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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 (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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BackgroundGreaves, 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
Implications of immune dysfunction on endometriosis associated infertility
Miller, J. E., Ahn, S. H., Monsanto, S. P., Khalaj, K., Koti, M., & Tayade, C. (2016) · Oncotarget · doi:10.18632/oncotarget.12577 · Cited by 195
“Increased expression of COX-2 mRNA is observed in the ectopic and eutopic endometrium of women with endometriosis compared to healthy controls [52].”
BackgroundEstrogen metabolism and action in endometriosis
Rižner, T. L. (2009) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2009.03.022 · Cited by 153
Endometrial biomarkers for the non-invasive diagnosis of endometriosis
Gupta, D., Hull, M. L., Fraser, I. S., Miller, L., Bossuyt, P. M., JOHNSON, N. P., & Nisenblat, V. (2016) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd012165 · Cited by 179
Local and systemic factors and implantation: what is the evidence?
Fox, C. W., Morin, S. J., Jeong, J., Scott, R. T., & Lessey, B. A. (2016) · Fertility and Sterility · doi:10.1016/j.fertnstert.2016.02.018 · Cited by 170
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
“, 2007)oreutopic endometrium (Brandenberger et al., 1999; Fujimoto et al., 1999; Bukulmez et al., 2007) has been described suggesting a unique E2-dependent growth of ovarian endometriomas.”
BackgroundInfluentialFerrero, S., Camerini, G., Seracchioli, R., Ragni, N., Venturini, P., & Remorgida, V. (2009) · Human Reproduction · doi:10.1093/humrep/dep302 · Cited by 145
“Since the late 1990s, several studies using either PCR or immunohistochemistry demonstrated the expression of aromatase P450 in both eutopic and ectopic endometrium from patients with endometriosis, but not in eutopic endometrium from disease-free women and in endometriosis-free peritoneal tissue (Noble et al., 1996;…”
BackgroundBurns, K. A., Rodriguez, K., Hewitt, S., Janardhan, K., Young, S., & Korach, K. (2012) · Endocrinology · doi:10.1210/en.2012-1294 · Cited by 143
Immunological changes associated with adenomyosis: a systematic review
Bourdon, M., Santulli, P., Jeljeli, M. M., Vannuccini, S., Marcellin, L., Doridot, L., Petraglia, F., Batteux, F., & Chapron, C. (2020) · Human Reproduction Update · doi:10.1093/humupd/dmaa038 · Cited by 195
Peritoneal endometriosis is an inflammatory disease.
Lousse, J., van Langendonckt, A., Defrère, S., Ramos, R. G., Colette, S., & Donnez, J. (2012) · Frontiers in Bioscience · doi:10.2741/358 · Cited by 137
“However, COX-2 mRNA expression was recently compared between peritoneal implants, eutopic endometrium of women with endometriosis and control endometrium, but differences among these groups did not reach levels of significance (108).”
BackgroundProgesterone Resistance in Endometriosis: an Acquired Property?
McKinnon, B. D., Mueller, M. D., & Montgomery, G. W. (2018) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2018.05.006 · Cited by 153
Prostaglandin E 2 : the master of endometriosis?
Wu, M., Lu, C.-W., Chuang, P., & Tsai, S. (2010) · Experimental Biology and Medicine · doi:10.1258/ebm.2010.009321 · Cited by 139
MicroRNA signature and regulatory functions in the endometrium during normal and disease states
Pan, Q., & Chegini, N. (2008) · Seminars in Reproductive Medicine · doi:10.1055/s-0028-1096128 · Cited by 134
Peritoneal endometriosis is an inflammatory disease
Donnez, J. (2012) · Frontiers in Bioscience · doi:10.2741/e358 · Cited by 127
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
“Furthermore, E inactivation is decreased because of the activity of 17b-hydrosteroid dehydrogenase type 2, which converts E2 to E1, is downregulated (7).”
BackgroundEutopic endometrium in women with endometriosis: ground zero for the study of implantation defects
Lessey, B., Lebovic, D., & Taylor, R. (2013) · Seminars in Reproductive Medicine · doi:10.1055/s-0032-1333476 · Cited by 113
异常在位子宫内膜是内异症的病因吗?-在位内膜在内异症发病中的作用
Liu, H., & Lang, J. H. (2011) · Medical Science Monitor · doi:10.12659/msm.881707 · Cited by 93
Sex hormone-dependent regulation of cilia beat frequency in airway epithelium.
Jain, R., Ray, J., Pan, J.-H., & Brody, S. (2012) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2011-0107oc · Cited by 109
“In endometrial tissue, PR-A and PR-B dually serve an antiinflammatory role (20).”
