MicroRNA‑574‑3p inhibits the malignant behavior of liver cancer cells by targeting ADAM28

Retraction in: /10.3892/ol.2023.13973

  • Authors:
    • Zhongming Zha
    • Fuxin Jia
    • Pingan Hu
    • Erhui Mai
    • Ting Lei
  • View Affiliations

  • Published online on: July 10, 2020     https://doi.org/10.3892/ol.2020.11852
  • Pages: 3015-3023
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Abstract

Liver cancer is one of the most common and aggressive tumors, and usually leads to a poor clinical outcome. Increasing evidence has demonstrated the important functions of microRNAs (miRs) in tumor progression. miR‑574‑3p has been reported as a tumor suppressor and potential therapeutic target in various types of cancer. However, the underlying mechanism of the effects of miR‑574‑3p in liver cancer remains unknown. In the present study, reverse transcription‑quantitative PCR was performed to detect miR‑574‑3p expression in liver cancer tissues, and the influence of miR‑574‑3p on cell growth was evaluated using the Cell Counting Kit‑8 assay, and cell migration and flow cytometry analyses. The present study revealed that miR‑574‑3p expression was downregulated in liver cancer tissues and cell lines. miR‑574‑3p overexpression, achieved by transfecting miR‑574‑3p mimics into liver cancer cells, reduced cell proliferation and migration, and promoted cell apoptosis. Mechanistically, ADAM metallopeptidase domain 28 (ADAM28) was identified as a miR‑574‑3p target via binding to the 3'‑untranslated region of the ADAM28 mRNA. Gain‑of‑function of miR‑574‑3p downregulated the expression levels of ADAM28 in liver cancer cells. Additionally, overexpression of ADAM28 significantly attenuated the suppressive effect of miR‑574‑3p on the growth of liver cancer cells. The present results provide novel insights into the function of the miR‑574‑3p/ADAM28 signaling pathway in liver cancer.

Introduction

Liver cancer is one of the most common malignancies and has been a leading cause of cancer-associated mortality worldwide (1,2). Currently, surgical resection combined with chemotherapy, radiotherapy, liver implant and intervention remains the major therapeutic strategy for patients with liver cancer (3). Although notable progress has been made in the diagnosis and treatment of this disease, the outcome of patients with liver cancer remains poor due to metastasis and recurrence (4,5). Therefore, the identification of novel factors involved in the development of liver cancer is required to improve the prognosis of patients with this disease.

MicroRNAs (miRNAs/miRs) are a class of non-coding single-stranded RNAs consisting of 19–25 nucleotides that negatively regulate gene expression (68). miRNAs bind the 3′-untranslated region (UTR) of target mRNAs, leading to translation inhibition or mRNA degradation (9). Bioinformatics analysis has indicated that the expression of up to 30% of human genes is regulated by miRNAs, which is consistent with the increasing involvement of miRNAs in a wide range of biological processes, such as cell proliferation, differentiation and apoptosis (10). Notably, accumulating evidence has demonstrated the key roles of miRNAs in the progression of liver cancer by acting as tumor suppressors or oncogenes (11). For example, miR-548b suppresses the proliferation and invasion of liver cancer cells by targeting specificity protein 1 (12). Previous studies have revealed that miR-574-3p acts as a tumor suppressor in numerous types of cancer (1317), such as esophageal squamous cell carcinoma (ESCC), in which miR-574-3p is downregulated and may be a predictor of the postoperative outcome of patients with ESCC (13). Next generation sequencing data has indicated that miR-574-3p is a promising prognostic marker for patients with breast cancer (17). Additionally, miR-574-3p expression is downregulated in prostate cancer tissues and inhibits tumorigenesis (14). Previous studies have revealed that the dysregulation of serum miR-574-3p in patients with liver cancer serves as an important biomarker for the diagnosis of liver cancer (18,19). However, to the best of our knowledge, the function of miR-574-3p in liver cancer has not been fully explored.

The ADAM metallopeptidases (ADAMs) are characterized by sequence similarity to the reprolysin family of snake venom endopeptidases, which share the metalloproteinase domain with matrix metalloproteinases (20). Increasing evidence has demonstrated that ADAM proteins serve important roles in multiple biological processes, such as cell proliferation, migration and adhesion (21). The critical function of ADAMs in human diseases, particularly cancer, has been illustrated by a previous study (22). ADAM domain 28 (ADAM28) is a member of the ADAMs family that is overexpressed in numerous types of cancer, including breast cancer, lung cancer and acute myeloid leukemia (2325). Mechanistically, ADAM28 promotes tumorigenesis by cleaving molecules involved in cancer metastasis, such as connective tissue growth factor, insulin-like growth factor binding protein-3 and von Willebrand's factor (26). However, the involvement of ADAM28 in liver cancer has not been fully established.

