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Endocrine, Metabolic & Immune Disorders - Drug Targets


ISSN (Print): 1871-5303
ISSN (Online): 2212-3873

Review Article (Mini-Review)

Circulating MicroRNAs as Potential Biomarkers in Glioma: A Mini-Review

Author(s): Lavanya Choppavarapu and Sibin M. Kandi*

Volume 21 , Issue 2 , 2021

Published on: 30 July, 2020

Page: [195 - 202] Pages: 8

DOI: 10.2174/1871530320666200730230422

Price: $65


Glioma comprises of a group of heterogeneous brain tumors originating from glial cells. Primary glioblastoma is among the most common glial cells that have a characteristic clinical and molecular profile. Advancement in the field of cancer research and inventions of various clinical methodologies could not improve the median survival of this deadly tumor from 12 months. The development of a non-invasive prognostic biomarker in blood would be a revolution in the diagnosis and therapeutic monitoring of this tumor. Extracellular vesicles (Evs) are released from the tumor microenvironment into the blood, which contains the genetic material that represents the genetics of tumor cells. It is also seen that these Evs contain a variety of RNA populations, including miRNAs. Several studies identified that circulating cell-free miRNAs, either free or present in Evs, could be considered as a potential biomarker in early diagnosis and prognosis of glioblastoma. Micro RNA studies in glioblastoma have found to be promising, as it reveals the biological pathway behind pathogenesis and helps in predicting the treatment targets. The literature says that various treatment methods change the type and quantity of miRNAs in biological fluids, which can be used to monitor the therapy. This review paper focuses on the role of circulating miRNAs as potential biomarkers in the diagnosis and clinical management of glioma patients.

Keywords: Glioblastoma, circulatory miRNA, diagnosis, biomarker, glioma, review.

