Hsa_circ_0091074 regulates TAZ expression via microRNA‑1297 in triple negative breast cancer cells

Hu,Jiashu; Ji,Changle; Hua,Kaiyao; Wang,Xuehui; Deng,Xiaochong; Li,Jiayi; Graham,Dinny; Fang,Lin

doi:10.3892/ijo.2020.5000

Hsa_circ_0091074 regulates TAZ expression via microRNA‑1297 in triple negative breast cancer cells

Authors:
- Jiashu Hu
- Changle Ji
- Kaiyao Hua
- Xuehui Wang
- Xiaochong Deng
- Jiayi Li
- Dinny Graham
- Lin Fang
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Affiliations: Department of Thyroid and Breast, Division of General Surgery, Shanghai Tenth People's Hospital, Tongji University School of Medicine, Shanghai 200072, P.R. China, Centre for Cancer Research, The Westmead Institute for Medical Research, The University of Sydney, Westmead, New South Wales 2145, Australia
Published online on: February 25, 2020 https://doi.org/10.3892/ijo.2020.5000
Pages: 1314-1326

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Abstract

Triple negative breast cancer (TNBC) has the highest recurrence, metastasis and mortality rate of all breast cancer subtypes, due to its typically more aggressive characteristics and lack of effective targeted treatment options. The Hippo pathway is a signaling cascade composed of a group of conserved kinases, which serves an important role in almost all cancer types. Both circular RNAs (circRNAs) and microRNAs (miRNAs) are types of non‑coding RNAs, which influence cancer progression. CircRNAs have been demonstrated to serve as miRNA ‘sponges’, binding to miRNAs to inhibit their function. In the present study, it was revealed that circular RNA hsa_circ_0091074 binds miR‑1297, and that there is an inverse association between the expression levels of the two non‑coding RNAs in breast cells, indicating that hsa_circ_0091074 may serve as an endogenous ‘sponge’ for miR‑1297. Subsequently, the potential function and mechanism underlying the involvement of miR‑1297 in breast cancer was investigated via MTT, colony formation, wound healing and cell cycle assays. Increased miR‑1297 expression resulted in a decrease in the protein levels of critical Hippo pathway transcriptional mediator Transcriptional coactivator with PDZ‑binding motif (TAZ), which is a putative target of miR‑1297. This was confirmed using dual‑luciferase reporter assays, which revealed that miR‑1297 targets TAZ by binding its 3'‑untranslated region (3'UTR). The current results indicate that miR‑1297 serves as a suppressor of breast cancer cell proliferation and invasiveness, and that this can be partially reversed by hsa_circ_0091074, suggesting that the hsa_circ_0091074/miR‑1297/TAZ/TEAD4 axis may represent a potential therapeutic target for triple negative breast cancer in the future.