In the present study, miR-574-3p expression in liver cancer tissues and cell lines was analyzed to reveal the role of miR-574-3p in the progression of liver cancer. Additionally, the effects of miR-574-3p on the growth of liver cancer cells and its potential downstream targets were explored.

Materials and methods

Clinical samples

Liver cancer tissues and paired adjacent normal tissues (~5 cm from the margin of the tumor tissues) were collected by surgical resection from 50 patients diagnosed at Luoyang Central Hospital Affiliated to Zhengzhou University (Luoyang, China) between May 2013 and October 2014. Patients who received radiotherapy or chemotherapy before surgery were excluded. Tissues were frozen in liquid nitrogen prior to the experiments. The pathological characteristics of patients with liver cancer enrolled in the present study are provided in Table SI. The present study was approved by the Ethics Committee of Luoyang Central Hospital Affiliated to Zhengzhou University and performed according to the Declaration of Helsinki. Written informed consent was obtained from all participants enrolled in the present study.

Cell culture and transfection

Liver cancer cell lines, including HepG2, Huh7 and Hep3B were obtained from The Cell Bank of Type Culture Collection of the Chinese Academy of Sciences. The immortalized normal liver THLE-3 epithelial cell line was purchased from the American Type Culture Collection. Cells were cultured in DMEM supplemented with 10% FBS (both Gibco; Thermo Fisher Scientific, Inc.), 100 µg/ml streptomycin and 100 U/ml penicillin (Sigma-Aldrich; Merck KGaA). Cells were cultured at 37°C with 5% CO2.

The miR-574-3p mimics (5′-CACGCUCAUGCACACACCCACA-3′) and negative control miRNA (5′-GUUCGUACGUACACUGUUCA-3′) were purchased from Guangzhou RiboBio Co., Ltd. The ADAM28 expression plasmid was constructed by inserting the full cDNA sequence of ADAM28 into the backbone of a pcDNA 3.1+ vector (Addgene, Inc.). When the cell confluence reached 70–80%, miRNAs (50 nM) or pcDNA-ADAM28 (0.5 µg) were transfected into cells using Lipofectamine® 2000 (Invitrogen; Thermo Fisher Scientific, Inc.) according to the manufacturer's protocol. Cells were harvested after 48 h of transfection for further analysis.

RNA extraction and reverse transcription-quantitative PCR (RT-qPCR)

Total RNA was extracted from tissues or cells using the TRIzol® reagent at room temperature (Invitrogen; Thermo Fisher Scientific, Inc.) according to the manufacturer's protocol. RT was performed using the Revert Aid First Strand cDNA synthesis kit (Thermo Fisher Scientific, Inc.) with a temperature protocol of 25°C for 5 min, followed by 42°C for 60 min and 70°C for 5 min. RT-qPCR was performed with the All-in-One™ miRNA qRT-PCR detection kit (GeneCopoeia, Inc.) to detect the levels of miR-574-3p. The expression levels of ADAM28 were quantified using the SYBR Premix Ex Taq II (Takara Biotechnology Co., Ltd.). The thermocycling conditions were: 95°C for 1 min, followed by 40 cycles at 95°C for 10 sec, 58°C for 30 sec and 72°C for 30 sec. miR-574-3p expression was normalized to U6 RNA, while ADAM28 expression was normalized to GAPDH. The primers used in the present study were: miR-574-3p forward, 5′-ATCGGAAGTTGAGTGAGCCGCGTC-3′ and reverse, 5′-GCCGTGAGTCAGGAGTGGT-3′; U6 forward, 5′-GCTTCGGCAGCACATATACTAAAAT-3′ and reverse, 5′-CGCTTCAGAATTTGCGTGTCAT-3′; ADAM28 forward, 5′-GTAAAAGAGAGACCCAAGAGCCAG-3′ and reverse, 5′-GTAGTCCTTGACAGGTGCTGATG-3′; GAPDH forward, 5′-CACCTGCGCTGTGTGGACT-3′ and reverse, 5′-GGATGGCTGATGTGTCGGGTGG-3′. The relative expression levels of miR-574-3p were determined using the 2−ΔΔCq method (27). The ratio (R=RQCancer/RQNormal; RQ, relative quantification) between the relative expression levels of miR-574-3p and ADAM28 in liver cancer and adjacent normal tissues was calculated. Expression was considered to be downregulated when R<0.7 and upregulated when R>1.3 (28).

