miR‑128‑3p serves as an oncogenic microRNA in osteosarcoma cells by downregulating ZC3H12D

Zhu,Maoshu; Wu,Yulong; Wang,Zhaowei; Lin,Minghua; Su,Bin; Li,Chunyang; Liang,Fulong; Chen,Xinjiang

doi:10.3892/ol.2020.12413

miR‑128‑3p serves as an oncogenic microRNA in osteosarcoma cells by downregulating ZC3H12D

Authors:
- Maoshu Zhu
- Yulong Wu
- Zhaowei Wang
- Minghua Lin
- Bin Su
- Chunyang Li
- Fulong Liang
- Xinjiang Chen
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Affiliations: Department of Central Laboratory, The Fifth Hospital of Xiamen, Xiang'an, Xiamen, Fujian 361000, P.R. China, Department of Urinary Surgery, The Fifth Hospital of Xiamen, Xiang'an, Xiamen, Fujian 361000, P.R. China, Department of Gynecology, The Fifth Hospital of Xiamen, Xiang'an, Xiamen, Fujian 361000, P.R. China, Department of Pathology, The Fifth Hospital of Xiamen, Xiang'an, Xiamen, Fujian 361000, P.R. China, Department of Pharmacy, The Fifth Hospital of Xiamen, Xiang'an, Xiamen, Fujian 361000, P.R. China, Department of Orthopedics, The Fifth Hospital of Xiamen, Xiang'an, Xiamen, Fujian 361000, P.R. China, Department of Neurology, The Fifth Hospital of Xiamen, Xiang'an, Xiamen, Fujian 361000, P.R. China
Published online on: December 31, 2020 https://doi.org/10.3892/ol.2020.12413
Article Number: 152
Copyright: © Zhu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Osteosarcoma is the second leading cause of cancer‑associated mortality worldwide in children and adolescents. ZC3H12D has been shown to negatively regulate Toll‑like receptor signaling and serves as a possible tumor suppressor gene. MicroRNAs (miRNAs/miRs) are known to play an important role in the proliferation of human osteosarcoma cells. However, whether miRNAs can affect tumor development by regulating the expression of ZC3H12D has not yet been investigated. The aim of the present study was to investigate the role of miR128‑3p in regulating ZC3H12D expression, as well as its function in tumor cell proliferation, apoptosis, and metastasis. Reverse transcription‑quantitative PCR, western blotting and dual luciferase reporter assays were performed to analyze the regulation of ZC3H12D expression by miR‑128‑3p. MTT, colony formation and flow cytometry assays were also used to analyze the effect of miR‑128‑3p on cell proliferation and apoptosis. A wound healing assay was performed to investigate the cell migration ability. The results demonstrated that miR‑128‑3p directly targeted ZC3H12D and downregulated its expression, thereby promoting cell proliferation and migration. miR‑128‑3p overexpression also improved resistance to cisplatin in MG‑63 and 143B cell lines, supporting the hypothesis that miR‑128‑3p may function as an oncogene in osteosarcoma cells. The potential clinical significance of miR‑128‑3p as a biomarker and therapeutic target provides rationale for further investigation into the miR‑128‑3p‑mediated molecular pathway and how it is associated with osteosarcoma development.

