Role of Estrogen Receptor-β in Endometriosis
Open accessAbstract
Endometriosis is an estrogen-dependent disease. The biologically active estrogen, estradiol, aggravates the pathological processes (e.g., inflammation and growth) and the symptoms (e.g., pain) associated with endometriosis. Abundant quantities of estradiol are available for endometriotic tissue via several mechanisms including local aromatase expression. The question remains, then, what mediates estradiol action. Because estrogen receptor (ER)β levels in endometriosis are >100 times higher than those in endometrial tissue, this review focuses on this nuclear receptor. Deficient methylation of the ERβ promoter results in pathological overexpression of ERβ in endometriotic stromal cells. High levels of ERβ suppress ERα expression. A severely high ERβ-to-ERα ratio in endometriotic stromal cells is associated with suppressed progesterone receptor and increased cyclo-oxygenase-2 levels contributing to progesterone resistance and inflammation. ERβ-selective estradiol antagonists may serve as novel therapeutics of endometriosis in the future.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
0 of 18 cited sources checked · 0 supported · 0 flagged
- Findingown data
A CpG island occupies the promoter region of the ERβ gene.
“We identified a CpG island occupying the promoter region of the ERβ gene (Fig. 3).”
Quote in the paperSubstantial claim - Findingnone given
ERβ expression may be more than 100 times higher in endometriotic tissue than in endometrium.
“Among these nuclear receptors, ERβ expression is maybe >100 times higher in endometriotic tissue than in endometrium.”
Quote in the paperNot a substantial claim - Findingown data
Insufficient methylation of the ERβ promoter causes pathological overexpression of ERβ in endometriotic stromal cells.
“Deficient methylation of the ERβ promoter results in pathological overexpression of ERβ in endometriotic stromal cells.”
- Also stated in: § Epigenetic Regulation of the ERβ Promoter is Responsible for Its High Levels in Endometriosis · boosted
“Thus high ERβ mRNA and protein expression in endometriotic cells were mediated by an epigenetic defect involving hypomethylation of a CpG island occupying its promoter (Fig. 3).”
Quote in the paperSubstantial claim - Also stated in: § Epigenetic Regulation of the ERβ Promoter is Responsible for Its High Levels in Endometriosis · boosted
- Findingnone given
ERα mRNA and protein levels are several fold lower in endometriotic tissue and stromal cells than in endometrial tissue and stromal cells.
“ERα mRNA and protein levels are several fold lower in endometriotic tissue and stromal cells compared with endometrial tissue and stromal cells.”
Quote in the paperSubstantial claim - Findingown data
In vitro methylation strongly inactivates ERβ promoter activity.
“The activity of the ERβ promoter was strongly inactivated by in vitro methylation.”
Quote in the paperSubstantial claim
- Findingown data
SF1 is differentially regulated in endometriosis compared with eutopic endometrium.
“In addition to ERα, ERβ, and PR, the orphan nuclear receptor SF1 is also differentially regulated in endometriosis versus eutopic endometrium (Fig. 2).”
Quote in the paperSubstantial claim - Findingown data
ERβ knockdown or overexpression most drastically alters the ERα mRNA species that arise from the far distal promoter C.
“ERβ knockdown or overexpression most drastically altered ERα mRNA species arising from the far distal promoter C.”
Quote in the paperNot a substantial claim - Findingown data
ERα binds to neither of the promoter C sequences.
“In contrast, ERα bound to neither promoter C sequences.”
Quote in the paperSubstantial claim - Findingown data
Ovarian endometriotic tissue SF1 mRNA levels are more than 12,000 times higher than in endometrium.
“Ovarian endometriotic tissue SF1 and ERβ mRNA levels were >12,000 times and 142 times higher than in endometrium, respectively.”
Quote in the paperNot a substantial claim - Findingown data
Treatment with a demethylating agent significantly increases ERβ mRNA levels in endometrial cells.
“Treatment with a demethylating agent significantly increased ERβ mRNA levels in endometrial cells.”
Quote in the paperSubstantial claim - Findingown data
ERα mRNA levels are sevenfold lower in endometriotic stromal cells than in endometrial stromal cells.
“ERα mRNA levels were significantly lower (sevenfold) in endometriotic stromal cells compared with endometrial stromal cells.”
Quote in the paperSubstantial claim - Findingcitation
Total PR and PR-B mRNA levels are significantly lower in endometriotic stromal cells than in endometrial stromal cells.
“Total PR and PR-B mRNA levels in endometriotic stromal cells were significantly lower than those in endometrial stromal cells.38”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [38]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- Findingcitation
The critical region that confers ERβ promoter activity bears the identical CpG island.
“The critical region that confers promoter activity also bears the identical CpG island (Fig. 3).38”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [38]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- Findingown data
ERβ overexpression in endometrial stromal cells decreases ERα mRNA and protein levels.
“Conversely, ERβ overexpression in endometrial stromal cells decreased ERα mRNA and protein levels.”
Quote in the paperSubstantial claim - Findingown data
Estradiol enhances binding of both ERα and ERβ to a region containing a nonclassical AP-1 motif in promoter A in endometriotic cells.
“Estradiol enhanced binding of both ERα and ERβ to a region containing a nonclassical activator protein (AP)-1 motif in promoter A in endometriotic cells.”
Quote in the paperNot a substantial claim - Findingcitation
High ERβ levels suppress ERα expression.
“High levels of ERβ suppress ERα expression.”
- Also stated in: § ERβ Is Responsible for Low ERα Expression in Endometriotic Stromal Cells · plain
“ERβ knockdown significantly increased ERα mRNA and protein levels in endometriotic stromal cells.44 Conversely, ERβ overexpression in endometrial stromal cells decreased ERα mRNA and protein levels.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [44]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- Also stated in: § ERβ Is Responsible for Low ERα Expression in Endometriotic Stromal Cells · plain
- Findingown data
With estradiol present, ERβ binds to a genomic region flanking an AP1 site upstream of promoter C and to a region bearing an Sp1 motif immediately downstream of promoter C in endometriotic stromal cells.
“In the presence of estradiol, ERβ bound to a genomic region flanking an AP1 site upstream of promoter C and a region bearing a specificity protein (Sp)1 motif immediately downstream of promoter C in endometriotic stromal cells.”
Quote in the paperSubstantial claim - Findingcitation
ERβ knockdown significantly decreases proliferation of endometriotic stromal cells.
“ERβ knockdown significantly decreased proliferation of endometriotic stromal cells.44”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [44]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- Findingown data
Unpublished observations suggest that reducing the ERα-to-ERβ ratio in endometrial stromal cells diminishes estradiol induction of PR expression.
“Our unpublished observations suggest that a reduction in the ERα-to-ERβ ratio in endometrial stromal cells diminishes estradiol induction of PR expression.”
Quote in the paperSubstantial claim - Findingown data
ERβ levels in endometriosis are more than 100 times higher than in endometrial tissue.
“Because estrogen receptor (ER)β levels in endometriosis are >100 times higher than those in endometrial tissue, this review focuses on this nuclear receptor.”
- Also stated in: § Nuclear Receptor Expression in Endometriosis · plain
“Ovarian endometriotic tissue SF1 and ERβ mRNA levels were >12,000 times and 142 times higher than in endometrium, respectively.”
Quote in the paperSubstantial claim - Also stated in: § Nuclear Receptor Expression in Endometriosis · plain
- Findingown data
Bisulfite sequencing shows significantly higher methylation in primary endometrial cells than in endometriotic cells.
“Bisulfite sequencing of this region showed significantly higher methylation in primary endometrial cells versus endometriotic cells.”
Quote in the paperSubstantial claim - Findingown data
ERα, PR, and PR-B levels are remarkably lower in endometriotic tissue than in endometrium.
“In contrast, ERα, PR, and PR-B levels were remarkably lower in endometriotic tissue (Fig. 2).”
Quote in the paperSubstantial claim - Findingown data
Ovarian endometriotic tissue ERβ mRNA levels are 142 times higher than in endometrium.
“Ovarian endometriotic tissue SF1 and ERβ mRNA levels were >12,000 times and 142 times higher than in endometrium, respectively.”
Quote in the paperSubstantial claim - Findingcitation
ERβ knockdown significantly increases ERα mRNA and protein levels in endometriotic stromal cells.
“ERβ knockdown significantly increased ERα mRNA and protein levels in endometriotic stromal cells.44”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [44]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- Premisecitation
Endometriosis depends on estrogen for its growth.
“Endometriosis is an estrogen-dependent disease.”
- Also stated in: § Abstract · plain
“The most striking aspect of endometriosis is its dependence on estrogen for growth, similar to that seen in eutopic endometrium.6,7”
Quote in the paperSubstantial claim0 of 2 sources checked- cites [6]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites [7]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- Also stated in: § Abstract · plain
- Interpretationown data
ERα, ERβ, and PR levels are markedly different between endometrial and endometriotic tissues or stromal cells derived from them.
“In conclusion, ERα, ERβ and PR levels were markedly different in endometrial versus endometriotic tissues or stromal cells derived from these tissues.”
Quote in the paperSubstantial claim - Interpretationreasoning
A severely high ERβ-to-ERα ratio in endometriotic stromal cells contributes to progesterone resistance and inflammation.
