Aromatase: a key molecule in the pathophysiology of endometriosis and a therapeutic target
Open accessAbstract
Objective To provide a clinically useful model illustrating the molecular aberrations affecting estrogen biosynthesis and metabolism in endometriosis and to discuss the therapeutic role of aromatase inhibitors.Design Literature review.Result(s) Several molecular aberrations were found in endometriotic lesions (in contrast to eutopic endometrium) that favor increased local concentrations of E2. Endometriotic stromal cells aberrantly express aromatase, which converts C19, steroids to estrogens. Aromatase activity in these cells is stimulated by prostaglandin (PG)E2. Estrogen stimulates cyclooxygenase-2, giving rise to increased PGE2 formation. Thus, this positive feedback loop produces increasing quantities of E2 and PGE2 in endometriosis. The lack of aromatase expression in eutopic endometrium is maintained by binding of an inhibitory transcription factor, COUP-TF, to the aromatase promoter. In endometriosis, however, an aberrantly expressed factor, SF-1, displaces COUP-TF to bind to this same promoter and activates aromatase expression and thus local estrogen biosynthesis. Additionally, endometriotic glandular cells are deficient in 17beta-hydroxysteroid dehydrogenase type 2, which converts E2 to estrone in the eutopic endometrium in response to P. Deficiency of this enzyme in endometriosis impairs the inactivation of E2 and may be a consequence of insensitivity to P.Conclusion(s) Molecular aberrations that increase local E2 concentrations may be important in the etiology of endometriosis. These molecules may be targeted to develop novel therapeutic strategies. The clinical relevance of aromatase expression in endometriosis was shown recently by the successful treatment of an unusually aggressive case of postmenopausal endometriosis with use of an aromatase inhibitor.
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Binding of SF-1 and CREB to promoters of steroidogenic genes is responsible for inducing expression and activity of these enzymes, thus promoting estrogen biosynthesis in endometriotic stromal cells.
“The binding of SF-1 and CREB to the promoters of steroidogenic genes is responsible for inducing the expression levels and activity of these enzymes, thus promoting the estrogen biosynthesis in endometriotic stromal cells10,17,18.”
From Platelets induce increased estrogen production through NF-κB and TGF-β1 signaling pathways in endometriotic stromal cells (2020) · cites this paper as [18]
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Bulun, S. E., Cheng, Y.-H., Yin, P., Imir, G., Utsunomiya, H., Attar, E., Innes, J., & Julie Kim, J. (2006) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2005.11.041 · Cited by 397 · see citing works
Self-citationOlive, D. L., & Pritts, E. A. (2001) · New England Journal of Medicine · doi:10.1056/nejm200107263450407 · Cited by 340 · see citing works
Role of Estrogen Receptor-β in Endometriosis
Bulun, S., Monsavais, D., Pavone, M., Dyson, M., Xue, Q., Attar, E., Tokunaga, H., & Su, E. (2012) · Seminars in Reproductive Medicine · doi:10.1055/s-0031-1299596 · Cited by 307 · see citing works
“11,22,23 There are substantial molecular differences with regard to progesterone response between normal endometrium and eutopic and ectopic tissues from women with endometriosis.”
BackgroundSelf-citationAromatase and other steroidogenic genes in endometriosis: translational aspects.
Attar, E., & Bulun, S. E. (2006) · Human Reproduction Update · doi:10.1093/humupd/dmi034 · Cited by 255 · see citing works
Self-citationEstrogen Receptor-β, Estrogen Receptor-α, and Progesterone Resistance in Endometriosis
Bulun, S., Cheng, Y.-H., Pavone, M., Xue, Q., Attar, E., Trukhacheva, E., Tokunaga, H., Utsunomiya, H., Yin, P., Luo, X., et al. (2010) · Seminars in Reproductive Medicine · doi:10.1055/s-0029-1242991 · Cited by 243 · see citing works
Self-citationSoysal, S. (2004) · Human Reproduction · doi:10.1093/humrep/deh035 · Cited by 227 · see citing works
Aromatase inhibitors: the next generation of therapeutics for endometriosis?
Attar, E., & Bulun, S. E. (2006) · Fertility and Sterility · doi:10.1016/j.fertnstert.2005.09.064 · Cited by 184 · see citing works
Self-citationExpression of estrogen receptor alpha and beta in peritoneal and ovarian endometriosis
Matsuzaki, S., Murakami, T., Uehara, S., Canis, M., Sasano, H., & Okamura, K. (2001) · Fertility and Sterility · doi:10.1016/s0015-0282(01)01783-6 · Cited by 133 · see citing works
Eutopic endometrium in women with endometriosis: ground zero for the study of implantation defects
Lessey, B., Lebovic, D., & Taylor, R. (2013) · Seminars in Reproductive Medicine · doi:10.1055/s-0032-1333476 · Cited by 113 · see citing works
Endometriosis, recurrent miscarriage and implantation failure: is there an immunological link?
