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Microrna-7 Inhibits the Malignant Phenotypes of Non-Small Cell Lung

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Microrna-7 Inhibits the Malignant Phenotypes of Non-Small Cell Lung MOLECULAR MEDICINE REPORTS 12: 5443-5448, 2015 MicroRNA-7 inhibits the malignant phenotypes of non-small cell lung cancer in vitro by targeting Pax6 JIASHUN LUO1,2, HUI LI1 and CHUNFANG ZHANG2 1Institute of Medical Research, Jishou University College of Medicine, Jishou, Hunan 416000; 2Department of Cardiothoracic Surgery, Xiangya Hospital of Central South University, Changsha, Hunan 410008, P.R. China Received June 25, 2014; Accepted June 15, 2015 DOI: 10.3892/mmr.2015.4032 Abstract. MicroRNA (miR)-7 has been reported to act as a chemotherapy, the overall survival rate of patients with lung suppressor in several types of cancer, including non-small cancer remains poor, with only 14% of patients surviving cell lung cancer (NSCLC). In addition, paired box 6 (Pax6), a 5 years from the date of diagnosis (1). As non-small cell lung highly conserved transcriptional factor, has been implicated in cancer (NSCLC) is the most common type of lung cancer, NSCLC. However, the exact role of miR-7, and the association the development of effective therapeutic targets for NSCLC is between miR-7 and Pax6 in NSCLC cells remain to be fully urgently required (1). elucidated. The present study demonstrated that miR-7 was The development and progression of NSCLC are associ- downregulated and Pax6 was upregulated in NSCLC cell ated with the dysregulation of oncogenes or tumor suppressors, lines. Subsequently, it was demonstrated that overexpression of including microRNAs (miRNAs) (2). miRNAs are 18-25 nucle- miR-7 notably inhibited the protein expression of Pax6, while otide, non-coding RNAs, which can result in the inhibition of inhibition of miR-7 enhanced the protein expression of Pax6 in gene expression at the post-transcriptional level, through direct NSCLC A549 cells. Further investigation identified Pax6 as a binding to the 3'-untranslational region (UTR) of mRNAs (3). target of miR-7 in A549 NSCLC cells. Ina ddition, the overex- In addition, the dysregulation of miRNAs has been reported to pression of miR-7 significantly inhibited A549 cell proliferation be associated with the development and progression of NSCLC, and invasion, which was reversed by upregulation of Pax6. including miRNA (miR)-7 (4,5). miR-7 has been demonstrated Investigation of the underlying molecular mechanism revealed to act as a tumor suppressor in NSCLC, through targeting that the extracellular signal-regulated kinase (ERK) and p38 B-cell lymphoma (BCL)-2 and PA28γ (6,7). As one miRNA mitogen-activated protein kinase (MAPK) signaling pathways can directly bind to several target mRNAs, whether other target were downregulated in the miR-7-overexpressed A549 cells, but genes of miR-7 exist in NSCLC remains to be fully elucidate. were activated in the Pax6-overexpressed A549 cells. Based on Paired box 6 (Pax6) has been demonstrated as a highly these findings, it was suggested that miR-7 negatively regulates conserved transcription factor during embryogenesis, and is the protein level of Pax6, which can promote the proliferation involved in the development and function of the central nervous and invasion of NSCLC cells via activation of the ERK and system, endocrine glands, eyes and pancreas (8-12). The role of MAPK signaling pathways. Therefore, miR-7/Pax6 may offer Pax6 in the development and progression of cancer been gradu- potential for use as a target for the treatment of NSCLC. ally revealed (13,14). Zhao et al reported that shRNA-induced RETRACTEDPAX6 downregulation notably suppressed proliferation and Introduction cell cycle progression in NCSLC cells. They further demon- strated that the extracellular signal-regulated kinase (ERK) Lung cancer is the leading cause of cancer-associated mortality, and p38 mitogen-activated protein kinase (MAPK) signaling with an increasing incidence worldwide (1). Despite improve- pathways are involved in Pax6-mediated cell cycle progression ments in diagnostic imaging, surgery, radiotherapy and in NCSLC cells (15). The present study aimed to examine the role of miR-7 in the regulation of NSCLC in vitro. In addition, as a previous study demonstrated a target association between miR-7 and Pax6 in colon cancer (16), the present study also investigated whether Correspondence to: Professor Chunfang Zhang, Department of Cardiothoracic Surgery, Xiangya Hospital of Central South Pax6 is involved in the regulatory effect of miR-7 on NSCLC University, 87 Xiangya Road, Changsha, Hunan 410008, P.R. China cells. E-mail: [email protected] Materials and methods Key words: non small cell lung cancer, microRNA-7, paired box 6, proliferation, invasion Agents. TRIzol reagent, fetal bovine serum (FBS) Lipofectamine 2000 and the mirVana™ qRT-PCR miRNA Detection kit were purchased from Invitrogen Life 5444 LUO et al: MicroRNA-7 INHIBITS NSCLC BY TARGETING PAX6 in vitro Technologies (Carlsbad, CA, USA). Mouse anti-Pax6, -total Cybernetics, Inc., Rockville, MD, USA), and