“A severely high ERβ-to-ERα ratio in endometriotic stromal cells is associated with suppressed progesterone receptor and increased cyclo-oxygenase-2 levels contributing to progesterone resistance and inflammation.”
Quote in the paperSubstantial claim - Interpretationreasoning
A severely high ERβ-to-ERα ratio in endometriotic stromal cells is associated with increased cyclo-oxygenase-2 levels.
“A severely high ERβ-to-ERα ratio in endometriotic stromal cells is associated with suppressed progesterone receptor and increased cyclo-oxygenase-2 levels contributing to progesterone resistance and inflammation.”
Quote in the paperSubstantial claim - Interpretationown data
Primarily ERα promoter C may mediate ERβ-mediated inhibition of ERα expression in endometriotic stromal cells.
“In summary, these findings collectively suggest that primarily ERα promoter C may mediate ERβ-mediated inhibition of ERα expression in endometriotic stromal cells (Fig. 3).”
Quote in the paperSubstantial claim - Premisecitation
Endocrine treatments that interrupt ovulation and ovarian estrogen production succeed in only half of treated endometriosis patients.
“These treatments, which interrupt ovulation and ovarian estrogen production, are successful in only half of the patients treated, however.9–11”
Quote in the paperSubstantial claim0 of 3 sources checked- cites [9]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites [10]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites [11]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- Interpretationown data
The differential expression of nuclear receptors seen in endometriotic versus endometrial tissues is preserved in stromal cells cultured from those tissues.
“Differential expression of nuclear receptors in endometriotic versus endometrial tissues are preserved in stromal cells cultured from these tissues.”
Quote in the paperSubstantial claim - Interpretationreasoning
ERα deficiency in endometriosis may cause the failure of estradiol to induce PR expression, contributing to secondary PR deficiency and progesterone resistance.
“ERα deficiency in endometriosis may be responsible for the failure of estradiol to induce PR expression, thus contributing to secondary PR deficiency and progesterone resistance in women with this disease.”
Quote in the paperSubstantial claim - Interpretationown data
A profoundly low ERα-to-ERβ ratio in endometriotic stromal cells may shift the response from estradiol stimulation to failure of PR induction.
“A profoundly low ERα-to-ERβ ratio in endometriotic stromal cells may be responsible for a shift from estradiol stimulation to failure of induction of PR expression in endometriotic stromal cells (Fig. 3).”
Quote in the paperSubstantial claim - Interpretationcitation
Endometriosis contains a unique complement of steroid hormone receptors compared with eutopic endometrium.
“Despite its sensitivity to estrogen, endometriosis appears to contain a unique complement of steroid hormone receptors compared with that of its normal tissue counterpart, the eutopic endometrium.”
Quote in the paperSubstantial claim - Interpretationnone given
The expression of steroid receptors and other nuclear receptors is strikingly different between endometriotic and eutopic endometrial tissues.
“Expression of steroid receptors and other nuclear receptors are strikingly different between endometriotic and eutopic endometrial tissues.”
Quote in the paperNot a substantial claim - Interpretationcitation
High estradiol from local aromatase activity together with high ERβ levels in endometriotic stromal cells may perturb ERα regulation and suppress ERα expression.
“However, strikingly high quantities of estradiol produced via local aromatase activity in addition to high ERβ levels in stromal cells of endometriosis may perturb this regulation and may suppress ERα expression.26,38”
Quote in the paperSubstantial claim0 of 2 sources checked- cites [26]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites [38]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- Premisecitation
Patients frequently become resistant to repeated treatment with the same agent over 6 months to 3 years.
“Patients often develop resistance to repeated treatments with the same agent over a period of 6 months to 3 years.12”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [12]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- Interpretationown data
High ERβ mRNA and protein expression in endometriotic cells is mediated by an epigenetic defect involving hypomethylation of a CpG island in its promoter.
“Thus high ERβ mRNA and protein expression in endometriotic cells were mediated by an epigenetic defect involving hypomethylation of a CpG island occupying its promoter (Fig. 3).”
Quote in the paperSubstantial claim - Interpretationreasoning
A severely high ERβ-to-ERα ratio in endometriotic stromal cells is associated with suppressed progesterone receptor levels.
“A severely high ERβ-to-ERα ratio in endometriotic stromal cells is associated with suppressed progesterone receptor and increased cyclo-oxygenase-2 levels contributing to progesterone resistance and inflammation.”
Quote in the paperSubstantial claim - Interpretationreasoning
Estradiol likely also plays a key role in regulating ERα expression in human endometrial stromal cells.
“It is quite likely that estradiol also plays a key role in regulating ERα expression in human endometrial stromal cells.”
Quote in the paperSubstantial claim - Interpretationnone given
Estradiol worsens the inflammatory and growth-related pathological processes and the pain symptoms of endometriosis.
“The biologically active estrogen, estradiol, aggravates the pathological processes (e.g., inflammation and growth) and the symptoms (e.g., pain) associated with endometriosis.”
Quote in the paperSubstantial claim - Interpretationcitation
Methylation of a CpG island at the ERβ promoter is a primary mechanism responsible for the differential expression of ERβ between endometriosis and endometrium.
“Therefore, methylation of a CpG island at the ERβ promoter region is a primary mechanism responsible for differential expression of ERβ in endometriosis and endometrium.38”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [38]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- Interpretationreasoning
ERβ is a key therapeutic target for endometriosis-associated pain.
“Thus ERβ represents a key therapeutic target for endometriosis-associated pain.”
Quote in the paperSubstantial claim - Interpretationown data
Knockdown studies suggest that ERβ has a positive role in endometriotic stromal cell cycle progression and proliferation.
“Knockdown studies also suggested a positive role of ERβ on endometriotic stromal cell cycle progression and proliferation.”
Quote in the paperNot a substantial claim - Interpretationreasoning
The already low response rate to endometriosis treatments is likely to fall further with repeated treatment attempts.
“This low response rate is likely further reduced with repeated treatment attempts.”
Quote in the paperSubstantial claim - Interpretationnone given
Defective DNA methylation and other epigenetic mechanisms may be responsible for the strikingly high ERβ expression in endometriosis.
“Defective DNA methylation and other accompanying epigenetic mechanisms may be responsible for strikingly high ERβ expression in endometriosis.”
Quote in the paperNot a substantial claim
- May combine two claims. 9
- Classified as probably not a substantial claim. 2
- The quote only partly states this claim. 1
May combine two claims.
FindingcitationERβ mRNA is about 34-fold higher in endometriotic stromal cells and is much lower or nearly absent in endometrial stromal cells.
“ERβ mRNA was strikingly higher (~34-fold) in endometriotic stromal cells, whereas it was much lower or nearly absent in endometrial stromal cells.38”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [38]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
May combine two claims.
FindingcitationThe average ERα-to-ERβ mRNA ratio is 841 in endometrial stromal cells and 21 in endometriotic stromal cells.
“The ratios of ERα to ERβ mRNA levels were, on average, 841 and 21 in endometrial and endometriotic stromal cells, respectively.38”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [38]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
May combine two claims.
Findingnone givenERβ suppresses ERα expression and produces strikingly high ERβ-to-ERα ratios in endometriotic cells.
“ERβ suppresses ERα expression and results in strikingly high ERβ-to-ERα ratios in endometriotic cells.”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataEndometriotic stromal cells have extraordinarily higher ERβ and significantly lower ERα and PR levels than endometrial stromal cells.
“Endometriotic stromal cells contained extraordinarily higher ERβ and significantly lower ERα and PR levels compared with endometrial stromal cells.”
Quote in the paperSubstantial claimMay combine two claims.
FindingcitationERα and ERβ protein levels differ significantly between endometriotic and endometrial stromal cells, matching the mRNA findings.
“Protein levels of ERα and ERβ were significantly different in these two groups similar to the findings regarding mRNA levels.38”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [38]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
May combine two claims.
PremisecitationEndometriotic tissue has access to large amounts of estradiol through multiple mechanisms, one of which is local aromatase expression.
“Abundant quantities of estradiol are available for endometriotic tissue via several mechanisms including local aromatase expression.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [26]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
May combine two claims.
InterpretationreasoningThe proposed mechanism may explain severely deficient PR-B in endometriotic stromal cells, which contributes to progesterone resistance in women with endometriosis.
“This proposed mechanism may explain severely deficient PR-B in endometriotic stromal cells, which contributes to progesterone resistance in women with endometriosis.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing). The quote only partly states this claim.
Study design and conductown dataA role of ERα promoter A in ERβ-mediated inhibition of ERα could not be ruled out.
“A role of ERα promoter A could not be ruled out.”
Quote in the paperNot a substantial claimMay combine two claims.
Interpretationnone givenEstradiol reaches endometriosis through the circulation or local production and regulates the growth of endometriotic tissue.
“Estradiol, which reaches endometriosis by circulation or is produced locally in endometriotic tissue, acts as a steroid hormone to regulate growth of endometriotic tissue.”
Quote in the paperNot a substantial claimMay combine two claims.
InterpretationreasoningEstradiol is a key hormone for the growth and persistence of endometriotic tissue and for the inflammation and pain associated with endometriosis.
“Circumstantial and laboratory evidence strongly support the notion that estradiol is a key hormone for the growth and persistence of endometriotic tissue as well as inflammation and pain associated with it.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S4 (based).
Interpretationnone givenERβ likely stimulates prostaglandin production in endometriotic tissues and cells by inducing COX2 expression.
