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Aromatase expression in endometriosis.
Abstract
The conversion of C19 steroids to estrogens occurs in a number of tissues, such as the ovary and placenta, and is catalyzed by aromatase P450 (P450arom; the product of the CYP19 gene). P450arom expression has also been detected in a number of uterine tumors, such as leiomyomas and endometrial cancer. On the other hand, P450arom expression was undetectable in normal endometrial and myometrial tissues. The present study was conducted to determine the presence or absence of aromatase expression in peritoneal endometriotic implants and in the eutopic endometrium of women with endometriosis. Endometriotic implants in pelvic peritoneum (n = 17; e.g. posterior culdesac, bladder, and anterior culdesac) and eutopic endometrial curettings (n = 11) of 14 patients with histologically documented pelvic endometriosis were obtained at the time of laparoscopy or laparotomy. Pelvic peritoneal biopsies distal to endometriotic implants as well as normal endometrial tissues (n = 7) from disease-free women were used as negative controls. We used competitive RT-PCR technology employing an internal standard to amplify P450arom transcripts in total ribonucleic acid (RNA) isolated from these tissues. P450arom transcripts were detected in all endometriotic implants and in all eutopic endometrial tissues from patients with endometriosis. P450arom messenger RNA species were not detectable in endometrial tissues from disease-free women or in endometriosis-free peritoneal tissues. The highest levels of transcripts were detected in an endometriotic implant that involved the full thickness of the anterior abdominal wall. The P450arom transcript level within the core of this endometriotic mass was 4-fold higher than that in the surrounding adipose tissue. It has been shown recently that aromatase expression in various human tissues is regulated by the use of tissue-specific promoters via alternative splicing. To analyze promoter usage, we amplified by RT-PCR the most likely promoter-specific untranslated 5'-termini of P450arom transcripts in 2 endometriotic implants. It appears that these endometriotic implants use both the adipose-type promoter I.4 and gonadal-type promoter II for aromatase expression. The use of promoter I.4 for aromatase expression in adipose tissue has been recently observed to be regulated by members of the interleukin-6 (IL-6) cytokine family. Based on these findings, we examined by RT-PCR, IL-6 and IL-11 messenger RNA expression in 5 endometriotic tissues and 1 eutopic endometrial sample from a patient with endometriosis. We detected IL-6 and IL-11 transcripts in all endometriotic tissues and in the eutopic endometrial tissue sample studied. Our findings indicate that both eutopic endometrial tissues and endometriotic implants from patients with endometriosis are biochemically different from normal endometrial tissues of disease-free women. The presence of aromatase expression in eutopic endometrial tissues from patients with endometriosis may be related to the capability of implantation of these tissues on peritoneal surfaces. Furthermore, the possibility of estrogen production in these implants may serve to promote their growth. Increased IL-6 and IL-11 expression in these tissues suggests that P450arom expression in endometriosis may be regulated in part by these cytokines.
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“Local E2 levels are increased in endometriosis due to upregulation of the aromatase gene CYP19A1 [34] and reduction of 17-hydroxysteroid dehydrogenase type 2 (17HSD2), which normally (induced by P4) converts E2 to the less potent estrone [35, 36].”
From Hormonal treatments for endometriosis: The endocrine background (2022) · cites this paper as [34]
In the citing paper
“the first report of aromatase upregulation used 17 lesion samples and 7 control endometrial samples (Noble et al., 1996), while that on ERα used 9 and 11 samples, respectively (Brandenberger et al., 1999).”
From Progressively diminished estrogen signaling concordant with increased fibrosis in ectopic endometrium (2025) · cites this paper as Noble et al., 1996
In the citing paper
“The products of some of these steroidogenic genes that catalyze the formation of estradiol from cholesterol, namely StAR, P450arom (CYP19A1), and HSD17B1 were demonstrated in stromal cells of endometriotic tissue (10 -13).”
From Prostaglandin E2 Via Steroidogenic Factor-1 Coordinately Regulates Transcription of Steroidogenic Genes Necessary for Estrogen Synthesis in Endometriosis (2009) · cites this paper as [12]
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InfluentialSelf-citationProgesterone action in endometrial cancer, endometriosis, uterine fibroids, and breast cancer
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“Local E2 levels are increased in endometriosis due to upregulation of E2-producing p450 aromatase expression [170] and reduction of 17 β -hydroxysteroid dehydrogenase type 2 (17 β HSD2), which is normally induced by P4 to convert E2 to the less potent estrone but is decreased in P4-resistant…”
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Self-citationPathogenic mechanisms in endometriosis-associated infertility
Gupta, S., Goldberg, J. M., Aziz, N., Goldberg, E., Krajcir, N., & Agarwal, A. (2008) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.02.093 · Cited by 409
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Prostaglandin E2 Stimulates Aromatase Expression in Endometriosis-Derived Stromal Cells
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Self-citationHOX gene expression is altered in the endometrium of women with endometriosis
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“, 1990), aromatase (Noble et al., 1996), CA-125 (McBean and Brunstead, 1993), heat shock protein (Ota et al.”
