2137-2150.
3. Chen DL, Zeng ZL, Yang J, Ren C, Wang DS, Wu WJ, Xu RH. L1cam promotes tumor progression and metastasis and is an independent unfavorable prognostic factor in gastric cancer. J Hematol Oncol. 2013; 6:43.
4. Chen DL, Wang ZQ, Ren C, Zeng ZL, Wang DS, Luo HY, Wang F, Qiu MZ, Bai L, Zhang DS, Wang FH, Li YH, Xu RH. Abnormal expression of paxillin correlates with tumor progression and poor survival in patients with gastric cancer. J Transl Med. 2013; 11:277.
5. Pillai RS. MicroRNA function: multiple mechanisms for a tiny RNA?. RNA. 2005; 11:1753-1761.
6. Zamore PD, Haley B. Ribo-gnome: the big world of small RNAs. Science. 2005; 309:1519-1524.
7. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004; 116:281-297.
8. Esquela-Kerscher A, Slack FJ. Oncomirs - microRNAs with a role in cancer. Nat Rev Cancer. 2006; 6:259-269.
9. Calin GA, Croce CM. MicroRNA signatures in human cancers. Nat Rev Cancer. 2006; 6:857-866.
10. Bueno MJ, Perez de Castro I, Malumbres M. Control of cell proliferation pathways by microRNAs. Cell Cycle. 2008; 7:3143-3148.
11. Nicoloso MS, Spizzo R, Shimizu M, Rossi S, Calin GA. MicroRNAs-the micro steering wheel of tumour metastases. Nat Rev Cancer. 2009; 9:293-302.
12. Zhang B, Pan X, Cobb GP, Anderson TA. microRNAs as oncogenes and tumor suppressors. Dev Biol. 2007; 302:1-12.
13. Hur K, Toiyama Y, Takahashi M, Balaguer F, Nagasaka T, Koike J, Hemmi H, Koi M, Boland CR, Goel A. MicroRNA-200c modulates epithelial-to-mesenchymal transition (EMT) in human colorectal cancer metastasis. Gut. 2013; 62:1315-1326.
14. Bier A, Giladi N, Kronfeld N, Lee HK, Cazacu S, Finniss S, Xiang C, Poisson L, deCarvalho AC, Slavin S, Jacoby E, Yalon M, Toren A, et al. MicroRNA-137 is downregulated in glioblastoma and inhibits the stemness of glioma stem cells by targeting RTVP-1. Oncotarget. 2013; 4:665-676.
15. Kinoshita T, Hanazawa T, Nohata N, Kikkawa N, Enokida H, Yoshino H, Yamasaki T, Hidaka H, Nakagawa M, Okamoto Y, Seki N. Tumor suppressive microRNA-218 inhibits cancer cell migration and invasion through targeting laminin-332 in head and neck squamous cell carcinoma. Oncotarget. 2012; 3:1386-1400.
16. Asangani IA, Harms PW, Dodson L, Pandhi M, Kunju LP, Maher CA, Fullen DR, Johnson TM, Giordano TJ, Palanisamy N, Chinnaiyan AM. Genetic and epigenetic loss of microRNA-31 leads to feed-forward expression of EZH2 in melanoma. Oncotarget. 2012; 3:1011-1025.
17. Song S, Ajani JA. The role of microRNAs in cancers of the upper gastrointestinal tract. Nat Rev Gastroenterol Hepatol. 2013; 10:109-118.
18. Ding XM. MicroRNAs: regulators of cancer metastasis and epithelial-mesenchymal transition (EMT). Chin J Cancer. 2014; 33:140-147.
19. Zhao WG, Yu SN, Lu ZH, Ma YH, Gu YM, Chen J. The miR-217 microRNA functions as a potential tumor suppressor in pancreatic ductal adenocarcinoma by targeting KRAS. Carcinogenesis. 2010; 31:1726-1733.
20. Li H, Zhao J, Zhang JW, Huang QY, Huang JZ, Chi LS, Tang HJ, Liu GQ, Zhu DJ, Ma WM. MicroRNA-217, down-regulated in clear cell renal cell carcinoma and associated with lower survival, suppresses cell proliferation and migration. Neoplasma. 2013; 60:511-515.
21. Wang W, Zhao LJ, Tan YX, Ren H, Qi ZT. MiR-138 induces cell cycle arrest by targeting cyclin D3 in hepatocellular carcinoma. Carcinogenesis. 2012; 33:1113-1120.
22. Valk-Lingbeek ME, Bruggeman SW, van Lohuizen M. Stem cells and cancer; the polycomb connection. Cell. 2004; 118:409-418.
23. Mahmoudi T, Verrijzer CP. Chromatin silencing and activation by Polycomb and trithorax group proteins. Oncogene. 2001; 20:3055-3066.
