Molecular classification of gliomas

Handbook of Clinical Neurology

Volumn 134, Issue , 2016, Pages 97-120

  Masui, Kenta ^a,b   Mischel, Paul S ^b   Reifenberger, Guido ^c  

^a TOKYO WOMEN'S MEDICAL UNIVERSITY   (Japan)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Genetics; Glioma; Integrated diagnosis; ISN Haarlem guidelines; Molecular classification; Targeted therapy; WHO classification

Indexed keywords

BRAIN TUMOR; CLASSIFICATION; GENETIC PROCEDURES; GENETICS; GLIOMA; HUMAN;

BRAIN NEOPLASMS; GLIOMA; HUMANS; MOLECULAR PROBE TECHNIQUES;

EID: 84976444914     PISSN: 00729752     EISSN: 22124152     Source Type: Book Series    
DOI: 10.1016/B978-0-12-802997-8.00006-2     Document Type: Chapter

References (138)

1. Abedalthagafi M., Phillips J.J., Kim G.E., et al. The alternative lengthening of telomere phenotype is significantly associated with loss of ATRX expression in high-grade pediatric and adult astrocytomas: a multi-institutional study of 214 astrocytomas. Mod Pathol 2013, 26:1425-1432.
2. Aldape K., Zadeh G., Mansouri S., et al. Glioblastoma: pathology, molecular mechanisms and markers. Acta Neuropathol 2015, 129:829-848.
3. Alexander B.M., Wen P.Y., Trippa L., et al. Biomarker-based adaptive trials for patients with glioblastoma-lessons from I-SPY 2. Neuro Oncol 2013, 15:972-978.
4. Arita H., Narita Y., Fukushima S., et al. Upregulating mutations in the TERT promoter commonly occur in adult malignant gliomas and are strongly associated with total 1p19q loss. Acta Neuropathol 2013, 126:267-276.
5. Bady P., Sciuscio D., Diserens A.C., et al. MGMT methylation analysis of glioblastoma on the Infinium methylation BeadChip identifies two distinct CpG regions associated with gene silencing and outcome, yielding a prediction model for comparisons across datasets, tumor grades, and CIMP-status. Acta Neuropathol 2012, 124:547-560.
6. Balss J., Meyer J., Mueller W., et al. Analysis of the IDH1 codon 132 mutation in brain tumors. Acta Neuropathol 2008, 116:597-602.
7. Bechet D., Gielen G.G., Korshunov A., et al. Specific detection of methionine 27 mutation in histone 3 variants (H3K27M) in fixed tissue from high-grade astrocytomas. Acta Neuropathol 2014, 128:733-741.
8. Bender S., Tang Y., Lindroth A.M., et al. Reduced H3K27me3 and DNA hypomethylation are major drivers of gene expression in K27M mutant pediatric high-grade gliomas. Cancer Cell 2013, 24:660-672.
9. Bettegowda C., Agrawal N., Jiao Y., et al. Mutations in CIC and FUBP1 contribute to human oligodendroglioma. Science 2011, 333:1453-1455.
10. Bhat K.P., Balasubramaniyan V., Vaillant B., et al. Mesenchymal differentiation mediated by NF-κB promotes radiation resistance in glioblastoma. Cancer Cell 2013, 24:331-346.
11. Brat D.J., Verhaak R.G., Aldape K.D., et al. Comprehensive, integrative genomic analysis of diffuse lower-grade gliomas. N Engl J Med 2015, 372:2481-2498.
12. Brennan C.W., Verhaak R.G., Mckenna A., et al. The somatic genomic landscape of glioblastoma. Cell 2013, 155:462-477.
13. Buczkowicz P., Hoeman C., Rakopoulos P., et al. Genomic analysis of diffuse intrinsic pontine gliomas identifies three molecular subgroups and recurrent activating ACVR1 mutations. Nat Genet 2014, 46:451-456.
14. Cairncross G., Wang M., Shaw E., et al. Phase III trial of chemoradiotherapy for anaplastic oligodendroglioma: long-term results of RTOG 9402. J Clin Oncol 2013, 31:337-343.
15. Cancer Genome Atlas Research Network Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 2008, 455:1061-1068.
16. Capper D., Weissert S., Balss J., et al. Characterization of R132H mutation-specific IDH1 antibody binding in brain tumors. Brain Pathol 2010, 20:245-254.
