Robust molecular subgrouping and reference-free aneuploidy detection in medulloblastoma using low-depth whole genome bisulfite sequencing

Abstract Medulloblastoma comprises four principal molecular disease groups and their component subgroups, each with distinct molecular and clinical features. Group assignment is currently achieved diagnostically using Illumina DNA methylation microarray. Whole-genome sequencing (WGS) capacity is rap...

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Main Authors: Dean Thompson, Jemma Castle, Martin Sill, Stefan M. Pfister, Simon Bailey, Debbie Hicks, Steven C. Clifford, Edward C. Schwalbe
Format: Article
Language:English
Published: BMC 2025-06-01
Series:Acta Neuropathologica Communications
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Online Access:https://doi.org/10.1186/s40478-025-02049-1
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author Dean Thompson
Jemma Castle
Martin Sill
Stefan M. Pfister
Simon Bailey
Debbie Hicks
Steven C. Clifford
Edward C. Schwalbe
author_facet Dean Thompson
Jemma Castle
Martin Sill
Stefan M. Pfister
Simon Bailey
Debbie Hicks
Steven C. Clifford
Edward C. Schwalbe
author_sort Dean Thompson
collection DOAJ
description Abstract Medulloblastoma comprises four principal molecular disease groups and their component subgroups, each with distinct molecular and clinical features. Group assignment is currently achieved diagnostically using Illumina DNA methylation microarray. Whole-genome sequencing (WGS) capacity is rapidly expanding in the clinical setting and the development of platform-independent, sequence-based assays of molecular group offers significant potential. Specifically, whole-genome bisulfite sequencing (WGBS) enables assessment of genome-wide methylation status at single-base resolution, however its routine application has been limited by high DNA input requirements, cost, and a lack of pipelines tailored to more rapidly-acquired and cost-effective low-depth (< 10x) sequencing data. We utilised WGBS data for 69 medulloblastomas, comprising 35 in-house low-depth (~ 10x) and 34 publicly available high-depth (~ 30x) samples, alongside cerebellar controls (n = 8), all with matched DNA methylation microarray data. We assessed quality (QC) and imputation approaches using low-pass WGBS data, assessed inter-platform correlation and identified molecular groups and subgroups by directly integrating matched/associated loci from WGBS sample data with the MNP classifier probeset. We further assessed and optimised reference-free aneuploidy detection using low-pass WGBS and assessed concordance with microarray-derived calls. We developed and optimised pipelines for processing, QC, and analysis of low-pass WGBS data, suitable for routine molecular subgrouping and reference-free aneuploidy assessment. We demonstrate that low-pass WGBS data can (i) be integrated into existing array-trained models with high assignment probabilities for both principal molecular groups (97% concordance) and molecular subgroups (94.2% concordance), and (ii) detect clinically relevant focal copy number changes, including SNCAIP, with greater sensitivity than microarray approaches. Low-pass WGBS performs equivalently to array-based methods at comparable cost. Finally, its ascertainment of the full methylome enables elucidation of additional biological complexity and inter-tumoural heterogeneity that has hitherto been inaccessible. These findings provide proof-of-concept for clinical adoption of low-pass WGBS, applied using standard WGS technology.
