Inflammatory Status Influences Aromatase and Steroid Receptor Expression in Endometriosis
Open accessAbstract
Aberrant up-regulation of aromatase in eutopic endometrium and implants from women with endometriosis has been reported. Aromatase induction may be mediated by increased cyclooxygenase-2 (COX-2). Recently, we demonstrated that progesterone receptor (PR)-A and PR-B serve an antiinflammatory role in the uterus by antagonizing nuclear factor kappaB activation and COX-2 expression. PR-C, which antagonizes PR-B, is up-regulated by inflammation. Although estrogen receptor alpha (ERalpha) is implicated in endometriosis, an antiinflammatory role of ERbeta has been suggested. We examined stage-specific expression of aromatase, COX-2, ER, and PR isoform expression in eutopic endometrium, implants, peritoneum, and endometrioma samples from endometriosis patients. Endometrial and peritoneal biopsies were obtained from unaffected women and those with fibroids. Aromatase expression in eutopic endometrium from endometriosis patients was significantly increased compared with controls. Aromatase expression in endometriosis implants was markedly increased compared with eutopic endometrium. Aromatase mRNA levels were increased significantly in red implants relative to black implants and endometrioma cyst capsule. Moreover, COX-2 expression was increased in implants and in eutopic endometrium of women with endometriosis as compared with control endometrium. As observed for aromatase mRNA, the highest levels of COX-2 mRNA were found in red implants. The ratio of ERbeta/ERalpha mRNA was significan…
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The eutopic endometrium of women with endometriosis demonstrates significantly elevated aromatase activity compared with unaffected women.
“The eutopic endometrium of women with endometriosis demonstrates significantly elevated aromatase activity compared with unaffected women (Bukulmez et al., 2008), and within affected women, aromatase expression positively predicts severity of dysmenorrhea (Maia et al., 2012).”
From Endometriosis and polycystic ovary syndrome are diametric disorders (2021) · cites this paper as Bukulmez et al., 2008
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“Recently, Bukulmez et al. (2008) reported a significantly elevated ratio of ERβ/ERα mRNA in endometriomas, compared with eutopic endometrium, in agreement with our data.”
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“Endometriotic lesions have altered ratios of ERa and ERb expression compared with eutopic endometrium (8), and both ERs are present in uterine andmultiple immune cell types (i.”
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“Environmental pollutants [18], immunological dysregulation [19], persistent inflammatory status [20] and epigenetic alterations [21] impose a risk of disease.”
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“However, some endometriotic tissues have higher levels of PR-B expression compared with the normal endometrium (Misao et al., 1999; Bukulmez et al., 2008).”
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“We also found an elevated expression of CYP19A1, StAR, and COX-2 in EC as compared to EU and EN; however, their expression in EN compared to EU contrasted from previously reported studies.(5,8,10,11,18,47,48) The most likely explanation for the difference could be the method of detection and primers used in these as c…”
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“One of the explanations for this aberrant behaviour in endometrial stromal cells of endometriosis could be related to the relative concentration of oestrogen a and b receptors, and suggests a non-genomic interaction between Akt, ICI and oestrogen receptors, since previous studies have also shown changes in the ratio o…”
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“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 (…”
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“Although endometrial expression of ERβ appears to be reduced in women with endometriosis (or in animals with induced endometriosis) [141,142] , ERβ expression in ectopic endometrium and in macrophages of women with endometriosis has been documented to be increased [143-145] .”
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“(20), this is in contrast to other reports that show altered expression of other apoptosis (56) and steroid hormone signaling genes (37, 57).”
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“It has been also suggested that ERβ agonists may also have anti-inflammatory effects on immune cells (Bukulmez et al., 2008).”
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“dominant (Misao et al., 1999; Bukulmez et al., 2008).”
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“ERα downregulation and/or ERβ upregulation are found in endometriotic tissue, causing the higher ratio of ERβ/ERα (46-52) whereas GPR30 overexpresses in endometriotic tissues (53, 54).”
BackgroundAngiogenesis lymphangiogenesis and neurogenesis in endometriosis
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Daidzein-rich isoflavone aglycones inhibit cell growth and inflammation in endometriosis
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“Biological actions of estrogen, synthesized by locally elevated aromatase, mediated mainly by ERβ, are crucial for the establishment and maintenance of this disease, as ERβ is highly expressed in local endometriotic lesions [4].”
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“Increased local production of E by aromatase expression has been linked to inflammatory changes associated with endometriosis (62, 63).”
