MicroRNA‑544 promotes colorectal cancer progression by targeting forkhead box O1

Yao,Guo‑Dong; Zhang,Ya‑Feng; Chen,Peng; Ren,Xiu‑Bao

doi:10.3892/ol.2017.7381

MicroRNA‑544 promotes colorectal cancer progression by targeting forkhead box O1

Authors:
- Guo‑Dong Yao
- Ya‑Feng Zhang
- Peng Chen
- Xiu‑Bao Ren
View Affiliations

Affiliations: Department of Immunology, Tianjin Medical University Cancer Institute and Hospital, National Clinical Research Center for Cancer, Tianjin 300060, P.R. China, Department of Surgery, Affiliated Hospital of Inner Mongolia Medical University, Huhhot, Inner Mongolia Autonomous Region 010050, P.R. China
Published online on: November 9, 2017 https://doi.org/10.3892/ol.2017.7381
Pages: 991-997
Copyright: © Yao 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

Dysregulation of microRNAs has been confirmed to serve an important role in cancer development and progression. However, the role of microRNA (miR)‑544 in colorectal cancer progression remains unknown. In the present study, it was observed that the expression level of miR‑544 was increased in breast cancer cell lines and tissues using the quantitative polymerase chain reaction. Overexpression of miR‑544 promoted cell proliferation and invasion in colorectal cancer, whereas inhibition of miR‑544 suppressed colorectal cancer progression as determined using MTT, colony formation and Transwell assays. Furthermore, forkhead box O1 (FOXO1) was a direct target of miR‑544. FOXO1 mediated miR‑544‑regulated colorectal cancer progression and cell cycle distribution. In conclusion, the results of the present study revealed that miR‑544 serves an important role in promoting human colorectal cancer cell progression.