“It is likely that ERβ simulates prostaglandin production in endometriotic tissues and cells via inducing COX2 expression.”
Quote in the paperNot a substantial claim
The paper relies on this without support.
Progestin or oral contraceptive treatment does not reliably suppress the growth of endometriotic tissue.
“Treatment with these agents, however, does not predictably suppress endometriotic tissue growth.”
The paper relies on this without support.
Prolonged progestin therapy or oral contraceptives containing progestins reliably cause atrophy of eutopic endometrium.
“The eutopic endometrium predictably becomes atrophic in response to prolonged progestin therapy or oral contraceptives that contain progestins.”
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Comparison between normal endometrium and samples of endometrial cancer and endometriosis lesions has revealed aberrant expression of both AR and ERs.
“Comparison between the patterns of expression of receptor proteins in normal endometrium with samples of endometrial cancer and endometriosis lesions has revealed evidence of aberrant expression of both AR and ERs, which may result in novel disease-specific targets for the action of steroids generated by intracrine activation/metabolism discussed below.”
From Endometrial Intracrinology: Oestrogens, Androgens and Endometrial Disorders (2018) · cites this paper as [35]
The “Nuclear Receptor Expression in Endometriosis” section (page not provided) reports higher ERβ and lower ERα expression in endometriotic tissue than in eutopic endometrium. The passages do not support the claimed comparison involving androgen receptors (AR) or endometrial cancer samples. (LLM, conf=0.88)
Experimental — accuracy not yet measuredThe highly expressed oestrogen in endometriotic tissue is present in its most biologically active form.
“Furthermore, the highly expressed oestrogen in endometriotic tissue is present in its most biologically active form [14,15].”
From HRT in Women Undergoing Pelvic Clearance for Endometriosis—A Case Report and a National Survey (2023) · cites this paper as [15]
Molecular studies have revealed the overexpression of oestrogen receptor beta (ERβ), which is >100 times higher in endometriotic lesions compared to normal endometrial tissue.
“Molecular studies have revealed the overexpression of oestrogen receptor beta (ERβ), which is >100 times higher in endometriotic lesions compared to normal endometrial tissue.”
From HRT in Women Undergoing Pelvic Clearance for Endometriosis—A Case Report and a National Survey (2023) · cites this paper as [15]
A meta-analysis showed that gene variants for interferon γ (IFNG CA repeat) and variants rs16826658 and rs2235529 of the WNT4 gene may be relevant to endometriosis.
“A recently published meta-analysis showed that in addition to the above-mentioned variants, gene variants for interferon γ (IFNG CA repeat) and variants of rs16826658 and rs2235529 of the WNT4 gene may be relevant.”
From Endometriosis: Epidemiology, Classification, Pathogenesis, Treatment and Genetics (Review of Literature) (2021) · cites this paper as [198]
The ERβ receptor encoded by the ESR2 gene is the dominant isoform in those with endometriosis.
“The ERβ receptor encoded by the ESR2 gene is the dominant isoform in those with endometriosis [198].”
From Endometriosis: Epidemiology, Classification, Pathogenesis, Treatment and Genetics (Review of Literature) (2021) · cites this paper as [198]
An unknown trend was confirmed for the PGR gene variant, rs1799969 of ICAM1, rs2292596 of AHRR, CYP17A1 rs743572 and rs1801282 of PPARγ.
“An unknown trend was also confirmed for the progesterone receptor (PGR) gene variant, the rs1799969 variants of the ICAM1 molecule, rs2292596 of the aromatic hydrocarbon receptor repressor gene (AHRR), the CYP17A1 rs743572 gene and the rs1801282 gene for the peroxisome γ proliferator-activated receptor (PPARγ–peroxisome proliferator-activated receptor γ) [198].”
From Endometriosis: Epidemiology, Classification, Pathogenesis, Treatment and Genetics (Review of Literature) (2021) · cites this paper as [198]
Estrogen receptors act as transcription factors and play a significant role in endometrial growth and differentiation and in numerous biological functions in eutopic endometrium and endometriosis.
“Estrogen receptors, acting as transcription factors, play a significant role in endometrial growth and differentiation, as well as in numerous biological functions in eutopic endometrium and endometriosis.”
From Endometriosis: Epidemiology, Classification, Pathogenesis, Treatment and Genetics (Review of Literature) (2021) · cites this paper as [198]
ERβ is the predominant isoform in patients with endometriosis.
“ERβ is the predominant isoform in patients with endometriosis [7,8].”
From Polymorphisms in the 3<a:math xmlns:a="http://www.w3.org/1998/Math/MathML" id="M1"> <a:msup> <a:mrow/> <a:mrow> <a:mo>′</a:mo> </a:mrow> </a:msup> </a:math>UTR Region of ESR2 and CYP19A1 Genes and Its Influence on Allele-Specific Gene Expression in Endometriosis (2020) · cites this paper as [7]
Symptoms occur after puberty and oestrogen action contributes to pathological processes including growth of lesions and inflammation, and to symptoms including pain.
“Symptoms occur after puberty and oestrogen action contributes to pathological processes including growth of lesions and inflammation, and to the symptoms including pain4142.”
From Meta-analysis identifies five novel loci associated with endometriosis highlighting key genes involved in hormone metabolism (2017) · cites this paper as [41]
Endometriosis is an oestrogen-dependent disease.
“Endometriosis is an oestrogen-dependent disease.”
From Meta-analysis identifies five novel loci associated with endometriosis highlighting key genes involved in hormone metabolism (2017) · cites this paper as [41]
Expression of estrogen receptor b (ER-b) is significantly higher in endometriosis due to hypermethylation of the CpG islands in the estrogen receptor 2 gene.
“Expression of estrogen receptor b (ER-b) is significantly higher in endometriosis due to the hypermethylation of the CpG islands in the estrogen receptor 2 gene.25,26”
From Altered genome-wide methylation in endometriosis (2014) · cites this paper as [25]
Cites
Cloning of a novel receptor expressed in rat prostate and ovary.
Kuiper, G. G. J. M., Enmark, E., Pelto‐Huikko, M., Nilsson, S., & Gustafsson, J.-Α. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.12.5925 · Cited by 4,792 · see citing works
Human oestrogen receptor cDNA: sequence, expression and homology to v-erb-A
Green, S., Walter, P., Kumar, V., Krust, A., Bornert, J., Argos, P., & Chambon, P. (1986) · Nature · doi:10.1038/320134a0 · Cited by 2,320 · see citing works
ERβ: Identification and characterization of a novel human estrogen receptor
Mosselman, S., Polman, J., & Dijkema, R. (1996) · FEBS Letters · doi:10.1016/0014-5793(96)00782-x · Cited by 2,269 · see citing works
Giudice, L. C. (2010) · New England Journal of Medicine · doi:10.1056/nejmcp1000274 · Cited by 1,924 · see citing works
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 · see citing works
Kastner, P., Krust, A., Turcotte, B., Stropp, U., Tora, L., Gronemeyer, H., & Chambon, P. (1990) · The EMBO Journal · doi:10.1002/j.1460-2075.1990.tb08280.x · Cited by 1,534 · cited 1× · see citing works
“46 49 Two major transcriptional start sites have been identi fi ed.”
BackgroundBurney, R. O., Talbi, S., Hamilton, A. E., Vo, K. C., Nyegaard, M., Nezhat, C. R., Lessey, B. A., & Giudice, L. C. (2007) · Endocrinology · doi:10.1210/en.2006-1692 · Cited by 735 · cited 1× · see citing works
“17,18 These fi ndings suggested that the eutopic endometrium of women with endometriosis exhibit the pathology found within endo-metriotic tissue.”
BackgroundGlobal gene profiling in human endometrium during the window of implantation
Kao, L. C., Tulac, S., Lobo, S., Imani, B., Yang, J. P., Germeyer, A., Osteen, K., Taylor, R. N., Lessey, B. A., & Giudice, L. C. (2002) · Endocrinology · doi:10.1210/endo.143.6.8885 · Cited by 727 · see citing works
Kao, L. C., Germeyer, A., Tulac, S., Lobo, S., Yang, J. P., Taylor, R. N., Osteen, K., Lessey, B. A., & Giudice, L. C. (2003) · Endocrinology · doi:10.1210/en.2003-0043 · Cited by 696 · see citing works
Bulun, S. E., Lin, Z., Imir, G., Amin, S., Demura, M., Yilmaz, B., Martin, R., Utsunomiya, H., Thung, S., Gurates, B., et al. (2005) · Pharmacological Reviews · doi:10.1124/pr.57.3.6 · Cited by 531 · cited 8× · see citing works
“26 The theca and granulosa cells of a preovulatory follicle convert cholesterol to estradiol that is actively secreted into the circulation in a cyclic fashion ( ► Fig.”
BackgroundInfluentialSelf-citationProgesterone Receptor Isoform A But Not B Is Expressed in Endometriosis
Attia, G. R. (2000) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.85.8.2897 · Cited by 488 · see citing works
Heritable aspects of endometriosis
Simpson, J. L., Elias, S., Malinak, L. R., & Buttram, V. C. (1980) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(80)90917-5 · Cited by 468 · see citing works
Endometriosis and pelvic pain: relation to disease stage and localization
Vercellini, P., Trespidi, L., De Giorgi, O., Cortesi, I., Parazzini, F., & Crosignani, P. G. (1996) · Fertility and Sterility · doi:10.1016/s0015-0282(16)58089-3 · Cited by 457 · see citing works
Progesterone resistance in endometriosis: link to failure to metabolize estradiol.
