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MicroRNAs in the Molecular Pathology of Gliomas

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Glioma Cell Biology

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Abstract

MicroRNAs (miRNAs) are endogenously expressed small noncoding RNAs that act as posttranscriptional regulators of gene expression. Dysregulation of these molecules has been observed in many types of cancers. Altered expression levels of several miRNAs were identified also in gliomas. It was been frequently shown that miRNAs are involved in core signaling pathways, which play key roles in cellular processes, such as proliferation, apoptosis, cell cycle regulation, invasion, angiogenesis, and stem cell behavior. Therefore, miRNAs have a great potential to act as new class of diagnostic, prognostic, and predictive biomarkers as well as promising therapeutic targets in gliomas. Here, we summarize the current knowledge about miRNAs significance in glioma molecular pathology, with special focus on their involvement in core signaling pathways, their roles in drug resistance, and their potential clinical implications.

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Abbreviations

BMI1:

BMI1 polycomb ring finger oncogene

Cdk:

Cyclin-dependent kinase

c-MYC:

v-myc avian myelocytomatosis viral oncogene homolog

EGFR:

Epidermal growth factor receptor

GBM:

Glioblastoma multiforme

GSC:

Glioma stem cell

IFN:

Interferon

IKKα/β/γ:

Conserved helix-loop-helix ubiquitous kinase α/β/γ

IRS:

Insulin receptor substrate

JAK-STAT:

Janus kinase-signal transducer and activator of transcription

miRNA:

MicroRNA

MMP:

Matrix metalloproteinase

NF-κB:

Nuclear factor of kappa light polypeptide gene enhancer in B-cells

p21CIP1:

Cyclin-dependent kinase inhibitor 1A

p27:

p27 protein

PDGFR:

Platelet-derived growth factor receptor

PI3K/AKT:

Phosphatidylinositol-4,5-bisphosphate 3-kinase/v-akt murine thymoma viral oncogene homolog)

PLD2:

Phospholipase D2

PTEN:

Phosphatase and tensin homolog

RAS:

Rat sarcoma viral oncogene homolog

TMZ:

Temozolomide

VEGF:

Vascular endothelial cell growth factor

VEGFR:

VEGF receptor

WHO:

World Health Organization

References

  • Aldaz B, Sagardoy A, Nogueira L, Guruceaga E, Grande L, Huse JT et al (2013) Involvement of miRNAs in the differentiation of human glioblastoma multiforme stem-like cells. PLoS One 8:e77098

    CAS  PubMed Central  PubMed  Google Scholar 

  • Alrfaei BM, Vemuganti R, Kuo JS (2013) microRNA-100 targets SMRT/NCOR2, reduces proliferation, and improves survival in glioblastoma animal models. PLoS One 8:e80865

    PubMed Central  PubMed  Google Scholar 

  • Altaner C (2008) Glioblastoma and stem cells. Neoplasma 55:369–374

    CAS  PubMed  Google Scholar 

  • Asuthkar S, Velpula KK, Chetty C, Gorantla B, Rao JS (2012) Epigenetic regulation of miRNA-211 by MMP-9 governs glioma cell apoptosis, chemosensitivity and radiosensitivity. Oncotarget 3:1439–1454

    PubMed Central  PubMed  Google Scholar 

  • Babar IA, Czochor J, Steinmetz A, Weidhaas JB, Glazer PM, Slack FJ (2011) Inhibition of hypoxia-induced miR-155 radiosensitizes hypoxic lung cancer cells. Cancer Biol Ther 12:908–914

    CAS  PubMed Central  PubMed  Google Scholar 

  • Besse A, Sana J, Fadrus P, Slaby O (2013) MicroRNAs involved in chemo- and radioresistance of high-grade gliomas. Tumour Biol 34(4):1969–1978

    CAS  PubMed  Google Scholar 

  • Bienertova-Vasku J, Sana J, Slaby O (2013) The role of microRNAs in mitochondria in cancer. Cancer Lett 336:1–7

    CAS  PubMed  Google Scholar 

  • Cao L, Kim S, Xiao C, Wang RH, Coumoul X, Wang X et al (2006) ATM-Chk2-p53 activation prevents tumorigenesis at an expense of organ homeostasis upon Brca1 deficiency. EMBO J 25:2167–2177

    CAS  PubMed Central  PubMed  Google Scholar 

  • Card DA, Hebbar PB, Li L, Trotter KW, Komatsu Y, Mishina Y et al (2008) Oct4/Sox2-regulated miR-302 targets cyclin D1 in human embryonic stem cells. Mol Cell Biol 28:6426–6438

    PubMed  Google Scholar 

  • Carmo A, Carvalheiro H, Crespo I, Nunes I, Lopes MC (2011) Effect of temozolomide on the U-118 glioma cell line. Oncol Lett 2:1165–1170

    CAS  PubMed Central  PubMed  Google Scholar 

  • Carthew RW, Sontheimer EJ (2009) Origins and mechanisms of miRNAs and siRNAs. Cell 136:642–655

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ciafre SA, Galardi S, Mangiola A, Ferracin M, Liu CG, Sabatino G et al (2005) Extensive modulation of a set of microRNAs in primary glioblastoma. Biochem Biophys Res Commun 334:1351–1358

    CAS  PubMed  Google Scholar 

  • Conti A, Aguennouz M, La Torre D, Tomasello C, Cardali S, Angileri FF et al (2009) miR-21 and 221 upregulation and miR-181b downregulation in human grade II-IV astrocytic tumors. J Neurooncol 93:325–332

    CAS  PubMed  Google Scholar 

  • Costa PM, Cardoso AL, Nobrega C, Pereira de Almeida LF, Bruce JN, Canoll P et al (2013) MicroRNA-21 silencing enhances the cytotoxic effect of the antiangiogenic drug sunitinib in glioblastoma. Hum Mol Genet 22:904–918

    CAS  PubMed Central  PubMed  Google Scholar 

  • D’Urso PI, D’Urso OF, Storelli C, Mallardo M, Gianfreda CD, Montinaro A et al (2012) miR-155 is up-regulated in primary and secondary glioblastoma and promotes tumour growth by inhibiting GABA receptors. Int J Oncol 41:228–234

