Paediatric and adult glioblastoma: multiform (epi)genomic culprits emerge

Sturm, Dominik; Bender, Sebastian; Jones, David T. W.; Lichter, Peter; Grill, Jacques; Becher, Oren; Hawkins, Cynthia; Majewski, Jacek; Jones, Chris; Costello, Joseph F.; Iavarone, Antonio; Aldape, Kenneth; Brennan, Cameron W.; Jabado, Nada; Pfister, Stefan M.

doi:10.1038/nrc3655

Cited by 555Glioma Diagnosis and TreatmentCancer Genomics and DiagnosticsChromatin Remodeling and Cancer

Paediatric and adult glioblastoma: multiform (epi)genomic culprits emerge

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Sturm, Dominik, Bender, Sebastian, Jones, David T. W., Lichter, Peter, Grill, Jacques, Becher, Oren, Hawkins, Cynthia, Majewski, Jacek +7 more·2014·Nature Reviews Cancer

DOI 10.1038/nrc3655PMC PMC4003223

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Abstract

We have extended our understanding of the molecular biology that underlies adult glioblastoma over many years. By contrast, high-grade gliomas in children and adolescents have remained a relatively under-investigated disease. The latest large-scale genomic and epigenomic profiling studies have yielded an unprecedented abundance of novel data and provided deeper insights into gliomagenesis across all age groups, which has highlighted key distinctions but also some commonalities. As we are on the verge of dissecting glioblastomas into meaningful biological subgroups, this Review summarizes the hallmark genetic alterations that are associated with distinct epigenetic features and patient characteristics in both paediatric and adult disease, and examines the complex interplay between the glioblastoma genome and epigenome.

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PDGFRA is an established glioma oncogene.
“Genes in top scoring domains include PDGFRA (p<10−21), an established glioma oncogene22, and other candidate regulators of gliomagenesis (Table S1).”
From Insulator dysfunction and oncogene activation in IDH mutant gliomas (2016) · cites this paper as [22]
FIP1L1 encodes an RNA processing protein that is constitutively expressed in neural tissues and particularly active in oligodendrocyte precursors.
“FIP1L1 encodes an RNA processing protein that is constitutively expressed in neural tissues, and particularly active in oligodendrocyte precursors, a putative glioma cell-of-origin22 (Extended Data Fig. 2a).”
From Insulator dysfunction and oncogene activation in IDH mutant gliomas (2016) · cites this paper as [22]

