Prediction of clinical outcome in glioblastoma using a biologically relevant nine-microRNA signature

Molecular Oncology

Volumn 9, Issue 3, 2015, Pages 704-714

  Hayes, Josie ^a   Thygesen, Helene ^a   Tumilson, Charlotte ^b   Droop, Alastair ^a   Boissinot, Marjorie ^a   Hughes, Thomas A ^a   Westhead, David ^c   Alder, Jane E ^b   Shaw, Lisa ^b   Short, Susan C ^a   Lawler, Sean E ^d  

^a ST JAMES S UNIVERSITY HOSPITAL   (United Kingdom)

^b UNIVERSITY OF CENTRAL LANCASHIRE   (United Kingdom)

^c UNIVERSITY OF LEEDS   (United Kingdom)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Glioblastoma; MicroRNA; Prognosis; Signature; TCGA

Indexed keywords

MESSENGER RNA; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; MICRORNA; MICRORNA 10B; MICRORNA 124A; MICRORNA 145; MICRORNA 148A; MICRORNA 182; MICRORNA 222; MICRORNA 34A; MICRORNA 370; MICRORNA 9; TEMOZOLOMIDE; UNCLASSIFIED DRUG; DACARBAZINE;

ADULT; ARTICLE; CANCER GRADING; CANCER PATIENT; CANCER SURVIVAL; CORRELATIONAL STUDY; FEMALE; GENE EXPRESSION; GLIOBLASTOMA; HIGH RISK POPULATION; HUMAN; HUMAN TISSUE; LOW RISK POPULATION; MAJOR CLINICAL STUDY; MALE; OUTCOME ASSESSMENT; PRIORITY JOURNAL; TREATMENT RESPONSE; VALIDATION STUDY; AGED; ANALOGS AND DERIVATIVES; BRAIN NEOPLASMS; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC DATABASE; GENETICS; METABOLISM; MIDDLE AGED; PROGNOSIS; REGRESSION ANALYSIS; RISK FACTOR; SURVIVAL; TREATMENT OUTCOME; TUMOR CELL LINE;

AGED; BRAIN NEOPLASMS; CELL LINE, TUMOR; DACARBAZINE; DATABASES, GENETIC; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOBLASTOMA; HUMANS; MALE; MICRORNAS; MIDDLE AGED; NEOPLASM GRADING; PROGNOSIS; REGRESSION ANALYSIS; RISK FACTORS; SURVIVAL ANALYSIS; TREATMENT OUTCOME;

EID: 84923586143     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2014.11.004     Document Type: Article

References (48)