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 · cited 1× · see citing works
“6,33 The estradiol-receptor complex acts as a transcription factor that becomes associated with the promoters of estra-diol-responsive genes via direct DNA binding or binding to other docking transcription factors at basal promoter regions.”
BackgroundSelf-citationPromoter Methylation Regulates Estrogen Receptor 2 in Human Endometrium and Endometriosis1
Xue, Q., Lin, Z., Cheng, Y.-H., Huang, C.-C., Marsh, E., Yin, P., Milad, M. P., Confino, E., Reierstad, S., Innes, J., et al. (2007) · Biology of Reproduction · doi:10.1095/biolreprod.107.061804 · Cited by 346 · see citing works
Self-citationVercellini, P., Trespidi, L., Colombo, A., Vendola, N., Marchini, M., & Crosignani, P. G. (1993) · Fertility and Sterility · doi:10.1016/s0015-0282(16)56039-7 · Cited by 311 · see citing works
Zeitoun, K., Takayama, K., Sasano, H., Suzuki, T., Moghrabi, N., Andersson, S., Johns, A., Meng, L., Putman, M., Carr, B., et al. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.83.12.5301 · Cited by 308 · see citing works
Self-citationIncreased activation of pelvic macrophages in infertile women with mild endometriosis
Halme, J. K., Becker, S., Hammond, M. G., Raj, M. H. G., & Raj, S. (1983) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(83)90720-2 · Cited by 305 · see citing works
Deficient cellular immunity in endometriosis
Dmowski, W. P., Steele, R. W., & Baker, G. F. (1981) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(81)90598-6 · Cited by 302 · see citing works
Prostaglandin E2 Stimulates Aromatase Expression in Endometriosis-Derived Stromal Cells
Noble, L. S. (1997) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.82.2.600 · Cited by 301 · see citing works
Self-citationLESSONS IN ESTROGEN BIOLOGY FROM KNOCKOUT AND TRANSGENIC ANIMALS
Hewitt, S. C., Harrell, J. C., & Korach, K. S. (2004) · Annual Review of Physiology · doi:10.1146/annurev.physiol.67.040403.115914 · Cited by 292 · cited 1× · see citing works
“30 Despite its sensitivity to estrogen, endometriosis appears to contain a unique complement of steroid hormone receptors compared with that of its normal tissue counterpart, the eutopic endometrium.”
BackgroundEstrogen Receptor-β: Recent Lessons from in Vivo Studies
Harris, H. A. (2006) · Molecular Endocrinology · doi:10.1210/me.2005-0459 · Cited by 278 · see citing works
Aromatase: a key molecule in the pathophysiology of endometriosis and a therapeutic target
Zeitoun, K. M., & Bulun, S. E. (1999) · Fertility and Sterility · doi:10.1016/s0015-0282(99)00393-3 · Cited by 256 · cited 1× · 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-citationHornung, D., Ryan, I. P., Chao, V. A., Vigne, J., Schriock, E. D., & Taylor, R. N. (1997) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.82.5.3919 · Cited by 238 · see citing works
Savouret, J., Bailly, A., Misrahi, M., Rauch, C., Redeuilh, G., Chauchereau, A., & Milgröm, E. (1991) · The EMBO Journal · doi:10.1002/j.1460-2075.1991.tb07713.x · Cited by 232 · see citing works
Progestins for symptomatic endometriosis: a critical analysis of the evidence
Vercellini, P., Cortesi, I., & Crosignani, P. G. (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)00193-3 · Cited by 229 · cited 1× · 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.”
BackgroundRead, L. D., Snider, C. E., Miller, J. S., Greene, G. L., & Katzeneilenbogen, B. S. (1988) · Molecular Endocrinology · doi:10.1210/mend-2-3-263 · Cited by 211 · cited 1× · see citing works
“46 49 Two major transcriptional start sites have been identi fi ed.”
BackgroundAttar, E., Tokunaga, H., Imir, G., Yilmaz, M. B., Redwine, D., Putman, M., Gurates, B., Attar, R., Yaegashi, N., Hales, D. B., et al. (2009) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2008-1180 · Cited by 207 · cited 1× · see citing works
“36 We recently used real-time polymerase chain reaction (RT-PCR) to compare tissue mRNA levels of these key nuclear receptors in endometriosis and eutopic endometrium ( ► Fig.”
MethodSelf-citationProgesterone Receptor Isoform A But Not B Is Expressed in Endometriosis1
Attia, G. R., Zeitoun, K., Edwards, D., Johns, A., Carr, B. R., & Bulun, S. E. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.8.6739 · Cited by 193 · see citing works
Self-citationNardulli, A. M., Greene, G. L., O’Malley, B. W., & Katzenellenbogen, B. S. (1988) · Endocrinology · doi:10.1210/endo-122-3-935 · Cited by 189 · see citing works
Wei, L. L., Krett, N. L., Francis, M. D., Gordon, D. F., Wood, W. M., O’Malley, B. W., & Horwitz, K. B. (1988) · Molecular Endocrinology · doi:10.1210/mend-2-1-62 · Cited by 187 · see citing works
Petz, L. N., & Nardulli, A. M. (2000) · Molecular Endocrinology · doi:10.1210/mend.14.7.0493 · Cited by 180 · see citing works
Matthews, J. B., Wihlén, B., Tujague, M., Wan, J., Ström, A., & Gustafsson, J.-Α. (2005) · Molecular Endocrinology · doi:10.1210/me.2005-0140 · Cited by 179 · see citing works
Peritoneal Macrophages From Patients With Endometriosis Release Growth Factor Activityin Vitro*
Halme, J. K., WHITE, C., Kauma, S. W., Estes, J. E., & Haskill, S. (1988) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-66-5-1044 · Cited by 179 · see citing works
Dendritic cell populations in the eutopic and ectopic endometrium of women with endometriosis
Schulke, L., Berbic, M., Manconi, F., Tokushige, N., Markham, R., & Fraser, I. S. (2009) · Human Reproduction · doi:10.1093/humrep/dep071 · Cited by 176 · see citing works
Brandenberger, A. W. (1999) · Molecular Human Reproduction · doi:10.1093/molehr/5.7.651 · Cited by 165 · see citing works
Kennedy, S., Mardon, H., & Barlow, D. (1995) · Journal of Assisted Reproduction and Genetics · doi:10.1007/bf02214126 · Cited by 157 · see citing works
Trukhacheva, E., Lin, Z., Reierstad, S., Cheng, Y.-H., Milad, M., & Bulun, S. E. (2009) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2008-1466 · Cited by 143 · see citing works
Self-citationPetz, L. N., Ziegler, Y., Schultz, J. R., Kim, H., Kemper, J. K., & Nardulli, A. M. (2004) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2003.11.008 · Cited by 142 · see citing works
Petz, L. N., Ziegler, Y., Loven, M. A., & Nardulli, A. M. (2002) · Endocrinology · doi:10.1210/en.2002-220369 · Cited by 133 · see citing works
Expression of oestrogen receptor-alpha and -beta in ovarian endometriomata
Fujimoto, J. (1999) · Molecular Human Reproduction · doi:10.1093/molehr/5.8.742 · Cited by 123 · see citing works
Osteen, K. G., Bruner-Tran, K. L., & Eisenberg, E. (2005) · Fertility and Sterility · doi:10.1016/j.fertnstert.2004.11.026 · Cited by 122 · cited 1× · see citing works
“17,19 This abnormal pattern of gene expression could also be traced to primary stromal cells isolated from endometriotic tissue, eutopic endometrium from endo-metriosis, and eutopic endometrium from disease-free women.”
BackgroundEstrogen receptor α and Sp1 regulate progesterone receptor gene expression
Schultz, J. R., Petz, L. N., & Nardulli, A. M. (2003) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(02)00415-x · Cited by 121 · see citing works
Bergman, M. D., Schachter, B. S., Karelus, K., Combatsiaris, E. P., Garcia, T., & Nelson, J. F. (1992) · Endocrinology · doi:10.1210/endo.130.4.1547720 · Cited by 105 · cited 1× · see citing works
“39 It is quite likely that estradiol also plays a key role in regulating ER α expression in human endometrial stromal cells.”
BackgroundSchultz, J. R., Petz, L. N., & Nardulli, A. M. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m407879200 · Cited by 105 · see citing works
Grandien, K., Bäckdahl, M., Ljunggren, Ö., Gustafsson, J., & Berkenstam, A. L. (1995) · Endocrinology · doi:10.1210/endo.136.5.7720671 · Cited by 103 · see citing works
Grandien, K. (1996) · Molecular and Cellular Endocrinology · doi:10.1016/0303-7207(95)03716-0 · Cited by 100 · see citing works
Lin, Z., Reierstad, S., Huang, C.-C., & Bulun, S. E. (2007) · Cancer Research · doi:10.1158/0008-5472.can-06-3696 · Cited by 93 · see citing works
Self-citationPetz, L. N., Ziegler, Y., Schultz, J. R., & Nardulli, A. M. (2003) · Molecular Endocrinology · doi:10.1210/me.2003-0105 · 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 · cited 1× · see citing works
“37 This review covers primarily ER β expression and action in endometriosis.”
