Prognostic microRNAs in high-grade glioma reveal a link to oligodendrocyte precursor differentiation

Oncoscience

Volumn 2, Issue 3, 2015, Pages 252-262

  Hayes, Josie ^a   Thygesen, Helene ^a   Droop, Alastair ^a   Hughes, Thomas A ^b   Westhead, David ^b   Lawler, Sean E ^c   Wurdak, Heiko ^a   Short, Susan C ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b UNIVERSITY OF LEEDS   (United Kingdom)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Astrocytoma; Glioblastoma; Glioma; MicroRNA; Oligodendrocyte; Prognosis

Indexed keywords

EID: 84943401362     PISSN: None     EISSN: 23314737     Source Type: Journal    
DOI: 10.18632/oncoscience.112     Document Type: Article

References (55)

1. Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, Scheithauer BW, Kleihues P. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol. 2007; 114(2):97-109.
2. Ohgaki H, Kleihues P. Genetic pathways to primary and secondary glioblastoma. Am J Pathol. 2007; 170(5):1445-1453.
3. Smoll NR, Hamilton B. Incidence and relative survival of anaplastic astrocytomas. Neuro-oncology. 2014; 16(10):1400-1407.
4. Weller M, Stupp R, Hegi ME, van den Bent M, Tonn JC, Sanson M, Wick W, Reifenberger G. Personalized care in neuro-oncology coming of age: why we need MGMT and 1p/19q testing for malignant glioma patients in clinical practice. Neuro-oncology. 2012;14(4):100-108.
5. Killela PJ, Pirozzi CJ, Reitman ZJ, Jones S, Rasheed BA, Lipp E, Friedman H, Friedman AH, He Y, McLendon RE, Bigner DD, Yan H. The genetic landscape of anaplastic astrocytoma. Oncotarget. 2013;5(6):1452-1457.
6. Riemenschneider MJ, Jeuken JWM, Wesseling P, Reifenberger G. Molecular diagnostics of gliomas: state of the art. Acta Neuropathol. 2010;120(5):567-584.
7. Noushmehr H, Weisenberger DJ, Diefes K, Phillips HS, Pujara K, Berman BP, Pan F, Pelloski CE, Sulman EP, Bhat KP, Verhaak RGW, Hoadley KA, Hayes DN, Perou CM, Schmidt HK, Ding L, Wilson RK, Van Den Berg D, Shen H, Bengtsson H, Neuvial P, Cope LM, Buckley J, Herman JG, Baylin SB, Laird PW, Aldape KD. Identification of a CpG Island Methylator Phenotype that Defines a Distinct Subgroup of Glioma. Cancer Cell. 2010;17(5):510-522.
8. Verhaak RGW, Hoadley KA, Purdom E, Wang V, Qi Y, Wilkerson MD, Miller CR, Ding L, Golub T, Mesirov JP, Alexe G, Lawrence M, O'Kelly M, Tamayo P et al. Integrated Genomic Analysis Identifies Clinically Relevant Subtypes of Glioblastoma Characterized by Abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell. 2010;17(1):98-110.
9. Kim T-M, Huang W, Park R, Park PJ, Johnson MD. A Developmental Taxonomy of Glioblastoma Defined and Maintained by MicroRNAs. Cancer Res. 2011;71(9):3387-3399.
10. Cancer Genome Atlas network. Comprehensive molecular portraits of human breast tumours. Nature. 2012; 490(7418):61-70.
11. Brennan CW, Verhaak RGW, McKenna A, Campos B, Noushmehr H, Salama SR, Zheng S, Chakravarty D, Sanborn JZ, Berman SH, Beroukhim R, Bernard B, Wu C-J, et al. The Somatic Genomic Landscape of Glioblastoma. Cell. 2013;155(2):462-477.
12. Ozawa T, Riester M, Cheng Y-K, Huse JT, Squatrito M, Helmy K, Charles N, Michor F, Holland EC. Most Human Non-GCIMP Glioblastoma Subtypes Evolve from a Common Proneural-like Precursor Glioma. Cancer Cell. 2014;26(2):288-300.
13. Dirks PB. Brain tumor stem cells: the cancer stem cell hypothesis writ large. Molecular Oncology. 2010(5):420-430.
14. Garrido W, Rocha JD, Jaramillo C, Fernandez K, Oyarzun C, Martin RS, Quezada C. Chemoresistance in high-grade gliomas: relevance of adenosine signalling in stem-like cells of glioblastoma multiforme. Curr Drug Targets. 2014;15(10):931-942.
15. Waghmare I, Roebke A, Minata M, Kango-Singh M, Nakano I. Intercellular Cooperation and Competition in Brain Cancers: Lessons From Drosophila and Human Studies. Stem Cells Transl Med. 2014; 2014-0086.
