A novel approach to the discovery of survival biomarkers in glioblastoma using a joint analysis of DNA methylation and gene expression

References

• Wen PY, Kesari S. Malignant gliomas in adults. N Engl J Med 2008; 359:492 - 507; http://dx.doi.org/10.1056/NEJMra0708126; PMID: 18669428
   PubMed Web of Science ®Google Scholar
• Phillips HS, Kharbanda S, Chen R, Forrest WF, Soriano RH, Wu TD, Misra A, Nigro JM, Colman H, Soroceanu L, et al. Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell 2006; 9:157 - 73; http://dx.doi.org/10.1016/j.ccr.2006.02.019; PMID: 16530701
   PubMed Web of Science ®Google Scholar
• Cancer Genome Atlas Research Network. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 2008; 455:1061 - 8; http://dx.doi.org/10.1038/nature07385; PMID: 18772890
   PubMed Web of Science ®Google Scholar
• Verhaak RG, Hoadley KA, Purdom E, Wang V, Qi Y, Wilkerson MD, Miller CR, Ding L, Golub T, Mesirov JP, et al, Cancer Genome Atlas Research Network. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 2010; 17:98 - 110; http://dx.doi.org/10.1016/j.ccr.2009.12.020; PMID: 20129251
   PubMed Web of Science ®Google Scholar
• Frattini V, Trifonov V, Chan JM, Castano A, Lia M, Abate F, Keir ST, Ji AX, Zoppoli P, Niola F, et al. The integrated landscape of driver genomic alterations in glioblastoma. Nat Genet 2013; 45:1141 - 9; http://dx.doi.org/10.1038/ng.2734; PMID: 23917401
   PubMed Web of Science ®Google Scholar
• Christensen BC, Smith AA, Zheng S, Koestler DC, Houseman EA, Marsit CJ, Wiemels JL, Nelson HH, Karagas MR, Wrensch MR, et al. DNA methylation, isocitrate dehydrogenase mutation, and survival in glioma. J Natl Cancer Inst 2011; 103:143 - 53; http://dx.doi.org/10.1093/jnci/djq497; PMID: 21163902
   PubMed Web of Science ®Google Scholar
• Ehrlich M. DNA hypomethylation in cancer cells. Epigenomics 2009; 1:239 - 59; http://dx.doi.org/10.2217/epi.09.33; PMID: 20495664
   PubMed Web of Science ®Google Scholar
• Lopez-Serra P, Esteller M. DNA methylation-associated silencing of tumor-suppressor microRNAs in cancer. Oncogene 2012; 31:1609 - 22; http://dx.doi.org/10.1038/onc.2011.354; PMID: 21860412
   PubMed Web of Science ®Google Scholar
• Wan J, Oliver VF, Zhu H, Zack DJ, Qian J, Merbs SL. Integrative analysis of tissue-specific methylation and alternative splicing identifies conserved transcription factor binding motifs. Nucleic Acids Res 2013; 41:8503 - 14; http://dx.doi.org/10.1093/nar/gkt652; PMID: 23887936
   PubMed Web of Science ®Google Scholar
• Icli B, Wara AK, Moslehi J, Sun X, Plovie E, Cahill M, Marchini JF, Schissler A, Padera RF, Shi J, et al. MicroRNA-26a regulates pathological and physiological angiogenesis by targeting BMP/SMAD1 signaling. Circ Res 2013; 113:1231 - 41; http://dx.doi.org/10.1161/CIRCRESAHA.113.301780; PMID: 24047927
   PubMed Web of Science ®Google Scholar
• Noushmehr H, Weisenberger DJ, Diefes K, Phillips HS, Pujara K, Berman BP, Pan F, Pelloski CE, Sulman EP, Bhat KP, et al, Cancer Genome Atlas Research Network. Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell 2010; 17:510 - 22; http://dx.doi.org/10.1016/j.ccr.2010.03.017; PMID: 20399149
   PubMed Web of Science ®Google Scholar