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1	Ferlay J, Ervik M, Lam F, Colombet M, Mery L, Piñeros M, Znaor A, Soerjomataram I and Bray F: global Cancer Observatory: Cancer Today. IARC; Lyon: 2018, https://gco.iarc.fr/today. Accessed March 8, 2019.
2	Kwapisz D: Cyclin-dependent kinase 4/6 inhibitors in breast cancer: Palbociclib, ribociclib, and abemaciclib. Breast Cancer Res Treat. 166:41–54. 2017. View Article : Google Scholar : PubMed/NCBI
3	Woodcock CC, Huang Y, Woodcock SR, Salvatore SR, Singh B, Golin-Bisello F, Davidson NE, Neumann CA, Freeman BA and Wendell SG: Nitro-fatty acid inhibition of triple negative breast cancer cell viability, migration, invasion and tumor growth. J Biol Chem. 293:1120–1137. 2018. View Article : Google Scholar
4	Cocquerelle C, Mascrez B, Hétuin D and Bailleul B: Mis-splicing yields circular RNA molecules. FASEB J. 7:155–160. 1993. View Article : Google Scholar : PubMed/NCBI
5	Memczak S, Jens M, Elefsinioti A, Torti F, Krueger J, Rybak A, Maier L, Mackowiak SD, Gregersen LH, Munschauer M, et al: Circular RNAs are a large class of animal RNAs with regulatory potency. Nature. 495:333–338. 2013. View Article : Google Scholar : PubMed/NCBI
6	Qu S, Yang X, Li X, Wang J, Gao Y, Shang R, Sun W, Dou K and Li H: Circular RNA: A new star of noncoding RNAs. Cancer Lett. 365:141–148. 2015. View Article : Google Scholar : PubMed/NCBI
7	Meng X, Hu D, Zhang P, Chen Q and Chen M: CircFunBase: A database for functional circular RNAs. Database (Oxford) 2019. baz0032019.
8	Zhang Y, Yang L and Chen LL: Characterization of circular RNAs. Methods Mol Biol. 1402:215–227. 2016. View Article : Google Scholar : PubMed/NCBI
9	Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B, Damgaard CK and Kjems J: Natural RNA circles function as efficient microRNA sponges. Nature. 495:3843882013. View Article : Google Scholar : PubMed/NCBI
10	Hansen TB, Wiklund ED, Bramsen JB, Villadsen SB, Statham AL, Clark SJ and Kjems J: miRNA-dependent gene silencing involving Ago2-mediated cleavage of a circular antisense RNA. EMBO J. 30:4414–4422. 2011. View Article : Google Scholar : PubMed/NCBI
11	Xin Z, Ma Q, Ren S, Wang G and Li F: The understanding of circular RNAs as special triggers in carcinogenesis. Brief Funct Genomics. 16:80–86. 2017.
12	Rybak‑Wolf A, Stottmeister C, Glažar P, Jens M, Pino N, Giusti S, Hanan M, Behm M, Bartok O, Ashwal-Fluss R, et al: Circular RNAs in the mammalian brain are highly abundant, conserved, and dynamically expressed. Mol Cell. 58:870–885. 2015. View Article : Google Scholar
13	Meng X, Zhu Y, Tao L, Zhao S and Qiu S: miR-590-3p mediates melatonin-induced cell apoptosis by targeting septin 7 in the human osteoblast cell line hFOB 1.19. Mol Med Rep. 17:7202–7208. 2018.PubMed/NCBI
14	Tang W, Ji M, He G, Yang L, Niu Z, Jian M, Wei Y, Ren L and Xu J: Silencing CDR1as inhibits colorectal cancer progression through regulating microRNA-7. Onco Targets Ther. 10:2045–2056. 2017. View Article : Google Scholar : PubMed/NCBI
15	Buglioni S, Vici P, Sergi D, Pizzuti L, Di Lauro L, Antoniani B, Sperati F, Terrenato I, Carosi M, Gamucci T, et al: Analysis of the hippo transducers TAZ and YAP in cervical cancer and its microenvironment. Oncoimmunology. 5:e11601872016. View Article : Google Scholar : PubMed/NCBI
16	Royer C, Koch S, Qin X, Zak J, Buti L, Dudziec E, Zhong S, Ratnayaka I, Srinivas S and Lu X: ASPP2 links the apical lateral polarity complex to the regulation of YAP activity in epithelial cells. PLos One. 9:e1113842014. View Article : Google Scholar : PubMed/NCBI