1. Alencar A.J., Malumbres R., Kozloski G.A., Advani R., Talreja N., Chinichian S., Briones J., Natkunam Y., Sehn L.H., Gascoyne R.D., Tibshirani R., Lossos I.S. MicroRNAs are independent predictors of outcome in diffuse large B-cell lymphoma patients treated with R-CHOP. Clin. Cancer Res. 2011, 17:4125-4135. 10.1158/1078-0432.CCR-11-0224.
2. Brennan C.W., Verhaak R.G.W., McKenna A., Campos B., Noushmehr H., Salama S.R., et al. The somatic genomic landscape of glioblastoma. Cell 2013, 155:462-477. 10.1016/j.cell.2013.09.034.
3. Calin G.A., Croce C.M. MicroRNA signatures in human cancers. Nat. Rev. Cancer 2006, 6:857-866. 10.1038/nrc1997.
4. Chaichana K.L., Pendleton C., Chambless L., Camara-Quintana J., Nathan J.K., Hassam-Malani L., Li G., Harsh G.R., Thompson R.C., Lim M., Quinones-Hinojosa A. Multi-institutional validation of a preoperative scoring system which predicts survival for patients with glioblastoma. J.Clin. Neurosci. 2013, 20:1422-1426. 10.1016/j.jocn.2013.02.007.
5. Cheang M.C.U., Chia S.K., Voduc D., Gao D., Leung S., Snider J., Watson M., Davies S., Bernard P.S., Parker J.S., Perou C.M., Ellis M.J., Nielsen T.O. Ki67 index, HER2 status, and prognosis of patients with luminal B breast cancer. J.Natl. Cancer Inst. 2009, 101:736-750. 10.1093/jnci/djp082.
6. Chen L., Zhang J., Han L., Zhang A., Zhang C., Zheng Y., Jiang T., Pu P., Jiang C., Kang C. Downregulation of miR-221/222 sensitizes glioma cells to temozolomide by regulating apoptosis independently of p53 status. Oncol. Rep. 2012, 27:854-860. 10.3892/or.2011.1535.
7. Favero, F., v2.14. RmiR: Package to Work with miRNAs and miRNA Targets with R.
8. Fowler A., Thomson D., Giles K., Maleki S., Mreich E., Wheeler H., Leedman P., Biggs M., Cook R., Little N., Robinson B., McDonald K. miR-124a is frequently down-regulated in glioblastoma and is involved in migration and invasion. Eur. J. Cancer 2011, 47:953-963. 10.1016/j.ejca.2010.11.026.
9. 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. 2011, 71:3563-3572. 10.1158/0008-5472.CAN-10-3568.
10. 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-signaling in glioblastoma. Cancer Discov. 2012, 2:736-749. 10.1158/2159-8290.CD-12-0111.
11. Goeman J.J. Penalized R Package, Version 0.9-42 2012.
12. Griffiths-Jones S., Saini H.K., Van Dongen S., Enright A.J. miRBase: tools for microRNA genomics. Nucleic Acids Res. 2008, 36:D154-D158.
13. Hayes J., Peruzzi P.P., Lawler S. MicroRNAs in cancer: biomarkers, functions and therapy. Trends Mol. Med. 2014, 20:460-469. 10.1016/j.molmed.2014.06.005.
14. Hummel R., Watson D.I., Smith C., Kist J., Michael M.Z., Haier J., Hussey D.J. Mir-148a improves response to chemotherapy in sensitive and resistant oesophageal adenocarcinoma and squamous cell carcinoma cells. J.Gastrointest. Surg. 2011, 15:429-438. 10.1007/s11605-011-1418-9.
15. Kaminska B., Kocyk M., Kijewska M. TGF beta signaling and its role in glioma pathogenesis. Adv. Exp. Med. Biol. 2013, 986:171-187. 10.1007/978-94-007-4719-7_9.
16. Kim J., Zhang Y., Skalski M., Hayes J., Kefas B., Schiff D., Purow B., Parsons S., Lawler S., Abounader R. microRNA-148a is a prognostic oncomiR that targets MIG6 and BIM to regulate EGFR and apoptosis in glioblastoma. Cancer Res. 2014, 74:1541-1553.
17. Kim T.-M., Huang W., Park R., Park P.J., Johnson M.D. A developmental taxonomy of glioblastoma defined and maintained by MicroRNAs. Cancer Res. 2011, 71:3387-3399. 10.1158/0008-5472.CAN-10-4117.
18. Krek A., Grun D., Poy M.N., Wolf R., Rosenberg L., Epstein E.J., MacMenamin P., da Piedade I., Gunsalus K.C., Stoffel M., Rajewsky N. Combinatorial microRNA target predictions. Nat. Genet. 2005, 37:495-500. 10.1038/ng1536.