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Kitawaki, J., Kado, N., Ishihara, H., Koshiba, H., Kitaoka, Y., & Honjo, H. (2002) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/s0960-0760(02)00260-1 · Cited by 370
Hormonal treatments for endometriosis: The endocrine background
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“A feed-forward loop connects hyperestrogenic stimulation with inflammation: the overexpression of cyclooxygenase 2 (COX2) and CYP19A1 increases local production of prostaglandins and estrogen, causing a vicious circle [38].”
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Struble, J., Reid, S., & Bedaiwy, M. A. (2015) · Journal of Minimally Invasive Gynecology · doi:10.1016/j.jmig.2015.09.018 · Cited by 323
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Endometriosis results from the dislocation of basal endometrium
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“Recent studies indicate that endometriotic lesions may be capable of producing estrogen, which may also contribute to the pathophysiology of this disease (27).”
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“Thus, the presence of aromatase cytochrome P-450 suggests a local estrogen production that may influence the disease.(45,46) Furthermore, endometriotic cell lines also express gp130, the common chain of the interleukin-6 receptor family that is typically found in sections of peritoneal endometriotic lesions (A.”
BackgroundTreatment of severe postmenopausal endometriosis with an aromatase inhibitor
Takayama, K., Zeitoun, K., Gunby, R. T., Sasano, H., Carr, B. R., & Bulun, S. E. (1998) · Fertility and Sterility · doi:10.1016/s0015-0282(98)00022-3 · Cited by 270
Self-citationAromatase and other steroidogenic genes in endometriosis: translational aspects.
Attar, E., & Bulun, S. E. (2006) · Human Reproduction Update · doi:10.1093/humupd/dmi034 · Cited by 255
“…and expression of protein and mRNA in the stromal cell component of endometriosis, whereas StAR or aromatase expression was either absent or barely detectable in the eutopic endometrium of disease-free women (Noble et al., 1996, 1997; Tsai et al., 2001; Gurates et al., 2002; Sun et al., 2003).”
BackgroundInfluentialSelf-citationAromatase: 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
Self-citationEndometriotic disease: the role of peritoneal fluid
Koninckx, P. (1998) · Human Reproduction Update · doi:10.1093/humupd/4.5.741 · Cited by 252
Endometrial alterations in endometriosis: a systematic review of putative biomarkers
May, K. E., Villar, J., Kirtley, S., Kennedy, S. H., & Becker, C. M. (2011) · Human Reproduction Update · doi:10.1093/humupd/dmr013 · Cited by 237
“Since Bulun’s initial report (Noble et al., 1996), there has been a great deal of interest in the possibility of endometrial aromatase expression identifying women with endometriosis.”
BackgroundAssessment of endometrial receptivity
Lessey, B. A. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2011.07.1095 · Cited by 235
Intratumoral Aromatase in Human Breast, Endometrial, and Ovarian Malignancies
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Anastrazole and oral contraceptives: a novel treatment for endometriosis
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Self-citationAromatase expression and regulation in breast and endometrial cancer
Zhao, H., Zhou, L., Shangguan, A. J., & Bulun, S. E. (2016) · Journal of Molecular Endocrinology · doi:10.1530/jme-15-0310 · Cited by 222
“Aromatase activity or mRNA cannot be induced by 466 PGE2 or cAMP analogs in stromal cells from disease-free women, which is the main molecular 467 mechanism responsible for increased expression of steroidogenic genes in stromal cells from 468 diseased tissue such as endometriosis (Bulun, et al. 2001; Noble et al. 1996…”
BackgroundSelf-citationPirtea, 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 232
Inflammation and nerve fiber interaction in endometriotic pain
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“This will be challenging , as the methylation defects may be rare occurrences in otherwise healthy stroma ; however , our preliminary findings show increased GATA6 and NR5A1 , as well as their downstream targets CYP19A1 and the steroidogenic acute regulatory protein STAR ( [ 50 , 79 ] and unpublished observations ) .”