BackgroundSelf-citationSelective Promoter Usage of the Human Estrogen Receptor-α Gene and Its Regulation by Estrogen
Donaghue, C., Westley, B. R., & May, F. E. B. (1999) · Molecular Endocrinology · doi:10.1210/mend.13.11.0366 · Cited by 72 · see citing works
Scott, R. E. M., Wu-Peng, X. S., Yen, P. M., Chin, W. W., & Pfaff, D. W. (1997) · Molecular Endocrinology · doi:10.1210/mend.11.11.0003 · Cited by 63 · see citing works
Long-Range Transcriptional Control of Progesterone Receptor Gene Expression
Bonéy-Montoya, J., Ziegler, Y., Curtis, C. D., Montoya, J. A., & Nardulli, A. M. (2009) · Molecular Endocrinology · doi:10.1210/me.2009-0429 · Cited by 56 · cited 2× · see citing works
“45 Our unpublished observations suggest that a reduction in the ER α -to-ER β ratio in endometrial stromal cells diminishes estradiol induction of PR expression.”
BackgroundPetz, L. N. (2000) · Molecular Endocrinology · doi:10.1210/me.14.7.972 · Cited by 55 · see citing works
Aromatase inhibition for refractory endometriosis-related chronic pelvic pain
Abushahin, F., Goldman, K. N., Barbieri, E., Milad, M. P., RADEMAKER, A. W., & Bulun, S. E. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2011.07.1136 · Cited by 53 · cited 2× · see citing works
“12 Patients often develop resistance to repeated treatments with the same agent over a period of 6 months to 3 years.”
BackgroundSelf-citationGrandien, K., Berkenstam, A. L., Nilsson, S., & Gustafsson, J.-Å. (1993) · Journal of Molecular Endocrinology · doi:10.1677/jme.0.0100269 · Cited by 51 · see citing works
Osteen, K. G., Bruner‐Tran, K. L., Keller, N. R., & Eisenberg, E. (2002) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2002.tb02764.x · Cited by 44 · see citing works
Su, E. J., Lin, Z.-H., Zeine, R. R., Yin, P., Reierstad, S., Innes, J. E., & Bulun, S. E. (2009) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2009.01.025 · Cited by 37 · cited 3× · see citing works
“59,60 Because COX2 expression is also severely higher in endo-metriotic versus endometrial tissues and cells, it is tempting to speculate that ER β is at least in part responsible for high COX2 levels and prostaglandin biosynthesis in endometriosis ( ► Fig.”
BackgroundSelf-citationSu, E. J., Ernst, L. M., Abdallah, N., Chatterton, R. T., Xin, H., Monsivais, D., Coon, J. S., & Bulun, S. E. (2011) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2011-1084 · Cited by 27 · see citing works
Self-citationMontano, M. M., Kraus, W. L., & Katzenellenbogen, B. S. (1997) · Molecular Endocrinology · doi:10.1210/mend.11.3.9899 · Cited by 19 · see citing works
Montano, M. M. (1997) · Molecular Endocrinology · doi:10.1210/me.11.3.330 · Cited by 9 · see citing works
Attar, E., Tokunaga, H., İmir, G., Yılmaz, M. B., Redwine, D. B., Putman, M., Gürateş, B., Attar, R., Yaegashi, N., Hales, D. B., et al. (2009) · Molecular Endocrinology · doi:10.1210/mend.23.1.9997 · Cited by 8 · see citing works
Self-citation
Flagged first, then by citations
11 of the 73 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Zondervan, K. T., Becker, C. M., & Missmer, S. A. (2020) · New England Journal of Medicine · doi:10.1056/nejmra1810764 · Cited by 2,249 · see citing works
Endometriosis: pathogenesis and treatment
Vercellini, P., Viganò, P., Somigliana, E., & Fedele, L. (2014) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2013.255 · Cited by 1,940 · see citing works
Bulun, S. E., Yilmaz, B. D., Sison, C., Miyazaki, K., Bernardi, L., Liu, S., Kohlmeier, A., Yin, P., Milad, M., & Wei, J. (2019) · Endocrine Reviews · doi:10.1210/er.2018-00242 · Cited by 844 · see citing works
Self-citationThe Immunopathophysiology of Endometriosis
Symons, L. K., Miller, J. E., Kay, V. R., Marks, R. M., Liblik, K., Koti, M., & Tayade, C. (2018) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2018.07.004 · Cited by 583 · see citing works
Smolarz, B., Szyłło, K., & Romanowicz, H. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms221910554 · Cited by 560 · see citing works
The Pathogenesis of Endometriosis: Molecular and Cell Biology Insights
Laganà, A. S., Garzon, S., Götte, M., Viganò, P., Franchi, M. P., Ghezzi, F., & Martin, D. C. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20225615 · Cited by 492 · see citing works
“Conversely, ERβwas reported overexpressed, determining an inversion of ERβ to ERα ratio as compared to eutopic endometrium [91].”
BackgroundThe Origin and Pathogenesis of Endometriosis
Wang, Y., Nicholes, K., & Shih, I. (2019) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathmechdis-012419-032654 · Cited by 466 · see citing works
Han, S. J., Jung, S. Y., Wu, S.-P., Hawkins, S. M., Park, M. J., Kyo, S., Qin, J., Lydon, J. P., Tsai, S. Y., Tsai, M.-J., et al. (2015) · Cell · doi:10.1016/j.cell.2015.10.034 · Cited by 380 · see citing works
Sanchez, A. M., Viganò, P., Somigliana, E., Panina-Bordignon, P., Vercellini, P., & Candiani, M. (2014) · Human Reproduction Update · doi:10.1093/humupd/dmt053 · Cited by 357 · see citing works
“…and mutations; (ii) an altered steroid hormone balance or responsiveness as estrogens have been linked to the pathogenesis of gynecological cancers (Bulun et al., 2012); (iii) iron-associated oxidative stress, currently considered the most important trigger, being able to attack ‘fragile’ sites in…”
BackgroundSapkota, Y., Steinthorsdottir, V., Morris, A. P., Fassbender, A., Rahmioglu, N., De Vivo, I., Buring, J. E., Zhang, F., Edwards, T. L., Jones, S., et al. (2017) · Nature Communications · doi:10.1038/ncomms15539 · Cited by 344 · see citing works
Hormonal treatments for endometriosis: The endocrine background
Vannuccini, S., Clemenza, S., Rossi, M., & Petraglia, F. (2022) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-021-09666-w · Cited by 336 · see citing works
“In terms of alterations in ERs activity, an overexpression of ERβ and a downregulation of ERα [39, 40] have been observed in endometriosis.”
BackgroundEstrogen Receptors and Endometriosis
Chantalat, É., Valera, M., Vaysse, C., Noirrit‐Esclassan, E., Rusidzé, M., Weyl, A., Vergriete, K., Buscail, É., Lluel, P., Fontaine, C., et al. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21082815 · Cited by 315 · see citing works
Endometriosis: hormone regulation and clinical consequences of chemotaxis and apoptosis
dos Reis, F. M., Petraglia, F., & Taylor, R. N. (2013) · Human Reproduction Update · doi:10.1093/humupd/dmt010 · Cited by 273 · see citing works
“One of the putative factors responsible for higher Akt phosphorylation in endometriotic cells may be the continuous local stimulation of ERs due to intralesional production of estradiol, as suggested by studies showing local expression of aromatase (Bulun et al., 2012).”
BackgroundEndometriosis and nuclear receptors
Yilmaz, B. D., & Bulun, S. E. (2019) · Human Reproduction Update · doi:10.1093/humupd/dmz005 · Cited by 243 · see citing works
“…PGR isoforms increase throughout the proliferative phase and peak before ovulation under the influence of increasing estrogen levels; in endometriosis, PGR levels remain very low to undetectable, possibly due to an abnormally low ESR1: ESR2 ratio in endometriotic stromal cells (Bulun et al., 2012).”
BackgroundSelf-citationEstrogen Receptor Function: Impact on the Human Endometrium
Yu, K., Huang, Z., Xu, X.-L., Li, J., Fu, X., & Deng, S. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.827724 · Cited by 236 · see citing works
“Compared with endometrial tissue, ERb mRNA and protein levels were more than 100-fold increased, while the levels of ERa were several times lower (98); inhibiting the enhanced ERb activity via an”
BackgroundPathogenetic Mechanisms of Deep Infiltrating Endometriosis
Tosti, C., Pinzauti, S., Santulli, P., Chapron, C., & Petraglia, F. (2015) · Reproductive Sciences · doi:10.1177/1933719115592713 · Cited by 222 · see citing works
“Endometriosis cells highly express vascular endothelial growth factor (VEGF) and this is increased in red vascular peritoneal endometriotic lesions compared to older black or white scarred lesions.49 The angiogenic characteristics of endometriotic lesions appear to differ between SPE, OMA, and DIE.”