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1	Glover J, Krailo M, Tello T, Marina N, Janeway K, Barkauskas D, Fan TM, Gorlick R and Khanna C; COG Osteosarcoma Biology Group, : A summary of the osteosarcoma banking efforts: A report from the Children's Oncology Group and the QuadW Foundation. Pediatr Blood Cancer. 62:450–455. 2015. View Article : Google Scholar : PubMed/NCBI
2	Grignani G, Palmerini E, Ferraresi V, D'Ambrosio L, Bertulli R, Asaftei SD, Tamburini A, Pignochino Y, Sangiolo D, Marchesi E, et al: Sorafenib and everolimus for patients with unresectable high-grade osteosarcoma progressing after standard treatment: A non-randomised phase 2 clinical trial. Lancet Oncol. 16:98–107. 2015. View Article : Google Scholar : PubMed/NCBI
3	Daw NC, Chou AJ, Jaffe N, Rao BN, Billups CA, Rodriguez-Galindo C, Meyers PA and Huh WW: Recurrent osteosarcoma with a single pulmonary metastasis: A multi-institutional review. Br J Cancer. 112:278–282. 2015. View Article : Google Scholar : PubMed/NCBI
4	Di Fiore R, Guercio A, Puleio R, Di Marco P, Drago-Ferrante R, D'Anneo A, De Blasio A, Carlisi D, Di Bella S, Pentimalli F, et al: Modeling human osteosarcoma in mice through 3AB-OS cancer stem cell xenografts. J Cell Biochem. 113:3380–3392. 2012. View Article : Google Scholar : PubMed/NCBI
5	Moreno F, Cacciavillano W, Cipolla M, Coirini M, Streitenberger P, López Martí J, Palladino M, Morici M, Onoratelli M, Drago G, et al: Childhood osteosarcoma: Incidence and survival in Argentina. Report from the National Pediatric Cancer Registry, ROHA Network 2000–2013. Pediatr Blood Cancer. 64:2017. View Article : Google Scholar
6	Durnali A, Alkis N, Cangur S, Yukruk FA, Inal A, Tokluoglu S, Seker MM, Bal O, Akman T, Inanc M, et al: Prognostic factors for teenage and adult patients with high-grade osteosarcoma: An analysis of 240 patients. Med Oncol. 30:6242013. View Article : Google Scholar : PubMed/NCBI
7	Osborne TS and Khanna C: A review of the association between osteosarcoma metastasis and protein translation. J Comp Pathol. 146:132–142. 2012. View Article : Google Scholar : PubMed/NCBI
8	Liang J, Song W, Tromp G, Kolattukudy PE and Fu M: Genome-wide survey and expression profiling of CCCH-zinc finger family reveals a functional module in macrophage activation. PLoS One. 3:e28802008. View Article : Google Scholar : PubMed/NCBI
9	Liang J, Wang J, Azfer A, Song W, Tromp G, Kolattukudy PE and Fu M: A novel CCCH-zinc finger protein family regulates proinflammatory activation of macrophages. J Biol Chem. 283:6337–6346. 2008. View Article : Google Scholar : PubMed/NCBI
10	Minagawa K, Yamamoto K, Nishikawa S, Ito M, Sada A, Yakushijin K, Okamura A, Shimoyama M, Katayama Y and Matsui T: Deregulation of a possible tumour suppressor gene, ZC3H12D, by translocation of IGK@ in transformed follicular lymphoma with t(2;6)(p12;q25). Br J Haematol. 139:161–163. 2008. View Article : Google Scholar
11	Huang S, Qi D, Liang J, Miao R, Minagawa K, Quinn T, Matsui T, Fan D, Liu J and Fu M: The putative tumor suppressor Zc3h12d modulates toll-like receptor signaling in macrophages. Cell Signal. 24:569–576. 2012. View Article : Google Scholar : PubMed/NCBI
12	Zhang H, Wang WC, Chen JK, Zhou L, Wang M, Wang ZD, Yang B, Xia YM, Lei S, Fu EQ and Jiang T: ZC3H12D attenuated inflammation responses by reducing mRNA stability of proinflammatory genes. Mol Immunol. 67:206–212. 2015. View Article : Google Scholar : PubMed/NCBI
13	Wang M, Vikis HG, Wang Y, Jia D, Wang D, Bierut LJ, Bailey-Wilson JE, Amos CI, Pinney SM, Petersen GM, et al: Identification of a novel tumor suppressor gene p34 on human chromosome 6q25.1. Cancer Res. 67:93–99. 2007. View Article : Google Scholar : PubMed/NCBI
14	Minagawa K, Katayama Y, Nishikawa S, Yamamoto K, Sada A, Okamura A, Shimoyama M and Matsui T: Inhibition of G₁ to S phase progression by a novel zinc finger protein P58^TFL at P-bodies. Mol Cancer Res. 7:880–889. 2009. View Article : Google Scholar : PubMed/NCBI
15	Nohata N, Hanazawa T, Kikkawa N, Mutallip M, Fujimura L, Yoshino H, Kawakami K, Chiyomaru T, Enokida H, Nakagawa M, et al: Caveolin-1 mediates tumor cell migration and invasion and its regulation by miR-133a in head and neck squamous cell carcinoma. Int J Oncol. 38:209–217. 2011.PubMed/NCBI
