Estrogen Receptors and Endometriosis

Elodie Chantalat, Marie-Cécile Valera, Charlotte Vaysse, Emmanuelle Noirrit, Mariam Rusidze, Ariane Weyl, Kelig Vergriete, Etienne Buscail, Philippe Lluel, Coralie Fontaine, Jean-François Arnal, Françoise Lenfant, Elodie Chantalat, Marie-Cécile Valera, Charlotte Vaysse, Emmanuelle Noirrit, Mariam Rusidze, Ariane Weyl, Kelig Vergriete, Etienne Buscail, Philippe Lluel, Coralie Fontaine, Jean-François Arnal, Françoise Lenfant

Abstract

Endometriosis is a frequent and chronic inflammatory disease with impacts on reproduction, health and quality of life. This disorder is highly estrogen-dependent and the purpose of hormonal treatments is to decrease the endogenous ovarian production of estrogens. High estrogen production is a consistently observed endocrine feature of endometriosis. mRNA and protein levels of estrogen receptors (ER) are different between a normal healthy endometrium and ectopic/eutopic endometrial lesions: endometriotic stromal cells express extraordinarily higher ERβ and significantly lower ERα levels compared with endometrial stromal cells. Aberrant epigenetic regulation such as DNA methylation in endometriotic cells is associated with the pathogenesis and development of endometriosis. Although there is a large body of data regarding ERs in endometriosis, our understanding of the roles of ERα and ERβ in the pathogenesis of endometriosis remains incomplete. The goal of this review is to provide an overview of the links between endometriosis, ERs and the recent advances of treatment strategies based on ERs modulation. We will also attempt to summarize the current understanding of the molecular and cellular mechanisms of action of ERs and how this could pave the way to new therapeutic strategies.

Keywords: endometriosis; estrogen receptors; modulation; treatment strategy.

Conflict of interest statement

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

Figures

Figure 1
Figure 1
Schematic lateral view of the pelvis illustrating the 4 forms of endometriosis: 1: endometrioma (OMA); 2: superficial peritoneal endometriosis (SUP); 3: deep subperitoneal infiltrating endometriosis (DIE); 4: adenomyoma (Ad).
Figure 2
Figure 2
Respective roles of estrogen receptor α (ERα) and estrogen receptor β (ERβ) in the normal endometrium and endometriosis lesions. On the normal endometrium (left), 17β-estradiol (E2) coming from the circulation acts mainly on ERα while ERβ and G protein-coupled receptor 30 (GPR30) are less expressed. In contrast, in the endometrial lesions, ERβ expression is upregulated and the expression of ERα is attenuated. Moreover, there is a local accumulation of E2 mainly because the endometriotic lesions have the ability to synthetize E2 de novo from cholesterol, due to a higher expressions of steroidogenic acute regulatory protein (StAR) and CYP19A (aromatase), the two enzymes involved in the process of steroidogenesis.
Figure 3
Figure 3
Molecular pathways of ER regulation in endometriosis lesions. (A). Overexpression of ERβ in the stromal endometriotic cells inhibits the TNFα-mediated apoptosis, acts as a suppressor of ERα, induces interleukin-1, co-stimulates Ras-related estrogen-regulated growth inhibitor (RERG) and serum and glucocorticoid-regulated kinase (SGK1) as key ERβ targets with co-stimulating prostaglandin E2 (PGE2) under the action of estradiol. (B). De novo increase of 17β-Estradiol (E2) in endometriosis lesions affecting the ratio of ERα and ERβ, impacting the inflammation and expression of some target genes such as Greb-1 and c-Myc that results in endometriosis progression [2,27].

References

    1. Giudice L.C., Kao L.C. Endometriosis. Lancet. 2004;364:1789–1799. doi: 10.1016/S0140-6736(04)17403-5.
    1. Bulun S.E., Yilmaz B.D., Sison C., Miyazaki K., Bernardi L., Liu S., Kohlmeier A., Yin P., Milad M., Wei J. Endometriosis. Endocr. Rev. 2019;40:1048–1079. doi: 10.1210/er.2018-00242.