    PubMed  Google Scholar 

  • Darkes MJM, Plosker GL, Jarvis B (2002) Temozolomide: a review of its use in the treatment of malignant gliomas, malignant melanoma and other advanced cancers. Am J Cancer 1:55–80

    CAS  Google Scholar 

  • Dong CG, Wu WK, Feng SY, Wang XJ, Shao JF, Qiao J (2012) Co-inhibition of microRNA-10b and microRNA-21 exerts synergistic inhibition on the proliferation and invasion of human glioma cells. Int J Oncol 41:1005–1012

    CAS  PubMed  Google Scholar 

  • Dontula R, Dinasarapu A, Chetty C, Pannuru P, Herbert E, Ozer H et al (2013) MicroRNA 203 modulates glioma cell migration via Robo1/ERK/MMP-9 signaling. Genes Cancer 4:285–296

    PubMed Central  PubMed  Google Scholar 

  • Ernst A, Campos B, Meier J, Devens F, Liesenberg F, Wolter M et al (2010) De-repression of CTGF via the miR-17-92 cluster upon differentiation of human glioblastoma spheroid cultures. Oncogene 29:3411–3422

    CAS  PubMed  Google Scholar 

  • Fang L, Deng Z, Shatseva T, Yang J, Peng C, Du WW et al (2011) MicroRNA miR-93 promotes tumor growth and angiogenesis by targeting integrin-beta8. Oncogene 30:806–821

    CAS  PubMed  Google Scholar 

  • Fareh M, Turchi L, Virolle V, Debruyne D, Almairac F, de-la-Forest Divonne S et al (2012) The miR 302-367 cluster drastically affects self-renewal and infiltration properties of glioma-initiating cells through CXCR4 repression and consequent disruption of the SHH-GLI-NANOG network. Cell Death Differ 19:232–244

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fell VL, Schild-Poulter C (2012) Ku regulates signaling to DNA damage response pathways through the Ku70 von Willebrand A domain. Mol Cell Biol 32:76–87

    CAS  PubMed Central  PubMed  Google Scholar 

  • Folkman J (2006) Angiogenesis. Annu Rev Med 57:1–18

    CAS  PubMed  Google Scholar 

  • Fowler A, Thomson D, Giles K, Maleki S, Mreich E, Wheeler H et al (2011) miR-124a is frequently down-regulated in glioblastoma and is involved in migration and invasion. Eur J Cancer 47:953–963

    CAS  PubMed  Google Scholar 

  • Fu J, Rodova M, Nanta R, Meeker D, Van Veldhuizen PJ, Srivastava RK et al (2013) NPV-LDE-225 (Erismodegib) inhibits epithelial mesenchymal transition and self-renewal of glioblastoma initiating cells by regulating miR-21, miR-128, and miR-200. Neuro Oncol 15:691–706

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gabriely G, Wurdinger T, Kesari S, Esau CC, Burchard J, Linsley PS et al (2008) MicroRNA 21 promotes glioma invasion by targeting matrix metalloproteinase regulators. Mol Cell Biol 28:5369–5380

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gabriely G, Yi M, Narayan RS, Niers JM, Wurdinger T, Imitola J et al (2011) Human glioma growth is controlled by microRNA-10b. Cancer Res 71:3563–3572

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gal H, Pandi G, Kanner AA, Ram Z, Lithwick-Yanai G, Amariglio N et al (2008) MIR-451 and Imatinib mesylate inhibit tumor growth of Glioblastoma stem cells. Biochem Biophys Res Commun 376:86–90

    CAS  PubMed  Google Scholar 

  • Gao H, Zhao H, Xiang W (2013) Expression level of human miR-34a correlates with glioma grade and prognosis. J Neurooncol 113:221–228

    CAS  PubMed  Google Scholar 

  • Gaur AB, Holbeck SL, Colburn NH, Israel MA (2011) Downregulation of Pdcd4 by mir-21 facilitates glioblastoma proliferation in vivo. Neuro Oncol 13:580–590

    CAS  PubMed Central  PubMed  Google Scholar 

  • Genovese G, Ergun A, Shukla SA, Campos B, Hanna J, Ghosh P et al (2012) microRNA regulatory network inference identifies miR-34a as a novel regulator of TGF-beta signaling in glioblastoma. Cancer Discov 2:736–749

    CAS  PubMed Central  PubMed  Google Scholar 

  • Geretti E, Klagsbrun M (2007) Neuropilins: novel targets for anti-angiogenesis therapies. Cell Adh Migr 1:56–61

    PubMed Central  PubMed  Google Scholar 

  • Ghosh S, Karin M (2002) Missing pieces in the NF-kappaB puzzle. Cell 109(Suppl):S81–S96

    CAS  PubMed  Google Scholar 

  • Godlewski J, Nowicki MO, Bronisz A, Williams S, Otsuki A, Nuovo G et al (2008) Targeting of the Bmi-1 oncogene/stem cell renewal factor by microRNA-128 inhibits glioma proliferation and self-renewal. Cancer Res 68:9125–9130

    CAS  PubMed  Google Scholar 

  • Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ (2008) miRBase: tools for microRNA genomics. Nucleic Acids Res 36:D154–D158

    CAS  PubMed Central  PubMed  Google Scholar 

  • Guan Y, Mizoguchi M, Yoshimoto K, Hata N, Shono T, Suzuki SO et al (2010) MiRNA-196 is upregulated in glioblastoma but not in anaplastic astrocytoma and has prognostic significance. Clin Cancer Res 16:4289–4297

    CAS  PubMed  Google Scholar 

  • Guessous F, Alvarado-Velez M, Marcinkiewicz L, Zhang Y, Kim J, Heister S et al (2013) Oncogenic effects of miR-10b in glioblastoma stem cells. J Neurooncol 112:153–163

    CAS  PubMed Central  PubMed  Google Scholar 

  • Guessous F, Zhang Y, Kofman A, Catania A, Li Y, Schiff D et al (2010) microRNA-34a is tumor suppressive in brain tumors and glioma stem cells. Cell Cycle (Georgetown, TX) 9:1031–1036

    CAS  Google Scholar 

  • Guillamo JS, de Bouard S, Valable S, Marteau L, Leuraud P, Marie Y et al (2009) Molecular mechanisms underlying effects of epidermal growth factor receptor inhibition on invasion, proliferation, and angiogenesis in experimental glioma. Clin Cancer Res 15:3697–3704