16. Auffinger B, Tobias AL, Han Y, Lee G, Guo D, Dey M, Lesniak MS, Ahmed AU. Conversion of differentiated cancer cells into cancer stem-like cells in a glioblastoma model after primary chemotherapy. Cell Death Differ. 2014;21(7):1119-1131.
17. Godlewski J, Bronisz A, Nowicki MO, Chiocca EA, Lawler S. microRNA-451: A conditional switch controlling glioma cell proliferation and migration. Cell Cycle. 2010;9(14):2742-2748.
18. O'Carroll D, Schaefer A. General Principals of miRNA Biogenesis and Regulation in the Brain. Neuropsychopharmacology. 2013;38(1):39-54.
19. Stahlhut C, Slack FJ. MicroRNAs and the cancer phenotype: profiling, signatures and clinical implications. Genome Med. 2013;5(12):111.
20. Schraivogel D, Weinmann L, Beier D, Tabatabai G, Eichner A, Zhu JY, Anton M, Sixt M, Weller M, Beier CP, Meister G. CAMTA1 is a novel tumour suppressor regulated by miR-9/9* in glioblastoma stem cells. EMBO J. 2011;30(20):4309-4322.
21. Stappert L, Roese-Koerner B, Brustle O. The role of microRNAs in human neural stem cells, neuronal differentiation and subtype specification. Cell Tissue Res. 2014; e25172833.
22. Brower JV, Clark PA, Lyon W, Kuo JS. MicroRNAs in cancer: Glioblastoma and glioblastoma cancer stem cells. Neurochem Int. 2014;77C:68-77.
23. Aldaz B, Sagardoy A, Nogueira L, Guruceaga E, Grande L, Huse JT, Aznar MA, Diez-Valle R, Tejada-Solis S, Alonso MM, Fernandez-Luna JL, Martinez-Climent JA, Malumbres R. Involvement of miRNAs in the differentiation of human glioblastoma multiforme stem-like cells. PLoS ONE. 2013;8(10):e77098.
24. Francis N, Moore M, Rutter GA, Burns C. The role of microRNAs in the pancreatic differentiation of pluripotent stem cells. Microrna. 2014;3(1):54-63.
25. Guo W. Breast cancer stem cells: regulatory networks, stem cell niches, and disease relevance. Stem Cells Transl Med. 2014;3(8):942-948.
26. Kane NM, Thrasher AJ, Angelini GD, Emanueli C. MicroRNAs as modulators of stem cells and angiogenesis. Stem cells. 2014;32(5):1059-1066.
27. Letzen BS, Liu C, Thakor NV, Gearhart JD, All AH, Kerr CL. MicroRNA Expression Profiling of Oligodendrocyte Differentiation from Human Embryonic Stem Cells. PLoS ONE. 2010;5(5):e10480.
28. The Cancer Genome Atlas-Data Portal. Available from: http://tcga-data.nci.nih.gov/.
29. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2009;26(1):139-140.
30. Smyth GK. Limma: linear models for microarray data. 2005.
31. Benjamini Y, Hochberg Y. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. Journal of the Royal Statistical Society Series B-Methodological; 1995;57(1):289-300.
32. Ujifuku K, Mitsutake N, Takakura S, Matsuse M, Saenko V, Suzuki K, Hayashi K, Matsuo T, Kamada K, Nagata I, Yamashita S. miR-195, miR-455-3p and miR-10a( *) are implicated in acquired temozolomide resistance in glioblastoma multiforme cells. Cancer Letters. 2010;296(2):241-248.
33. Asuthkar S, Velpula KK, Chetty C, Gorantla B, Rao JS. Epigenetic regulation of miRNA-211 by MMP-9 governs glioma cell apoptosis, chemosensitivity and radiosensitivity. Oncotarget. 2012;3(11):1439-1454.
34. Zhu S, Wu H, Wu F, Nie D, Sheng S, Mo Y-Y. MicroRNA-21 targets tumor suppressor genes in invasion and metastasis. Cell Res. 2008;18(3):350-359.
35. 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(5):1541-1553.
36. Quintavalle C, Garofalo M, Zanca C, Romano G, Iaboni M, del Basso De Caro M, Martinez-Montero JC, Incoronato M, Nuovo G, Croce CM, Condorelli G. miR-221/222 overexpession in human glioblastoma increases invasiveness by targeting the protein phosphate PTPmu. Oncogene. 2012;31(7):858-868.
37. Miranda KC, Huynh T, Tay Y, Ang Y-S, Tam W-L, Thomson AM, Lim B, Rigoutsos I. A Pattern-Based Method for the Identification of MicroRNA Binding Sites and Their Corresponding Heteroduplexes. Cell. 2006;126(6):1203-1217.