    1. Zondervan K.T., Becker C.M., Koga K., Missmer S.A., Taylor R.N., Vigano P. Endometriosis. Nat. Rev. Dis. Prim. 2018;4:9. doi: 10.1038/s41572-018-0008-5.
    1. Chantalat E., Vidal F., Leguevaque P., Lepage B., Lambaudie E., Hebert T., Motton S. Para-aortic workup in locally advanced cervical cancer: Heterogeneity is still the rule. Results from a retrospective multicenter study. Arch. Gynecol. Obstet. 2016;293:1081–1086. doi: 10.1007/s00404-015-3885-9.
    1. Bulun S.E. Endometriosis. New Engl. J. Med. 2009;360:268–279. doi: 10.1056/NEJMra0804690.
    1. Chapron C., Marcellin L., Borghese B., Santulli P. Rethinking mechanisms, diagnosis and management of endometriosis. Nat. Rev. Endocrinol. 2019;15:666–682. doi: 10.1038/s41574-019-0245-z.
    1. Prescott J., Farland L.V., Tobias D.K., Gaskins A.J., Spiegelman D., Chavarro J.E., Rich-Edwards J.W., Barbieri R.L., Missmer S.A. A prospective cohort study of endometriosis and subsequent risk of infertility. Hum. Reprod. 2016;31:1475–1482. doi: 10.1093/humrep/dew085.
    1. de Ziegler D., Borghese B., Chapron C. Endometriosis and infertility: Pathophysiology and management. Lancet. 2010;376:730–738. doi: 10.1016/S0140-6736(10)60490-4.
    1. Pluchino N., Wenger J.M., Petignat P., Tal R., Bolmont M., Taylor H.S., Bianchi-Demicheli F. Sexual function in endometriosis patients and their partners: Effect of the disease and consequences of treatment. Hum. Reprod. Update. 2016;22:762–774. doi: 10.1093/humupd/dmw031.
    1. Nnoaham K.E., Hummelshoj L., Webster P., d’Hooghe T., de Cicco Nardone F., de Cicco Nardone C., Jenkinson C., Kennedy S.H., Zondervan K.T., World Endometriosis Research Foundation Global Study of Women’s Health Consortium Impact of endometriosis on quality of life and work productivity: A multicenter study across ten countries. Fertil. Steril. 2011;96:366–373 e368. doi: 10.1016/j.fertnstert.2011.05.090.
    1. Canis M., Donnez J.G., Guzick D.S., Halme J.K., Rock J.A., Schenken R.S., Vernon M.W. Revised American Society for Reproductive Medicine classification of endometriosis: 1996. Fertil. Steril. 1997;67:817–821. doi: 10.1016/s0015-0282(97)81391-x.
    1. Wang W., Li R., Fang T., Huang L., Ouyang N., Wang L., Zhang Q., Yang D. Endometriosis fertility index score maybe more accurate for predicting the outcomes of in vitro fertilisation than r-AFS classification in women with endometriosis. Reprod. Biol. Endocrinol. 2013;11:112. doi: 10.1186/1477-7827-11-112.
    1. Foti P.V., Farina R., Palmucci S., Vizzini I.A.A., Libertini N., Coronella M., Spadola S., Caltabiano R., Iraci M., Basile A., et al. Endometriosis: Clinical features, MR imaging findings and pathologic correlation. Insights Imaging. 2018;9:149–172. doi: 10.1007/s13244-017-0591-0.
    1. Facchin F., Barbara G., Saita E., Mosconi P., Roberto A., Fedele L., Vercellini P. Impact of endometriosis on quality of life and mental health: Pelvic pain makes the difference. J. Psychosom. Obstet. Gynaecol. 2015;36:135–141. doi: 10.3109/0167482X.2015.1074173.
