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Anti-Cancer Agents in Medicinal Chemistry

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ISSN (Print): 1871-5206
ISSN (Online): 1875-5992

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Research Article

Propolis Extract Regulates microRNA Expression in Glioblastoma and Brain Cancer Stem Cells

Author(s): Ugur C.Yilmaz, Bakiye Goker Bagca*, Emin Karaca, Asude Durmaz, Burak Durmaz, Ayca Aykut, Husniye Kayalar, Cigir Biray Avci, Sunde Yilmaz Susluer, Erhan Pariltay, Cumhur Gunduz and Ozgur Cogulu

Volume 22, Issue 2, 2022

Published on: 04 May, 2021

Page: [378 - 389] Pages: 12

DOI: 10.2174/1871520621666210504082528

Price: $65

Abstract

Background: Grade IV gliomas are classified as glioblastoma (GBM), which is the most malignant brain cancer type. Various genetic and epigenetic mechanisms play a role in the initiation and progression of GBM. MicroRNAs (miRNAs) are small, non-coding RNA molecules that belong to the main epigenetic regulatory RNA class that plays different roles in either physiological or pathological conditions, including GBM pathogenesis regulating expression levels of the target genes. Brain Cancer Stem Cells (BCSCs) are responsible for poor prognosis, including therapy resistance and relapse. Epigenetic regulation mediated by miRNAs is also a critical component of BCSC selfrenewal and differentiation properties. Propolis is a resinous substance collected by honey bees from various plant sources. The flavonoid content of propolis varies depending on the collection region and the extraction method. Although there are studies that include the effects of different originated-propolis on the miRNA expression levels of the glioblastoma cells, the impact on the BCSCs has not been studied yet.

Objective: This study aims to evaluate the effects of propolis obtained from Aydın, a city in western Turkey, on miRNA expression levels of BCSCs and GBM cells.

Methods: Aydin propolis was dissolved in 60% ethanol, and after evaporation, distilled water was added to prepare the propolis stock solution. The flavonoids content of the Aydin propolis was determined by MS Q-TOF analysis. Commercially obtained U87MG and BCSCs were used as in-vitro brain cancer models. Cytotoxic and apoptotic effects of Aydın propolis were determined via WST-1 assay and Annexin V test, respectively. The miRNA expression profile was investigated using the real-time qRT-PCR method. The fold changes were calculated by the2-ΔΔCt method. The miRNA-mRNA-pathway interactions, including significantly altered miRNAs, were determined using different bioinformatics tools and databases.

Results: Quercetin 3-methyl ether was the main component of the Aydin propolis. Aydin propolis did not show significant cytotoxic and apoptotic effects on both GBM and BCSCs up to 2mg/ml concentration. Aydin propolis treatment decreased the expression of nine miRNAs in the U87MG and five miRNAs in the BCSCs. Moreover, ten miRNAs have upregulated from 2.22 to 10.56 folds in propolis treated GBM cells compared to the control group significantly (p<0.05). In the study, the potential roles of two new miRNAs, whose regulations in glioma were not previously defined, were identified. One of them was miR-30d-5p, a novel potential oncomiR in GBM, which was 2.46 folds downregulated in Aydin propolis treated GBM cells. The other one is miR-335-5p, which is a potential tumor suppressor miR in GBM, that was 5.66 folds upregulated in Aydin propolis treated GBM cells. FOXO pathway, its upstream and downstream regulators, and critically neuronal developmental regulators, NOTCH and WNT pathways, were determined as the most deregulated pathways in Aydin propolis treated cells.

Conclusion: The determination of the anti-cancer effect of Aydın propolis on the miRNA expression of GBM, especially on cancer stem cells, may contribute to the elucidation of brain cancer genetics by supporting further analyses.

Keywords: Gene expression, in vitro cell culture, microRNA, propolis, miRNA-mRNA-pathway interactions, glioblastoma.