    CAS  PubMed  Google Scholar 

  • Guo P, Nie Q, Lan J, Ge J, Qiu Y, Mao Q (2013) C-Myc negatively controls the tumor suppressor PTEN by upregulating miR-26a in glioblastoma multiforme cells. Biochem Biophys Res Commun 441:186–190

    CAS  PubMed  Google Scholar 

  • Gwak HS, Kim TH, Jo GH, Kim YJ, Kwak HJ, Kim JH et al (2012) Silencing of microRNA-21 confers radio-sensitivity through inhibition of the PI3K/AKT pathway and enhancing autophagy in malignant glioma cell lines. PLoS One 7:e47449

    CAS  PubMed Central  PubMed  Google Scholar 

  • Haapa-Paananen S, Chen P, Hellstrom K, Kohonen P, Hautaniemi S, Kallioniemi O et al (2013) Functional profiling of precursor MicroRNAs identifies MicroRNAs essential for glioma proliferation. PLoS One 8:e60930

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hao J, Zhang C, Zhang A, Wang K, Jia Z, Wang G et al (2012) miR-221/222 is the regulator of Cx43 expression in human glioblastoma cells. Oncol Rep 27:1504–1510

    CAS  PubMed  Google Scholar 

  • Hatanpaa KJ, Burma S, Zhao D, Habib AA (2010) Epidermal growth factor receptor in glioma: signal transduction, neuropathology, imaging, and radioresistance. Neoplasia 12:675–684

    CAS  PubMed Central  PubMed  Google Scholar 

  • He J, Deng Y, Yang G, Xie W (2013) MicroRNA-203 down-regulation is associated with unfavorable prognosis in human glioma. J Surg Oncol 108:121–125

    CAS  PubMed  Google Scholar 

  • Hermansen SK, Dahlrot RH, Nielsen BS, Hansen S, Kristensen BW (2013) MiR-21 expression in the tumor cell compartment holds unfavorable prognostic value in gliomas. J Neurooncol 111:71–81

    CAS  PubMed  Google Scholar 

  • Hermansen SK, Kristensen BW (2013) MicroRNA biomarkers in glioblastoma. J Neurooncol 114:13–23

    CAS  PubMed  Google Scholar 

  • Hong L, Han Y, Zhang Y, Zhang H, Zhao Q, Wu K et al (2013) MicroRNA-21: a therapeutic target for reversing drug resistance in cancer. Expert Opin Ther Targets 17:1073–1080

    CAS  PubMed  Google Scholar 

  • Hua D, Ding D, Han X, Zhang W, Zhao N, Foltz G et al (2012) Human miR-31 targets radixin and inhibits migration and invasion of glioma cells. Oncol Rep 27:700–706

    CAS  PubMed  Google Scholar 

  • Huang PH, Xu AM, White FM (2009) Oncogenic EGFR signaling networks in glioma. Sci Signal 2:re6

    PubMed  Google Scholar 

  • Huse JT, Brennan C, Hambardzumyan D, Wee B, Pena J, Rouhanifard SH et al (2009) The PTEN-regulating microRNA miR-26a is amplified in high-grade glioma and facilitates gliomagenesis in vivo. Genes Dev 23:1327–1337

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chakravarti A, Zhai G, Suzuki Y, Sarkesh S, Black PM, Muzikansky A et al (2004) The prognostic significance of phosphatidylinositol 3-kinase pathway activation in human gliomas. J Clin Oncol 22:1926–1933

    CAS  PubMed  Google Scholar 

  • Chamberlain MC (2011) Bevacizumab for the treatment of recurrent glioblastoma. Clin Med Insights Oncol 5:117–129

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chan JA, Krichevsky AM, Kosik KS (2005) MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res 65:6029–6033

    CAS  PubMed  Google Scholar 

  • Chan XH, Nama S, Gopal F, Rizk P, Ramasamy S, Sundaram G et al (2012) Targeting glioma stem cells by functional inhibition of a prosurvival oncomiR-138 in malignant gliomas. Cell Rep 2:591–602

    CAS  PubMed  Google Scholar 

  • Chang C, Shi H, Wang C, Wang J, Geng N, Jiang X et al (2012) Correlation of microRNA-375 downregulation with unfavorable clinical outcome of patients with glioma. Neurosci Lett 531:204–208

    CAS  PubMed  Google Scholar 

  • Chaudhry MA, Kreger B, Omaruddin RA (2010a) Transcriptional modulation of micro-RNA in human cells differing in radiation sensitivity. Int J Radiat Biol 86:569–583

    CAS  PubMed  Google Scholar 

  • Chaudhry MA, Sachdeva H, Omaruddin RA (2010b) Radiation-induced micro-RNA modulation in glioblastoma cells differing in DNA-repair pathways. DNA Cell Biol 29:553–561

    CAS  PubMed  Google Scholar 

  • Chen C-Z (2005) MicroRNAs as oncogenes and tumor suppressors. New Engl J Med 353:1768–1771

    CAS  PubMed  Google Scholar 

  • Chen G, Zhu W, Shi D, Lv L, Zhang C, Liu P et al (2010a) MicroRNA-181a sensitizes human malignant glioma U87MG cells to radiation by targeting Bcl-2. Oncol Rep 23:997–1003

    CAS  PubMed  Google Scholar 

  • Chen L, Chen XR, Chen FF, Liu Y, Li P, Zhang R et al (2013a) MicroRNA-107 inhibits U87 glioma stem cells growth and invasion. Cell Mol Neurobiol 33:651–657

    CAS  PubMed  Google Scholar 

  • Chen L, Zhang J, Han L, Zhang A, Zhang C, Zheng Y et al (2012) Downregulation of miR-221/222 sensitizes glioma cells to temozolomide by regulating apoptosis independently of p53 status. Oncol Rep 27:854–860

    CAS  PubMed  Google Scholar 

  • Chen L, Zhang R, Li P, Liu Y, Qin K, Fa ZQ et al (2013b) P53-induced microRNA-107 inhibits proliferation of glioma cells and down-regulates the expression of CDK6 and Notch-2. Neurosci Lett 534:327–332