    1. Marki G., Bokor A., Rigo J., Rigo A. Physical pain and emotion regulation as the main predictive factors of health-related quality of life in women living with endometriosis. Hum. Reprod. 2017;32:1432–1438. doi: 10.1093/humrep/dex091.
    1. Minelli L., Fanfani F., Fagotti A., Ruffo G., Ceccaroni M., Mereu L., Landi S., Pomini P., Scambia G. Laparoscopic colorectal resection for bowel endometriosis: Feasibility, complications, and clinical outcome. Arch. Surg. 2009;144:234–239. doi: 10.1001/archsurg.2008.555.
    1. Guo S.W. Recurrence of endometriosis and its control. Hum. Reprod. Update. 2009;15:441–461. doi: 10.1093/humupd/dmp007.
    1. Millochau J.C., Abo C., Darwish B., Huet E., Dietrich G., Roman H. Continuous Amenorrhea May Be Insufficient to Stop the Progression of Colorectal Endometriosis. J. Minim. Invas. Gynecol. 2016;23:839–842. doi: 10.1016/j.jmig.2016.04.008.
    1. Sampson J.A. Metastatic or Embolic Endometriosis, due to the Menstrual Dissemination of Endometrial Tissue into the Venous Circulation. Am. J. Pathol. 1927;3:93–110.43.
    1. Khan A.W., Craig M., Jarmulowicz M., Davidson B.R. Liver tumours due to endometriosis and endometrial stromal sarcoma. HPB Offic. J. Int. Hepato Pancreat. Biliary Assoc. 2002;4:43–45. doi: 10.1080/136518202753598735.
    1. Koninckx P.R., Barlow D., Kennedy S. Implantation versus infiltration: The Sampson versus the endometriotic disease theory. Gynecol. Obstet. Invest. 1999;47:3–9. doi: 10.1159/000052853.
    1. Eychenne C., Suc B., Delchier M.C., Vidal F., Rimailho J., Illac C., Breibach F., Vaysse C., Chantalat E. Hepatic pedicle endometriosis: Case report and review of the literature. J. Obstet. Gynecol. Res. 2019;45:2121–2127. doi: 10.1111/jog.14078.
    1. Ahn S.H., Monsanto S.P., Miller C., Singh S.S., Thomas R., Tayade C. Pathophysiology and Immune Dysfunction in Endometriosis. BioMed Res. Int. 2015;2015:795976. doi: 10.1155/2015/795976.
    1. Greene A.D., Lang S.A., Kendziorski J.A., Sroga-Rios J.M., Herzog T.J., Burns K.A. Endometriosis: Where are we and where are we going? Reproduction. 2016;152:R63–R78. doi: 10.1530/REP-16-0052.
    1. Zhao Y., Gong P., Chen Y., Nwachukwu J.C., Srinivasan S., Ko C., Bagchi M.K., Taylor R.N., Korach K.S., Nettles K.W., et al. Dual suppression of estrogenic and inflammatory activities for targeting of endometriosis. Sci. Transl. Med. 2015;7 doi: 10.1126/scitranslmed.3010626.
    1. Bulun S.E., Monsavais D., Pavone M.E., Dyson M., Xue Q., Attar E., Tokunaga H., Su E.J. Role of estrogen receptor-beta in endometriosis. Semin. Reprod. Med. 2012;30:39–45. doi: 10.1055/s-0031-1299596.
    1. Tang Z.R., Zhang R., Lian Z.X., Deng S.L., Yu K. Estrogen-Receptor Expression and Function in Female Reproductive Disease. Cells. 2019;8:1123. doi: 10.3390/cells8101123.
    1. Zeitoun K.M., Bulun S.E. Aromatase: A key molecule in the pathophysiology of endometriosis and a therapeutic target. Fertil. Steril. 1999;72:961–969. doi: 10.1016/S0015-0282(99)00393-3.
