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[Preprint]. 2024 Mar 20:2024.03.19.585212. [Version 1] doi: 10.1101/2024.03.19.585212

Epigenetic landscape reorganization and reactivation of embryonic development genes are associated with malignancy in IDH-mutant astrocytoma

Santoesha A Ghisai, Levi van Hijfte, Wies R Vallentgoed, C Mircea S Tesileanu, Iris de Heer, Johan M Kros, Marc Sanson, Thierry Gorlia, Wolfgang Wick, Michael A Vogelbaum, Alba A Brandes, Enrico Franceschi, Paul M Clement, Anna K Nowak, Vassilis Golfinopoulos, Martin J van den Bent, Pim J French, Youri Hoogstrate
PMCID: PMC10983878  PMID: 38562747

Abstract

Accurate grading of IDH-mutant gliomas defines patient prognosis and guides the treatment path. Histological grading is however difficult and, apart from CDKN2A/B homozygous deletions in IDH-mutant astrocytomas, there are no other objective molecular markers used for grading. Experimental Design: RNA-sequencing was conducted on primary IDH-mutant astrocytomas (n=138) included in the prospective CATNON trial, which was performed to assess the prognostic effect of adjuvant and concurrent temozolomide. We integrated the RNA sequencing data with matched DNA-methylation and NGS data. We also used multi-omics data from IDH-mutant astrocytomas included in the TCGA dataset and validated results on matched primary and recurrent samples from the GLASS-NL study. We used the DNA-methylation profiles to generate a Continuous Grading Coefficient (CGC) that is based on classification scores derived from a CNS-tumor classifier. We found that the CGC was an independent predictor of survival outperforming current WHO-CNS5 and methylation-based classification. Our RNA-sequencing analysis revealed four distinct transcription clusters that were associated with i) an upregulation of cell cycling genes; ii) a downregulation of glial differentiation genes; iii) an upregulation of embryonic development genes (e.g. HOX, PAX and TBX) and iv) an upregulation of extracellular matrix genes. The upregulation of embryonic development genes was associated with a specific increase of CpG island methylation near these genes.

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