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[1]
Wesseling, P.; Capper, D. WHO 2016 Classification of gliomas. Neuropathol. Appl. Neurobiol., 2018, 44(2), 139-150.
[http://dx.doi.org/10.1111/nan.12432] [PMID: 28815663]
[2]
Mesfin, F.B.; Al-Dhahir, M.A. Cancer, Brain, Gliomas; StatPearls Publishing: Treasure Island, FL, USA, 2018.
[3]
Grech, N.; Dalli, T.; Mizzi, S.; Meilak, L.; Calleja, N.; Zrinzo, A. Rising incidence of glioblastoma multiforme in a well-defined population. Cureus, 2020, 12(5)e8195
[http://dx.doi.org/10.7759/cureus.8195] [PMID: 32572354]
[4]
Kanehisa, M.; Sato, Y.; Furumichi, M.; Morishima, K.; Tanabe, M. New approach for understanding genome variations in KEGG. Nucleic Acids Res., 2019, 47(D1), D590-D595.
[http://dx.doi.org/10.1093/nar/gky962] [PMID: 30321428]
[5]
Li, P.; Wu, M. Epigenetic mechanisms of glioblastoma.Glioblastoma, De Vleeschouwer, S; Exon Publications: Australia, 2017. Chapter 3
[http://dx.doi.org/10.15586/codon.glioblastoma.2017.ch3.]
[6]
Lathia, J.D.; Mack, S.C.; Mulkearns-Hubert, E.E.; Valentim, C.L.L.; Rich, J.N. Cancer stem cells in glioblastoma. Genes Dev., 2015, 29(12), 1203-1217.
[http://dx.doi.org/10.1101/gad.261982.115] [PMID: 26109046]
[7]
Ishida, Y.; Gao, R.; Shah, N.; Bhargava, P.; Furune, T.; Kaul, S.C.; Terao, K.; Wadhwa, R. Anticancer activity in honeybee propolis: Functional insights to the role of caffeic acid phenethyl ester and its complex with γ-cyclodextrin. Integr. Cancer Ther., 2018, 17(3), 867-873.
[http://dx.doi.org/10.1177/1534735417753545] [PMID: 29390900]
[8]
Piwecka, M.; Rolle, K.; Belter, A.; Barciszewska, A.M.; Żywicki, M.; Michalak, M.; Nowak, S.; Naskręt-Barciszewska, M.Z.; Barciszewski, J. Comprehensive analysis of microRNA expression profile in malignant glioma tissues. Mol. Oncol., 2015, 9(7), 1324-1340.
[http://dx.doi.org/10.1016/j.molonc.2015.03.007] [PMID: 25864039]
[9]
Yilmaz, U.C.; Bagca, B.G.; Karaca, E.; Durmaz, A.; Durmaz, B.; Aykut, A.; Kayalar, H.; Avci, C.B.; Susluer, S.Y.; Gunduz, C.; Cogulu, O. Evaluation of the miRNA profiling and effectiveness of the propolis on B-cell acute lymphoblastic leukemia cell line. Biomed. Pharmacother., 2016, 84, 1266-1273.
[http://dx.doi.org/10.1016/j.biopha.2016.10.056]
[10]
Licursi, V.; Conte, F.; Fiscon, G.; Paci, P. MIENTURNET: An interactive web tool for microRNA-target enrichment and network-based analysis. BMC Bioinformatics, 2019, 20(1), 545.
[http://dx.doi.org/10.1186/s12859-019-3105-x] [PMID: 31684860]
[11]
Kehl, T.; Kern, F.; Backes, C.; Fehlmann, T.; Stöckel, D.; Meese, E.; Lenhof, H.P.; Keller, A. miRPathDB 2.0: A novel release of the miRNA pathway dictionary database. Nucleic Acids Res., 2020, 48(D1), D142-D147.
[http://dx.doi.org/10.1093/nar/gkz1022] [PMID: 31691816]
[12]
Pian, C.; Zhang, G.; Gao, L.; Fan, X.; Li, F. miR+Pathway: The integration and visualization of miRNA and KEGG pathways. Brief. Bioinform., 2020, 21(2), 699-708.
[http://dx.doi.org/10.1093/bib/bby128] [PMID: 30649247]
[13]
Sun, S.; Liu, M.; He, J.; Li, K.; Zhang, X.; Yin, G. Identification and determination of seven phenolic acids in Brazilian green propolis by UPLC-ESI-QTOF-MS and HPLC. Molecules, 2019, 24(9)E1791
[http://dx.doi.org/10.3390/molecules24091791] [PMID: 31075821]
[14]
Saftić, L. Peršurić, Ž.; Kraljević Pavelić, S. LC-QQQ and LC-QTOF MS methods for comprehensive detection of potential allergens in various propolis extracts. Eur. Food Res. Technol., 2019, 245, 1981-1995.