    CAS  PubMed  Google Scholar 

  • Chen R, Nishimura MC, Bumbaca SM, Kharbanda S, Forrest WF, Kasman IM et al (2010b) A hierarchy of self-renewing tumor-initiating cell types in glioblastoma. Cancer Cell 17:362–375

    CAS  PubMed  Google Scholar 

  • Chen SM, Chen HC, Chen SJ, Huang CY, Chen PY, Wu TW et al (2013c) MicroRNA-495 inhibits proliferation of glioblastoma multiforme cells by downregulating cyclin-dependent kinase 6. World J Surg Oncol 11:87

    PubMed Central  PubMed  Google Scholar 

  • Chen Y, Liu W, Chao T, Zhang Y, Yan X, Gong Y et al (2008) MicroRNA-21 down-regulates the expression of tumor suppressor PDCD4 in human glioblastoma cell T98G. Cancer Lett 272:197–205

    CAS  PubMed  Google Scholar 

  • Chen Z, Li D, Cheng Q, Ma Z, Jiang B, Peng R et al (2013d) MicroRNA-203 inhibits the proliferation and invasion of U251 glioblastoma cells by directly targeting PLD2. Mol Med Rep 9(2):503–508

    PubMed  Google Scholar 

  • Ishitani T, Hirao T, Suzuki M, Isoda M, Ishitani S, Harigaya K et al (2010) Nemo-like kinase suppresses Notch signalling by interfering with formation of the Notch active transcriptional complex. Nat Cell Biol 12:278–285

    CAS  PubMed  Google Scholar 

  • Jia Z, Wang K, Zhang A, Wang G, Kang C, Han L et al (2013) miR-19a and miR-19b overexpression in gliomas. Pathol Oncol Res 19:847–853

    CAS  PubMed  Google Scholar 

  • Jiang J, Sun X, Wang W, Jin X, Bo X, Li Z et al (2012) Tumor microRNA-335 expression is associated with poor prognosis in human glioma. Med Oncol 29:3472–3477

    CAS  PubMed  Google Scholar 

  • Jiang J, Yang J, Wang Z, Wu G, Liu F (2013) TFAM is directly regulated by miR-23b in glioma. Oncol Rep 30:2105–2110

    CAS  PubMed  Google Scholar 

  • Kao GD, Jiang Z, Fernandes AM, Gupta AK, Maity A (2007) Inhibition of phosphatidylinositol-3-OH kinase/Akt signaling impairs DNA repair in glioblastoma cells following ionizing radiation. J Biol Chem 282:21206–21212

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kefas B, Comeau L, Erdle N, Montgomery E, Amos S, Purow B (2010) Pyruvate kinase M2 is a target of the tumor-suppressive microRNA-326 and regulates the survival of glioma cells. Neuro Oncol 12:1102–1112

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kefas B, Comeau L, Floyd DH, Seleverstov O, Godlewski J, Schmittgen T et al (2009) The neuronal microRNA miR-326 acts in a feedback loop with notch and has therapeutic potential against brain tumors. J Neurosci 29:15161–15168

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kefas B, Godlewski J, Comeau L, Li Y, Abounader R, Hawkinson M et al (2008) microRNA-7 inhibits the epidermal growth factor receptor and the Akt pathway and is down-regulated in glioblastoma. Cancer Res 68:3566–3572

    CAS  PubMed  Google Scholar 

  • Kim H, Huang W, Jiang X, Pennicooke B, Park PJ, Johnson MD (2010) Integrative genome analysis reveals an oncomir/oncogene cluster regulating glioblastoma survivorship. Proc Natl Acad Sci U S A 107:2183–2188

    CAS  PubMed Central  PubMed  Google Scholar 

  • Koo S, Martin GS, Schulz KJ, Ronck M, Toussaint LG (2012) Serial selection for invasiveness increases expression of miR-143/miR-145 in glioblastoma cell lines. BMC Cancer 12:143

    CAS  PubMed Central  PubMed  Google Scholar 

  • Koshkin PA, Chistiakov DA, Chekhonin VP (2013) Role of microRNAs in mechanisms of glioblastoma resistance to radio- and chemotherapy. Biochemistry (Mosc) 78:325–334

    CAS  Google Scholar 

  • Kozomara A, Griffiths-Jones S (2011) miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 39:D152–D157

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kwiatkowska A, Symons M (2013) Signaling determinants of glioma cell invasion. Adv Exp Med Biol 986:121–141

    CAS  PubMed  Google Scholar 

  • Ladomery MR, Maddocks DG, Wilson ID (2011) MicroRNAs: their discovery, biogenesis, function and potential use as biomarkers in non-invasive prenatal diagnostics. Int J Mol Epidemiol Genet 2:253–260

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lakomy R, Sana J, Hankeova S, Fadrus P, Kren L, Lzicarova E et al (2011) MiR-195, miR-196b, miR-181c, miR-21 expression levels and O-6-methylguanine-DNA methyltransferase methylation status are associated with clinical outcome in glioblastoma patients. Cancer Sci 102:2186–2190

    CAS  PubMed  Google Scholar 

  • Lawler S, Chiocca EA (2009) Emerging functions of microRNAs in glioblastoma. J Neurooncol 92:297–306

    CAS  PubMed  Google Scholar 

  • Le MT, Xie H, Zhou B, Chia PH, Rizk P, Um M et al (2009) MicroRNA-125b promotes neuronal differentiation in human cells by repressing multiple targets. Mol Cell Biol 29:5290–5305

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lee KM, Choi EJ, Kim IA (2011a) microRNA-7 increases radiosensitivity of human cancer cells with activated EGFR-associated signaling. Radiother Oncol 101:171–176

    CAS  PubMed  Google Scholar 

  • Lee ST, Chu K, Oh HJ, Im WS, Lim JY, Kim SK et al (2011b) Let-7 microRNA inhibits the proliferation of human glioblastoma cells. J Neurooncol 102:19–24

    CAS  PubMed  Google Scholar 

  • Li G, Zhang Z, Tu Y, Jin T, Liang H, Cui G et al (2013a) Correlation of microRNA-372 upregulation with poor prognosis in human glioma. Diagn Pathol 8:1

    PubMed Central  PubMed  Google Scholar 

  • Li M, Li J, Liu L, Li W, Yang Y, Yuan J (2013b) MicroRNA in human glioma. Cancers (Basel) 5:1306–1331