16	Chiche J, Pommier S, Beneteau M, Mondragón L, Meynet O, Zunino B, Mouchotte A, Verhoeyen E, Guyot M, Pagès G, et al: GAPDH enhances the aggressiveness and the vascularization of non-Hodgkin's B lymphomas via NF-κB-dependent induction of HIF-1α. Leukemia. 29:1163–1176. 2015. View Article : Google Scholar : PubMed/NCBI
17	Liberti MV, Dai Z, Wardell SE, Baccile JA, Liu X, Gao X, Baldi R, Mehrmohamadi M, Johnson MO, Madhukar NS, et al: A predictive model for selective targeting of the Warburg effect through GAPDH inhibition with a natural product. Cell Metab. 26:648–659.e8. 2017. View Article : Google Scholar : PubMed/NCBI
18	Révillion F, Pawlowski V, Hornez L and Peyrat JP: Glyceraldehyde-3-phosphate dehydrogenase gene expression in human breast cancer. Eur J Cancer. 36:1038–1042. 2000. View Article : Google Scholar : PubMed/NCBI
19	Zhu LJ and Altmann SW: mRNA and 18S-RNA coapplication-reverse transcription for quantitative gene expression analysis. Anal Biochem. 345:102–109. 2005. View Article : Google Scholar : PubMed/NCBI
20	Wang XJ, Yan ZJ, Luo GC, Chen YY and Bai PM: miR-26 suppresses renal cell cancer via down-regulating coronin-3. Mol Cell Biochem. 463:137–146. 2020. View Article : Google Scholar : PubMed/NCBI
21	Bai P, Li W, Wan Z, Xiao Y, Xiao W, Wang X, Wu Z, Zhang K, Wang Y, Chen B, et al: miR-489-3p inhibits prostate cancer progression by targeting DLX1. Cancer Manag Res. 12:2719–2729. 2020. View Article : Google Scholar : PubMed/NCBI
22	Liu L, Liu S, Duan Q, Chen L, Wu T, Qian H, Yang S, Xin D, He Z and Guo Y: MicroRNA-142-5p promotes cell growth and migration in renal cell carcinoma by targeting BTG3. Am J Transl Res. 9:2394–2402. 2017.PubMed/NCBI
23	Wakahashi S, Kawakami F, Wakahashi K, Minagawa K, Matsuo K, Katayama Y, Yamada H, Matsui T and Sudo T: Transformed follicular lymphoma (TFL) predicts outcome in advanced endometrial cancer. Cancer Epidemiol Biomarkers Prev. 27:963–969. 2018. View Article : Google Scholar : PubMed/NCBI
24	Li Z, Ni J, Song D and Ding M: Regulatory mechanism of microRNA-128 in osteosarcoma tumorigenesis and evolution by targeting SASH1. Oncol Lett. 15:8687–8694. 2018.PubMed/NCBI
25	Tian Z, Guo B, Yu M, Wang C, Zhang H, Liang Q, Jiang K and Cao L: Upregulation of micro-ribonucleic acid-128 cooperating with downregulation of PTEN confers metastatic potential and unfavorable prognosis in patients with primary osteosarcoma. Onco Targets Ther. 7:1601–1608. 2014.PubMed/NCBI
26	Liu X, Liang Z, Gao K, Li H, Zhao G, Wang S and Fang J: MicroRNA-128 inhibits EMT of human osteosarcoma cells by directly targeting integrin α2. Tumour Biol. 37:7951–7957. 2016. View Article : Google Scholar : PubMed/NCBI
27	Guo XL, Wang HB, Yong JK, Zhong J and Li QH: MiR-128-3p overexpression sensitizes hepatocellular carcinoma cells to sorafenib induced apoptosis through regulating DJ-1. Eur Rev Med Pharmacol Sci. 22:6667–6677. 2018.PubMed/NCBI
28	Zhao J, Li D and Fang L: MiR-128-3p suppresses breast cancer cellular progression via targeting LIMK1. Biomed Pharmacother. 115:1089472019. View Article : Google Scholar : PubMed/NCBI
29	Huang CY, Huang XP, Zhu JY, Chen ZG, Li XJ, Zhang XH, Huang S, He JB, Lian F, Zhao YN, et al: miR-128-3p suppresses hepatocellular carcinoma proliferation by regulating PIK3R1 and is correlated with the prognosis of HCC patients. Oncol Rep. 33:2889–2898. 2015. View Article : Google Scholar : PubMed/NCBI
30	Meyers PA, Heller G, Healey JH, Huvos A, Applewhite A, Sun M and LaQuaglia M: Osteogenic sarcoma with clinically detectable metastasis at initial presentation. J Clin Oncol. 11:449–453. 1993. View Article : Google Scholar : PubMed/NCBI
31	Kager L, Zoubek A, Pötschger U, Kastner U, Flege S, Kempf-Bielack B, Branscheid D, Kotz R, Salzer-Kuntschik M, Winkelmann W, et al: Primary metastatic osteosarcoma: Presentation and outcome of patients treated on neoadjuvant Cooperative Osteosarcoma Study Group protocols. J Clin Oncol. 21:2011–2018. 2003. View Article : Google Scholar : PubMed/NCBI
32	Kim M, Jung JY, Choi S, Lee H, Morales LD, Koh JT, Kim SH, Choi YD, Choi C, Slaga TJ, et al: GFRA1 promotes cisplatin-induced chemoresistance in osteosarcoma by inducing autophagy. Autophagy. 13:149–168. 2017. View Article : Google Scholar : PubMed/NCBI
33	Duan Z, Zhang J, Ye S, Shen J, Choy E, Cote G, Harmon D, Mankin H, Hua Y, Zhang Y, et al: A-770041 reverses paclitaxel and doxorubicin resistance in osteosarcoma cells. BMC Cancer. 14:6812014. View Article : Google Scholar : PubMed/NCBI