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Estrogen metabolism and action in endometriosis
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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“Imbalance in the biosynthesis and inactivation of steroids can lead to development of disease, including hormonally dependent cancer”
From Role of aldo-keto reductase family 1 (AKR1) enzymes in human steroid metabolism (2014) · cites this paper as [3]
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Cites
Giudice, L. C., & Kao, L. C. (2004) · The Lancet · doi:10.1016/s0140-6736(04)17403-5 · Cited by 3,166
Sampson, J. A. (1927) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(15)30003-x · Cited by 2,334
Estrogen Receptor Null Mice: What Have We Learned and Where Will They Lead Us?
Couse, J. F., & Korach, K. S. (1999) · Endocrine Reviews · doi:10.1210/edrv.20.3.0370 · Cited by 2,045
The complex role of estrogens in inflammation
Straub, R. H. (2007) · Endocrine Reviews · doi:10.1210/er.2007-0001 · Cited by 1,950
Eskenazi, B., & Warner, M. L. (1997) · Obstetrics and Gynecology Clinics of North America · doi:10.1016/s0889-8545(05)70302-8 · Cited by 1,617
Nisolle, M., & Donnez, J. (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)00191-x · Cited by 1,279
Sources of estrogen and their importance
Simpson, E. R. (2003) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/s0960-0760(03)00360-1 · Cited by 936
Integration of the extranuclear and nuclear actions of estrogen
Levin, E. R. (2005) · Molecular Endocrinology · doi:10.1210/me.2004-0390 · Cited by 708
Labrie, F. (1991) · Molecular and Cellular Endocrinology · doi:10.1016/0303-7207(91)90116-a · Cited by 685
Olive, D. L., & Schwartz, L. B. (1993) · New England Journal of Medicine · doi:10.1056/nejm199306173282407 · Cited by 675
Cited by
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
“The main function of regulatory T cells is modulation of the immune system, maintaining tolerance to self-antigens and preventing autoimmune diseases [29].”
BackgroundInfluentialEndometriosis-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 243
“Estrogen signalling modulates a large number of down-stream disease processes within endometriosis lesions, which are reviewed in(30, 31) and (32).”
BackgroundRole 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
“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-citationVasculogenesis: 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
“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.”
BackgroundUterine disorders and pregnancy complications: insights from mouse models
Lim, H. J., & Wang, H. (2010) · Journal of Clinical Investigation · doi:10.1172/jci41210 · Cited by 126
“Altered expression of enzymes involved in estrogen metabolism further enhances the accumulation of estradiol in patients with endometriosis (83, 96).”
BackgroundYu, 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 116
“Endometriosis (EMS) is one of the common estrogendependent inflammatory diseases, which affects 10–15% of women of reproductive age (Rizner 2009).”
BackgroundEndometriosis: 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
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
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
“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-citationNew 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 97
“Although endometriosis is an estrogen-dependent disease, hormone derangement has been proposed as the cause of endometriosis [4].”
BackgroundGarcía–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
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
“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.”
BackgroundInfluentialChoi, J., Jo, M., Lee, E., Lee, D., & Choi, D. (2015) · Fertility and Sterility · doi:10.1016/j.fertnstert.2015.05.020 · Cited by 87
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
Zhang, L., Xiong, W., Xiong, Y., Liu, H., & Liu, Y. (2016) · Molecular Human Reproduction · doi:10.1093/molehr/gaw025 · Cited by 69
Hevir, N., Šinkovec, J., & Rižner, T. L. (2011) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2010.09.011 · Cited by 69
Self-citationYang, H., Mei, J., Chang, K., Zhou, W., Huang, L., & Li, M. (2017) · Europe PMC (PubMed Central) · Cited by 73
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
Hevir, N., Trošt, N., Debeljak, N., & Rižner, T. L. (2010) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2010.12.013 · Cited by 66
Self-citationVicente-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 65
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
“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…”
BackgroundEMAS 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
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
“2012), E2 concentrations in endometriotic lesions are known to be elevated (Rizner 2009).”
BackgroundInfluentialCurcumin 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
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
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 53
Self-citationHevir, 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
“In contrast to estrogens, which enhance proliferation of the endometrium, progesterone counteracts the estrogen effects and instead promotes differentiation of endometrial cells [6,7].”
BackgroundLi, 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
“…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…”
BackgroundDelvoux, 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
“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).”
BackgroundLu, 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
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 48
“Thisknowledgemay facilitate understanding of the metabolic plasticity of EcE in maintaining its homeostasis and growth in a context of unfavorable microenvironment.”