24. Varambally S, Dhanasekaran SM, Zhou M, Barrette TR, Kumar-Sinha C, Sanda MG, Ghosh D, Pienta KJ, Sewalt RG, Otte AP, Rubin MA, Chinnaiyan AM. The polycomb group protein EZH2 is involved in progression of prostate cancer. Nature. 2002; 419:624-629.
25. Matsukawa Y, Semba S, Kato H, Ito A, Yanagihara K, Yokozaki H. Expression of the enhancer of zeste homolog 2 is correlated with poor prognosis in human gastric cancer. Cancer Sci. 2006; 97:484-491.
26. Raman JD, Mongan NP, Tickoo SK, Boorjian SA, Scherr DS, Gudas LJ. Increased expression of the polycomb group gene, EZH2, in transitional cell carcinoma of the bladder. Clin Cancer Res. 2005; 11:8570-8576.
27. Carvalho J, van Grieken NC, Pereira PM, Sousa S, Tijssen M, Buffart TE, Diosdado B, Grabsch H, Santos MA, Meijer G, Seruca R, Carvalho B, Oliveira C. Lack of microRNA-101 causes E-cadherin functional deregulation through EZH2 up-regulation in intestinal gastric cancer. J Pathol. 2012; 228:31-44.
28. Wang HJ, Ruan HJ, He XJ, Ma YY, Jiang XT, Xia YJ, Ye ZY, Tao HQ. MicroRNA-101 is down-regulated in gastric cancer and involved in cell migration and invasion. Eur J Cancer. 2010; 46:2295-2303.
29. Smits M, Nilsson J, Mir SE, van der Stoop PM, Hulleman E, Niers JM, de Witt Hamer PC, Marquez VE, Cloos J, Krichevsky AM, Noske DP, Tannous BA, Wurdinger T. miR-101 is down-regulated in glioblastoma resulting in EZH2-induced proliferation, migration, and angiogenesis. Oncotarget. 2010; 1:710-720.
30. Zhang K, Sun X, Zhou X, Han L, Chen L, Shi Z, Zhang A, Ye M, Wang Q, Liu C, Wei J, Ren Y, Yang J, et al. Long non-coding RNA HOTAIR promotes glioblastoma cell cycle progression in an EZH2 dependent manner. Oncotarget. 2015; 6:537-546.
31. Su J, Wang Q, Liu Y, Zhong M. miR-217 inhibits invasion of hepatocellular carcinoma cells through direct suppression of E2F3. Mol Cell Biochem. 2014.
32. Xue Y, Abou Tayoun AN, Abo KM, Pipas JM, Gordon SR, Gardner TB, Barth RJ, Jr., Suriawinata AA, Tsongalis GJ. MicroRNAs as diagnostic markers for pancreatic ductal adenocarcinoma and its precursor, pancreatic intraepithelial neoplasm. Cancer Genet. 2013; 206:217-221.
33. Oh HK, Tan AL, Das K, Ooi CH, Deng NT, Tan IB, Beillard E, Lee J, Ramnarayanan K, Rha SY, Palanisamy N, Voorhoeve PM, Tan P. Genomic loss of miR-486 regulates tumor progression and the OLFM4 antiapoptotic factor in gastric cancer. Clin Cancer Res. 2011; 17:2657-2667.
34. Guo L, Yang TF, Liang SC, Guo JX, Wang Q. Role of EZH2 protein expression in gastric carcinogenesis among Asians: a meta-analysis. Tumour Biol. 2014; 35:6649-6656.
35. He LJ, Cai MY, Xu GL, Li JJ, Weng ZJ, Xu DZ, Luo GY, Zhu SL, Xie D. Prognostic significance of overexpression of EZH2 and H3k27me3 proteins in gastric cancer. Asian Pac J Cancer Prev. 2012; 13:3173-3178.
36. Konno Y, Dong P, Xiong Y, Suzuki F, Lu J, Cai M, Watari H, Mitamura T, Hosaka M, Hanley SJ, Kudo M, Sakuragi N. MicroRNA-101 targets EZH2, MCL-1 and FOS to suppress proliferation, invasion and stem cell-like phenotype of aggressive endometrial cancer cells. Oncotarget. 2014; 5:6049-6062.
37. Guo Y, Ying L, Tian Y, Yang P, Zhu Y, Wang Z, Qiu F, Lin J. miR-144 downregulation increases bladder cancer cell proliferation by targeting EZH2 and regulating Wnt signaling. FEBS J. 2013; 280:4531-4538.
38. Chen DL, Wang DS, Wu WJ, Zeng ZL, Luo HY, Qiu MZ, Ren C, Zhang DS, Wang ZQ, Wang FH, Li YH, Kang TB, Xu RH. Overexpression of paxillin induced by miR-137 suppression promotes tumor progression and metastasis in colorectal cancer. Carcinogenesis. 2013; 34:803-811.
39. Huang S, Jean D, Luca M, Tainsky MA, Bar-Eli M. Loss of AP-2 results in downregulation of c-KIT and enhancement of melanoma tumorigenicity and metastasis. EMBO J. 1998; 17:4358-4369.