Self-citationAttar, 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
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“We recently demonstrated, however, significant levels of P450arom mRNA and activity in the stromal cell component of endometriotic tissues, whereas aromatase expression is either only barely detectable or most commonly absent in the eutopic endometrium (7, 8).”
Self-citationEndometriosis and adenomyosis: shared pathophysiology
Bulun, S. E., Yildiz, S., Adli, M., Chakravarti, D., Parker, J. B., Milad, M., Yang, L., Chaudhari, A., Tsai, S., Wei, J. J., et al. (2023) · Fertility and Sterility · doi:10.1016/j.fertnstert.2023.03.006 · Cited by 216
Self-citationAdenomyosis: Review of the Literature
Garcia, L., & Isaacson, K. (2011) · Journal of Minimally Invasive Gynecology · doi:10.1016/j.jmig.2011.04.004 · Cited by 203
Adenomyosis pathogenesis: insights from next-generation sequencing
Bulun, S. E., Yıldız, Ş., Adli, M., & Wei, J. (2021) · Human Reproduction Update · doi:10.1093/humupd/dmab017 · Cited by 216
“The presence of aromatase activity and gene expression in adenomyotic tissue was reported even before they were revealed in endometriotic tissue (Yamamoto et al., 1993; Noble et al., 1996; Fang et al., 2002; Pavone and Bulun, 2012).”
BackgroundSelf-citationEndometriosis: A dysfunction and disease of the archimetra
Leyendecker, G. (1998) · Human Reproduction Update · doi:10.1093/humupd/4.5.752 · Cited by 199
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 202
“COX2 promotes an increase of the synthesis of prostaglandin E2 (PGE2 ), and PGE2 induces aromatase activity (CYP19A1), leading to E2 increased levels.”
BackgroundKinase signalling pathways in endometriosis: potential targets for non-hormonal therapeutics
McKinnon, B. D., Kocbek, V., Nirgianakis, K., Bersinger, N. A., & Mueller, M. D. (2016) · Human Reproduction Update · doi:10.1093/humupd/dmv060 · Cited by 195
“through endometrial cell expression of aromatase p450 (Noble et al., 1996) and a reduction in 17b-hydroxysteroid dehydrogenase type II”
BackgroundWu, Y., Strawn, E., Basir, Z., Halverson, G., & Guo, S.-W. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2006.05.077 · Cited by 193
Бурлев, В. А., Volkov, N. I., Pavlovitch, S. V., Lets, N., Larsson, A. O., & Olovsson, M. (2006) · Reproduction · doi:10.1530/rep.1.01110 · Cited by 192
“those of disease-free women (Noble et al. 1996).”
Aromatase inhibitors: the next generation of therapeutics for endometriosis?
Attar, E., & Bulun, S. E. (2006) · Fertility and Sterility · doi:10.1016/j.fertnstert.2005.09.064 · Cited by 184
Self-citationBruner‐Tran, K. L., Eisenberg, E., Yeaman, G. R., Anderson, T. A., McBean, J. H., & Osteen, K. G. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-020418 · Cited by 187
Follicular hormonal environment and embryo quality in women with endometriosis
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“P-450 aromatase enzyme than women without the disease (Noble et al., 1996; Kitawaki et al., 1997).”
BackgroundSmooth muscles are frequent components of endometriotic lesions
Anaf, V. (2000) · Human Reproduction · doi:10.1093/humrep/15.4.767 · Cited by 183
“P-450 aromatase, which converts androgens into oestrone and oestradiol, is not expressed in the endometrium of patients without endometriosis (Prefontaine et al., 1990; Noble et al., 1996; Kitawaki et al., 1997) but its expression has been demonstrated in the eutopic endometrium of patients with endometriosis and in t…”
BackgroundDHEA, Important Source of Sex Steroids in Men and Even More in Women
Labrie, F. (2010) · Progress in brain research · doi:10.1016/s0079-6123(10)82004-7 · Cited by 187
“Both steroidogenic acute regulatory protein (StAR) and aromatase are either absent or barely detectable in normal human endometrium – the lack of both enzymes preventing local estrogen formation (Gurates et al., 2002; Noble et al., 1996; Noble et al., 1997; Sun et al., 2003; Tsai et al., 2001).”
BackgroundKunz, G., Beil, D., Huppert, P., & Leyendecker, G. (2000) · Human Reproduction · doi:10.1093/humrep/15.1.76 · Cited by 177
“…expression of P450-aromatose resulting in elevated tissue concentrations of myometrium allowing the determination of the boundary between adenomyotic and normal tissue only by real-timeoestrogen has been demonstrated (Yamamoto et al., 1993; Noble et al., 1996, 1997; Kitawaki et al., 1997).”
