General Gynecology · Gynecologic Oncology

Cancer-Associated Mutations in Endometriosis without Cancer

Anglesio MS, Papadopoulos N, Ayhan A, Nazeran TM, Noë M, Horlings HM, Lum A, Jones S, Senz J, Seckin T, Ho J, Wu RC, Lac V, Ogawa H, Tessier-Cloutier B, Alhassan R, Wang A, Wang Y, Cohen JD, Wong F, Hasanovic A, Orr N, Zhang M, Popoli M, McMahon W, Wood LD, Mattox A, Allaire C, Segars J, Williams C, Tomasetti C, Boyd N, Kinzler KW, Gilks CB, Diaz L, Wang TL, Vogelstein B, Yong PJ, Huntsman DG, Shih IM

Published May 11, 2017 The New England Journal of Medicine, 376(19), 1835-1848
DOI 10.1056/NEJMoa1614814 PMID 28489996 PMC PMC5555376
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RRM Academy Synopsis

Deep endometriosis lesions can carry cancer-driver gene mutations

A 2017 laboratory sequencing study of deep endometriosis lesions from 39 women found that 10 of 39 lesions carried cancer driver gene mutations. No lesion contained cancer. Where the cell types could be separated, the mutations sat in gland-lining cells and were absent from stromal cells.

Key Findings

  • Whole-exome sequencing of 24 patients found somatic mutations in 19 (79%).
  • Five patients had mutations in genes that drive cancer: ARID1A, PIK3CA, KRAS, and PPP2R1A. The authors put the odds of that rate arising without selection at P=0.001 (binomial test).
  • Targeted sequencing found KRAS mutations in 2 of 3 patients, and droplet digital PCR in 3 of 12. Where cells were separated, mutations were in the epithelium, absent from the stroma.
  • One patient carried two different KRAS mutations. Another carried the identical KRAS mutation in three distinct lesions.
  • Across all 39 lesions, 10 (26%) carried driver mutations. Every mutation tested appeared to sit in the epithelial cells.

Interpretation

The study analyzed archived surgical tissue from 39 women with deep infiltrating endometriosis (mean age 37) at three centers. None had cancer or dysplasia. The study sampled tissue once, with no follow-up, so it cannot show who goes on to develop cancer. The authors cite a malignant transformation rate near 1%. They suggest that driver mutations alone do not suffice to drive transformation and do not indicate likely progression to cancer. Only a minority of patients had detectable driver mutations. Superficial and ovarian lesions were outside the study.

RRM Context

Restorative reproductive medicine asks what drives a woman's disease. The authors say current classification of endometriosis does not predict well how lesions behave. They note that hormonal therapy causes unacceptable side effects in many patients, and some do not respond, especially with deep disease. All samples came from removed tissue. Excision makes that tissue available for study.

Abstract

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.

Topics

By this author

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General Gynecology › Gynecologic Oncology › Ovarian Cancer · Endometriosis › Pathophysiology › Genetics
Michael S Anglesio, Nickolas Papadopoulos, Ayse Ayhan, Michaël Noë, Hugo M Horlings, Amy Lum, Siân Jones, Janine Senz, Tamer Seckin, Ren-Chin Wu, Vivian Lac, Hiroshi Ogawa, Yuanyuan Wang, Joshua D Cohen, Minming Zhang, Maria Popoli, Laura D Wood, Catherine Allaire, Cristian Tomasetti, Kenneth W Kinzler, Tian-Li Wang, Bert Vogelstein, Paul J Yong, David G Huntsman, Ie-Ming Shih, Rami Alhassan, Niki Boyd, Luis Diaz, C Blake Gilks, Adnan Hasanovic, Julie Ho, Wyatt McMahon, Tayyebeh M Nazeran, Amy Wang, Christina Williams, Fontayne Wong
Mike Anglesio, M Anglesio, N Papadopoulos, A Ayhan, M Noë, H Horlings, A Lum, S Jones, J Senz, T Seckin, R Wu, V Lac, H Ogawa, Y Wang, Josh Cohen, J Cohen, M Zhang, M Popoli, L Wood, Cathy Allaire, Kate Allaire, C Allaire, C Tomasetti, Ken Kinzler, K Kinzler, T Wang, B Vogelstein, P Yong, Dave Huntsman, D Huntsman, I Shih, R Alhassan, N Boyd, L Diaz, A Hasanovic, J Ho, W McMahon, T Nazeran, A Wang, C Williams, F Wong
PMID 28489996 28489996 DOI 10.1056/NEJMoa1614814 10.1056/NEJMoa1614814 Anglesio et al. 2017, Anglesio 2017

Cite this article

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., Lac, V., Ogawa, H., Tessier-Cloutier, B., Alhassan, R., Wang, A., Wang, Y., Cohen, J. D., . . . Shih, I. (2017). Cancer-Associated Mutations in Endometriosis without Cancer. The New England journal of medicine, 376(19), 1835-1848. https://doi.org/10.1056/NEJMoa1614814