Estrogen metabolism and action in endometriosis

Rižner, Tea Lanišnik

doi:10.1016/j.mce.2009.03.022

Cited by 156Endometriosis Research and TreatmentEstrogen and related hormone effectsEndometrial and Cervical Cancer Treatments

Estrogen metabolism and action in endometriosis

Rižner, Tea Lanišnik·2009·Molecular and Cellular Endocrinology

DOI 10.1016/j.mce.2009.03.022

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Abstract

Endometriosis is a complex estrogen-dependent disease that is defined as the presence of endometrial glands and stroma outside the uterine cavity. The etiology of endometriosis is multifactorial and includes complex interactions of genetic, immunological, hormonal and environmental factors. Many theories have been proposed, but no single theory can explain all aspects of endometriosis, suggesting that endometriosis is a heterogeneous disease. This review presents the current theories on the pathogenesis of endometriosis, followed by an overview on estrogen metabolism in normal endometrium and diseased endometrium of endometriosis patients. The potential role of aberrant expression of individual estrogen-metabolizing enzymes is discussed, and a model mechanism for increased formation of estradiol is presented separately for different types of endometriosis. The disturbed expression of estrogen receptors in endometriosis is detailed, and the estrogen biosynthetic enzymes and receptors are discussed as novel therapeutic targets for the treatment of endometriosis.

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Endometriosis: The way forward
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Analysis of Estrogen Receptor ?? and ?? in Endometrial Carcinomas: Correlation with ER?? and Clinicopathologic Findings in 45 Cases
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Purification, Reconstitution, and Steady-state Kinetics of the Trans-membrane 17β-Hydroxysteroid Dehydrogenase 2
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Expression of aromatase (P450 aromatase/CYP19) in peritoneal and ovarian endometriotic tissues and deep endometriotic (adenomyotic) nodules of the rectovaginal septum
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Cystic endometriosis of the epididymis
Giannarini, G., Scott, C. A., Moro, U., Grossetti, B., Pomara, G., & Selli, C. (2006) · Urology · doi:10.1016/j.urology.2006.01.017 · Cited by 37 · see citing works
Human oestrogenic 17β-hydroxysteroid dehydrogenase specificity: enzyme regulation through an NADPH-dependent substrate inhibition towards the highly specific oestrone reduction
Gangloff, A., GARNEAU, A., Huang, Y., et al. (2001) · Biochemical Journal · doi:10.1042/bj3560269 · Cited by 37 · see citing works
Metabolism of estrone sulfate in endometriotic tissue and in uterine endometrium in proliferative and secretory cycle phase
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Complexity in Endometrial Estradiol Signaling
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Etiology of endometriosis
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Flagged first, then by citations

2 of the 120 references couldn’t be matched to a known paper.