BackgroundEndometriosis: A Disease That Remains Enigmatic
Acién, P., & Velasco, I. (2013) · ISRN Obstetrics and Gynecology · doi:10.1155/2013/242149 · Cited by 182
“Other alterations are related to the hormone dependence of ectopic endometrium, such as the expression of estrogen and progesterone-specific receptors [29] or the aberrant expression of active P450 aromatase [30].”
BackgroundEstrogen biosynthesis in endometriosis: molecular basis and clinical relevance
Bulun, S. E., Zeitoun, K. M., Takayama, K., & Sasano, H. (2000) · Journal of Molecular Endocrinology · doi:10.1677/jme.0.0250035 · Cited by 170
“Additionally, aromatase mRNA was also detected in the eutopic endometrial samples of women with moderate to severe endometriosis (but not in those of disease-free women) albeit in much smaller quantities compared with endometriotic implants (Noble et al. 1996).”
BackgroundInfluentialSelf-citationEndometrial 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
The Role of Endometrium in Endometriosis
Ulukuş, M., Çakmak, H., & Arici, A. M. (2006) · Journal of the Society for Gynecologic Investigation · doi:10.1016/j.jsgi.2006.07.005 · Cited by 173
Medical and surgical management of adenomyosis
Farquhar, C. M., & Brosens, I. A. (2006) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2006.01.012 · Cited by 171
Aghajanova, L., Hamilton, A., Kwintkiewicz, J., Vo, K. C., & Giudice, L. C. (2009) · Biology of Reproduction · doi:10.1095/biolreprod.108.070300 · Cited by 168
“expression in eutopic endometrium of women without endometriosis has been reported [43, 55, 71], and was confirmed in the current study using sensitive quantitative RT-PCR and endometrial samples from women without disease who had indications for surgical procedures that included uterine prolapse, pelvic pain, and a n…”
Huhtinen, K., Desai, R., Ståhle, M., Salminen, A., Handelsman, D. J., Perheentupa, A., & Poutanen, M. (2012) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-1154 · Cited by 195
The endometrium versus embryonic quality in endometriosis-related infertility
Garrido, N. (2002) · Human Reproduction Update · doi:10.1093/humupd/8.1.95 · Cited by 166
“Furthermore, it has been demonstrated that eutopic endometrium from women with endometriosis is able to express aromatase (the enzyme that catalyses the production of estradiol), and this suggests a possible mechanism by which implantation is damaged in these patients, although more efforts on this topic are needed to…”
BackgroundLocal 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
“An over-expression of this enzyme coupled with a decreased expression of the estrogen metabolizing enzyme (17hydroxysteroid dehydrogenase II) (90, 92, 93), increases bioavailable estrogen in the endometrium, potentially accounting for aberrantly high ESR1 and proliferation (32, 34, 94, 95).”
BackgroundChemokines and human reproduction
García-Velasco, J. A., & Arici, A. M. (1999) · Fertility and Sterility · doi:10.1016/s0015-0282(99)00120-x · Cited by 158
Kyama, C. M., Overbergh, L., Mihalyi, A., Meuleman, C., Mwenda, J. M., Mathieu, C., & D’Hooghe, T. M. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2007.02.057 · Cited by 157
Tsai, S.-J., Wu, M.-H., Lin, C.-C., Sun, H. S., & Chen, H.-M. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.12.8082 · Cited by 155
“Our results are in agreement with previous reports that the transcripts of aromatase were detected only in the endometriotic samples, not in normal endometrium (10, 12).”