Luciferase reporter assay

The wild-type (WT) or mutant (Mut) 3′-UTR sequences of ADAM28 containing the potential seeding region of miR-574-3p were inserted into the pmirGLO vector (Promega Corporation). Cells (5,000 cells/well) were seeded into a 96-well plate and co-transfected with pmirGLO-UTR-WT or pmirGLO-UTR-Mut with miR-574-3p mimics or control miRNA using Lipofectamine® 2000 (Invitrogen; Thermo Fisher Scientific, Inc.). Following 48 h of transfection, cells were harvested and the luciferase activity was detected using a Dual-luciferase Reporter assay kit (Promega Corporation) with an iMark Fluorometer Microplate Reader (Bio-Rad Laboratories, Inc.). Renilla luciferase activity was detected for normalization. The assay was performed with three independent repeats.

Cell Counting Kit-8 (CCK-8) assay

A total of 2×103 cells/well expressing miR-574-3p mimics or control miRNA were seeded into a 96-well plate. Cell proliferation was evaluated after 1, 2, 3, 4 and 5 days using the CCK-8 assay (Dojindo Molecular Technologies, Inc.) according to the manufacturer's protocol. Briefly, 10 µl CCK-8 solution was added to the medium and incubated at 37°C for 3 h. The absorbance of each well was measured at 450 nm using the EnSpire 2300 Multilabel Reader (PerkinElmer, Inc.).

Target prediction

The potential targets of miR-574-3p were predicted using miRDB (http://mirdb.org/; version 6.0) and TargetScan (http://www.targetscan.org/vert_72/; release no. 7.2) by inputting the name of the miRNA as ‘miR-574-3p’.

Western blotting

Proteins were extracted from cells using RIPA buffer containing protease inhibitor (Beyotime Institute of Biotechnology). The protein concentration was determined using a bicinchoninic acid protein assay kit (Beyotime Institute of Biotechnology). An equal amount of protein (20 µg/lane) was separated by 15% SDS-PAGE and transferred onto PVDF membranes (EMD Millipore). The membranes were blocked with 5% skimmed milk in TBS buffer at room temperature for 1 h, followed by incubation with ADAM28 (cat. no. sc-393877; Santa Cruz Biotechnology, Inc.) and GAPDH (cat. no. ab9485; Abcam) primary antibodies (both 1:1,000 dilution) overnight at 4°C. After three washes with TBS-Tween-20 (0.1%), the membranes were incubated with goat anti-mouse (cat. no. 170-6516) or goat anti-rabbit (cat. no. 170-6515) IgG (H+L)-horseradish peroxidase-conjugated secondary antibodies (both 1:5,000 dilution; Bio-Rad Laboratories, Inc.) for 2 h at room temperature. The bands were visualized using the Enhanced Chemiluminescence Detection reagent (Pierce; Thermo Fisher Scientific, Inc.).

Cell migration

The migration of liver cancer cells was determined using Transwell chambers (8-µm pore size; Corning Inc.) following the manufacturer's protocol. A total of 5×104 cells transfected with miR-574-3p mimics or miR-NC were seeded into the upper chamber containing 200 µl medium without serum. Medium supplemented with 10% FBS was added into the lower chamber and served as the chemoattractant. After incubation for 24 h at 37°C, cells in the upper chamber were removed using a cell scraper and those attached to the lower surface of the membrane were fixed with 4% paraformaldehyde at room temperature for 10 min. Subsequently cells were stained with 0.1% crystal violet (Beyotime Institute of Biotechnology) for 15 min at room temperature and counted using an inverted light microscope (magnification, ×100).

Cell apoptosis

Apoptosis of liver cancer cells was determined using the FITC Annexin V Apoptosis Detection kit (Beijing 4A Biotech Co., Ltd.) according to the manufacturer's protocol. Briefly, 1×106 cells/well were transfected with miR-574-3p mimics or control miRNA, collected after 48 h of transfection and washed twice with PBS. Cells were resuspended with binding buffer and stained with Annexin V-FITC for 15 min at room temperature in the dark. Subsequently, cells were incubated with propidium iodide for 5 min at room temperature. Apoptosis was analyzed using a FACScan flow cytometer (BD Biosciences) and the data (both early and late apoptosis) were analyzed using the Cellquest software v10.6.4 (BD Biosciences).

Statistical analysis

Data are presented as the mean ± SD from three independent experiments. Statistical analysis was performed using SPSS v16.0 (SPSS, Inc.). Paired Student's t-test was used to determine the significance between adjacent and cancer tissues. Unpaired Student's t-test was used for analyzing differences between miRNAs and miR mimics, and between pcDNA-vector and pcDNA-ADAM28 groups. One-way ANOVA followed by Tukey's post hoc test was used for the statistical analysis of differences among multiple groups. The correlation between the expression levels of miR-574-3p and ADAM28 was analyzed using Spearman's correlation test. P<0.05 was considered to indicate a statistically significant difference.