Graphical Abstract
Arroyo, J.D.; Chevillet, J.R.; Kroh, E.M.; Ruf, I.K.; Pritchard, C.C.; Gibson, D.F.; Mitchell, P.S.; Bennett, C.F.; Pogosova-Agadjanyan, E.L.; Stirewalt, D.L.; Tait, J.F.; Tewari, M. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc. Natl. Acad. Sci. USA, 2011, 108(12), 5003-5008.
[] [PMID: 21383194]
Wang, K.; Zhang, S.; Weber, J.; Baxter, D.; Galas, D.J. Export of microRNAs and microRNA-protective protein by mammalian cells. Nucleic Acids Res., 2010, 38(20), 7248-7259.
[] [PMID: 20615901]
Turchinovich, A.; Weiz, L.; Langheinz, A.; Burwinkel, B. Characterization of extracellular circulating microRNA. Nucleic Acids Res., 2011, 39(16), 7223-7233.
[] [PMID: 21609964]
Chen, X.; Ba, Y.; Ma, L.; Cai, X.; Yin, Y.; Wang, K.; Guo, J.; Zhang, Y.; Chen, J.; Guo, X.; Li, Q.; Li, X.; Wang, W.; Zhang, Y.; Wang, J.; Jiang, X.; Xiang, Y.; Xu, C.; Zheng, P.; Zhang, J.; Li, R.; Zhang, H.; Shang, X.; Gong, T.; Ning, G.; Wang, J.; Zen, K.; Zhang, J.; Zhang, C.Y. Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res., 2008, 18(10), 997-1006.
[] [PMID: 18766170]
Lee, Y.; Ahn, C.; Han, J.; Choi, H.; Kim, J.; Yim, J.; Lee, J.; Provost, P.; Rådmark, O.; Kim, S.; Kim, V.N. The nuclear RNase III Drosha initiates microRNA processing. Nature, 2003, 425(6956), 415-419.
[] [PMID: 14508493]
Zeng, Y.; Yi, R.; Cullen, B.R. Recognition and cleavage of primary microRNA precursors by the nuclear processing enzyme Drosha. EMBO J., 2005, 24(1), 138-148.
[] [PMID: 15565168]
Lund, E.; Güttinger, S.; Calado, A.; Dahlberg, J.E.; Kutay, U. Nuclear export of microRNA precursors. Science, 2004, 303(5654), 95-98.
[] [PMID: 14631048]
Yi, R.; Qin, Y.; Macara, I.G.; Cullen, B.R. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev., 2003, 17(24), 3011-3016.
[] [PMID: 14681208]
Ding, X.C.; Weiler, J.; Grosshans, H. Regulating the regulators: mechanisms controlling the maturation of microRNAs. Trends Biotechnol., 2009, 27(1), 27-36.
[] [PMID: 19012978]
Giraldez, A.J.; Mishima, Y.; Rihel, J.; Grocock, R.J.; Van Dongen, S.; Inoue, K.; Enright, A.J.; Schier, A.F. Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs. Science, 2006, 312(5770), 75-79.
[] [PMID: 16484454]
Pillai, R.S.; Bhattacharyya, S.N.; Artus, C.G.; Zoller, T.; Cougot, N.; Basyuk, E.; Bertrand, E.; Filipowicz, W. Inhibition of translational initiation by Let-7 microRNA in human cells. Science, 2005, 309(5740), 1573-1576.
[] [PMID: 16081698]
Noferesti, S.S.; Sohel, M.M.; Hoelker, M.; Salilew-Wondim, D.; Tholen, E.; Looft, C.; Rings, F.; Neuhoff, C.; Schellander, K.; Tesfaye, D. Controlled ovarian hyperstimulation induced changes in the expression of circulatory miRNA in bovine follicular fluid and blood plasma. J. Ovarian Res., 2015, 8(81), 81.
[] [PMID: 26645573]
Chim, S.S.C.; Shing, T.K.F.; Hung, E.C.W.; Leung, T-Y.; Lau, T-K.; Chiu, R.W.K.; Lo, Y.M.D. Detection and characterization of placental microRNAs in maternal plasma. Clin. Chem., 2008, 54(3), 482-490.
[] [PMID: 18218722]
Weber, J.A.; Baxter, D.H.; Zhang, S.; Huang, D.Y.; Huang, K.H.; Lee, M.J.; Galas, D.J.; Wang, K. The microRNA spectrum in 12 body fluids. Clin. Chem., 2010, 56(11), 1733-1741.
[] [PMID: 20847327]
da Silveira, J.C.; Veeramachaneni, D.N.; Winger, Q.A.; Carnevale, E.M.; Bouma, G.J. Cell-secreted vesicles in equine ovarian follicular fluid contain miRNAs and proteins: a possible new form of cell communication within the ovarian follicle. Biol. Reprod., 2012, 86(3), 71.
[] [PMID: 22116803]