[http://dx.doi.org/10.1007/s00217-019-03308-x]
[15]
Cisilotto, J.; Sandjo, L.P.; Faqueti, L.G.; Fernandes, H.; Joppi, D.; Biavatti, M.W.; Creczynski-Pasa, T.B. Cytotoxicity mechanisms in melanoma cells and UPLC-QTOF/MS2 chemical characterization of two Brazilian stingless bee propolis: Uncommon presence of piperidinic alkaloids. J. Pharm. Biomed. Anal., 2018, 149, 502-511.
[http://dx.doi.org/10.1016/j.jpba.2017.11.038] [PMID: 29197804]
[16]
Saftić, L.; Peršurić, Ž.; Fornal, E.; Pavlešić, T.; Kraljević Pavelić, S. Targeted and untargeted LC-MS polyphenolic profiling and chemometric analysis of propolis from different regions of Croatia. J. Pharm. Biomed. Anal., 2019, 165, 162-172.
[http://dx.doi.org/10.1016/j.jpba.2018.11.061] [PMID: 30551071]
[17]
Kocot, J.; Kiełczykowska, M.; Luchowska-Kocot, D.; Kurzepa, J.; Musik, I. Antioxidant potential of propolis, bee pollen, and royal jelly: Possible medical application. Oxid. Med. Cell. Longev., 2018, 20187074209
[http://dx.doi.org/10.1155/2018/7074209] [PMID: 29854089]
[18]
Szulc, J.; Machnowski, W.; Kowalska, S.; Jachowicz, A.; Ruman, T.; Steglińska, A.; Gutarowska, B. Beeswax-modified textiles: Method of preparation and assessment of antimicrobial properties. Polymers (Basel), 2020, 12(2)E344
[http://dx.doi.org/10.3390/polym12020344] [PMID: 32033396]
[19]
Abubakar, M.B.; Abdullah, W.Z.; Sulaiman, S.A.; Suen, A.B. A review of molecular mechanisms of the anti-leukemic effects of phenolic compounds in honey. Int. J. Mol. Sci., 2012, 13(11), 15054-15073.
[http://dx.doi.org/10.3390/ijms131115054] [PMID: 23203111]
[20]
Devi, A.; Jangir, J.; Anu-Appaiah, K.A. Chemical characterization complemented with chemometrics for the botanical origin identification of unifloral and multifloral honeys from India. Food Res. Int., 2018, 107, 216-226.
[http://dx.doi.org/10.1016/j.foodres.2018.02.017] [PMID: 29580480]
[21]
Borawska, M.H.; Naliwajko, S.K.; Moskwa, J.; Markiewicz-Żukowska, R.; Puścion-Jakubik, A.; Soroczyńska, J. Anti-proliferative and anti-migration effects of Polish propolis combined with Hypericum perforatum L. on glioblastoma multiforme cell line U87MG. BMC Complement. Altern. Med., 2016, 16, 367.
[http://dx.doi.org/10.1186/s12906-016-1351-2] [PMID: 27647142]
[22]
Borges, K.S.; Brassesco, M.S.; Scrideli, C.A.; Soares, A.E.E.; Tone, L.G. Antiproliferative effects of Tubi-bee propolis in glioblastoma cell lines. Genet. Mol. Biol., 2011, 34(2), 310-314.
[http://dx.doi.org/10.1590/S1415-47572011000200024] [PMID: 21734835]
[23]
Zhao, S.; Jiang, Y.; Zhao, J.; Li, H.; Yin, X.; Wang, Y.; Xie, Y.; Chen, X.; Lu, J.; Dong, Z.; Liu, K. Quercetin-3-methyl ether inhibits esophageal carcinogenesis by targeting the AKT/mTOR/p70S6K and MAPK pathways. Mol. Carcinog., 2018, 57(11), 1540-1552.
[http://dx.doi.org/10.1002/mc.22876] [PMID: 30035335]
[24]
Cao, L.; Yang, Y.; Ye, Z.; Lin, B.; Zeng, J.; Li, C.; Liang, T.; Zhou, K.; Li, J. Quercetin 3 methyl ether suppresses human breast cancer stem cell formation by inhibiting the Notch1 and PI3K/Akt signaling pathways. Int. J. Mol. Med., 2018, 42(3), 1625-1636.
[http://dx.doi.org/10.3892/ijmm.2018.3741] [PMID: 29956731]
[25]
Hung, J.Y.; Chang, W.A.; Tsai, Y.M.; Hsu, Y.L.; Chiang, H.H.; Chou, S.H.; Huang, M.S.; Kuo, P.L. Tricetin, a dietary flavonoid, suppresses benzo(a)pyrene induced human non small cell lung cancer bone metastasis. Int. J. Oncol., 2015, 46(5), 1985-1993.
