miR‑365 overexpression promotes cell proliferation and invasion by targeting ADAMTS-1 in breast cancer

Li,Min; Liu,Lulu; Zang,Wenqiao; Wang,Yuanyuan; Du,Yuwen; Chen,Xiaonan; Li,Ping; Li,Juan; Zhao,Guoqiang

doi:10.3892/ijo.2015.3015

miR‑365 overexpression promotes cell proliferation and invasion by targeting ADAMTS-1 in breast cancer

Authors:
- Min Li
- Lulu Liu
- Wenqiao Zang
- Yuanyuan Wang
- Yuwen Du
- Xiaonan Chen
- Ping Li
- Juan Li
- Guoqiang Zhao
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Affiliations: College of Basic Medical Sciences, Zhengzhou University, Zhengzhou 450001, P.R. China, Department of Respiratory Medicine, The First Affiliated Hospital of Zhengzhou University, Zhengzhou 450052, P.R. China
Published online on: May 20, 2015 https://doi.org/10.3892/ijo.2015.3015
Pages: 296-302

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Abstract

MicroRNAs (miRNAs) have important roles in the initiation and progression of human cancer, including breast cancer. We evaluated miR‑365 expression in breast cancer tissues, and investigated its effects on cell growth, cell cycle, cell invasion, and expression of its target gene ADAMTS-1. miR‑365 expression levels were analyzed in breast cancer tissues and adjacent normal tissues using qRT-PCR. CCK-8, cell cycle, and invasion assays were used to explore the role of miR‑365 expression in breast cancer cells. We conducted luciferase reporter and western blot assays to test whether ADAMTS-1 is a direct target of miR‑365. We found that miR‑365 expression levels were significantly higher in breast cancer tissues compared with adjacent non-tumor tissues (P<0.05). These relatively high expression levels were significantly associated with advanced clinical stages (P<0.05). In breast cancer cell lines, transfection with miR‑365 inhibitor suppressed proliferation and invasion, and resulted in cell cycle arrest. Subsequent experiments indicated that miR‑365 bound the 3'-UTR of ADAMTS-1 and downregulated its expression. Our findings indicated that the inhibition of miR‑365 reduced cell proliferation and cell invasion. Additionally, miR‑365 may function as a novel oncogene in breast cancer through targeting ADAMTS-1. These findings provide insight into the mechanism of breast cancer pathogenesis.