Sang, Q.; Yao, Z.; Wang, H.; Feng, R.; Wang, H.; Zhao, X.; Xing, Q.; Jin, L.; He, L.; Wu, L.; Wang, L. Identification of microRNAs in human follicular fluid: characterization of microRNAs that govern steroidogenesis in vitro and are associated with polycystic ovary syndrome in vivo. J. Clin. Endocrinol. Metab., 2013, 98(7), 3068-3079.
[] [PMID: 23666971]
Sohel, M.M.; Hoelker, M.; Noferesti, S.S.; Salilew-Wondim, D.; Tholen, E.; Looft, C.; Rings, F.; Uddin, M.J.; Spencer, T.E.; Schellander, K.; Tesfaye, D. Exosomal and non-exosomal transport of extracellular microRNAs in follicular fluid: implications for bovine oocyte developmental competence. PLoS One, 2013, 8(11), e78505.
[] [PMID: 24223816]
Gilad, S.; Meiri, E.; Yogev, Y.; Benjamin, S.; Lebanony, D.; Yerushalmi, N.; Benjamin, H.; Kushnir, M.; Cholakh, H.; Melamed, N.; Bentwich, Z.; Hod, M.; Goren, Y.; Chajut, A. Serum microRNAs are promising novel biomarkers. PLoS One, 2008, 3(9)e3148
[] [PMID: 18773077]
Taylor, D.D.; Gercel-Taylor, C. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol. Oncol., 2008, 110(1), 13-21.
[] [PMID: 18589210]
Valadi, H.; Ekström, K.; Bossios, A.; Sjöstrand, M.; Lee, J.J.; Lötvall, J.O. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol., 2007, 9(6), 654-659.
[] [PMID: 17486113]
Hunter, M.P.; Ismail, N.; Zhang, X.; Aguda, B.D.; Lee, E.J.; Yu, L.; Xiao, T.; Schafer, J.; Lee, M.L.T.; Schmittgen, T.D.; Nana-Sinkam, S.P.; Jarjoura, D.; Marsh, C.B. Detection of microRNA expression in human peripheral blood microvesicles. PLoS One, 2008, 3(11), e3694.
[] [PMID: 19002258]
Simpson, R.J.; Kalra, H.; Mathivanan, S. ExoCarta as a resource for exosomal research. J. Extracell. Vesicles, 2012, 1, 18374.
[] [PMID: 24009883]
Pegtel, D.M.; Cosmopoulos, K.; Thorley-Lawson, D.A.; van Eijndhoven, M.A.; Hopmans, E.S.; Lindenberg, J.L.; de Gruijl, T.D.; Würdinger, T.; Middeldorp, J.M. Functional delivery of viral miRNAs via exosomes. Proc. Natl. Acad. Sci. USA, 2010, 107(14), 6328-6333.
[] [PMID: 20304794]
Sun, J.; Aswath, K.; Schroeder, S.G.; Lippolis, J.D.; Reinhardt, T.A.; Sonstegard, T.S. MicroRNA expression profiles of bovine milk exosomes in response to Staphylococcus Aureus infection. BMC Genomics, 2015, 16, 806.
[] [PMID: 26475455]
Cheng, L.; Sharples, R.A.; Scicluna, B.J.; Hill, A.F. Exosomes provide a protective and enriched source of miRNA for biomarker profiling compared to intracellular and cell-free blood. J. Extracell. Vesicles, 2014, 3, 23743.
[] [PMID: 24683445]
Gruenberg, J.; van der Goot, F.G. Mechanisms of pathogen entry through the endosomal compartments. Nat. Rev. Mol. Cell Biol., 2006, 7(7), 495-504.
[] [PMID: 16773132]
Kowal, J.; Tkach, M.; Théry, C. Biogenesis and secretion of exosomes. Curr. Opin. Cell Biol., 2014, 29, 116-125.
[] [PMID: 24959705]
Wang, Z.F.; Liao, F.; Wu, H.; Dai, J. Glioma stem cells-derived exosomal miR-26a promotes angiogenesis of microvessel endothelial cells in glioma. J. Exp. Clin. Cancer Res., 2019, 38(1), 201.
[] [PMID: 31101062]
Villarroya-Beltri, C.; Gutiérrez-Vázquez, C.; Sánchez-Cabo, F.; Pérez-Hernández, D.; Vázquez, J.; Martin-Cofreces, N.; Martinez-Herrera, D.J.; Pascual-Montano, A.; Mittelbrunn, M.; Sánchez-Madrid, F. Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs. Nat. Commun., 2013, 4, 2980.
[] [PMID: 24356509]
Qian, X.; Zhao, P.; Li, W.; Shi, Z.M.; Wang, L.; Xu, Q.; Wang, M.; Liu, N.; Liu, L.Z.; Jiang, B.H. MicroRNA-26a promotes tumor growth and angiogenesis in glioma by directly targeting prohibitin. CNS Neurosci. Ther., 2013, 19(10), 804-812.
[] [PMID: 23870455]
