Regulatory effect of the MAFG‑AS1/miR‑150‑5p/MYB axis on the proliferation and migration of breast cancer cells

Jia,Hongyao; Wu,Di; Zhang,Zhiru; Li,Sijie

doi:10.3892/ijo.2020.5150

Regulatory effect of the MAFG‑AS1/miR‑150‑5p/MYB axis on the proliferation and migration of breast cancer cells

Authors:
- Hongyao Jia
- Di Wu
- Zhiru Zhang
- Sijie Li
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Affiliations: Department of Breast Surgery, The First Hospital of Jilin University, Changchun, Jilin 130021, P.R. China
Published online on: November 20, 2020 https://doi.org/10.3892/ijo.2020.5150
Pages: 33-44
Copyright: © Jia et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Long noncoding RNA (lncRNA) MAF BZIP transcription factor G antisense RNA 1 (MAFG‑AS1) has been demonstrated to serve an important role in the progression of various types of cancer, whereas its role in breast cancer has not been fully elucidated. The present study aimed to explore the potential role and underlying mechanism of MAFG‑AS1 in breast cancer. To achieve this, the expression of MAFG‑AS1, microRNA (miR)‑150‑5p and MYB was detected by reverse transcription‑quantitative PCR. The binding between miR‑150‑5p and MAFG‑AS1 or MYB was verified using a luciferase reporter assay. Cell proliferation was analyzed by MTS, apoptosis and cell cycle were detected by Annexin V/propidium iodide, and cell migration was analyzed by wound healing assay. The results demonstrated that the expression levels of MAFG‑AS1 were significantly upregulated in breast cancer tissues and cells compared with those in normal breast tissues and cells. High MAFG‑AS1 expression promoted the proliferation, migration and epithelial‑mesenchymal transition of breast cancer cells. By contrast, miR‑150‑5p expression was reduced in breast cancer tissues compared with that in healthy breast tissues, and low expression of miR‑150‑5p was associated with poor overall survival in patients with breast cancer. Bioinformatics and luciferase assay revealed that MAFG‑AS1 served as a sponge of miR‑150‑5p, and that miR‑150‑5p bound to MYB. The functional rescue assay results demonstrated that MAFG‑AS1 knockdown suppressed the proliferation and migration of breast cancer cells by regulating miR‑150‑5p, which in turn targeted MYB. In conclusion, the results of the present study demonstrated that MAFG‑AS1 functioned as a novel oncogenic lncRNA in the development of human breast cancer via regulating the miR‑150‑5p/MYB axis, which suggested that MAFG‑AS1 may be a novel biomarker for the diagnosis and prognosis of human breast cancer.