BackgroundAndrogens and endometrium: new insights and new targets
Simitsidellis, I., Saunders, P. T. K., & Gibson, D. A. (2018) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2017.09.022 · Cited by 107
Estrogen biosynthesis and signaling in endometriosis
Huhtinen, K., Ståhle, M., Perheentupa, A., & Poutanen, M. (2012) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2011.08.022 · Cited by 107
Dawson, A., Llauradó Fernandez, M., Anglesio, M., Yong, P. J., & Carey, M. S. (2018) · ecancermedicalscience · doi:10.3332/ecancer.2018.803 · Cited by 106
DNA methylation in endometriosis (Review)
KOUKOURA, O., SIFAKIS, S., & SPANDIDOS, D. A. (2016) · Molecular Medicine Reports · doi:10.3892/mmr.2016.4925 · Cited by 103
“In contrast with the above observations, there are certain studies that report higher levels of PRβ in endometriotic tissues (68,69).”
ResultDisturbed estrogen and progesterone action in ovarian endometriosis
Šmuc, T., Hevir, N., Ribič-Pucelj, M., Husen, B., Thole, H., & Rižner, T. L. (2009) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2008.07.020 · Cited by 101
“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.”
BackgroundResultBurns, K. A., Thomas, S. Y., Hamilton, K. J., Young, S. L., Cook, D. N., & Korach, K. S. (2017) · Endocrinology · doi:10.1210/en.2017-00562 · Cited by 116
“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.”
BackgroundMonsivais, D., Dyson, M. T., Yin, P., Coon, J. S., Navarro, A., Feng, G., Malpani, S. S., Ono, M., Ercan, C. M., Wei, J. J., et al. (2014) · Molecular Endocrinology · doi:10.1210/me.2013-1421 · Cited by 91
Targeting oxidative stress to treat endometriosis
Harlev, A., Gupta, S., & Agarwal, A. K. (2015) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728222.2015.1077226 · Cited by 92
“Environmental pollutants [18], immunological dysregulation [19], persistent inflammatory status [20] and epigenetic alterations [21] impose a risk of disease.”
BackgroundHan, S. J., & O’Malley, B. W. (2014) · Human Reproduction Update · doi:10.1093/humupd/dmu002 · Cited by 98
“However, some endometriotic tissues have higher levels of PR-B expression compared with the normal endometrium (Misao et al., 1999; Bukulmez et al., 2008).”
BackgroundResultInfluentialEndometriosis and polycystic ovary syndrome are diametric disorders
Dinsdale, N. L., & Crespi, B. J. (2021) · Evolutionary Applications · doi:10.1111/eva.13244 · Cited by 90
Absence of aromatase protein and mRNA expression in endometriosis
Colette, S., Lousse, J. C., Defrère, S., Curaba, M., Heilier, J.-F., Langendonckt, A. V., Mestdagt, M., Foidart, J. M., Loumaye, E., & Donnez, J. (2009) · Human Reproduction · doi:10.1093/humrep/dep199 · Cited by 86
“…(Kitawaki et al., 1997; Noble et al., 1997; Murakami et al., 2006; Purohit et al., 2007) and protein level (Kitawaki et al., 1997, 1999a, b; Ishihara et al., 2003; Wölfler et al., 2005; Murakami et al., 2006; Velasco et al., 2006; Acien et al., 2007; Bukulmez et al., 2007; Hudelist et al., 2007).”
BackgroundMethodInfluentialThe Expression and Ovarian Steroid Regulation of Endometrial Micro-RNAs
Toloubeydokhti, T., Pan, Q., Luo, X., Bukulmez, O., & Chegini, N. (2008) · Reproductive Sciences · doi:10.1177/1933719108324132 · Cited by 83
“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…”
MethodResultSelf-citationRetractedLessey, B., & Young, S. (2014) · Seminars in Reproductive Medicine · doi:10.1055/s-0034-1376355 · Cited by 82
Differential regulation of Akt phosphorylation in endometriosis.
Cinar, O., Seval, Y., Uz, Y. H., Cakmak, H., Ulukus, M., Kayisli, U., & Arıcı, A. (2009) · Reproductive Biomedicine Online · doi:10.1016/j.rbmo.2009.10.001 · Cited by 82
“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…”
ResultJones, R. L., Tanadini‐Lang, S., Kendziorski, J. A., Greene, A., & Burns, K. A. (2018) · Environmental Health Perspectives · doi:10.1289/ehp3802 · Cited by 88
“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 (…”
Cicinelli, E., Bettocchi, S., de Ziegler, D., Loizzi, V., Cormio, G., Marinaccio, M., Trojano, G., Crupano, F., Francescato, R., Vitagliano, A., et al. (2019) · Journal of minimally invasive gynecology · doi:10.1016/j.jmig.2019.01.012 · Cited by 73
Salama, S., Kamel, M., Diaz-Arrastia, C., Xu, X., Veenstra, T., Salih, S., Botting, S., & Kumar, R. (2009) · Journal of Clinical Endocrinology and Metabolism · doi:10.1210/jc.2008-1389 · Cited by 72
Effect of progestogens and combined oral contraceptives on nerve fibers in peritoneal endometriosis.
Tokushige, N., Markham, R., Russell, P., & Fraser, I. (2009) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.07.1774 · Cited by 69
Emerging drugs for endometriosis
Guo, S. (2008) · Expert Opinion on Emerging Drugs · doi:10.1517/14728210802548360 · Cited by 25
“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] .”