Hevir, N., Ribič-Pucelj, M., & Rižner, T. L. (2012) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2012.12.019 · Cited by 45
“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-citationProgestins 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
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
“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].”
BackgroundEndocrinology 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 44
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
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
“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…”
BackgroundGonzález-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
Liang, Y., & Yao, S. (2016) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2016.01.012 · Cited by 41
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
“Endometriosis is known to be an estrogen-dependent disorder (Rizner, 2009).”
BackgroundInvestigation 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
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 38
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
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
Immune and endocrine regulation in endometriosis: what we know
Zhang, H., Sheng, S., Pan, Z., Zhao, L., Yang, C., Li, C., & Wang, F. (2023) · Journal of Endometriosis and Uterine Disorders · doi:10.1016/j.jeud.2023.100049 · Cited by 32
Estrogen is essential but not sufficient to induce endometriosis
Galvankar, M., Singh, N., & Modi, D. N. (2017) · Journal of Biosciences · doi:10.1007/s12038-017-9687-4 · Cited by 31
Chen, Y., Huang, Q., Chen, Q., Lin, Y., Sun, X., Zhang, H., Zhu, M., & Dong, S. (2014) · Toxicology in Vitro · doi:10.1016/j.tiv.2014.11.008 · Cited by 28
Huang, Z., Lin, D., Zhang, H., Yang, M., Chen, J., Ding, X., Dai, S., Hong, Y., Liang, G., Li, Q., et al. (2024) · Immunology · doi:10.1111/imm.13786 · Cited by 31
“Furthermore, endometriosis is considered an oestrogen-dependent disease [28], and the oestrogen synthesis-associated enzymes including aromatase [29], HSD3B1 [30] and HSD17B1 [31] were noticeably increased.”
BackgroundTang, Q., Shang, F.-H., Wang, X., Yang, Y., Chen, G., Chen, Y., Zhang, J., & Xu, X. (2014) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2013.12.047 · Cited by 27
“Recent studies suggest that endometriosis sufferers have higher content of estrogen than normal ones (Rižner, 2009).”
BackgroundDodds, K. N., Beckett, E. A. H., Evans, S., & Hutchinson, M. R. (2017) · Biology of Reproduction · doi:10.1093/biolre/iox132 · Cited by 27
“It has long been hypothesized that endometriosis lesions thrive under the influence of heightened or prolonged estrogen stimulation [17, 18], since symptoms of the condition often first present at, or soon after menarche, and improve when estrogen levels fall at menopause; and the endometrium involutes in the absence…”
BackgroundRecent Advances in Gene Therapy of Endometriosis
Shubina, A., Egorova, A., Баранов, В. С., & Kiselev, A. (2014) · Recent Patents on DNA & Gene Sequences · doi:10.2174/18722156113079990021 · Cited by 28
“Endometriosis is also characterized by high levels of 17 -hydroxysteroid dehydrogenase type 1 (17 -HSD1), an enzyme that catalyzes the process of converting estrone (E1) to the more potent E2, and by low levels of 17 -hydroxysteroid dehydrogenase type 2 (17 -HSD2), an enzyme that catalyzes the reverse process [14].”
BackgroundTargeting the formation of estrogens for treatment of hormone dependent diseases–current status
Rižner, T. L., & Romano, A. (2023) · Frontiers in Pharmacology · doi:10.3389/fphar.2023.1155558 · Cited by 29
“In endometrial cancer, studies that compared cancer tissue with adjacent morphologically normal tissue reported unchanged (Smuc and Rizner, 2009; Rizner, 2013; Sinreih et al., 2017; Cornel et al., 2018; Cornel et al., 2019) or increased STS expression (Lepine et al., 2010).”
BackgroundResultInfluentialSelf-citationWang, W., Li, Y., Maitituoheti, M., Yang, R., Wu, Z., Wang, T., Ma, D., & Wang, S. (2012) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2012.09.007 · Cited by 26
“Although the aetiology of endometriosis is still unclear, various evidence has been found to show that endometriosis is a complex disease, which is affected by inflammation, hormonal regulation and genetic and environmental factors (Falconer et al., 2007; Olive and Schwartz, 1993; Rizner, 2009).”
