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Cancer-Associated Mutations in Endometriosis without Cancer
Open accessAbstract
BACKGROUND: Endometriosis, defined as the presence of ectopic endometrial stroma and epithelium, affects approximately 10% of reproductive-age women and can cause pelvic pain and infertility. Endometriotic lesions are considered to be benign inflammatory lesions but have cancerlike features such as local invasion and resistance to apoptosis. METHODS: We analyzed deeply infiltrating endometriotic lesions from 27 patients by means of exomewide sequencing (24 patients) or cancer-driver targeted sequencing (3 patients). Mutations were validated with the use of digital genomic methods in microdissected epithelium and stroma. Epithelial and stromal components of lesions from an additional 12 patients were analyzed by means of a droplet digital polymerase-chain-reaction (PCR) assay for recurrent activating KRAS mutations. RESULTS: Exome sequencing revealed somatic mutations in 19 of 24 patients (79%). Five patients harbored known cancer driver mutations in ARID1A, PIK3CA, KRAS, or PPP2R1A, which were validated by Safe-Sequencing System or immunohistochemical analysis. The likelihood of driver genes being affected at this rate in the absence of selection was estimated at P=0.001 (binomial test). Targeted sequencing and a droplet digital PCR assay identified KRAS mutations in 2 of 3 patients and 3 of 12 patients, respectively, with mutations in the epithelium but not the stroma. One patient harbored two different KRAS mutations, c.35G→T and c.35G→C, and another carried identical KRAS c.35G→A mutations in three distinct lesions. CONCLUSIONS: We found that lesions in deep infiltrating endometriosis, which are associated with virtually no risk of malignant transformation, harbor somatic cancer driver mutations. Ten of 39 deep infiltrating lesions (26%) carried driver mutations; all the tested somatic mutations appeared to be confined to the epithelial compartment of endometriotic lesions.
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In the citing paper
“While nucleotide variants or mutations were noted sporadically in the epithelial component of ovarian endometriomas or deep-infiltrating endometriosis, stromal cells consistently lack any somatic mutations (Anglesio et al., 2017).”
From Endometriosis and nuclear receptors (2019) · cites this paper as Anglesio et al., 2017
Experimental — accuracy not yet measuredIn the citing paper
“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 [104]
In the citing paper
“Cancer genomic mutations have also been reported for extraovarian endometriosis in recent years, and mutations in cancer-associated genes, such as PIK3CA, KRAS, and ARID1A, have been identified [106].”
From Malignancies Associated with Extraovarian Endometriosis: A Literature Review (2021) · cites this paper as [106]
In the citing paper
“Cancer genomic mutations have also been reported for extraovarian endometriosis in recent years, and mutations in cancer-associated genes, such as PIK3CA, KRAS, and ARID1A, have been identified [106].”
From Malignancies Associated with Extraovarian Endometriosis: A Literature Review (2021) · cites this paper as [106]
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Gristina, V., Russo, G., Russo, T. D. B., Busuito, G., Iannì, G., Pisapia, P., Scimone, C., Palumbo, L., Incorvaia, L., Badalamenti, G., et al. (2024) · Expert Review of Respiratory Medicine · doi:10.1080/17476348.2024.2423824 · Cited by 6
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Esposito, G., D’Angelo, G., Falco, L. D., Evangelista, E., Savarese, G., Fico, A., Cinque, F., Giampaolino, P., Sardo, A. D. S., Bifulco, G., et al. (2025) · Cancers · doi:10.3390/cancers17071078 · Cited by 5
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Metadata
- Authors
- Anglesio, M. S., Papadopoulos, N., Ayhan, A., Nazeran, T. M., Noë, M., Horlings, H. M., Lum, A., Jones, S., Senz, J., Seckin, T., Ho, J., Wu, R.-C., Lac, V., Ogawa, H., Tessier-Cloutier, B., Alhassan, R., Wang, A., Wang, Y., Cohen, J. D., Wong, F., Hasanovic, A., Orr, N., Zhang, M., Popoli, M., McMahon, W., Wood, L. D., Mattox, A., Allaire, C., Segars, J., Williams, C., Tomasetti, C., Boyd, N., Kinzler, K. W., Gilks, C. B., Diaz, L., Wang, T.-L., Vogelstein, B., Yong, P. J., Huntsman, D. G., & Shih, I.-M.
- Affiliations
- University of British Columbia (CA)
- Hiroshima University (JP)
- BC Cancer Agency (CA)
- Howard Hughes Medical Institute (US)
- ORCID
- Anglesio, Michael S.
- Papadopoulos, Nickolas
- Ayhan, Ayse
- Noë, Michaël
- Horlings, Hugo M.
- Lum, Amy
- Jones, Siân
- Senz, Janine
- Seckin, Tamer
- Wu, Ren-Chin
- Lac, Vivian
- Ogawa, Hiroshi
- Wang, Yuxuan
- Cohen, Joshua D.
- Orr, Natasha
- Zhang, Ming
- Popoli, Maria
- Wood, Laura D.
- Mattox, Austin
- Allaire, Catherine
- Segars, James
- Tomasetti, Cristian
- Boyd, Niki
- Kinzler, Kenneth W.
- Gilks, C. Blake
- Diaz, Luis
- Wang, Tian-Li
- Vogelstein, Bert
- Yong, Paul J.
- Shih, Ie-Ming
- Venue
- New England Journal of Medicine
- Publisher
- Massachusetts Medical Society
- Published
- 2017-05-11
- Volume
- 376
- Issue
- 19
- Pages
- 1835-1848
- ISSN
- 0028-4793 (ISSN-L)
- 1533-4406
- PMC
- PMC5555376
- OpenAlex
- W2612851374
- Cited by
- 628
- References
- 50
- Citations by year
- 2026: 57 · 2025: 62 · 2024: 51 · 2023: 75 · 2022: 72 · 2021: 75 · 2020: 80 · 2019: 68 · 2018: 69 · 2017: 19
- FWCI
- 74.93
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- New England Journal of Medicine (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Cancer Institute (R01CA215483, U01CA200469, R01CA057345, T32CA009243, P50CA062924, R37CA057345, P30CA006973)
- National Institute of General Medical Sciences (T32GM007309, T32GM007184)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
- Keywords
- endometriosis, deep infiltrating endometriosis, somatic mutations, cancer driver mutations, KRAS mutation, ARID1A, PIK3CA, PPP2R1A, malignant transformation risk, droplet digital PCR
- MeSH terms
- Adult, Cell Transformation, Neoplastic, DNA Mutational Analysis, DNA-Binding Proteins, Endometriosis, Endometrium, Female, Humans, Middle Aged, Mutation, Nuclear Proteins, Transcription Factors, Polymerase Chain Reaction, Proto-Oncogene Proteins p21(ras), Phosphatidylinositol 3-Kinases, Protein Phosphatase 2, Class I Phosphatidylinositol 3-Kinases, Exome
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