Cancer-associated mutations in endometriosis: shedding light on the pathogenesis and pathophysiology
Abstract
BACKGROUND: Endometriosis is a benign gynaecological disease. Thus, it came as a complete surprise when it was reported recently that the majority of deep endometriosis lesions harbour somatic mutations and a sizeable portion of them contain known cancer-associated mutations (CAMs). Four more studies have since been published, all demonstrating the existence of CAMs in different subtypes of endometriosis. While the field is still evolving, the confirmation of CAMs has raised many questions that were previously overlooked. OBJECTIVE AND RATIONALE: A comprehensive overview of CAMs in endometriosis has been produced. In addition, with the recently emerged understanding of the natural history of endometriotic lesions as well as CAMs in normal and apparently healthy tissues, this review attempts to address the following questions: Why has there been such a wild discrepancy in reported mutation frequencies? Why does ectopic endometrium have a higher mutation rate than that of eutopic endometrium? Would the presence of CAMs in endometriotic lesions increase the risk of cancer to the bearers? Why do endometriotic epithelial cells have much higher mutation frequencies than their stromal counterpart? What clinical implications, if any, do the CAMs have for the bearers? Do these CAMs tell us anything about the pathogenesis and/or pathophysiology of endometriosis? SEARCH METHODS: The PubMed database was searched, from its inception to September 2019, for all papers in English using the term ‘endometriosis and CAM’, ‘endometriosis and cancer-driver mutation’, ‘somatic mutations’, ‘fibrosis’, ‘fibrosis and epigenetic’, ‘CAMs and tumorigenesis’, ‘somatic mutation and normal tissues’, ‘oestrogen receptor and fibrosis’, ‘oxidative stress and fibrosis’, ‘ARID1A mutation’, and ‘Kirsten rat sarcoma mutation and therapeutics’. All retrieved papers were read and, when relevant, incorporated into the review results. OUTCOMES: Seven papers that identified CAMs in endometriosis using various sequencing methods were retrieved, and their results were somewhat different. Yet, it is apparent that those using microdissection techniques and more accurate sequencing methods found more CAMs, echoing recent discoveries that apparently healthy tissues also harbour CAMs as a result of the replicative aging process. Hence endometriotic lesions, irrespective of subtype, if left intact, would generate CAMs as part of replicative aging, oxidative stress and perhaps other factors yet to be identified and, in some rare cases, develop cancer. The published data still are unable to paint a clear picture on pathogenesis of endometriosis. However, since endometriotic epithelial cells have a higher turnover than their stromal counterpart due to cyclic bleeding, and since the endometriotic stromal component can be formed by refresh influx of mesenchymal cells through epithelial–mesenchymal transition, endothelial–mesenchymal transition, mesothelial–mesenchymal transition and other processes as well as recruitment of bone-marrow-derived stem cells and outflow due to smooth muscle metaplasia, endometriotic epithelial cells have much higher mutation frequencies than their stromal counterpart. The epithelial and stromal cellular components develop in a dependent and co-evolving manner. Genes involved in CAMs are likely to be active players in lesional fibrogenesis, and hyperestrogenism and oxidative stress are likely drivers of both CAMs and fibrogenesis. Finally, endometriotic lesions harbouring CAMs would conceivably be more refractory to medical treatment, due, in no small part, to their high fibrotic content and reduced vascularity and cellularity. WIDER IMPLICATIONS: The accumulating data on CAMs in endometriosis have shed new light on the pathogenesis and pathophysiology of endometriosis. They also suggest new challenges in management. The distinct yet co-evolving developmental trajectories of endometriotic stroma and epithelium underscore the importance of the lesional microenvironment and ever-changing cellular identity. Mutational profiling of normal endometrium from women of different ages and reproductive history is needed in order to gain a deeper understanding of the pathogenesis. Moreover, one area that has conspicuously received scant attention is the epigenetic landscape of ectopic, eutopic and normal endometrium.
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Molecular biology techniques using next-generation sequencing have provided clues to the origin of endometriosis and pathogenesis that cannot be elucidated by epidemiological investigations alone.
“Recently, molecular biology techniques using a next‐generation sequencing have also provided clues to the origin of endometriosis and pathogenesis that cannot be elucidated by epidemiological investigations alone.”
From Extra-pelvic endometriosis: a review. (2020) · cites this paper as [102]
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Self-citationEpigenetic Modification Mechanisms Involved in Inflammation and Fibrosis in Renal Pathology
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Estrogen receptor-dependent activation of AP-1 via non-genomic signalling
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Self-citation
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Extra-pelvic endometriosis: a review.
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The Double Engines and Single Checkpoint Theory of Endometriosis
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- Authors
- Guo, S.-W.
- Affiliations
- Fudan University (CN)
- Corresponding author
- Guo, Sun-Wei
- ORCID
- Guo, Sun-Wei
- Venue
- Human Reproduction Update
- Publisher
- Oxford University Press (OUP)
- Published
- 2020-03-10
- Volume
- 26
- Issue
- 3
- Pages
- 423-449
- ISSN
- 1355-4786 (ISSN-L)
- 1460-2369
- OpenAlex
- W3011721387
- Cited by
- 96
- References
- 280
- Citations by year
- 2026: 15 · 2025: 15 · 2024: 8 · 2023: 15 · 2022: 20 · 2021: 13 · 2020: 10
- FWCI
- 1.51
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
- Locations
- Human Reproduction Update (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation of China (81771553, 81530040)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Plant and fungal interactions
- Health Sciences › Medicine › Obstetrics and Gynecology › Endometrial and Cervical Cancer Treatments
- Keywords
- endometriosis, cancer-associated mutations, somatic mutations, deep infiltrating endometriosis, endometriotic lesions, endometriosis pathogenesis, endometriosis pathophysiology, ectopic endometrium, eutopic endometrium, replicative senescence, oxidative stress, fibrosis, epigenetics, oestrogen receptor, ARID1A mutation, KRAS mutation, carcinogenesis
- MeSH terms
- Bone Marrow Cells, Endometriosis, Endometrium, Epithelial Cells, Female, Humans, Mutation, Neoplasms, Ovarian Diseases, Epithelial-Mesenchymal Transition, Tumor Microenvironment
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