BackgroundLü, X., Wu, Y. R., Gao, X., Wang, Y., Wang, L., & Sun, X. (2012) · Fertility and Sterility · doi:10.1016/j.fertnstert.2012.03.055 · Cited by 26
Żabińska, M., Wiśniewska, K., Węgrzyn, G., & Pierzynowska, K. (2024) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2024.107070 · Cited by 26
“The etiology of endometriosis is complex and multifactorial, involving complex interactions of genetic, immunological, hormonal, and environmental factors (Rizner, 2009).”
BackgroundZhao, L., Gu, C., Huang, K., Fan, W., Li, J., Ye, M., Han, W., & Meng, Y. (2016) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2016.06.003 · Cited by 24
“Previous evidence has shown that endometriosis is a complex hormonedependent disorder influenced by multiple environmental and genetic factors (Falconer et al., 2007; Rizner, 2009).”
BackgroundAberrant PTEN expression in response to progesterone reduces endometriotic stromal cell apoptosis
Choi, J., Jo, M., Lee, E., Hwang, S., & Choi, D. (2016) · Reproduction · doi:10.1530/rep-16-0322 · Cited by 23
Markers of Local and Systemic Estrogen Metabolism in Endometriosis
Othman, E. R., Markeb, A. A., Khashbah, M. Y., Abdelaal, I. I., ElMelegy, T. T. H., Fetih, A. N., van der Houwen, L. E. E., Lambalk, C. B., & Mijatovic, V. (2020) · Reproductive Sciences · doi:10.1007/s43032-020-00383-4 · Cited by 24
Chang, K., Liu, L.-B., Li, H., Mei, J., Shao, J., Xie, F., Li, M., & Li, D. (2014) · PubMed Central · Cited by 23
Maltais, R., Ayan, D. P., & Poirier, D. (2011) · ACS Medicinal Chemistry Letters · doi:10.1021/ml200093v · Cited by 23
Hilal, T., Puetter, V., Otto, C., Parczyk, K., & Bader, B. (2010) · SLAS DISCOVERY · doi:10.1177/1087057109359196 · Cited by 23
Machado-Linde, F., Pelegrín, P., Sanchez-Ferrer, M., León, J., Cascales, P., & Parrilla, J. (2012) · Reproductive Sciences · doi:10.1177/1933719112446080 · Cited by 22
“In turn, this can lead to high E2 biosynthesis and low E2 degradation, excess local E2, and decreased levels of protective progesterone, 55 which results in further proliferation of ectopic endometrium as reported by Rizner.(40) 1020 Reproductive Sciences 19(10)”
BackgroundInfluentialIdentification and Analysis of Potential Autophagy-Related Biomarkers in Endometriosis by WGCNA
Wang, J., Cong, S., Wu, H., He, Y., Liu, X., Sun, L., Zhao, X., & Zhang, G. (2021) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2021.743012 · Cited by 21
“Many factors have been shown to contribute to abnormal autophagy in endometrial tissues, including estrogen, certain drugs, oxidative stress, and hypoxia (Rižner, 2009; Zhao et al., 2018).”
BackgroundLiu, Y., Kang, J., Zhang, Y., Song, S., Xu, Q., Zhang, H., Lü, L., Wei, S., Chen, L., & Su, R. (2023) · Food & Function · doi:10.1039/d3fo00750b · Cited by 21
Polymorphic variants of CYP 17 and CYP 19A and risk of infertility in endometriosis
Szczepańska, M., Wirstlein, P. K., Skrzypczak, J., & Jagodziński, P. P. (2013) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1111/aogs.12210 · Cited by 21
“Aberrant levels of several estrogen-metabolizing enzymes have been demonstrated in ectopic endometrium (24).”
BackgroundKISS1/KISS1R expression in eutopic and ectopic endometrium of women suffering from endometriosis.
Makri, A., Msaouel, P., Petraki, C. D., Milingos, D. S., Πρωτόπαπας, Α., Liapi, A., Antsaklis, A. J., Μagkou, C., & Koutsilieris, M. (2012) · PubMed · Cited by 21
Brassica Bioactives Could Ameliorate the Chronic Inflammatory Condition of Endometriosis
García-Ibáñez, P., Yepes‐Molina, L., Ruiz‐Alcaraz, A. J., Martinez‐Esparza, M., Moreno, D. A., Carvajal, M., & García–Peñarrubia, P. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21249397 · Cited by 21
“Current treatments are based on the estrogen dependence of this pathology [42,43].”