BackgroundResultEstrogen Production and Metabolism in Endometriosis
Bulun, S. E., Yang, S., FANG, Z., Gürateş, B., Tamura, M., & Sebastian, S. (2002) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2002.tb02767.x · Cited by 153
Self-citationEstrogen metabolism and action in endometriosis
Rižner, T. L. (2009) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2009.03.022 · Cited by 153
Aromatase in endometriosis and uterine leiomyomata
Bulun, S. E., Imir, G., Utsunomiya, H., Thung, S., Gurates, B., Tamura, M., & Lin, Z. (2005) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2005.04.012 · Cited by 154
Self-citationCurrent Concepts in the Pathogenesis of Endometriosis
Witz, C. A. (1999) · Clinical Obstetrics & Gynecology · doi:10.1097/00003081-199909000-00013 · Cited by 151
Han, S. J., Hawkins, S. M., Begum, K., Jung, S. Y., Kovanci, E., Qin, J., Lydon, J. P., DeMayo, F. J., & O'Malley, B. W. (2012) · Nature Medicine · doi:10.1038/nm.2826 · Cited by 149
Endocrine Disorders Associated with Inappropriately High Aromatase Expression
Bulun, S. E., Noble, L. S., Takayama, K., Michael, M. D., Agarwal, V. R., Fisher, C., Zhao, Y., Hinshelwood, M. M., Ito, Y., & Simpson, E. R. (1997) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/s0960-0760(97)80004-0 · Cited by 148
Self-citationCurrent concepts of the pathogenesis of endometriosis
Osuga, Y. (2009) · Reproductive Medicine and Biology · doi:10.1007/s12522-009-0031-z · Cited by 147
Seli, E. U., Berkkanoğlu, M., & Arici, A. M. (2003) · Obstetrics and Gynecology Clinics of North America · doi:10.1016/s0889-8545(02)00052-9 · Cited by 147
A new concept of endometriosis and adenomyosis, tissue injury and repair (TIAR)
Leyendecker, G., & Wildt, L. (2011) · hmbci · doi:10.1515/hmbci.2011.002 · Cited by 147
Inflammatory Status Influences Aromatase and Steroid Receptor Expression in Endometriosis
Bukulmez, O., Hardy, D. B., Carr, B. R., Word, R. A., & Mendelson, C. R. (2008) · Endocrinology · doi:10.1210/en.2007-0665 · Cited by 186
“Aberrant expression of aromatase in endometriosis has previously been reported (16, 17).”
BackgroundEndometriosis: a premenopausal disease? Age pattern in 42,079 patients with endometriosis
Haas, D., Chvátal, R., Reichert, B., Renner, S. P., Shebl, O. J., Binder, H., Wurm, P., & Oppelt, P. (2012) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-012-2361-z · Cited by 149
Meinsohn, M.-C., Smith, O. E., Bertolin, K., & Murphy, B. D. (2019) · Physiological Reviews · doi:10.1152/physrev.00019.2018 · Cited by 146
Oestrogen deficiency in men: where are we today?
Faustini‐Fustini, M., Rochira, V., & Carani, C. (1999) · European Journal of Endocrinology · doi:10.1530/eje.0.1400111 · Cited by 148
Adenomyosis: the pathophysiology of an oestrogen-dependent disease
Kitawaki, J. (2006) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2006.01.010 · Cited by 143
Estrogen receptor-alpha (ER-alpha) and defects in uterine receptivity in women
Lessey, B. A., Palomino, W. A., Apparao, K. B. C., Young, S. L., & Lininger, R. A. (2006) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-4-s1-s9 · Cited by 147
Estrogen metabolizing enzymes in endometrium and endometriosis
Dassen, H., Punyadeera, C., Kamps, R., Delvoux, B., Van Langendonckt, A., Donnez, J., Husen, B., Thole, H., Dunselman, G., & Groothuis, P. (2007) · Human Reproduction · doi:10.1093/humrep/dem310 · Cited by 141
“Aromatase overexpression has now indeed been confirmed in numerous reports at the transcript level (Noble et al., 1996; Bulun et al., 1997; Matsuzaki et al., 2006; Smuc et al., 2007), at the protein level (Kitawaki et al., 1997,1999; Murakami et al., 2006; Velasco et al., 2006), as well as at the…”
BackgroundResultInfluentialTaniguchi, F. (2011) · Frontiers in Bioscience · doi:10.2741/e277 · Cited by 141
“Aromatase overexpression has recently been observed in endometriotic tissues (113, 114).”
BackgroundEnvironmental PCB exposure and risk of endometriosis
Louis, G. M. B., Weiner, J. M., Whitcomb, B. W., Sperrazza, R., Schisterman, E. F., Lobdell, D. T., Crickard, K., Greizerstein, H. B., & Kostyniak, P. J. (2004) · Human Reproduction · doi:10.1093/humrep/deh575 · Cited by 139
“Recently, Noble et al. (1996) reported that endometrial cysts might produce their own estrogens in situ from circulating androgens produced by adrenal glands.”