38. Krek A, Grun D, Poy MN, Wolf R, Rosenberg L, Epstein EJ, MacMenamin P, da Piedade I, Gunsalus KC, Stoffel M, Rajewsky N. Combinatorial microRNA target predictions. Nat Genet. 2005;37(5):495-500.
39. Lewis BP, Shih I-H, Jones-Rhoades MW, Bartel DP, Burge CB. Prediction of mammalian microRNA targets. Cell. 2003;115(7):787-798.
40. Risueño RM, Sachlos E, Lee J-H, Lee JB, Hong S-H, Szabo E, Bhatia M. Inability of human induced pluripotent stem cell-hematopoietic derivatives to downregulate microRNAs in vivo reveals a block in xenograft hematopoietic regeneration. Stem Cells. 2012;30(2):131-139.
41. Goff LA, Davila J, Swerdel MR, Moore JC, Cohen RI, Wu H, Sun YE, Hart RP. Ago2 immunoprecipitation identifies predicted microRNAs in human embryonic stem cells and neural precursors. PLoS ONE. 2009;4(9):e7192.
42. Sottoriva A, Spiteri I, Piccirillo SG, Touloumis A, Collins VP, Marioni JC, Curtis C, Watts C, Tavaré S. Intratumor heterogeneity in human glioblastoma reflects cancer evolutionary dynamics. Proc Natl Acad Sci USA. National Acad Sciences; 2013;110(10):4009-4014.
43. Patel AP, Tirosh I, Trombetta JJ, Shalek AK, Gillespie SM, Wakimoto H, Cahill DP, Nahed BV, Curry WT, Martuza RL, Louis DN, Rozenblatt-Rosen O, Suva ML, Regev A, Bernstein BE. Single-cell RNA-seq highlights intratumoral heterogeneity in primary glioblastoma. Science. 2014;344(6190):1396-1401.
44. Lei L, Sonabend AM, Guarnieri P, Soderquist C, Ludwig T, Rosenfeld S, Bruce JN, Canoll P. Glioblastoma Models Reveal the Connection between Adult Glial Progenitors and the Proneural Phenotype. PLoS ONE. 2011;6(5):e20041.
45. Sukhdeo K, Hambardzumyan D, Rich JN. Glioma Development:Where Did It All Go Wrong? Cell. 2011;146(2):187-188.
46. Liu C, Sage JC, Miller MR, Verhaak RGW, Hippenmeyer S, Vogel H, Foreman O, Bronson RT, Nishiyama A, Luo L, Zong H. Mosaic analysis with double markers reveals tumor cell of origin in glioma. Cell. 2011;146(2):209-221.
47. Hall JS, Taylor J, Valentine HR, Irlam JJ, Eustace A, Hoskin PJ, Miller CJ, West CML. Enhanced stability of microRNA expression facilitates classification of FFPE tumour samples exhibiting near total mRNA degradation. Br J Cancer. 2012;107(4):684-694.
48. Huang Y, Hoffman C, Rajappa P, Kim JH, Hu W, Huse J, Tang Z, Li X, Weksler B, Bromberg J, Lyden DC, Greenfield JP. Oligodendrocyte Progenitor Cells Promote Neovascularization in Glioma by Disrupting the Blood-Brain Barrier. Cancer Res. 2014;7 (4):1011-21.
49. Sugiarto S, Persson AI, Munoz EG, Waldhuber M, Lamagna C, Andor N, Hanecker P, Ayers-Ringler J, Phillips J, Siu J, Lim DA, Vandenberg S, Stallcup W, Berger MS, Bergers G, Weiss WA, Petritsch C. Asymmetry-Defective Oligodendrocyte Progenitors Are Glioma Precursors. Cancer Cell. 2011;20(3):328-340.
50. Zhang Y, Chen K, Sloan SA, Bennett ML, Scholze AR, O'Keeffe S, Phatnani HP, Guarnieri P, Caneda C, Ruderisch N, Deng S, Liddelow SA, Zhang C, et al. An RNASequencing Transcriptome and Splicing Database of Glia, Neurons, and Vascular Cells of the Cerebral Cortex. Journal of Neuroscience. 2014;34(36):11929-11947.
51. Havrda MC, Paolella BR, Ran C, Jering KS, Wray CM, Sullivan JM, Nailor A, Hitoshi Y, Israel MA. Id2 mediates oligodendrocyte precursor cell maturation arrest and is tumorigenic in a PDGF-rich microenvironment. Cancer Res. 2014;74(6):1822-1832.
52. 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(12):2186-2190.
53. Srinivasan S, Patric IRP, Somasundaram K. A tenmicroRNA expression signature predicts survival in glioblastoma. PLoS ONE. 2011;6(3):e17438.
54. Zhang W, Zhang J, Yan W, You G, Bao Z, Li S, Kang C, Jiang C, You Y, Zhang Y, Chen CC, Song SW, Jiang T. Whole-genome microRNA expression profiling identifies a 5-microRNA signature as a prognostic biomarker in Chinese patients with primary glioblastoma multiforme. Cancer. 2012;119(4):814-824.
55. Favero F. RmiR: Package to work with miRNAs and miRNA targets with R. R package version 1.20.0.