Results

miR-574-3p expression is downregulated in liver cancer

To investigate miR-574-3p expression in liver cancer, the expression levels of miR-574-3p in 50 paired cancer and adjacent normal tissues were detected via RT-qPCR. The data indicated that miR-574-3p expression was significantly downregulated in cancer tissues compared with in non-tumor tissues (Fig. 1A). Accordingly, miR-574-3p expression was downregulated in the liver cancer HepG2, Huh7 and Hep3B cell lines compared with in the immortalized normal liver THLE-3 cell line (Fig. 1B). The present data indicate that miR-574-3p expression is downregulated in liver cancer.

Overexpression of miR-574-3p inhibits the proliferation of liver cancer cells

To characterize the effect of miR-574-3p in liver cancer, miR-574-3p was overexpressed by transfecting miR-574-3p mimics into HepG2 and Huh7 cells. The transfection efficiency was analyzed using an RT-qPCR assay (Fig. 2A). The effects of miR-574-3p on the proliferation of cancer cells were determined using the CCK-8 assay. As indicated in Fig. 2B and C, miR-574-3p overexpression significantly suppressed the proliferation of both HepG2 and Huh7 cells after 4 and 5 days. Additionally, the suppressive effect of miR-574-3p in liver cancer was investigated by evaluating the impact of miR-574-3p on cell migration. The present results revealed that transfection of miR-574-3p inhibited the migratory capacity of HepG2 and Huh7 cells (Fig. 2D). Additionally, the flow cytometry analysis indicated that transfection with miR-574-3p mimics significantly increased apoptosis of both HepG2 and Huh7 cells (Fig. 2E). The present results suggest that miR-574-3p overexpression inhibits the malignant abilities of liver cancer cells, indicating a suppressive role of miR-574-3p in the tumorigenesis of liver cancer.

ADAM28 is a target of miR-574-3p in liver cancer

To further understand the functional mechanism of miR-574-3p in liver cancer, potential targets of miR-574-3p were predicted. The bioinformatics analysis suggested that ADAM28 was a putative target of miR-574-3p. The potential binding site of miR-574-3p at the 3′-UTR of ADAM28 is presented in Fig. 3A. To validate the binding between miR-574-3p and the 3′-UTR of ADAM28, a luciferase reporter assay was performed by co-transfecting luciferase vectors expressing a WT or Mut 3′-UTR of ADAM28, and a miR-574-3p mimic. miR-574-3p overexpression significantly decreased the luciferase activity of cells carrying the WT but not the Mut 3′-UTR of ADAM28 (Fig. 3B and C). To illustrate whether the binding of miR-574-3p affected the stability of ADAM28 mRNA, RT-qPCR was performed in liver cancer cells expressing the miR-574-3p mimic or the control miRNA. The results revealed that miR-574-3p overexpression significantly decreased the mRNA expression levels of ADAM28 in both HepG2 and Huh7 cells (Fig. 3D). Similarly, the protein expression levels of ADAM28 were decreased by miR-574-3p transfection (Fig. 3E). The present results suggest that ADAM28 is a target of miR-574-3p and that it is negatively regulated by miR-574-3p in liver cancer.

miR-574-3p expression is inversely correlated with ADAM28 expression in liver cancer

Since miR-574-3p negatively regulated ADAM28 expression in liver cancer cells, the abundance of ADAM28 in liver cancer tissues was evaluated by RT-qPCR. As indicated in Fig. 4A, ADAM28 expression was significantly upregulated in cancer tissues compared with in matched adjacent normal tissues. The correlation between miR-574-3p and ADAM28 expression was analyzed by Spearman's correlation test. The data revealed that the expression levels of miR-574-3p were inversely correlated with those of ADAM28 in cancer tissues (Fig. 4B). Additionally, the mRNA expression levels of ADAM28 in liver cancer cell lines were detected by RT-qPCR. The results revealed that ADAM28 expression was significantly upregulated in liver cancer cells compared with in the immortalized normal liver THLE-3 cell line (Fig. 4C). The present findings suggest that ADAM28 expression is upregulated in liver cancer.

Recovered ADAM28 expression reverses the inhibitory effect of miR-574-3p in liver cancer cells

To confirm the involvement of ADAM28 in the anticancer activity of miR-574-3p in liver cancer cells, HepG2 and Huh7 cells were transfected with the pcDNA-ADAM28 plasmid. ADAM28 overexpression was analyzed by RT-qPCR and western blot analysis, respectively (Fig. 5A and B). Functional analysis revealed that overexpression of ADAM28 significantly attenuated the inhibitory effect of miR-574-3p on the proliferation of liver cancer cells after 5 days (Fig. 5C and D). The present results suggest that the tumor suppressive role of miR-574-3p in liver cancer is partially mediated by ADAM28 downregulation.

