Integrated genomic characterization of IDH1-mutant glioma malignant progression

Nature Genetics

Volumn 48, Issue 1, 2015, Pages 59-66

  Bai, Hanwen ^a   Harmanci, Akdes Serin ^a   Erson Omay, E Zeynep ^a   Li, Jie ^a   Coşkun, Süleyman ^a   Simon, Matthias ^b   Krischek, Boris ^c   Özduman, Koray ^d   Omay, S Bülent ^a   Sorensen, Eric A ^e   Turcan, Sevin ^f   Bakirciʇlu, Mehmet ^d   Carrión Grant, Geneive ^a   Murray, Phillip B ^a   Clark, Victoria E ^a   Ercan Sencicek, A Gulhan ^a   Knight, James ^a   Sencar, Leman ^a   Altinok, Selin ^a   Kaulen, Leon D ^a   Gülez, Burcu ^a   Timmer, Marco ^c   Schramm, Johannes ^b   Mishra Gorur, Ketu ^a   Henegariu, Octavian ^a   Moliterno, Jennifer ^a   Louvi, Angeliki ^a   Chan, Timothy A ^f   Tannheimer, Stacey L ^e   Pamir, M Necmettin ^d   Vortmeyer, Alexander O ^a   Bilguvar, Kaya ^a   Yasuno, Katsuhito ^a   Günel, Murat ^a,g   more..

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF BONN   (Germany)

^c UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

^d ACIBADEM UNIVERSITY   (Turkey)

^e GILEAD SCIENCES   (United States)

^f MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^g YALE CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; ISOCITRATE DEHYDROGENASE 1; MYC PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; POLYCOMB REPRESSIVE COMPLEX 2; RAS PROTEIN; FORKHEAD BOX PROTEIN M1; FORKHEAD TRANSCRIPTION FACTOR; FOXM1 PROTEIN, HUMAN; IDH1 PROTEIN, HUMAN; ISOCITRATE DEHYDROGENASE; NOTCH1 PROTEIN, HUMAN; NOTCH1 RECEPTOR;

ARTICLE; CLINICAL ARTICLE; CLONAL EVOLUTION; CONTROLLED STUDY; COPY NUMBER VARIATION; EMBRYONIC STEM CELL; EPIGENETICS; GENE EXPRESSION; GENE SILENCING; GENOMICS; GLIOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; METHYLATION; MOLECULAR MECHANICS; PRIORITY JOURNAL; TUMOR GROWTH; CENTRAL NERVOUS SYSTEM TUMOR; DNA METHYLATION; GENE DOSAGE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MUTATION; ONCOGENE MYC; PATHOLOGY;

CENTRAL NERVOUS SYSTEM NEOPLASMS; DNA METHYLATION; EMBRYONIC STEM CELLS; FORKHEAD BOX PROTEIN M1; FORKHEAD TRANSCRIPTION FACTORS; GENE DOSAGE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, MYC; GLIOMA; HUMANS; ISOCITRATE DEHYDROGENASE; MUTATION; PHOSPHATIDYLINOSITOL 3-KINASES; RECEPTOR, NOTCH1;

EID: 84949035547     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.3457     Document Type: Article

References (83)