[http://dx.doi.org/10.3892/ijo.2015.2915] [PMID: 25738754]
[26]
Chao, R.; Chow, J.M.; Hsieh, Y.H.; Chen, C.K.; Lee, W.J.; Hsieh, F.K.; Yu, N.Y.; Chou, M.C.; Cheng, C.W.; Yang, S.F.; Chien, M.H. Tricetin suppresses the migration/invasion of human glioblastoma multiforme cells by inhibiting matrix metalloproteinase-2 through modulation of the expression and transcriptional activity of specificity protein 1. Expert Opin. Ther. Targets, 2015, 19(10), 1293-1306.
[http://dx.doi.org/10.1517/14728222.2015.1075509] [PMID: 26245494]
[27]
Aroui, S.; Dardevet, L.; Najlaoui, F.; Kammoun, M.; Laajimi, A.; Fetoui, H.; De Waard, M.; Kenani, A. PTEN-regulated AKT/FoxO3a/Bim signaling contributes to human cell glioblastoma apoptosis by platinum-maurocalcin conjugate. Int. J. Biochem. Cell Biol., 2016, 77(Pt A), 15-22.
[http://dx.doi.org/10.1016/j.biocel.2016.05.013] [PMID: 27210502]
[28]
Firat, E.; Niedermann, G.; Fox, O. FoxO proteins or loss of functional p53 maintain stemness of glioblastoma stem cells and survival after ionizing radiation plus PI3K/mTOR inhibition. Oncotarget, 2016, 7(34), 54883-54896.
[http://dx.doi.org/10.18632/oncotarget.10702] [PMID: 27448972]
[29]
Bazzoni, R.; Bentivegna, A. Role of notch signaling pathway in glioblastoma pathogenesis. Cancers (Basel), 2019, 11(3)E292
[http://dx.doi.org/10.3390/cancers11030292] [PMID: 30832246]
[30]
Brafman, D.; Willert, K. Wnt/β-catenin signaling during early vertebrate neural development. Dev. Neurobiol., 2017, 77(11), 1239-1259.
[http://dx.doi.org/10.1002/dneu.22517] [PMID: 28799266]
[31]
Iacona, J.R.; Lutz, C.S. miR-146a-5p: Expression, regulation, and functions in cancer. Wiley Interdiscip. Rev. RNA, 2019, 10(4)e1533
[http://dx.doi.org/10.1002/wrna.1533] [PMID: 30895717]
[32]
Kogo, R.; Mimori, K.; Tanaka, F.; Komune, S.; Mori, M. Clinical significance of miR-146a in gastric cancer cases. Clin. Cancer Res., 2011, 17(13), 4277-4284.
[http://dx.doi.org/10.1158/1078-0432.CCR-10-2866] [PMID: 21632853]
[33]
Xu, B.; Wang, N.; Wang, X.; Tong, N.; Shao, N.; Tao, J.; Li, P.; Niu, X.; Feng, N.; Zhang, L.; Hua, L.; Wang, Z.; Chen, M. MiR-146a suppresses tumor growth and progression by targeting EGFR pathway and in a p-ERK-dependent manner in castration-resistant prostate cancer. Prostate, 2012, 72(11), 1171-1178.
[http://dx.doi.org/10.1002/pros.22466] [PMID: 22161865]
[34]
Hurst, D.R.; Edmonds, M.D.; Scott, G.K.; Benz, C.C.; Vaidya, K.S.; Welch, D.R. Breast cancer metastasis suppressor 1 up-regulates miR-146, which suppresses breast cancer metastasis. Cancer Res., 2009, 69(4), 1279-1283.
[http://dx.doi.org/10.1158/0008-5472.CAN-08-3559] [PMID: 19190326]
[35]
Chen, G.; Umelo, I.A.; Lv, S.; Teugels, E.; Fostier, K.; Kronenberger, P.; Dewaele, A.; Sadones, J.; Geers, C.; De Grève, J. miR-146a inhibits cell growth, cell migration and induces apoptosis in non-small cell lung cancer cells. PLoS One, 2013, 8(3)e60317
[http://dx.doi.org/10.1371/journal.pone.0060317] [PMID: 23555954]
[36]
Ali, S.; Ahmad, A.; Aboukameel, A.; Ahmed, A.; Bao, B.; Banerjee, S.; Philip, P.A.; Sarkar, F.H. Deregulation of miR-146a expression in a mouse model of pancreatic cancer affecting EGFR signaling. Cancer Lett., 2014, 351(1), 134-142.
[http://dx.doi.org/10.1016/j.canlet.2014.05.013] [PMID: 24839931]
[37]