Discussion

Increasing evidence has demonstrated that miRNAs are abnormally expressed in liver cancer and regulate cancer progression (29,30). Therefore, understanding the mechanisms of miRNAs in liver cancer may provide novel targets for the treatment of this disease, and may improve the outcome of patients with liver cancer. In the present study, the expression levels and the functional mechanism of miR-574-3p in liver cancer were investigated. miR-574-3p downregulation was observed in liver cancer tissues and cell lines, highlighting the potential clinical significance of miR-574-3p in liver cancer.

The tumor suppressive function of miR-574-3p has been reported in several types of cancer, such as ovarian and gastric cancer, and osteosarcoma (13,15,18,3133). A recent study revealed that miR-574-3p inhibits the metastasis and chemoresistance of epithelial ovarian cancer (32). Circulating miR-574-3p in the plasma has been proposed as a promising biomarker for the prognosis and therapy monitoring of patients with head and neck squamous cell cancer (34). miR-574-3p overexpression induces cell cycle arrest in response to X-ray irradiation by targeting the production of the enhancer of rudimentary homolog protein (35). In the present study, miR-574-3p was markedly downregulated in liver cancer tissues and cell lines. Further studies are required to explore the underlying mechanisms that contribute to decreased miR-574-3p expression in liver cancer. Additionally, to strengthen the potential clinical significance of miR-574-3p in liver cancer, the association between miR-574-3p expression and the prognosis of patients with liver cancer should be investigated using a larger sample size. In the present study, miR-574-3p transfection inhibited cell proliferation and migration, and induced apoptosis of liver cancer cells, suggesting a tumor suppressive role of miR-574-3p in liver cancer. However, experiments with loss-of-function of miR-574-3p and in vivo assays in mice are required to fully characterize the inhibitory effects of miR-574-3p on the development of liver cancer. Interestingly, some miRNAs, such as miR-23b-3p, can promote or inhibit tumor progression in different types of cancer depending on the alternation of downstream targets (36). miR-574-3p exerts tumor-promoting effects in osteosarcoma (OS), and miR-574-3p overexpression promotes the growth of OS cells by targeting SMAD family member 4 (31). A recent study revealed that serum miR-574-3p expression in patients with liver cancer is higher than that in patients with cirrhosis or in healthy controls (18), suggesting an oncogenic function of miR-574-3p in cancer. It is possible that miR-574-3p serves promoting or inhibitory roles in liver cancer depending on the targeted proteins. It would be useful to investigate the expression levels and functions of miR-574-3p in other types of cancer to confirm the suppressive or oncogenic role of miR-574-3p in cancer.

Based on the involvement of ADAMs in cancer, ADAMs can be regulated by miRNAs to modulate the progression of tumorigenesis (3745). A previous study revealed that miR-552 targets ADAM28 in colorectal cancer and enhances the metastasis of cancer cells (26). Additionally, ADAM28 is negatively regulated by miR-198 in colorectal cancer and inhibits cancer cell proliferation (42). In the present study, miR-574-3p bound the 3′-UTR of ADAM28 and reduced ADAM28 expression in liver cancer cells, suggesting that miR-574-3p targets ADAM28 and negatively regulates its expression. Consistently, the expression levels of ADAM28 were inversely correlated with those of miR-574-3p in liver cancer tissues. Overexpression of ADAM28 attenuated the inhibitory effect of miR-574-3p on the proliferation of liver cancer cells. To further validate that miR-574-3p suppresses the growth of liver cancer cells by targeting ADAM28, it would be useful to perform rescue assays by transfecting with 3′-UTR-mutated ADAM28 to investigate its effects on miR-574-3p-mediated proliferation of liver cancer cells.

In conclusion, the present study revealed that miR-574-3p expression was downregulated in liver cancer tissues. Overexpression of miR-574-3p inhibited the malignant phenotype of liver cancer cells by targeting ADAM28. The present results shed light on the critical involvement of the miR-574-3p/ADAM28 signaling pathway in liver cancer. Further studies should explore the therapeutic potential of miR-574-3p and identify other genome-wide targets in addition to ADAM28.

Supplementary Material

Supporting Data

Acknowledgements

Not applicable.

Funding

No funding was received.

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Authors' contributions

ZZ and TL designed the study. ZZ performed most of the experiments and analyzed the data. FJ, PH and EM contributed to performing the experiments, and analyzed and interpreted the data. ZZ and TL wrote the manuscript. All authors read and approved the final manuscript.

Ethics approval and consent to participate

The present study was approved by the Ethics Committee of Luoyang Central Hospital Affiliated to Zhengzhou University (Luoyang, China). Written informed consent was provided by all patients.