1. Ostrom, Q.T., et al. CBTRUS statistical report: primary brain and central nervous system tumors diagnosed in the United States in 2007-2011. Neuro-oncol. 16 (suppl. 4), iv1-iv63 (2014).
2. Louis, D.N., et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol. 114, 97-109 (2007).
3. Claus, E.B., & Black, P.M. Survival rates and patterns of care for patients diagnosed with supratentorial low-grade gliomas. Cancer 106, 1358-1363 (2006).
4. Stupp, R., et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med. 352, 987-996 (2005).
5. Stupp, R., et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol. 10, 459-466 (2009).
6. Suzuki, H., et al. Mutational landscape and clonal architecture in grade II and III gliomas. Nat. Genet. 47, 458-468 (2015).
7. Cancer Genome Atlas Research Network. Comprehensive, integrative genomic analysis of diffuse lower-grade gliomas. N. Engl. J. Med. 372, 2481-2498 (2015).
8. Eckel-Passow, J.E., et al. Glioma groups based on 1p/19q, IDH, and TERT promoter mutations in tumors. N. Engl. J. Med. 372, 2499-2508 (2015).
9. Turcan, S., et al. IDH1 mutation is sufficient to establish the glioma hypermethylator phenotype. Nature 483, 479-483 (2012).
10. Jaeckle, K.A., et al. Transformation of low grade glioma and correlation with outcome: an NCCTG database analysis. J. Neurooncol. 104, 253-259 (2011).
11. Artavanis-Tsakonas, S. Notch signaling: cell fate control and signal integration in development. Science 284, 770-776 (1999).
12. Stransky, N., et al. The mutational landscape of head and neck squamous cell carcinoma. Science 333, 1157-1160 (2011).
13. Agrawal, N., et al. Exome sequencing of head and neck squamous cell carcinoma reveals inactivating mutations in NOTCH1. Science 333, 1154-1157 (2011).
14. Pickering, C.R., et al. Mutational landscape of aggressive cutaneous squamous cell carcinoma. Clin. Cancer Res. 20, 6582-6592 (2014).
15. Cordle, J., et al. A conserved face of the Jagged/Serrate DSL domain is involved in Notch trans-Activation and cis-inhibition. Nat. Struct. Mol. Biol. 15, 849-857 (2008).
16. Harvey, K.F., Zhang, X., & Thomas, D.M. The Hippo pathway and human cancer. Nat. Rev. Cancer 13, 246-257 (2013).
17. Johnson, B.E., et al. Mutational analysis reveals the origin and therapy-Driven evolution of recurrent glioma. Science 343, 189-193 (2014).
18. Mäkinen, N., et al. MED12, the mediator complex subunit 12 gene, is mutated at high frequency in uterine leiomyomas. Science 334, 252-255 (2011).
19. Barbieri, C.E., et al. Exome sequencing identifies recurrent SPOP, FOXA1 and MED12 mutations in prostate cancer. Nat. Genet. 44, 685-689 (2012).
20. Lim, W.K., et al. Exome sequencing identifies highly recurrent MED12 somatic mutations in breast fibroadenoma. Nat. Genet. 46, 877-880 (2014).
21. Hill, D.A., et al. DICER1 mutations in familial pleuropulmonary blastoma. Science 325, 965 (2009).
22. Kumar, M.S., et al. Dicer1 functions as a haploinsufficient tumor suppressor. Genes Dev. 23, 2700-2704 (2009).
23. Labreche, K., et al. TCF12 is mutated in anaplastic oligodendroglioma. Nat. Commun. 6, 7207 (2015).
24. Comino-Méndez, I., et al. Exome sequencing identifies MAX mutations as a cause of hereditary pheochromocytoma. Nat. Genet. 43, 663-667 (2011).
25. van Thuijl, H.F., et al. Spatial and temporal evolution of distal 10q deletion, a prognostically unfavorable event in diffuse low-grade gliomas. Genome Biol. 15, 471 (2014).
26. Laoukili, J., Stahl, M., & Medema, R.H. FoxM1: at the crossroads of ageing and cancer. Biochim. Biophys. Acta 1775, 92-102 (2007).
27. van den Boom, J., et al. Characterization of gene expression profiles associated with glioma progression using oligonucleotide-based microarray analysis and real-Time reverse transcription-polymerase chain reaction. Am. J. Pathol. 163, 1033-1043 (2003).