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Oncogenic EGFR signaling cooperates with loss of tumor suppressor gene functions in gliomagenesis
Zhu, H., Acquaviva, J., Ramachandran, P., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0813314106 · Cited by 231 · see citing works
Phase II Study of Imatinib in Patients With Recurrent Gliomas of Various Histologies: A European Organisation for Research and Treatment of Cancer Brain Tumor Group Study
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The tumorigenic FGFR3-TACC3 gene fusion escapes miR-99a regulation in glioblastoma.
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Molecular Profiling Identifies Prognostic Subgroups of Pediatric Glioblastoma and Shows Increased YB-1 Expression in Tumors
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Asymmetry-Defective Oligodendrocyte Progenitors Are Glioma Precursors
Sugiarto, S., Persson, A. I., González-Muñoz, E., Waldhuber, M., Lamagna, C., Andor, N., Hanecker, P., Ayers-Ringler, J. R., Phillips, J. J., Siu, J. J., et al. (2011) · Cancer Cell · doi:10.1016/j.ccr.2011.08.011 · Cited by 223 · see citing works
Distinct Transcription Profiles of Primary and Secondary Glioblastoma Subgroups
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The Telomerase Antagonist, Imetelstat, Efficiently Targets Glioblastoma Tumor-Initiating Cells Leading to Decreased Proliferation and Tumor Growth
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PDGFRA gene rearrangements are frequent genetic events in PDGFRA-amplified glioblastomasPreprint
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Distinct Neural Stem Cell Populations Give Rise to Disparate Brain Tumors in Response to N-MYC
Swartling, F. J., Savov, V., Persson, A. I., Chen, J., Hackett, C. S., Northcott, P. A., Grimmer, M., Lau, J., Chesler, L., Perry, A., et al. (2012) · Cancer Cell · doi:10.1016/j.ccr.2012.04.012 · Cited by 215 · see citing works
Combinations of genetic mutations in the adult neural stem cell compartment determine brain tumour phenotypes
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Phase II trial of vorinostat in combination with bortezomib in recurrent glioblastoma: a north central cancer treatment group study
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Graded methylation in the promoter and body of the O6-methylguanine DNA methyltransferase (MGMT) gene correlates with MGMT expression in human glioma cells.
Costello, J., Futscher, B., Tano, K., Graunke, D. M., & Pieper, R. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)32544-9 · Cited by 212 · see citing works
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Gefitinib in patients with progressive high-grade gliomas: a multicentre phase II study by Gruppo Italiano Cooperativo di Neuro-Oncologia (GICNO)
Franceschi, E., Cavallo, G., Lonardi, S., Magrini, E., Tosoni, A., Grosso, D., Scopece, L., Blatt, V., Urbini, B., Pession, A., et al. (2007) · British Journal of Cancer · doi:10.1038/sj.bjc.6603669 · Cited by 211 · see citing works
Marked Genomic Differences Characterize Primary and Secondary Glioblastoma Subtypes and Identify Two Distinct Molecular and Clinical Secondary Glioblastoma Entities
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Integrated genomic and epigenomic analyses pinpoint biallelic gene inactivation in tumors
Zardo, G., Tiirikainen, M., Hong, C., Misra, A., Feuerstein, B. G., Volik, S. V., Collins, C. C., Lamborn, K. R., Bollen, A. W., Pinkel, D., et al. (2002) · Nature Genetics · doi:10.1038/ng1007 · Cited by 204 · see citing works
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MGMT promoter methylation correlates with survival benefit and sensitivity to temozolomide in pediatric glioblastoma
Donson, A. M., Addo‐Yobo, S. O., Handler, M. H., et al. (2006) · Pediatric Blood & Cancer · doi:10.1002/pbc.20803 · Cited by 198 · see citing works
An in vivo patient-derived model of endogenous IDH1-mutant glioma
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Pathway Analysis of Glioblastoma Tissue after Preoperative Treatment with the EGFR Tyrosine Kinase Inhibitor Gefitinib—A Phase II Trial
Hegi, M. E., Diserens, A., Bady, P., Kamoshima, Y., Kouwenhoven, M. C. M., Delorenzi, M., Lambiv, W. L., Hamou, M., Matter, M. S., Koch, A., et al. (2011) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-11-0048 · Cited by 194 · see citing works
