A systems-based approach to uterine fibroids identifies differential splicing associated with abnormal uterine bleeding

Abstract Background Uterine fibroids (UFs), benign tumours prevalent in up to 80% of women of reproductive age, are associated with significant morbidity, including abnormal uterine bleeding, pain and infertility. Despite identification of key genomic alterations in MED12 and HMGA2, the pathogenic m...

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Main Authors: Chen-Yi Wang, Martin Philpott, Darragh P O’Brien, Anne Ndungu, Jessica Malzahn, Marina Maritati, Neelam Mehta, Vicki Gamble, Beatriz Martinez-Burgo, Sarah Bonham, Roman Fischer, Kurtis Garbutt, Christian M. Becker, Sanjiv Manek, Adrian L. Harris, Frank Sacher, Maik Obendorf, Nicole Schmidt, Jörg Müller, Thomas M. Zollner, Krina T. Zondervan, Benedikt M. Kessler, Udo Oppermann, Adam P. Cribbs
Format: Article
Language:English
Published: Nature Portfolio 2025-07-01
Series:Communications Medicine
Online Access:https://doi.org/10.1038/s43856-025-01051-x
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author Chen-Yi Wang
Martin Philpott
Darragh P O’Brien
Anne Ndungu
Jessica Malzahn
Marina Maritati
Neelam Mehta
Vicki Gamble
Beatriz Martinez-Burgo
Sarah Bonham
Roman Fischer
Kurtis Garbutt
Christian M. Becker
Sanjiv Manek
Adrian L. Harris
Frank Sacher
Maik Obendorf
Nicole Schmidt
Jörg Müller
Thomas M. Zollner
Krina T. Zondervan
Benedikt M. Kessler
Udo Oppermann
Adam P. Cribbs
author_facet Chen-Yi Wang
Martin Philpott
Darragh P O’Brien
Anne Ndungu
Jessica Malzahn
Marina Maritati
Neelam Mehta
Vicki Gamble
Beatriz Martinez-Burgo
Sarah Bonham
Roman Fischer
Kurtis Garbutt
Christian M. Becker
Sanjiv Manek
Adrian L. Harris
Frank Sacher
Maik Obendorf
Nicole Schmidt
Jörg Müller
Thomas M. Zollner
Krina T. Zondervan
Benedikt M. Kessler
Udo Oppermann
Adam P. Cribbs
author_sort Chen-Yi Wang
collection DOAJ
description Abstract Background Uterine fibroids (UFs), benign tumours prevalent in up to 80% of women of reproductive age, are associated with significant morbidity, including abnormal uterine bleeding, pain and infertility. Despite identification of key genomic alterations in MED12 and HMGA2, the pathogenic mechanisms underlying UFs and heavy menstrual bleeding (HMB) remain poorly understood. Methods To correlate systematically genetic, transcriptional and proteomic phenotypes, we conducted an integrative multi-omic approach utilising targeted DNA sequencing, RNA sequencing and proteomic methodologies, encompassing fibroid, myometrium, and endometrium tissues from 91 patients. Results In addition to confirming the presence of MED12 mutations, we identify variants in AHR and COL4A6. Multi-omic analysis of endometrium identifies latent factors that correlate with HMB and fibroid presence with driver mutations of MED12, AHR, and COL4A6, which are associated with pathways involved in angiogenesis, extracellular matrix organisation and RNA splicing. We propose a model, supported by in vivo evidence, where altered signalling of MED12-mutated fibroids influences RNA transcript isoform expression in endometrium, potentially leading to abnormal uterine bleeding. Conclusions This study presents a comprehensive integrative approach, revealing that genetic alterations in UF may influence endometrial function via signalling impacts on the RNA splicing mechanism. Our findings advance the understanding of complex molecular pathways in UF pathogenesis and UF-associated endometrial dysfunction, offering insights for targeted therapeutic development.