Skog, J.; Würdinger, T.; van Rijn, S.; Meijer, D.H.; Gainche, L.; Sena-Esteves, M.; Curry, W.T., Jr; Carter, B.S.; Krichevsky, A.M.; Breakefield, X.O. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat. Cell Biol., 2008, 10(12), 1470-1476.
[] [PMID: 19011622]
Tűzesi, Á.; Kling, T.; Wenger, A.; Lunavat, T.R.; Jang, S.C.; Rydenhag, B.; Lötvall, J.; Pollard, S.M.; Danielsson, A.; Carén, H. Pediatric brain tumor cells release exosomes with a miRNA repertoire that differs from exosomes secreted by normal cells. Oncotarget, 2017, 8(52), 90164-90175.
[] [PMID: 29163818]
Regazzo, G.; Terrenato, I.; Spagnuolo, M.; Carosi, M.; Cognetti, G.; Cicchillitti, L.; Sperati, F.; Villani, V.; Carapella, C.; Piaggio, G.; Pelosi, A.; Rizzo, M.G. A restricted signature of serum miRNAs distinguishes glioblastoma from lower grade gliomas. J. Exp. Clin. Cancer Res., 2016, 35(1), 124.
[] [PMID: 27476114]
Roth, P.; Wischhusen, J.; Happold, C.; Chandran, P.A.; Hofer, S.; Eisele, G.; Weller, M.; Keller, A. A specific miRNA signature in the peripheral blood of glioblastoma patients. J. Neurochem., 2011, 118(3), 449-457.
[] [PMID: 21561454]
Akers, J.C.; Ramakrishnan, V.; Kim, R.; Skog, J.; Nakano, I.; Pingle, S.; Kalinina, J.; Hua, W.; Kesari, S.; Mao, Y.; Breakefield, X.O.; Hochberg, F.H.; Van Meir, E.G.; Carter, B.S.; Chen, C.C. MiR-21 in the extracellular vesicles (EVs) of cerebrospinal fluid (CSF): a platform for glioblastoma biomarker development. PLoS One, 2013, 8(10), e78115.
[] [PMID: 24205116]
Sohel, M.H. Extracellular/circulating microRNAs: release mechanisms, functions and challenges. Achiev. Life Sci., 2016, 10(2), 175-186.
Marzesco, A.M.; Janich, P.; Wilsch-Bräuninger, M.; Dubreuil, V.; Langenfeld, K.; Corbeil, D.; Huttner, W.B. Release of extracellular membrane particles carrying the stem cell marker prominin-1 (CD133) from neural progenitors and other epithelial cells. J. Cell Sci., 2005, 118(Pt 13), 2849-2858.
[] [PMID: 15976444]
Shet, A.S. Characterizing blood microparticles: technical aspects and challenges. Vasc. Health Risk Manag., 2008, 4(4), 769-774.
[] [PMID: 19065994]
Castellana, D.; Kunzelmann, C.; Freyssinet, J.M. Pathophysiologic significance of procoagulant microvesicles in cancer disease and progression. Hamostaseologie, 2009, 29(1), 51-57.
[] [PMID: 19151847]
Akao, Y.; Iio, A.; Itoh, T.; Noguchi, S.; Itoh, Y.; Ohtsuki, Y.; Naoe, T. Microvesicle-mediated RNA molecule delivery system using monocytes/macrophages. Mol. Ther., 2011, 19(2), 395-399.
[] [PMID: 21102562]
Bebawy, M.; Combes, V.; Lee, E.; Jaiswal, R.; Gong, J.; Bonhoure, A.; Grau, G.E. Membrane microparticles mediate transfer of P-glycoprotein to drug sensitive cancer cells. Leukemia, 2009, 23(9), 1643-1649.
[] [PMID: 19369960]
Teplyuk, N.M.; Mollenhauer, B.; Gabriely, G.; Giese, A.; Kim, E.; Smolsky, M.; Kim, R.Y.; Saria, M.G.; Pastorino, S.; Kesari, S.; Krichevsky, A.M. MicroRNAs in cerebrospinal fluid identify glioblastoma and metastatic brain cancers and reflect disease activity. Neurooncol., 2012, 14(6), 689-700.
[] [PMID: 22492962]
D’Souza-Schorey, C.; Clancy, J.W. Tumor-derived microvesicles: shedding light on novel microenvironment modulators and prospective cancer biomarkers. Genes Dev., 2012, 26(12), 1287-1299.
[] [PMID: 22713869]
Manterola, L.; Guruceaga, E.; Gállego Pérez-Larraya, J.; González-Huarriz, M.; Jauregui, P.; Tejada, S.; Diez-Valle, R.; Segura, V.; Samprón, N.; Barrena, C.; Ruiz, I.; Agirre, A.; Ayuso, A.; Rodríguez, J.; González, A.; Xipell, E.; Matheu, A.; López de Munain, A.; Tuñón, T.; Zazpe, I.; García-Foncillas, J.; Paris, S.; Delattre, J.Y.; Alonso, M.M. A small noncoding RNA signature found in exosomes of GBM patient serum as a diagnostic tool. Neuro-oncol., 2014, 16(4), 520-527.