    Google Scholar 

  • Li W-Q, Li Y-M, Tao B-B, Lu Y-C, Hu G-H, Liu H-M et al (2010) Downregulation of ABCG2 expression in glioblastoma cancer stem cells with miRNA-328 may decrease their chemoresistance. Med Sci Monit 16:HY27–HY30

    PubMed  Google Scholar 

  • Li WB, Ma MW, Dong LJ, Wang F, Chen LX, Li XR (2011) MicroRNA-34a targets notch1 and inhibits cell proliferation in glioblastoma multiforme. Cancer Biol Ther 12:477–483

    CAS  PubMed  Google Scholar 

  • Li Y, Guessous F, Zhang Y, Dipierro C, Kefas B, Johnson E et al (2009a) MicroRNA-34a inhibits glioblastoma growth by targeting multiple oncogenes. Cancer Res 69:7569–7576

    CAS  PubMed Central  PubMed  Google Scholar 

  • Li Y, Li W, Yang Y, Lu Y, He C, Hu G et al (2009b) MicroRNA-21 targets LRRFIP1 and contributes to VM-26 resistance in glioblastoma multiforme. Brain Res 1286:13–18

    CAS  PubMed  Google Scholar 

  • Li Y, Xu J, Chen H, Bai J, Li S, Zhao Z et al (2013c) Comprehensive analysis of the functional microRNA-mRNA regulatory network identifies miRNA signatures associated with glioma malignant progression. Nucleic Acids Res 41(22):e203

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lin J, Teo S, Lam DH, Jeyaseelan K, Wang S (2012) MicroRNA-10b pleiotropically regulates invasion, angiogenicity and apoptosis of tumor cells resembling mesenchymal subtype of glioblastoma multiforme. Cell Death Dis 3:e398

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lin YX, Yu F, Gao N, Sheng JP, Qiu JZ, Hu BC (2011) microRNA-143 protects cells from DNA damage-induced killing by downregulating FHIT expression. Cancer Biother Radiopharm 26:365–372

    CAS  PubMed  Google Scholar 

  • Ling N, Gu J, Lei Z, Li M, Zhao J, Zhang HT et al (2013) microRNA-155 regulates cell proliferation and invasion by targeting FOXO3a in glioma. Oncol Rep 30:2111–2118

    CAS  PubMed  Google Scholar 

  • Liu L, Chen L, Xu Y, Li R, Du X (2010) microRNA-195 promotes apoptosis and suppresses tumorigenicity of human colorectal cancer cells. Biochem Biophys Res Commun 400:236–240

    CAS  PubMed  Google Scholar 

  • Lu S, Wang S, Geng S, Ma S, Liang Z, Jiao B (2012) Increased expression of microRNA-17 predicts poor prognosis in human glioma. J Biomed Biotechnol 2012:970761

    PubMed Central  PubMed  Google Scholar 

  • Lu S, Wang S, Geng S, Ma S, Liang Z, Jiao B (2013) Upregulation of microRNA-224 confers a poor prognosis in glioma patients. Clin Transl Oncol 15:569–574

    CAS  PubMed  Google Scholar 

  • Luan S, Sun L, Huang F (2010) MicroRNA-34a: a novel tumor suppressor in p53-mutant glioma cell line U251. Arch Med Res 41:67–74

    CAS  PubMed  Google Scholar 

  • Malzkorn B, Wolter M, Liesenberg F, Grzendowski M, Stuhler K, Meyer HE et al (2010) Identification and functional characterization of microRNAs involved in the malignant progression of gliomas. Brain Pathol 20:539–550

    CAS  PubMed  Google Scholar 

  • Martin V, Sanchez-Sanchez AM, Herrera F, Gomez-Manzano C, Fueyo J, Alvarez-Vega MA et al (2013) Melatonin-induced methylation of the ABCG2/BCRP promoter as a novel mechanism to overcome multidrug resistance in brain tumour stem cells. Br J Cancer 108:2005–2012

    CAS  PubMed Central  PubMed  Google Scholar 

  • Meng W, Jiang L, Lu L, Hu H, Yu H, Ding D et al (2012) Anti-miR-155 oligonucleotide enhances chemosensitivity of U251 cell to taxol by inducing apoptosis. Cell Biol Int 36:653–659

    CAS  PubMed  Google Scholar 

  • Mizoguchi M, Guan Y, Yoshimoto K, Hata N, Amano T, Nakamizo A et al (2012) MicroRNAs in human malignant gliomas. J Oncol 2012:732874

    PubMed Central  PubMed  Google Scholar 

  • Mueller AC, Sun D, Dutta A (2013) The miR-99 family regulates the DNA damage response through its target SNF2H. Oncogene 32(9):1164–1172

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nakada M, Kita D, Teng L, Pyko IV, Watanabe T, Hayashi Y et al (2013) Receptor tyrosine kinases: principles and functions in glioma invasion. Adv Exp Med Biol 986:143–170

    CAS  PubMed  Google Scholar 

  • Nakano I, Kornblum HI (2006) Brain tumor stem cells. Pediatr Res 59:54R–58R

    PubMed  Google Scholar 

  • Nan Y, Han L, Zhang A, Wang G, Jia Z, Yang Y et al (2010) MiRNA-451 plays a role as tumor suppressor in human glioma cells. Brain Res 1359:14–21

    CAS  PubMed  Google Scholar 

  • Ng WL, Yan D, Zhang X, Mo YY, Wang Y (2010) Over-expression of miR-100 is responsible for the low-expression of ATM in the human glioma cell line: M059J. DNA Repair (Amst) 9:1170–1175

    CAS  Google Scholar 

  • Nikaki A, Piperi C, Papavassiliou AG (2012) Role of microRNAs in gliomagenesis: targeting miRNAs in glioblastoma multiforme therapy. Expert Opin Investig Drugs 21:1475–1488

    CAS  PubMed  Google Scholar 

  • Niyazi M, Zehentmayr F, Niemoller OM, Eigenbrod S, Kretzschmar H, Schulze-Osthoff K et al (2011) MiRNA expression patterns predict survival in glioblastoma. Radiat Oncol 6:153

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ohno M, Natsume A, Kondo Y, Iwamizu H, Motomura K, Toda H et al (2009) The modulation of microRNAs by type I IFN through the activation of signal transducers and activators of transcription 3 in human glioma. Mol Cancer Res 7:2022–2030

