Cited by 566Endometriosis Research and TreatmentEstrogen and related hormone effectsEndometrial and Cervical Cancer Treatments

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Aromatase expression in endometriosis.

Noble, L S, Simpson, E R, Johns, A, Bulun, S E·1996·The Journal of Clinical Endocrinology & Metabolism

DOI 10.1210/jcem.81.1.8550748

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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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Self-citation
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Background
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Background
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Background
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Background
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Aromatase expression in endometriotic tissues and its relationship to clinical and analytical findings
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Background
Cytokine pleiotropy and redundancy – gp130 cytokines in human implantation
Sánchez-Cuenca, J. M., Martín, J., Pellicer, A., & Simón, C. (1999) · Immunology Today · doi:10.1016/s0167-5699(98)01374-7 · Cited by 40
Risk Factors for Endometriosis in a German Case–Control Study
Burghaus, S., Klingsiek, P., Fasching, P. A., Engel, A., Häberle, L., Strissel, P. L., Schmidt, M., Jonas, K., Strehl, J. D., Hartmann, A., et al. (2011) · Geburtshilfe und Frauenheilkunde · doi:10.1055/s-0031-1280436 · Cited by 40
Emerging drugs in endometriosis
Mihalyi, A., Simsa, P., Kyama, C. M., Meuleman, C., Mwenda, J. M., & D’Hooghe, T. (2006) · Expert Opinion on Emerging Drugs · doi:10.1517/14728214.11.3.503 · Cited by 38
“In addition, aromatase mRNA has been detected in the eutopic endometrial samples of women with moderate-to-severe endometriosis, although in much smaller quantities than in endometriotic implants [72].”
Background
Vaporisation laser des endométriomes ovariens : impact sur la réponse aux gonadotrophines
Wyns, C., & Donnez, J. (2003) · Gynécologie Obstétrique & Fertilité · doi:10.1016/s1297-9589(03)00069-9 · Cited by 39
Impaired CRH and Urocortin Expression and Function in Eutopic Endometrium of Women with Endometriosis
Novembri, R., Borges, L. E., Carrarelli, P., Rocha, A. L. L., De Pascalis, F., Florio, P., & Petraglia, F. (2011) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2010-2263 · Cited by 38
Reduction in Endometrioma Size with Three Months of Aromatase Inhibition and Progestin Add-Back
Agarwal, S. K., & Foster, W. G. (2015) · BioMed Research International · doi:10.1155/2015/878517 · Cited by 38
“Endometriosis contains the aromatase enzyme [8], inhibition of which shrinks endometriosis lesions in postmenopausal women [9].”
Evaluation of clinical parameters and estrogen receptor alpha gene polymorphisms for patients with endometriosis
Renner, S. P., Strick, R., Oppelt, P., Fasching, P. A., Engel, S., Baumann, R., Beckmann, M. W., & Strissel, P. L. (2005) · Reproduction · doi:10.1530/rep.1.00787 · Cited by 37
“…expression of CYP19 and 17b-hydroxysteroid dehydrogenase type 2 (17-HSD2) was present in the lesions and uterine endometrium from patients (Noble et al. 1996, Kitawaki et al. 1999) but, in contrast, expression of 17b-hydroxysteroid dehydrogenase type 1 (17-HSD1) was deficient (Zeitoun et…”
Background
Expectant, Medical, and Surgical Management of Ovarian Endometriomas
Muzii, L., Galati, G., Mattei, G., Chinè, A., Perniola, G., Donato, V. D., Tucci, C. D., & Palaia, I. (2023) · Journal of Clinical Medicine · doi:10.3390/jcm12051858 · Cited by 44
“In patients with endometriosis, high levels of aromatase P450 enzyme expression have been shown in eutopic endometrial tissue as well as in ectopic endometrial implants [54].”
Background
Androgen receptor and 5α‐reductase are expressed in pelvic endometriosis
Carneiro, M. M., Morsch, D. M., Camargos, A. F., dos Reis, F. M., & Spritzer, P. M. (2007) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.2007.01521.x · Cited by 37
Concomitant treatment of severe uterine adenomyosis in a premenopausal woman with an aromatase inhibitor and a gonadotropin-releasing hormone agonist
Kimura, F., Takahashi, K., Takebayashi, K., Fujiwara, M., Kita, N., Noda, Y., & Harada, N. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2006.09.010 · Cited by 37
Role of nociceptor estrogen receptor GPR30 in a rat model of endometriosis pain
Álvarez, P., Bogen, O., & Levine, J. D. (2014) · Pain · doi:10.1016/j.pain.2014.09.035 · Cited by 37
“Because ectopic uterine tissue in humans [22,32,35,38,43,44,58] and rats [15] express the enzyme aromatase, which is critical for the synthesis of estrogen [10], locally produced estrogen acting on GPR30 might sensitize nociceptors innervating the endometriosis lesion.”