Long-Term Survival in Primary Glioblastoma With Versus Without Isocitrate Dehydrogenase Mutations
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IDH1 mutations are common in malignant gliomas arising in adolescents: a report from the Children’s Oncology Group
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Promoter Hypermethylation of the RB1 Gene in Glioblastomas
Nakamura, M., Yonekawa, Y., Kleihues, P., & Ohgaki, H. (2001) · Laboratory Investigation · doi:10.1038/labinvest.3780213 · Cited by 184 · see citing works
Oligodendrocyte lineage genes ( OLIG ) as molecular markers for human glial brain tumors
Lü, Q., Park, J. K., Noll, E., Chan, J. A.-W., Alberta, J. A., Yuk, D., Alzamora, M. G., Louis, D. N., Stiles, C. D., Rowitch, D. H., et al. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.181340798 · Cited by 175 · see citing works
Genetic determinants of malignancy in a mouse model for oligodendroglioma.
Weiss, W. A., Burns, M. J., Hackett, C. S., Aldape, K. D., Hill, J. R., Kuriyama, H., Kuriyama, N., Milshteyn, N., Roberts, T. P. L., Wendland, M. F., et al. (2003) · PubMed · Cited by 174 · see citing works
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Breakpoint profiling of 64 cancer genomes reveals numerous complex rearrangements spawned by homology-independent mechanismsPreprint
Malhotra, A., Lindberg, M. R., Faust, G. G., Leibowitz, M. L., Clark, R. A., Layer, R. M., Quinlan, A. R., & Hall, I. M. (2013) · Genome Research · doi:10.1101/gr.143677.112 · Cited by 171 · see citing works
Molecular structure of double-minute chromosomes bearing amplified copies of the epidermal growth factor receptor gene in gliomas
Vogt, N., Lefèvre, S.-H., Apiou, F., Dutrillaux, A., Cör, A., Leuraud, P., Poupon, M., Dutrillaux, B., Debatisse, M., & Malfoy, B. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0402979101 · Cited by 170 · see citing works
Meta-analysis of IDH-mutant cancers identifies EBF1 as an interaction partner for TET2
Guilhamon, P., Eskandarpour, M., Halai, D., Wilson, G. A., Feber, A., Teschendorff, A. E., Gómez, V., Hergovich, A., Tirabosco, R., Amary, F. M., et al. (2013) · Nature Communications · doi:10.1038/ncomms3166 · Cited by 169 · see citing works
Preclinical Evaluation of Radiation and Perifosine in a Genetically and Histologically Accurate Model of Brainstem Glioma
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PIK3CA Gene Mutations in Pediatric and Adult Glioblastoma Multiforme
Gallia, G. L., Rand, V., Siu, I., Eberhart, C. G., James, C. D., Marie, S. K. N., Oba‐Shinjo, S. M., Carlotti, C. G., Caballero, O. L., Simpson, A. J. G., et al. (2006) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-06-0172 · Cited by 161 · see citing works
Imatinib in combination with hydroxyurea versus hydroxyurea alone as oral therapy in patients with progressive pretreated glioblastoma resistant to standard dose temozolomide
Dresemann, G. P., Weller, M., Rosenthal, M. A., Wedding, U., Wagner, W., Engel, E., Heinrich, B., Mayer‐Steinacker, R., Krarup‐Hansen, A., Fluge, Ø., et al. (2009) · Journal of Neuro-Oncology · doi:10.1007/s11060-009-9976-3 · Cited by 156 · see citing works
A Distinct Spectrum of Copy Number Aberrations in Pediatric High-Grade Gliomas
Bax, D. A., Mackay, A. G., Little, S. E., Carvalho, D. M., Viana‐Pereira, M., Tamber, N., Grigoriadis, A. E., Ashworth, A., Reis, R. M., Ellison, D. W., et al. (2010) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-10-0438 · Cited by 155 · see citing works
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EMP3, a Myelin-Related Gene Located in the Critical 19q13.3 Region, Is Epigenetically Silenced and Exhibits Features of a Candidate Tumor Suppressor in Glioma and Neuroblastoma
Alaminos, M., Dávalos, V., Ropero, S., Setién, F., Paz, M. F., Herranz, M., Fraga, M. F., Mora, J., Cheung, N. V., Gerald, W. L., et al. (2005) · Cancer Research · doi:10.1158/0008-5472.can-04-4283 · Cited by 154 · see citing works
Targeted Therapy for BRAFV600E Malignant Astrocytoma
Nicolaides, T. P., Li, H., Solomon, D. A., Hariono, S., Hashizume, R., Barkovich, K. J., Baker, S. J., Paugh, B. S., Jones, C., Forshew, T., et al. (2011) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-11-1456 · Cited by 152 · see citing works