Peta, E.; Cappellesso, R.; Masi, G.; Sinigaglia, A.; Trevisan, M.; Grassi, A.; Di Camillo, B.; Vassarotto, E.; Fassina, A.; Palù, G.; Barzon, L. Down-regulation of microRNA-146a is associated with high-risk human papillomavirus infection and epidermal growth factor receptor overexpression in penile squamous cell carcinoma. Hum. Pathol., 2017, 61, 33-40.
[http://dx.doi.org/10.1016/j.humpath.2016.10.019] [PMID: 27818285]
[38]
Li, Y.; Vandenboom, T.G., II; Wang, Z.; Kong, D.; Ali, S.; Philip, P.A.; Sarkar, F.H. miR-146a suppresses invasion of pancreatic cancer cells. Cancer Res., 2010, 70(4), 1486-1495.
[http://dx.doi.org/10.1158/0008-5472.CAN-09-2792] [PMID: 20124483]
[39]
Borgdorff, V.; Lleonart, M.E.; Bishop, C.L.; Fessart, D.; Bergin, A.H.; Overhoff, M.G.; Beach, D.H. Multiple microRNAs rescue from Ras-induced senescence by inhibiting p21(Waf1/Cip1). Oncogene, 2010, 29(15), 2262-2271.
[http://dx.doi.org/10.1038/onc.2009.497] [PMID: 20101223]
[40]
Chang, Y.L.; Ho, B.C.; Sher, S.; Yu, S.L.; Yang, P.C. miR-146a and miR-370 coordinate enterovirus 71-induced cell apoptosis through targeting SOS1 and GADD45β. Cell. Microbiol., 2015, 17(6), 802-818.
[http://dx.doi.org/10.1111/cmi.12401] [PMID: 25469565]
[41]
Li, Y.L.; Wang, J.; Zhang, C.Y.; Shen, Y.Q.; Wang, H.M.; Ding, L.; Gu, Y.C.; Lou, J.T.; Zhao, X.T.; Ma, Z.L.; Jin, Y.X. MiR-146a-5p inhibits cell proliferation and cell cycle progression in NSCLC cell lines by targeting CCND1 and CCND2. Oncotarget, 2016, 7(37), 59287-59298.
[http://dx.doi.org/10.18632/oncotarget.11040] [PMID: 27494902]
[42]
Wang, N.; Tan, H.Y.; Feng, Y.G.; Zhang, C.; Chen, F.; Feng, Y. MicroRNA-23a in human cancer: Its roles, mechanisms and therapeutic relevance. Cancers (Basel), 2018, 11(1), 7.
[http://dx.doi.org/10.3390/cancers11010007] [PMID: 30577536]
[43]
Lou, W.; Ding, B.; Xu, L.; Fan, W. Construction of potential glioblastoma multiforme-related miRNA-mRNA regulatory network. Front. Mol. Neurosci., 2019, 12, 66.
[http://dx.doi.org/10.3389/fnmol.2019.00066] [PMID: 30971889]
[44]
Xu, W.; Liu, M.; Peng, X.; Zhou, P.; Zhou, J.; Xu, K.; Xu, H.; Jiang, S. miR-24-3p and miR-27a-3p promote cell proliferation in glioma cells via cooperative regulation of MXI1. Int. J. Oncol., 2013, 42(2), 757-766.
[http://dx.doi.org/10.3892/ijo.2012.1742] [PMID: 23254855]
[45]
Chen, P.H.; Cheng, C.H.; Shih, C.M.; Ho, K.H.; Lin, C.W.; Lee, C.C.; Liu, A.J.; Chang, C.K.; Chen, K.C. The inhibition of microRNA-128 on IGF-1-activating mTOR signaling involves in temozolomide-induced glioma cell apoptotic death. PLoS One, 2016, 11(11)e0167096
[http://dx.doi.org/10.1371/journal.pone.0167096] [PMID: 27893811]
[46]
Rooj, A.K.; Mineo, M.; Godlewski, J. MicroRNA and extracellular vesicles in glioblastoma: Small but powerful. Brain Tumor Pathol., 2016, 33(2), 77-88.
[http://dx.doi.org/10.1007/s10014-016-0259-3] [PMID: 26968172]
[47]
Xia, L.; Li, D.; Lin, C.; Ou, S.; Li, X.; Pan, S. Comparative study of joint bioinformatics analysis of underlying potential of ‘neurimmiR’, miR-212-3P/miR-132-3P, being involved in epilepsy and its emerging role in human cancer. Oncotarget, 2017, 8(25), 40668-40682.
[http://dx.doi.org/10.18632/oncotarget.16541] [PMID: 28380454]
[48]
Jacob, H.; Stanisavljevic, L.; Storli, K.E.; Hestetun, K.E.; Dahl, O.; Myklebust, M.P. Identification of a sixteen-microRNA signature as prognostic biomarker for stage II and III colon cancer. Oncotarget, 2017, 8(50), 87837-87847.