BackgroundEstrogen restricts the apoptosis of endometrial stromal cells by promoting TSLP secretion
Yang, H.-L., Chang, K.-K., Mei, J., Zhou, W.-J., Liu, L.-B., Yao, L., Meng, Y., Wang, M.-Y., Ha, S., Lai, Z.-Z., et al. (2018) · Molecular Medicine Reports · doi:10.3892/mmr.2018.9428 · Cited by 22
“It has been well reported that EMS is a hormone-responsive disease associated with increased estrogen production and resistance against the progesterone-based response (6,7).”
BackgroundKoleini, N., Taherian, A., Tehrany, H. G., & Roghaei, M. A. (2010) · DOAJ (DOAJ: Directory of Open Access Journals) · doi:10.22074/ijfs.2010.45826 · Cited by 20
Beranič, N., Brožič, P., Brus, B., Sosič, I., Gobec, S., & Rižner, T. L. (2012) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2011.12.011 · Cited by 16
Self-citationToit, R. L.-D., Storbeck, K., Cartwright, M., Cabral, A., & Africander, D. (2016) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2016.09.004 · Cited by 20
Choi, J., Jo, M., Lee, E., Lee, D., & Choi, D. (2019) · Molecular Human Reproduction · doi:10.1093/molehr/gaz002 · Cited by 19
“In contrast, some ectopic and eutopic endometrial stromal cells in women with endometriosis exhibit progesterone resistance (Attia et al., 2000; Bulun et al., 2006; Rizner, 2009).”
BackgroundLin, Y., Yuan, M., & Wang, G. (2024) · Journal of Trace Elements in Medicine and Biology · doi:10.1016/j.jtemb.2024.127436 · Cited by 20
Barra, F., Romano, A., Grandi, G., Facchinetti, F., & Ferrero, S. (2019) · Expert Opinion on Investigational Drugs · doi:10.1080/13543784.2019.1618269 · Cited by 18
Shinohara, A., Kutsukake, M., Takahashi, M., Kyo, S., Tachikawa, E., & Tamura, K. (2012) · Journal of Pharmacological Sciences · doi:10.1254/jphs.11216fp · Cited by 18
Endometriosis Gene Expression Heterogeneity and Biosignature: A Phylogenetic Analysis
Abu-Asab, M. S., Zhang, M., Amini, D., Abu-Asab, N., & Amri, H. (2011) · Obstetrics and Gynecology International · doi:10.1155/2011/719059 · Cited by 17
The activation of cGAS‐STING pathway causes abnormal uterine receptivity in aged mice
Chen, S., Shi, W., Ran, F., Liu, C., Luo, H., Wu, L., Wu, Y., Zhang, T., & Yang, Z. (2024) · Aging Cell · doi:10.1111/acel.14303 · Cited by 17
Wang, P., Dang, L., & Zhu, B. T. (2015) · Steroids · doi:10.1016/j.steroids.2015.11.001 · Cited by 17
Yano, M., Matsuda, A., Natsume, T., Ogawa, S., Awaga, Y., Hayashi, I., Hama, A. T., & Takamatsu, H. (2018) · Human Reproduction · doi:10.1093/humrep/dey383 · Cited by 17
Émond, J.-P., Caron, P., Pušić, M. N., Turcotte, V., Simonyan, D., Vogler, A., Osredkar, J., Rižner, T. L., & Guillemette, C. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.1034614 · Cited by 18
Self-citationThe mixture of non-persistent endocrine-disrupting chemicals in relation to endometriosis
Ao, J., Zhu, W., Jiang, W., Zeng, X., Qiu, W., Yin, S., Wang, W.-J., & Zhang, J. (2024) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2024.117129 · Cited by 16
Pharmacologic Interventions for Endometriosis-Related Pain
Kou, L., Huang, C., Xiao, D., Liao, S., Li, Y., & Wang, Q. (2025) · Obstetrics and Gynecology · doi:10.1097/aog.0000000000005923 · Cited by 14
Amanda, C. R., Asmarinah, A., Hestiantoro, A., Tulandi, T., & Febriyeni (2024) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2024.07.061 · Cited by 14
Kataoka, H., Mori, T., Okimura, H., Matsushima, H., Ito, F., Koshiba, A., Tanaka, Y., Akiyama, K., Maeda, E., Sugahara, T., et al. (2019) · Human Reproduction · doi:10.1093/humrep/dez067 · Cited by 14
“…biosynthesis, is more highly expressed in endometriotic tissues than in the endometrium (Huhtinen et al., 2012), and estrogen, produced by the abnormally elevated aromatase, promotes the growth of endometriotic tissue (Bulun, 2009; Rizner, 2009; Huhtinen et al., 2012; Colette et al., 2013).”
