MicroRNA-326 functions as a tumor suppressor in colorectal cancer by targeting the nin one binding protein

Wu,Lei; Hui,Hui; Wang,Li-Juan; Wang,Hao; Liu,Qiu-Fang; Han,Su-Xia

doi:10.3892/or.2015.3840

MicroRNA-326 functions as a tumor suppressor in colorectal cancer by targeting the nin one binding protein

Authors:
- Lei Wu
- Hui Hui
- Li-Juan Wang
- Hao Wang
- Qiu-Fang Liu
- Su-Xia Han
View Affiliations

Affiliations: Department of Radiotherapy, The First Affiliated Hospital of Medical College of Xi'an Jiaotong University, Xi'an, Shaanxi 710061, P.R. China, Center of Gynecological Oncology, Shaanxi Provincial Tumor Hospital, Xi'an, Shaanxi 710068, P.R. China, Department of Oncology, The First Affiliated Hospital of Medical College of Xi'an Jiaotong University, Xi'an, Shaanxi 710061, P.R. China, Center of Radiotherapy, Shaanxi Provincial Tumor Hospital, Xi'an, Shaanxi 710068, P.R. China
Published online on: March 6, 2015 https://doi.org/10.3892/or.2015.3840
Pages: 2309-2318

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

Accumulating evidence has demonstrated that microRNAs (miRNAs) are involved in multiple processes in cancer development and progression. miR-326 has been identified as a tumor suppressor miRNA in several types of human cancer. However, the specific function of miR-326 and its target the nin one binding protein (NOB1) in colorectal carcinoma (CRC) remains unclear. In the present study, we found that miR-326 inhibited cell proliferation, migration and invasion, and induced cell apoptosis and cell cycle arrest of CRC cells by directly targeting NOB1. Furthermore, the upregulation of miR-326 in CRC cells was revealed to be associated with a feedback loop involving downregulation of the NOB1, which mimics the phenotype induced by miR-326. Importantly, we found that the CRC patients with high expression of miR-326 or low expression of NOB1 tend to obtain a better prognosis. Thus, for the first time, we provide convincing evidence that downregulation of miR-326 inhibited tumor proliferation and tumor metastasis by directly targeting NOB1 in CRC. NOB1 and miR-326 could be potential therapeutic targets for CRC.