17. Capper D., Preusser M., Habel A., et al. Assessment of BRAF V600E mutation status by immunohistochemistry with a mutation-specific monoclonal antibody. Acta Neuropathol 2011, 122:11-19.
18. Chamberlain M.C. Salvage therapy with BRAF inhibitors for recurrent pleomorphic xanthoastrocytoma: a retrospective case series. J Neurooncol 2013, 114:237-240.
19. Chan J.A., Zhang H., Roberts P.S., et al. Pathogenesis of tuberous sclerosis subependymal giant cell astrocytomas: biallelic inactivation of TSC1 or TSC2 leads to mTOR activation. J Neuropathol Exp Neurol 2004, 63:1236-1242.
20. Chen L., Voronovich Z., Clark K., et al. Predicting the likelihood of an isocitrate dehydrogenase 1 or 2 mutation in diagnoses of infiltrative glioma. Neuro Oncol 2014, 16:1478-1483.
21. Choi C., Ganji S.K., Deberardinis R.J., et al. 2-hydroxyglutarate detection by magnetic resonance spectroscopy in IDH-mutated patients with gliomas. Nat Med 2012, 18:624-629.
22. Cloughesy T.F., Cavenee W.K., Mischel P.S. Glioblastoma: from molecular pathology to targeted treatment. Annu Rev Pathol 2014, 9:1-25.
23. Collins V.P., Jones D.T., Giannini C. Pilocytic astrocytoma: pathology, molecular mechanisms and markers. Acta Neuropathol 2015, 129:775-788.
24. Dubbink H.J., Deans Z.C., Tops B.B., et al. Next generation diagnostic molecular pathology: critical appraisal of quality assurance in Europe. Mol Oncol 2014, 8:830-839.
25. Ebert C., von Haken M., Meyer-Puttlitz B., et al. Molecular genetic analysis of ependymal tumors. NF2 mutations and chromosome 22q loss occur preferentially in intramedullary spinal ependymomas. Am J Pathol 1999, 155:627-632.
26. Eckel-Passow J.E., Lachance D.H., Molinaro A.M., et al. Glioma groups based on 1p/19q, IDH, and TERT promoter mutations in tumors. N Engl J Med 2015, 372:2499-2508.
27. Esteller M., Garcia-Foncillas J., Andion E., et al. Inactivation of the DNA-repair gene MGMT and the clinical response of gliomas to alkylating agents. N Engl J Med 2000, 343:1350-1354.
28. Felsberg J. Molecular diagnostics of glioma - results of the first interlaboratory comparison of MGMT promoter methylation testing at twenty-three academic centers in Germany, Austria and the Netherlands. Clin Neuropathol 2013, 32:414-415.
29. Felsberg J., Wolter M., Seul H., et al. Rapid and sensitive assessment of the IDH1 and IDH2 mutation status in cerebral gliomas based on DNA pyrosequencing. Acta Neuropathol 2010, 119:501-507.
30. Furnari F.B., Cloughesy T.F., Cavenee W.K., et al. Heterogeneity of epidermal growth factor receptor signalling networks in glioblastoma. Nat Rev Cancer 2015, 15:302-310.
31. Gessi M., Gielen G.H., Dreschmann V., et al. High frequency of H3F3A (K27M) mutations characterizes pediatric and adult high-grade gliomas of the spinal cord. Acta Neuropathol 2015, 130:435-437.
32. Grasso C.S., Tang Y., Truffaux N., et al. Functionally defined therapeutic targets in diffuse intrinsic pontine glioma. Nat Med 2015, 21:555-559.
33. Griffin C.A., Burger P., Morsberger L., et al. Identification of der(1;19)(q10;p10) in five oligodendrogliomas suggests mechanism of concurrent 1p and 19q loss. J Neuropathol Exp Neurol 2006, 65:988-994.
34. Hartmann C., Meyer J., Balss J., et al. Type and frequency of IDH1 and IDH2 mutations are related to astrocytic and oligodendroglial differentiation and age: a study of 1,010 diffuse gliomas. Acta Neuropathol 2009, 118:469-474.
35. Hartmann C., Hentschel B., Wick W., et al. Patients with IDH1 wild type anaplastic astrocytomas exhibit worse prognosis than IDH1-mutated glioblastomas, and IDH1 mutation status accounts for the unfavorable prognostic effect of higher age: implications for classification of gliomas. Acta Neuropathol 2010, 120:707-718.