    1. Mori T., Ito F., Koshiba A., Kataoka H., Takaoka O., Okimura H., Khan K.N., Kitawaki J. Local estrogen formation and its regulation in endometriosis. Reprod. Med. Biol. 2019;18:305–311. doi: 10.1002/rmb2.12285.
    1. Zeitoun K., Takayama K., Sasano H., Suzuki T., Moghrabi N., Andersson S., Johns A., Meng L., Putman M., Carr B., et al. Deficient 17beta-hydroxysteroid dehydrogenase type 2 expression in endometriosis: Failure to metabolize 17beta-estradiol. J. Clin. Endocrinol. Metab. 1998;83:4474–4480. doi: 10.1210/jcem.83.12.5301.
    1. Arnal J.F., Lenfant F., Metivier R., Flouriot G., Henrion D., Adlanmerini M., Fontaine C., Gourdy P., Chambon P., Katzenellenbogen B., et al. Membrane and Nuclear Estrogen Receptor Alpha Actions: From Tissue Specificity to Medical Implications. Physiol. Rev. 2017;97:1045–1087. doi: 10.1152/physrev.00024.2016.
    1. Ascenzi P., Bocedi A., Marino M. Structure-function relationship of estrogen receptor alpha and beta: Impact on human health. Mol. Aspects Med. 2006;27:299–402. doi: 10.1016/j.mam.2006.07.001.
    1. Sagae S., Monk B.J., Pujade-Lauraine E., Gaffney D.K., Narayan K., Ryu S.Y., McCormack M., Plante M., Casado A., Reuss A., et al. Advances and Concepts in Cervical Cancer Trials: A Road Map for the Future. Int. J. Gynecol. Cancer. 2016;26:199–207. doi: 10.1097/IGC.0000000000000587.
    1. Reslan O.M., Khalil R.A. Vascular effects of estrogenic menopausal hormone therapy. Rev. Recent Clin. Trials. 2012;7:47–70. doi: 10.2174/157488712799363253.
    1. Feldman R.D., Limbird L.E. GPER (GPR30): A Nongenomic Receptor (GPCR) for Steroid Hormones with Implications for Cardiovascular Disease and Cancer. Ann. Rev. Pharmacol. Toxicol. 2017;57:567–584. doi: 10.1146/annurev-pharmtox-010716-104651.
    1. Muka T., Vargas K.G., Jaspers L., Wen K.X., Dhana K., Vitezova A., Nano J., Brahimaj A., Colpani V., Bano A., et al. Estrogen receptor beta actions in the female cardiovascular system: A systematic review of animal and human studies. Maturitas. 2016;86:28–43. doi: 10.1016/j.maturitas.2016.01.009.
    1. Enmark E., Pelto-Huikko M., Grandien K., Lagercrantz S., Lagercrantz J., Fried G., Nordenskjold M., Gustafsson J.A. Human estrogen receptor beta-gene structure, chromosomal localization, and expression pattern. J. Clin. Endocrinol. Metab. 1997;82:4258–4265. doi: 10.1210/jcem.82.12.4470.
    1. Pellegrini C., Gori I., Achtari C., Hornung D., Chardonnens E., Wunder D., Fiche M., Canny G.O. The expression of estrogen receptors as well as GREB1, c-MYC, and cyclin D1, estrogen-regulated genes implicated in proliferation, is increased in peritoneal endometriosis. Fertil. Steril. 2012;98:1200–1208. doi: 10.1016/j.fertnstert.2012.06.056.
    1. Matsuzaki S., Murakami T., Uehara S., Canis M., Sasano H., Okamura K. Expression of estrogen receptor alpha and beta in peritoneal and ovarian endometriosis. Fertil. Steril. 2001;75:1198–1205. doi: 10.1016/S0015-0282(01)01783-6.
    1. Xue Q., Lin Z., Cheng Y.H., Huang C.C., Marsh E., Yin P., Milad M.P., Confino E., Reierstad S., Innes J., et al. Promoter methylation regulates estrogen receptor 2 in human endometrium and endometriosis. Biol. Reprod. 2007;77:681–687. doi: 10.1095/biolreprod.107.061804.