Background
Aromatase as a target for treating endometriosis
Mori, T., Ito, F., Koshiba, A., Kataoka, H., Tanaka, Y., Okimura, H., Khan, K. N., & Kitawaki, J. (2018) · Journal of obstetrics and gynaecology research · doi:10.1111/jog.13743 · Cited by 36
Three-Dimensional Biofabrication Models of Endometriosis and the Endometriotic Microenvironment
Wendel, J. R. H., Wang, X., Smith, L. J., & Hawkins, S. M. (2020) · Biomedicines · doi:10.3390/biomedicines8110525 · Cited by 35
“This de novo estrogen synthesis may be caused by available cholesterol coupled with increased aromatase [cytochrome p450, family 19a1 (CYP19A1)] and hydroxysteroid 17-beta dehydrogenase 1 (HSD17β1) expression, critical enzymes involved in estradiol synthesis [53-55].”
Background
Estrogen-induced stromal cell-derived factor-1 (SDF-1/Cxcl12) expression is repressed by progesterone and by Selective Estrogen Receptor Modulators via estrogen receptor α in rat uterine cells and tissues
Glace, L. E., Grygielko, E. T., Boyle, R., Wang, Q., Laping, N. J., Sulpizio, A. C., & Bray, J. D. (2009) · Steroids · doi:10.1016/j.steroids.2009.07.011 · Cited by 37
Functional Characterization of W147A: A High-Affinity Interleukin-11 Antagonist
Underhill-Day, N., McGovern, L. A., Karpovich, N., Mardon, H. J., Barton, V. A., & Heath, J. K. (2003) · Endocrinology · doi:10.1210/en.2002-0144 · Cited by 37
Medical Management of Endometriosis: Novel Targets and Approaches towards the Development of Future Treatment Regimes
Nothnick, W. B., & D’Hooghe, T. M. (2003) · Gynecologic and Obstetric Investigation · doi:10.1159/000072073 · Cited by 37
Potential for Estrogen Synthesis and Action in Human Normal and Neoplastic Thyroid Tissues
Valle, L. D. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.83.10.3702 · Cited by 37
Aromatase inhibitors for the treatment of endometriosis: a systematic review about efficacy, safety and early clinical development
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 39
Novel Promoter I.8 and Promoter Usage in the CYP19 (Aromatase) Gene
Demura, M., Reierstad, S., Innes, J. E., & Bulun, S. E. (2008) · Reproductive Sciences · doi:10.1177/1933719108322441 · Cited by 36
Self-citation
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
Vitamin D binding protein plays an important role in the progression of endometriosis
Hwang, J. H., Wang, T., Lee, K. S., JOO, J.-K., & Lee, H. (2013) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2013.1506 · Cited by 35
Macrophage Migration Inhibitory Factor Is Involved in a Positive Feedback Loop Increasing Aromatase Expression in Endometriosis
Veillat, V., Sengers, V., Metz, C. N., Roger, T., Leboeuf, M., Mailloux, J. R., & Akoum, A. (2012) · American Journal Of Pathology · doi:10.1016/j.ajpath.2012.05.018 · Cited by 35
“Aromatase, the key enzyme in estrogen synthesis, is upregulated in ectopic endometrial tissue.(19) Although challenged by some studies,(47,48) abnormal aromatase expression in ectopic and eutopic endometrial tissue of women with endometriosis and estrogen production has been confirmed by many other studies.”
Result
c-fos gene and protein expression in pelvic endometriosis: a local marker of estrogen action
Morsch, D. M., Carneiro, M. M., Lecke, S. B., Araujo, F. C., Camargos, A. F., dos Reis, F. M., & Spritzer, P. M. (2009) · Journal of Molecular Histology · doi:10.1007/s10735-009-9212-7 · Cited by 35
“*P = 0.011 c-fos in ECT vs. EU and C (oneway ANOVA followed by Duncan’s test) for the local synthesis of estrogens, normal endometrial tissue does not express aromatase gene (Noble et al. 1996).”