36. Hashizume R., Andor N., Ihara Y., et al. Pharmacologic inhibition of histone demethylation as a therapy for pediatric brainstem glioma. Nat Med 2014, 20:1394-1396.
37. Hegi M.E., Diserens A.C., Gorlia T., et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 2005, 352:997-1003.
38. Horbinski C., Kelly L., Nikiforov Y.E., et al. Detection of IDH1 and IDH2 mutations by fluorescence melting curve analysis as a diagnostic tool for brain biopsies. J Mol Diagn 2010, 12:487-492.
39. Horn S., Figl A., Rachakonda P.S., et al. TERT promoter mutations in familial and sporadic melanoma. Science 2013, 339:959-961.
40. Hovestadt V., Remke M., Kool M., et al. Robust molecular subgrouping and copy-number profiling of medulloblastoma from small amounts of archival tumour material using high-density DNA methylation arrays. Acta Neuropathol 2013, 125:913-916.
41. Huang F.W., Hodis E., Xu M.J., et al. Highly recurrent TERT promoter mutations in human melanoma. Science 2013, 339:957-959.
42. Jenkins R.B., Blair H., Ballman K.V., et al. A t(1;19)(q10;p10) mediates the combined deletions of 1p and 19q and predicts a better prognosis of patients with oligodendroglioma. Cancer Res 2006, 66:9852-9861.
43. Jiao Y., Killela P.J., Reitman Z.J., et al. Frequent ATRX, CIC, FUBP1 and IDH1 mutations refine the classification of malignant gliomas. Oncotarget 2012, 3:709-722.
44. Jones D.T., Hutter B., Jäger N., et al. Recurrent somatic alterations of FGFR1 and NTRK2 in pilocytic astrocytoma. Nat Genet 2013, 45:927-932.
45. Kato Y. Specific monoclonal antibodies against IDH1/2 mutations as diagnostic tools for gliomas. Brain Tumor Pathol 2015, 32:3-11.
46. Khuong-Quang D.A., Buczkowicz P., Rakopoulos P., et al. K27M mutation in histone H3.3 defines clinically and biologically distinct subgroups of pediatric diffuse intrinsic pontine gliomas. Acta Neuropathol 2012, 124:439-447.
47. Killela P.J., Reitman Z.J., Jiao Y., et al. TERT promoter mutations occur frequently in gliomas and a subset of tumors derived from cells with low rates of self-renewal. Proc Natl Acad Sci U S A 2013, 110:6021-6026.
48. Killela P.J., Pirozzi C.J., Healy P., et al. Mutations in IDH1, IDH2, and in the TERT promoter define clinically distinct subgroups of adult malignant gliomas. Oncotarget 2014, 5:1515-1525.
49. Kleinschmidt-Demasters B.K., Aisner D.L., Birks D.K., et al. Epithelioid GBMs show a high percentage of BRAF V600E mutation. Am J Surg Pathol 2013, 37:685-698.
50. Kleinschmidt-Demasters B.K., Aisner D.L., Foreman N.K. BRAF VE1 immunoreactivity patterns in epithelioid glioblastomas positive for BRAF V600E mutation. Am J Surg Pathol 2015, 39:528-540.
51. Knobbe C.B., Reifenberger J., Reifenberger G. Mutation analysis of the Ras pathway genes NRAS, HRAS, KRAS and BRAF in glioblastomas. Acta Neuropathol 2004, 108:467-470.
52. Koelsche C., Sahm F., Wöhrer A., et al. BRAF-mutated pleomorphic xanthoastrocytoma is associated with temporal location, reticulin fiber deposition and CD34 expression. Brain Pathol 2014, 24:221-229.
53. Koivunen P., Lee S., Duncan C.G., et al. Transformation by the (R)-enantiomer of 2-hydroxyglutarate linked to EGLN activation. Nature 2012, 483:484-488.
54. Korshunov A., Meyer J., Capper D., et al. Combined molecular analysis of BRAF and IDH1 distinguishes pilocytic astrocytoma from diffuse astrocytoma. Acta Neuropathol 2009, 118:401-405.
55. Korshunov A., Ryzhova M., Hovestadt V., et al. Integrated analysis of pediatric glioblastoma reveals a subset of biologically favorable tumors with associated molecular prognostic markers. Acta Neuropathol 2015, 129:669-678.
