Hotspot Mutations in H3F3A and IDH1 Define Distinct Epigenetic and Biological Subgroups of Glioblastoma
Open accessAbstract
Glioblastoma (GBM) is a brain tumor that carries a dismal prognosis and displays considerable heterogeneity. We have recently identified recurrent H3F3A mutations affecting two critical amino acids (K27 and G34) of histone H3.3 in one-third of pediatric GBM. Here, we show that each H3F3A mutation defines an epigenetic subgroup of GBM with a distinct global methylation pattern, and that they are mutually exclusive with IDH1 mutations, which characterize a third mutation-defined subgroup. Three further epigenetic subgroups were enriched for hallmark genetic events of adult GBM and/or established transcriptomic signatures. We also demonstrate that the two H3F3A mutations give rise to GBMs in separate anatomic compartments, with differential regulation of transcription factors OLIG1, OLIG2, and FOXG1, possibly reflecting different cellular origins.
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All IPTOs cluster together with PTs, including IDH-mutant gliomas and the RTK I, RTK II, and mesenchymal subtypes of IDH wild-type GBM.
“We used the probes identified previously for GBM patient clus- tering24 and found that all IPTOs cluster together with PTs, including IDH-mut gliomas and the other three subtypes of IDH wild-type GBM, namely receptor tyrosine kinase I (RTK I), RTK II, andmesenchymal (MES) (Figure 3C).”
From Individualized patient tumor organoids faithfully preserve human brain tumor ecosystems and predict patient response to therapy (2025) · cites this paper as [24]
Global H3K27me3 loss in H3K27M DIPG was initially proposed due to inactivation of polycomb repressive complex 2 (PRC2), of which EZH2 is a canonical subunit, via sequestration of EZH2 to H3K27M.
“Global H3K27me3 loss in H3K27M DIPG was initially proposed due to inactivation of polycomb repressive complex 2 (PRC2), of which EZH2 is a canonical subunit, via sequestration of EZH2 to H3K27M 107 .”
From The roles of DNA, RNA and histone methylation in ageing and cancer (2019) · cites this paper as [107]
Several studies have shown that the loss of H3K27 trimethylation leads to major gene expression changes that are accompanied by a concomitant gain of acetylation at H3K27.
“Several studies have shown that the loss of H3K27 trimethylation leads to major gene expression changes that are accompanied by a concomitant gain of acetylation at H3K27 107,111,114 .”
From The roles of DNA, RNA and histone methylation in ageing and cancer (2019) · cites this paper as [107]
The mouse tumors show characteristic invasive nature, migration along blood vessels, colonization of the contralateral hemisphere, upregulation of Olig2, and scattered GFAP expression.
“This includes 1) the characteristic invasive nature of these tumors, 2) migration along blood vessels, 3) colonization of the contralateral hemisphere, 4) upregulation of Olig2, an established diagnostic marker for H3.3K27M pHGG (Sturm et al., 2012), which positively correlates with the extent of invasion of transformed cells in vivo, and 5) scattered GFAP expression is in tumor samples.”
From H3.3K27M Cooperates with Trp53 Loss and PDGFRA Gain in Mouse Embryonic Neural Progenitor Cells to Induce Invasive High-Grade Gliomas (2017) · cites this paper as Sturm et al., 2012
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- Authors
- Sturm, D., Witt, H., Hovestadt, V., Khuong-Quang, D.-A., Jones, D. T. W., Konermann, C., Pfaff, E., Tönjes, M., Sill, M., Bender, S., Kool, M., Zapatka, M., Becker, N., Zucknick, M., Hielscher, T., Liu, X.-Y., Fontebasso, A. M., Ryzhova, M., Albrecht, S., Jacob, K., Wolter, M., Ebinger, M., Schuhmann, M. U., van Meter, T., Frühwald, M. C., Hauch, H., Pekrun, A., Radlwimmer, B., Niehues, T., von Komorowski, G., Dürken, M., Kulozik, A. E., Madden, J., Donson, A., Foreman, N. K., Drissi, R., Fouladi, M., Scheurlen, W., von Deimling, A., Monoranu, C., Roggendorf, W., Herold-Mende, C., Unterberg, A., Kramm, C. M., Felsberg, J., Hartmann, C., Wiestler, B., Wick, W., Milde, T., Witt, O., Lindroth, A. M., Schwartzentruber, J., Faury, D., Fleming, A., Zakrzewska, M., Liberski, P. P., Zakrzewski, K., Hauser, P., Garami, M., Klekner, A., Bognar, L., Morrissy, S., Cavalli, F., Taylor, M. D., van Sluis, P., Koster, J., Versteeg, R., Volckmann, R., Mikkelsen, T., Aldape, K., Reifenberger, G., Collins, V. P., Majewski, J., Korshunov, A., Lichter, P., Plass, C., Jabado, N., & Pfister, S. M.