BackgroundInfluentialPirtea, P., Cicinelli, E., Nola, R. D., de Ziegler, D., & Ayoubi, J. M. (2021) · Fertility and Sterility · doi:10.1016/j.fertnstert.2020.12.010 · Cited by 226 · see citing works
Dyson, M. T., Roqueiro, D., Monsivais, D., Ercan, C. M., Pavone, M. E., Brooks, D. C., Kakinuma, T., Ono, M., Jafari, N., Dai, Y., et al. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004158 · Cited by 211 · see citing works
Self-citationPeripheral changes in endometriosis-associated pain
Morotti, M., Vincent, K., Brawn, J., Zondervan, K. T., & Becker, C. M. (2014) · Human Reproduction Update · doi:10.1093/humupd/dmu021 · Cited by 198 · see citing works
“Estrogens have been shown to support the growth and inflammation processes in endometriotic lesions (Bulun et al., 2012).”
Regulation of Inflammation Pathways and Inflammasome by Sex Steroid Hormones in Endometriosis
García-Gómez, E., Vázquez-Martínez, E. R., Reyes-Mayoral, C., Cruz-Orozco, O., Camacho‐Arroyo, I., & Cerbón, M. A. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00935 · Cited by 198 · see citing works
“Recently, to investigate the role of non-genomic activation of ER-β in this disease, a mouse model of surgically induced endometriosis was used through autotransplantation of fragments of endometrial tissue in the peritoneal cavity, both in mice with overexpression of ER-β (ERβ-OE) and in ERβ-null mice.”
BackgroundInfluentialGreaves, E., Cousins, F., Murray, A., Esnal-Zufiaurre, A., Fassbender, A., Horne, A., & Saunders, P. (2014) · American Journal of Pathology · doi:10.1016/j.ajpath.2014.03.011 · Cited by 170 · see citing works
Endometriosis: where are we and where are we going?
Greene, A. D., Lang, S. A., Kendziorski, J. A., Sroga-Rios, J. M., Herzog, T. J., & Burns, K. A. (2016) · Reproduction · doi:10.1530/rep-16-0052 · Cited by 187 · see citing works
Dual suppression of estrogenic and inflammatory activities for targeting of endometriosis
Zhao, Y., Gong, P., Chen, Y., Nwachukwu, J. C., Srinivasan, S., Ko, C., Bagchi, M. K., Taylor, R. N., Korach, K. S., Nettles, K. W., et al. (2015) · Science Translational Medicine · doi:10.1126/scitranslmed.3010626 · Cited by 170 · see citing works
Epithelial-to-mesenchymal transition in the development of endometriosis
Yang, Y., & Yang, W. (2017) · Oncotarget · doi:10.18632/oncotarget.16472 · Cited by 167 · see citing works
“In the previous studies, people believed that whether of ovarian or peritoneal locations, had higher ERβ expression rather than ERα compared with normal human endometrial cells [48], which was similarly detected in many animal models of endometriosis [49, 50].”
ResultLocal and Systemic Factors and Implantation: what is the Evidence?
Fox, C., Morin, S., Jeong, J., Scott, R., & Lessey, B. (2016) · Fertility and Sterility · doi:10.1016/j.fertnstert.2016.02.018 · Cited by 146 · see citing works
Cyclooxygenase-2 in Endometriosis
Lai, Z., Yang, H., Ha, S., Chang, K., Mei, J., Zhou, W.-J., Qiu, X., Wang, X.-Q., Zhu, R., Li, D., et al. (2019) · International Journal of Biological Sciences · doi:10.7150/ijbs.35128 · Cited by 165 · see citing works
Diet and endometriosis risk: A literature review
Parazzini, F., Viganò, P., Candiani, M., & Fedele, L. (2013) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2012.12.011 · Cited by 165 · see citing works
The management of menopause in women with a history of endometriosis: A systematic review
Gemmell, L. C., Webster, K. E., Kirtley, S., Vincent, K., Zondervan, K. T., & Becker, C. M. (2017) · Human Reproduction Update · doi:10.1093/humupd/dmx011 · Cited by 154 · see citing works
“This expression profile results in locally elevated levels of the biologically active form of oestrogen (oestradiol) (Kitawaki et al., 2002; Bulun et al., 2012).”
BackgroundBurns, K. A., Rodriguez, K., Hewitt, S., Janardhan, K., Young, S., & Korach, K. (2012) · Endocrinology · doi:10.1210/en.2012-1294 · Cited by 143 · see citing works
Estrogen receptor β: the guardian of the endometrium
Hapangama, D. K., Kamal, A. M., & Bulmer, J. N. (2015) · Human Reproduction Update · doi:10.1093/humupd/dmu053 · Cited by 145 · see citing works
Gou, Y., Li, X., Li, P., Zhang, H., Xu, T., Wang, H., Wang, B., Ma, X., Xue, J., & Zhang, Z. (2019) · Human Reproduction · doi:10.1093/humrep/dez019 · Cited by 133 · see citing works
Di-(2-ethylhexyl)-phthalate induces oxidative stress in human endometrial stromal cells in vitro
Cho, Y. J., Park, S. B., & Han, M. S. (2015) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2015.03.003 · Cited by 130 · see citing works
Treatment of pain associated with deep endometriosis: alternatives and evidence
Ferrero, S., Alessandri, F., Racca, A., & Maggiore, U. L. R. (2015) · Fertility and Sterility · doi:10.1016/j.fertnstert.2015.08.031 · Cited by 124 · see citing works
Proestling, K., Birner, P., Gamperl, S., Nirtl, N., Márton, E., Yerlikaya‐Schatten, G., Wenzl, R. J., Streubel, B., & Husslein, H. (2015) · Reproductive Biology and Endocrinology · doi:10.1186/s12958-015-0063-7 · Cited by 116 · see citing works
Zhou, S., Yi, T., Liu, R., Bian, C., Qi, X., He, X., Wang, K., Li, J., Zhao, X., Huang, C., et al. (2012) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m112.017988 · Cited by 113 · see citing works
The Role of Peritoneal Macrophages in Endometriosis
Ramírez-Pavez, T. N., Martinez‐Esparza, M., Ruiz‐Alcaraz, A. J., Marín‐Sánchez, P., Machado‐Linde, F., & García–Peñarrubia, P. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms221910792 · Cited by 113 · see citing works
“This, in conjunction with the increased expression of ERβ [127] in both ovarian and peritoneal lesions, could over-activate estrogen-dependent signaling pathways in endometrial tissues, stimulating its corresponding biological effects.”
BackgroundLiu, X., Zhang, Q., & Guo, S.-W. (2018) · Reproductive Sciences · doi:10.1177/1933719117718275 · Cited by 110 · see citing works
Ovarian hormones-autophagy-immunity axis in menstruation and endometriosis
Shen, H., Zhang, T., Yang, H., Lai, Z., Zhou, W., Mei, J., Shi, J., Zhu, R., Xu, F., Li, D., et al. (2021) · Theranostics · doi:10.7150/thno.55241 · Cited by 107 · see citing works
Han, S. J., & O’Malley, B. W. (2014) · Human Reproduction Update · doi:10.1093/humupd/dmu002 · Cited by 98 · see citing works
“Interestingly, elevated ERb enhances progesterone resistance in endometriotic tissues (Bulun et al., 2012).”
BackgroundIs it time for a paradigm shift in drug research and development in endometriosis/adenomyosis?
Guo, S., & Groothuis, P. G. (2018) · Human Reproduction Update · doi:10.1093/humupd/dmy020 · Cited by 93 · see citing works
“…investigators demonstrated that ERβ expression is strongly elevated in endometriotic tissue as a result of demethylation of the gene promoter region (Bulun et al., 2012), and that ERβ, binding to estradiol with the same affinity as ERα, could be a key player in the pathophysiology of endometriosis.”
BackgroundThree Types of Endometriosis: Pathogenesis, Diagnosis and Treatment. State of the Art
Imperiale, L., Nisolle, M., Noël, J., & Fastrez, M. (2023) · Journal of Clinical Medicine · doi:10.3390/jcm12030994 · Cited by 99 · see citing works
“Endometriotic lesions show an increased expression of aromatase, estrogen receptor β, and steroidogenic acute regulatory protein [16] and decreased expression of 17β-hydroxysteroid dehydrogenase 2 [17].”
BackgroundHammarstrand, S., Jakobsson, K., Andersson, E., Xu, Y., Li, Y., Olovsson, M. H., & Andersson, E. M. (2021) · Environment International · doi:10.1016/j.envint.2021.106819 · Cited by 90 · see citing works
“Whereas both uterine leiomyoma and endometriosis are estrogen-dependent diseases (Borahay et al., 2017; Bulun et al., 2012), PCOS is characterized by an excess of androgens, in particular testosterone (Escobar-Morreale 2018).”
BackgroundJones, R. L., Tanadini‐Lang, S., Kendziorski, J. A., Greene, A., & Burns, K. A. (2018) · Environmental Health Perspectives · doi:10.1289/ehp3802 · Cited by 88 · see citing works
“We further examined expression levels of genes known to be involved in endometriosis (Bukulmez et al. 2008; Bulun et al. 2012; Chang et al. 2011; Osteen et al. 2003): Estrogen Receptor 1 and 2 ( Esr1, Esr2 ), Matrix Metallopeptidase 9 ( Mmp9 ), Matrix Metallopepti-dase 7 ( Mmp7 ), and Mucin 4 (…”
Li, Y., Adur, M. K., Kannan, A., Dávila, J., Zhao, Y., Nowak, R. A., Bagchi, M. K., Bagchi, I. C., & Li, Q. (2016) · PLoS ONE · doi:10.1371/journal.pone.0165347 · Cited by 88 · see citing works
Aromatase and endometriosis: estrogens play a role
Ferrero, S., Remorgida, V., Maganza, C., Venturini, P. L., Salvatore, S., Papaleo, E., Candiani, M., & Maggiore, U. L. R. (2014) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12411 · Cited by 84 · see citing works
Exploring diagnostic m6A regulators in endometriosis
Jiang, L., Zhang, M., Wu, J., Wang, S., Xiang, Y., Yi, M., Zhang, X., & Fang, X. (2020) · Aging · doi:10.18632/aging.202163 · Cited by 83 · see citing works
“However, the ‘protagonist’ in EMs is thought to be ESR2 (ESRβ); the preferential expression of this gene would reduce the expression level of ESR1 in endometriotic stromal cells [32].”