28. Liu, M., et al. FoxM1B is overexpressed in human glioblastomas and critically regulates the tumorigenicity of glioma cells. Cancer Res. 66, 3593-3602 (2006).
29. Koo, C.-Y., Muir, K.W., & Lam, E.W.F. FOXM1: from cancer initiation to progression and treatment. Biochim. Biophys. Acta 1819, 28-37 (2012).
30. Wu, L., et al. The E2F1-3 transcription factors are essential for cellular proliferation. Nature 414, 457-462 (2001).
31. Hollern, D.P., Honeysett, J., Cardiff, R.D., & Andrechek, E.R. The E2F transcription factors regulate tumor development and metastasis in a mouse model of metastatic breast cancer. Mol. Cell. Biol. 34, 3229-3243 (2014).
32. Topham, C., et al. MYC is a major determinant of mitotic cell fate. Cancer Cell 28, 129-140 (2015).
33. Dang, C.V., et al. The c-Myc target gene network. Semin. Cancer Biol. 16, 253-264 (2006).
34. Wang, J., et al. c-Myc is required for maintenance of glioma cancer stem cells. PLoS ONE 3, e3769 (2008).
35. Zheng, H., et al. p53 and Pten control neural and glioma stem/progenitor cell renewal and differentiation. Nature 455, 1129-1133 (2008).
36. Kim, H.S., et al. Gliomagenesis arising from Pten-and Ink4a/Arf-Deficient neural progenitor cells is mediated by the p53-Fbxw7/Cdc4 pathway, which controls c-Myc. Cancer Res. 72, 6065-6075 (2012).
37. McLean, C.Y., et al. GREAT improves functional interpretation of cis-regulatory regions. Nat. Biotechnol. 28, 495-501 (2010).
38. ENCODE Project Consortium. An integrated encyclopedia of DNA elements in the human genome. Nature 489, 57-74 (2012).
39. Schlesinger, Y., et al. Polycomb-mediated methylation on Lys27 of histone H3 pre-marks genes for de novo methylation in cancer. Nat. Genet. 39, 232-236 (2007).
40. Keshet, I., et al. Evidence for an instructive mechanism of de novo methylation in cancer cells. Nat. Genet. 38, 149-153 (2006).
41. Cedar, H., & Bergman, Y. Linking DNA methylation and histone modification: patterns and paradigms. Nat. Rev. Genet. 10, 295-304 (2009).
42. Viré, E., et al. The Polycomb group protein EZH2 directly controls DNA methylation. Nature 439, 871-874 (2006).
43. Varambally, S., et al. The polycomb group protein EZH2 is involved in progression of prostate cancer. Nature 419, 624-629 (2002).
44. Cheng, Z., et al. Inhibition of BET bromodomain targets genetically diverse glioblastoma. Clin. Cancer Res. 19, 1748-1759 (2013).
45. Pastori, C., et al. BET bromodomain proteins are required for glioblastoma cell proliferation. Epigenetics 9, 611-620 (2014).
46. Shi, J., & Vakoc, C.R. The mechanisms behind the therapeutic activity of BET bromodomain inhibition. Mol. Cell 54, 728-736 (2014).
47. Filippakopoulos, P., et al. Selective inhibition of BET bromodomains. Nature 468, 1067-1073 (2010).
48. Rohle, D., et al. An inhibitor of mutant IDH1 delays growth and promotes differentiation of glioma cells. Science 340, 626-630 (2013).
49. Mertz, J.A., et al. Targeting MYC dependence in cancer by inhibiting BET bromodomains. Proc. Natl. Acad. Sci. USA 108, 16669-16674 (2011).
50. Bilgüvar, K., et al. Whole-Exome sequencing identifies recessive WDR62 mutations in severe brain malformations. Nature 467, 207-210 (2010).
51. Martin, M. Cutadapt removes adapter sequences from high-Throughput sequencing reads. EMBnet.journal 17, 10-12 (2011).
52. Lunter, G., & Goodson, M. Stampy: a statistical algorithm for sensitive and fast mapping of Illumina sequence reads. Genome Res. 21, 936-939 (2011).
53. Li, H., & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760 (2009).
54. DePristo, M.A., et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43, 491-498 (2011).
55. Li, H. A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics 27, 2987-2993 (2011).
56. McLaren, W., et al. Deriving the consequences of genomic variants with the Ensembl API and SNP Effect Predictor. Bioinformatics 26, 2069-2070 (2010).