Influential
FOXO1 and c-jun transcription factors mRNA are modulated in endometriosis
Shazand, K., Baban, S., Privé, C., Malette, B., Croteau, P., Lagacé, M., Racine, J.-B., & Hugo, P. (2004) · Molecular Human Reproduction · doi:10.1093/molehr/gah119 · Cited by 35
“This observation recently found a molecular explanation through modulation of the genes involved in the metabolism of estradiol (E2), cyp19 encoding P450 aromatase (Noble et al., 1996) and 17bhydroxysteroid dehydrogenase type 2 enzyme (Zeitoun et al.”
Background
Ovarian hormones modulate monocyte chemotactic protein-1 expression in endometrial cells of women with endometriosis
Boucher, A. (2000) · Molecular Human Reproduction · doi:10.1093/molehr/6.7.618 · Cited by 35
Autoantibody Responses to Carbohydrate Epitopes in Endometriosis
Yeaman, G. R., COLLINS, J. E., & Lang, G. A. (2002) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2002.tb02778.x · Cited by 35
Risk of endometrial polyps in women with endometriosis: a meta-analysis
Zheng, Q., Mao, H., Zhao, Y.-J., Zhao, J., Wei, X., & Liu, P. (2015) · Reproductive Biology and Endocrinology · doi:10.1186/s12958-015-0092-2 · Cited by 34
“The expression patterns of ER and aromatase are both altered in endometriosis and EP patients [4, 6, 9, 11].”
Background
Estrogen induced changes in uterine brain-derived neurotrophic factor and its receptors
Wessels, J. M., Leyland, N. A., Agarwal, S. K., & Foster, W. G. (2015) · Human Reproduction · doi:10.1093/humrep/dev018 · Cited by 35
“…when mice were exposed to daily high dose estrogen, which models the chronic estrogen present in endometriotic lesions in women with endometriosis (Noble et al., 1996; Huhtinen et al., 2012) or other estrogen-dependent diseases, the exposure had profoundly different effects on the uterine…”
Background
Elinzanetant (NT-814), a Neurokinin 1,3 Receptor Antagonist, Reduces Estradiol and Progesterone in Healthy Women
Pawsey, S., Mills, E. G., Ballantyne, E., Donaldson, K. M., Kerr, M., Trower, M., & Dhillo, W. S. (2021) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgab108 · Cited by 34
Surface plasmon resonance imaging biosensors for aromatase based on a potent inhibitor and a specific antibody: Sensor development and application for biological material
Gorodkiewicz, E., Sankiewicz, A., & Laudański, P. (2014) · Open Chemistry · doi:10.2478/s11532-014-0512-8 · Cited by 34
Aromatase gene (CYP19A1) variants, female infertility and ovarian stimulation outcome: a preliminary report
Altmäe, S., Haller, K., Peters, M., Saare, M., Hovatta, O., Stavreus-Evers, A. C., Velthut‐Meikas, A., Karro, H., Metspalu, A., & Salumets, A. (2009) · Reproductive BioMedicine Online · doi:10.1016/s1472-6483(10)60009-0 · Cited by 34
“Although eutopic endometrial tissue lacks aromatase expression, elevated CYP19A1 transcription via the recruitment of ovarian-specific promoter PII is characteristic of pelvic endometriotic lesions (Noble et al., 1996; Zeitoun et al., 1999).”
Background
Peritoneal endometriotic lesions differentially express a haptoglobin-like gene*
Piva, M. A. (1999) · Molecular Human Reproduction · doi:10.1093/molehr/5.1.71 · Cited by 34
“Molecular Human Reproduction vol.5 no.1 pp. 71–78, 1999 Peritoneal endometriotic lesions differentially express a haptoglobin-like gene*”
Background
IMMUNOLOGY AND ENDOMETRIOSIS
Hill, J. A. (1997) · Obstetrics and Gynecology Clinics of North America · doi:10.1016/s0889-8545(05)70305-3 · Cited by 34
Paracrine regulation of endometriotic tissue
Minici, F., Tiberi, F., Tropea, A., Miceli, F., Orlando, M., Gangale, M. F., Romani, F., Catino, S., Campo, S., Lanzone, A., et al. (2007) · Gynecological Endocrinology · doi:10.1080/09513590701581721 · Cited by 33
“The principal mechanism responsible is the pathological expression of P450 aromatase in both eutopic and ectopic endometrium of women with endometriosis [9,10].”