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1	Ferlay J, Colombet M, Soerjomataram I, Mathers C, Parkin DM, Piñeros M, Znaor A and Bray F: Estimating the global cancer incidence and mortality in 2018: GLOBOCAN sources and methods. Int J Cancer. 144:1941–1953. 2019. View Article : Google Scholar
2	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
3	Feng RM, Zong YN, Cao SM and Xu RH: Current cancer situation in China: Good or bad news from the 2018 global cancer statistics? Cancer Commun (Lond). 39:222019. View Article : Google Scholar
4	de la Mare JA, Contu L, Hunter MC, Moyo B, Sterrenberg JN, Dhanani KC, Mutsvunguma LZ and Edkins AL: Breast cancer: Current developments in molecular approaches to diagnosis and treatment. Recent Pat Anticancer Drug Discov. 9:153–175. 2014. View Article : Google Scholar
5	Shi X, Sun M, Liu H, Yao Y and Song Y: Long non-coding RNAs: A new frontier in the study of human diseases. Cancer Lett. 339:159–166. 2013. View Article : Google Scholar : PubMed/NCBI
6	Tsai MC, Spitale RC and Chang HY: Long intergenic noncoding RNAs: New links in cancer progression. Cancer Res. 71:3–7. 2011. View Article : Google Scholar : PubMed/NCBI
7	Chen X, Dai M, Zhu H, Li J, Huang Z, Liu X, Huang Y, Chen J and Dai S: Evaluation on the diagnostic and prognostic values of long non-coding RNA BLACAT1 in common types of human cancer. Mol Cancer. 16:1602017. View Article : Google Scholar : PubMed/NCBI
8	Dai M, Chen X, Mo S, Li J, Huang Z, Huang S, Xu J, He B, Zou Y, Chen J and Dai S: Meta-signature LncRNAs serve as novel biomarkers for colorectal cancer: Integrated bioinformatics analysis, experimental validation and diagnostic evaluation. Sci Rep. 7:465722017. View Article : Google Scholar : PubMed/NCBI
9	Ye JR, Liu L and Zheng N: Long noncoding RNA bladder cancer associated transcript 1 promotes the proliferation, migration, and invasion of nonsmall cell lung cancer through sponging miR-144. DNA Cell Biol. 36:845–852. 2017. View Article : Google Scholar : PubMed/NCBI
10	Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, Goodnough LH, Helms JA, Farnham PJ, Segal E and Chang HY: Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell. 129:1311–1323. 2007. View Article : Google Scholar : PubMed/NCBI
11	Bhan A, Soleimani M and Mandal SS: Long noncoding RNA and cancer: A new paradigm. Cancer Res. 77:3965–3981. 2017. View Article : Google Scholar : PubMed/NCBI
12	Huang HW, Xie H, Ma X, Zhao F and Gao Y: Upregulation of LncRNA PANDAR predicts poor prognosis and promotes cell proliferation in cervical cancer. Eur Rev Med Pharmacol Sci. 21:4529–4535. 2017.PubMed/NCBI
13	Zang W, Wang T, Huang J, Li M, Wang Y, Du Y, Chen X and Zhao G: Long noncoding RNA PEG10 regulates proliferation and invasion of esophageal cancer cells. Cancer Gene Ther. 22:138–144. 2015. View Article : Google Scholar : PubMed/NCBI
14	Ding X, Zhang S, Li X, Feng C, Huang Q, Wang S, Wang S, Xia W, Yang F, Yin R, et al: Profiling expression of coding genes, long noncoding RNA, and circular RNA in lung adenocarcinoma by ribosomal RNA-depleted RNA sequencing. FEBS Open Bio. 8:544–555. 2018. View Article : Google Scholar : PubMed/NCBI
15	Hu X, Liu Y, Du Y, Cheng T and Xia W: Long non-coding RNA BLACAT1 promotes breast cancer cell proliferation and metastasis by miR-150-5p/CCR2. Cell Biosci. 9:142019. View Article : Google Scholar : PubMed/NCBI
16	Jia YC, Wang JY, Liu YY, Li B, Guo H and Zang AM: LncRNA MAFG-AS1 facilitates the migration and invasion of NSCLC cell via sponging miR-339-5p from MMP15. Cell Biol Int. 43:384–393. 2019. View Article : Google Scholar : PubMed/NCBI
17	Cui S, Yang X, Zhang L, Zhao Y and Yan W: LncRNA MAFG-AS1 promotes the progression of colorectal cancer by sponging miR-147b and activation of NDUFA4. Biochem Biophys Res Commun. 506:251–258. 2018. View Article : Google Scholar : PubMed/NCBI
18	Li H, Zhang GY, Pan CH, Zhang XY and Su XY: LncRNA MAFG-AS1 promotes the aggressiveness of breast carcinoma through regulating miR-339-5p/MMP15. Eur Rev Med Pharmacol Sci. 23:2838–2846. 2019.PubMed/NCBI
19	Wang JS, Liu QH, Cheng XH, Zhang WY and Jin YC: The long noncoding RNA ZFAS1 facilitates bladder cancer tumorigenesis by sponging miR-329. Biomed Pharmacother. 103:174–181. 2018. View Article : Google Scholar : PubMed/NCBI
20	Lu S, Sun Z, Tang L and Chen L: LINC00355 promotes tumor progression in HNSCC by hindering MicroRNA-195-mediated suppression of HOXA10 expression. Mol Ther Nucleic Acids. 19:61–71. 2020. View Article : Google Scholar
21	Xiao H: MiR-7-5p suppresses tumor metastasis of non-small cell lung cancer by targeting NOVA2. Cell Mol Biol Lett. 24:602019. View Article : Google Scholar : PubMed/NCBI
22	Zhang Q, Zheng J and Liu L: The long noncoding RNA PCGEM1 promotes cell proliferation, migration and invasion via targeting the miR-182/FBXW11 axis in cervical cancer. Cancer Cell Int. 19:3042019. View Article : Google Scholar : PubMed/NCBI
23	Chen X, Xu X, Pan B, Zeng K, Xu M, Liu X, He B, Pan Y, Sun H and Wang S: miR-150-5p suppresses tumor progression by targeting VEGFA in colorectal cancer. Aging (Albany NY). 10:3421–3437. 2018. View Article : Google Scholar