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1	Jemal A, Bray F, Center MM, Ferlay J, Ward E and Forman D: Global cancer statistics. CA Cancer J Clin. 61:69–90. 2011. View Article : Google Scholar : PubMed/NCBI
2	Iorio MV, Ferracin M, Liu CG, Veronese A, Spizzo R, Sabbioni S, Magri E, Pedriali M, Fabbri M, Campiglio M, et al: MicroRNA gene expression deregulation in human breast cancer. Cancer Res. 65:7065–7070. 2005. View Article : Google Scholar : PubMed/NCBI
3	O’Day E and Lal A: MicroRNAs and their target gene networks in breast cancer. Breast Cancer Res. 12:2012010. View Article : Google Scholar
4	Lee RC, Feinbaum RL and Ambros V: The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell. 75:843–854. 1993. View Article : Google Scholar : PubMed/NCBI
5	Brennecke J and Cohen SM: Towards a complete description of the microRNA complement of animal genomes. Genome Biol. 4:2282003. View Article : Google Scholar : PubMed/NCBI
6	Plummer PN, Freeman R, Taft RJ, Vider J, Sax M, Umer BA, Gao D, Johns C, Mattick JS, Wilton SD, et al: MicroRNAs regulate tumor angiogenesis modulated by endothelial progenitor cells. Cancer Res. 73:341–352. 2013. View Article : Google Scholar
7	Li Q, Zhu F and Chen P: miR-7 and miR-218 epigenetically control tumor suppressor genes RASSF1A and Claudin-6 by targeting HoxB3 in breast cancer. Biochem Biophys Res Commun. 424:28–33. 2012. View Article : Google Scholar : PubMed/NCBI
8	Markou A, Yousef GM, Stathopoulos E, Georgoulias V and Lianidou E: Prognostic significance of metastasis-related microRNAs in early breast cancer patients with a long follow-up. Clin Chem. 60:197–205. 2014. View Article : Google Scholar
9	Bartel DP: MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell. 116:281–297. 2004. View Article : Google Scholar : PubMed/NCBI
10	Meister G, Landthaler M, Dorsett Y and Tuschl T: Sequence-specific inhibition of microRNA- and siRNA-induced RNA silencing. RNA. 10:544–550. 2004. View Article : Google Scholar : PubMed/NCBI
11	Krol J, Loedige I and Filipowicz W: The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet. 11:597–610. 2010.PubMed/NCBI
12	Bartel DP: MicroRNAs: Target recognition and regulatory functions. Cell. 136:215–233. 2009. View Article : Google Scholar : PubMed/NCBI
13	Fabian MR, Sonenberg N and Filipowicz W: Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem. 79:351–379. 2010. View Article : Google Scholar : PubMed/NCBI
14	Sachdeva M and Mo YY: MicroRNA-145 suppresses cell invasion and metastasis by directly targeting mucin 1. Cancer Res. 70:378–387. 2010. View Article : Google Scholar :
15	Ma L, Teruya-Feldstein J and Weinberg RA: Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature. 449:682–688. 2007. View Article : Google Scholar : PubMed/NCBI
16	Nie J, Liu L, Zheng W, Chen L, Wu X, Xu Y, Du X and Han W: microRNA-365, down-regulated in colon cancer, inhibits cell cycle progression and promotes apoptosis of colon cancer cells by probably targeting Cyclin D1 and Bcl-2. Carcinogenesis. 33:220–225. 2012. View Article : Google Scholar
17	Zhou M, Liu W, Ma S, Cao H, Peng X, Guo L, Zhou X, Zheng L, Guo L, Wan M, et al: A novel onco-miR-365 induces cutaneous squamous cell carcinoma. Carcinogenesis. 34:1653–1659. 2013. View Article : Google Scholar : PubMed/NCBI
18	Yan LX, Huang XF, Shao Q, Huang MY, Deng L, Wu QL, Zeng YX and Shao JY: MicroRNA miR-21 overexpression in human breast cancer is associated with advanced clinical stage, lymph node metastasis and patient poor prognosis. RNA. 14:2348–2360. 2008. View Article : Google Scholar : PubMed/NCBI
19	Shah NR and Chen H: MicroRNAs in pathogenesis of breast cancer: Implications in diagnosis and treatment. World J Clin Oncol. 5:48–60. 2014. View Article : Google Scholar : PubMed/NCBI
