Expression of 19 microRNAs in glioblastoma and comparison with other brain neoplasia of grades I-III

Molecular Oncology

Volumn 8, Issue 2, 2014, Pages 417-430

  Visani, Michela ^a   de Biase, Dario ^a   Marucci, Gianluca ^a   Cerasoli, Serenella ^b   Nigrisoli, Evandro ^b   Bacchi Reggiani, Maria Letizia ^a   Albani, Fiorenzo ^c,d   Baruzzi, Agostino ^c,d   Pession, Annalisa ^a   Baruzzi, A ^c   Albani, F ^c   Calbucci, F ^c   D'Alessandro, R ^c   Michelucci, R ^c   Brandes, A ^e   Eusebi, V ^f   Ceruti, S ^g   Fainardi, E ^g   Tamarozzi, R ^g   Emiliani, E ^h   Cavallo, M ^g   Franceschi, E ^e   Tosoni, A ^e   Fiorica, F ^g   Valentini, A ⁱ   Depenni, R ^j   Mucciarini, C ^k   Crisi, G ^l   Sasso, E ^l   Biasini, C ^m   Cavanna, L ^m   Guidetti, D ^m   Marcello, N ⁿ   Pisanello, A ⁿ   Cremonini, A M ^o   Guiducci, G ^o   de Pasqua, S ^c   Testoni, S ^c   Agati, R ^p   Ambrosetto, G ^p   Bacci, A ^p   Baldin, E ^p   Baldrati, A ^p   Barbieri, E ^p   Bartolini, S ^p   Bellavista, E ^p   Bisulli, F ^p   Bonora, E ^p   Bunkheila, F ^p   Carelli, V ^p   Crisci, M ^p   Dall'Occa, P ^p   Ferro, S ^p   Franceschi, C ^p   Frezza, G ^p   Grasso, V ^p   Leonardi, M ^p   Morandi, L ^p   Mostacci, B ^p   Palandri, G ^p   Pasini, E ^p   Pastore Trossello, M ^p   Poggi, R ^p   Riguzzi, P ^p   Rinaldi, R ^p   Rizzi, S ^p   Romeo, G ^p   Spagnolli, F ^p   Tinuper, P ^p   Trocino, C ^p   Dall'Agata, M ^p   Frattarelli, M ^p   Gentili, G ^p   Giovannini, A ^p   Iorio, P ^p   Pasquini, U ^p   Galletti, G ^p   Guidi, C ^p   Neri, W ^p   Patuelli, A ^p   Strumia, S ^p   Faedi, M ^q   Casmiro, M ^r   Gamboni, A ^r   Rasi, F ^r   Cruciani, G ^s   Cenni, P ^p   Dazzi, C ^p   Guidi, A R ^p   Zumaglini, F ^p   Amadori, A ^p   Pasini, G ^p   Pasquinelli, M ^p   Pasquini, E ^p   Polselli, A ^p   Ravasio, A ^p   Viti, B ^p   Sintini, M ^t   Ariatti, A ^p   Bertolini, F ^p   Bigliardi, G ^p   Carpeggiani, P ^p   Cavalleri, F ^p   Meletti, S ^p   Nichelli, P ^p   Pettorelli, E ^p   Pinna, G ^p   Zunarelli, E ^p   Artioli, F ^u   Bernardini, I ^u   Costa, M ^u   Greco, G ^u   Guerzoni, R ^u   Stucchi, C ^u   Iaccarino, C ^v   Ragazzi, M ^v   Rizzi, R ^v   Zuccoli, G ^v   Api, P ^p   Cartei, F ^p   Fallica, E ^p   Granieri, E ^p   Latini, F ^p   Lelli, G ^p   Monetti, C ^p   Saletti, A ^p   Schivalocchi, R ^p   Seraceni, S ^p   Tola, M R ^p   Urbini, B ^p   Giorgi, C ^w   Montanari, E ^w   Cerasti, D ^p   Crafa, P ^p   Dascola, I ^p   Florindo, I ^p   Giombelli, E ^p   Mazza, S ^p   Ramponi, V ^p   Servadei, F ^p   Silini, E M ^p   Torelli, P ^p   Immovilli, P ^p   Morelli, N ^p   Vanzo, C ^p   Nobile, C ^p   more..