Tomassetti, C., Meuleman, C., Pexsters, A., Mihalyi, A., Kyama, C., Simsa, P., & D'Hooghe, T. (2006) · Reproductive BioMedicine Online · doi:10.1016/s1472-6483(10)62016-0 · Cited by 106 · see citing works
Cyr61, a deregulated gene in endometriosis
Absenger, Y. (2004) · Molecular Human Reproduction · doi:10.1093/molehr/gah053 · Cited by 95 · see citing works
Lafay Pillet, M.-C., Schneider, A., Borghese, B., Santulli, P., Souza, C., Streuli, I., de Ziegler, D., & Chapron, C. (2012) · Human Reproduction · doi:10.1093/humrep/der346 · Cited by 91 · see citing works
Genetic or enzymatic disruption of aromatase inhibits the growth of ectopic uterine tissue
Fang, Z., Yang, S., Gurates, B., Tamura, M., Simpson, E., Evans, D., & Bulun, S. E. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.87.7.8683 · Cited by 91 · see citing works
Self-citationEndometrium from women with endometriosis shows increased proliferation activity
Park, J. S., Lee, J. H., Kim, M., Chang, H. J., Hwang, K. J., & Chang, K. H. (2009) · Fertility and Sterility · doi:10.1016/j.fertnstert.2009.04.025 · Cited by 88 · see citing works
Gashaw, I., Hastings, J. M., Jackson, K. S., Winterhager, E., & Fazleabas, A. T. (2006) · Biology of Reproduction · doi:10.1095/biolreprod.105.049320 · Cited by 81 · see citing works
Steroidogenic factor-1 and endometriosis
Bulun, S. E., Utsunomiya, H., Lin, Z., Yin, P., Cheng, Y.-H., Pavone, M. E., Tokunaga, H., Trukhacheva, E., Attar, E., Gurates, B., et al. (2009) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2008.12.012 · Cited by 80 · see citing works
Self-citationNasu, K., Nishida, M., Kawano, Y., Tsuno, A., Abe, W., Yuge, A., Takai, N., & Narahara, H. (2011) · Reproductive Sciences · doi:10.1177/1933719110392059 · Cited by 73 · see citing works
Hudelist, G., Czerwenka, K., Keckstein, J., Haas, C., Fink-Retter, A., Gschwantler-Kaulich, D., Kubista, E., & Singer, C. F. (2007) · Reproductive Sciences · doi:10.1177/1933719107309120 · Cited by 70 · see citing works
Two unsuccessful clinical trials on endometriosis and a few lessons learned
Guo, S.-W., & Olive, D. L. (2007) · Gynecologic and Obstetric Investigation · doi:10.1159/000098413 · Cited by 49 · see citing works
On-label and off-label drug use in the treatment of endometriosis
Quaas, A. M., Weedin, E. A., & Hansen, K. R. (2015) · Fertility and Sterility · doi:10.1016/j.fertnstert.2015.01.006 · Cited by 45 · see citing works
Qi, Q., Liu, X., Zhang, Q., & Guo, S.-W. (2020) · Scientific Reports · doi:10.1038/s41598-020-57997-6 · Cited by 44 · see citing works
A Low-Testosterone State Associated with Endometrioma Leads to the Apoptosis of Granulosa Cells
Ono, Y. J., Tanabe, A., Nakamura, Y., Yamamoto, H., Hayashi, A., Tanaka, T., Sasaki, H., Hayashi, M., Terai, Y., & Ohmichi, M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0115618 · Cited by 32 · see citing works
Androgens, Endometriosis and Pain
Evans, S. F., Hull, M. L., Hutchinson, M. R., & Rolan, P. E. (2021) · Frontiers in Reproductive Health · doi:10.3389/frph.2021.792920 · Cited by 14 · see citing works
De Abreu, L. G., Silveira, V. S., Scrideli, C. A., Ramos, E. S., Dos Reis, R. M., Ferriani, R. A., & De Sá, M. F. S. (2011) · Journal of Endometriosis · doi:10.5301/je.2012.9070 · Cited by 11 · see citing works
- Authors
- Zeitoun, K. M., & Bulun, S. E.
- Affiliations
- The University of Texas Southwestern Medical Center (US)
- Corresponding author
- Bulun, Serdar E
- ORCID
- Bulun, Serdar E
- Venue
- Fertility and Sterility
- Publisher
- Elsevier BV
- Published
- 1999-12
- Volume
- 72
- Issue
- 6
- Pages
- 961-969
- ISSN
- 0015-0282 (ISSN-L)
- OpenAlex
- W2170554336
- Cited by
- 256
- References
- 96
- Citations by year
- 2026: 6 · 2025: 3 · 2024: 6 · 2023: 9 · 2022: 8 · 2021: 11 · 2020: 9 · 2019: 8 · 2018: 5 · 2017: 10 · 2016: 1 · 2015: 10 · 2014: 11 · 2013: 7 · 2012: 9
- FWCI
- 1.96
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Fertility and Sterility (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Cancer Institute (CA-67167)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Estrogen and related hormone effects
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Ectopic Pregnancy Diagnosis and Management
- Keywords
- endometriosis, aromatase, estrogen synthesis, aromatase inhibitors, prostaglandin E2, cyclooxygenase-2, COUP-TF, SF-1, 17β-hydroxysteroid dehydrogenase type 2, estrone, endometriotic stromal cells, postmenopausal endometriosis, endometriosis pathophysiology
- MeSH terms
- Aromatase, Endometriosis, Endometrium, Enzyme Inhibitors, Epithelial Cells, Estrogens, Female, Humans, Gene Expression Regulation, Enzymologic, Stromal Cells, Aromatase Inhibitors
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