    1. Hewitt S.C., Harrell J.C., Korach K.S. Lessons in estrogen biology from knockout and transgenic animals. Annu. Rev. Physiol. 2005;67:285–308. doi: 10.1146/annurev.physiol.67.040403.115914.
    1. Bukulmez O., Hardy D.B., Carr B.R., Word R.A., Mendelson C.R. Inflammatory status influences aromatase and steroid receptor expression in endometriosis. Endocrinology. 2008;149:1190–1204. doi: 10.1210/en.2007-0665.
    1. Fujimoto J., Hirose R., Sakaguchi H., Tamaya T. Expression of oestrogen receptor-alpha and -beta in ovarian endometriomata. Mol. Hum. Reprod. 1999;5:742–747. doi: 10.1093/molehr/5.8.742.
    1. Monsivais 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. ERbeta- and prostaglandin E2-regulated pathways integrate cell proliferation via Ras-like and estrogen-regulated growth inhibitor in endometriosis. Mol. Endocrinol. 2014;28:1304–1315. doi: 10.1210/me.2013-1421.
    1. Cheng C.W., Licence D., Cook E., Luo F., Arends M.J., Smith S.K., Print C.G., Charnock-Jones D.S. Activation of mutated K-ras in donor endometrial epithelium and stroma promotes lesion growth in an intact immunocompetent murine model of endometriosis. J. Pathol. 2011;224:261–269. doi: 10.1002/path.2852.
    1. Maekawa R., Mihara Y., Sato S., Okada M., Tamura I., Shinagawa M., Shirafuta Y., Takagi H., Taketani T., Tamura H., et al. Aberrant DNA methylation suppresses expression of estrogen receptor 1 (ESR1) in ovarian endometrioma. J. Ovar. Res. 2019;12:14. doi: 10.1186/s13048-019-0489-1.
    1. Trukhacheva E., Lin Z., Reierstad S., Cheng Y.H., Milad M., Bulun S.E. Estrogen receptor (ER) beta regulates ERalpha expression in stromal cells derived from ovarian endometriosis. J. Clin. Endocrinol. Metab. 2009;94:615–622. doi: 10.1210/jc.2008-1466.
    1. Dyson M.T., Roqueiro D., Monsivais D., Ercan C.M., Pavone M.E., Brooks D.C., Kakinuma T., Ono M., Jafari N., Dai Y., et al. Genome-wide DNA methylation analysis predicts an epigenetic switch for GATA factor expression in endometriosis. PLoS Genet. 2014;10:e1004158. doi: 10.1371/journal.pgen.1004158.
    1. Han S.J., O’Malley B.W. The dynamics of nuclear receptors and nuclear receptor coregulators in the pathogenesis of endometriosis. Hum. Reprod. Update. 2014;20:467–484. doi: 10.1093/humupd/dmu002.
    1. Beliard A., Noel A., Foidart J.M. Reduction of apoptosis and proliferation in endometriosis. Fertil. Steril. 2004;82:80–85. doi: 10.1016/j.fertnstert.2003.11.048.
    1. Burns K.A., Rodriguez K.F., Hewitt S.C., Janardhan K.S., Young S.L., Korach K.S. Role of estrogen receptor signaling required for endometriosis-like lesion establishment in a mouse model. Endocrinology. 2012;153:3960–3971. doi: 10.1210/en.2012-1294.
    1. Burns K.A., Thomas S.Y., Hamilton K.J., Young S.L., Cook D.N., Korach K.S. Early Endometriosis in Females Is Directed by Immune-Mediated Estrogen Receptor alpha and IL-6 Cross-Talk. Endocrinology. 2018;159:103–118. doi: 10.1210/en.2017-00562.