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Glioblastoma Models Reveal the Connection between Adult Glial Progenitors and the Proneural Phenotype
Lei, L., Sonabend, A. M., Guarnieri, P., Soderquist, C. R., Ludwig, T. E., Rosenfeld, S. A., Bruce, J. N., & Canoll, P. (2011) · PLoS ONE · doi:10.1371/journal.pone.0020041 · Cited by 145 · see citing works
Age and TP53 mutation frequency in childhood malignant gliomas: results in a multi-institutional cohort.
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OLIG2 as a specific marker of oligodendroglial tumour cells
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Rarity ofPTENdeletions andEGFRamplification in malignant gliomas of childhood: results from the Children’s Cancer Group 945 cohort
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Self-Renewal Does Not Predict Tumor Growth Potential in Mouse Models of High-Grade Glioma
Barrett, L. E., Granot, Z., Coker, C., Iavarone, A., Hambardzumyan, D., Holland, E. C., Nam, H.-S., & Benezra, R. (2012) · Cancer Cell · doi:10.1016/j.ccr.2011.11.025 · Cited by 137 · see citing works
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Oligodendrogliomas result from the expression of an activated mutant epidermal growth factor receptor in a RAS transgenic mouse astrocytoma model.
Ding, H., Shannon, P. T., Lau, N., et al. (2003) · PubMed · Cited by 136 · see citing works
PTEN methylation and expression in glioblastomas
Baeza, N., Weller, M., Yonekawa, Y., Kleihues, P., & Ohgaki, H. (2003) · Acta Neuropathologica · doi:10.1007/s00401-003-0748-4 · Cited by 134 · see citing works
Analysis of oncogene and tumor suppressor gene alterations in pediatric malignant astrocytomas reveals reduced survival for patients with PTEN mutations.
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Molecular pathogenesis of IDH mutations in gliomas
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Multicentre phase II studies evaluating imatinib plus hydroxyurea in patients with progressive glioblastoma
Reardon, D. A., Dresemann, G. P., Taillibert, S., Campone, M., van den Bent, M. J., Clément, P. M., Blomquist, E., Gordower, L., Schultz, H., Raizer, J. J., et al. (2009) · British Journal of Cancer · doi:10.1038/sj.bjc.6605411 · Cited by 132 · see citing works
IDH1/2 mutations target a key hallmark of cancer by deregulating cellular metabolism in glioma
Zhang, C., Moore, L. M., Li, X., Yung, W. K. A., & Zhang, W. (2013) · Neuro-Oncology · doi:10.1093/neuonc/not087 · Cited by 132 · see citing works
Valproic Acid Use During Radiation Therapy for Glioblastoma Associated With Improved Survival
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Predominant Expression of Mutant EGFR (EGFRvIII) is Rare in Primary Glioblastomas
Biernat, W., Huang, H., Yokoo, H., Kleihues, P., & Ohgaki, H. (2004) · Brain Pathology · doi:10.1111/j.1750-3639.2004.tb00045.x · Cited by 129 · see citing works
Hypofractionation vs Conventional Radiation Therapy for Newly Diagnosed Diffuse Intrinsic Pontine Glioma: A Matched-Cohort Analysis
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Receptor Tyrosine Kinase Genes Amplified in Glioblastoma Exhibit a Mutual Exclusivity in Variable Proportions Reflective of Individual Tumor Heterogeneity
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EZH2 Codon 641 Mutations are Common in BCL2-Rearranged Germinal Center B Cell Lymphomas
Ryan, R. J. H., Nitta, M., Borger, D. R., Zukerberg, L. R., Ferry, J. A., Harris, N. L., Iafrate, A. J., Bernstein, B., Sohani, A. R., & Le, L. P. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028585 · Cited by 122 · see citing works
Homozygous loss of ADAM3A revealed by genome-wide analysis of pediatric high-grade glioma and diffuse intrinsic pontine gliomas
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Methylation-related chromatin structure is associated with exclusion of transcription factors from and suppressed expression of the O-6-methylguanine DNA methyltransferase gene in human glioma cell lines.
Costello, J., Futscher, B. W., Kroes, R. A., & Pieper, R. O. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.10.6515 · Cited by 117 · see citing works
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Double Minute Chromosomes in Glioblastoma Multiforme Are Revealed by Precise Reconstruction of Oncogenic Amplicons