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“…et al, 2014), as some studies have shown PRA and B are decreased, or absent in endometriomas (Attia et al, 2000, Bergqvist and Ferno 1993), whereas other studies failed to show a consistent expression in extra-ovarian endometriosis (Bukulmez et al, 2008; Jones et al, 1995; Prentice et al, 1992).”
Sutrisno, S., Aprina, H., Simanungkalit, H. M., Andriyani, A., Barlıanto, W., Sujuti, H., Santoso, S., Dwijayasa, P. M., Wahyuni, E. S., & Mustofa, E. (2017) · Journal of Traditional and Complementary Medicine · doi:10.1016/j.jtcme.2017.03.002 · Cited by 60 · see citing works
Carrarelli, P., Luddi, A., Funghi, L., Arcuri, F., Batteux, F., Dela Cruz, C., Tosti, C., Reis, F. M., Chapron, C., & Petraglia, F. (2016) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2016.07.009 · Cited by 51 · see citing works
Hevir, N., Vouk, K., Šinkovec, J., Ribič-Pucelj, M., & Lanišnik Rižner, T. (2011) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2011.01.003 · Cited by 48 · see citing works
Sarsenova, M., Lawarde, A., Pathare, A. D. S., Saare, M., Modhukur, V., Soplepmann, P., Terasmaa, A., Käämbre, T., Gemzell‐Danielsson, K., Lalitkumar, P. G., et al. (2024) · Communications Biology · doi:10.1038/s42003-024-06713-5 · Cited by 45 · see citing works
Hapangama, D. K., Turner, M. A., Drury, J. A., Heathcote, L., Afshar, Y., Mavrogianis, P. A., & Fazleabas, A. T. (2010) · Human Reproduction · doi:10.1093/humrep/deq248 · Cited by 41 · see citing works
Aldo-keto reductase 1C3—Assessment as a new target for the treatment of endometriosis
Rižner, T. L., & Penning, T. M. (2019) · Pharmacological Research · doi:10.1016/j.phrs.2019.104446 · Cited by 51 · see citing works
Ichioka, M., Mita, S., Shimizu, Y., Imada, K., Kiyono, T., Bono, Y., & Kyo, S. (2014) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2014.12.008 · Cited by 38 · see citing works
Vouk, K., Šmuc, T., Guggenberger, C., Ribič-pucelj, M., Šinkovec, J., Husen, B., Thole, H., Houba, P. H. J., Thaete, C., Adamski, J., et al. (2011) · Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2011.03.010 · Cited by 40 · see citing works
Bukulmez, O., Hardy, D., Carr, B. R., Auchus, R., Toloubeydokhti, T., Word, R., & Mendelson, C. R. (2008) · Journal of Clinical Endocrinology and Metabolism · doi:10.1210/jc.2008-0248 · Cited by 40 · see citing works
“Thermocycling was performed as reported previously (3).”
BackgroundSelf-citationMaia Jr., H., Haddad, & Casoy (2012) · International Journal of Women's Health · doi:10.2147/ijwh.s29154 · Cited by 39 · see citing works
“The aggressiveness of endometriosis appears to correlate with the intensity of the expression of this enzyme in lesions, with the most aggressive occurring in red peritoneal lesions.(2) A correlation was also found between the severity of endometriosis and the intensity of Cox-2 expression in both lesions and the euto…”
BackgroundResearch advances in drug therapy of endometriosis
Shi, J., Tan, X., Feng, G., Yuan, Z., Jiang, Z., Banda, S., Wang, L., Zheng, W., Chen, L., Yu, D., et al. (2023) · Frontiers in Pharmacology · doi:10.3389/fphar.2023.1199010 · Cited by 30 · see citing works
Mortality attributable to smoking in China.
Chen, R.-L. (2009) · New England Journal of Medicine · doi:10.1056/nejmc090277 · Cited by 38 · 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
“Estrogen production is also increased in endometriosis,(180) likely influenced by the inflammatory environment.(181) Here, the COX-2-derived eicosanoid PGE2, as a potent inducer of aromatase and Steroidogenic acute regulatory protein expression, has a pivotal role.”
BackgroundActivated glucocorticoid and eicosanoid pathways in endometriosis
Monsivais, D., Bray, J. D., Su, E. J., Pavone, M. E., Dyson, M. T., Navarro, A., Kakinuma, T., & Bulun, S. E. (2012) · Fertility and Sterility · doi:10.1016/j.fertnstert.2012.03.030 · Cited by 37 · see citing works
“Although previously reported to be elevated in endometriosis, we found no significant difference in the gene expression levels COX-1 or COX-2 between normal and endometriotic tissues; this however, does not preclude the possibility that COX-1 and COX-2 are upregulated at the translational level (21, 22).”