presented as the ERK, -phosphorylated (p)-ERK, -p38 MAPK and -GAPDH density ratio, vs. GAPDH. primary antibodies, and rabbit anti-mouse secondary antibody were purchased from Abcam (Cambridge, UK). Transfection. The plasmid of Pax6, scramble miRNA mimics, Bioinformatics analysis was conducted to predicate the puta- miR-7 mimics and miR-7 inhibitor were constructed by tive target genes of miR-7 using the Targetscan online software Nlunbio (Changsha, China). Lipofectamine 2000 was used (http://www.targetscan.org/). The Quick-Change Site-Directed to perform transfection, according to the manufacture's Mutagenesis kit was purchased from Stratagene (La Jolla, instruction. Briefly, the plasmid or miRNA mimics and CA, USA). The PsiCHECK™2 vector was purchased from Lipofectamine 2000 were diluted with 100 nM serum-free Promega Corporation (Madison, WI, USA). The enhanced medium, respectively. The diluted Lipofectamine 2000 was chemiluminescence (ECL) kit was purchased from Pierce added into the diluted plasmid or miRNA mimics, respectively, Biotechnology, Inc. (Rockford, IL, USA). and incubated for 20 min at room temperature, following which they were added to the cell suspension. The cells (105 cells/ml), Cell lines and cell culture. The A549, H460, SK-MES-1 and which were suspended in DMEM were then incubated at 37˚C, SPC-A1 human NSCLC cell lines, and normal BEAS-2B 5% CO2 for 6 h. Following incubation, the medium in each human lung epithelial cell line were purchased from the Cell well was replaced with normal serum-containing medium, and bank of Central South University (Changsha, China). All the cells were cultured for 24 h prior to performing the subse- cells were cultured in Dulbecco's modified Eagle's medium quent assays. The successful transfection was confirmed by (DMEM; Invitrogen Life Technologies) supplemented with detecting the expression levels of PAX6 or miR-7, respectively. 10% FBS at 37˚C with 5% CO2. Dual luciferase reporter assays. A Quick-Change Site-Directed RNA extraction and reverse transcription-quantitative poly- Mutagenesis kit was used to generate a mutant 3'-UTR of Pax6, merase chain reaction (RT-qPCR). Total RNA was extracted according to the manufacturer's instructions. The wild-type or from the cells using TRIzol reagent, according to the manu- mutant 3'-UTR of Pax6 were inserted into the psiCHECK™2 facturer's instructions. The relative expression level of miR-7 vector, respectively. A549 cells (105 cells/well), which were was determined by RT-qPCR using a mirVana™ qRT-PCR cultured to ~70% confluence, were the transfected with either miRNA Detection kit, according to the manufacturer's the psiCHECK™2-Pax6-3'-UTR or psiCHECK™2-mutant instruction. Specific primer sets for miR-7 and U6 (internal Pax6 -3'-UTR vector, with or without 100 nM miR-7 mimic, reference) were obtained from GeneCopoeia, Inc. (Maryland respectively. Following transfection for 48 h, the luciferase Rockville, MD, USA). The PCR cycling conditions were as activities were determined using an LD400 luminometer follows: 95˚C for 10 min, denaturation at 95˚C for 15 sec and an (Beckman Coulter, Fullerton, CA, USA). The activity of annealing/elongation step at 60˚C for 1 min for 40 cycles. The Renilla luciferase was normalized to that of firefly luciferase. data were analyzed with SDS relative quantification software version 2.2.2 (Applied Biosystems, Foster City, CA, USA). The Cell proliferation assay. An MTT assay was performed to 2-ΔΔCt method was used for the relative quantification of the measure cell proliferation. Cells in the exponential growth differences in expression levels of each target. were plated, at a final concentration of 2,000 cells per well, into 96-well plates. The viability of the cells were evaluated using Western blotting. The cells (107) were solubilized in cold radio- an MTT assay (20 µl MTT) 24, 48, 72 and 96 h after seeding. immunoprecipitation assay lysis buffer (Beyotime Institute of The optical density (OD) at 570 nm of each well was measured Biotechnology, Shanghai, China). The proteins (60 µg) were using an ELISA reader (ELX-800; BioTek Instruments, Inc., separated with 12% SDS-PAGE (Beijing Biolab Science and Winooski, VT, USA). Technology Co., Ltd., Beijing, China), and transferred onto a polyvinylidene difluorideRETRACTED (PVDF) membrane (Invitrogen Life Cell invasion assay. The invasive abilities of the A549 Technologies), which was then incubated with Tris-buffered cells were determined using 24-well Transwell chambers saline with Tween 20 (TBST; Fanke Biotech Co., Ltd., (Chemicon, Temecula, CA, USA), which contained a layer of Shanghai, China) containing 5% milk at room temperature for Matrigel. For each group, the cell suspension was added to the 3 h. The PVDF membrane was then incubated with primary upper chamber, and DMEM, containing 10% FBS, was added antibodies at room temperature for 3 h. The primary antibodies to the lower chamber. Following incubation for 24 h at 37˚C, were as follows: Monoclonal mouse anti-human PAX6 (1:100, the non-invading cells and the matrix gel on the interior of the cat. no.
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