The mutational landscape of normal human endometrial epithelium
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Abstract
All normal somatic cells are thought to acquire mutations, but understanding of the rates, patterns, causes and consequences of somatic mutations in normal cells is limited. The uterine endometrium adopts multiple physiological states over a lifetime and is lined by a gland-forming epithelium1,2. Here, using whole-genome sequencing, we show that normal human endometrial glands are clonal cell populations with total mutation burdens that increase at about 29 base substitutions per year and that are many-fold lower than those of endometrial cancers. Normal endometrial glands frequently carry ‘driver’ mutations in cancer genes, the burden of which increases with age and decreases with parity. Cell clones with drivers often originate during the first decades of life and subsequently progressively colonize the epithelial lining of the endometrium. Our results show that mutational landscapes differ markedly between normal tissues—perhaps shaped by differences in their structure and physiology—and indicate that the procession of neoplastic change that leads to endometrial cancer is initiated early in life. Whole-genome sequencing of normal human endometrial glands shows that most are clonal cell populations and frequently carry cancer driver mutations that occur early in life, and that parity has a protective effect.
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The toolkit has a significant advantage to generate isogenic models of novel mutations in early tumorigenesis.
“Taken together, these results demonstrate the significant advantage the toolkit we have developed in this study has to generate isogenic models of novel mutations in early tumorigenesis48,50–52.”
From One-step generation of tumor models by base editor multiplexing in adult stem cell-derived organoids (2023) · cites this paper as [51]
This hypothesis had never before been tested in an isogenic model.
“While this hypothesis has been previously proposed48,50–52, it had never before been tested in an isogenic model.”
From One-step generation of tumor models by base editor multiplexing in adult stem cell-derived organoids (2023) · cites this paper as [51]
The cited paper’s Clonality of endometrial glands section discusses a proposed genetic-drift process, but does not say whether that hypothesis had previously been tested in an isogenic model. Searches for “isogenic model” and “hypothesis proposed tested model” found no passage addressing that claim. In the citing sentence, the references are attached to “previously proposed,” not explicitly to the assertion about prior testing. (LLM, conf=0.75)
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“found two or more driver mutations in single endometrial glands in 22% of specimens[35], suggesting an elevated probability, albeit still nonconclusive, that driver mutations may co-exist in the same non-cancerous cells.”
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The origin of human mutation in light of genomic data
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Accurate and sensitive mutational signature analysis with MuSiCal
Jin, H., Gulhan, D., Geiger, B., Ben-Isvy, D., Geng, D., Ljungström, V., & Park, P. J. (2024) · Nature Genetics · doi:10.1038/s41588-024-01659-0 · Cited by 54 · see citing works
“Some studies have noticed this problem and have manually combined SBS40 with other flat signatures 46,47 .”
BackgroundDevelopmental and temporal characteristics of clonal sperm mosaicism
Yang, X., Breuss, M. W., Xu, X., Antaki, D., James, K. N., Stanley, V., Ball, L., George, R. D., Wirth, S. A., Cao, B., et al. (2021) · Cell · doi:10.1016/j.cell.2021.07.024 · Cited by 53 · see citing works
Spatiotemporal dynamics of clonal selection and diversification in normal endometrial epithelium
Yamaguchi, M., Nakaoka, H., Suda, K., Yoshihara, K., Ishiguro, T., Yachida, N., Saito, K., Ueda, H., Sugino, K., Mori, Y., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-28568-2 · Cited by 54 · see citing works
The DNA methylome of cervical cells can predict the presence of ovarian cancer
Barrett, J. J. E., Jones, A., Evans, I., Reisel, D., Herzog, C. M. S., Chindera, K., Kristiansen, M., Leavy, O. C., Manchanda, R., Bjørge, L., et al. (2022) · Nature Communications · doi:10.1038/s41467-021-26615-y · Cited by 53 · see citing works
Doyle, S. R., Sankaranarayanan, G., Allan, F., Berger, D., Castro, P. D. J., Collins, J. B., Crellen, T., Correa, M. A. D., Ellis, P., Jaleta, T. G., et al. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.00826 · Cited by 54 · see citing works
“CGP (CGP): Extraction using the CGP protocol (Moore et al., 2018) involved adding 30 μl of lysis buffer (1.”