    CAS  PubMed  Google Scholar 

  • Pan SJ, Zhan SK, Pei BG, Sun QF, Bian LG, Sun BM (2012) MicroRNA-149 inhibits proliferation and invasion of glioma cells via blockade of AKT1 signaling. Int J Immunopathol Pharmacol 25:871–881

    CAS  PubMed  Google Scholar 

  • Papagiannakopoulos T, Friedmann-Morvinski D, Neveu P, Dugas JC, Gill RM, Huillard E et al (2012) Pro-neural miR-128 is a glioma tumor suppressor that targets mitogenic kinases. Oncogene 31:1884–1895

    CAS  PubMed Central  PubMed  Google Scholar 

  • Papagiannakopoulos T, Shapiro A, Kosik KS (2008) MicroRNA-21 targets a network of key tumor-suppressive pathways in glioblastoma cells. Cancer Res 68:8164–8172

    CAS  PubMed  Google Scholar 

  • Platanias LC (2005) Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat Rev Immunol 5:375–386

    CAS  PubMed  Google Scholar 

  • Qian X, Zhao P, Li W, Shi ZM, Wang L, Xu Q et al (2013) MicroRNA-26a promotes tumor growth and angiogenesis in glioma by directly targeting prohibitin. CNS Neurosci Ther 19:804–812

    CAS  PubMed  Google Scholar 

  • Qiu S, Huang D, Yin D, Li F, Li X, Kung HF et al (2013) Suppression of tumorigenicity by microRNA-138 through inhibition of EZH2-CDK4/6-pRb-E2F1 signal loop in glioblastoma multiforme. Biochim Biophys Acta 1832:1697–1707

    CAS  PubMed  Google Scholar 

  • Qu S, Yao Y, Shang C, Xue Y, Ma J, Li Z et al (2012) MicroRNA-330 is an oncogenic factor in glioblastoma cells by regulating SH3GL2 gene. PLoS One 7:e46010

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rao SA, Santosh V, Somasundaram K (2010) Genome-wide expression profiling identifies deregulated miRNAs in malignant astrocytoma. Mod Pathol 23:1404–1417

    CAS  PubMed  Google Scholar 

  • Ren Y, Kang CS, Yuan XB, Zhou X, Xu P, Han L et al (2010a) Co-delivery of as-miR-21 and 5-FU by poly(amidoamine) dendrimer attenuates human glioma cell growth in vitro. J Biomater Sci Polym Ed 21:303–314

    CAS  PubMed  Google Scholar 

  • Ren Y, Zhou X, Mei M, Yuan XB, Han L, Wang GX et al (2010b) MicroRNA-21 inhibitor sensitizes human glioblastoma cells U251 (PTEN-mutant) and LN229 (PTEN-wild type) to taxol. BMC Cancer 10:27

    PubMed Central  PubMed  Google Scholar 

  • Sana J, Hajduch M, Michalek J, Vyzula R, Slaby O (2011) MicroRNAs and glioblastoma: roles in core signalling pathways and potential clinical implications. J Cell Mol Med 15:1636–1644

    CAS  PubMed  Google Scholar 

  • Sasaki A, Udaka Y, Tsunoda Y, Yamamoto G, Tsuji M, Oyamada H et al (2012) Analysis of p53 and miRNA expression after irradiation of glioblastoma cell lines. Anticancer Res 32:4709–4713

    CAS  PubMed  Google Scholar 

  • Sasayama T, Nishihara M, Kondoh T, Hosoda K, Kohmura E (2009) MicroRNA-10b is overexpressed in malignant glioma and associated with tumor invasive factors, uPAR and RhoC. Int J Cancer 125:1407–1413

    CAS  PubMed  Google Scholar 

  • Sharma S, Salehi F, Scheithauer BW, Rotondo F, Syro LV, Kovacs K (2009) Role of MGMT in tumor development, progression, diagnosis, treatment and prognosis. Anticancer Res 29:3759–3768

    CAS  PubMed  Google Scholar 

  • Shi L, Chen J, Yang J, Pan T, Zhang S, Wang Z (2010) MiR-21 protected human glioblastoma U87MG cells from chemotherapeutic drug temozolomide induced apoptosis by decreasing Bax/Bcl-2 ratio and caspase-3 activity. Brain Res 1352:255–264

    CAS  PubMed  Google Scholar 

  • Shi L, Zhang S, Feng K, Wu F, Wan Y, Wang Z, Zhang J, Wang Y, Yan W, Fu Z, You Y (2012) MicroRNA-125b-2 confers human glioblastoma stem cells resistance to temozolomide through the mitochondrial pathway of apoptosis. Int J Oncol 40:119–129

    PubMed  Google Scholar 

  • Shi L, Wan Y, Sun G, Zhang S, Wang Z, Zeng Y (2013) miR-125b inhibitor may enhance the invasion-prevention activity of temozolomide in glioblastoma stem cells by targeting PIAS3. BioDrugs 28(1):41–54

    Google Scholar 

  • Schraivogel D, Weinmann L, Beier D, Tabatabai G, Eichner A, Zhu JY et al (2011) CAMTA1 is a novel tumour suppressor regulated by miR-9/9* in glioblastoma stem cells. EMBO J 30:4309–4322

    CAS  PubMed Central  PubMed  Google Scholar 

  • Schramedei K, Morbt N, Pfeifer G, Lauter J, Rosolowski M, Tomm JM et al (2011) MicroRNA-21 targets tumor suppressor genes ANP32A and SMARCA4. Oncogene 30:2975–2985

    CAS  PubMed Central  PubMed  Google Scholar 

  • Schwarz DS, Hutvagner G, Du T, Xu Z, Aronin N, Zamore PD (2003) Asymmetry in the assembly of the RNAi enzyme complex. Cell 115:199–208

    CAS  PubMed  Google Scholar 

  • Siddique HR, Saleem M (2012) Role of BMI1, a stem cell factor, in cancer recurrence and chemoresistance: preclinical and clinical evidences. Stem Cells 30:372–378

    CAS  PubMed  Google Scholar 

  • Silber J, Lim DA, Petritsch C, Persson AI, Maunakea AK, Yu M et al (2008) miR-124 and miR-137 inhibit proliferation of glioblastoma multiforme cells and induce differentiation of brain tumor stem cells. BMC Med 6:14