^a UNIVERSITY OF BOLOGNA   (Italy)

^b M Bufalini Hospital   (Italy)

^c IRCCS ISTITUTO DELLE SCIENZE NEUROLOGICHE DI BOLOGNA   (Italy)

^d UNIVERSITY OF BOLOGNA   (Italy)

^e MAGGIORE HOSPITAL   (Italy)

^f BELLARIA HOSPITAL   (Italy)

^g S ANNA HOSPITAL   (Italy)

^h SANTA MARIA DELLE CROCI HOSPITAL   (Italy)

ⁱ Nuovo Ospedale S Agostino   (Italy)

^j UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^k Ramazzini Hospital   (Italy)

^l UNIVERSITY OF PARMA   (Italy)

^m GUGLIELMO DA SALICETO HOSPITAL   (Italy)

ⁿ S MARIA NUOVA HOSPITAL   (Italy)

^o BUFALINI HOSPITAL   (Italy)

^p Istituto di Ricovero e Cura a Carattere Scientifico ^*  (Italy)

^q DEPARTMENT OF MEDICAL ONCOLOGY   (Italy)

^r NONE   (Italy)

^s Lugo Hospital   (Italy)

^t UO di Oncologia Ospedale Infermi Rimini Ospedale Cervesi Azienda USL di Rimini   (Italy)

^u NONE   (Italy)

^v Rheumatology Unit   (Italy)

^w NONE   (Italy)

more..

Author keywords

Brain neoplasia; Glioblastoma; Low grade brain tumors; MicroRNA; Real time PCR

Indexed keywords

FORMALDEHYDE; MICRORNA; MICRORNA 101; MICRORNA 10A; MICRORNA 10B; MICRORNA 137; MICRORNA 17; MICRORNA 182; MICRORNA 20A; MICRORNA 21; MICRORNA 221; MICRORNA 222; MICRORNA 26A; MICRORNA 27A; MICRORNA 31; MICRORNA 330; MICRORNA 34A; MICRORNA 519D; MICRORNA 7; MICRORNA 9; PARAFFIN; UNCLASSIFIED DRUG;

ADOLESCENT; ADULT; AGED; ARTICLE; ASTROCYTOMA; BRAIN CANCER; CANCER GRADING; CHILD; COMPARATIVE STUDY; CONTROLLED STUDY; DOWN REGULATION; EPENDYMOMA; FEMALE; GENE EXPRESSION; GENETIC ANALYSIS; GLIOBLASTOMA; GLIOMA; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; NEUROEPITHELIOMA; OLIGODENDROGLIOMA; PILOCYTIC ASTROCYTOMA; PLEOMORPHIC XANTHOASTROCYTOMA; PRESCHOOL CHILD; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RNA METHYLATION; SCHOOL CHILD; UPREGULATION; VALIDATION PROCESS; YOUNG ADULT;

BRAIN NEOPLASIA; GLIOBLASTOMA; LOW-GRADE BRAIN TUMORS; MICRORNA; REAL-TIME PCR;

ADULT; AGED; BRAIN NEOPLASMS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOBLASTOMA; HUMANS; MALE; MICRORNAS; MIDDLE AGED; NEOPLASM GRADING; RNA, NEOPLASM;

EID: 84894376146     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2013.12.010     Document Type: Article

References (63)