BackgroundSamalecos, A., & Gellersen, B. (2008) · Endocrinology · doi:10.1210/en.2008-0602 · Cited by 68
Endometriosis and possible inflammation markers
Wu, M., Hsiao, K., & Tsai, S. (2015) · Gynecology and Minimally Invasive Therapy · doi:10.1016/j.gmit.2015.05.001 · Cited by 78
Aberrant gene expression profile in a mouse model of endometriosis mirrors that observed in women
Pelch, K. E., Schroder, A. L., Kimball, P. A., Sharpe-Timms, K. L., Davis, J., & Nagel, S. C. (2009) · Fertility and Sterility · doi:10.1016/j.fertnstert.2009.03.086 · Cited by 64
“(20), this is in contrast to other reports that show altered expression of other apoptosis (56) and steroid hormone signaling genes (37, 57).”
BackgroundResultEndometriosis, leiomyoma and adenomyosis: the risk of gynecologic malignancy.
Verit, F., & Yucel, O. (2013) · Asian Pacific Journal of Cancer Prevention · doi:10.7314/apjcp.2013.14.10.5589 · Cited by 63
“It has been also suggested that ERβ agonists may also have anti-inflammatory effects on immune cells (Bukulmez et al., 2008).”
BackgroundInfluentialMonsivais, D., Dyson, M. T., Yin, P., Navarro, A., Coon, J. S., Pavone, M. E., & Bulun, S. E. (2016) · Fertility and Sterility · doi:10.1016/j.fertnstert.2016.01.012 · Cited by 62
Shimizu, Y., Takeuchi, T., Mita, S., Mizuguchi, K., Kiyono, T., Inoue, M., & Kyo, S. (2009) · Molecular Human Reproduction · doi:10.1093/molehr/gap042 · Cited by 60
“dominant (Misao et al., 1999; Bukulmez et al., 2008).”
Pathological functions of hypoxia in endometriosis
Hsiao, K.-Y. (2015) · Frontiers in Bioscience · doi:10.2741/e736 · Cited by 61
“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
Hey‐Cunningham, A. J. (2013) · Frontiers in Bioscience-Elite · doi:10.2741/e682 · Cited by 68
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
“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].”
Franasiak, J., Holoch, K., Yuan, L.-W., Schammel, D., Young, S., & Lessey, B. (2014) · Fertility and Sterility · doi:10.1016/j.fertnstert.2014.02.027 · Cited by 60
“Increased local production of E by aromatase expression has been linked to inflammatory changes associated with endometriosis (62, 63).”
BackgroundKonings, G. F. J., Brentjens, L. S., Delvoux, B., Linnanen, T., Cornel, K. M. C., Koskimies, P., Bongers, M. Y., Kruitwagen, R. F. P. M., Xanthoulea, S., & Romano, A. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.00940 · Cited by 66
International Journal of Current Microbiology and Applied Sciences
Publishers, P. E. (2020) · International Journal of Current Microbiology and Applied Sciences · doi:10.20546/ijcmas · Cited by 57
Grandi, G., Mueller, M., Papadia, A., Kocbek, V., Bersinger, N., Petraglia, F., Cagnacci, A., & Mckinnon, B. (2016) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2016.06.004 · Cited by 57
“…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
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
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
Sarsenova, M., Lawarde, A., Pathare, A. D. S., Saare, M., Modhukur, V., Soplepmann, P., Terasmaa, A., Käämbre, T., Gemzell‐Danielsson, K., Lalitkumar, P. G., et al. (2024) · Communications Biology · doi:10.1038/s42003-024-06713-5 · Cited by 48
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
Aldo-keto reductase 1C3—Assessment as a new target for the treatment of endometriosis
Rižner, T. L., & Penning, T. M. (2019) · Pharmacological Research · doi:10.1016/j.phrs.2019.104446 · Cited by 53
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
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
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
“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
“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
Mortality attributable to smoking in China.
Chen, R.-L. (2009) · New England Journal of Medicine · doi:10.1056/nejmc090277 · Cited by 38
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
“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
“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
“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
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 60
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
“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
“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
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
“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 30
Guzeloglu‐Kayisli, O., Halis, G., Taskiran, S. A., Kayisli, U. A., & Arici, A. M. (2008) · Reproductive Sciences · doi:10.1177/1933719108317583 · Cited by 32
PTGS2 down-regulation in cumulus cells of infertile women with endometriosis
da Luz, C. M., Broi, M. G. D., Donabela, F. C., de Paz, C. C. P., Meola, J., & Navarro, P. A. (2017) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2017.06.021 · Cited by 34
“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
“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
“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
“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 30
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
“38 [0–17]) 1.”
Sanchez, A. M., Viganò, P., Somigliana, E., Cioffi, R., Panina‐Bordignon, P., & Candiani, M. (2014) · Reproductive Sciences · doi:10.1177/1933719114529374 · Cited by 30
“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
“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
Metadata
- 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 › Endocrinology › Estrogen and related hormone effects
- Health Sciences › Medicine › Pharmacology (medical) › 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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