Patient consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

References

1 

Di Sandro S, Danieli M, Ferla F, Lauterio A, Carlis RD, Benuzzi L, Buscemi V, Pezzoli I and Carlis LD: The current role of laparoscopic resection for HCC: A systematic review of past ten years. Transl Gastroenterol Hepatol. 3:682018. View Article : Google Scholar : PubMed/NCBI

2 

Aghemo A: Update on HCC management and review of the new EASL guidelines. Gastroenterol Hepatol (N Y). 14:384–386. 2018.PubMed/NCBI

3 

Bolondi L, Piscaglia F, Camaggi V, Grazi GL and Cavallari A: Review article: Liver transplantation for HCC. Treatment options on the waiting list. Aliment Pharmacol Ther. 17 (Suppl 2):S145–S150. 2003. View Article : Google Scholar

4 

Liu CY, Chen KF and Chen PJ: Treatment of liver cancer. Cold Spring Harb Perspect Med. 5:a0215352015. View Article : Google Scholar : PubMed/NCBI

5 

Marengo A, Rosso C and Bugianesi E: Liver cancer: Connections with obesity, fatty liver, and cirrhosis. Annu Rev Med. 67:103–117. 2016. View Article : Google Scholar : PubMed/NCBI

6 

Ambros V: The functions of animal microRNAs. Nature. 431:350–355. 2004. View Article : Google Scholar : PubMed/NCBI

7 

Bartel DP: MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell. 116:281–297. 2004. View Article : Google Scholar : PubMed/NCBI

8 

Mohr AM and Mott JL: Overview of microRNA biology. Semin Liver Dis. 35:3–11. 2015. View Article : Google Scholar : PubMed/NCBI

9 

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

10 

Gentilin E, Degli Uberti E and Zatelli MC: Strategies to use microRNAs as therapeutic targets. Best Pract Res Clin Endocrinol Metab. 30:629–639. 2016. View Article : Google Scholar : PubMed/NCBI

11 

Mizuguchi Y, Takizawa T, Yoshida H and Uchida E: Dysregulated miRNA in progression of hepatocellular carcinoma: A systematic review. Hepatol Res. 46:391–406. 2016. View Article : Google Scholar : PubMed/NCBI

12 

Qiu H, Zhang G, Song B and Jia J: MicroRNA-548b inhibits proliferation and invasion of hepatocellular carcinoma cells by directly targeting specificity protein 1. Exp Ther Med. 18:2332–2340. 2019.PubMed/NCBI

13 

Okumura T, Kojima H, Miwa T, Sekine S, Hashimoto I, Hojo S, Nagata T and Shimada Y: The expression of microRNA 574-3p as a predictor of postoperative outcome in patients with esophageal squamous cell carcinoma. World J Surg Oncol. 14:2282016. View Article : Google Scholar : PubMed/NCBI

14 

Chiyomaru T, Yamamura S, Fukuhara S, Hidaka H, Majid S, Saini S, Arora S, Deng G, Shahryari V, Chang I, et al: Genistein up-regulates tumor suppressor microRNA-574-3p in prostate cancer. PLoS One. 8:e589292013. View Article : Google Scholar : PubMed/NCBI

15 

Wang M, Zhang R, Zhang S, Xu R and Yang Q: MicroRNA-574-3p regulates epithelial mesenchymal transition and cisplatin resistance via targeting ZEB1 in human gastric carcinoma cells. Gene. 700:110–119. 2019. View Article : Google Scholar : PubMed/NCBI

16 

Ujihira T, Ikeda K, Suzuki T, Yamaga R, Sato W, Horie-Inoue K, Shigekawa T, Osaki A, Saeki T, Okamoto K, et al: MicroRNA-574-3p, identified by microRNA library-based functional screening, modulates tamoxifen response in breast cancer. Sci Rep. 5:76412015. View Article : Google Scholar : PubMed/NCBI

17 

Krishnan P, Ghosh S, Wang B, Li D, Narasimhan A, Berendt R, Graham K, Mackey JR, Kovalchuk O and Damaraju S: Next generation sequencing profiling identifies miR-574-3p and miR-660-5p as potential novel prognostic markers for breast cancer. BMC Genomics. 16:7352015. View Article : Google Scholar : PubMed/NCBI

18 

Shen X, Xue Y, Cong H, Wang X and Ju S: Dysregulation of serum microRNA-574-3p and its clinical significance in hepatocellular carcinoma. Ann Clin Biochem. 55:478–484. 2018. View Article : Google Scholar : PubMed/NCBI

19 

Gui J, Tian Y, Wen X, Zhang W, Zhang P, Gao J, Run W, Tian L, Jia X and Gao Y: Serum microRNA characterization identifies miR-885-5p as a potential marker for detecting liver pathologies. Clin Sci (Lond). 120:183–193. 2011. View Article : Google Scholar : PubMed/NCBI

