Histone H3.3K27M Represses p16 to Accelerate Gliomagenesis in a Murine Model of DIPG
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Abstract
Abstract Diffuse intrinsic pontine glioma (DIPG) is a highly aggressive pediatric brainstem tumor genetically distinguished from adult GBM by the high prevalence of the K27M mutation in the histone H3 variant H3.3 (H3F3A). This mutation reprograms the H3K27me3 epigenetic landscape of DIPG by inhibiting the H3K27-specific histone methyltransferase EZH2. This globally reduces H3K27me2/3, critical repressive marks responsible for cell fate decisions, and also causes focal gain of H3K27me3 throughout the epigenome. To date, the tumor-driving effects of H3.3K27M remain largely unknown. Here, it is demonstrated that H3.3K27M cooperates with PDGF-B in vivo, enhancing gliomagenesis and reducing survival of p53 wild-type (WT) and knockout murine models of DIPG. H3.3K27M expression drives increased proliferation of tumor-derived murine neurospheres, suggesting that cell-cycle deregulation contributes to increased malignancy in mutant tumors. RNA sequencing on tumor tissue from H3.3K27M-expressing mice indicated global upregulation of PRC2 target genes, and a subset of newly repressed genes enriched in regulators of development and cell proliferation. Strikingly, H3.3K27M induced targeted repression of the p16/ink4a (CDKN2A) locus, a critical regulator of the G0–G1 to S-phase transition. Increased levels of H3K27me3 were observed at the p16 promoter; however, pharmacologic reduction of methylation at this promoter did not rescue p16 expression. Although DNA methylation is also present at this promoter, it is not K27M dependent. Intriguingly, inhibition of DNA methylation restores p16 levels and is cytotoxic against murine tumor cells. Importantly, these data reveal that H3.3K27M-mediated p16 repression is an important mechanism underlying the proliferation of H3.3K27M tumor cells, as in vivo cdkn2a knockout eliminates the survival difference between H3.3K27M and H3.3WT tumor-bearing mice. Implications: This study shows that H3.3K27M mutation and PDGF signaling act in concert to accelerate gliomagenesis in a genetic mouse model and identifies repression of p16 tumor suppressor as a target of H3.3K27M, highlighting the G1–S cell-cycle transition as a promising therapeutic avenue. Mol Cancer Res; 15(9); 1243–54. ©2017 AACR.
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Other in vivo H3.3K27M-DIPG models required constitutive PDGF-B ligand, which is not present in pediatric high-grade glioma, and could induce tumors even with wild-type H3.3.
“Other attempts to model H3.3K27M-DIPG in vivo have required constitutive expression of the PDGF-B ligand, which is not present in pHGG and can induce tumors even with wild-type (WT) H3.3”
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 Cordero et al., 2017
Unlike wild-type PDGFRA, PDGFRAD842V does not require H3.3K27M to drive tumorigenesis in vivo.
“suggesting that, unlike WT PDGFRA, PDGFRAD842V does not require H3.3K27M to drive tumorigenesis in vivo”
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 Cordero et al., 2017
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- Authors
- Cordero, F. J., Huang, Z., Grenier, C., He, X., Hu, G., McLendon, R. E., Murphy, S. K., Hashizume, R., & Becher, O. J.
- Affiliations
- Duke University (US)
- Duke Medical Center (US)
- Northwestern University (US)
- Corresponding author
- Becher, Oren J.
- Venue
- Molecular Cancer Research
- Published
- 2017-08-31
- Volume
- 15
- Issue
- 9
- Pages
- 1243-1254
- ISSN
- 1541-7786 (ISSN-L)
- 1557-3125
- PMC
- PMC5581686
- OpenAlex
- W2616008385
- Cited by
- 157
- References
- 56
- Citations by year
- 2026: 10 · 2025: 13 · 2024: 8 · 2023: 15 · 2022: 25 · 2021: 28 · 2020: 24 · 2019: 21 · 2018: 10 · 2017: 3
- FWCI
- 9.11
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Molecular Cancer Research (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- NIH (NS093986-01, NS086917)
- Topics
- Health Sciences › Medicine › Genetics › Glioma Diagnosis and Treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Keywords
- diffuse intrinsic pontine glioma, H3.3K27M mutation, histone H3.3, gliomagenesis, EZH2, H3K27me3, polycomb repressive complex 2, DNA methylation, cell proliferation, tumor cell survival, pediatric brainstem tumors
- MeSH terms
- Animals, Disease Models, Animal, Glioma, Histones, Mice, Inbred C57BL, Cyclin-Dependent Kinase Inhibitor p16, Brain Stem Neoplasms, Cell Line, Tumor, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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