[] [PMID: 24435880]
Turiák, L.; Misják, P.; Szabó, T.G.; Aradi, B.; Pálóczi, K.; Ozohanics, O.; Drahos, L.; Kittel, A.; Falus, A.; Buzás, E.I.; Vékey, K. Proteomic characterization of thymocyte-derived microvesicles and apoptotic bodies in BALB/c mice. J. Proteomics, 2011, 74(10), 2025-2033.
[] [PMID: 21635979]
Holmgren, L.; Szeles, A.; Rajnavölgyi, E.; Folkman, J.; Klein, G.; Ernberg, I.; Falk, K.I. Horizontal transfer of DNA by the uptake of apoptotic bodies. Blood, 1999, 93(11), 3956-3963.
[] [PMID: 10339505]
Zernecke, A.; Bidzhekov, K.; Noels, H.; Shagdarsuren, E.; Gan, L.; Denecke, B.; Hristov, M.; Köppel, T.; Jahantigh, M.N.; Lutgens, E.; Wang, S.; Olson, E.N.; Schober, A.; Weber, C. Delivery of microRNA-126 by apoptotic bodies induces CXCL12-dependent vascular protection. Sci. Signal., 2009, 2(100), ra81.
[] [PMID: 19996457]
Hergenreider, E.; Heydt, S.; Tréguer, K.; Boettger, T.; Horrevoets, A.J.; Zeiher, A.M.; Scheffer, M.P.; Frangakis, A.S.; Yin, X.; Mayr, M.; Braun, T.; Urbich, C.; Boon, R.A.; Dimmeler, S. Atheroprotective communication between endothelial cells and smooth muscle cells through miRNAs. Nat. Cell Biol., 2012, 14(3), 249-256.
[] [PMID: 22327366]
Lin, J.; Teo, S.; Lam, D.H.; Jeyaseelan, K.; Wang, S. MicroRNA-10b pleiotropically regulates invasion, angiogenicity and apoptosis of tumor cells resembling mesenchymal subtype of glioblastoma multiforme. Cell Death Dis., 2012, 3(10), e398.
[] [PMID: 23034333]
Zhang, X.; Zhang, X.; Hu, S.; Zheng, M.; Zhang, J.; Zhao, J.; Zhang, X.; Yan, B.; Jia, L.; Zhao, J.; Wu, K.; Yang, A.; Zhang, R. Identification of miRNA-7 by genome-wide analysis as a critical sensitizer for TRAIL-induced apoptosis in glioblastoma cells. Nucleic Acids Res., 2017, 45(10), 5930-5944.
[] [PMID: 28459998]
Sun, J.; Liao, K.; Wu, X.; Huang, J.; Zhang, S.; Lu, X. Serum microRNA-128 as a biomarker for diagnosis of glioma. Int. J. Clin. Exp. Med., 2015, 8(1), 456-463.
[PMID: 25785017]
Wang, Q.; Li, P.; Li, A.; Jiang, W.; Wang, H.; Wang, J.; Xie, K. Plasma specific miRNAs as predictive biomarkers for diagnosis and prognosis of glioma. J. Exp. Clin. Cancer Res., 2012, 31(1), 97.
[] [PMID: 23174013]
Yang, C.; Wang, C.; Chen, X.; Chen, S.; Zhang, Y.; Zhi, F.; Wang, J.; Li, L.; Zhou, X.; Li, N.; Pan, H.; Zhang, J.; Zen, K.; Zhang, C.Y.; Zhang, C. Identification of seven serum microRNAs from a genomewide serum microRNA expression profile as potential noninvasive biomarkers for malignant astrocytomas. Int. J. Cancer, 2013, 132(1), 116-127.
[] [PMID: 22674182]
Zhi, F.; Shao, N.; Wang, R.; Deng, D.; Xue, L.; Wang, Q.; Zhang, Y.; Shi, Y.; Xia, X.; Wang, S.; Lan, Q.; Yang, Y. Identification of 9 serum microRNAs as potential noninvasive biomarkers of human astrocytoma. Neuro-oncol., 2015, 17(3), 383-391.
[] [PMID: 25140035]
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.
[] [PMID: 27047250]
Pang, C.; Guan, Y.; Zhao, K.; Chen, L.; Bao, Y.; Cui, R.; Li, G.; Wang, Y. Up-regulation of microRNA-15b correlates with unfavorable prognosis and malignant progression of human glioma. Int. J. Clin. Exp. Pathol., 2015, 8(5), 4943-4952.
[PMID: 26191187]
Shang, C.; Hong, Y.; Guo, Y.; Liu, Y.H.; Xue, Y.X. miR-128 regulates the apoptosis and proliferation of glioma cells by targeting RhoE. Oncol. Lett., 2016, 11(1), 904-908.
[] [PMID: 26870304]
Wei, X.; Chen, D.; Lv, T.; Li, G.; Qu, S. Serum microRNA-125b as a potential biomarker for glioma diagnosis. Mol. Neurobiol., 2016, 53(1), 163-170.