Sanborn, Z., Salama, S. R., Grifford, M., Brennan, C. W., Mikkelsen, T., Jhanwar, S. C., Katzman, S. J., Chin, L., & Haussler, D. H. (2013) · Cancer Research · doi:10.1158/0008-5472.can-13-0186 · Cited by 111 · see citing works
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High-Grade Glioma Formation Results from Postnatal Pten Loss or Mutant Epidermal Growth Factor Receptor Expression in a Transgenic Mouse Glioma Model
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Reciprocal Regulation of SOCS 1 and SOCS3 Enhances Resistance to Ionizing Radiation in Glioblastoma Multiforme
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PDGFRA Amplification is Common in Pediatric and Adult High‐Grade Astrocytomas and Identifies a Poor Prognostic Group in IDH 1 Mutant Glioblastoma
Phillips, J. J., Aranda, D., Ellison, D. W., Judkins, A. R., Croul, S. E., Brat, D. J., Ligon, K. L., Horbinski, C., Venneti, S., Zadeh, G. M., et al. (2013) · Brain Pathology · doi:10.1111/bpa.12043 · Cited by 108 · see citing works
Epigenetic Silencing of the Protocadherin Family Member PCDH-γ-All in Astrocytomas
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Evidence of Focal Genetic Microheterogeneity in Glioblastoma Multiforme by Area-Specific CGH on Microdissected Tumor Cells
Jung, V., Romeike, B. F. M., Henn, W., Feiden, W., Moringlane, J. R., Zang, K. D., & Urbschat, S. (1999) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-199909000-00009 · Cited by 104 · see citing works
Resistance to EGF receptor inhibitors in glioblastoma mediated by phosphorylation of the PTEN tumor suppressor at tyrosine 240
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EGFRvIII Deletion Mutations in Pediatric High-Grade Glioma and Response to Targeted Therapy in Pediatric Glioma Cell Lines
Bax, D. A., Gaspar, N., Little, S. E., Marshall, L. V., Perryman, L., Regairaz, M., Viana‐Pereira, M., Vuononvirta, R., Sharp, S. Y., Reis-Filho, J. S., et al. (2009) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-08-3210 · Cited by 100 · see citing works
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TP53 promoter methylation in human gliomas
Amatya, V. J., Naumann, U., Weller, M., & Ohgaki, H. (2005) · Acta Neuropathologica · doi:10.1007/s00401-005-1041-5 · Cited by 99 · see citing works
Genetic modeling of gliomas in mice: New tools to tackle old problems
Hambardzumyan, D., Parada, L. F., Holland, E. C., & Charest, A. (2011) · Glia · doi:10.1002/glia.21142 · Cited by 99 · see citing works
Immunohistopathological and neuroimaging characterization of murine orthotopic xenograft models of glioblastoma multiforme recapitulating the most salient features of human disease.
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Genome-wide profiling using single-nucleotide polymorphism arrays identifies novel chromosomal imbalances in pediatric glioblastomas
Qu, H., Jacob, K., Fattet, S., Ge, B., Barnett, D., Delattre, O., Faury, D., Montpetit, A., Solomon, L. A., Hauser, P., et al. (2010) · Neuro-Oncology · doi:10.1093/neuonc/nop001 · Cited by 95 · see citing works
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Susceptibility to astrocytoma in mice mutant for Nf1 and Trp53 is linked to chromosome 11 and subject to epigenetic effects
Reilly, K. M., Tuskan, R. G., Christy, E. S., Loisel, D. A., Ledger, J., Bronson, R. T., Smith, C., Tsang, S. X., Munroe, D. J., & Jacks, T. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0401236101 · Cited by 94 · see citing works
Chromatin Remodeling Defects in Pediatric and Young Adult Glioblastoma: A Tale of a Variant <scp>H</scp>istone 3 Tail
Fontebasso, A. M., Liu, X., Sturm, D., & Jabado, N. (2013) · Brain Pathology · doi:10.1111/bpa.12023 · Cited by 89 · see citing works
Feasibility, safety, and indications for surgical biopsy of intrinsic brainstem tumors in children
Cage, T. A., Samagh, S. P., Mueller, S., et al. (2013) · Child s Nervous System · doi:10.1007/s00381-013-2101-0 · Cited by 88 · see citing works
Expression of the Oligodendroglial Lineage‐Associated Markers Olig1 and Olig2 in Different Types of Human Gliomas
Ohnishi, A., Sawa, H., Tsuda, M., Sawamura, Y., Itoh, T., Iwasaki, Y., & Nagashima, K. (2003) · Journal of Neuropathology and Experimental Neurology · doi:10.1093/jnen/62.10.1052 · Cited by 86 · see citing works

