Integrative analysis of epigenetic and transcriptional interrelations identifies histotype-specific biomarkers in early-stage ovarian carcinoma

Abstract Background Epithelial ovarian cancer (EOC) is a deadly and heterogenous disease comprising five major histotypes: clear cell carcinoma (CCC), endometrioid carcinoma (EC), low- and high-grade serous carcinoma (LGSC, HGSC), and mucinous carcinoma (MC). Despite this heterogeneity, EOC is often...

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Main Authors: Hugo Swenson, Ella Ittner, Lucas Werner, Elisabeth Werner Rönnerman, Claudia Mateoiu, Anikó Kovács, Pernilla Dahm-Kähler, Ghassan M. Saed, Szilárd Nemes, Per Karlsson, Toshima Z. Parris, Khalil Helou
Format: Article
Language:English
Published: BMC 2025-05-01
Series:Journal of Ovarian Research
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Online Access:https://doi.org/10.1186/s13048-025-01676-5
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author Hugo Swenson
Ella Ittner
Lucas Werner
Elisabeth Werner Rönnerman
Claudia Mateoiu
Anikó Kovács
Pernilla Dahm-Kähler
Ghassan M. Saed
Szilárd Nemes
Per Karlsson
Toshima Z. Parris
Khalil Helou
author_facet Hugo Swenson
Ella Ittner
Lucas Werner
Elisabeth Werner Rönnerman
Claudia Mateoiu
Anikó Kovács
Pernilla Dahm-Kähler
Ghassan M. Saed
Szilárd Nemes
Per Karlsson
Toshima Z. Parris
Khalil Helou
author_sort Hugo Swenson
collection DOAJ
description Abstract Background Epithelial ovarian cancer (EOC) is a deadly and heterogenous disease comprising five major histotypes: clear cell carcinoma (CCC), endometrioid carcinoma (EC), low- and high-grade serous carcinoma (LGSC, HGSC), and mucinous carcinoma (MC). Despite this heterogeneity, EOC is often treated as a homogenous disease, and reliable screening tests are lacking. Although progress has been made, there is a pressing need for biomarkers to refine patient stratification, guide treatment, and improve outcomes. Here, we elucidated the relationship between DNA methylation and gene expression patterns in EOC to identify histotype-specific biomarkers. Methods Differential DNA methylation and gene expression analyses were performed for 86 early-stage EOC samples after histopathological reclassification stratified by histotype. The correlation between DNA methylation and gene expression was examined, and histotype-specific biomarkers were identified. Hierarchical clustering and predictive machine learning modeling were employed to assess the performance of the histotype-specific biomarkers using four external cohorts. Results EOC histotypes exhibited distinct epigenetic, transcriptional, and functional profiles, with candidate histotype-specific biomarkers such as CTSE and VCAN effectively distinguishing CCC, HGSC, and MC on the transcriptional level. Gene expression for the candidate biomarkers was found to be reproducible across external cohorts, with histotype-specific differences remaining homogenous. Conclusions This study identified promising histotype-specific biomarkers for EOC using integrative transcriptomic and epigenomic analysis. Furthermore, these findings indicate that additional stratification or potential reclassification of the EC histotype is warranted in future studies.