    1. Han S.J., Jung S.Y., Wu S.P., Hawkins S.M., Park M.J., Kyo S., Qin J., Lydon J.P., Tsai S.Y., Tsai M.J., et al. Estrogen Receptor beta Modulates Apoptosis Complexes and the Inflammasome to Drive the Pathogenesis of Endometriosis. Cell. 2015;163:960–974. doi: 10.1016/j.cell.2015.10.034.
    1. Han S.J., Lee J.E., Cho Y.J., Park M.J., O’Malley B.W. Genomic Function of Estrogen Receptor beta in Endometriosis. Endocrinology. 2019;160:2495–2516. doi: 10.1210/en.2019-00442.
    1. Monsivais D., Dyson M.T., Yin P., Navarro A., Coon J.S.T., Pavone M.E., Bulun S.E. Estrogen receptor beta regulates endometriotic cell survival through serum and glucocorticoid-regulated kinase activation. Fertil. Steril. 2016;105:1266–1273. doi: 10.1016/j.fertnstert.2016.01.012.
    1. Brandenberger A.W., Lebovic D.I., Tee M.K., Ryan I.P., Tseng J.F., Jaffe R.B., Taylor R.N. Oestrogen receptor (ER)-alpha and ER-beta isoforms in normal endometrial and endometriosis-derived stromal cells. Mol. Hum. Reprod. 1999;5:651–655. doi: 10.1093/molehr/5.7.651.
    1. Othman E.E., Salama S., Ismail N., Al-Hendy A. Toward gene therapy of endometriosis: Adenovirus-mediated delivery of dominant negative estrogen receptor genes inhibits cell proliferation, reduces cytokine production, and induces apoptosis of endometriotic cells. Fertil. Steril. 2007;88:462–471. doi: 10.1016/j.fertnstert.2006.11.046.
    1. Xu Z., Zhang L., Yu Q., Zhang Y., Yan L., Chen Z.J. The estrogen-regulated lncRNA H19/miR-216a-5p axis alters stromal cell invasion and migration via ACTA2 in endometriosis. Mol. Hum. Reprod. 2019;25:550–561. doi: 10.1093/molehr/gaz040.
    1. Noble L.S., Takayama K., Zeitoun K.M., Putman J.M., Johns D.A., Hinshelwood M.M., Agarwal V.R., Zhao Y., Carr B.R., Bulun S.E. Prostaglandin E2 stimulates aromatase expression in endometriosis-derived stromal cells. J. Clin. Endocrinol. Metab. 1997;82:600–606. doi: 10.1210/jc.82.2.600.
    1. Sun H.S., Hsiao K.Y., Hsu C.C., Wu M.H., Tsai S.J. Transactivation of steroidogenic acute regulatory protein in human endometriotic stromalcells is mediated by the prostaglandin EP2 receptor. Endocrinology. 2003;144:3934–3942. doi: 10.1210/en.2003-0289.
    1. Tamura M., Deb S., Sebastian S., Okamura K., Bulun S.E. Estrogen up-regulates cyclooxygenase-2 via estrogen receptor in human uterine microvascular endothelial cells. Fertil. Steril. 2004;81:1351–1356. doi: 10.1016/j.fertnstert.2003.09.076.
    1. Daniels J., Gray R., Hills R.K., Latthe P., Buckley L., Gupta J., Selman T., Adey E., Xiong T., Champaneria R., et al. Laparoscopic uterosacral nerve ablation for alleviating chronic pelvic pain: A randomized controlled trial. Jama. 2009;302:955–961. doi: 10.1001/jama.2009.1268.
    1. Boretto M., Cox B., Noben M., Hendriks N., Fassbender A., Roose H., Amant F., Timmerman D., Tomassetti C., Vanhie A., et al. Development of organoids from mouse and human endometrium showing endometrial epithelium physiology and long-term expandability. Development. 2017;144:1775–1786. doi: 10.1242/dev.148478.