1. Brandes A.A., Tosoni A., Franceschi E., Sotti G., Frezza G., Amista P., Morandi L., Spagnolli F., Ermani M. Recurrence pattern after temozolomide concomitant with and adjuvant to radiotherapy in newly diagnosed patients with glioblastoma: correlation with MGMT promoter methylation status. J.Clin. Oncol. 2009, 27:1275-1279.
2. Bulnes S., Bengoetxea H., Ortuzar N., Argandona E.G., Garcia-Blanco A., Rico-Barrio I., Lafuente J.V. Angiogenic signalling pathways altered in gliomas: selection mechanisms for more aggressive neoplastic subpopulations with invasive phenotype. J.Signal Transduct. 2012, 2012:597915.
3. Chan J.A., Krichevsky A.M., Kosik K.S. MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res. 2005, 65:6029-6033.
4. Chen Y., Liu W., Chao T., Zhang Y., Yan X., Gong Y., Qiang B., Yuan J., Sun M., Peng X. MicroRNA-21 down-regulates the expression of tumor suppressor PDCD4 in human glioblastoma cell T98G. Cancer Lett. 2008, 272:197-205.
5. Cho R.J., Campbell M.J. Transcription, genomes, function. Trends Genet. 2000, 16:409-415.
6. Ciafre S.A., Galardi S., Mangiola A., Ferracin M., Liu C.G., Sabatino G., Negrini M., Maira G., Croce C.M., Farace M.G. Extensive modulation of a set of microRNAs in primary glioblastoma. Biochem. Biophys. Res. Commun. 2005, 334:1351-1358.
7. Clarke J., Butowski N., Chang S. Recent advances in therapy for glioblastoma. Arch. Neurol. 2010, 67:279-283.
8. Conti A., Aguennouz M., La Torre D., Tomasello C., Cardali S., Angileri F.F., Maio F., Cama A., Germano A., Vita G., Tomasello F. miR-21 and 221 upregulation and miR-181b downregulation in human grade II-IV astrocytic tumors. J.Neurooncol. 2009, 93:325-332.
9. Davis B.N., Hilyard A.C., Nguyen P.H., Lagna G., Hata A. Induction of microRNA-221 by platelet-derived growth factor signaling is critical for modulation of vascular smooth muscle phenotype. J.Biol. Chem. 2009, 284:3728-3738.
10. de Biase D., Visani M., Morandi L., Marucci G., Taccioli C., Cerasoli S., Baruzzi A., Pession A. miRNAs expression analysis in paired fresh/frozen and dissected formalin fixed and paraffin embedded glioblastoma using real-time pCR. PLoS ONE 2012, 7:e35596.
11. de la Iglesia N., Konopka G., Lim K.L., Nutt C.L., Bromberg J.F., Frank D.A., Mischel P.S., Louis D.N., Bonni A. Deregulation of a STAT3-interleukin 8 signaling pathway promotes human glioblastoma cell proliferation and invasiveness. J.Neurosci. 2008, 28:5870-5878.
12. Dong H., Luo L., Hong S., Siu H., Xiao Y., Jin L., Chen R., Xiong M. Integrated analysis of mutations, miRNA and mRNA expression in glioblastoma. BMC Syst. Biol. 2010, 4:163.
13. Dweep H., Sticht C., Pandey P., Gretz N. miRWalk-database: prediction of possible miRNA binding sites by "walking" the genes of three genomes. J.Biomed. Inform. 2011, 44:839-847.
14. Ermoian R.P., Furniss C.S., Lamborn K.R., Basila D., Berger M.S., Gottschalk A.R., Nicholas M.K., Stokoe D., Haas-Kogan D.A. Dysregulation of PTEN and protein kinase B is associated with glioma histology and patient survival. Clin. Cancer Res. 2002, 8:1100-1106.
15. Gabriely G., Yi M., Narayan R.S., Niers J.M., Wurdinger T., Imitola J., Ligon K.L., Kesari S., Esau C., Stephens R.M., Tannous B.A., Krichevsky A.M. Human glioma growth is controlled by microRNA-10b. Cancer Res. 2010, 71:3563-3572.
16. Gal H., Pandi G., Kanner A.A., Ram Z., Lithwick-Yanai G., Amariglio N., Rechavi G., Givol D. MIR-451 and Imatinib mesylate inhibit tumor growth of Glioblastoma stem cells. Biochem. Biophys. Res. Commun. 2008, 376:86-90.