20 

Tortorella MD, Malfait F, Barve RA, Shieh HS and Malfait AM: A review of the ADAMTS family, pharmaceutical targets of the future. Curr Pharm Des. 15:2359–2374. 2009. View Article : Google Scholar : PubMed/NCBI

21 

Reiss K and Saftig P: The ‘a disintegrin and metalloprotease’ (ADAM) family of sheddases: Physiological and cellular functions. Semin Cell Dev Biol. 20:126–137. 2009. View Article : Google Scholar : PubMed/NCBI

22 

Duffy MJ, McKiernan E, O'Donovan N and McGowan PM: Role of ADAMs in cancer formation and progression. Clin Cancer Res. 15:1140–1144. 2009. View Article : Google Scholar : PubMed/NCBI

23 

Mitsui Y, Mochizuki S, Kodama T, Shimoda M, Ohtsuka T, Shiomi T, Chijiiwa M, Ikeda T, Kitajima M and Okada Y: ADAM28 is overexpressed in human breast carcinomas: Implications for carcinoma cell proliferation through cleavage of insulin-like growth factor binding protein-3. Cancer Res. 66:9913–9920. 2006. View Article : Google Scholar : PubMed/NCBI

24 

Mochizuki S, Shimoda M, Abe H, Miyamae Y, Kuramoto J, Aramaki-Hattori N, Ishii K, Ueno H, Miyakoshi A, Kojoh K and Okada Y: Selective inhibition of ADAM28 suppresses lung carcinoma cell growth and metastasis. Mol Cancer Ther. 17:2427–2438. 2018. View Article : Google Scholar : PubMed/NCBI

25 

Zhang JM, Wang CC, Zhang GC, Jiang Q, Yang SM, Fu HX, Wang QM, Zhu XL, Zhu HH, Jiang H, et al: ADAM28 promotes tumor growth and dissemination of acute myeloid leukemia through IGFBP-3 degradation and IGF-I-induced cell proliferation. Cancer Lett. 442:193–201. 2019. View Article : Google Scholar : PubMed/NCBI

26 

Wang J, Li H, Wang Y, Wang L, Yan X, Zhang D, Ma X, Du Y, Liu X and Yang Y: MicroRNA-552 enhances metastatic capacity of colorectal cancer cells by targeting a disintegrin and metalloprotease 28. Oncotarget. 7:70194–70210. 2016. View Article : Google Scholar : PubMed/NCBI

27 

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

28 

Grossi I, Arici B, Portolani N, De Petro G and Salvi A: Clinical and biological significance of miR-23b and miR-193a in human hepatocellular carcinoma. Oncotarget. 8:6955–6969. 2017. View Article : Google Scholar : PubMed/NCBI

29 

Huang X and Jia Z: Construction of HCC-targeting artificial miRNAs using natural miRNA precursors. Exp Ther Med. 6:209–215. 2013. View Article : Google Scholar : PubMed/NCBI

30 

Lou W, Liu J, Ding B, Chen D, Xu L, Ding J, Jiang D, Zhou L, Zheng S and Fan W: Identification of potential miRNA-mRNA regulatory network contributing to pathogenesis of HBV-related HCC. J Transl Med. 17:72019. View Article : Google Scholar : PubMed/NCBI

31 

Xu H, Liu X, Zhou J, Chen X and Zhao J: miR-574-3p acts as a tumor promoter in osteosarcoma by targeting SMAD4 signaling pathway. Oncol Lett. 12:5247–5253. 2016. View Article : Google Scholar : PubMed/NCBI

32 

Zheng J, Zhou Y, Li XJ and Hu JM: miR-574-3p exerts as a tumor suppressor in ovarian cancer through inhibiting MMP3 expression. Eur Rev Med Pharmacol Sci. 23:6839–6848. 2019.PubMed/NCBI

33 

Zhang P, Zhu J, Zheng Y, Zhang H, Sun H and Gao S: miRNA-574-3p inhibits metastasis and chemoresistance of epithelial ovarian cancer (EOC) by negatively regulating epidermal growth factor receptor (EGFR). Am J Transl Res. 11:4151–4165. 2019.PubMed/NCBI

34 

Summerer I, Unger K, Braselmann H, Schuettrumpf L, Maihoefer C, Baumeister P, Kirchner T, Niyazi M, Sage E, Specht HM, et al: Circulating microRNAs as prognostic therapy biomarkers in head and neck cancer patients. Br J Cancer. 113:76–82. 2015. View Article : Google Scholar : PubMed/NCBI