- Affiliations
- German Cancer Research Center (DE)
- McGill University Health Centre (CA)
- Montreal Children's Hospital (CA)
- Burdenko Neurosurgery Institute (RU)
- Heinrich Heine University Düsseldorf (DE)
- University Children's Hospital Tübingen (DE)
- Universitätsklinikum Tübingen (DE)
- University Hospital Augsburg (DE)
- SLK-Kliniken Heilbronn (DE)
- Prof. Hess Kinderklinik (DE)
- Helios Klinikum Krefeld (DE)
- University Hospital Heidelberg (DE)
- University of Colorado Denver (US)
- Cincinnati Children's Hospital Medical Center (US)
- Cnopf´sche Kinderklinik (DE)
- University of Würzburg (DE)
- Martin Luther University Halle-Wittenberg (DE)
- Medizinische Hochschule Hannover (DE)
- McGill University and Génome Québec Innovation Centre (CA)
- Medical University of Lodz (PL)
- Polish Mother’s Memorial Hospital Research Institute (PL)
- University of Toronto (CA)
- Amsterdam UMC Location University of Amsterdam (NL)
- Henry Ford Hospital (US)
- The University of Texas MD Anderson Cancer Center (US)
- University of Cambridge (GB)
- McGill University (CA)
- Corresponding author
- Plass, Christoph
- Jabado, Nada
- Pfister, Stefan M.
- ORCID
- Sturm, Dominik
- Witt, Hendrik
- Hovestadt, Volker
- Khuong-Quang, Dong-Anh
- Jones, David T.W.
- Pfaff, Elke
- Sill, Martin
- Kool, Marcel
- Zapatka, Marc
- Zucknick, Manuela
- Hielscher, Thomas
- Ryzhova, Marina
- Albrecht, Steffen
- Ebinger, Martin
- Schuhmann, Martin U.
- Frühwald, Michael C.
- Hauch, Holger
- Radlwimmer, Bernhard
- Niehues, Tim
- Dürken, Matthias
- Kulozik, Andreas E.
- Donson, Andrew
- Foreman, Nicholas K.
- Drissi, Rachid
- Fouladi, Maryam
- Unterberg, Andreas
- Kramm, Christof M.
- Felsberg, Jörg
- Hartmann, Christian
- Wiestler, Benedikt
- Wick, Wolfgang
- Milde, Till
- Witt, Olaf
- Lindroth, Anders M.
- Schwartzentruber, Jeremy
- Faury, Damien
- Fleming, Adam
- Zakrzewska, Magdalena
- Liberski, Pawel P.
- Zakrzewski, Krzysztof
- Cavalli, Florence
- Taylor, Michael D.
- Versteeg, Rogier
- Volckmann, Richard
- Mikkelsen, Tom
- Aldape, Kenneth
- Reifenberger, Guido
- Collins, V. Peter
- Majewski, Jacek
- Korshunov, Andrey
- Lichter, Peter
- Plass, Christoph
- Jabado, Nada
- Pfister, Stefan M.
- Venue
- Cancer Cell
- Publisher
- Elsevier BV
- Published
- 2012-10
- Volume
- 22
- Issue
- 4
- Pages
- 425-437
- ISSN
- 1535-6108 (ISSN-L)
- OpenAlex
- W2145489645
- Cited by
- 1,828
- References
- 10
- Citations by year
- 2026: 43 · 2025: 75 · 2024: 113 · 2023: 113 · 2022: 145 · 2021: 180 · 2020: 186 · 2019: 136 · 2018: 149 · 2017: 164 · 2016: 127 · 2015: 141 · 2014: 141 · 2013: 109 · 2012: 4
- FWCI
- 59.78
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 380 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Cancer Cell (publishedVersion)
- PubMed (publishedVersion)
- Pure Amsterdam UMC (publishedVersion)
- Repository of the Academy's Library (Library of the Hungarian Academy of Sciences) (acceptedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- University of Debrecen Electronic Archive (University of Debrecen) (submittedVersion)
- Semmelweis University Repository (Semmelweis University) (submittedVersion)
- OPUS (Augsburg University) (submittedVersion)
- Funders
- Deutsche Krebshilfe (108456, 109252)
- Stichting Kinderen Kankervrij
- Genome Canada
- Warren H. and Clara Cole Foundation
- Bundesministerium für Bildung und Forschung
- Institute of Cancer Research
- Topics
- Health Sciences › Medicine › Genetics › Glioma Diagnosis and Treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
- Health Sciences › Medicine › Hematology › Acute Myeloid Leukemia Research
- Keywords
- glioblastoma, H3F3A mutation, histone H3.3, IDH1 mutation, DNA methylation, tumor heterogeneity, pediatric glioblastoma, Olig1, Olig2, FOXG1, transcription factor regulation, tumor cell of origin
- MeSH terms
- Adult, Brain Neoplasms, Child, Glioblastoma, Histones, Humans, Isocitrate Dehydrogenase, Mutation, DNA Methylation, Receptor, Platelet-Derived Growth Factor alpha, Epigenesis, Genetic, Transcriptome
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