17. Galasso M., Sandhu S.K., Volinia S. MicroRNA expression signatures in solid malignancies. Cancer J. 2012, 18:238-243.
18. Genovese G., Ergun A., Shukla S.A., Campos B., Hanna J., Ghosh P., Quayle S.N., Rai K., Colla S., Ying H., Wu C.J., Sarkar S., Xiao Y., Zhang J., Zhang H., Kwong L., Dunn K., Wiedemeyer W.R., Brennan C., Zheng H., Rimm D.L., Collins J.J., Chin L. microRNA regulatory network inference identifies miR-34a as a novel regulator of TGF-beta signaling in glioblastoma. Cancer Discov. 2012, 2:736-749.
19. Godlewski J., Nowicki M.O., Bronisz A., Williams S., Otsuki A., Nuovo G., Raychaudhury A., Newton H.B., Chiocca E.A., Lawler S. Targeting of the Bmi-1 oncogene/stem cell renewal factor by microRNA-128 inhibits glioma proliferation and self-renewal. Cancer Res. 2008, 68:9125-9130.
20. Guan Y., Mizoguchi M., Yoshimoto K., Hata N., Shono T., Suzuki S.O., Araki Y., Kuga D., Nakamizo A., Amano T., Ma X., Hayashi K., Sasaki T. MiRNA-196 is upregulated in glioblastoma but not in anaplastic astrocytoma and has prognostic significance. Clin. Cancer Res. 2010, 16:4289-4297.
21. Hsu S.D., Lin F.M., Wu W.Y., Liang C., Huang W.C., Chan W.L., Tsai W.T., Chen G.Z., Lee C.J., Chiu C.M., Chien C.H., Wu M.C., Huang C.Y., Tsou A.P., Huang H.D. miRTarBase: a database curates experimentally validated microRNA-target interactions. Nucleic Acids Res. 2011, 39:D163-D169.
22. Hua D., Mo F., Ding D., Li L., Han X., Zhao N., Foltz G., Lin B., Lan Q., Huang Q. A catalogue of glioblastoma and brain MicroRNAs identified by deep sequencing. OMICS 2012, 16:690-699.
23. Huse J.T., Brennan C., Hambardzumyan D., Wee B., Pena J., Rouhanifard S.H., Sohn-Lee C., le Sage C., Agami R., Tuschl T., Holland E.C. The PTEN-regulating microRNA miR-26a is amplified in high-grade glioma and facilitates gliomagenesis invivo. Genes Dev. 2009, 23:1327-1337.
24. Kefas B., Godlewski J., Comeau L., Li Y., Abounader R., Hawkinson M., Lee J., Fine H., Chiocca E.A., Lawler S., Purow B. microRNA-7 inhibits the epidermal growth factor receptor and the Akt pathway and is down-regulated in glioblastoma. Cancer Res. 2008, 68:3566-3572.
25. Lakomy R., Sana J., Hankeova S., Fadrus P., Kren L., Lzicarova E., Svoboda M., Dolezelova H., Smrcka M., Vyzula R., Michalek J., Hajduch M., Slaby O. 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. 2011, 102:2186-2190.
26. Lang M.F., Yang S., Zhao C., Sun G., Murai K., Wu X., Wang J., Gao H., Brown C.E., Liu X., Zhou J., Peng L., Rossi J.J., Shi Y. Genome-wide profiling identified a set of miRNAs that are differentially expressed in glioblastoma stem cells and normal neural stem cells. PLoS ONE 2012, 7:e36248.
27. Lawler S., Chiocca E.A. Emerging functions of microRNAs in glioblastoma. J.Neurooncol. 2009, 92:297-306.
28. LeBrun D.G., Li M. MicroRNAs in glioblastoma multiforme: profiling studies and therapeutic Impacts. Mol. Cell Pharmacol. 2011, 3:93-105.
29. Li Y., Guessous F., Zhang Y., Dipierro C., Kefas B., Johnson E., Marcinkiewicz L., Jiang J., Yang Y., Schmittgen T.D., Lopes B., Schiff D., Purow B., Abounader R. MicroRNA-34a inhibits glioblastoma growth by targeting multiple oncogenes. Cancer Res. 2009, 69:7569-7576.
30. Li W.B., Ma M.W., Dong L.J., Wang F., Chen L.X., Li X.R. MicroRNA-34a targets notch1 and inhibits cell proliferation in glioblastoma multiforme. Cancer Biol. Ther. 2011, 12:477-483.
31. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402-408.