56. Krueger D.A., Care M.M., Holland K., et al. Everolimus for subependymal giant-cell astrocytomas in tuberous sclerosis. N Engl J Med 2010, 363:1801-1811.
57. Labreche K., Simeonova I., Kamoun A., et al. TCF12 is mutated in anaplastic oligodendroglioma. Nat Commun 2015, 6:7207.
58. Labussière M., Di Stefano A.L., Gleize V., et al. TERT promoter mutations in gliomas, genetic associations and clinico-pathological correlations. Br J Cancer 2014, 111:2024-2032.
59. Lalezari S., Chou A.P., Tran A., et al. Combined analysis of O6-methylguanine-DNA methyltransferase protein expression and promoter methylation provides optimized prognostication of glioblastoma outcome. Neuro Oncol 2013, 15:370-381.
60. Lambert S.R., Witt H., Hovestadt V., et al. Differential expression and methylation of brain developmental genes define location-specific subsets of pilocytic astrocytoma. Acta Neuropathol 2013, 126:291-301.
61. Laplante M., Sabatini D.M. mTOR signaling in growth control and disease. Cell 2012, 149:274-293.
62. Lawrence M.S., Stojanov P., Mermel C.H., et al. Discovery and saturation analysis of cancer genes across 21 tumour types. Nature 2014, 505:495-501.
63. World Health Organization classification of tumours of the central nervous system 2007, International Agency for Research on Cancer, Lyon. D.N. Louis, H. Ohgaki, O.D. Wiestler (Eds.).
64. Louis D.N., Perry A., Burger P., et al. International Society Of Neuropathology - Haarlem consensus guidelines for nervous system tumor classification and grading. Brain Pathol 2014, 24:429-435.
65. Mack S.C., Witt H., Piro R.M., et al. Epigenomic alterations define lethal CIMP-positive ependymomas of infancy. Nature 2014, 506:445-450.
66. Malmström A., Grønberg B.H., Marosi C., et al. Temozolomide versus standard 6-week radiotherapy versus hypofractionated radiotherapy in patients older than 60 years with glioblastoma: the Nordic randomised, phase 3 trial. Lancet Oncol 2012, 13:916-926.
67. Masui K., Tanaka K., Akhavan D., et al. mTOR complex 2 controls glycolytic metabolism in glioblastoma through FoxO acetylation and upregulation of c-Myc. Cell Metab 2013, 18:726-739.
68. Masui K., Cavenee W.K., Mischel P.S. mTORC2 in the center of cancer metabolic reprogramming. Trends Endocrinol Metab 2014, 25:364-373.
69. Masui K., Tanaka K., Ikegami S., et al. Glucose-dependent acetylation of Rictor promotes targeted cancer therapy resistance. Proc Natl Acad Sci U S A 2015, 112:9406-9411.
70. Meyer J., Pusch S., Balss J., et al. PCR- and restriction endonuclease-based detection of IDH1 mutations. Brain Pathol 2010, 20:298-300.
71. Mistry M., Zhukova N., Merico D., et al. BRAF mutation and CDKN2A deletion define a clinically distinct subgroup of childhood secondary high-grade glioma. J Clin Oncol 2015, 33:1015-1022.
72. Molenaar R.J., Radivoyevitch T., Maciejewski J.P., et al. The driver and passenger effects of isocitrate dehydrogenase 1 and 2 mutations in oncogenesis and survival prolongation. Biochim Biophys Acta 2014, 1846:326-341.
73. Nathanson D.A., Gini B., Mottahedeh J., et al. Targeted therapy resistance mediated by dynamic regulation of extrachromosomal mutant EGFR DNA. Science 2014, 343:72-76.
74. Noushmehr H., Weisenberger D.J., Diefes K., et al. Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell 2010, 17:510-522.
75. Ohgaki H., Kleihues P. The definition of primary and secondary glioblastoma. Clin Cancer Res 2013, 19:764-772.
76. Olar A., Wani K.M., Alfaro-Munoz K.D., et al. IDH mutation status and role of WHO grade and mitotic index in overall survival in grade II-III diffuse gliomas. Acta Neuropathol 2015, 129:585-596.
77. Pajtler K.W., Witt H., Sill M., et al. Molecular classification of ependymal tumors across all CNS compartments, histopathological grades, and age groups. Cancer Cell 2015, 27:728-743.
