Cited by 157Glioma Diagnosis and TreatmentChromatin Remodeling and CancerEpigenetics and DNA Methylation

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Histone H3.3K27M Represses p16 to Accelerate Gliomagenesis in a Murine Model of DIPG

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Cordero, Francisco J., Huang, Zhiqing, Grenier, Carole, He, Xingyao, Hu, Guo, McLendon, Roger E., Murphy, Susan K., Hashizume, Rintaro, Becher, Oren J.·2017·Molecular Cancer Research

DOI 10.1158/1541-7786.mcr-16-0389PMC PMC5581686

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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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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.
ORCID: Huang, Zhiqing
Hu, Guo
McLendon, Roger E.
Murphy, Susan K.
Hashizume, Rintaro
Becher, Oren J.
Venue: Molecular Cancer Research
Publisher: American Association for Cancer Research (AACR)
Published: 2017-08-31
Volume: 15
Issue: 9
Pages: 1243-1254
ISSN: 1541-7786 (ISSN-L)
1557-3125
DOI: 10.1158/1541-7786.mcr-16-0389
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 › Oncology › 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

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Histone H3.3K27M Represses p16 to Accelerate Gliomagenesis in a Murine Model of DIPG

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