View Figures

View References

1	Siegel RL, Miller KD and Jemal A: Cancer statistics, 2015. CA Cancer J Clin. 65:5–29. 2015. View Article : Google Scholar : PubMed/NCBI
2	Bartel DP: MicroRNAs: Target recognition and regulatory functions. Cell. 136:215–233. 2009. View Article : Google Scholar : PubMed/NCBI
3	Ambros V: The functions of animal microRNAs. Nature. 431:350–355. 2004. View Article : Google Scholar : PubMed/NCBI
4	Friedman RC, Farh KK, Burge CB and Bartel DP: Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 19:92–105. 2009. View Article : Google Scholar : PubMed/NCBI
5	Esquela-Kerscher A and Slack FJ: Oncomirs-microRNAs with a role in cancer. Nat Rev Cancer. 6:259–269. 2006. View Article : Google Scholar : PubMed/NCBI
6	Sakaguchi M, Hisamori S, Oshima N, Sato F, Shimono Y and Sakai Y: miR-137 regulates the tumorigenicity of colon cancer stem cells through the inhibition of DCLK1. Mol Cancer Res. 14:354–362. 2016. View Article : Google Scholar : PubMed/NCBI
7	Pathak S, Meng WJ, Nandy SK, Ping J, Bisgin A, Helmfors L, Waldmann P and Sun XF: Radiation and SN38 treatments modulate the expression of microRNAs, cytokines and chemokines in colon cancer cells in a p53-directed manner. Oncotarget. 6:44758–44780. 2015. View Article : Google Scholar : PubMed/NCBI
8	Sakai H, Sato A, Aihara Y, Ikarashi Y, Midorikawa Y, Kracht M, Nakagama H and Okamoto K: MKK7 mediates miR-493-dependent suppression of liver metastasis of colon cancer cells. Cancer Sci. 105:425–430. 2014. View Article : Google Scholar : PubMed/NCBI
9	Nagaraju GP, Madanraj AS, Aliya S, Rajitha B, Alese OB, Kariali E, Alam A and El-Rayes BF: MicroRNAs as biomarkers and prospective therapeutic targets in colon and pancreatic cancers. Tumour Biol. 37:97–104. 2016. View Article : Google Scholar : PubMed/NCBI
10	Gao YQ, Chen X, Wang P, Lu L, Zhao W, Chen C, Chen CP, Tao T, Sun J, Zheng YY, et al: Regulation of DLK1 by the maternally expressed miR-379/miR-544 cluster may underlie callipyge polar overdominance inheritance. Proc Natl Acad Sci USA. 112:pp. 13627–13632. 2015; View Article : Google Scholar : PubMed/NCBI
11	Song W, Mu H, Wu J, Liao M, Zhu H, Zheng L, He X, Niu B, Zhai Y, Bai C, et al: miR-544 regulates dairy goat male germline stem cell self-renewal via targeting PLZF. J Cell Biochem. 116:2155–2165. 2015. View Article : Google Scholar : PubMed/NCBI
12	Song WQ, Gu WQ, Qian YB, Ma X, Mao YJ and Liu WJ: Identification of long non-coding RNA involved in osteogenic differentiation from mesenchymal stem cells using RNA-Seq data. Genet Mol Res. 14:18268–18279. 2015. View Article : Google Scholar : PubMed/NCBI
13	Haga CL, Velagapudi SP, Strivelli JR, Yang WY, Disney MD and Phinney DG: Small molecule inhibition of miR-544 biogenesis disrupts adaptive responses to hypoxia by modulating ATM-mTOR signaling. ACS Chem Biol. 10:2267–2276. 2015. View Article : Google Scholar : PubMed/NCBI
14	Lu P, Gu Y, Li L, Wang F and Qiu X: miR-544a promotes breast cancer cell migration and invasion reducing cadherin 1 expression. Oncol Res. 23:165–170. 2016. View Article : Google Scholar : PubMed/NCBI
15	Mo X, Zhang F, Liang H, Liu M, Li H and Xia H: miR-544a promotes the invasion of lung cancer cells by targeting cadherina 1 in vitro. Onco Targets Ther. 7:895–900. 2014. View Article : Google Scholar : PubMed/NCBI
16	Mao L, Zhang Y, Deng X, Mo W, Yu Y and Lu H: Transcription factor KLF4 regulates microRNA-544 that targets YWHAZ in cervical cancer. Am J Cancer Res. 5:1939–1953. 2015.PubMed/NCBI
17	Zhi Q, Guo X, Guo L, Zhang R, Jiang J, Ji J, Zhang J, Zhang J, Chen X, Cai Q, et al: Oncogenic miR-544 is an important molecular target in gastric cancer. Anticancer Agents Med Chem. 13:270–275. 2013. View Article : Google Scholar : PubMed/NCBI
18	Yanaka Y, Muramatsu T, Uetake H, Kozaki K and Inazawa J: miR-544a induces epithelial-mesenchymal transition through the activation of WNT signaling pathway in gastric cancer. Carcinogenesis. 36:1363–1371. 2015. View Article : Google Scholar : PubMed/NCBI
19	Sarver AL, Thayanithy V, Scott MC, Cleton-Jansen AM, Hogendoorn PC, Modiano JF and Subramanian S: MicroRNAs at the human 14q32 locus have prognostic significance in osteosarcoma. Orphanet J Rare Dis. 8:72013. View Article : Google Scholar : PubMed/NCBI