BackgroundInvolvement of estrogen receptor-related receptors in human ovarian endometriosis.
Cavallini, A., Resta, L., Caringella, A., Naro, E. D., Lippolis, C., & Loverro, G. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2011.04.032 · Cited by 34 · see citing works
“A second explanation is based on the anti-inflammatory properties exhibited by ER-b protein in the endometriotic lesion (19).”
BackgroundIs aromatase expression in the endometrium the cause of endometriosis and related infertility?
Maia, H., Casoy, J., & Filho, J. V. (2009) · Gynecological Endocrinology · doi:10.1080/09513590802627647 · Cited by 35 · 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
Winkler, N., Bükülmez, O., Hardy, D. B., & Carr, B. R. (2009) · Fertility and Sterility · doi:10.1016/j.fertnstert.2009.09.032 · Cited by 31 · see citing works
“We calculated the relative fold changes using the comparative cycle times (Ct) method with human ribosomal protein (h36B4) mRNA as the reference guide (42).”
MethodSelf-citationUreteral endometriosis: A systematic literature review
Palla, V., Karaolanis, G., Katafigiotis, I. S., & Anastasiou, I. P. (2017) · Indian Journal of Urology · doi:10.4103/iju.iju_84_17 · Cited by 37 · see citing works
“This fact, in combination with the upregulation of prostaglandin receptors leads to the presence of high concentrations of prostaglandins in DIE.[13-16]”
BackgroundMicroRNAs in Endometriosis: Insights into Inflammation and Progesterone Resistance
Hon, J.-X., Wahab, N. A., Karim, A., Mokhtar, N. M., & Mokhtar, M. H. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241915001 · Cited by 33 · see citing works
Phytoestrogens for the Management of Endometriosis: Findings and Issues
Cai, X., Liu, M., Zhang, B., Zhao, S., & Jiang, S. (2021) · Pharmaceuticals · doi:10.3390/ph14060569 · Cited by 36 · see citing works
“It was reported that in endometriotic lesions there were relatively higher levels of ERβ and altered ERα/ERβ ratios [22,23].”
BackgroundWölfler, M. M., Küppers, M., Rath, W. H., Buck, V. U., Meinhold-Heerlein, I. M., & Classen-Linke, I. (2016) · Annals of Anatomy - Anatomischer Anzeiger · doi:10.1016/j.aanat.2016.03.004 · Cited by 29 · see citing works
Guzeloglu‐Kayisli, O., Halis, G., Taskiran, S. A., Kayisli, U. A., & Arici, A. M. (2008) · Reproductive Sciences · doi:10.1177/1933719108317583 · Cited by 32 · see citing works
PTGS2 down-regulation in cumulus cells of infertile women with endometriosis.
Luz, C. D. D., Broi, M. D. D., Donabela, F. C., de Paz, C. C. P., Meola, J., & Navarro, P. (2017) · Reproductive Biomedicine Online · doi:10.1016/j.rbmo.2017.06.021 · Cited by 28 · see citing works
“In the endometrial tissue of patients with endometriosis, aberrant aromatase is induced via cyclooxygenase-2 prostaglandine-2 (COX-2–PGE2) pathway deregulation, with a positive feedback cycle (Bukulmez et al., 2008; Bulun et al., 2002).”
BackgroundClinical Assessment and Management of the Endometrium in Recurrent Early Pregnancy Loss
Patel, B., & Lessey, B. (2011) · Seminars in Reproductive Medicine · doi:10.1055/s-0031-1293203 · Cited by 28
New treatment strategies and emerging drugs in endometriosis
Streuli, I., de Ziegler, D., Borghese, B., Santulli, P., Batteux, F., & Chapron, C. (2012) · Expert Opinion on Emerging Drugs · doi:10.1517/14728214.2012.668885 · Cited by 27 · see citing works
“ER-b has been suggested to play an antiinflammatory role and to antagonize the development of endometriotic lesions [96].”