[http://dx.doi.org/10.18632/oncotarget.21237] [PMID: 29152124]
[49]
Kumar, M.; Lu, Z.; Takwi, A.A.L.; Chen, W.; Callander, N.S.; Ramos, K.S.; Young, K.H.; Li, Y. Negative regulation of the tumor suppressor p53 gene by microRNAs. Oncogene, 2011, 30(7), 843-853.
[http://dx.doi.org/10.1038/onc.2010.457] [PMID: 20935678]
[50]
Wu, J.; Zheng, C.; Fan, Y.; Zeng, C.; Chen, Z.; Qin, W.; Zhang, C.; Zhang, W.; Wang, X.; Zhu, X.; Zhang, M.; Zen, K.; Liu, Z. Downregulation of microRNA-30 facilitates podocyte injury and is prevented by glucocorticoids. J. Am. Soc. Nephrol., 2014, 25(1), 92-104.
[http://dx.doi.org/10.1681/ASN.2012111101] [PMID: 24029422]
[51]
Zhao, J.J.; Lin, J.; Zhu, D.; Wang, X.; Brooks, D.; Chen, M.; Chu, Z.B.; Takada, K.; Ciccarelli, B.; Admin, S.; Tao, J.; Tai, Y.T.; Treon, S.; Pinkus, G.; Kuo, W.P.; Hideshima, T.; Bouxsein, M.; Munshi, N.; Anderson, K.; Carrasco, R. miR-30-5p functions as a tumor suppressor and novel therapeutic tool by targeting the oncogenic Wnt/β-catenin/BCL9 pathway. Cancer Res., 2014, 74(6), 1801-1813.
[http://dx.doi.org/10.1158/0008-5472.CAN-13-3311-T] [PMID: 24599134]
[52]
Cheng, Z.; Shu, H.; Cui, Y.; Zhang, Q.; Zhao, B.; Pan, D.; Chao, Q.; Wang, D. MiR-424-5p inhibits proliferation, invasion and promotes apoptosis and predicts good prognosis in glioma by directly targeting BFAR. Pathol. Oncol. Res., 2020, 26(4), 2327-2335.
[http://dx.doi.org/10.1007/s12253-020-00831-1] [PMID: 32483702]
[53]
Wang, L.; Ma, J.; Wang, X.; Peng, F.; Chen, X.; Zheng, B.; Wang, C.; Dai, Z.; Ai, J.; Zhao, S. Kaiso (ZBTB33) downregulation by MiRNA-181a inhibits cell proliferation, invasion, and the epithelial-mesenchymal transition in glioma cells. Cell. Physiol. Biochem., 2018, 48(3), 947-958.
[http://dx.doi.org/10.1159/000491963] [PMID: 30036882]
[54]
Zheng, Y.; Lu, S.; Xu, Y.; Zheng, J. Long non-coding RNA AGAP2-AS1 promotes the proliferation of glioma cells by sponging miR-15a/b-5p to upregulate the expression of HDGF and activating Wnt/β-catenin signaling pathway. Int. J. Biol. Macromol., 2019, 128, 521-530.
[http://dx.doi.org/10.1016/j.ijbiomac.2019.01.121] [PMID: 30684575]
[55]
Chen, Y.; Deng, X.; Chen, W.; Shi, P.; Lian, M.; Wang, H.; Wang, K.; Qian, D.; Xiao, D.; Long, H. Silencing of microRNA-708 promotes cell growth and epithelial-to-mesenchymal transition by activating the SPHK2/AKT/β-catenin pathway in glioma. Cell Death Dis., 2019, 10(6), 448.
[http://dx.doi.org/10.1038/s41419-019-1671-5] [PMID: 31171769]
[56]
Zhang, H.; Qin, D.; Jiang, Z.; Zhang, J. SNHG9/miR-199a-5p/Wnt2 axis regulates cell growth and aerobic glycolysis in glioblastoma. J. Neuropathol. Exp. Neurol., 2019, 78(10), 939-948.
[http://dx.doi.org/10.1093/jnen/nlz078] [PMID: 31504670]
[57]
Chi, G.; Yang, F.; Xu, D.; Liu, W. Silencing hsa_circ_PVT1 (circPVT1) suppresses the growth and metastasis of glioblastoma multiforme cells by up-regulation of miR-199a-5p. Artif. Cells Nanomed. Biotechnol., 2020, 48(1), 188-196.
[http://dx.doi.org/10.1080/21691401.2019.1699825] [PMID: 31865777]
[58]
Luo, W.; Yan, D.; Song, Z.; Zhu, X.; Liu, X.; Li, X.; Zhao, S. miR-126-3p sensitizes glioblastoma cells to temozolomide by inactivating Wnt/β-catenin signaling via targeting SOX2. Life Sci., 2019, 226, 98-106.
[http://dx.doi.org/10.1016/j.lfs.2019.04.023] [PMID: 30980849]
[59]