• Rivenbark AG, Coleman WB. Dissecting the molecular mechanisms of cancer through bioinformatics-based experimental approaches. J Cell Biochem 2007; 101:1074 - 86; http://dx.doi.org/10.1002/jcb.21283; PMID: 17372928
   PubMed Web of Science ®Google Scholar
• Ferté C, Trister AD, Huang E, Bot BM, Guinney J, Commo F, Sieberts S, André F, Besse B, Soria JC, et al. Impact of bioinformatic procedures in the development and translation of high-throughput molecular classifiers in oncology. Clin Cancer Res 2013; 19:4315 - 25; http://dx.doi.org/10.1158/1078-0432.CCR-12-3937; PMID: 23780890
   PubMed Web of Science ®Google Scholar
• Wang W, Baladandayuthapani V, Morris JS, Broom BM, Manyam G, Do KA. iBAG: integrative Bayesian analysis of high-dimensional multiplatform genomics data. Bioinformatics 2013; 29:149 - 59; http://dx.doi.org/10.1093/bioinformatics/bts655; PMID: 23142963
   PubMed Web of Science ®Google Scholar
• Etcheverry A, Aubry M, de Tayrac M, Vauleon E, Boniface R, Guenot F, Saikali S, Hamlat A, Riffaud L, Menei P, et al. DNA methylation in glioblastoma: impact on gene expression and clinical outcome. BMC Genomics 2010; 11:701; http://dx.doi.org/10.1186/1471-2164-11-701; PMID: 21156036
   PubMed Web of Science ®Google Scholar
• Rao SK, Edwards J, Joshi AD, Siu IM, Riggins GJ. A survey of glioblastoma genomic amplifications and deletions. J Neurooncol 2010; 96:169 - 79; http://dx.doi.org/10.1007/s11060-009-9959-4; PMID: 19609742
   PubMed Web of Science ®Google Scholar
• Chattopadhyay S, Tracy E, Liang P, Robledo O, Rose-John S, Baumann H. Interleukin-31 and oncostatin-M mediate distinct signaling reactions and response patterns in lung epithelial cells. J Biol Chem 2007; 282:3014 - 26; http://dx.doi.org/10.1074/jbc.M609655200; PMID: 17148439
   PubMed Web of Science ®Google Scholar
• Priester M, Copanaki E, Vafaizadeh V, Hensel S, Bernreuther C, Glatzel M, Seifert V, Groner B, Kögel D, Weissenberger J. STAT3 silencing inhibits glioma single cell infiltration and tumor growth. Neuro Oncol 2013; 15:840 - 52; http://dx.doi.org/10.1093/neuonc/not025; PMID: 23486688
   PubMed Web of Science ®Google Scholar
• Papadopoulos MC, Verkman AS. Aquaporin water channels in the nervous system. Nat Rev Neurosci 2013; 14:265 - 77; http://dx.doi.org/10.1038/nrn3468; PMID: 23481483
   PubMed Web of Science ®Google Scholar
• Bonomini F, Rezzani R. Aquaporin and blood brain barrier. Curr Neuropharmacol 2010; 8:92 - 6; http://dx.doi.org/10.2174/157015910791233132; PMID: 21119879
   PubMed Web of Science ®Google Scholar
• Wolburg H, Noell S, Fallier-Becker P, Mack AF, Wolburg-Buchholz K. The disturbed blood-brain barrier in human glioblastoma. Mol Aspects Med 2012; 33:579 - 89; http://dx.doi.org/10.1016/j.mam.2012.02.003; PMID: 22387049
   PubMed Web of Science ®Google Scholar
• El Hindy N, Bankfalvi A, Herring A, Adamzik M, Lambertz N, Zhu Y, Siffert W, Sure U, Sandalcioglu IE. Correlation of aquaporin-1 water channel protein expression with tumor angiogenesis in human astrocytoma. Anticancer Res 2013; 33:609 - 13; PMID: 23393355
   PubMed Web of Science ®Google Scholar
• Saadoun S, Papadopoulos MC, Hara-Chikuma M, Verkman AS. Impairment of angiogenesis and cell migration by targeted aquaporin-1 gene disruption. Nature 2005; 434:786 - 92; http://dx.doi.org/10.1038/nature03460; PMID: 15815633