57. Clark, V.E., et al. Genomic analysis of non-NF2 meningiomas reveals mutations in TRAF7, KLF4, AKT1, and SMO. Science 339, 1077-1080 (2013).
58. Erson-Omay, E.Z., et al. Somatic POLE mutations cause an ultramutated giant cell high-grade glioma subtype with better prognosis. Neuro-oncol. 17, 1356-1364 (2015).
59. A1000 Genomes Project Consortium. An integrated map of genetic variation from 1, 092 human genomes. Nature 491, 56-65 (2012).
60. Forbes, S.A., et al. COSMIC: mining complete cancer genomes in the Catalogue of Somatic Mutations in Cancer. Nucleic Acids Res. 39, D945-D950 (2011).
61. Van der Auwera, G.A., et al. From FastQ data to high confidence variant calls: the Genome Analysis Toolkit best practices pipeline. Curr. Protoc. Bioinformatics 11, 11.10.1-11.10.33 (2013).
62. Wang, K., Li, M., & Hakonarson, H. ANNOVAR: functional annotation of genetic variants from high-Throughput sequencing data. Nucleic Acids Res. 38, e164 (2010).
63. Song, S., et al. qpure: a tool to estimate tumor cellularity from genome-wide single-nucleotide polymorphism profiles. PLoS ONE 7, e45835 (2012).
64. Zack, T.I., et al. Pan-cancer patterns of somatic copy number alteration. Nat. Genet. 45, 1134-1140 (2013).
65. Bolli, N., et al. Heterogeneity of genomic evolution and mutational profiles in multiple myeloma. Nat. Commun. 5, 2997 (2014).
66. Therneau, T.M., & Grambsch, P.M. Modeling Survival Data: Extending the Cox Model (Springer Science & Business Media, 2000).
67. Shi, W., Oshlack, A., & Smyth, G.K. Optimizing the noise versus bias trade-off for Illumina whole genome expression BeadChips. Nucleic Acids Res. 38, e204 (2010).
68. Leek, J.T., Johnson, W.E., Parker, H.S., Jaffe, A.E., & Storey, J.D. The sva package for removing batch effects and other unwanted variation in high-Throughput experiments. Bioinformatics 28, 882-883 (2012).
69. Wilkerson, M.D., & Hayes, D.N. ConsensusClusterPlus: a class discovery tool with confidence assessments and item tracking. Bioinformatics 26, 1572-1573 (2010).
70. Subramanian, A., et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 102, 15545-15550 (2005).
71. Efron, B., & Tibshirani, R. On testing the significance of sets of genes. Ann. Appl. Stat. 1, 107-129 (2007).
72. Smyth, G.K. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, Article3 (2004).
73. Croft, D., et al. Reactome: a database of reactions, pathways and biological processes. Nucleic Acids Res. 39, D691-D697 (2011).
74. Saito, R., et al. A travel guide to Cytoscape plugins. Nat. Methods 9, 1069-1076 (2012).
75. Langfelder, P., & Horvath, S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9, 559 (2008).
76. Triche, T.J., Weisenberger, D.J., Van Den Berg, D., Laird, P.W., & Siegmund, K.D. Low-level processing of Illumina Infinium DNA Methylation BeadArrays. Nucleic Acids Res. 41, e90 (2013).
77. Teschendorff, A.E., et al. A beta-mixture quantile normalization method for correcting probe design bias in Illumina Infinium 450 k DNA methylation data. Bioinformatics 29, 189-196 (2013).
78. Wang, D., et al. IMA: an R package for high-Throughput analysis of Illumina's 450K Infinium methylation data. Bioinformatics 28, 729-730 (2012).
79. Shin, H., Liu, T., Manrai, A.K., & Liu, X.S. CEAS: cis-regulatory element annotation system. Bioinformatics 25, 2605-2606 (2009).
80. Gao, J., et al. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci. Signal. 6, pl1 (2013).
81. Cerami, E., et al. The cBio Cancer Genomics Portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov. 2, 401-404 (2012).
82. Azari, H., et al. Isolation and expansion of human glioblastoma multiforme tumor cells using the neurosphere assay. J. Vis. Exp. 56, e3633 (2011).
83. Ritz, C., & Streibig, J.C. Bioassay analysis using R. J. Stat. Softw. 12, 1-22 (2005).