    PubMed Central  PubMed  Google Scholar 

  • Skalsky RL, Cullen BR (2011) Reduced expression of brain-enriched microRNAs in glioblastomas permits targeted regulation of a cell death gene. PLoS One 6:e24248

    CAS  PubMed Central  PubMed  Google Scholar 

  • Slaby O, Lakomy R, Fadrus P, Hrstka R, Kren L, Lzicarova E et al (2010) MicroRNA-181 family predicts response to concomitant chemoradiotherapy with temozolomide in glioblastoma patients. Neoplasma 57:264–269

    CAS  PubMed  Google Scholar 

  • Song L, Huang Q, Chen K, Liu L, Lin C, Dai T et al (2010) miR-218 inhibits the invasive ability of glioma cells by direct downregulation of IKK-beta. Biochem Biophys Res Commun 402:135–140

    CAS  PubMed  Google Scholar 

  • Soon PS, Tacon LJ, Gill AJ, Bambach CP, Sywak MS, Campbell PR et al (2009) miR-195 and miR-483-5p Identified as Predictors of Poor Prognosis in Adrenocortical Cancer. Clin Cancer Res 15:7684–7692

    CAS  PubMed  Google Scholar 

  • Squatrito M, Brennan CW, Helmy K, Huse JT, Petrini JH, Holland EC (2010) Loss of ATM/Chk2/p53 pathway components accelerates tumor development and contributes to radiation resistance in gliomas. Cancer Cell 18:619–629

    CAS  PubMed  Google Scholar 

  • Srinivasan S, Patric IR, Somasundaram K (2011) A ten-microRNA expression signature predicts survival in glioblastoma. PLoS One 6:e17438

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sternlicht MD, Lochter A, Sympson CJ, Huey B, Rougier JP, Gray JW et al (1999) The stromal proteinase MMP3/stromelysin-1 promotes mammary carcinogenesis. Cell 98:137–146

    CAS  PubMed Central  PubMed  Google Scholar 

  • Stockhausen MT, Kristoffersen K, Poulsen HS (2010) The functional role of Notch signaling in human gliomas. Neuro Oncol 12:199–211

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sun B, Pu B, Chu D, Chu X, Li W, Wei D (2013) MicroRNA-650 expression in glioma is associated with prognosis of patients. J Neurooncol 115:375–380

    CAS  PubMed  Google Scholar 

  • Ujifuku K, Mitsutake N, Takakura S, Matsuse M, Saenko V, Suzuki K et al (2010) miR-195, miR-455-3p and miR-10a( *) are implicated in acquired temozolomide resistance in glioblastoma multiforme cells. Cancer Lett 296:241–248

    CAS  PubMed  Google Scholar 

  • Ulasov IV, Nandi S, Dey M, Sonabend AM, Lesniak MS (2011) Inhibition of Sonic hedgehog and Notch pathways enhances sensitivity of CD133(+) glioma stem cells to temozolomide therapy. Mol Med 17:103–112

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wang J, Li Y, Wang X, Jiang C (2012a) Ursolic acid inhibits proliferation and induces apoptosis in human glioblastoma cell lines U251 by suppressing TGF-beta1/miR-21/PDCD4 pathway. Basic Clin Pharmacol Toxicol 111:106–112

    CAS  PubMed  Google Scholar 

  • Wang J, Wakeman TP, Lathia JD, Hjelmeland AB, Wang XF, White RR et al (2010) Notch promotes radioresistance of glioma stem cells. Stem Cells 28:17–28

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wang K, Wang X, Zou J, Zhang A, Wan Y, Pu P et al (2013a) miR-92b controls glioma proliferation and invasion through regulating Wnt/beta-catenin signaling via Nemo-like kinase. Neuro Oncol 15:578–588

    PubMed Central  PubMed  Google Scholar 

  • Wang L, Shi M, Hou S, Ding B, Liu L, Ji X et al (2012b) MiR-483-5p suppresses the proliferation of glioma cells via directly targeting ERK1. FEBS Lett 586:1312–1317

    CAS  PubMed  Google Scholar 

  • Wang S, Jiao B, Geng S, Ma S, Liang Z, Lu S (2014) Combined aberrant expression of microRNA-214 and UBC9 is an independent unfavorable prognostic factor for patients with gliomas. Med Oncol 31:767

    PubMed  Google Scholar 

  • Wang S, Lu S, Geng S, Ma S, Liang Z, Jiao B (2013b) Expression and clinical significance of microRNA-326 in human glioma miR-326 expression in glioma. Med Oncol 30:373

    PubMed  Google Scholar 

  • Wang X, Wang J, Ma H, Zhang J, Zhou X (2012c) Downregulation of miR-195 correlates with lymph node metastasis and poor prognosis in colorectal cancer. Med Oncol 29:919–927

    CAS  PubMed  Google Scholar 

  • Wang XR, Luo H, Li HL, Cao L, Wang XF, Yan W et al (2013c) Overexpressed let-7a inhibits glioma cell malignancy by directly targeting K-ras, independently of PTEN. Neuro Oncol 15:1491–1501

    CAS  PubMed Central  PubMed  Google Scholar 

  • Webster RJ, Giles KM, Price KJ, Zhang PM, Mattick JS, Leedman PJ (2009) Regulation of epidermal growth factor receptor signaling in human cancer cells by microRNA-7. J Biol Chem 284:5731–5741

    CAS  PubMed  Google Scholar 

  • Wu N, Xiao L, Zhao X, Zhao J, Wang J, Wang F et al (2012) miR-125b regulates the proliferation of glioblastoma stem cells by targeting E2F2. FEBS Lett 586:3831–3839

    CAS  PubMed  Google Scholar 

  • Wu Z, Wang L, Li G, Liu H, Fan F, Li Z et al (2013) Increased expression of microRNA-9 predicts an unfavorable prognosis in human glioma. Mol Cell Biochem 384(1–2):263–268

    CAS  PubMed  Google Scholar 

  • Wurdinger T, Tannous BA, Saydam O, Skog J, Grau S, Soutschek J et al (2008) miR-296 regulates growth factor receptor overexpression in angiogenic endothelial cells. Cancer Cell 14:382–393