BackgroundSilva, N., Tennekoon, K. H., Senanayake, H. M., & Samarakoon, S. R. (2013) · Taiwanese Journal of Obstetrics and Gynecology · doi:10.1016/j.tjog.2013.10.015 · Cited by 14
“The lack of similar effects in women without endometriosis is perhaps partly attributable to the differences in the ER levels in the eutopic endometria of the two groups, where higher numbers of ERs are expressed in women with endometriosis [33,34].”
BackgroundActivin A Stimulates Aromatase via the ALK4-Smad Pathway in Endometriosis
Zheng, J., Qu, J., Lu, P., Hou, Z., Cui, Y., Mao, Y., Qi, X., Ji, H., & Liu, J. (2016) · BioMed Research International · doi:10.1155/2016/5791510 · Cited by 14
Beranič, N., & Rižner, T. L. (2012) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2012.07.004 · Cited by 14
Self-citationResearch progress of dydrogesterone in the treatment of endometriosis
Tang, W., Zhu, X., Bian, L., & Zhang, B. (2024) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2024.02.034 · Cited by 16
Maltais, R., Trottier, A., Delhomme, A., Barbeau, X., Lagüe, P., & Poirier, D. (2015) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2015.01.059 · Cited by 13
Knific, T., Vouk, K., Vogler, A., Osredkar, J., Gstoettner, M., Wenzl, R. J., & Rižner, T. L. (2018) · Biomarkers in Medicine · doi:10.2217/bmm-2017-0426 · Cited by 13
Self-citationKamergorodsky, G., Invitti, A. L., D’Amora, P., Parreira, R. M., Kopelman, A., Bonetti, T. C., Girão, M. J. B. C., & Schor, E. (2020) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2020.110743 · Cited by 12
Muhammad, A. I., Forcados, G. E., Yusuf, A. P., Abubakar, M. B., Sadiq, I. Z., Elhussin, I. A., Siddique, M. A. T., Aminu, S., Suleiman, R. B., Abubakar, Y. S., et al. (2022) · Molecules · doi:10.3390/molecules27248943 · Cited by 14
Zhang, C., Yuan, X., & Zhang, Y. (2015) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-015-3807-x · Cited by 12
SULFATION PATHWAYS: Contribution of intracrine oestrogens to the aetiology of endometriosis
Piccinato, C. D. A., Malvezzi, H., Gibson, D. A., & Saunders, P. T. K. (2018) · Journal of Molecular Endocrinology · doi:10.1530/jme-17-0297 · Cited by 12
Beranič, N., & Rižner, T. L. (2012) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2012.10.028 · Cited by 12
Self-citationEffects of TSLP on obstetrical and gynecological diseases
Zhang, Y., & Jin, L. (2016) · American Journal of Reproductive Immunology · doi:10.1111/aji.12612 · Cited by 12
Delsouc, M. B., Conforti, R. A., Vitale, D. L., Alaniz, L. D., Pacheco, P. H., Andújar, S. A., Vallcaneras, S. S., & Casais, M. (2021) · Life Sciences · doi:10.1016/j.lfs.2021.120099 · Cited by 11
The role of SRC1 and SRC2 in steroid-induced SDF1 expression in normal and ectopic endometrium
Shi, X., Xu, W. D., Dai, H.-H., Sun, Y., & Wang, X.-L. (2014) · Reproduction · doi:10.1530/rep-14-0027 · Cited by 11
“Estrogen can be synthesized locally in the endometriotic lesions (Rizner 2009).”
BackgroundCheng, Y.-H., Huang, C., Lien, H.-T., Hsiao, Y.-Y., Weng, P.-L., Chang, Y.-C., Cheng, J., & Lan, K. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25073873 · Cited by 10
“Its levels are elevated in the menstrual blood of women with endometriosis [112,113], suggesting that estrogen is formed locally in the endometrium of patients with endometriosis [114].”
BackgroundAziz, M., Beaton, M., Aziz, M. A., Opoku-Anane, J., & Elhadad, N. (2025) · npj Women s Health · doi:10.1038/s44294-025-00086-8 · Cited by 11
“DefectsinT cell and regulatory cellfunctioning, aswellasabnormal levelsofprostaglandins,cytokines,andin fl ammatoryproductshaveallbeen observed among patients with endometriosis 24,25,27 as well as patients with several autoimmune conditions 32,33 .”
Metadata
- 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)
- 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
- 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 › Endocrinology › 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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