19. Krex D., Klink B., Hartmann C., Deimling von A., Pietsch T., Simon M., Sabel M., Steinbach J.P., Heese O., Reifenberger G., Weller M., Schackert G., Network F.T.G.G. Long-term survival with glioblastoma multiforme. Brain 2007, 130:2596-2606.
20. Krol J., Loedige I., Filipowicz W. The widespread regulation of microRNA biogenesis, function and decay. Nat. Rev. Genet. 2010, 11:597-610. 10.1038/nrg2843.
21. 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. 10.1371/journal.pone.0036248.t002.
22. Lewis B.P., Burge C.B., Bartel D.P. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005, 120:15-20. 10.1016/j.cell.2004.12.035.
23. Li R., Gao K., Luo H., Wang X., Shi Y., Dong Q., Luan W., You Y. Identification of intrinsic subtype-specific prognostic microRNAs in primary glioblastoma. J.Exp. Clin.Cancer Res. 2014, 33:1-6. 10.1186/1756-9966-33-9.
24. Lo S.-S., Hung P.-S., Chen J.-H., Tu H.-F., Fang W.-L., Chen C.Y., Chen W.-T., Gong N.-R., Wu C.-W. Overexpression of miR-370 and downregulation of its novel target TGFbeta-RII contribute to the progression of gastric carcinoma. Oncogene 2012, 31:226-237. 10.1038/onc.2011.226.
25. Louis D.N., Ohgaki H., Wiestler O.D., Cavenee W.K., Burger P.C., Jouvet A., Scheithauer B.W., Kleihues P. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol. 2007, 114:97-109. 10.1007/s00401-007-0243-4.
26. Miranda K.C., Huynh T., Tay Y., Ang Y.-S., Tam W.-L., Thomson A.M., Lim B., Rigoutsos I. A pattern-based method for the identification of MicroRNA binding sites and their corresponding heteroduplexes. Cell 2006, 126:1203-1217. 10.1016/j.cell.2006.07.031.
27. Mizoguchi M., Guan Y., Yoshimoto K., Hata N., Amano T., Nakamizo A., Sasaki T. MicroRNAs in human malignant gliomas. J.Oncol. 2012, 2012:1-7. 10.1523/JNEUROSCI.4966-09.2009.
28. Mucaj V., Lee S.S., Skuli N., Giannoukos D.N., Qiu B., Eisinger-Mathason T.S.K., Nakazawa M.S., Shay J.E.S., Gopal P.P., Venneti S., Lal P., Minn A.J., Simon M.C., Mathew L.K. MicroRNA-124 expression counteracts pro-survival stress responses in glioblastoma. Oncogene 2014, 10.1038/onc.2014.168.
29. Munoz J.L., Bliss S.A., Greco S.J., Ramkissoon S.H., Ligon K.L., Rameshwar P. Delivery of functional anti-miR-9 by mesenchymal stem cell-derived exosomes to glioblastoma multiforme cells conferred chemosensitivity. Mol. Ther. Nucl. Acids 2013, 10.1038/mtna.2013.60.
30. Niyazi M., Zehentmayr F., Niemöller O.M., Eigenbrod S., Kretzschmar H., Schulze-Osthoff K., Tonn J.-C., Atkinson M., Mörtl S., Belka C. MiRNA expression patterns predict survival in glioblastoma. Radiat. Oncol. 2011, 6:153. 10.1186/1748-717X-6-153.
31. Northcott P.A., Shih D.J.H., Remke M., Cho Y.-J., Kool M., Hawkins C., Eberhart C.G., Dubuc A., Guettouche T., Cardentey Y., Bouffet E., Pomeroy S.L., Marra M., Malkin D., Rutka J.T., Korshunov A., Pfister S., Taylor M.D. Rapid, reliable, and reproducible molecular sub-grouping of clinical medulloblastoma samples. Acta Neuropathol. 2012, 123:615-626. 10.1007/s00401-011-0899-7.
32. Ohgaki H., Kleihues P. Genetic pathways to primary and secondary glioblastoma. Am. J. Pathol. 2007, 170:1445-1453. 10.2353/ajpath.2007.070011.
33. Parsons D.W., Jones S., Zhang X., Lin J.C.H., Leary R.J., Angenendt P., Mankoo P., Carter H., Siu I.-M., Gallia G.L., Olivi A., McLendon R., Rasheed B.A., Keir S., Nikolskaya T., Nikolsky Y., Busam D.A., Tekleab H., Diaz L.A., Hartigan J., Smith D.R., Strausberg R.L., Marie S.K.N., Shinjo S.M.O., Yan H., Riggins G.J., Bigner D.D., Karchin R., Papadopoulos N., Parmigiani G., Vogelstein B., Velculescu V.E., Kinzler K.W. An integrated genomic analysis of human glioblastoma multiforme. Science 2008, 321:1807-1812. 10.1126/science.1164382.