20	Thayanithy V, Sarver AL, Kartha RV, Li L, Angstadt AY, Breen M, Steer CJ, Modiano JF and Subramanian S: Perturbation of 14q32 miRNAs-cMYC gene network in osteosarcoma. Bone. 50:171–181. 2012. View Article : Google Scholar : PubMed/NCBI
21	Ma R, Zhang G, Wang H, Lv H, Fang F and Kang X: Downregulation of miR-544 in tissue, but not in serum, is a novel biomarker of malignant transformation in glioma. Oncol Lett. 4:1321–1324. 2012.PubMed/NCBI
22	Bhattacharyya NP, Das E, Bucha S, Das S and Choudhury A: Regulation of cell cycle associated genes by microRNA and transcription factor. Microrna. 5:180–200. 2016. View Article : Google Scholar : PubMed/NCBI
23	Hou T, Ou J, Zhao X, Huang X, Huang Y and Zhang Y: MicroRNA-196a promotes cervical cancer proliferation through the regulation of FOXO1 and p27Kip1. Br J Cancer. 110:1260–1268. 2014. View Article : Google Scholar : PubMed/NCBI
24	Cao XC, Yu Y, Hou LK, Sun XH, Ge J, Zhang B and Wang X: miR-142-3p inhibits cancer cell proliferation by targeting CDC25C. Cell Prolif. 49:58–68. 2016. View Article : Google Scholar : PubMed/NCBI
25	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
26	Betel D, Wilson M, Gabow A, Marks DS and Sander C: The microRNA.org resource: Targets and expression. Nucleic Acids Res. 36:D149–D153. 2008. View Article : Google Scholar : PubMed/NCBI
27	Markopoulos GS, Roupakia E, Tokamani M, Chavdoula E, Hatziapostolou M, Polytarchou C, Marcu KB, Papavassiliou AG, Sandaltzopoulos R and Kolettas E: A step-by-step microRNA guide to cancer development and metastasis. Cell Oncol (Dordr). 40:303–339. 2017. View Article : Google Scholar : PubMed/NCBI
28	Luo Z, Zhang L, Li Z, Li X and Li G, Yu H, Jiang C, Dai Y, Guo X, Xiang J and Li G: An in silico analysis of dynamic changes in microRNA expression profiles in stepwise development of nasopharyngeal carcinoma. BMC Med Genomics. 5:32012. View Article : Google Scholar : PubMed/NCBI
29	Shao H, Mohamed EM, Xu GG, Waters M, Jing K, Ma Y, Zhang Y, Spiegel S, Idowu MO and Fang X: Carnitine palmitoyltransferase 1A functions to repress FoxO transcription factors to allow cell cycle progression in ovarian cancer. Oncotarget. 7:3832–3846. 2016. View Article : Google Scholar : PubMed/NCBI
30	Bicknell KA: Forkhead (FOX) transcription factors and the cell cycle: Measurement of DNA binding by FoxO and FoxM transcription factors. Methods Mol Biol. 296:247–262. 2005.PubMed/NCBI
31	Kuscu N and Celik-Ozenci C: FOXO1, FOXO3, and FOXO4 are differently expressed during mouse oocyte maturation and preimplantation embryo development. Gene Expr Patterns. 18:16–20. 2015. View Article : Google Scholar : PubMed/NCBI
32	Wang Q, Sztukowska M, Ojo A, Scott DA, Wang H and Lamont RJ: FOXO responses to Porphyromonas gingivalis in epithelial cells. Cell Microbiol. 17:1605–1617. 2015. View Article : Google Scholar : PubMed/NCBI
33	Schmidt M, Fernandez de Mattos S, van der Horst A, Klompmaker R, Kops GJ, Lam EW, Burgering BM and Medema RH: Cell cycle inhibition by FoxO forkhead transcription factors involves downregulation of cyclin D. Mol Cell Biol. 22:7842–7852. 2002. View Article : Google Scholar : PubMed/NCBI
34	Huang H and Tindall DJ: Dynamic FoxO transcription factors. J Cell Sci. 120:2479–2487. 2007. View Article : Google Scholar : PubMed/NCBI
35	Zhang Y, Gan B, Liu D and Paik JH: FoxO family members in cancer. Cancer Biol Ther. 12:253–259. 2011. View Article : Google Scholar : PubMed/NCBI
36	Myatt SS, Wang J, Monteiro LJ, Christian M, Ho KK, Fusi L, Dina RE, Brosens JJ, Ghaem-Maghami S and Lam EW: Definition of microRNAs that repress expression of the tumor suppressor gene FOXO1 in endometrial cancer. Cancer Res. 70:367–377. 2010. View Article : Google Scholar : PubMed/NCBI
37	Gao F and Wang W: MicroRNA-96 promotes the proliferation of colorectal cancer cells and targets tumor protein p53 inducible nuclear protein 1, forkhead box protein O1 (FOXO1) and FOXO3a. Mol Med Rep. 11:1200–1206. 2015. View Article : Google Scholar : PubMed/NCBI
38	Wu L, Li H, Jia CY, Cheng W, Yu M, Peng M, Zhu Y, Zhao Q, Dong YW, Shao K, et al: MicroRNA-223 regulates FOXO1 expression and cell proliferation. FEBS Lett. 586:1038–1043. 2012. View Article : Google Scholar : PubMed/NCBI
39	Roy UK, Henkhaus RS, Ignatenko NA, Mora J, Fultz KE and Gerner EW: Wild-type APC regulates caveolin-1 expression in human colon adenocarcinoma cell lines via FOXO1a and C-myc. Mol Carcinog. 47:947–955. 2008. View Article : Google Scholar : PubMed/NCBI