Sorted by citations

The Main Theories on the Pathogenesis of Endometriosis
Lamceva, J., Uljanovs, R., & Strumfa, I. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24054254 · Cited by 324 · see citing works
“The main function of regulatory T cells is modulation of the immune system, maintaining tolerance to self-antigens and preventing autoimmune diseases [29].”
BackgroundInfluential
Endometriosis-Associated Macrophages: Origin, Phenotype, and Function
Hogg, C., Horne, A. W., & Greaves, E. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.00007 · Cited by 241 · see citing works
“Estrogen signalling modulates a large number of down-stream disease processes within endometriosis lesions, which are reviewed in(30, 31) and (32).”
Background
Role of aldo-keto reductase family 1 (AKR1) enzymes in human steroid metabolism
Rižner, T. L., & Penning, T. M. (2014) · Steroids · doi:10.1016/j.steroids.2013.10.012 · Cited by 217 · see citing works
“Imbalance in the biosynthesis and inactivation of steroids can lead to development of disease, including hormonally dependent cancer, of the breast, prostate, endometrium and ovary [1], and to diseases such as benign prostatic hyperplasia, endometriosis, cholestasis, neonatal liver failure, neurological disorders [2–6…”
BackgroundSelf-citation
Vasculogenesis: A new piece of the endometriosis puzzle
Laschke, M. W., Giebels, C., & Menger, M. D. (2011) · Human Reproduction Update · doi:10.1093/humupd/dmr023 · Cited by 136 · see citing works
“Considering the fact that endometriosis is an E2-dependent disease (Rizner, 2009), these findings imply that hormonally regulated EPC mobilization may also play a crucial role in endometriosis (Fig.”
Background
Uterine disorders and pregnancy complications: insights from mouse models
Lim, H. J., & Wang, H. (2010) · Journal of Clinical Investigation · doi:10.1172/jci41210 · Cited by 124 · see citing works
“Altered expression of enzymes involved in estrogen metabolism further enhances the accumulation of estradiol in patients with endometriosis (83, 96).”
Background
IL15 promotes growth and invasion of endometrial stromal cells and inhibits killing activity of NK cells in endometriosis
Yu, J., Sun, H., Zhang, Z., Shi, R., Liu, L.-B., Shang, W.-Q., Weı, C., Chang, K., Shao, J., Wang, M., et al. (2016) · Reproduction · doi:10.1530/rep-16-0089 · Cited by 114 · see citing works
“Endometriosis (EMS) is one of the common estrogendependent inflammatory diseases, which affects 10–15% of women of reproductive age (Rizner 2009).”
Background
Endometriosis: Perspective, lights, and shadows of etiology
Asghari, S., Valizadeh, A., Maleki, L. A., Nouri, M., & Yousefi, M. (2018) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2018.06.109 · Cited by 110 · see citing works
Estrogen biosynthesis and signaling in endometriosis
Huhtinen, K., Ståhle, M., Perheentupa, A., & Poutanen, M. (2012) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2011.08.022 · Cited by 107 · see citing works
The important roles of steroid sulfatase and sulfotransferases in gynecological diseases
Rižner, T. L. (2016) · Frontiers in Pharmacology · doi:10.3389/fphar.2016.00030 · Cited by 98 · see citing works
“No significant differences in STS expression (Smuc and Rizner, 2009) and increased mRNA levels of STS (Lépine et al., 2010) have been reported in endometrial cancer vs. adjacent control tissue.”
BackgroundSelf-citation
New insights into the pathophysiology of endometriosis: from chronic inflammation to danger signal
Kajihara, H., Yamada, Y., Kanayama, S., Furukawa, N., 野口, 武., Haruta, S., Yoshida, S., Sado, T., Oi, H., & Kobayashi, H. (2010) · Gynecological Endocrinology · doi:10.3109/09513590.2010.507292 · Cited by 96 · see citing works
“Although endometriosis is an estrogen-dependent disease, hormone derangement has been proposed as the cause of endometriosis [4].”
Background
Hypothetical roadmap towards endometriosis: prenatal endocrine-disrupting chemical pollutant exposure, anogenital distance, gut-genital microbiota and subclinical infections
García–Peñarrubia, P., Ruiz‐Alcaraz, A. J., Martinez‐Esparza, M., Marín‐Sánchez, P., & Machado‐Linde, F. (2019) · Human Reproduction Update · doi:10.1093/humupd/dmz044 · Cited by 89 · see citing works
Endometriomas and deep infiltrating endometriosis in adulthood are strongly associated with anogenital distance, a biomarker for prenatal hormonal environment