17	Zhou X, Su J, Feng S, Wang L, Yin X, Yan J and Wang Z: Antitumor activity of curcumin is involved in down-regulation of YAP/TAZ expression in pancreatic cancer cells. Oncotarget. 7:79076–79088. 2016. View Article : Google Scholar : PubMed/NCBI
18	Shi P, Feng J and Chen C: Hippo pathway in mammary gland development and breast cancer. Acta Biochim Biophys Sin (Shanghai). 47:53–59. 2015. View Article : Google Scholar
19	Plouffe SW, Hong AW and Guan KL: Disease implications of the Hippo/YAP pathway. Trends Mol Med. 21:212–222. 2015. View Article : Google Scholar : PubMed/NCBI
20	Bartucci M, Dattilo R, Moriconi C, Pagliuca A, Mottolese M, Federici G, Benedetto AD, Todaro M, Stassi G, Sperati F, et al: TAZ is required for metastatic activity and chemoresistance of breast cancer stem cells. Oncogene. 34:681–690. 2015. View Article : Google Scholar
21	Cordenonsi M, Zanconato F, Azzolin L, Forcato M, Rosato A, Frasson C, Inui M, Montagner M, Parenti AR, Poletti A, et al: The Hippo transducer TAZ confers cancer stem cell-related traits on breast cancer cells. Cell. 147:759–772. 2011. View Article : Google Scholar : PubMed/NCBI
22	Passaniti A, Brusgard JL, Qiao Y, Sudol M and Finch-Edmondson M: Roles of RUNX in Hippo pathway signaling. Adv Exp Med Biol. 962:435–448. 2017. View Article : Google Scholar : PubMed/NCBI
23	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
24	Li JH, Liu S, Zhou H, Qu LH and Yang JH: starBase v2.0: Decoding miRNA-ceRNA, miRNA-ncRNA and protein-RNA interaction networks from large-scale CLIP-Seq data. Nucleic Acids Res. 42(Database Issue): D92–D97. 2014. View Article : Google Scholar
25	Glažar P, Papavasileiou P and Rajewsky N: circBase: A database for circular RNAs. RNA. 20:1666–1670. 2014. View Article : Google Scholar
26	Barrett T, Wilhite SE, Ledoux P, Evangelista C, Kim IF, Tomashevsky M, Marshall KA, Phillippy KH, Sherman PM, Holko M, et al: NCBI GEO: Archive for functional genomics data sets-update. Nucleic Acids Res. 41(Database Issue): D991–D995. 2013. View Article : Google Scholar
27	Lappalainen I, Almeida-King J, Kumanduri V, Senf A, Spalding JD, Ur-Rehman S, Saunders G, Kandasamy J, Caccamo M, Leinonen R, et al: The European Genome-phenome Archive of human data consented for biomedical research. Nat Genet. 47:692–695. 2015. View Article : Google Scholar : PubMed/NCBI
28	Tomczak K, Czerwińska P and Wiznerowicz M: The Cancer Genome Atlas (TCGA): An immeasurable source of knowledge. Contemp Oncol (Pozn). 19:A68–A77. 2015.
29	Lánczky A, Nagy Á, Bottai G, Munkácsy G, Szabó A, Santarpia L and Győrffy B: miRpower: A web‑tool to validate survival‑associated miRNAs utilizing expression data from 2178 breast cancer patients. Breast Cancer Res Treat. 160:439–446. 2016. View Article : Google Scholar
30	Agarwal V, Bell GW, Nam JW and Bartel DP: Predicting effective microRNA target sites in mammalian mRNAs. Elife. 4:e050052015. View Article : Google Scholar :
31	Cowell JK, LaDuca J, Rossi MR, Burkhardt T, Nowak NJ and Matsui S: Molecular characterization of the t(3;9) associated with immortalization in the MCF10A cell line. Cancer Genet Cytogenet. 163:23–29. 2005. View Article : Google Scholar : PubMed/NCBI
32	Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA and Jemal A: Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 68:394–424. 2018. View Article : Google Scholar : PubMed/NCBI