    1. Turco M.Y., Gardner L., Hughes J., Cindrova-Davies T., Gomez M.J., Farrell L., Hollinshead M., Marsh S.G.E., Brosens J.J., Critchley H.O., et al. Long-term, hormone-responsive organoid cultures of human endometrium in a chemically defined medium. Nat. Cell Biol. 2017;19:568–577. doi: 10.1038/ncb3516.
    1. Boretto M., Maenhoudt N., Luo X., Hennes A., Boeckx B., Bui B., Heremans R., Perneel L., Kobayashi H., Van Zundert I., et al. Patient-derived organoids from endometrial disease capture clinical heterogeneity and are amenable to drug screening. Nat. Cell Biol. 2019;21:1041–1051. doi: 10.1038/s41556-019-0360-z.
    1. Andersson S., Sundberg M., Pristovsek N., Ibrahim A., Jonsson P., Katona B., Clausson C.M., Zieba A., Ramstrom M., Soderberg O., et al. Insufficient antibody validation challenges oestrogen receptor beta research. Nat. Commun. 2017;8:15840. doi: 10.1038/ncomms15840.
    1. Samartzis N., Samartzis E.P., Noske A., Fedier A., Dedes K.J., Caduff R., Fink D., Imesch P. Expression of the G protein-coupled estrogen receptor (GPER) in endometriosis: A tissue microarray study. Reprod. Biol. Endocrinol. 2012;10:30. doi: 10.1186/1477-7827-10-30.
    1. Plante B.J., Lessey B.A., Taylor R.N., Wang W., Bagchi M.K., Yuan L., Scotchie J., Fritz M.A., Young S.L. G protein-coupled estrogen receptor (GPER) expression in normal and abnormal endometrium. Reprod. Sci. 2012;19:684–693. doi: 10.1177/1933719111431000.
    1. Heublein S., Vrekoussis T., Kuhn C., Friese K., Makrigiannakis A., Mayr D., Lenhard M., Jeschke U. Inducers of G-protein coupled estrogen receptor (GPER) in endometriosis: Potential implications for macrophages and follicle maturation. J. Reprod. Immunol. 2013;97:95–103. doi: 10.1016/j.jri.2012.10.013.
    1. Bedaiwy M.A., Allaire C., Yong P., Alfaraj S. Medical Management of Endometriosis in Patients with Chronic Pelvic Pain. Semin. Reprod. Med. 2017;35:38–53. doi: 10.1055/s-0036-1597308.
    1. Harris H.A., Bruner-Tran K.L., Zhang X., Osteen K.G., Lyttle C.R. A selective estrogen receptor-beta agonist causes lesion regression in an experimentally induced model of endometriosis. Hum. Reprod. 2005;20:936–941. doi: 10.1093/humrep/deh711.
    1. Falconer H., Mwenda J.M., Chai D.C., Wagner C., Song X.Y., Mihalyi A., Simsa P., Kyama C., Cornillie F.J., Bergqvist A., et al. Treatment with anti-TNF monoclonal antibody (c5N) reduces the extent of induced endometriosis in the baboon. Hum. Reprod. 2006;21:1856–1862. doi: 10.1093/humrep/del044.
    1. Olive D.L., Pritts E.A. Treatment of endometriosis. New Engl. J. Med. 2001;345:266–275. doi: 10.1056/NEJM200107263450407.
    1. Guo S.W., Groothuis P.G. Is it time for a paradigm shift in drug research and development in endometriosis/adenomyosis? Hum. Reprod. Update. 2018;24:577–598. doi: 10.1093/humupd/dmy020.
    1. Altintas D., Kokcu A., Kandemir B., Tosun M., Cetinkaya M.B. Comparison of the effects of raloxifene and anastrozole on experimental endometriosis. Eur. J. Obstet. Gynecol. Reprod. Biol. 2010;150:84–87. doi: 10.1016/j.ejogrb.2010.02.004.