    CAS  PubMed Central  PubMed  Google Scholar 

  • Xia H, Qi Y, Ng SS, Chen X, Chen S, Fang M et al (2009) MicroRNA-15b regulates cell cycle progression by targeting cyclins in glioma cells. Biochem Biophys Res Commun 380:205–210

    CAS  PubMed  Google Scholar 

  • Xu T, Zhu Y, Xiong Y, Ge YY, Yun JP, Zhuang SM (2009) MicroRNA-195 suppresses tumorigenicity and regulates G1/S transition of human hepatocellular carcinoma cells. Hepatology 50:113–121

    CAS  PubMed  Google Scholar 

  • Yamada R, Nakano I (2012) Glioma stem cells: their role in chemoresistance. World Neurosurg 77:237–240

    PubMed  Google Scholar 

  • Yan D, Ng WL, Zhang X, Wang P, Zhang Z, Mo YY et al (2010) Targeting DNA-PKcs and ATM with miR-101 sensitizes tumors to radiation. PLoS One 5:e11397

    PubMed Central  PubMed  Google Scholar 

  • Ying Z, Li Y, Wu J, Zhu X, Yang Y, Tian H et al (2013) Loss of miR-204 expression enhances glioma migration and stem cell-like phenotype. Cancer Res 73:990–999

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yue X, Wang P, Xu J, Zhu Y, Sun G, Pang Q et al (2012) MicroRNA-205 functions as a tumor suppressor in human glioblastoma cells by targeting VEGF-A. Oncol Rep 27:1200–1206

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zbinden M, Duquet A, Lorente-Trigos A, Ngwabyt SN, Borges I, Ruiz i Altaba A (2010) NANOG regulates glioma stem cells and is essential in vivo acting in a cross-functional network with GLI1 and p53. EMBO J 29:2659–2674

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang C, Han L, Zhang A, Yang W, Zhou X, Pu P et al (2010a) Global changes of mRNA expression reveals an increased activity of the interferon-induced signal transducer and activator of transcription (STAT) pathway by repression of miR-221/222 in glioblastoma U251 cells. Int J Oncol 36:1503–1512

    CAS  PubMed  Google Scholar 

  • Zhang J, Han L, Ge Y, Zhou X, Zhang A, Zhang C et al (2010b) miR-221/222 promote malignant progression of glioma through activation of the Akt pathway. Int J Oncol 36:913–920

    CAS  PubMed  Google Scholar 

  • Zhang QQ, Xu H, Huang MB, Ma LM, Huang QJ, Yao Q et al (2012a) MicroRNA-195 plays a tumor-suppressor role in human glioblastoma cells by targeting signaling pathways involved in cellular proliferation and invasion. Neuro Oncol 14:278–287

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang S, Wan Y, Pan T, Gu X, Qian C, Sun G et al (2012b) MicroRNA-21 inhibitor sensitizes human glioblastoma U251 stem cells to chemotherapeutic drug temozolomide. J Mol Neurosci 47:346–356

    CAS  PubMed  Google Scholar 

  • Zhang W, Zhang J, Hoadley K, Kushwaha D, Ramakrishnan V, Li S et al (2012c) miR-181d: a predictive glioblastoma biomarker that downregulates MGMT expression. Neuro Oncol 14:712–719

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang Y, Chao T, Li R, Liu W, Chen Y, Yan X et al (2009) MicroRNA-128 inhibits glioma cells proliferation by targeting transcription factor E2F3a. J Mol Med (Berl) 87:43–51

    CAS  Google Scholar 

  • Zhao S, Deng Y, Liu Y, Chen X, Yang G, Mu Y et al (2013a) MicroRNA-153 is tumor suppressive in glioblastoma stem cells. Mol Biol Rep 40:2789–2798

    CAS  PubMed  Google Scholar 

  • Zhao WH, Wu SQ, Zhang YD (2013b) Downregulation of miR-124 promotes the growth and invasiveness of glioblastoma cells involving upregulation of PPP1R13L. Int J Mol Med 32:101–107

    PubMed  Google Scholar 

  • Zheng X, Chopp M, Lu Y, Buller B, Jiang F (2013) MiR-15b and miR-152 reduce glioma cell invasion and angiogenesis via NRP-2 and MMP-3. Cancer Lett 329:146–154

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhou J, Xu T, Yan Y, Qin R, Wang H, Zhang X et al (2013) MicroRNA-326 functions as a tumor suppressor in glioma by targeting the Nin one binding protein (NOB1). PLoS One 8:e68469

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhou X, Ren Y, Moore L, Mei M, You Y, Xu P et al (2010a) Downregulation of miR-21 inhibits EGFR pathway and suppresses the growth of human glioblastoma cells independent of PTEN status. Lab Invest 90:144–155

    CAS  PubMed  Google Scholar 

  • Zhou X, Zhang J, Jia Q, Ren Y, Wang Y, Shi L et al (2010b) Reduction of miR-21 induces glioma cell apoptosis via activating caspase 9 and 3. Oncol Rep 24:195–201

    CAS  PubMed  Google Scholar 

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Acknowledgment

This work was supported by grants of Internal Grant Agency of the Czech Ministry of Health no. NT13514-4/2012 and NT11214-4/2010; project “CEITEC—Central European Institute of Technology” (CZ.1.05/1.1.00/02.0068).

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Authors and Affiliations

  1. Masaryk Memorial Cancer Institute, Zluty kopec 7, 656 53, Brno, Czech Republic

    Jiri Sana, Andrej Besse & Ondrej Slaby

  2. Central European Institute of Technology, Kamenice 5, 625 00, Brno, Czech Republic

    Jiri Sana, Andrej Besse & Ondrej Slaby

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  1. Jiri Sana
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  2. Andrej Besse
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Correspondence to Ondrej Slaby .

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  1. Biochemistry and Experimental Oncology, Charles University Prague 1st Faculty of Medicine, Prague, Czech Republic

    Aleksi Sedo

  2. Anatomisches Institut, Christian-Albrechts-Universität zu Kiel, Kiel, Germany

    Rolf Mentlein

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Sana, J., Besse, A., Slaby, O. (2014). MicroRNAs in the Molecular Pathology of Gliomas. In: Sedo, A., Mentlein, R. (eds) Glioma Cell Biology. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1431-5_4

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