Long non‑coding RNA OIP5‑AS1 facilitates the progression of ovarian cancer via the miR‑128‑3p/CCNG1 axis

Liu,Yuanyuan; Fu,Xiaomin; Wang,Xiuyun; Liu,Yanling; Song,Xiaoyan

doi:10.3892/mmr.2021.12027

Long non‑coding RNA OIP5‑AS1 facilitates the progression of ovarian cancer via the miR‑128‑3p/CCNG1 axis

Authors:
- Yuanyuan Liu
- Xiaomin Fu
- Xiuyun Wang
- Yanling Liu
- Xiaoyan Song
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Affiliations: Department of Obstetrics and Gynecology, The Shengli Oilfield Central Hospital, Dongying, Shandong 257034, P.R. China, Ultrasound Department of Obstetrics and Gynecology, The Shengli Oilfield Central Hospital, Dongying, Shandong 257034, P.R. China
Published online on: March 22, 2021 https://doi.org/10.3892/mmr.2021.12027
Article Number: 388
Copyright: © Liu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Long non‑coding RNA (LncRNA) o‑phthalaldehyde-interacting protein 5 antisense transcript 1 (OIP5‑AS1) serves major roles in the progression of various types of cancer. The present study investigated its biological function in ovarian cancer (OC) and its mechanisms. The levels of OIP5‑AS1, microRNA‑128‑3p (miR‑128‑3p) and cyclin G1 (CCNG1) were examined by reverse transcription‑quantitative PCR. Cell viability, apoptosis, migration and invasion were detected to analyze cellular progression. Glycolytic metabolism was assessed by detecting the levels of glucose consumption and lactate production. CCNG1 and hexokinase 2 protein levels were measured by western blotting. Dual‑luciferase reporter assay, RNA immunoprecipitation and RNA pull‑down assays were performed to affirm the interaction between two molecules. OIP5‑AS1 was found to be upregulated in OC tissues and cells. Knockdown of OIP5‑AS1 suppressed cell viability, migration, invasion and glycolysis while promoting apoptosis in OC cells. OIP5‑AS1 interacted with miR‑128‑3p and functioned as an oncogene by sequestering miR‑128‑3p. In addition, CCNG1 was a target gene for miR‑128‑3p and miR‑128‑3p regulated the CCNG1‑induced effects on OC cells by downregulating CCNG1. OIP5‑AS1 upregulated the expression of CCNG1 via targeting miR‑128‑3p. OIP5‑AS1 knockdown also inhibited tumor growth of OC in vivo by modulating the expression of miR‑128‑3p and CCNG1. Collectively, these data illustrated that the oncogenic role of OIP5‑AS1 in OC was associated with the miR‑128‑3p/CCNG1 axis at least in part. OIP5‑AS1 might be a probable diagnostic and therapeutic biomarker for the treatment of OC patients.