BackgroundEndometriosis-Associated Angiogenesis and Anti-angiogenic Therapy for Endometriosis
Chung, M. S., & Han, S. J. (2022) · Frontiers in Global Women s Health · doi:10.3389/fgwh.2022.856316 · Cited by 89 · see citing works
“Furthermore, women with endometriosis display significantly elevated levels of ERβ in ovarian endometrioma when compared to normal endometrium (125).”
BackgroundRole of nuclear receptors in blastocyst implantation
Vasquez, Y. M., & DeMayo, F. J. (2013) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2013.08.004 · Cited by 82 · see citing works
Altered genome-wide methylation in endometriosis
Naqvi, H., Ilagan, Y., Krikun, G., & Taylor, H. S. (2014) · Reproductive Sciences · doi:10.1177/1933719114532841 · Cited by 82 · see citing works
“Expression of estrogen receptor b (ER-b) is significantly higher in endometriosis due to the hypermethylation of the CpG islands in the estrogen receptor 2 gene.(25,26) Higher expression of estrogen receptor amplifies estrogenic effects and the proliferative capacity of endometrial cells.”
BackgroundPolyphenols as a Diet Therapy Concept for Endometriosis—Current Opinion and Future Perspectives
Gołąbek-Grenda, A., Kowalska, K., & Olejnik, A. M. (2021) · Nutrients · doi:10.3390/nu13041347 · Cited by 93 · see citing works
“These are ovaries, which primarily convert cholesterol to estradiol and secrete it periodically into the circulation, peripheral tissues such as the adipose tissue and skin, that convert androstenedione to estrone in relatively small quantities, and endometriotic tissue, synthesizing de novo high amounts of estradiol…”
BackgroundIncreased Association Between Endometriosis and Endometrial Cancer
Yu, H.-C., Lin, C.-Y., Chang, W., Shen, B., Chang, W.-P., & Chuang, C.-M. (2015) · International Journal of Gynecological Cancer · doi:10.1097/igc.0000000000000384 · Cited by 79 · see citing works
Daidzein-rich isoflavone aglycones inhibit cell growth and inflammation in endometriosis
Takaoka, O., Mori, T., Ito, F., Okimura, H., Kataoka, H., Tanaka, Y., Koshiba, A., Kusuki, I., Shigehiro, S., Amami, T., et al. (2018) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2018.04.004 · Cited by 81 · see citing works
Minireview: Steroid-Regulated Paracrine Mechanisms Controlling Implantation
Pawar, S., Hantak, A. M., Bagchi, I. C., & Bagchi, M. K. (2014) · Molecular Endocrinology · doi:10.1210/me.2014-1074 · Cited by 78 · see citing works
“Bulun et al (103) have shown that specific steroid hormone receptor isoforms are differentially regulated in stromal cells isolated from normal and endometriotic tissue.”
BackgroundRole of Oxidative Stress in Epigenetic Modification in Endometriosis
Ito, F., Yamada, Y., 重光, 愛., Akinishi, M., Kaniwa, H., Miyake, R., Yamanaka, S., & Kobayashi, H. (2017) · Reproductive Sciences · doi:10.1177/1933719117704909 · Cited by 79 · see citing works
Challenges in endometriosis miRNA studies — From tissue heterogeneity to disease specific miRNAs
Saare, M., Rekker, K., Laisk, T., Rahmioğlu, N., Zondervan, K. T., Salumets, A., Götte, M., & Peters, M. (2017) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2017.06.018 · Cited by 76 · see citing works
da Silva, D. M., Gross, L. A., Neto, E. D. P. G., Lessey, B. A., & Savaris, R. F. (2017) · Journal of the Endocrine Society · doi:10.1210/js.2017-00053 · Cited by 81 · 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
MAP kinases and the inflammatory signaling cascade as targets for the treatment of endometriosis?
Santulli, P., Marcellin, L., Tosti, C., Chouzenoux, S., Cerles, O., Borghese, B., Batteux, F., & Chapron, C. (2015) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728222.2015.1090974 · Cited by 75 · see citing works
Estradiol promotes EMT in endometriosis via MALAT1/miR200s sponge function
Du, Y., Zhang, Z., Xiong, W., Li, N., Liu, H., He, H., Li, Q., Liu, Y., & Zhang, L. (2018) · Reproduction · doi:10.1530/rep-18-0424 · Cited by 73 · see citing works
Bruner‐Tran, K. L., Mokshagundam, S., Herington, J. L., Ding, T., & Osteen, K. G. (2018) · Current Women s Health Reviews · doi:10.2174/1573404813666170921162041 · Cited by 77 · see citing works
The role of mitogen‐activated protein kinase signaling pathway in endometriosis
Bora, G., & Yaba, A. (2021) · Journal of obstetrics and gynaecology research · doi:10.1111/jog.14710 · Cited by 73 · see citing works
Transvaginal Elastosonography as an Imaging Technique for Diagnosing Adenomyosis
Liu, X., Ding, D., Ren, Y., & Guo, S. (2018) · Reproductive Sciences · doi:10.1177/1933719117750752 · Cited by 78 · see citing works
Zhang, B., Zhou, W., Gu, C., Wu, K., Yang, H., Mei, J., Yu, J.-J., Hou, X.-F., Sun, J., Xu, F., et al. (2018) · Cell Death and Disease · doi:10.1038/s41419-018-0581-2 · Cited by 72 · see citing works
Endometriosis and cardiovascular disease
Marchandot, B., Curtiaud, A., Matsushita, K., Trimaille, A., Host, A., Faller, É., Garbin, O., Akladios, C. Y., Jesel, L., & Morel, O. (2022) · European Heart Journal Open · doi:10.1093/ehjopen/oeac001 · Cited by 72 · see citing works
NLRP3 inflammasome: a new therapeutic target for high-risk reproductive disorders?
Zhou, F., Li, C., & Zhang, S. (2020) · Chinese Medical Journal · doi:10.1097/cm9.0000000000001214 · Cited by 70 · see citing works
Endometriosis: Update of Pathophysiology, (Epi) Genetic and Environmental Involvement
Monnin, N., Fattet, A.-J., & Koscinski, I. (2023) · Biomedicines · doi:10.3390/biomedicines11030978 · Cited by 67 · see citing works
“ESR and SF-1 receptors epigenetic modifications in endometriosis [4,22,23].”
BackgroundEndometriosis and the Fallopian Tubes: Theories of Origin and Clinical Implications
Hill, C. J., Fakhreldin, M., Maclean, A., Dobson, L., Nancarrow, L., Bradfield, A., Choi, F., Daley, D., Tempest, N., & Hapangama, D. K. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9061905 · Cited by 66 · see citing works
“The pathological overexpression of ERβ, considered to be the result of deficient methylation of the ERβ promoter, stimulates both inflammation [44,45] and loss of PR expression [46].”
BackgroundEndometrial 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
“Examples include epithelial cell expression of AR in endometrial cancers [26] and upregulation of ERbeta in endometriosis [35].”
BackgroundThe known, the unknown and the future of the pathophysiology of endometriosis
Ochoa Bernal, M. A., & Fazleabas, A. T. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25115815 · Cited by 59 · see citing works
“…of ESR2 in human Several studies have reported lower levels of ESR1 and higher levels of ESR2 in human endometriotic tissues and primary stromal cells compared with endometrial tissue and cells [55]. endometriotic tissues and primary stromal cells compared with endometrial tissue and cells [55].”
BackgroundPaola, R. D., Fusco, R., Gugliandolo, E., Crupi, R., Evangelista, M., Granese, R., & Cuzzocrea, S. (2016) · Frontiers in Pharmacology · doi:10.3389/fphar.2016.00382 · Cited by 59 · see citing works
“…tissue of patients affected by disease; in particular elevated expression of Extrogen receptor β is predicted to play a role in the development of endometriosis; probably, it contributes to the resistance to progesterone action in some of patients suffering from endometriosis (Bulun et al., 2012).”