78. Parker M., Mohankumar K.M., Punchihewa C., et al. C11orf95-RELA fusions drive oncogenic NF-κB signalling in ependymoma. Nature 2014, 506:451-455.
79. Parsons D.W., Jones S., Zhang X., et al. An integrated genomic analysis of human glioblastoma multiforme. Science 2008, 321:1807-1812.
80. Patel A.P., Tirosh I., Trombetta J.J., et al. Single-cell RNA-seq highlights intratumoral heterogeneity in primary glioblastoma. Science 2014, 344:1396-1401.
81. Pietsch T., Wohlers I., Goschzik T., et al. Supratentorial ependymomas of childhood carry C11orf95-RELA fusions leading to pathological activation of the NF-κB signaling pathway. Acta Neuropathol 2014, 127:609-611.
82. Preusser M., Charles Janzer R., Felsberg J., et al. Anti-O6-methylguanine-methyltransferase (MGMT) immunohistochemistry in glioblastoma multiforme: observer variability and lack of association with patient survival impede its use as clinical biomarker. Brain Pathol 2008, 18:520-532.
83. Reardon D.A., Schuster J.M., Tran D.D., et al. 107 ReACT: overall survival from a randomized phase II study of rindopepimut (CDX-110) plus bevacizumab in relapsed glioblastoma. Neurosurgery 2015, 62(Suppl 1):198-199.
84. Reuss D.E., Kratz A., Sahm F., et al. Adult IDH wild type astrocytomas biologically and clinically resolve into other tumor entities. Acta Neuropathol 2015, 130:407-417.
85. Reuss D.E., Mamatjan Y., Schrimpf D., et al. IDH mutant diffuse and anaplastic astrocytomas have similar age at presentation and little difference in survival: a grading problem for WHO. Acta Neuropathol 2015, 129:867-873.
86. Reuss D.E., Sahm F., Schrimpf D., et al. ATRX and IDH1-R132H immunohistochemistry with subsequent copy number analysis and IDH sequencing as a basis for an "integrated" diagnostic approach for adult astrocytoma, oligodendroglioma and glioblastoma. Acta Neuropathol 2015, 129:133-146.
87. Riemenschneider M.J., Jeuken J.W., Wesseling P., et al. Molecular diagnostics of gliomas: state of the art. Acta Neuropathol 2010, 120:567-584.
88. Robinson G.W., Orr B.A., Gajjar A. Complete clinical regression of a BRAF V600E-mutant pediatric glioblastoma multiforme after BRAF inhibitor therapy. BMC Cancer 2014, 14:258.
89. Rodriguez F.J., Tihan T., Lin D., et al. Clinicopathologic features of pediatric oligodendrogliomas: a series of 50 patients. Am J Surg Pathol 2014, 38:1058-1070.
90. Rohle D., Popovici-Muller J., Palaskas N., et al. An inhibitor of mutant IDH1 delays growth and promotes differentiation of glioma cells. Science 2013, 340:626-630.
91. Sahm F., Reuss D., Koelsche C., et al. Farewell to oligoastrocytoma: in situ molecular genetics favor classification as either oligodendroglioma or astrocytoma. Acta Neuropathol 2014, 128:551-559.
92. Sandmann T., Bourgon R., Garcia J., et al. Patients with proneural glioblastoma may derive overall survival benefit from the addition of bevacizumab to first-line radiotherapy and temozolomide: retrospective analysis of the AVAglio trial. J Clin Oncol 2015, 33:2735-2744.
93. Sanson M., Marie Y., Paris S., et al. Isocitrate dehydrogenase 1 codon 132 mutation is an important prognostic biomarker in gliomas. J Clin Oncol 2009, 27:4150-4154.
94. Santagata S., Eberlin L.S., Norton I., et al. Intraoperative mass spectrometry mapping of an onco-metabolite to guide brain tumor surgery. Proc Natl Acad Sci U S A 2014, 111:11121-11126.
95. Sasaki M., Knobbe C.B., Itsumi M., et al. D-2-hydroxyglutarate produced by mutant IDH1 perturbs collagen maturation and basement membrane function. Genes Dev 2012, 26:2038-2049.
96. Schindler G., Capper D., Meyer J., et al. Analysis of BRAF V600E mutation in 1,320 nervous system tumors reveals high mutation frequencies in pleomorphic xanthoastrocytoma, ganglioglioma and extra-cerebellar pilocytic astrocytoma. Acta Neuropathol 2011, 121:397-405.