BackgroundBabayev, S., Park, C. W., Keller, P. W., Carr, B., Word, R., & Bukulmez, O. (2017) · Reproductive Sciences · doi:10.1177/1933719117691145 · Cited by 27 · see citing works
“Inflammation itself may also lead to perturbations of PR isoform expression in endometriosis as reported.(3,4) One prospective randomized trial found that the continuous use of combined oral contraceptive pills (OCPs) can be as effective as leuprolide acetate when used in patients with chronic pelvic pain due to endom…”
BackgroundSelf-citationAre aromatase inhibitors effective in endometriosis treatment?
Colette, S., & Donnez, J. (2011) · Expert Opinion on Investigational Drugs · doi:10.1517/13543784.2011.581226 · Cited by 26 · see citing works
“Indeed, from the end of the 1990s until very recently, aromatase was widely believed to be expressed at the transcriptional [20-48], protein [21,23,27,29,33,37,49-55] and activity levels [21,22,26,33,41,56-58].”
BackgroundGuo, S., Habiba, M. A., & Benagiano, G. (2023) · Biomolecules · doi:10.3390/biom13020336 · Cited by 29 · see citing works
How can macroscopically normal peritoneum contribute to the pathogenesis of endometriosis?
Fassbender, A., Overbergh, L., Verdrengh, E., Kyama, C., Vodolazakaia, A., Bokor, A., Meuleman, C., Peeraer, K., Tomassetti, C., Waelkens, E., et al. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2011.06.034 · Cited by 25 · see citing works
“38 [0–17]) 1.”
The Endometriotic Tissue Lining the Internal Surface of Endometrioma
Sanchez, A., Viganò, P., Somigliana, E., Cioffi, R., Panina-Bordignon, P., & Candiani, M. (2015) · Reproductive Sciences · doi:10.1177/1933719114529374 · Cited by 23 · see citing works
“However, since contamination by a specific tissue is likely to occur when extracting mRNA from endometrioma capsule, results from studies that have visually analyzed glands and stroma of the ectopic lesion should be taken into higher consideration.(11,12) Data derived from these analyses were not always in line with r…”
ResultYang, Y., Zhang, X.-M., Zhou, C.-Y., Huang, X.-F., Lin, J., & Xu, H. (2013) · Acta Histochemica · doi:10.1016/j.acthis.2012.10.006 · Cited by 23 · see citing works
“Several studies have revealed changed expression of ER- and ER- of the endometriotic lesions in patients with peritoneal and ovarian endometriosis (Brandenberger et al., 1999; Matsuzaki et al., 2001; Bukulmez et al., 2008).”
BackgroundGonadotropin-Releasing Hormone Agonists for Endometriosis
Olive, D. L. (2008) · New England Journal of Medicine · doi:10.1056/nejmct0803719 · Cited by 57 · see citing works
- Authors
- Bukulmez, O., Hardy, D. B., Carr, B. R., Word, R. A., & Mendelson, C. R.
- Affiliations
- Departments of Obstetrics and Gynecology (O.B., B.R.C., R.A.W., C.R.M.), The University of Texas Southwestern Medical Center at Dallas, Dallas, Texas 75390
- The University of Texas Southwestern Medical Center (US)
- Corresponding author
- Mendelson, Carole R.
- Venue
- Endocrinology
- Publisher
- The Endocrine Society
- Published
- 2007-11-29
- Volume
- 149
- Issue
- 3
- Pages
- 1190-1204
- ISSN
- 0013-7227 (ISSN-L)
- 1945-7170
- PMC
- PMC2275353
- OpenAlex
- W2052591056
- Cited by
- 186
- References
- 0
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 4 · 2023: 9 · 2022: 4 · 2021: 9 · 2020: 8 · 2019: 10 · 2018: 12 · 2017: 11 · 2016: 10 · 2015: 11 · 2014: 15 · 2013: 10 · 2012: 12
- FWCI
- 15.10
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Endocrinology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK031206, DK31206)
- 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 › Pharmacology › Inflammatory mediators and NSAID effects
- Keywords
- endometriosis, aromatase, cyclooxygenase-2, progesterone receptor isoforms, estrogen receptor alpha, estrogen receptor beta, endometrioma, eutopic endometrium, inflammation, NF-κB, disease progression
- MeSH terms
- Adult, Aromatase, Cross-Sectional Studies, Endometriosis, Endometrium, Female, Humans, Inflammation, Ovary, Peritoneum, Prospective Studies, Receptors, Estrogen, Receptors, Progesterone, RNA, Messenger, Up-Regulation, Case-Control Studies, Protein Isoforms, Estrogen Receptor alpha, Estrogen Receptor beta, Cyclooxygenase 2
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