32. Loftus J.C., Ross J.T., Paquette K.M., Paulino V.M., Nasser S., Yang Z., Kloss J., Kim S., Berens M.E., Tran N.L. miRNA expression profiling in migrating glioblastoma cells: regulation of cell migration and invasion by miR-23b via targeting of Pyk2. PLoS ONE 2012, 7:e39818.
33. Louis D.N., Ohgaki H., Wiestler O.D., Cavenee W.K. WHO. Classification of Tumours of the Central Nervous System 2007, IARC, Lyon.
34. Low S., Vougioukas V.I., Hielscher T., Schmidt U., Unterberg A., Halatsch M.E. Pathogenetic pathways leading to glioblastoma multiforme: association between gene expressions and resistance to erlotinib. Anticancer Res. 2008, 28:3729-3732.
35. Malzkorn B., Wolter M., Liesenberg F., Grzendowski M., Stuhler K., Meyer H.E., Reifenberger G. Identification and functional characterization of microRNAs involved in the malignant progression of gliomas. Brain Pathol. 2009, 20:539-550.
36. Mi H., Muruganujan A., Thomas P.D. PANTHER in 2013: modeling the evolution of gene function, and other gene attributes, in the context of phylogenetic trees. Nucleic Acids Res. 2013, 41:D377-D386.
37. Mizoguchi M., Guan Y., Yoshimoto K., Hata N., Amano T., Nakamizo A., Sasaki T. MicroRNAs in human malignant gliomas. J.Oncol. 2012, 2012:732874.
38. Montagnani Marelli M., Moretti R.M., Mai S., Muller O., Van Groeninghen J.C., Limonta P. Novel insights into GnRH receptor activity: role in the control of human glioblastoma cell proliferation. Oncol. Rep. 2009, 21:1277-1282.
39. Morandi L., Franceschi E., de Biase D., Marucci G., Tosoni A., Ermani M., Pession A., Tallini G., Brandes A. Promoter methylation analysis of O6-methylguanine-DNA methyltransferase in glioblastoma: detection by locked nucleic acid based quantitative PCR using an imprinted gene (SNURF) as a reference. BMC Cancer 2010, 10:48.
40. Morandi L., de Biase D., Visani M., Cesari V., De Maglio G., Pizzolitto S., Pession A., Tallini G. Allele specific locked nucleic acid quantitative PCR (ASLNAqPCR): an accurate and cost-effective assay to diagnose and quantify KRAS and BRAF mutation. PLoS ONE 2012, 7:e36084.
41. Nakada M., Kita D., Watanabe T., Hayashi Y., Teng L., Pyko I.V., Hamada J. Aberrant signaling pathways in glioma. Cancer 2011, 3:3242-3278.
42. Nana-Sinkam S.P., Croce C.M. Clinical applications for microRNAs in cancer. Clin. Pharmacol. Ther. 2013, 93:98-104.
43. Niyazi M., Zehentmayr F., Niemoller O.M., Eigenbrod S., Kretzschmar H., Schulze-Osthoff K., Tonn J.C., Atkinson M., Mortl S., Belka C. MiRNA expression patterns predict survival in glioblastoma. Radiat. Oncol. 2011, 6:153.
44. Quintavalle C., Garofalo M., Zanca C., Romano G., Iaboni M., del Basso De Caro M., Martinez-Montero J.C., Incoronato M., Nuovo G., Croce C.M., Condorelli G. miR-221/222 overexpession in human glioblastoma increases invasiveness by targeting the protein phosphate PTPmu. Oncogene 2012, 31:858-868.
45. Quintavalle C., Magnani D., Roscino G., Romano G., Diaz-Lagares A., Iaboni M., Donnarumma E., Fiore D., De Marinis P., Soini Y., Esteller M., Condorelli G. miR-221/222 target the DNA methyltransferase MGMT in glioma cells. PLoS ONE 2013, 8:e74466.
46. Rao S.A., Santosh V., Somasundaram K. Genome-wide expression profiling identifies deregulated miRNAs in malignant astrocytoma. Mod. Pathol. 2010, 23:1404-1417.
47. Sasayama T., Nishihara M., Kondoh T., Hosoda K., Kohmura E. MicroRNA-10b is overexpressed in malignant glioma and associated with tumor invasive factors, uPAR and RhoC. Int. J. Cancer 2009, 125:1407-1413.