View Figures

View References

1	Siegel R, Ma J, Zou Z and Jemal A: Cancer statistics, 2014. CA Cancer J Clin. 64:9–29. 2014. View Article : Google Scholar : PubMed/NCBI
2	Kumar MS, Lu J, Mercer KL, Golub TR and Jacks T: Impaired microRNA processing enhances cellular transformation and tumorigenesis. Nat Genet. 39:673–677. 2007. View Article : Google Scholar : PubMed/NCBI
3	Ma Y, Zhang P, Wang F, Zhang H, Yang J, Peng J, Liu W and Qin H: miR-150 as a potential biomarker associated with prognosis and therapeutic outcome in colorectal cancer. Gut. 61:1447–1453. 2012. View Article : Google Scholar
4	Almeida MI, Nicoloso MS, Zeng L, et al: Strand-specific miR-28-5p and miR-28-3p have distinct effects in colorectal cancer cells. Gastroenterology. 142:886–896.e9. 2012. View Article : Google Scholar : PubMed/NCBI
5	Pichler M, Ress AL, Winter E, Stiegelbauer V, Karbiener M, Schwarzenbacher D, Scheideler M, Ivan C, Jahn SW, Kiesslich T, et al: MiR-200a regulates epithelial to mesenchymal transition-related gene expression and determines prognosis in colorectal cancer patients. Br J Cancer. 110:1614–1621. 2014. View Article : Google Scholar : PubMed/NCBI
6	Sun HB, Chen X, Ji H, Wu T, Lu HW, Zhang Y, Li H and Li YM: miR-494 is an independent prognostic factor and promotes cell migration and invasion in colorectal cancer by directly targeting PTEN. Int J Oncol. 45:2486–2494. 2014.PubMed/NCBI
7	Zhou J, Xu T, Yan Y, Qin R, Wang H, Zhang X, Huang Y, Wang Y, Lu Y, Fu D, et al: MicroRNA-326 functions as a tumor suppressor in glioma by targeting the Nin one binding protein (NOB1). PLoS One. 8:e684692013. View Article : Google Scholar : PubMed/NCBI
8	Du W, Liu X, Chen L, et al: Targeting the SMO oncogene by miR-326 inhibits glioma biological behaviors and stemness. Neuro Oncol. 17:243–253. 2015. View Article : Google Scholar
9	Ferretti E, De Smaele E, Miele E, Laneve P, Po A, Pelloni M, Paganelli A, Di Marcotullio L, Caffarelli E, Screpanti I, et al: Concerted microRNA control of Hedgehog signalling in cerebellar neuronal progenitor and tumour cells. EMBO J. 27:2616–2627. 2008. View Article : Google Scholar : PubMed/NCBI
10	Meng F, Henson R, Lang M, Wehbe H, Maheshwari S, Mendell JT, Jiang J, Schmittgen TD and Patel T: Involvement of human micro-RNA in growth and response to chemotherapy in human cholangiocarcinoma cell lines. Gastroenterology. 130:2113–2129. 2006. View Article : Google Scholar : PubMed/NCBI
11	Babashah S, Sadeghizadeh M, Hajifathali A, Tavirani MR, Zomorod MS, Ghadiani M and Soleimani M: Targeting of the signal transducer Smo links microRNA-326 to the oncogenic Hedgehog pathway in CD34⁺ CML stem/progenitor cells. Int J Cancer. 133:579–589. 2013. View Article : Google Scholar : PubMed/NCBI
12	Makarova KS, Aravind L, Galperin MY, Grishin NV, Tatusov RL, Wolf YI and Koonin EV: Comparative genomics of the Archaea (Euryarchaeota): Evolution of conserved protein families, the stable core, and the variable shell. Genome Res. 9:608–628. 1999.PubMed/NCBI
13	Zhang Y, Ni J, Zhou G, Yuan J, Ren W, Shan Y, Tang W, Yu L and Zhao S: Cloning, expression and characterization of the human NOB1 gene. Mol Biol Rep. 32:185–189. 2005. View Article : Google Scholar : PubMed/NCBI
14	Fatica A, Oeffinger M, Dlakić M and Tollervey D: Nob1p is required for cleavage of the 3′ end of 18S rRNA. Mol Cell Biol. 23:1798–1807. 2003. View Article : Google Scholar : PubMed/NCBI
15	Huang WY, Chen DH, Ning L and Wang LW: siRNA mediated silencing of NIN1/RPN12 binding protein 1 homolog inhibits proliferation and growth of breast cancer cells. Asian Pac J Cancer Prev. 13:1823–1827. 2012. View Article : Google Scholar : PubMed/NCBI
16	Lin Y, Peng S, Yu H, Teng H and Cui M: RNAi-mediated downregulation of NOB1 suppresses the growth and colony-formation ability of human ovarian cancer cells. Med Oncol. 29:311–317. 2012. View Article : Google Scholar
17	Li Y, Ma C, Qian M, Wen Z, Jing H and Qian D: Downregulation of NOB1 suppresses the proliferation and tumor growth of non-small cell lung cancer in vitro and in vivo. Oncol Rep. 31:1271–1276. 2014.PubMed/NCBI