   PubMed Web of Science ®Google Scholar
• Sepramaniam S, Armugam A, Lim KY, Karolina DS, Swaminathan P, Tan JR, Jeyaseelan K. MicroRNA 320a functions as a novel endogenous modulator of aquaporins 1 and 4 as well as a potential therapeutic target in cerebral ischemia. J Biol Chem 2010; 285:29223 - 30; http://dx.doi.org/10.1074/jbc.M110.144576; PMID: 20628061
   PubMed Web of Science ®Google Scholar
• Blagitko N, Mergenthaler S, Schulz U, Wollmann HA, Craigen W, Eggermann T, Ropers HH, Kalscheuer VM. Human GRB10 is imprinted and expressed from the paternal and maternal allele in a highly tissue- and isoform-specific fashion. Hum Mol Genet 2000; 9:1587 - 95; http://dx.doi.org/10.1093/hmg/9.11.1587; PMID: 10861285
   PubMed Web of Science ®Google Scholar
• Monk D, Arnaud P, Frost J, Hills FA, Stanier P, Feil R, Moore GE. Reciprocal imprinting of human GRB10 in placental trophoblast and brain: evolutionary conservation of reversed allelic expression. Hum Mol Genet 2009; 18:3066 - 74; http://dx.doi.org/10.1093/hmg/ddp248; PMID: 19487367
   PubMed Web of Science ®Google Scholar
• Yu Y, Yoon SO, Poulogiannis G, Yang Q, Ma XM, Villén J, Kubica N, Hoffman GR, Cantley LC, Gygi SP, et al. Phosphoproteomic analysis identifies Grb10 as an mTORC1 substrate that negatively regulates insulin signaling. Science 2011; 332:1322 - 6; http://dx.doi.org/10.1126/science.1199484; PMID: 21659605
   PubMed Web of Science ®Google Scholar
• Nord H, Hartmann C, Andersson R, Menzel U, Pfeifer S, Piotrowski A, Bogdan A, Kloc W, Sandgren J, Olofsson T, et al. Characterization of novel and complex genomic aberrations in glioblastoma using a 32K BAC array. Neuro Oncol 2009; 11:803 - 18; http://dx.doi.org/10.1215/15228517-2009-013; PMID: 19304958
   PubMed Web of Science ®Google Scholar
• Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M, Kros JM, Hainfellner JA, Mason W, Mariani L, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 2005; 352:997 - 1003; http://dx.doi.org/10.1056/NEJMoa043331; PMID: 15758010
   PubMed Web of Science ®Google Scholar
• Weller M, Felsberg J, Hartmann C, Berger H, Steinbach JP, Schramm J, Westphal M, Schackert G, Simon M, Tonn JC, et al. Molecular predictors of progression-free and overall survival in patients with newly diagnosed glioblastoma: a prospective translational study of the German Glioma Network. J Clin Oncol 2009; 27:5743 - 50; http://dx.doi.org/10.1200/JCO.2009.23.0805; PMID: 19805672
   PubMed Web of Science ®Google Scholar
• Silber JR, Bobola MS, Ghatan S, Blank A, Kolstoe DD, Berger MS. O6-methylguanine-DNA methyltransferase activity in adult gliomas: relation to patient and tumor characteristics. Cancer Res 1998; 58:1068 - 73; PMID: 9500473
   PubMed Web of Science ®Google Scholar
• Melguizo C, Prados J, González B, Ortiz R, Concha A, Alvarez PJ, Madeddu R, Perazzoli G, Oliver JA, López R, et al. MGMT promoter methylation status and MGMT and CD133 immunohistochemical expression as prognostic markers in glioblastoma patients treated with temozolomide plus radiotherapy. J Transl Med 2012; 10:250; http://dx.doi.org/10.1186/1479-5876-10-250; PMID: 23245659