Background
Estradiol-mediated hepatocyte growth factor is involved in the implantation of endometriotic cells via the mesothelial-to-mesenchymal transition in the peritoneum
Ono, Y. J., Hayashi, M., Tanabe, A., Hayashi, A., Kanemura, M., Terai, Y., & Ohmichi, M. (2015) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00573.2014 · Cited by 33
“It is reported that ectopic endometrium, including extraovarian endometriotic lesions and ovarian endometriomas, expresses elevated levels of aromatase P450, which leads to local production of estradiol by conversion of testosterone (23).”
Background
A predictive model for endometriosis
Wölfler, M. M., Nagele, F., Kolbus, A., Seidl, S., Schneider, B., Huber, J. C., & Tschugguel, W. (2005) · Human Reproduction · doi:10.1093/humrep/deh796 · Cited by 33
“Several earlier studies have shown that endometriosis and other pelvic pathologies are strongly associated with aberrantly high aromatase expression ( Noble et al., 1996; Bulun et al., 1997; Kitawaki et al., 1997).”
Background
Theories on the Pathogenesis of Endometriosis
Nap, A. W. (2011) · Wiley eBooks · doi:10.1002/9781444398519.ch5 · Cited by 33
Persistent bilateral ureteral obstruction secondary to endometriosis despite treatment with an aromatase inhibitor
Bohrer, J. C., Chen, C. C. G., & Falcone, T. (2008) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.03.040 · Cited by 32
Tumour necrosis factor- blockers: potential limitations in the management of advanced endometriosis? A Case Report
Shakiba, K. (2006) · Human Reproduction · doi:10.1093/humrep/del179 · Cited by 32
“Both the eutopic endometrium of women with endometriosis and the ectopic endometrial tissue may have the inherent capability to produce estrogen locally, as they were found to express P450 aromatase ( Noble et al., 1996 ).”
Background
Complementary approaches demonstrate that cellular aromatization in the bank vole testis is related to photoperiod
Kotula‐Balak, M., Słomczyńska, M., Fraczek, B., Bourguiba, S., Tabarowski, Z., Carreau, S., & Bilińska, B. (2009) · European Journal of Histochemistry · doi:10.4081/807 · Cited by 32
Steroid Sulfatase Expression in Ovarian Clear Cell Adenocarcinoma: Immunohistochemical Study
Okuda, T., Saito, H., Sekizawa, A., Shimizu, Y., Akamatsu, T., Kushima, M., Yanaihara, T., Okai, T., & Farina, A. (2001) · Gynecologic Oncology · doi:10.1006/gyno.2001.6322 · Cited by 32
Danazol inhibits aromatase activity of endometriosis-derived stromal cells by a competitive mechanism
Murakami, K., Nomura, K., Shinohara, K., Kasai, T., Shozu, M., & Inoue, M. (2006) · Fertility and Sterility · doi:10.1016/j.fertnstert.2005.12.074 · Cited by 31
Follicle-Stimulating Hormone Receptor Expression in Endometriotic Lesions and the Associated Vasculature: An Immunohistochemical Study
Robin, B., Planeix, F., Sastre‐Garau, X., Pichon, C., Olesen, T. K., Gogusev, J., & Ghinea, N. (2015) · Reproductive Sciences · doi:10.1177/1933719115623647 · Cited by 31
Soy product intake and premenopausal hysterectomy in a follow-up study of Japanese women
Nagata, C., Takatsuka, N., Kawakami, N., & Shimizu, H. (2001) · European Journal of Clinical Nutrition · doi:10.1038/sj.ejcn.1601223 · Cited by 31
“Uterine tissue has estro- gen receptors (Wang & Miksicek, 1994), and diseases originating from uterine tissue, such as uterine leiomyoma and endometriosis, are estrogen-dependent diseases (Burroughs et al, 1997; Noble et al, 1996).”
Background
Cyclic Adenosine 3′,5′-Monophosphate Response Element-Binding Protein and CCAAT/Enhancer-Binding Protein Mediate Prostaglandin E2-Induced Steroidogenic Acute Regulatory Protein Expression in Endometriotic Stromal Cells
Hsu, C.-C., Lu, C.-W., Huang, B.-M., Wu, M.-H., & Tsai, S.-J. (2008) · The American Journal of Pathology · doi:10.2353/ajpath.2008.080199 · Cited by 30

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
DOI: 10.1210/jcem.81.1.8550748
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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Aromatase expression in endometriosis.

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