18	Lu Z, Guo Q, Shi A, Xie F and Lu Q: Downregulation of NIN/RPN12 binding protein inhibit the growth of human hepatocellular carcinoma cells. Mol Biol Rep. 39:501–507. 2012. View Article : Google Scholar
19	He XW, Tao F, Luo SS and Yu XK: Effect of lentivirus-mediated NOB1 gene silencing by RNA interference on proliferation and apoptosis of human colon cancer cells. Zhonghua Wei Chang Wai Ke Za Zhi. 15:1182–1186. 2012.In Chinese. PubMed/NCBI
20	Gao F and Wang W: MicroRNA-96 promotes the proliferation of colorectal cancer cells and targets tumor protein p53 inducible nuclear protein S1, forkhead box protein O1 (FOXO1) and FOXO3a. Mol Med Rep. 11:1200–1206. 2015.
21	Xue G, Yan HL, Zhang Y, Hao LQ, Zhu XT, Mei Q and Sun SH: c-Myc-mediated repression of miR-15-16 in hypoxia is induced by increased HIF-2α and promotes tumor angiogenesis and metastasis by upregulating FGF2. Oncogene. Apr 7–2014.Epub ahead of print. View Article : Google Scholar
22	Fernandez S, Risolino M, Mandia N, et al: miR-340 inhibits tumor cell proliferation and induces apoptosis by targeting multiple negative regulators of p27 in non-small cell lung cancer. Oncogene. 0:2014.PubMed/NCBI
23	Li T, Yang J, Lv X, Liu K, Gao C, Xing Y and Xi T: miR-155 regulates the proliferation and cell cycle of colorectal carcinoma cells by targeting E2F2. Biotechnol Lett. 36:1743–1752. 2014. View Article : Google Scholar : PubMed/NCBI
24	Wu DP and He XW: Expression of NOB1 and its significance in colorectal cancer. Nan Fang Yi Ke Da Xue Xue Bao. 32:420–422. 2012.In Chinese. PubMed/NCBI
25	Liu Y, Huang H, Yuan B, Zhuang LY, Luo TP and Zhang Q: Lentivirus-mediated knockdown of NOB1 suppresses the proliferation of colon cancer cells. Z Gastroenterol. 52:429–435. 2014. View Article : Google Scholar : PubMed/NCBI
26	Meng W, Wang PS, Liu J, Xue S, Wang GM, Meng XY and Chen G: Adenovirus-mediated siRNA targeting NOB1 inhibits tumor growth and enhances radiosensitivity of human papillary thyroid carcinoma in vitro and in vivo. Oncol Rep. 32:2411–2420. 2014.PubMed/NCBI
27	Granneman S, Nandineni MR and Baserga SJ: The putative NTPase Fap7 mediates cytoplasmic 20S pre-rRNA processing through a direct interaction with Rps14. Mol Cell Biol. 25:10352–10364. 2005. View Article : Google Scholar : PubMed/NCBI
28	Raychaudhuri S, Fontanes V, Barat B and Dasgupta A: Activation of ribosomal RNA transcription by hepatitis C virus involves upstream binding factor phosphorylation via induction of cyclin D1. Cancer Res. 69:2057–2064. 2009. View Article : Google Scholar : PubMed/NCBI
29	Meraner J, Lechner M, Loidl A, Goralik-Schramel M, Voit R, Grummt I and Loidl P: Acetylation of UBF changes during the cell cycle and regulates the interaction of UBF with RNA polymerase I. Nucleic Acids Res. 34:1798–1806. 2006. View Article : Google Scholar : PubMed/NCBI
30	Fasanaro P, Capogrossi MC and Martelli F: Regulation of the endothelial cell cycle by the ubiquitin-proteasome system. Cardiovasc Res. 85:272–280. 2010. View Article : Google Scholar
31	Xu G, Bernaudo S, Fu G, Lee DY, Yang BB and Peng C: Cyclin G2 is degraded through the ubiquitin-proteasome pathway and mediates the antiproliferative effect of activin receptor-like kinase 7. Mol Biol Cell. 19:4968–4979. 2008. View Article : Google Scholar : PubMed/NCBI
32	Li W, Liu M, Feng Y, Xu YF, Huang YF, Che JP, Wang GC, Yao XD and Zheng JH: Downregulated miR-646 in clear cell renal carcinoma correlated with tumour metastasis by targeting the nin one binding protein (NOB1). Br J Cancer. 111:1188–1200. 2014. View Article : Google Scholar : PubMed/NCBI
33	Song M, Yin Y, Zhang J, Zhang B, Bian Z, Quan C, Zhou L, Hu Y, Wang Q, Ni S, et al: MiR-139-5p inhibits migration and invasion of colorectal cancer by downregulating AMFR and NOTCH1. Protein Cell. 5:851–861. 2014. View Article : Google Scholar : PubMed/NCBI
34	Kjersem JB, Ikdahl T, Lingjaerde OC, Guren T, Tveit KM and Kure EH: Plasma microRNAs predicting clinical outcome in metastatic colorectal cancer patients receiving first-line oxaliplatin-based treatment. Mol Oncol. 8:59–67. 2014. View Article : Google Scholar
35	No authors listed. MicroRNA miR-133 represses HERG K⁺ channel expression contributing to QT prolongation in diabetic hearts. J Biol Chem. 286:286562011.