48. Silber J., Lim D.A., Petritsch C., Persson A.I., Maunakea A.K., Yu M., Vandenberg S.R., Ginzinger D.G., James C.D., Costello J.F., Bergers G., Weiss W.A., Alvarez-Buylla A., Hodgson J.G. miR-124 and miR-137 inhibit proliferation of glioblastoma multiforme cells and induce differentiation of brain tumor stem cells. BMC Med. 2008, 6:14.
49. Silber J., Jacobsen A., Ozawa T., Harinath G., Pedraza A., Sander C., Holland E.C., Huse J.T. miR-34a repression in proneural malignant gliomas upregulates expression of its target PDGFRA and promotes tumorigenesis. PLoS ONE 2012, 7:e33844.
50. Skalsky R.L., Cullen B.R. Reduced expression of brain-enriched microRNAs in glioblastomas permits targeted regulation of a cell death gene. PLoS ONE 2011, 6:e24248.
51. Slaby O., Lakomy R., Fadrus P., Hrstka R., Kren L., Lzicarova E., Smrcka M., Svoboda M., Dolezalova H., Novakova J., Valik D., Vyzula R., Michalek J. MicroRNA-181 family predicts response to concomitant chemoradiotherapy with temozolomide in glioblastoma patients. Neoplasma 2010, 57:264-269.
52. Smits M., Nilsson J., Mir S.E., van der Stoop P.M., Hulleman E., Niers J.M., de Witt Hamer P.C., Marquez V.E., Cloos J., Krichevsky A.M., Noske D.P., Tannous B.A., Wurdinger T. miR-101 is down-regulated in glioblastoma resulting in EZH2-induced proliferation, migration, and angiogenesis. Oncotarget 2010, 1:710-720.
53. Srinivasan S., Patric I.R., Somasundaram K. A ten-microRNA expression signature predicts survival in glioblastoma. PLoS ONE 2011, 6:e17438.
54. Trojan J., Cloix J.F., Ardourel M.Y., Chatel M., Anthony D.D. Insulin-like growth factor type I biology and targeting in malignant gliomas. Neuroscience 2007, 145:795-811.
55. van Groeninghen J.C., Kiesel L., Winkler D., Zwirner M. Effects of luteinising-hormone-releasing hormone on nervous-system tumours. Lancet 1998, 352:372-373.
56. Visani M., de Biase D., Marucci G., Taccioli C., Baruzzi A., Pession A. Definition of miRNAs expression profile in glioblastoma samples: the relevance of non-neoplastic brain reference. PLoS ONE 2012, 8:e55314.
57. Wang L., Liu Z., Balivada S., Shrestha T., Bossmann S., Pyle M., Pappan L., Shi J., Troyer D. Interleukin-1beta and transforming growth factor-beta cooperate to induce neurosphere formation and increase tumorigenicity of adherent LN-229 glioma cells. Stem Cell Res. Ther. 2012, 3:5.
58. Xiao F., Zuo Z., Cai G., Kang S., Gao X., Li T. miRecords: an integrated resource for microRNA-target interactions. Nucleic Acids Res. 2009, 37:D105-D110.
59. Yan H., Parsons D.W., Jin G., McLendon R., Rasheed B.A., Yuan W., Kos I., Batinic-Haberle I., Jones S., Riggins G.J., Friedman H., Friedman A., Reardon D., Herndon J., Kinzler K.W., Velculescu V.E., Vogelstein B., Bigner D.D. IDH1 and IDH2 mutations in gliomas. N.Engl. J. Med. 2009, 360:765-773.
60. Zhang B., Pan X., Cobb G.P., Anderson T.A. microRNAs as oncogenes and tumor suppressors. Dev. Biol. 2007, 302:1-12.
61. Zhang C., Han L., Zhang A., Yang W., Zhou X., Pu P., Du Y., Zeng H., Kang C. 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. 2010, 36:1503-1512.
62. Zhang W., Zhang J., Yan W., You G., Bao Z., Li S., Kang C., Jiang C., You Y., Zhang Y., Chen C.C., Song S.W., Jiang T. Whole-genome microRNA expression profiling identifies a 5-microRNA signature as a prognostic biomarker in Chinese patients with primary glioblastoma multiforme. Cancer 2013, 119:814-824.
63. Zhou X., Ren Y., Moore L., Mei M., You Y., Xu P., Wang B., Wang G., Jia Z., Pu P., Zhang W., Kang C. Downregulation of miR-21 inhibits EGFR pathway and suppresses the growth of human glioblastoma cells independent of PTEN status. Lab. Invest. 2010, 90:144-155.