35 

Ishikawa K, Ishikawa A, Shoji Y and Imai T: A genotoxic stress-responsive miRNA, miR-574-3p, delays cell growth by suppressing the enhancer of rudimentary homolog gene in vitro. Int J Mol Sci. 15:2971–2990. 2014. View Article : Google Scholar : PubMed/NCBI

36 

Grossi I, Salvi A, Baiocchi G, Portolani N and De Petro G: Functional role of microRNA-23b-3p in cancer biology. Microrna. 7:156–166. 2018. View Article : Google Scholar : PubMed/NCBI

37 

Li H, Guo X, Li Q, Ran P, Xiang X, Yuan Y, Dong T, Zhu B, Wang L, Li F, et al: Long non-coding RNA 1308 promotes cell invasion by regulating the miR-124/ADAM 15 axis in non-small-cell lung cancer cells. Cancer Manag Res. 10:6599–6609. 2018. View Article : Google Scholar : PubMed/NCBI

38 

Yang X, Cui Y, Yang F, Sun C and Gao X: MicroRNA302a suppresses cell proliferation, migration and invasion in osteosarcoma by targeting ADAM9. Mol Med Rep. 16:3565–3572. 2017. View Article : Google Scholar : PubMed/NCBI

39 

Ji T, Zhang X and Li W: MicroRNA543 inhibits proliferation, invasion and induces apoptosis of glioblastoma cells by directly targeting ADAM9. Mol Med Rep. 16:6419–6427. 2017. View Article : Google Scholar : PubMed/NCBI

40 

Hua Y, Liang C, Miao C, Wang S, Su S, Shao P, Liu B, Bao M, Zhu J, Xu A, et al: MicroRNA-126 inhibits proliferation and metastasis in prostate cancer via regulation of ADAM9. Oncol Lett. 15:9051–9060. 2018.PubMed/NCBI

41 

Liu Q, Jiang J, Fu Y, Liu T, Yu Y and Zhang X: miR-129-5p functions as a tumor suppressor in gastric cancer progression through targeting ADAM9. Biomed Pharmacother. 105:420–427. 2018. View Article : Google Scholar : PubMed/NCBI

42 

Li LX, Lam IH, Liang FF, Yi SP, Ye LF, Wang JT, Guo WW and Xu M: miR-198 affects the proliferation and apoptosis of colorectal cancer through regulation of ADAM28/JAK-STAT signaling pathway. Eur Rev Med Pharmacol Sci. 23:1487–1493. 2019.PubMed/NCBI

43 

Ge X, Cui H, Zhou Y, Yin D, Feng Y, Xin Q, Xu X, Liu W, Liu S and Zhang Q: miR-320a modulates cell growth and chemosensitivity via regulating ADAM10 in gastric cancer. Mol Med Rep. 16:9664–9670. 2017. View Article : Google Scholar : PubMed/NCBI

44 

Li J, Lu M, Jin J, Lu X, Xu T and Jin S: miR-449a suppresses tamoxifen resistance in human breast cancer cells by targeting ADAM22. Cell Physiol Biochem. 50:136–149. 2018. View Article : Google Scholar : PubMed/NCBI

45 

van Kampen JGM, van Hooij O, Jansen CF, Smit FP, van Noort PI, Schultz I, Schaapveld RQJ, Schalken JA and Verhaegh GW: miRNA-520f reverses epithelial-to-mesenchymal transition by targeting ADAM9 and TGFBR2. Cancer Res. 77:2008–2017. 2017. View Article : Google Scholar : PubMed/NCBI

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September-2020
Volume 20 Issue 3

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Spandidos Publications style
Zha Z, Jia F, Hu P, Mai E and Lei T: MicroRNA‑574‑3p inhibits the malignant behavior of liver cancer cells by targeting ADAM28 Retraction in /10.3892/ol.2023.13973. Oncol Lett 20: 3015-3023, 2020
APA
Zha, Z., Jia, F., Hu, P., Mai, E., & Lei, T. (2020). MicroRNA‑574‑3p inhibits the malignant behavior of liver cancer cells by targeting ADAM28 Retraction in /10.3892/ol.2023.13973. Oncology Letters, 20, 3015-3023. https://doi.org/10.3892/ol.2020.11852
MLA
Zha, Z., Jia, F., Hu, P., Mai, E., Lei, T."MicroRNA‑574‑3p inhibits the malignant behavior of liver cancer cells by targeting ADAM28 Retraction in /10.3892/ol.2023.13973". Oncology Letters 20.3 (2020): 3015-3023.
Chicago
Zha, Z., Jia, F., Hu, P., Mai, E., Lei, T."MicroRNA‑574‑3p inhibits the malignant behavior of liver cancer cells by targeting ADAM28 Retraction in /10.3892/ol.2023.13973". Oncology Letters 20, no. 3 (2020): 3015-3023. https://doi.org/10.3892/ol.2020.11852