Kurogi, R.; Nakamizo, A.; Suzuki, S.O.; Mizoguchi, M.; Yoshimoto, K.; Amano, T.; Amemiya, T.; Takagishi, S.; Iihara, K. Inhibition of glioblastoma cell invasion by hsa-miR-145-5p and hsa-miR-31-5p co-overexpression in human mesenchymal stem cells. J. Neurosurg., 2018, 130(1), 44-55.
[http://dx.doi.org/10.3171/2017.8.JNS1788] [PMID: 29521593]
[60]
Jiang, H.; Jin, C.; Liu, J.; Hua, D.; Zhou, F.; Lou, X.; Zhao, N.; Lan, Q.; Huang, Q.; Yoon, J-G.; Zheng, S.; Lin, B. Next generation sequencing analysis of miRNAs: MiR-127-3p inhibits glioblastoma proliferation and activates TGF-β signaling by targeting SKI. OMICS, 2014, 18(3), 196-206.
[http://dx.doi.org/10.1089/omi.2013.0122] [PMID: 24517116]
[61]
Qin, W.; Rong, X.; Dong, J.; Yu, C.; Yang, J. miR-142 inhibits the migration and invasion of glioma by targeting Rac1. Oncol. Rep., 2017, 38(3), 1543-1550.
[http://dx.doi.org/10.3892/or.2017.5816] [PMID: 28714015]
[62]
Lee, Y.Y.; Yarmishyn, A.A.; Wang, M.L.; Chen, H.Y.; Chiou, S.H.; Yang, Y.P.; Lin, C.F.; Huang, P.I.; Chen, Y.W.; Ma, H.I.; Chen, M.T. MicroRNA-142-3p is involved in regulation of MGMT expression in glioblastoma cells. Cancer Manag. Res., 2018, 10, 775-785.
[http://dx.doi.org/10.2147/CMAR.S157261] [PMID: 29695934]
[63]
Zhang, L-L.; Zhang, L-F.; Guo, X-H.; Zhang, D-Z.; Yang, F.; Fan, Y-Y. Downregulation of miR-335-5p by long noncoding RNA ZEB1-AS1 in gastric cancer promotes tumor proliferation and invasion. DNA Cell Biol., 2018, 37(1), 46-52.
[http://dx.doi.org/10.1089/dna.2017.3926] [PMID: 29215918]
[64]
Song, H.; Zhang, Y.; Liu, N.; Zhao, S.; Kong, Y.; Yuan, L. miR-92a-3p exerts various effects in glioma and glioma stem-like cells specifically targeting CDH1/β-catenin and Notch-1/Akt signaling pathways. Int. J. Mol. Sci., 2016, 17(11)E1799
[http://dx.doi.org/10.3390/ijms17111799] [PMID: 27801803]
[65]
Floyd, D.H.; Zhang, Y.; Dey, B.K.; Kefas, B.; Breit, H.; Marks, K.; Dutta, A.; Herold-Mende, C.; Synowitz, M.; Glass, R.; Abounader, R.; Purow, B.W. Novel anti-apoptotic microRNAs 582-5p and 363 promote human glioblastoma stem cell survival via direct inhibition of caspase 3, caspase 9, and Bim. PLoS One, 2014, 9(5)e96239
[http://dx.doi.org/10.1371/journal.pone.0096239] [PMID: 24805821]
[66]
Patterson, M.; Gaeta, X.; Loo, K.; Edwards, M.; Smale, S.; Cinkornpumin, J.; Xie, Y.; Listgarten, J.; Azghadi, S.; Douglass, S.M.; Pellegrini, M.; Lowry, W.E. let-7 miRNAs can act through notch to regulate human gliogenesis. Stem Cell Reports, 2014, 3(5), 758-773.
[http://dx.doi.org/10.1016/j.stemcr.2014.08.015] [PMID: 25316189]
[67]
Liu, J.; Liu, S.; Deng, X.; Rao, J.; Huang, K.; Xu, G.; Wang, X. MicroRNA-582-5p suppresses non-small cell lung cancer cells growth and invasion via downregulating Notch1. PLoS One, 2019, 14(6)e0217652
[http://dx.doi.org/10.1371/journal.pone.0217652] [PMID: 31170211]
[68]
Sato, T.; Kataoka, K.; Ito, Y.; Yokoyama, S.; Inui, M.; Mori, M.; Takahashi, S.; Akita, K.; Takada, S.; Ueno-Kudoh, H.; Asahara, H. Lin28a/let-7 pathway modulates the Hox code via Polycomb regulation during axial patterning in vertebrates. eLife, 2020, 9e53608
[http://dx.doi.org/10.7554/eLife.53608] [PMID: 32479258]
[69]
Wang, W.; Zhang, A.; Hao, Y.; Wang, G.; Jia, Z. The emerging role of miR-19 in glioma. J. Cell. Mol. Med., 2018, 22(10), 4611-4616.
[http://dx.doi.org/10.1111/jcmm.13788] [PMID: 30073755]
[70]
Ivo D’Urso, P.; Fernando D’Urso, O.; Damiano Gianfreda, C.; Mezzolla, V.; Storelli, C.; Marsigliante, S. miR-15b and miR-21 as circulating biomarkers for diagnosis of glioma. Curr. Genomics, 2015, 16(5), 304-311.