97. Schumacher T., Bunse L., Pusch S., et al. A vaccine targeting mutant IDH1 induces antitumour immunity. Nature 2014, 512:324-327.
98. Schuster J., Lai R.K., Recht L.D., et al. A phase II, multicenter trial of rindopepimut (CDX-110) in newly diagnosed glioblastoma: the ACT III study. Neuro Oncol 2015, 17:854-861.
99. Schwartzentruber J., Korshunov A., Liu X.Y., et al. Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma. Nature 2012, 482:226-231.
100. Singh D., Chan J.M., Zoppoli P., et al. Transforming fusions of FGFR and TACC genes in human glioblastoma. Science 2012, 337:1231-1235.
101. Singh R.R., Patel K.P., Routbort M.J., et al. Clinical validation of a next-generation sequencing screen for mutational hotspots in 46 cancer-related genes. J Mol Diagn 2013, 15:607-622.
102. Singh R.R., Patel K.P., Routbort M.J., et al. Clinical massively parallel next-generation sequencing analysis of 409 cancer-related genes for mutations and copy number variations in solid tumours. Br J Cancer 2014, 111:2014-2023.
103. Sturm D., Witt H., Hovestadt V., et al. Hotspot mutations in H3F3A and IDH1 define distinct epigenetic and biological subgroups of glioblastoma. Cancer Cell 2012, 22:425-437.
104. Sturm D., Bender S., Jones D.T., et al. Paediatric and adult glioblastoma: multiform (epi)genomic culprits emerge. Nat Rev Cancer 2014, 14:92-107.
105. Suzuki H., Aoki K., Chiba K., et al. Mutational landscape and clonal architecture in grade II and III gliomas. Nat Genet 2015, 47:458-468.
106. Tanaka K., Babic I., Nathanson D., et al. Oncogenic EGFR signaling activates an mTORC2-NF-κB pathway that promotes chemotherapy resistance. Cancer Discov 2011, 1:524-538.
107. Tian Y., Rich B.E., Vena N., et al. Detection of KIAA1549-BRAF fusion transcripts in formalin-fixed paraffin-embedded pediatric low-grade gliomas. J Mol Diagn 2011, 13:669-677.
108. van Den Bent M.J. Interobserver variation of the histopathological diagnosis in clinical trials on glioma: a clinician's perspective. Acta Neuropathol 2010, 120:297-304.
109. van Den Bent M.J., Dubbink H.J., Marie Y., et al. IDH1 and IDH2 mutations are prognostic but not predictive for outcome in anaplastic oligodendroglial tumors: a report of the European Organization for Research and Treatment of Cancer Brain Tumor Group. Clin Cancer Res 2010, 16:1597-1604.
110. van Den Bent M.J., Brandes A.A., Taphoorn M.J., et al. Adjuvant procarbazine, lomustine, and vincristine chemotherapy in newly diagnosed anaplastic oligodendroglioma: long-term follow-up of EORTC brain tumor group study 26951. J Clin Oncol 2013, 31:344-350.
111. van Den Bent M.J., Hartmann C., Preusser M., et al. Interlaboratory comparison of IDH mutation detection. J Neurooncol 2013, 112:173-178.
112. van Krieken J.H., Siebers A.G., Normanno N., et al. European consensus conference for external quality assessment in molecular pathology. Ann Oncol 2013, 24:1958-1963.
113. Venneti S., Santi M., Felicella M.M., et al. A sensitive and specific histopathologic prognostic marker for H3F3A K27M mutant pediatric glioblastomas. Acta Neuropathol 2014, 128:743-753.
114. Verhaak R.G., Hoadley K.A., Purdom E., et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 2010, 17:98-110.
115. Vivanco I., Robins H.I., Rohle D., et al. Differential sensitivity of glioma- versus lung cancer-specific EGFR mutations to EGFR kinase inhibitors. Cancer Discov 2012, 2:458-471.
116. Vogazianou A.P., Chan R., Bäcklund L.M., et al. Distinct patterns of 1p and 19q alterations identify subtypes of human gliomas that have different prognoses. Neuro Oncol 2010, 12:664-678.
117. Wani K., Armstrong T.S., Vera-Bolanos E., et al. A prognostic gene expression signature in infratentorial ependymoma. Acta Neuropathol 2012, 123:727-738.