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Insulator dysfunction and oncogene activation in IDH mutant gliomas
Flavahan, W. A., Drier, Y., Liau, B. B., Gillespie, S. M., Venteicher, A. S., Stemmer-Rachamimov, A. O., Suvà, M. L., & Bernstein, B. E. (2016) · Nature · doi:10.1038/nature16490 · Cited by 1,288 · see citing works
Integrated Molecular Meta-Analysis of 1,000 Pediatric High-Grade and Diffuse Intrinsic Pontine Glioma
Mackay, A., Burford, A., Carvalho, D., Izquierdo, E., Fazal-Salom, J., Taylor, K. R., Bjerke, L., Clarke, M., Vinci, M., Nandhabalan, M., et al. (2017) · Cancer Cell · doi:10.1016/j.ccell.2017.08.017 · Cited by 1,212 · see citing works
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Glioblastoma in adults: a Society for Neuro-Oncology (SNO) and European Society of Neuro-Oncology (EANO) consensus review on current management and future directions
Wen, P. Y., Weller, M., Lee, E. Q., Alexander, B. M., Barnholtz-Sloan, J. S., Barthel, F. P., Batchelor, T. T., Bindra, R. S., Chang, S. M., Chiocca, E. A., et al. (2020) · Neuro-Oncology · doi:10.1093/neuonc/noaa106 · Cited by 1,168 · see citing works
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Histologically distinct neuroepithelial tumors with histone 3 G34 mutation are molecularly similar and comprise a single nosologic entity
Korshunov, A., Capper, D., Reuss, D., Schrimpf, D., Ryzhova, M., Hovestadt, V., Sturm, D., Meyer, J., Jones, C., Zheludkova, O., et al. (2016) · Acta Neuropathologica · doi:10.1007/s00401-015-1493-1 · Cited by 236 · see citing works
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Assessment of programmed death-ligand 1 expression and tumor-associated immune cells in pediatric cancer tissues
Majzner, R. G., Simon, J. S., Grosso, J. F., Martinez, D., Pawel, B. R., Santi, M., Merchant, M. S., Geoerger, B., Hezam, I., Marty, V., et al. (2017) · Cancer · doi:10.1002/cncr.30724 · Cited by 179 · see citing works
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VRK1 as a synthetic lethal target in VRK2 promoter-methylated cancers of the nervous system
So, J., Mabe, N. W., Englinger, B., Chow, K.-H., Moyer, S. M., Yerrum, S., Trissal, M. C., Marques, J. G., Kwon, J. J., Shim, B., et al. (2022) · JCI Insight · doi:10.1172/jci.insight.158755 · Cited by 45 · see citing works
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MicroRNA-96 Regulates Apoptosis by Targeting PDCD4 in Human Glioma Cells
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Authors: Sturm, D., Bender, S., Jones, D. T. W., Lichter, P., Grill, J., Becher, O., Hawkins, C., Majewski, J., Jones, C., Costello, J. F., Iavarone, A., Aldape, K., Brennan, C. W., Jabado, N., & Pfister, S. M.
Affiliations: German Cancer Research Center (DE)
Université Paris-Sud (FR)
Duke University (US)
Hospital for Sick Children (CA)
McGill University Health Centre (CA)
Institute of Cancer Research (GB)
University of California, San Francisco (US)
Columbia University Irving Medical Center (US)
The University of Texas MD Anderson Cancer Center (US)
Memorial Sloan Kettering Cancer Center (US)
Corresponding author: Jabado, Nada
Pfister, Stefan M.
ORCID: Sturm, Dominik
Jones, David T. W.
Lichter, Peter
Grill, Jacques
Becher, Oren
Hawkins, Cynthia
Majewski, Jacek
Jones, Chris
Costello, Joseph F.
Iavarone, Antonio
Aldape, Kenneth
Brennan, Cameron W.
Jabado, Nada
Pfister, Stefan M.
Venue: Nature Reviews Cancer
Publisher: Springer Science and Business Media LLC
Published: 2014-01-24
Volume: 14
Issue: 2
Pages: 92-107
ISSN: 1474-175X (ISSN-L)
1474-1768
DOI: 10.1038/nrc3655
PMC: PMC4003223
OpenAlex: W2114551767
Cited by: 555
References: 230
Citations by year: 2026: 10 · 2025: 31 · 2024: 25 · 2023: 34 · 2022: 38 · 2021: 43 · 2020: 56 · 2019: 57 · 2018: 50 · 2017: 80 · 2016: 49 · 2015: 48 · 2014: 33 · 2013: 1
FWCI: 10.68
Type: journal article
Language: en
Open access: green
europepmc.org
Licence: www.springer.com/tdm (tdm)
Locations: Nature reviews. Cancer (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
eScholarship (California Digital Library) (submittedVersion)
Funders: Cancer Research UK (13982, 11736)
Rosetrees Trust (M200-F1)
Brain Tumour Charity
Canadian Institutes of Health Research
National Cancer Institute (R01CA169316, P01CA118816)
Topics: Health Sciences › Medicine › Genetics › Glioma Diagnosis and Treatment
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
Keywords: adult glioblastoma, high-grade glioma, gliomagenesis, genetic alterations, epigenetic modifications, epigenome, molecular subtypes, age differences
MeSH terms: Age Factors, Glioblastoma, Humans, Neoplasms, Nerve Tissue, Epigenomics

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