[] [PMID: 25416859]
Shao, N.; Wang, L.; Xue, L.; Wang, R.; Lan, Q. Plasma miR-454-3p as a potential prognostic indicator in human glioma. Neurol. Sci., 2015, 36(2), 309-313.
[] [PMID: 25190548]
Yue, X.; Lan, F.; Hu, M.; Pan, Q.; Wang, Q.; Wang, J. Downregulation of serum microRNA-205 as a potential diagnostic and prognostic biomarker for human glioma. J. Neurosurg., 2016, 124(1), 122-128.
[] [PMID: 26230475]
Siegal, T.; Charbit, H.; Paldor, I.; Zelikovitch, B.; Canello, T.; Benis, A.; Wong, M.L.; Morokoff, A.P.; Kaye, A.H.; Lavon, I. Dynamics of circulating hypoxia-mediated miRNAs and tumor response in patients with high-grade glioma treated with bevacizumab. J. Neurosurg., 2016, 125(4), 1008-1015.
[] [PMID: 26799295]
Zhang, R.; Pang, B.; Xin, T.; Guo, H.; Xing, Y.; Xu, S.; Feng, B.; Liu, B.; Pang, Q. Plasma miR-221/222 family as novel descriptive and prognostic biomarkers for glioma. Mol. Neurobiol., 2016, 53(3), 1452-1460.
[] [PMID: 25636684]
Wu, J.; Li, L.; Jiang, C. Identification and evaluation of serum microRNA-29 family for glioma screening. Mol. Neurobiol., 2015, 52(3), 1540-1546.
[] [PMID: 25367878]
Ma, C.; Nguyen, H.P.T.; Luwor, R.B.; Stylli, S.S.; Gogos, A.; Paradiso, L.; Kaye, A.H.; Morokoff, A.P. A comprehensive meta-analysis of circulation miRNAs in glioma as potential diagnostic biomarker. PLoS One, 2018, 13(2)e0189452
[] [PMID: 29444091]
Bhaskaran, V.; Nowicki, M.O.; Idriss, M.; Jimenez, M.A.; Lugli, G.; Hayes, J.L.; Mahmoud, A.B.; Zane, R.E.; Passaro, C.; Ligon, K.L.; Haas-Kogan, D.; Bronisz, A.; Godlewski, J.; Lawler, S.E.; Chiocca, E.A.; Peruzzi, P. The functional synergism of microRNA clustering provides therapeutically relevant epigenetic interference in glioblastoma. Nat. Commun., 2019, 10(1), 442.
[] [PMID: 30683859]
Santangelo, A.; Tamanini, A.; Cabrini, G.; Dechecchi, M.C. Circulating microRNAs as emerging non-invasive biomarkers for gliomas. Ann. Transl. Med., 2017, 5(13), 277.
[] [PMID: 28758103]
Wong, S.T.S.; Zhang, X-Q.; Zhuang, J.T-F.; Chan, H-L.; Li, C-H.; Leung, G.K.K. MicroRNA-21 inhibition enhances in vitro chemosensitivity of temozolomide-resistant glioblastoma cells. Anticancer Res., 2012, 32(7), 2835-2841.
[PMID: 22753745]
Griveau, A.; Bejaud, J.; Anthiya, S.; Avril, S.; Autret, D.; Garcion, E. Silencing of miR-21 by locked nucleic acid-lipid nanocapsule complexes sensitize human glioblastoma cells to radiation-induced cell death. Int. J. Pharm., 2013, 454(2), 765-774.
[] [PMID: 23732394]
Ebrahimkhani, S.; Vafaee, F.; Hallal, S.; Wei, H.; Lee, M.Y.T.; Young, P.E.; Satgunaseelan, L.; Beadnall, H.; Barnett, M.H.; Shivalingam, B.; Suter, C.M.; Buckland, M.E.; Kaufman, K.L. Deep sequencing of circulating exosomal microRNA allows non-invasive glioblastoma diagnosis. NPJ Precis Oncol, 2018, 2(1), 28.
[] [PMID: 30564636]
Shen, X.; Li, J.; Liao, W.; Wang, J.; Chen, H.; Yao, Y.; Liu, H.; Ding, K. microRNA-149 targets caspase-2 in glioma progression. Oncotarget, 2016, 7(18), 26388-26399.
[] [PMID: 27049919]
Vlachos, I.S.; Zagganas, K.; Paraskevopoulou, M.D.; Georgakilas, G.; Karagkouni, D.; Vergoulis, T.; Dalamagas, T.; Hatzigeorgiou, A.G. DIANA-miRPath v3.0: deciphering microRNA function with experimental support. Nucleic Acids Res., 2015, 43(W1), W460-W466.
[] [PMID: 25977294]
Lai, N.S.; Wu, D.G.; Fang, X.G.; Lin, Y.C.; Chen, S.S.; Li, Z.B.; Xu, S.S. Serum microRNA-210 as a potential noninvasive biomarker for the diagnosis and prognosis of glioma. Br. J. Cancer, 2015, 112(7), 1241-1246.
[] [PMID: 25756397]

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