Mendiola, J., Sánchez-Ferrer, M. L., Jiménez-Velázquez, R., Cánovas-López, L., Hernández-Peñalver, A. I., Corbalán-Biyang, S., Carmona-Barnosi, A., Prieto-Sánchez, M. T., Nieto, A., & Torres-Cantero, A. M. (2016) · Human Reproduction · doi:10.1093/humrep/dew163 · Cited by 80 · see citing works
“Women with DEI and AGDAF below the median were 41.6 times (95% CI 3.9–438; P-value ¼ 0.002) more likely to have endometriosis than those above the median.”
BackgroundInfluential
Dienogest enhances autophagy induction in endometriotic cells by impairing activation of AKT, ERK1/2, and mTOR
Choi, J., Jo, M., Lee, E., Lee, D., & Choi, D. (2015) · Fertility and Sterility · doi:10.1016/j.fertnstert.2015.05.020 · Cited by 85 · see citing works
Androgens, oestrogens and endometrium: a fine balance between perfection and pathology
Gibson, D. A., Simitsidellis, I., Collins, F., & Saunders, P. T. K. (2020) · Journal of Endocrinology · doi:10.1530/joe-20-0106 · Cited by 76 · see citing works
17 β-Estradiol promotes vascular endothelial growth factor expression via the Wnt/β-catenin pathway during the pathogenesis of endometriosis
Zhang, L., Xiong, W., Xiong, Y., Liu, H., & Liu, Y. (2016) · Molecular Human Reproduction · doi:10.1093/molehr/gaw025 · Cited by 69 · see citing works
Disturbed expression of phase I and phase II estrogen-metabolizing enzymes in endometrial cancer: lower levels of CYP1B1 and increased expression of S-COMT
Hevir, N., Šinkovec, J., & Rižner, T. L. (2011) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2010.09.011 · Cited by 69 · see citing works
Self-citation
Autophagy in endometriosis.
Yang, H., Mei, J., Chang, K., Zhou, W., Huang, L., & Li, M. (2017) · Europe PMC (PubMed Central) · Cited by 68 · see citing works
Effects of dehydroepiandrosterone on proliferation, migration, and death of breast cancer cells
López‐Marure, R., Contreras, P. G., & Dillon, J. S. (2011) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2011.03.040 · Cited by 66 · see citing works
Expression of estrogen and progesterone receptors and estrogen metabolizing enzymes in different breast cancer cell lines
Hevir, N., Trošt, N., Debeljak, N., & Rižner, T. L. (2010) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2010.12.013 · Cited by 64 · see citing works
Self-citation
Nuclear magnetic resonance metabolomic profiling of urine provides a noninvasive alternative to the identification of biomarkers associated with endometriosis
Vicente-Muñoz, S., Morcillo, I., Puchades‐Carrasco, L., Payá, V., Pellicer, A., & Pineda‐Lucena, A. (2015) · Fertility and Sterility · doi:10.1016/j.fertnstert.2015.07.1149 · Cited by 63 · see citing works
Endometrial Intracrinology: Oestrogens, Androgens and Endometrial Disorders
Gibson, D. A., Simitsidellis, I., Collins, F., & Saunders, P. T. K. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19103276 · Cited by 70 · see citing works
“There has also been a rapid increase in the number of studies considering the role of locally produced (intracrine) steroids in the aetiology of pathologies including cancers of the breast [8,9] and endometrium [10–12], as well as in regulation of fertility [13] and the aetiology of the oestrogen-dependent disorder en…”
Background
EMAS position statement: Managing the menopause in women with a past history of endometriosis
Moen, M. H., REES, M. C. P., Brincat, M., Erel, C. T., Gambacciani, M., Lambrinoudaki, I. V., Schenck-Gustafsson, K. G., Trémollières, F., Vujović, S., & Rozenberg, S. (2010) · Maturitas · doi:10.1016/j.maturitas.2010.04.018 · Cited by 62 · see citing works
Estrogen is an important mediator of mast cell activation in ovarian endometriomas
Zhu, T., Ding, S., Li, T., Zhu, L., Huang, X., & Zhang, X. (2017) · Reproduction · doi:10.1530/rep-17-0457 · Cited by 59 · see citing works
“2012), E2 concentrations in endometriotic lesions are known to be elevated (Rizner 2009).”
BackgroundInfluential
Curcumin inhibits endometriosis endometrial cells by reducing estradiol production.
Zhang, Y., Cao, H., Yu, Z. Y., Peng, H.-Y., & Chang-jun, Z. (2013) · Europe PMC (PubMed Central) · Cited by 57 · see citing works
Metabolomics Reveals Altered Lipid Metabolism in a Mouse Model of Endometriosis
Dutta, M., Anitha, M., Smith, P. B. W., Chiaro, C. R., Maan, M., Chaudhury, K., & Patterson, A. D. (2016) · Journal of Proteome Research · doi:10.1021/acs.jproteome.6b00197 · Cited by 56 · see citing works
Aldo-keto reductase 1C3—Assessment as a new target for the treatment of endometriosis
Rižner, T. L., & Penning, T. M. (2019) · Pharmacological Research · doi:10.1016/j.phrs.2019.104446 · Cited by 51 · see citing works
