miR-214 promotes the proliferation and invasion of osteosarcoma cells through direct suppression of LZTS1

https://doi.org/10.1016/j.bbrc.2014.04.140Get rights and content

Highlights

  • miR-214 is upregulated in human OS tissues and inversely correlated with LZTS1 expression.

  • miR-214 directly targets LZTS1 by binding to its 3′-UTR.

  • miR-214 promotes OS cell proliferation, invasion and tumor growth.

  • Overexpression of LZTS1 reverses miR-214-induced proliferation and invasion of OS cells.

Abstract

Previous studies have shown that miR-214 functions either as an oncogene or a tumor suppressor in various human cancer types. The role of this microRNA in osteosarcoma (OS) is presently unclear. Here, we demonstrated that miR-214 is frequently upregulated in OS specimens, compared with noncancerous bone tissues. Bioinformatics analysis further revealed leucine zipper, putative tumor suppressor 1 (LZTS1) as a potential target of miR-214. Expression patterns of miR-214 were inversely correlated with those of LZTS1 mRNA and protein in OS tissues. Data from reporter assays showed that miR-214 directly binds to the 3′-untranslated region (3′-UTR) of LZTS1 mRNA and suppresses expression at both transcriptional and translational levels. In functional assays, miR-214 promoted OS cell proliferation, invasion and tumor growth in nude mice, which could be reversed by overexpression of LZTS1. Taken together, our data provide compelling evidence that miR-214 functions as an onco-miRNA in OS, and its oncogenic effects are mediated chiefly through downregulation of LZTS1.

Introduction

Osteosarcoma (OS) is the most common primary sarcoma of bone in adolescents and young adults [1]. The incidence of OS in the general population is three cases per million per year, with peak occurrence in the 15–19-year age group, in which 8–11 cases/million/year are recorded [2]. Despite extensive advancements in diagnostic methods and surgical techniques in recent years, the 5-year survival rate of osteosarcoma patients remains at 60–70% [3]. Thus, improved understanding of the mechanisms underlying osteosarcoma development and progression is urgently required to optimize therapeutic options.

MicroRNAs (miRNAs) are an emerging class of small, non-coding, single-stranded RNAs that serve as important regulators of gene expression by binding to the 3′ untranslated region (UTR) of target mRNAs, thereby leading to their translational repression and/or degradation [4], [5]. miRNAs regulate a variety of biological processes, including cell proliferation, differentiation, migration, metabolism and apoptosis [6]. In cancers, homeostatic expression of miRNAs is disrupted, resulting in aberrant gene expression in tumor initiation, development and metastasis. Multiple miRNAs have been implicated in carcinogenesis and tumor progression in OS. For example, miR-143 is reported to function as a tumor suppressor by downregulating Bcl-2 and MMP-13 [7], [8]. miR-199b-5p, miR-183, miR-34a, miR-340 and miR-16 exert tumor suppressor effects in osteosarcomagenesis through suppression of the Notch pathway [9], the oncogenes Ezrin [10], c-Met [11], ROCK1 [12], and Raf1-MEK1/2-ERK1/2 signaling [13] in OS cells, respectively. A recent miRNA microarray analysis by Jones et al. [1] revealed higher miR-214 expression in OS tissues, compared with normal bone tissues. However, the precise role of miR-214 in OS cells remains unclear at present.

In this study, we demonstrated that miR-214 is upregulated in OS and inversely correlated with LZTS1 levels. Our collective findings suggest that miR-214 directly targets 3′-UTR of the LZTS1 transcript and suppresses its expression, eventually promoting OS cell proliferation, invasion and tumor growth in nude mice.

Section snippets

Clinical specimens

Eight OS tissues and adjacent normal bone tissues were obtained from OS patients at Shanghai Jiao Tong University Affiliated Sixth People’s Hospital (Shanghai, China). The study was approved by the ethics committee of Shanghai Municipality. Written informed consent was obtained from all patients.

Cell culture

Human OS cell lines, Saos-2 and U2OS, were obtained from Cell Bank of Institute of Biochemistry and Cell Biology, Shanghai Institutes for Biological Sciences. Cells were maintained in RPMI 1640

miR-214 is upregulated in human OS tissues and inversely correlated with LZTS1 expression

To explore the potential role of miR-214 in OS development, its expression was evaluated in eight pairs of human OS and adjacent normal bone tissues using qRT-PCR. As shown in Fig. 1A, miR-214 expression was significantly higher in tumors than normal bone tissues. Potential targets of miR-214 were predicted using bioinformatics methods. LZTS1, a tumor suppressor gene containing a binding site for miR-214, was selected as the target for further analysis (Fig. 1B). qRT-PCR analysis of the above

Discussion

Emerging data have shown that miR-214 is downregulated and functions as a potential tumor suppressor in several human cancer types, including cervical cancer, intrahepatic cholangiocarcinoma, hepatoma and colorectal cancer [16], [17], [18], [19]. Conversely, miR-214 is upregulated, and displays oncogenic properties in ovarian cancer, nasopharyngeal carcinoma and gastric cancer [20], [21], [22]. These dual effects of miR-214 may be attributable to organ-specific actions and different cellular

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