33	Beatty A, Fink LS, Singh T, Strigun A, Peter E, Ferrer CM, Nicolas E, Cai KQ, Moran TP, Reginato MJ, et al: Metabolite profiling reveals the glutathione biosynthetic pathway as a therapeutic target in triple-negative breast cancer. Mol Cancer Ther. 17:264–275. 2018. View Article : Google Scholar
34	Chen LL, Zhang ZJ, Yi ZB and Li JJ: MicroRNA-211-5p suppresses tumour cell proliferation, invasion, migration and metastasis in triple-negative breast cancer by directly targeting SETBP1. Br J Cancer. 117:78–88. 2017. View Article : Google Scholar : PubMed/NCBI
35	Verduci L, Strano S, Yarden Y and Blandino G: The circ RNA-micro RNA code: Emerging implications for cancer diagnosis and treatment. Mol Oncol. 13:669–680. 2019.PubMed/NCBI
36	Hosseinahli N, Aghapour M, Duijf PH and Baradaran B: Treating cancer with microRNA replacement therapy: A literature review. J Cell Physiol. 233:5574–5588. 2018. View Article : Google Scholar : PubMed/NCBI
37	Shah MY, Ferrajoli A, Sood AK, Lopez-Berestein G and Calin GA: microRNA therapeutics in cancer-an emerging concept. EBioMedicine. 12:34–42. 2016. View Article : Google Scholar : PubMed/NCBI
38	Liu Y, Liang H and Jiang X: MiR-1297 promotes apoptosis and inhibits the proliferation and invasion of hepatocellular carcinoma cells by targeting HMGA2. Int J Mol Med. 36:1345–1352. 2015. View Article : Google Scholar : PubMed/NCBI
39	Li J, Gao J, Tian W, Li Y and Zhang J: Long non-coding RNA MALAT1 drives gastric cancer progression by regulating HMGB2 modulating the miR-1297. Cancer Cell Int. 17:442017. View Article : Google Scholar : PubMed/NCBI
40	Bu W and Luo T: miR-1297 promotes cell proliferation of non-small cell lung cancer cells: Involving in PTEN/Akt/Skp2 signaling pathway. DNA Cell Biol. 36:976–982. 2017. View Article : Google Scholar : PubMed/NCBI
41	Li X, Wang HL, Peng X, Zhou HF and Wang X: miR-1297 mediates PTEN expression and contributes to cell progression in LSCC. Biochem Biophys Res Commun. 427:254–260. 2012. View Article : Google Scholar : PubMed/NCBI
42	Yang NQ, Zhang J, Tang QY, Guo JM and Wang GM: miRNA-1297 induces cell proliferation by targeting phosphatase and tensin homolog in testicular germ cell tumor cells. Asian Pac J Cancer Prev. 15:6243–6246. 2014. View Article : Google Scholar : PubMed/NCBI
43	Liu C, Liu Z, Li X, Tang X, He J and Lu S: MicroRNA-1297 contributes to tumor growth of human breast cancer by targeting PTEN/PI3K/AKT signaling. Oncol Rep. 38:2435–2443. 2017. View Article : Google Scholar : PubMed/NCBI
44	Svoronos AA, Engelman DM and Slack FJ: OncomiR or tumor suppressor? The duplicity of microRNAs in cancer. Cancer Res. 76:3666–3670. 2016. View Article : Google Scholar : PubMed/NCBI
45	Liu J, Ye L, Li Q, Wu X, Wang B, Ouyang Y, Yuan Z, Li J and Lin C: Synaptopodin-2 suppresses metastasis of triple-negative breast cancer via inhibition of YAP/TAZ activity. J Pathol. 244:71–83. 2018. View Article : Google Scholar
46	Yu FX, Zhao B and Guan KL: Hippo pathway in organ size control, tissue homeostasis, and cancer. Cell. 163:811–828. 2015. View Article : Google Scholar : PubMed/NCBI
47	Park JH, Shin JE and Park HW: The role of hippo pathway in cancer stem cell biology. Mol Cells. 41:83–92. 2018.PubMed/NCBI
48	Ferraiuolo M, Verduci L, Blandino G and Strano S: Mutant p53 protein and the hippo transducers YAP and TAZ: A critical oncogenic node in human cancers. Int J Mol Sci. 18:pii: E961. 2017.PubMed/NCBI