34. Rani S.B., Rathod S.S., Karthik S., Kaur N., Muzumdar D., Shiras A.S. MiR-145 functions as a tumor-suppressive RNA by targeting Sox9 and adducin 3 in human glioma cells. Neuro-oncology 2013, 15:1302-1316. 10.1093/neuonc/not090.
35. Riemenschneider M.J., Jeuken J.W.M., Wesseling P., Reifenberger G. Molecular diagnostics of gliomas: state of the art. Acta Neuropathol. 2010, 120:567-584. 10.1007/s00401-010-0736-4.
36. Song L., Liu L., Wu Z., Li Y., Ying Z., Lin C., Wu J., Hu B., Cheng S.-Y., Li M., Li J. TGF-beta induces miR-182 to sustain NF-kappaB activation in glioma subsets. J.Clin. Invest. 2012, 122:3563-3578. 10.1172/JCI62339.
37. Sorlie T., Perou C.M., Tibshirani R., Aas T., Geisler S., Johnsen H., Hastie T., Eisen M.B., van de Rijn M., Jeffrey S.S., Thorsen T., Quist H., Matese J.C., Brown P.O., Botstein D., Lonning P.E., Borresen-Dale A.L. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:10869-10874.
38. Srinivasan S., Patric I.R.P., Somasundaram K. A ten-microRNA expression signature predicts survival in glioblastoma. PLoS ONE 2011, 6:e17438. 10.1371/journal.pone.0017438.
39. Stupp R., Roila F. Malignant glioma: ESMO clinical recommendations for diagnosis, treatment and follow-up. Ann. Oncol. 2009, 20:126-128. 10.1093/annonc/mdp151.
40. Tan X., Wang S., Yang B., Zhu L., Yin B., Chao T., Zhao J., Yuan J., Qiang B., Peng X. The CREB-miR-9 negative feedback minicircuitry coordinates the migration and proliferation of glioma cells. PLoS ONE 2012, 7:e49570. 10.1371/journal.pone.0049570.s006.
41. Tang H., Bian Y., Tu C., Wang Z., Yu Z., Liu Q., Xu G., Wu M., Li G. The miR-183/96/182 cluster regulates oxidative apoptosis and sensitizes cells to chemotherapy in gliomas. Curr. Cancer Drug Targets 2013, 13:221-231.
42. The Cancer Genome Atlas - Data Portal [WWW Document]. URL: (accessed 24.04.13). http://tcga-data.nci.nih.gov/.
43. Tibshirani R. Regression shrinkage and selection via the Lasso. J.R. Stat. Soc. Ser. B-Methodol. 1996, 58:267-288. 10.1021/np300902g.
44. 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 2013, 8:e55314. the PERNO Study group. 10.1371/journal.pone.0055314.s002.
45. Vlachos I.S., Kostoulas N., Vergoulis T., Georgakilas G., Reczko M., Maragkakis M., Paraskevopoulou M.D., Prionidis K., Dalamagas T., Hatzigeorgiou A.G. DIANA miRPath v.2.0: investigating the combinatorial effect of microRNAs in pathways. Nucleic Acids Res. 2012, 40:W498-W504. 10.1093/nar/gks494.
46. Volinia S., Calin G.A., Liu C.-G., Ambs S., Cimmino A., Petrocca F., Visone R., Iorio M., Roldo C., Ferracin M., Prueitt R.L., Yanaihara N., Lanza G., Scarpa A., Vecchione A., Negrini M., Harris C.C., Croce C.M. AmicroRNA expression signature of human solid tumorsdefines cancer gene targets. Proc. Natl. Acad.Sci.U.S.A. 2006, 103:2257-2261. 10.1073/pnas.0510565103.
47. Yang Y.-P., Chien Y., Chiou G.-Y., Cherng J.-Y., Wang M.-L., Lo W.-L., Chang Y.-L., Huang P.-I., Chen Y.-W., Shih Y.-H., Chen M.-T., Chiou S.-H. Inhibition of cancer stem cell-like properties and reduced chemoradioresistance of glioblastoma using microRNA145 with cationic polyurethane-short branch PEI. Biomaterials 2012, 33:1462-1476. 10.1016/j.biomaterials.2011.10.071.
48. Zhang C.-Z., Zhang J.-X., Zhang A.-L., Shi Z.-D., Han L., Jia Z.-F., Yang W.-D., Wang G.-X., Jiang T., You Y.-P., Pu P.-Y., Cheng J.-Q., Kang C.-S. MiR-221 and miR-222 target PUMA to induce cell survival in glioblastoma. Mol. Cancer 2010, 9:229. 10.1186/1476-4598-9-229.