   PubMed Web of Science ®Google Scholar
• Zheng S, Houseman EA, Morrison Z, Wrensch MR, Patoka JS, Ramos C, Haas-Kogan DA, McBride S, Marsit CJ, Christensen BC, et al. DNA hypermethylation profiles associated with glioma subtypes and EZH2 and IGFBP2 mRNA expression. Neuro Oncol 2011; 13:280 - 9; http://dx.doi.org/10.1093/neuonc/noq190; PMID: 21339190
   PubMed Web of Science ®Google Scholar
• Costa BM, Caeiro C, Guimarães I, Martinho O, Jaraquemada T, Augusto I, Castro L, Osório L, Linhares P, Honavar M, et al. Prognostic value of MGMT promoter methylation in glioblastoma patients treated with temozolomide-based chemoradiation: a Portuguese multicentre study. Oncol Rep 2010; 23:1655 - 62; PMID: 20428822
   PubMed Web of Science ®Google Scholar
• Oberstadt MC, Bien-Möller S, Weitmann K, Herzog S, Hentschel K, Rimmbach C, Vogelgesang S, Balz E, Fink M, Michael H, et al. Epigenetic modulation of the drug resistance genes MGMT, ABCB1 and ABCG2 in glioblastoma multiforme. BMC Cancer 2013; 13:617; http://dx.doi.org/10.1186/1471-2407-13-617; PMID: 24380367
   PubMed Web of Science ®Google Scholar
• Cecener G, Tunca B, Egeli U, Bekar A, Tezcan G, Erturk E, Bayram N, Tolunay S. The promoter hypermethylation status of GATA6, MGMT, and FHIT in glioblastoma. Cell Mol Neurobiol 2012; 32:237 - 44; http://dx.doi.org/10.1007/s10571-011-9753-7; PMID: 21928112
   PubMed Web of Science ®Google Scholar
• Houseman EA, Christensen BC, Yeh RF, Marsit CJ, Karagas MR, Wrensch M, Nelson HH, Wiemels J, Zheng S, Wiencke JK, et al. Model-based clustering of DNA methylation array data: a recursive-partitioning algorithm for high-dimensional data arising as a mixture of beta distributions. BMC Bioinformatics 2008; 9:365; http://dx.doi.org/10.1186/1471-2105-9-365; PMID: 18782434
   PubMed Web of Science ®Google Scholar
• VanderWeele TJ. Causal mediation analysis with survival data. Epidemiology 2011; 22:582 - 5; http://dx.doi.org/10.1097/EDE.0b013e31821db37e; PMID: 21642779
   PubMed Web of Science ®Google Scholar
• Johnson WE, Li C, Rabinovic A. Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics 2007; 8:118 - 27; http://dx.doi.org/10.1093/biostatistics/kxj037; PMID: 16632515
   PubMed Web of Science ®Google Scholar
• Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc, B 1995; 57:289 - 300
   Google Scholar
• Ruan B, Pong K, Jow F, Bowlby M, Crozier RA, Liu D, Liang S, Chen Y, Mercado ML, Feng X, et al. Binding of rapamycin analogs to calcium channels and FKBP52 contributes to their neuroprotective activities. Proc Natl Acad Sci U S A 2008; 105:33 - 8; http://dx.doi.org/10.1073/pnas.0710424105; PMID: 18162540
   PubMed Web of Science ®Google Scholar
• Hanissian SH, Teng B, Akbar U, Janjetovic Z, Zhou Q, Duntsch C, Robertson JH. Regulation of myeloid leukemia factor-1 interacting protein (MLF1IP) expression in glioblastoma. Brain Res 2005; 1047:56 - 64; http://dx.doi.org/10.1016/j.brainres.2005.04.017; PMID: 15893739
   PubMed Web of Science ®Google Scholar
• Zagzag D, Salnikow K, Chiriboga L, Yee H, Lan L, Ali MA, Garcia R, Demaria S, Newcomb EW. Downregulation of major histocompatibility complex antigens in invading glioma cells: stealth invasion of the brain. Lab Invest 2005; 85:328 - 41; http://dx.doi.org/10.1038/labinvest.3700233; PMID: 15716863