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spelling doaj-art-e820dbea1f874493a90f603ce582e8b12025-08-20T03:27:13ZengBMCActa Neuropathologica Communications2051-59602025-06-0113111210.1186/s40478-025-02049-1Robust molecular subgrouping and reference-free aneuploidy detection in medulloblastoma using low-depth whole genome bisulfite sequencingDean Thompson0Jemma Castle1Martin Sill2Stefan M. Pfister3Simon Bailey4Debbie Hicks5Steven C. Clifford6Edward C. Schwalbe7Wolfson Childhood Cancer Research Centre, Newcastle University Centre for CancerWolfson Childhood Cancer Research Centre, Newcastle University Centre for CancerHopp Children´s Cancer Center (KiTZ)Hopp Children´s Cancer Center (KiTZ)Wolfson Childhood Cancer Research Centre, Newcastle University Centre for CancerWolfson Childhood Cancer Research Centre, Newcastle University Centre for CancerWolfson Childhood Cancer Research Centre, Newcastle University Centre for CancerWolfson Childhood Cancer Research Centre, Newcastle University Centre for CancerAbstract Medulloblastoma comprises four principal molecular disease groups and their component subgroups, each with distinct molecular and clinical features. Group assignment is currently achieved diagnostically using Illumina DNA methylation microarray. Whole-genome sequencing (WGS) capacity is rapidly expanding in the clinical setting and the development of platform-independent, sequence-based assays of molecular group offers significant potential. Specifically, whole-genome bisulfite sequencing (WGBS) enables assessment of genome-wide methylation status at single-base resolution, however its routine application has been limited by high DNA input requirements, cost, and a lack of pipelines tailored to more rapidly-acquired and cost-effective low-depth (< 10x) sequencing data. We utilised WGBS data for 69 medulloblastomas, comprising 35 in-house low-depth (~ 10x) and 34 publicly available high-depth (~ 30x) samples, alongside cerebellar controls (n = 8), all with matched DNA methylation microarray data. We assessed quality (QC) and imputation approaches using low-pass WGBS data, assessed inter-platform correlation and identified molecular groups and subgroups by directly integrating matched/associated loci from WGBS sample data with the MNP classifier probeset. We further assessed and optimised reference-free aneuploidy detection using low-pass WGBS and assessed concordance with microarray-derived calls. We developed and optimised pipelines for processing, QC, and analysis of low-pass WGBS data, suitable for routine molecular subgrouping and reference-free aneuploidy assessment. We demonstrate that low-pass WGBS data can (i) be integrated into existing array-trained models with high assignment probabilities for both principal molecular groups (97% concordance) and molecular subgroups (94.2% concordance), and (ii) detect clinically relevant focal copy number changes, including SNCAIP, with greater sensitivity than microarray approaches. Low-pass WGBS performs equivalently to array-based methods at comparable cost. Finally, its ascertainment of the full methylome enables elucidation of additional biological complexity and inter-tumoural heterogeneity that has hitherto been inaccessible. These findings provide proof-of-concept for clinical adoption of low-pass WGBS, applied using standard WGS technology.https://doi.org/10.1186/s40478-025-02049-1MedulloblastomaMethylationMicroarrayWGBSSequencingAneuploidy
spellingShingle Dean Thompson
Jemma Castle
Martin Sill
Stefan M. Pfister
Simon Bailey
Debbie Hicks
Steven C. Clifford
Edward C. Schwalbe
Robust molecular subgrouping and reference-free aneuploidy detection in medulloblastoma using low-depth whole genome bisulfite sequencing
Acta Neuropathologica Communications
Medulloblastoma
Methylation
Microarray
WGBS
Sequencing
Aneuploidy
title Robust molecular subgrouping and reference-free aneuploidy detection in medulloblastoma using low-depth whole genome bisulfite sequencing
title_full Robust molecular subgrouping and reference-free aneuploidy detection in medulloblastoma using low-depth whole genome bisulfite sequencing
title_fullStr Robust molecular subgrouping and reference-free aneuploidy detection in medulloblastoma using low-depth whole genome bisulfite sequencing
title_full_unstemmed Robust molecular subgrouping and reference-free aneuploidy detection in medulloblastoma using low-depth whole genome bisulfite sequencing
title_short Robust molecular subgrouping and reference-free aneuploidy detection in medulloblastoma using low-depth whole genome bisulfite sequencing
title_sort robust molecular subgrouping and reference free aneuploidy detection in medulloblastoma using low depth whole genome bisulfite sequencing
topic Medulloblastoma
Methylation
Microarray
WGBS
Sequencing
Aneuploidy
url https://doi.org/10.1186/s40478-025-02049-1
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