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1	Reid BM, Permuth JB and Sellers TA: Epidemiology of ovarian cancer: A review. Cancer Biol Med. 14:9–32. 2017. View Article : Google Scholar : PubMed/NCBI
2	Iorio MV, Visone R, Di Leva G, Donati V, Petrocca F, Casalini P, Taccioli C, Volinia S, Liu CG, Alder H, et al: MicroRNA signatures in human ovarian cancer. Cancer Res. 67:8699–8707. 2007. View Article : Google Scholar : PubMed/NCBI
3	Liu E, Liu Z and Zhou Y: Carboplatin-docetaxel-induced activity against ovarian cancer is dependent on up-regulated lncRNA PVT1. Int J Clin Exp Pathol. 8:3803–3810. 2015.PubMed/NCBI
4	Gao Y, Meng H, Liu S, Hu J, Zhang Y, Jiao T, Liu Y, Ou J, Wang D, Yao L, et al: LncRNA-HOST2 regulates cell biological behaviors in epithelial ovarian cancer through a mechanism involving microRNA let-7b. Hum Mol Genet. 24:841–852. 2015. View Article : Google Scholar : PubMed/NCBI
5	Chai Y, Liu J, Zhang Z and Liu L: HuR-regulated lncRNA NEAT1 stability in tumorigenesis and progression of ovarian cancer. Cancer Med. 5:1588–1598. 2016. View Article : Google Scholar : PubMed/NCBI
6	Ganapathy-Kanniappan S: Molecular intricacies of aerobic glycolysis in cancer: Current insights into the classic metabolic phenotype. Crit Rev Biochem Mol Biol. 53:667–682. 2018. View Article : Google Scholar : PubMed/NCBI
7	Vaupel P, Schmidberger H and Mayer A: The warburg effect: Essential part of metabolic reprogramming and central contributor to cancer progression. Int J Radiat Biol. 95:912–919. 2019. View Article : Google Scholar : PubMed/NCBI
8	Yang B, Zhang L, Cao Y, Chen S, Cao J, Wu D, Chen J, Xiong H, Pan Z, Qiu F, et al: Overexpression of lncRNA IGFBP4-1 reprograms energy metabolism to promote lung cancer progression. Mol Cancer. 16:1542017. View Article : Google Scholar : PubMed/NCBI
9	Hu Y, Sun H, Hu J and Zhang X: LncRNA DLX6-AS1 promotes the progression of neuroblastoma by activating STAT2 via targeting miR-506-3p. Cancer Manag Res. 12:7451–7463. 2020. View Article : Google Scholar : PubMed/NCBI
10	Li N and Zhan X and Zhan X: The lncRNA SNHG3 regulates energy metabolism of ovarian cancer by an analysis of mitochondrial proteomes. Gynecol Oncol. 150:343–354. 2018. View Article : Google Scholar : PubMed/NCBI
11	Peng WX, Koirala P and Mo YY: LncRNA-mediated regulation of cell signaling in cancer. Oncogene. 36:5661–5667. 2017. View Article : Google Scholar : PubMed/NCBI
12	Gutschner T and Diederichs S: The hallmarks of cancer: A long non-coding RNA point of view. RNA Biol. 9:703–719. 2012. View Article : Google Scholar : PubMed/NCBI
13	Nagano T and Fraser P: No-nonsense functions for long noncoding RNAs. Cell. 145:178–181. 2011. View Article : Google Scholar : PubMed/NCBI
14	Wang M, Sun X, Yang Y and Jiao W: Long non-coding RNA OIP5-AS1 promotes proliferation of lung cancer cells and leads to poor prognosis by targeting miR-378a-3p. Thorac Cancer. 9:939–949. 2018. View Article : Google Scholar : PubMed/NCBI
15	Liu X, Zheng J, Xue Y, Yu H, Gong W, Wang P, Li Z and Liu Y: PIWIL3/OIP5-AS1/miR-367-3p/CEBPA feedback loop regulates the biological behavior of glioma cells. Theranostics. 8:1084–1105. 2018. View Article : Google Scholar : PubMed/NCBI
16	Guo L, Chen J, Liu D and Liu L: OIP5-AS1/miR-137/ZNF217 axis promotes malignant behaviors in epithelial ovarian cancer. Cancer Manag Res. 12:6707–6717. 2020. View Article : Google Scholar : PubMed/NCBI
17	Liu QY, Jiang XX, Tian HN, Guo HL, Guo H and Guo Y: Long non-coding RNA OIP5-AS1 plays an oncogenic role in ovarian cancer through targeting miR-324-3p/NFIB axis. Eur Rev Med Pharmacol Sci. 24:7266–7275. 2020.PubMed/NCBI
18	Cho WC: OncomiRs: The discovery and progress of microRNAs in cancers. Mol Cancer. 6:602007. View Article : Google Scholar : PubMed/NCBI
19	Gregory RI and Shiekhattar R: MicroRNA biogenesis and cancer. Cancer Res. 65:3509–3512. 2005. View Article : Google Scholar : PubMed/NCBI
20	Chen J, Zhao D and Meng Q: Knockdown of HCP5 exerts tumor-suppressive functions by up-regulating tumor suppressor miR-128-3p in anaplastic thyroid cancer. Biomed Pharmacother. 116:1089662019. View Article : Google Scholar : PubMed/NCBI
21	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
22	Zhang C, Xie L, Liang H and Cui Y: LncRNA MIAT facilitates osteosarcoma progression by regulating mir-128-3p/VEGFC axis. IUBMB Life. 71:845–853. 2019. View Article : Google Scholar : PubMed/NCBI
23	Xu M, Zhou K, Wu Y, Wang L and Lu S: Linc0a0161 regulated the drug resistance of ovarian cancer by sponging microRNA-128 and modulating MAPK1. Mol Carcinog. 58:577–587. 2019. View Article : Google Scholar : PubMed/NCBI
24	Li R, Gong L, Li P, Wang J and Bi L: MicroRNA-128/homeobox B8 axis regulates ovarian cancer cell progression. Basic Clin Pharmacol Toxicol. 125:499–507. 2019. View Article : Google Scholar : PubMed/NCBI
25	Baek WK, Kim D, Jung N, Yi YW, Kim JM, Cha SD, Bae I and Cho CH: Increased expression of cyclin G1 in leiomyoma compared with normal myometrium. Am J Obstet Gynecol. 188:634–639. 2003. View Article : Google Scholar : PubMed/NCBI