118. Weber R.G., Hoischen A., Ehrler M., et al. Frequent loss of chromosome 9, homozygous CDKN2A/p14(ARF)/CDKN2B deletion and low TSC1 mRNA expression in pleomorphic xanthoastrocytomas. Oncogene 2007, 26:1088-1097.
119. Weiler M., Blaes J., Pusch S., et al. mTOR target NDRG1 confers MGMT-dependent resistance to alkylating chemotherapy. Proc Natl Acad Sci U S A 2014, 111:409-414.
120. Weller M., Felsberg J., Hartmann C., 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, 27:5743-5750.
121. Weller M., Kaulich K., Hentschel B., et al. Assessment and prognostic significance of the epidermal growth factor receptor vIII mutation in glioblastoma patients treated with concurrent and adjuvant temozolomide radiochemotherapy. Int J Cancer 2014, 134:2437-2447.
122. Weller M., van Den Bent M., Hopkins K., et al. EANO guideline for the diagnosis and treatment of anaplastic gliomas and glioblastoma. Lancet Oncol 2014, 15:e395-e403.
123. Weller M., Wick W., Aldape K., et al. Glioma. Nat Rev Dis Primers 2015, Article number: 15017.
124. Wick W., Hartmann C., Engel C., et al. NOA-04 randomized phase III trial of sequential radiochemotherapy of anaplastic glioma with procarbazine, lomustine, and vincristine or temozolomide. J Clin Oncol 2009, 27:5874-5880.
125. Wick W., Platten M., Meisner C., et al. Temozolomide chemotherapy alone versus radiotherapy alone for malignant astrocytoma in the elderly: the NOA-08 randomised, phase 3 trial. Lancet Oncol 2012, 13:707-715.
126. Wick W., Meisner C., Hentschel B., et al. Prognostic or predictive value of MGMT promoter methylation in gliomas depends on IDH1 mutation. Neurology 2013, 81:1515-1522.
127. Wick W., Weller M., van Den Bent M., et al. MGMT testing-the challenges for biomarker-based glioma treatment. Nat Rev Neurol 2014, 10:372-385.
128. Wiestler B., Capper D., Hovestadt V., et al. Assessing CpG island methylator phenotype, 1p/19q codeletion, and MGMT promoter methylation from epigenome-wide data in the biomarker cohort of the NOA-04 trial. Neuro Oncol 2014, 16:1630-1638.
129. Wiestler B., Capper D., Sill M., et al. Integrated DNA methylation and copy-number profiling identify three clinically and biologically relevant groups of anaplastic glioma. Acta Neuropathol 2014, 128:561-571.
130. Witt H., Mack S.C., Ryzhova M., et al. Delineation of two clinically and molecularly distinct subgroups of posterior fossa ependymoma. Cancer Cell 2011, 20:143-157.
131. Wong S.Q., Fellowes A., Doig K., et al. Assessing the clinical value of targeted massively parallel sequencing in a longitudinal, prospective population-based study of cancer patients. Br J Cancer 2015, 112:1411-1420.
132. Wu G., Broniscer A., Mceachron T.A., et al. Somatic histone H3 alterations in pediatric diffuse intrinsic pontine gliomas and non-brainstem glioblastomas. Nat Genet 2012, 44:251-253.
133. Xu W., Yang H., Liu Y., et al. Oncometabolite 2-hydroxyglutarate is a competitive inhibitor of alpha-ketoglutarate-dependent dioxygenases. Cancer Cell 2011, 19:17-30.
134. Yan H., Parsons D.W., Jin G., et al. IDH1 and IDH2 mutations in gliomas. N Engl J Med 2009, 360:765-773.
135. 6-methylguanine-DNA-methyltransferase promoter methylation assessment by microdissection-assisted methylation-specific PCR and high resolution melting analysis in patients with glioblastomas. J Neurooncol 2012, 106:243-250.
136. Yip S., Butterfield Y.S., Morozova O., et al. Concurrent CIC mutations, IDH mutations, and 1p/19q loss distinguish oligodendrogliomas from other cancers. J Pathol 2012, 226:7-16.
137. Yoshimoto K., Dang J., Zhu S., et al. Development of a real-time RT-PCR assay for detecting EGFRvIII in glioblastoma samples. Clin Cancer Res 2008, 14:488-493.
138. Zhang J., Wu G., Miller C.P., et al. Whole-genome sequencing identifies genetic alterations in pediatric low-grade gliomas. Nat Genet 2013, 45:602-612.