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spelling doaj-art-dc3b3e4d79c6498ebd032b2f7b4e204f2025-08-20T03:48:18ZengBMCJournal of Ovarian Research1757-22152025-05-0118111510.1186/s13048-025-01676-5Integrative analysis of epigenetic and transcriptional interrelations identifies histotype-specific biomarkers in early-stage ovarian carcinomaHugo Swenson0Ella Ittner1Lucas Werner2Elisabeth Werner Rönnerman3Claudia Mateoiu4Anikó Kovács5Pernilla Dahm-Kähler6Ghassan M. Saed7Szilárd Nemes8Per Karlsson9Toshima Z. Parris10Khalil Helou11Department of Oncology, Sahlgrenska Academy, Institute of Clinical Sciences, University of GothenburgDepartment of Oncology, Sahlgrenska Academy, Institute of Clinical Sciences, University of GothenburgDepartment of Oncology, Sahlgrenska Academy, Institute of Clinical Sciences, University of GothenburgDepartment of Clinical Pathology, Region Västra Götaland, Sahlgrenska University HospitalDepartment of Clinical Pathology, Region Västra Götaland, Sahlgrenska University HospitalDepartment of Clinical Pathology, Region Västra Götaland, Sahlgrenska University HospitalDepartment of Obstetrics and Gynecology, Sahlgrenska Academy, Institute of Clinical Sciences, University of GothenburgDepartment of Obstetrics and Gynecology, Wayne State University School of MedicineAstraZenecaDepartment of Oncology, Sahlgrenska Academy, Institute of Clinical Sciences, University of GothenburgDepartment of Oncology, Sahlgrenska Academy, Institute of Clinical Sciences, University of GothenburgDepartment of Oncology, Sahlgrenska Academy, Institute of Clinical Sciences, University of GothenburgAbstract Background Epithelial ovarian cancer (EOC) is a deadly and heterogenous disease comprising five major histotypes: clear cell carcinoma (CCC), endometrioid carcinoma (EC), low- and high-grade serous carcinoma (LGSC, HGSC), and mucinous carcinoma (MC). Despite this heterogeneity, EOC is often treated as a homogenous disease, and reliable screening tests are lacking. Although progress has been made, there is a pressing need for biomarkers to refine patient stratification, guide treatment, and improve outcomes. Here, we elucidated the relationship between DNA methylation and gene expression patterns in EOC to identify histotype-specific biomarkers. Methods Differential DNA methylation and gene expression analyses were performed for 86 early-stage EOC samples after histopathological reclassification stratified by histotype. The correlation between DNA methylation and gene expression was examined, and histotype-specific biomarkers were identified. Hierarchical clustering and predictive machine learning modeling were employed to assess the performance of the histotype-specific biomarkers using four external cohorts. Results EOC histotypes exhibited distinct epigenetic, transcriptional, and functional profiles, with candidate histotype-specific biomarkers such as CTSE and VCAN effectively distinguishing CCC, HGSC, and MC on the transcriptional level. Gene expression for the candidate biomarkers was found to be reproducible across external cohorts, with histotype-specific differences remaining homogenous. Conclusions This study identified promising histotype-specific biomarkers for EOC using integrative transcriptomic and epigenomic analysis. Furthermore, these findings indicate that additional stratification or potential reclassification of the EC histotype is warranted in future studies.https://doi.org/10.1186/s13048-025-01676-5Ovarian cancerGene expressionDNA methylationBioinformaticsMachine learning
spellingShingle Hugo Swenson
Ella Ittner
Lucas Werner
Elisabeth Werner Rönnerman
Claudia Mateoiu
Anikó Kovács
Pernilla Dahm-Kähler
Ghassan M. Saed
Szilárd Nemes
Per Karlsson
Toshima Z. Parris
Khalil Helou
Integrative analysis of epigenetic and transcriptional interrelations identifies histotype-specific biomarkers in early-stage ovarian carcinoma
Journal of Ovarian Research
Ovarian cancer
Gene expression
DNA methylation
Bioinformatics
Machine learning
title Integrative analysis of epigenetic and transcriptional interrelations identifies histotype-specific biomarkers in early-stage ovarian carcinoma
title_full Integrative analysis of epigenetic and transcriptional interrelations identifies histotype-specific biomarkers in early-stage ovarian carcinoma
title_fullStr Integrative analysis of epigenetic and transcriptional interrelations identifies histotype-specific biomarkers in early-stage ovarian carcinoma
title_full_unstemmed Integrative analysis of epigenetic and transcriptional interrelations identifies histotype-specific biomarkers in early-stage ovarian carcinoma
title_short Integrative analysis of epigenetic and transcriptional interrelations identifies histotype-specific biomarkers in early-stage ovarian carcinoma
title_sort integrative analysis of epigenetic and transcriptional interrelations identifies histotype specific biomarkers in early stage ovarian carcinoma
topic Ovarian cancer
Gene expression
DNA methylation
Bioinformatics
Machine learning
url https://doi.org/10.1186/s13048-025-01676-5
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