BackgroundRole of aromatase in endometrial disease
Bulun, S. E., Yang, S., Fang, Z., Gürateş, B., Tamura, M., Zhou, J., & Sebastian, S. (2001) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/s0960-0760(01)00134-0 · Cited by 137
Self-citationOral, E., & Arici, A. M. (1997) · Obstetrics and Gynecology Clinics of North America · doi:10.1016/s0889-8545(05)70301-6 · Cited by 133
Expression of estrogen receptor alpha and beta in peritoneal and ovarian endometriosis
Matsuzaki, S., Murakami, T., Uehara, S., Canis, M., Sasano, H., & Okamura, K. (2001) · Fertility and Sterility · doi:10.1016/s0015-0282(01)01783-6 · Cited by 133
Pathogenesis of endometriosis: The role of defective ‘immunosurveillance’
Christodoulakos, G., Augoulea, A., Lambrinoudaki, I., Sioulas, V., & Creatsas, G. (2007) · The European Journal of Contraception & Reproductive Health Care · doi:10.1080/13625180701387266 · Cited by 133
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
Ferrero, 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;…”
BackgroundKitawaki, J., Kusuki, I., Koshiba, H., Tsukamoto, K., Fushiki, S., & Honjo, H. (1999) · Fertility and Sterility · doi:10.1016/s0015-0282(99)00424-0 · Cited by 133
Akoum, A. (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)84754-1 · Cited by 132
Bulun, S. E., Fang, Z., İmir, G., Gürateş, B., Tamura, M., Yilmaz, B., Langoi, D., Amin, S. A., Yang, S., & Deb, S. (2004) · Seminars in Reproductive Medicine · doi:10.1055/s-2004-823026 · Cited by 131
“Among estrogen-responsive pelvic disorders, aromatase expression was studied in greatest detail in endometriosis.(6,7,22,23) First, extremely high levels of aromatase mRNA were found in extraovarian endometriotic implants and endometriomas.”
BackgroundResultSelf-citationEndometrial receptivity defects during IVF cycles with and without letrozole
Miller, P. B. W., Parnell, B. A., Bushnell, G., Tallman, N., Forstein, D. A., Higdon, H. L., Kitawaki, J., & Lessey, B. A. (2012) · Human Reproduction · doi:10.1093/humrep/der452 · Cited by 128
“The enzyme P450 aromatase is the expression in the eutopic endometrium of women with endometriosis (Noble et al., 1996; Kitawaki et al., 1999) and endometrial aromatase expression has been associated with poor reproductive outcomes in IVF (Brosens et al.”
BackgroundDistinct Regulation of Cyclooxygenase-2 by Interleukin-1β in Normal and Endometriotic Stromal Cells
Wu, M., Wang, C.-A., Lin, C.-C., Chen, L.-C., Chang, W., & Tsai, S. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-1612 · Cited by 128
Wiwatpanit, T., Murphy, A. R., Lu, Z., Urbanek, M., Burdette, J. E., Woodruff, T. K., & Kim, J. J. (2019) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgz100 · Cited by 124
Metadata
- Authors
- Noble, L. S., Simpson, E. R., Johns, A., & Bulun, S. E.
- Affiliations
- The University of Texas Southwestern Medical Center (US)
- ORCID
- Bulun, S E
- Venue
- The Journal of Clinical Endocrinology & Metabolism
- Publisher
- The Endocrine Society
- Published
- 1996-01
- Volume
- 81
- Issue
- 1
- Pages
- 174-179
- ISSN
- 0021-972X (ISSN-L)
- 1945-7197
- OpenAlex
- W2023838867
- Cited by
- 566
- References
- 10
- Citations by year
- 2025: 9 · 2024: 6 · 2023: 10 · 2022: 7 · 2021: 14 · 2020: 17 · 2019: 14 · 2018: 9 · 2017: 10 · 2016: 20 · 2015: 28 · 2014: 22 · 2013: 18 · 2012: 22
- FWCI
- 17.42
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Clinical Endocrinology & Metabolism (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute on Aging (R-37AG08174, R37AG008174)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Estrogen and related hormone effects
- Health Sciences › Medicine › Obstetrics and Gynecology › Endometrial and Cervical Cancer Treatments
- Keywords
- endometriosis, aromatase, P450arom, endometriotic implants, eutopic endometrium, estrogen synthesis, promoter usage, alternative splicing, tissue-specific gene expression, peritoneal endometriosis, aromatase mRNA expression
- MeSH terms
- Adult, Aromatase, Base Sequence, Endometriosis, Endometrium, Female, Humans, Molecular Sequence Data, Promoter Regions, Genetic, RNA, Messenger, Interleukin-6, Gene Expression Regulation, Enzymologic, Interleukin-11
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