BackgroundNothnick, W. B., & Alali, Z. (2016) · F1000Research · doi:10.12688/f1000research.7504.1 · Cited by 55 · see citing works
Stress, pain, anxiety, and depression in endometriosis–Targeting glial activation and inflammation
Mokhtari, T., Irandoost, E., & Sheikhbahaei, F. (2024) · International Immunopharmacology · doi:10.1016/j.intimp.2024.111942 · Cited by 56 · see citing works
Structure, Function, and Evaluation of the Female Reproductive Tract
Lessey, B. A., & Young, S. L. (2019) · Elsevier eBooks · doi:10.1016/b978-0-323-47912-7.00009-3 · Cited by 58 · see citing works
Colón-Caraballo, M., García, M., Mendoza, A., & Flores, I. (2018) · Applied immunohistochemistry & molecular morphology · doi:10.1097/pai.0000000000000663 · Cited by 52 · see citing works
Amaya, S. C., Savaris, R. F., Filipovic, C. J., Wise, J. D., Hestermann, E. V., Young, S. L., & Lessey, B. A. (2014) · Reproductive Sciences · doi:10.1177/1933719114525271 · Cited by 54 · see citing works
Epigenetic Modulation of Collagen 1A1: Therapeutic Implications in Fibrosis and Endometriosis1
Zheng, Y., Khan, Z., Zanfagnin, V., Correa, L. F., Delaney, A. A., & Daftary, G. S. (2016) · Biology of Reproduction · doi:10.1095/biolreprod.115.138115 · Cited by 50 · see citing works
Endometriosis and autoimmunity
Blanco, L. P., Salmeri, N., Temkin, S. M., Shanmugam, V. K., & Stratton, P. (2025) · Autoimmunity Reviews · doi:10.1016/j.autrev.2025.103752 · Cited by 55 · see citing works
Epigenetic Factors in Eutopic Endometrium in Women with Endometriosis and Infertility
Adamczyk, M., Wender-Ożegowska, E., & Kędzia, M. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23073804 · Cited by 48 · see citing works
“Endometriotic implants comprise stromal cells whose epigenetic pattern is similar to the phenotype of thecal and granulosa ovarian cells and tissue macrophages [64,65].”
Vercellini, P., Bandini, V., Viganò, P., Stefano, G. D., Merli, C. E. M., & Somigliana, E. (2023) · Human Reproduction · doi:10.1093/humrep/dead229 · Cited by 49 · see citing works
“…in endometriosis, as E2 is crucial for endometrial gland survival, with subsequent production of a number of inflammatory molecules leading to peritoneal and subperitoneal tissue remodelling, adhesions, and fibrosis (Bulun et al. , 2012, 2019; Reis et al. , 2013; Clemenza et al. , 2022).”
Reversal of fortune: estrogen receptor-β in endometriosis
Simmen, R. C. M., & Kelley, A. S. (2016) · Journal of Molecular Endocrinology · doi:10.1530/jme-16-0080 · Cited by 46 · see citing works
“locations, display higher ERβ expression compared with normal human endometrial cells; this was not shown for ERα (Bulun et al. 2012).”
BackgroundCao, Y., Zhuang, M., Yang, Y., et al. (2014) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2014/781684 · Cited by 45 · see citing works
“The past researches suggested that estrogen took effect only through the single and classic ERα, and with the discovery of ERβ, more evidence indicates that the pathophysiology mechanism of estrogen to target cells is regulated by ERα and ERβ [12].”
BackgroundLe, N., Cregger, M. A., Brown, V. A., de Mola, J. R. L., Bremer, P., Nguyen, L., Groesch, K. A., Wilson, T. S., Díaz‐Sylvester, P., & Braundmeier‐Fleming, A. (2021) · PLoS ONE · doi:10.1371/journal.pone.0261362 · Cited by 45 · see citing works
Liao, T.-L., Lee, Y.-C., Tzeng, C.-R., Wang, Y.-P., Chang, H.-Y., Lin, Y.-F., & Kao, S.-H. (2019) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2019.01.022 · Cited by 44 · see citing works
Role of tight junctions in signal transduction: an update
Takano, K., Kojima, T., Sawada, N., & Himi, T. (2014) · Europe PMC (PubMed Central) · doi:10.17877/de290r-7042 · Cited by 44 · see citing works
“tors (Bulun et al., 2012).”
BackgroundDysfunctional signaling underlying endometriosis: current state of knowledge
Cho, Y. J., Lee, S. H., Park, J. W., Han, M. S., Park, M. J., & Han, S. J. (2018) · Journal of Molecular Endocrinology · doi:10.1530/jme-17-0227 · Cited by 48 · see citing works
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
Kobayashi, H., Kimura, M., Maruyama, S., Nagayasu, M., & Imanaka, S. (2020) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2020.12.044 · Cited by 40 · see citing works
Developmental Toxicant Exposure Is Associated with Transgenerational Adenomyosis in a Murine Model
Bruner‐Tran, K. L., Dulęba, A. J., Taylor, H. S., & Osteen, K. G. (2016) · Biology of Reproduction · doi:10.1095/biolreprod.116.138370 · Cited by 39 · see citing works
Targeting YAP1 ameliorates progesterone resistance in endometriosis
Lin, S., Li, W., Lin, S.-C., Hou, H.-T., Tsai, Y.-C., Lin, T.-C., Wu, M., & Tsai, S. (2023) · Human Reproduction · doi:10.1093/humrep/dead071 · Cited by 38 · see citing works
Lai, Z., Yang, H., Shi, J.-W., Shen, H., Wang, Y., Chang, K., Zhang, T., Ye, J., Sun, J., Qiu, X., et al. (2021) · International Journal of Biological Sciences · doi:10.7150/ijbs.58657 · Cited by 38 · see citing works
Dyson, M. T., Kakinuma, T., Pavone, M. E., Monsivais, D., Navarro, A., Malpani, S. S., Ono, M., & Bulun, S. E. (2015) · Fertility and Sterility · doi:10.1016/j.fertnstert.2015.06.046 · Cited by 37 · see citing works
Self-citationTaylor, H. S., Dun, E. C., & Chwalisz, K. (2019) · Pain Management · doi:10.2217/pmt-2019-0010 · Cited by 38 · see citing works
Effect of simvastatin on baboon endometriosis†
Taylor, H. S., Alderman, M. H., D’Hooghe, T. M., Fazleabas, A. T., & Dulęba, A. J. (2017) · Biology of Reproduction · doi:10.1093/biolre/iox058 · Cited by 38 · see citing works
Rakhila, H., Carli, C., Daris, M., Lemyre, M., Lebœuf, M., & Akoum, A. (2013) · Fertility and Sterility · doi:10.1016/j.fertnstert.2013.08.016 · Cited by 36 · see citing works
The role of Lipoxin A4 in endometrial biology and endometriosis
Canny, G., & Lessey, B. A. (2013) · Mucosal Immunology · doi:10.1038/mi.2013.9 · Cited by 35 · see citing works
Link between Endometriosis, Atherosclerotic Cardiovascular Disease, and the Health of Women Midlife
Taşkın, Ö., Rikhraj, K. J. K., Tan, J., Sedlak, T., Rowe, T., & Bedaiwy, M. A. (2019) · Journal of Minimally Invasive Gynecology · doi:10.1016/j.jmig.2019.02.022 · Cited by 35 · see citing works
Gadducci, A., & Zannoni, G. F. (2020) · Anticancer Research · doi:10.21873/anticanres.14212 · Cited by 37 · see citing works
Garzon, S., Laganà, A. S., Barra, F., Casarin, J., Cromi, A., Raffaelli, R., Uccella, S., Franchi, M. P., Ghezzi, F., & Ferrero, S. (2020) · Expert Opinion on Investigational Drugs · doi:10.1080/13543784.2020.1842356 · Cited by 36 · see citing works
Wu, Y. T., Zhu, Y., Xie, N., et al. (2022) · PLoS ONE · doi:10.1371/journal.pone.0263614 · Cited by 33 · see citing works
“Cyclooxygenase 2 (COX-2), encoded by PTGS2, plays an important role in the development of endometriosis [24].”
BackgroundAdvances in targeting estrogen synthesis and receptors in patients with endometriosis
Clemenza, S., Vannuccini, S., Ruotolo, A., Capezzuoli, T., & Petraglia, F. (2022) · Expert Opinion on Investigational Drugs · doi:10.1080/13543784.2022.2152325 · Cited by 34 · see citing works
- Authors
- Bulun, S., Monsavais, D., Pavone, M., Dyson, M., Xue, Q., Attar, E., Tokunaga, H., & Su, E.
- Affiliations
- Northwestern University (US)
- Peking University (CN)
- Istanbul University-Cerrahpaşa (TR)
- Tohoku University (JP)
- Venue
- Seminars in Reproductive Medicine
- Publisher
- Georg Thieme Verlag KG
- Published
- 2012-01
- Volume
- 30
- Issue
- 01
- Pages
- 39-45
- ISSN
- 1526-4564 (ISSN-L)
- 1526-8004
- PMC
- PMC4034571
- OpenAlex
- W2045579344
- Cited by
- 307
- References
- 73
- Citations by year
- 2026: 17 · 2025: 25 · 2024: 30 · 2023: 25 · 2022: 35 · 2021: 24 · 2020: 19 · 2019: 22 · 2018: 22 · 2017: 13 · 2016: 13 · 2015: 23 · 2014: 18 · 2013: 15 · 2012: 4
- FWCI
- 21.53
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Seminars in Reproductive Medicine (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (submittedVersion)
- PubMed Central (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 receptor beta, estradiol, aromatase, endometriotic stromal cells, promoter methylation, estrogen receptor alpha, progesterone resistance
- MeSH terms
- Animals, Endometriosis, Endometrium, Estrogen Antagonists
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Claims read under definition version 3 (extract-v3) on 2026-09-28.
Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-09-28.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