20	Blondal T, Jensby Nielsen S, Baker A, Andreasen D, Mouritzen P, Wrang Teilum M and Dahlsveen IK: Assessing sample and miRNA profile quality in serum and plasma or other biofluids. Methods. 59:S1–S6. 2013. View Article : Google Scholar
21	Jiang Q, Wang Y, Hao Y, Juan L, Teng M, Zhang X, Li M, Wang G and Liu Y: miR2Disease: A manually curated database for microRNA deregulation in human disease. Nucleic Acids Res. 37:Database. D98–D104. 2009. View Article : Google Scholar :
22	Li P, Xie XB, Chen Q, Pang GL, Luo W, Tu JC, Zheng F, Liu SM, Han L, Zhang JK, et al: MiRNA-15a mediates cell cycle arrest and potentiates apoptosis in breast cancer cells by targeting synuclein-γ. Asian Pac J Cancer Prev. 15:6949–6954. 2014. View Article : Google Scholar
23	Dobson JR, Taipaleenmäki H, Hu YJ, Hong D, van Wijnen AJ, Stein JL, Stein GS, Lian JB and Pratap J: hsa-miR-30c promotes the invasive phenotype of metastatic breast cancer cells by targeting NOV/CCN3. Cancer Cell Int. 14:732014. View Article : Google Scholar : PubMed/NCBI
24	Ahmad A, Sethi S, Chen W, Ali-Fehmi R, Mittal S and Sarkar FH: Up-regulation of microRNA-10b is associated with the development of breast cancer brain metastasis. Am J Transl Res. 6:384–390. 2014.PubMed/NCBI
25	Shen J, Hu Q, Schrauder M, Yan L, Wang D, Medico L, Guo Y, Yao S, Zhu Q, Liu B, et al: Circulating miR-148b and miR-133a as biomarkers for breast cancer detection. Oncotarget. 5:5284–5294. 2014.PubMed/NCBI
26	Ma T, Zhang J, Wu J and Tang J: Effect of miR-342-3p on chemotherapy sensitivity in triple-negative breast cancer. Zhong Nan Da Xue Xue Bao Yi Xue Ban. 39:488–495. 2014.(In Chinese). PubMed/NCBI
27	Llamazares M, Obaya AJ, Moncada-Pazos A, Heljasvaara R, Espada J, López-Otín C and Cal S: The ADAMTS12 metalloproteinase exhibits anti-tumorigenic properties through modulation of the Ras-dependent ERK signalling pathway. J Cell Sci. 120:3544–3552. 2007. View Article : Google Scholar : PubMed/NCBI
28	Porter S, Scott SD, Sassoon EM, Williams MR, Jones JL, Girling AC, Ball RY and Edwards DR: Dysregulated expression of adamalysin-thrombospondin genes in human breast carcinoma. Clin Cancer Res. 10:2429–2440. 2004. View Article : Google Scholar : PubMed/NCBI
29	Porter S, Span PN, Sweep FC, Tjan-Heijnen VC, Pennington CJ, Pedersen TX, Johnsen M, Lund LR, Rømer J and Edwards DR: ADAMTS8 and ADAMTS15 expression predicts survival in human breast carcinoma. Int J Cancer. 118:1241–1247. 2006. View Article : Google Scholar
30	Rocks N, Paulissen G, Quesada Calvo F, Polette M, Gueders M, Munaut C, Foidart JM, Noel A, Birembaut P and Cataldo D: Expression of a disintegrin and metalloprotease (ADAM and ADAMTS) enzymes in human non-small-cell lung carcinomas (NSCLC). Br J Cancer. 94:724–730. 2006.PubMed/NCBI
31	Kuno K, Terashima Y and Matsushima K: ADAMTS-1 is an active metalloproteinase associated with the extracellular matrix. J Biol Chem. 274:18821–18826. 1999. View Article : Google Scholar : PubMed/NCBI
32	Rocks N, Paulissen G, Quesada-Calvo F, Munaut C, Gonzalez ML, Gueders M, Hacha J, Gilles C, Foidart JM, Noel A, et al: ADAMTS-1 metalloproteinase promotes tumor development through the induction of a stromal reaction in vivo. Cancer Res. 68:9541–9550. 2008. View Article : Google Scholar : PubMed/NCBI
33	Masui T, Hosotani R, Tsuji S, Miyamoto Y, Yasuda S, Ida J, Nakajima S, Kawaguchi M, Kobayashi H, Koizumi M, et al: Expression of METH-1 and METH-2 in pancreatic cancer. Clin Cancer Res. 7:3437–3443. 2001.PubMed/NCBI
34	Freitas VM, do Amaral JB, Silva TA, Santos ES, Mangone FR, Pinheiro JJ, Jaeger RG, Nagai MA and Machado-Santelli GM: Decreased expression of ADAMTS-1 in human breast tumors stimulates migration and invasion. Mol Cancer. 12:22013. View Article : Google Scholar : PubMed/NCBI