[http://dx.doi.org/10.2174/1389202916666150707155610] [PMID: 27047250]
[71]
Chen, H.S.; Lu, A.Q.; Yang, P.Y.; Liang, J.; Wei, Y.; Shang, Y.W.; Li, Q. MicroRNA-28-5p regulates glioma cell proliferation, invasion and migration by targeting SphK1. Eur. Rev. Med. Pharmacol. Sci., 2019, 23(15), 6621-6628.
[http://dx.doi.org/10.26355/eurrev_201908_18551] [PMID: 31378904]
[72]
Xu, H.; Hu, Y.; Qiu, W. Potential mechanisms of microRNA-129-5p in inhibiting cell processes including viability, proliferation, migration and invasiveness of glioblastoma cells U87 through targeting FNDC3B. Biomed. Pharmacother., 2017, 87, 405-411.
[http://dx.doi.org/10.1016/j.biopha.2016.12.100] [PMID: 28068630]
[73]
Feng, L.; Ma, J.; Ji, H.; Liu, Y.; Hu, W. miR-330-5p suppresses glioblastoma cell proliferation and invasiveness through targeting ITGA5. Biosci. Rep., 2017, 37(3)BSR20170019
[http://dx.doi.org/10.1042/BSR20170019] [PMID: 28336765]
[74]
Ma, X.L.; Shang, F.; Ni, W.; Zhu, J.; Luo, B.; Zhang, Y.Q. MicroRNA-338-5p plays a tumor suppressor role in glioma through inhibition of the MAPK-signaling pathway by binding to FOXD1. J. Cancer Res. Clin. Oncol., 2018, 144(12), 2351-2366.
[http://dx.doi.org/10.1007/s00432-018-2745-y] [PMID: 30225541]
[75]
Wang, Y.; Wei, Y.; Tong, H.; Chen, L.; Fan, Y.; Ji, Y.; Jia, W.; Liu, D.; Wang, G. MiR-302c-3p suppresses invasion and proliferation of glioma cells via down-regulating Metadherin (MTDH) expression. Cancer Biol. Ther., 2015, 16(9), 1308-1315.
[http://dx.doi.org/10.1080/15384047.2015.1056413] [PMID: 26176806]
[76]
Zhang, J.; Deng, M.; Tong, H.; Xue, W.; Guo, Y.; Wang, J.; Chen, L.; Wang, S. A novel miR-7156-3p-HOXD13 axis modulates glioma progression by regulating tumor cell stemness. Int. J. Biol. Sci., 2020, 16(16), 3200-3209.
[http://dx.doi.org/10.7150/ijbs.51293] [PMID: 33162825]
[77]
Xu, D.; Chi, G.; Xu, D. Transcriptional regulation of miR-483-3p mediated by IL-6/STAT3 axis promoted epithelial-mesenchymal transition and tumor stemness in glioma. Aging (Albany NY), 2020, 12. [Ahead of Print]
[http://dx.doi.org/10.18632/aging.103761] [PMID: 33154190]
[78]
Sun, T.; Xu, Y.J.; Jiang, S.Y.; Xu, Z.; Cao, B.Y.; Sethi, G.; Zeng, Y.Y.; Kong, Y.; Mao, X.L. Suppression of the USP10/CCND1 axis induces glioblastoma cell apoptosis. Acta Pharmacol. Sin., 2021, 42(8), 1338-1346.
[http://dx.doi.org/10.1038/s41401-020-00551-x] [PMID: 33184448]
[79]
Zhang, D.; Dai, D.; Zhou, M.; Li, Z.; Wang, C.; Lu, Y.; Li, Y.; Wang, J. Inhibition of cyclin D1 expression in human glioblastoma cells is associated with increased temozolomide chemosensitivity. Cell. Physiol. Biochem., 2018, 51(6), 2496-2508.
[http://dx.doi.org/10.1159/000495920] [PMID: 30562739]
[80]
Ye, J.; Zhu, J.; Chen, H.; Qian, J.; Zhang, L.; Wan, Z.; Chen, F.; Sun, S.; Li, W.; Luo, C. A novel lncRNA-LINC01116 regulates tumorigenesis of glioma by targeting VEGFA. Int. J. Cancer, 2020, 146(1), 248-261.
[http://dx.doi.org/10.1002/ijc.32483] [PMID: 31144303]
[81]
Treps, L.; Perret, R.; Edmond, S.; Ricard, D.; Gavard, J. Glioblastoma stem-like cells secrete the pro-angiogenic VEGF-A factor in extracellular vesicles. J. Extracell. Vesicles, 2017, 6(1)1359479
[http://dx.doi.org/10.1080/20013078.2017.1359479] [PMID: 28815003]

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