Self-citation
Aldo–keto reductases AKR1C1, AKR1C2 and AKR1C3 may enhance progesterone metabolism in ovarian endometriosis
Hevir, N., Vouk, K., Šinkovec, J., Ribič-Pucelj, M., & Lanišnik Rižner, T. (2011) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2011.01.003 · Cited by 48 · see citing works
“In contrast to estrogens, which enhance proliferation of the endometrium, progesterone counteracts the estrogen effects and instead promotes differentiation of endometrial cells [6,7].”
Background
NME1 suppression promotes growth, adhesion and implantation of endometrial stromal cells via Akt and MAPK/Erk1/2 signal pathways in the endometriotic milieu
Li, M., Shao, J., Meng, Y., Mei, J., Wang, Y., Li, H., Zhang, L., Chang, K., Wang, X.-Q., Zhu, X., et al. (2013) · Human Reproduction · doi:10.1093/humrep/det248 · Cited by 49 · see citing works
“…suppressor gene that plays an important role in suppressing the invasion and metastasis of tumor cells. study design, size, duration: An in vitro investigation of the effect of NME1 on the proliferation, adhesion and invasion of eutopic ESCs from patients with…”
Background
Inhibition of type 1 17β-hydroxysteroid dehydrogenase impairs the synthesis of 17β-estradiol in endometriosis lesions
Delvoux, B., D'Hooghe, T., Kyama, C., Koskimies, P., Hermans, R. J. J., Dunselman, G. A., & Romano, A. (2014) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2013-2851 · Cited by 59 · see citing works
“The sulfatase pathway controls the activation of estrone-sulfate to estrone [catalyzed by the steroid sulfatase (STS)] and the opposite reaction [catalyzed by the sulfotransferase (11, 31).”
Background
Emerging hallmarks of endometriosis metabolism: A promising target for the treatment of endometriosis
Lu, J., Ling, X., Liu, L., Jiang, A., Ren, C., Lü, C., & Yu, Z. (2022) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2022.119381 · Cited by 48 · see citing works
Endometriotic lesions exhibit distinct metabolic signature compared to paired eutopic endometrium at the single-cell level
Sarsenova, M., Lawarde, A., Pathare, A. D. S., Saare, M., Modhukur, V., Soplepmann, P., Terasmaa, A., Käämbre, T., Gemzell‐Danielsson, K., Lalitkumar, P. G., et al. (2024) · Communications Biology · doi:10.1038/s42003-024-06713-5 · Cited by 45 · see citing works
“Thisknowledgemay facilitate understanding of the metabolic plasticity of EcE in maintaining its homeostasis and growth in a context of unfavorable microenvironment.”
Disturbed balance between phase I and II metabolizing enzymes in ovarian endometriosis: A source of excessive hydroxy-estrogens and ROS?
Hevir, N., Ribič-Pucelj, M., & Rižner, T. L. (2012) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2012.12.019 · Cited by 45 · see citing works
“53 54 On the one hand, endometriosis can be described as a chronic pelvic inflammatory process 55 with increased reactive oxygen species (ROS) generation (Agarwal et al., 2005), while on the 56 other hand, it is known as an estrogen-dependent disorder, where estrogens, especially 57 estradiol (E2), enhance cell prolif…”
BackgroundInfluentialSelf-citation
Progestins as inhibitors of the human 20-ketosteroid reductases, AKR1C1 and AKR1C3
Beranič, N., Gobec, S., & Rižner, T. L. (2011) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2010.12.012 · Cited by 39 · see citing works
The involvement of osteopontin and matrix metalloproteinase- 9 in the migration of endometrial epithelial cells in patients with endometriosis
Yang, M., Jiang, C., Chen, H., Nian, Y., Zhimiao, B., & Ha, C. (2015) · Reproductive Biology and Endocrinology · doi:10.1186/s12958-015-0090-4 · Cited by 43 · see citing works
“Currently, endometriosis is regarded as an estrogendependent disorder, and the initiation and development of this disorder can be promoted by systemic or locally synthesized estrogen [15].”
Background
Endocrinology Meets Metabolomics: Achievements, Pitfalls, and Challenges
Tokarz, J., Haid, M., Cecil, A., Prehn, C. P., Artati, A., Möller, G., & Adamski, J. (2017) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2017.07.001 · Cited by 43 · see citing works
PDCD4 suppresses proliferation, migration, and invasion of endometrial cells by inhibiting autophagy and NF-κB/MMP2/MMP9 signal pathway†
Li, Y., Wang, X., Wang, X., Wan, L., Liu, Y., Shi, Y., Zhang, L., Fang, Z., & Wei, Z. (2018) · Biology of Reproduction · doi:10.1093/biolre/ioy052 · Cited by 42 · see citing works