26	Perez R, Wu N, Klipfel AA and Beart RW Jr: A better cell cycle target for gene therapy of colorectal cancer: Cyclin G. Gastroenterology. 7:884–889. 2003.
27	Gramantieri L, Ferracin M, Fornari F, Veronese A, Sabbioni S, Liu CG, Calin GA, Giovannini C, Ferrazzi E, Grazi GL, et al: Cyclin G1 is a target of miR-122a, a microRNA frequently down-regulated in human hepatocellular carcinoma. Cancer Res. 67:6092–6099. 2007. View Article : Google Scholar : PubMed/NCBI
28	Liu X, Ma L, Rao Q, Mao Y, Xin Y, Xu H, Li C and Wang X: MiR-1271 inhibits ovarian cancer growth by targeting cyclin G1. Med Sci Monit. 21:3152–3158. 2015. View Article : Google Scholar : PubMed/NCBI
29	Yan J, Jiang JY, Meng XN, Xiu YL and Zong ZH: MiR-23b targets cyclin G1 and suppresses ovarian cancer tumorigenesis and progression. J Exp Clin Cancer Res. 35:312016. View Article : Google Scholar : PubMed/NCBI
30	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
31	Albright JL: Dairy animal welfare: Current and needed research. J Dairy Sci. 70:2711–2731. 1987. View Article : Google Scholar : PubMed/NCBI
32	Swearengen JR: Common challenges in safety: A review and analysis of AAALAC findings. ILAR J. 59:127–133. 2018. View Article : Google Scholar : PubMed/NCBI
33	Lou W, Ding B and Fu P: Pseudogene-derived lncRNAs and their miRNA sponging mechanism in human cancer. Front Cell Dev Biol. 8:852020. View Article : Google Scholar : PubMed/NCBI
34	Wu DD, Chen X, Sun KX, Wang LL, Chen S and Zhao Y: Role of the lncRNA ABHD11-AS1 in the tumorigenesis and progression of epithelial ovarian cancer through targeted regulation of RhoC. Mol Cancer. 16:1382017. View Article : Google Scholar : PubMed/NCBI
35	Zhu FF, Zheng FY, Wang HO, Zheng JJ and Zhang Q: Downregulation of lncRNA TUBA4B is associated with poor prognosis for epithelial ovarian cancer. Pathol Oncol Res. 24:419–425. 2018. View Article : Google Scholar : PubMed/NCBI
36	Arunkumar G, Anand S, Raksha P, Dhamodharan S, Prasanna Srinivasa Rao H, Subbiah S, Murugan AK and Munirajan AK: LncRNA OIP5-AS1 is overexpressed in undifferentiated oral tumors and integrated analysis identifies as a downstream effector of stemness-associated transcription factors. Sci Rep. 8:70182018. View Article : Google Scholar : PubMed/NCBI
37	Hu GW, Wu L, Kuang W, Chen Y, Zhu XG, Guo H and Lang HL: Knockdown of linc-OIP5 inhibits proliferation and migration of glioma cells through down-regulation of YAP-NOTCH signaling pathway. Gene. 610:24–31. 2017. View Article : Google Scholar : PubMed/NCBI
38	Naemura M, Kuroki M, Tsunoda T, Arikawa N, Sawata Y, Shirasawa S and Kotake Y: The long noncoding RNA OIP5-AS1 is involved in the regulation of cell proliferation. Anticancer Res. 38:77–81. 2018.PubMed/NCBI
39	Bai Y and Li S: Long noncoding RNA OIP5-AS1 aggravates cell proliferation, migration in gastric cancer by epigenetically silencing NLRP6 expression via binding EZH2. J Cell Biochem. 121:353–362. 2020. View Article : Google Scholar : PubMed/NCBI
40	Sen R, Ghosal S, Das S, Balti S and Chakrabarti J: Competing endogenous RNA: The key to posttranscriptional regulation. Sci World J. 2014:8962062014. View Article : Google Scholar
41	Tan JY, Sirey T, Honti F, Graham B, Piovesan A, Merkenschlager M, Webber C, Ponting CP and Marques AC: Extensive microRNA-mediated crosstalk between lncRNAs and mRNAs in mouse embryonic stem cells. Genome Res. 25:655–666. 2015. View Article : Google Scholar : PubMed/NCBI
42	Sui J, Li YH, Zhang YQ, Li CY, Shen X, Yao WZ, Peng H, Hong WW, Yin LH, Pu YP and Liang GY: Integrated analysis of long non-coding RNA-associated ceRNA network reveals potential lncRNA biomarkers in human lung adenocarcinoma. Int J Oncol. 49:2023–2036. 2016. View Article : Google Scholar : PubMed/NCBI
43	Sun WL, Kang T, Wang YY, Sun JP, Li C, Liu HJ, Yang Y and Jiao BH: Long noncoding RNA OIP5-AS1 targets Wnt-7b to affect glioma progression via modulation of miR-410. Biosci Rep. 39:BSR201803952019. View Article : Google Scholar : PubMed/NCBI
44	Escoté X and Fajas L: Metabolic adaptation to cancer growth: From the cell to the organism. Cancer Lett. 356:171–175. 2015. View Article : Google Scholar : PubMed/NCBI
45	Icard P, Fournel L, Wu Z, Alifano M and Lincet H: Interconnection between metabolism and cell cycle in cancer. Trends Biochem Sci. 44:490–501. 2019. View Article : Google Scholar : PubMed/NCBI
46	Horne MC, Goolsby GL, Donaldson KL, Tran D, Neubauer M and Wahl AF: Cyclin G1 and cyclin G2 comprise a new family of cyclins with contrasting tissue-specific and cell cycle-regulated expression. J Biol Chem. 271:6050–6061. 1996. View Article : Google Scholar : PubMed/NCBI
47	Jensen MR, Factor VM, Fantozzi A, Helin K, Huh CG and Thorgeirsson SS: Reduced hepatic tumor incidence in cyclin G1-deficient mice. Hepatology. 37:862–870. 2003. View Article : Google Scholar : PubMed/NCBI