MethodSelf-citationSaini, N., Giacobone, C. K., Klimczak, L. J., Papas, B. N., Burkholder, A., Li, J., Fargo, D. C., Bai, R., Gerrish, K., Innes, C. L., et al. (2021) · PLoS Genetics · doi:10.1371/journal.pgen.1009302 · Cited by 53 · see citing works
Williams, N., Lee, J., Moore, L., Baxter, E. J., Hewinson, J., Dawson, K. J., Menzies, A. H., Godfrey, A. L., Green, A. R., Campbell, P. J., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.11.09.374710 · Cited by 53 · see citing works
Self-citationThe mutational landscape of human somatic and germline cells
Moore, L., Cagan, A., Coorens, T. H. H., Neville, M. D. C., Sanghvi, R., Sanders, M. A., Oliver, T. R. W., Leongamornlert, D. A., Ellis, P., Noorani, A., et al. (2022) · Yearbook of pediatric endocrinology · doi:10.1101/2020.11.25.398172 · Cited by 55 · see citing works
Self-citation
- Authors
- Moore, L., Leongamornlert, D., Coorens, T. H. H., Sanders, M. A., Ellis, P., Dentro, S. C., Dawson, K. J., Butler, T., Rahbari, R., Mitchell, T. J., Maura, F., Nangalia, J., Tarpey, P. S., Brunner, S. F., Lee-Six, H., Hooks, Y., Moody, S., Mahbubani, K. T., Jimenez-Linan, M., Brosens, J. J., Iacobuzio-Donahue, C. A., Martincorena, I., Saeb-Parsy, K., Campbell, P. J., & Stratton, M. R.
- Affiliations
- Cambridge University Hospitals NHS Foundation Trust (GB)
- Wellcome Sanger Institute (GB)
- Erasmus MC (NL)
- European Bioinformatics Institute (GB)
- Memorial Sloan Kettering Cancer Center (US)
- University of Cambridge (GB)
- University of Warwick (GB)
- Corresponding author
- Stratton, Michael R.
- ORCID
- Moore, Luiza
- Leongamornlert, Daniel
- Coorens, Tim H. H.
- Sanders, Mathijs A.
- Dentro, Stefan C.
- Butler, Tim
- Rahbari, Raheleh
- Mitchell, Thomas J.
- Maura, Francesco
- Nangalia, Jyoti
- Tarpey, Patrick S.
- Lee-Six, Henry
- Moody, Sarah
- Mahbubani, Krishnaa T.
- Brosens, Jan J.
- Iacobuzio-Donahue, Christine A.
- Saeb-Parsy, Kourosh
- Campbell, Peter J.
- Stratton, Michael R.
- Venue
- Nature
- Published
- 2020-04-22
- Volume
- 580
- Issue
- 7805
- Pages
- 640-646
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W3020114628
- Semantic Scholar
- 64bced314a97056c50b400d859c78993c4ce2fd8
- Cited by
- 499
- References
- 64
- Citations by year
- 2026: 42 · 2025: 54 · 2024: 69 · 2023: 87 · 2022: 91 · 2021: 89 · 2020: 51 · 2019: 16
- FWCI
- 27.19
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Licence
- Locations
- Nature (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nd)
- PubMed (publishedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (publishedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Science Foundation
- European Hematology Association (TRTH182)
- Wellcome Trust (103858/Z/14/Z)
- Cancer Research UK (C20/A20917, 23917, 27176, 21777, 27114)
- Pathological Society of Great Britain and Ireland
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (171753, 180790)
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek (019.153LW.038)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
- Health Sciences › Medicine › Epidemiology › Cervical Cancer and HPV Research
- Health Sciences › Medicine › Pathology and Forensic Medicine › Genetic factors in colorectal cancer
- Keywords
- somatic mutations, endometrial epithelium, endometrial cancer, clonal cell populations, mutational burden, driver mutations, cancer genes, parity, aging, mutational landscape, tumor progression, endometrial glands
- MeSH terms
- Adult, Aged, Aged, 80 and over, Aging, Clone Cells, DNA Mutational Analysis, Endometrium, Epithelial Cells, Epithelium, Female, Health, Humans, Middle Aged, Mutation, Parity, Time Factors, Endometrial Neoplasms, Age of Onset, Young Adult, Carcinogenesis
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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