CD82 gene suppression in endometrial stromal cells leads to increase of the cell invasiveness in the endometriotic milieu
Li, M., Hou, X.-F., Lv, S., Meng, Y., Wang, X.-Q., Tang, C.-L., & Li, D. (2011) · Journal of Molecular Endocrinology · doi:10.1530/jme-10-0165 · Cited by 41 · see citing works
“Since endometriosis is an estrogen-dependent disease (Rizner 2009), and the inflammatory milieu in the peritoneal cavity of women with endometriosis has been extensively characterized, altered metabolism of estradiol by TCDD or other dioxin-like halogenated aromatic hydrocarbons, and…”
Background
Patients with endometriosis and patients with poor ovarian reserve have abnormal follicle-stimulating hormone receptor signaling pathways
González-Fernández, R., Peña, Ó., Hernández, J., Martín-Vasallo, P., Palumbo, A., & Ávila, J. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2011.03.030 · Cited by 48 · see citing works
Potential role of estrogen in maintaining the imbalanced sympathetic and sensory innervation in endometriosis
Liang, Y., & Yao, S. (2016) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2016.01.012 · Cited by 41 · see citing works
Inhibition of steroid sulfatase decreases endometriosis in an in vivo murine model
Colette, S., Defrere, S., Lousse, J. C., Van Langendonckt, A., Gotteland, J. P., Loumaye, E., & Donnez, J. (2011) · Human Reproduction · doi:10.1093/humrep/der079 · Cited by 45 · see citing works
“Endometriosis is known to be an estrogen-dependent disorder (Rizner, 2009).”
Background
Investigation of anogenital distance as a diagnostic tool in endometriosis
Sánchez-Ferrer, M. L., Mendiola, J., Jiménez-Velázquez, R., Cánovas-López, L., Corbalán-Biyang, S., Hernández-Peñalver, A. I., Carmona-Barnosi, A., Maldonado-Cárceles, A. B., Prieto-Sánchez, M. T., Machado-Linde, F., et al. (2017) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2017.01.002 · Cited by 37 · see citing works
Dioxin-like rather than non-dioxin-like PCBs promote the development of endometriosis through stimulation of endocrine–inflammation interactions
Huang, Q., Chen, Y., Chen, Q., Zhang, H., Lin, Y., Zhu, M., & Dong, S. (2016) · Archives of Toxicology · doi:10.1007/s00204-016-1854-0 · Cited by 37 · see citing works
Discovery of a Non-Estrogenic Irreversible Inhibitor of 17β-Hydroxysteroid Dehydrogenase Type 1 from 3-Substituted-16β-( m -carbamoylbenzyl)-estradiol Derivatives
Maltais, R., Ayan, D. P., Trottier, A., Barbeau, X., Lagüe, P., Bouchard, J., & Poirier, D. (2013) · Journal of Medicinal Chemistry · doi:10.1021/jm401639v · Cited by 33 · see citing works
Lipoxin A4 regulates expression of the estrogen receptor and inhibits 17β-estradiol induced p38 mitogen-activated protein kinase phosphorylation in human endometriotic stromal cells
Chen, S., Wu, R., Su, L., Zhou, W., Zhu, M.-B., & Chen, Q. (2014) · Fertility and Sterility · doi:10.1016/j.fertnstert.2014.03.029 · Cited by 31 · see citing works
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Estrogen biosynthesis and signaling in endometriosis
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Role of estrogen and estrogen-related factors in endometriosis
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Authors: Rižner, T. L.
Affiliations: University of Ljubljana (SI)
Corresponding author: Rižner, Tea Lanišnik
ORCID: Rižner, Tea Lanišnik
Venue: Molecular and Cellular Endocrinology
Publisher: Elsevier BV
Published: 2009-08
Volume: 307
Issue: 1-2
Pages: 8-18
ISSN: 0303-7207 (ISSN-L)
DOI: 10.1016/j.mce.2009.03.022
OpenAlex: W2163825655
Semantic Scholar: c603753d7a96016b2da52a05cc0370ed18a55340
Cited by: 153
References: 120
Citations by year: 2026: 5 · 2025: 10 · 2024: 13 · 2023: 8 · 2022: 6 · 2021: 6 · 2020: 7 · 2019: 10 · 2018: 9 · 2017: 9 · 2016: 13 · 2015: 9 · 2014: 9 · 2013: 8 · 2012: 11
FWCI: 1.46
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Molecular and Cellular Endocrinology (publishedVersion)
PubMed (publishedVersion)
Trinity's Access to Research Output (TARA) (Trinity College Dublin) (submittedVersion)
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 › Obstetrics and Gynecology › Endometrial and Cervical Cancer Treatments
Keywords: endometriosis, estrogen metabolism, estradiol synthesis, estrogen receptor, endometrium, endometriosis pathogenesis, therapeutic target
MeSH terms: Endometriosis, Endometrium, Estrogens, Female, Humans, Receptors, Estrogen

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Estrogen metabolism and action in endometriosis

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