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spelling doaj-art-e9437efd468b482f8f302ec62eab89f82025-08-20T03:46:29ZengNature PortfolioCommunications Medicine2730-664X2025-07-015111610.1038/s43856-025-01051-xA systems-based approach to uterine fibroids identifies differential splicing associated with abnormal uterine bleedingChen-Yi Wang0Martin Philpott1Darragh P O’Brien2Anne Ndungu3Jessica Malzahn4Marina Maritati5Neelam Mehta6Vicki Gamble7Beatriz Martinez-Burgo8Sarah Bonham9Roman Fischer10Kurtis Garbutt11Christian M. Becker12Sanjiv Manek13Adrian L. Harris14Frank Sacher15Maik Obendorf16Nicole Schmidt17Jörg Müller18Thomas M. Zollner19Krina T. Zondervan20Benedikt M. Kessler21Udo Oppermann22Adam P. Cribbs23Botnar Research Centre, NIHR BRC, University of OxfordBotnar Research Centre, NIHR BRC, University of OxfordTarget Discovery Institute, Centre for Medicines Discovery, Nuffield Department of Medicine, University of OxfordNuffield Department of Women’s & Reproductive Health, University of OxfordBotnar Research Centre, NIHR BRC, University of OxfordBotnar Research Centre, NIHR BRC, University of OxfordBotnar Research Centre, NIHR BRC, University of OxfordBotnar Research Centre, NIHR BRC, University of OxfordNuffield Department of Women’s & Reproductive Health, University of OxfordTarget Discovery Institute, Centre for Medicines Discovery, Nuffield Department of Medicine, University of OxfordTarget Discovery Institute, Centre for Medicines Discovery, Nuffield Department of Medicine, University of OxfordNuffield Department of Women’s & Reproductive Health, University of OxfordNuffield Department of Women’s & Reproductive Health, University of OxfordNuffield Department of Women’s & Reproductive Health, University of OxfordDepartment of Oncology, University of OxfordResearch and Early Development, Bayer AGResearch and Early Development, Bayer AGResearch and Early Development, Bayer AGResearch and Early Development, Bayer AGResearch and Early Development, Bayer AGNuffield Department of Women’s & Reproductive Health, University of OxfordTarget Discovery Institute, Centre for Medicines Discovery, Nuffield Department of Medicine, University of OxfordBotnar Research Centre, NIHR BRC, University of OxfordBotnar Research Centre, NIHR BRC, University of OxfordAbstract Background Uterine fibroids (UFs), benign tumours prevalent in up to 80% of women of reproductive age, are associated with significant morbidity, including abnormal uterine bleeding, pain and infertility. Despite identification of key genomic alterations in MED12 and HMGA2, the pathogenic mechanisms underlying UFs and heavy menstrual bleeding (HMB) remain poorly understood. Methods To correlate systematically genetic, transcriptional and proteomic phenotypes, we conducted an integrative multi-omic approach utilising targeted DNA sequencing, RNA sequencing and proteomic methodologies, encompassing fibroid, myometrium, and endometrium tissues from 91 patients. Results In addition to confirming the presence of MED12 mutations, we identify variants in AHR and COL4A6. Multi-omic analysis of endometrium identifies latent factors that correlate with HMB and fibroid presence with driver mutations of MED12, AHR, and COL4A6, which are associated with pathways involved in angiogenesis, extracellular matrix organisation and RNA splicing. We propose a model, supported by in vivo evidence, where altered signalling of MED12-mutated fibroids influences RNA transcript isoform expression in endometrium, potentially leading to abnormal uterine bleeding. Conclusions This study presents a comprehensive integrative approach, revealing that genetic alterations in UF may influence endometrial function via signalling impacts on the RNA splicing mechanism. Our findings advance the understanding of complex molecular pathways in UF pathogenesis and UF-associated endometrial dysfunction, offering insights for targeted therapeutic development.https://doi.org/10.1038/s43856-025-01051-x
spellingShingle Chen-Yi Wang
Martin Philpott
Darragh P O’Brien
Anne Ndungu
Jessica Malzahn
Marina Maritati
Neelam Mehta
Vicki Gamble
Beatriz Martinez-Burgo
Sarah Bonham
Roman Fischer
Kurtis Garbutt
Christian M. Becker
Sanjiv Manek
Adrian L. Harris
Frank Sacher
Maik Obendorf
Nicole Schmidt
Jörg Müller
Thomas M. Zollner
Krina T. Zondervan
Benedikt M. Kessler
Udo Oppermann
Adam P. Cribbs
A systems-based approach to uterine fibroids identifies differential splicing associated with abnormal uterine bleeding
Communications Medicine
title A systems-based approach to uterine fibroids identifies differential splicing associated with abnormal uterine bleeding
title_full A systems-based approach to uterine fibroids identifies differential splicing associated with abnormal uterine bleeding
title_fullStr A systems-based approach to uterine fibroids identifies differential splicing associated with abnormal uterine bleeding
title_full_unstemmed A systems-based approach to uterine fibroids identifies differential splicing associated with abnormal uterine bleeding
title_short A systems-based approach to uterine fibroids identifies differential splicing associated with abnormal uterine bleeding
title_sort systems based approach to uterine fibroids identifies differential splicing associated with abnormal uterine bleeding
url https://doi.org/10.1038/s43856-025-01051-x
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