24	Lu W, Zhang H, Niu Y, Wu Y, Sun W, Li H, Kong J, Ding K, Shen HM, Wu H, et al: Long non-coding RNA linc00673 regulated non-small cell lung cancer proliferation, migration, invasion and epithelial mesenchymal transition by sponging miR-150-5p. Mol Cancer. 16:1182017. View Article : Google Scholar : PubMed/NCBI
25	Sakr M, Takino T, Sabit H, Nakada M, Li Z and Sato H: miR-150-5p and miR-133a suppress glioma cell proliferation and migration through targeting membrane-type-1 matrix metallo-proteinase. Gene. 587:155–162. 2016. View Article : Google Scholar : PubMed/NCBI
26	Edge SB and Compton CC: The American joint committee on cancer: The 7th edition of the AJCC cancer staging manual and the future of TNM. Ann Surg Oncol. 17:1471–1474. 2010. 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
28	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:D92–D97. 2014. View Article : Google Scholar
29	Sen R, Ghosal S, Das S, Balti S and Chakrabarti J: Competing endogenous RNA: The key to posttranscriptional regulation. ScientificWorldJournal. 2014:8962062014. View Article : Google Scholar : PubMed/NCBI
30	Tay Y, Rinn J and Pandolfi PP: The multilayered complexity of ceRNA crosstalk and competition. Nature. 505:344–352. 2014. View Article : Google Scholar : PubMed/NCBI
31	Khatib A, Solaimuthu B, Yosef MB, Rmaileh AA, Tanna M, Oren G, Frisch MS, Axelrod JH, Lichtenstein M and Shaul YD: The glutathione peroxidase 8 (GPX8)/IL-6/STAT3 axis is essential in maintaining an aggressive breast cancer phenotype. Proc Natl Acad Sci USA. 117:21420–21431. 2020. View Article : Google Scholar : PubMed/NCBI
32	Cataldo A, Romero-Cordoba S, Plantamura I, Cosentino G, Hidalgo-Miranda A, Tagliabue E and Iorio MV: MiR-302b as a combinatorial therapeutic approach to improve cisplatin chemotherapy efficacy in human triple-negative breast cancer. Cancers (Basel). 12:22612020. View Article : Google Scholar
33	Naik SK, Lam EWF, Parija M, Prakash S, Jiramongkol Y, Adhya AK, Parida DK and Mishra SK: NEDDylation negatively regulates ERRβ expression to promote breast cancer tumorigenesis and progression. Cell Death Dis. 11:7032020. View Article : Google Scholar
34	Rodríguez Bautista R, Ortega Gómez A, Hidalgo Miranda A, Zentella Dehesa A, Villarreal-Garza C, Ávila-Moreno F and Arrieta O: Long non-coding RNAs: Implications in targeted diagnoses, prognosis, and improved therapeutic strategies in human non- and triple-negative breast cancer. Clin Epigenetics. 10:882018. View Article : Google Scholar : PubMed/NCBI
35	Dong H, Wang W, Mo S, Liu Q, Chen X, Chen R, Zhang Y, Zou K, Ye M, He X, et al: Long non-coding RNA SNHG14 induces trastuzumab resistance of breast cancer via regulating PABPC1 expression through H3K27 acetylation. J Cell Mol Med. 22:4935–4947. 2018. View Article : Google Scholar : PubMed/NCBI
36	Liu M, Gou L, Xia J, Wan Q, Jiang Y, Sun S, Tang M, He T and Zhang Y: LncRNA ITGB2-AS1 could promote the migration and invasion of breast cancer cells through up-regulating ITGB2. Int J Mol Sci. 19:18662018. View Article : Google Scholar :
37	Gu J, Wang Y, Wang X, Zhou D, Wang X, Zhou M and He Z: Effect of the LncRNA GAS5-MiR-23a-ATG3 axis in regulating autophagy in patients with breast cancer. Cell Physiol Biochem. 48:194–207. 2018. View Article : Google Scholar : PubMed/NCBI
38	Yang F, Shen Y, Zhang W, Jin J, Huang D, Fang H, Ji W, Shi Y, Tang L, Chen W, et al: An androgen receptor negatively induced long non-coding RNA ARNILA binding to miR-204 promotes the invasion and metastasis of triple-negative breast cancer. Cell Death Differ. 25:2209–2220. 2018. View Article : Google Scholar : PubMed/NCBI
39	Schwarzenbacher D, Klec C, Pasculli B, Cerk S, Rinner B, Karbiener M, Ivan C, Barbano R, Ling H, Wulf-Goldenberg A, et al: MiR-1287-5p inhibits triple negative breast cancer growth by interaction with phosphoinositide 3-kinase CB, thereby sensitizing cells for PI3Kinase inhibitors. Breast Cancer Res. 21:202019. View Article : Google Scholar : PubMed/NCBI
40	Li S, Xu JJ and Zhang QY: MicroRNA-132-3p inhibits tumor malignant progression by regulating lysosomal-associated protein transmembrane 4 beta in breast cancer. Cancer Sci. 110:3098–3109. 2019. View Article : Google Scholar : PubMed/NCBI
41	Rettig EM, Tan M, Ling S, Yonescu R, Bishop JA, Fakhry C and Ha PK: MYB rearrangement and clinicopathologic characteristics in head and neck adenoid cystic carcinoma. Laryngoscope. 125:E292–E299. 2015. View Article : Google Scholar : PubMed/NCBI
42	West RB, Kong C, Clarke N, Gilks T, Lipsick JS, Cao H, Kwok S, Montgomery KD, Varma S and Le QT: MYB expression and translocation in adenoid cystic carcinomas and other salivary gland tumors with clinicopathologic correlation. Am J Surg Pathol. 35:92–99. 2011. View Article : Google Scholar :
43	Andersson MK, Afshari MK, Andrén Y, Wick MJ and Stenman G: Targeting the oncogenic transcriptional regulator MYB in adenoid cystic carcinoma by inhibition of IGF1R/AKT signaling. J Natl Cancer Inst. 109:2017. View Article : Google Scholar : PubMed/NCBI
44	Mitra P: Transcription regulation of MYB: A potential and novel therapeutic target in cancer. Ann Transl Med. 6:4432018. View Article : Google Scholar :