   PubMed Web of Science ®Google Scholar
• Halestrap AP. The SLC16 gene family - structure, role and regulation in health and disease. Mol Aspects Med 2013; 34:337 - 49; http://dx.doi.org/10.1016/j.mam.2012.05.003; PMID: 23506875
   PubMed Web of Science ®Google Scholar
• Miranda-Gonçalves V, Honavar M, Pinheiro C, Martinho O, Pires MM, Pinheiro C, Cordeiro M, Bebiano G, Costa P, Palmeirim I, et al. Monocarboxylate transporters (MCTs) in gliomas: expression and exploitation as therapeutic targets. Neuro Oncol 2013; 15:172 - 88; http://dx.doi.org/10.1093/neuonc/nos298; PMID: 23258846
   PubMed Web of Science ®Google Scholar
• Colen CB, Shen Y, Ghoddoussi F, Yu P, Francis TB, Koch BJ, Monterey MD, Galloway MP, Sloan AE, Mathupala SP. Metabolic targeting of lactate efflux by malignant glioma inhibits invasiveness and induces necrosis: an in vivo study. Neoplasia 2011; 13:620 - 32; PMID: 21750656
   PubMed Web of Science ®Google Scholar
• Atkinson GP, Nozell SE, Benveniste ET. NF-kappaB and STAT3 signaling in glioma: targets for future therapies. Expert Rev Neurother 2010; 10:575 - 86; http://dx.doi.org/10.1586/ern.10.21; PMID: 20367209
   PubMed Web of Science ®Google Scholar
• Smith SJ, Tilly H, Ward JH, Macarthur DC, Lowe J, Coyle B, Grundy RG. CD105 (Endoglin) exerts prognostic effects via its role in the microvascular niche of paediatric high grade glioma. Acta Neuropathol 2012; 124:99 - 110; http://dx.doi.org/10.1007/s00401-012-0952-1; PMID: 22311740
   PubMed Web of Science ®Google Scholar
• Akhtar S, McIntosh P, Bryan-Sisneros A, Barratt L, Robertson B, Dolly JO. A functional spliced-variant of beta 2 subunit of Kv1 channels in C6 glioma cells and reactive astrocytes from rat lesioned cerebellum. Biochemistry 1999; 38:16984 - 92; http://dx.doi.org/10.1021/bi992114x; PMID: 10606534
   PubMed Web of Science ®Google Scholar
• Yang X, Zhang Y, Li S, Liu C, Jin Z, Wang Y, Ren F, Chang Z. Rab21 attenuates EGF-mediated MAPK signaling through enhancing EGFR internalization and degradation. Biochem Biophys Res Commun 2012; 421:651 - 7; http://dx.doi.org/10.1016/j.bbrc.2012.04.049; PMID: 22525675
   PubMed Web of Science ®Google Scholar
• Totong R, Schell T, Lescroart F, Ryckebüsch L, Lin YF, Zygmunt T, Herwig L, Krudewig A, Gershoony D, Belting HG, et al. The novel transmembrane protein Tmem2 is essential for coordination of myocardial and endocardial morphogenesis. Development 2011; 138:4199 - 205; http://dx.doi.org/10.1242/dev.064261; PMID: 21896630
   PubMed Web of Science ®Google Scholar
• Smith KA, Lagendijk AK, Courtney AD, Chen H, Paterson S, Hogan BM, Wicking C, Bakkers J. Transmembrane protein 2 (Tmem2) is required to regionally restrict atrioventricular canal boundary and endocardial cushion development. Development 2011; 138:4193 - 8; http://dx.doi.org/10.1242/dev.065375; PMID: 21896629
   PubMed Web of Science ®Google Scholar
• Halestrap AP, Meredith D. The SLC16 gene family-from monocarboxylate transporters (MCTs) to aromatic amino acid transporters and beyond. Pflugers Arch 2004; 447:619 - 28; http://dx.doi.org/10.1007/s00424-003-1067-2; PMID: 12739169
   PubMed Web of Science ®Google Scholar