    1. Stratton P., Sinaii N., Segars J., Koziol D., Wesley R., Zimmer C., Winkel C., Nieman L.K. Return of chronic pelvic pain from endometriosis after raloxifene treatment: A randomized controlled trial. Obstet. Gynecol. 2008;111:88–96. doi: 10.1097/01.AOG.0000297307.35024.b5.
    1. Kulak J., Jr., Fischer C., Komm B., Taylor H.S. Treatment with bazedoxifene, a selective estrogen receptor modulator, causes regression of endometriosis in a mouse model. Endocrinology. 2011;152:3226–3232. doi: 10.1210/en.2010-1010.
    1. Naqvi H., Sakr S., Presti T., Krikun G., Komm B., Taylor H.S. Treatment with bazedoxifene and conjugated estrogens results in regression of endometriosis in a murine model. Biol. Reprod. 2014;90:121. doi: 10.1095/biolreprod.113.114165.
    1. Flores V.A., Leone C., Taylor H.S., Stachenfeld N.S. Effects of bazedoxifene/conjugated estrogens on reproductive endocrinology and reproductive tract ultrasonographic appearance in premenopausal women: A preliminary study. Gynecol. Endocrinol. 2019;35:390–394. doi: 10.1080/09513590.2018.1559288.
    1. Khine Y.M., Taniguchi F., Nagira K., Nakamura K., Ohbayashi T., Osaki M., Harada T. New insights into the efficacy of SR-16234, a selective estrogen receptor modulator, on the growth of murine endometriosis-like lesions. Am. J. Reprod. Immunol. 2018;80:e13023. doi: 10.1111/aji.13023.
    1. Streuli I., de Ziegler D., Santulli P., Marcellin L., Borghese B., Batteux F., Chapron C. An update on the pharmacological management of endometriosis. Expert Opin. Pharmacother. 2013;14:291–305. doi: 10.1517/14656566.2013.767334.
    1. Attar E., Bulun S.E. Aromatase inhibitors: The next generation of therapeutics for endometriosis? Fertil. Steril. 2006;85:1307–1318. doi: 10.1016/j.fertnstert.2005.09.064.
    1. Abushahin F., Goldman K.N., Barbieri E., Milad M., Rademaker A., Bulun S.E. Aromatase inhibition for refractory endometriosis-related chronic pelvic pain. Fertil. Steril. 2011;96:939–942. doi: 10.1016/j.fertnstert.2011.07.1136.
    1. Amsterdam L.L., Gentry W., Jobanputra S., Wolf M., Rubin S.D., Bulun S.E. Anastrazole and oral contraceptives: A novel treatment for endometriosis. Fertil. Steril. 2005;84:300–304. doi: 10.1016/j.fertnstert.2005.02.018.
    1. Takayama K., Zeitoun K., Gunby R.T., Sasano H., Carr B.R., Bulun S.E. Treatment of severe postmenopausal endometriosis with an aromatase inhibitor. Fertil. Steril. 1998;69:709–713. doi: 10.1016/S0015-0282(98)00022-3.
    1. Gargiulo A.R., Strauss J.F., Barbieri R.L. Yen & Jaffe’s Reproductive Endocrinology E-Book: Physiology, Pathophysiology, and Clinical Management. 8th ed. Elsevier; Amsterdam, The Netherlands: 2019. pp. 609–642.
    1. Abdul Karim A.K., Shafiee M.N., Abd Aziz N.H., Omar M.H., Abdul Ghani N.A., Lim P.S., Md Zin R.R., Mokhtar N. Reviewing the role of progesterone therapy in endometriosis. Gynecol. Endocrinol. 2019;35:10–16. doi: 10.1080/09513590.2018.1490404.
    1. Bedaiwy M.A., Alfaraj S., Yong P., Casper R. New developments in the medical treatment of endometriosis. Fertil. Steril. 2017;107:555–565. doi: 10.1016/j.fertnstert.2016.12.025.
    1. Zhang T., De Carolis C., Man G.C.W., Wang C.C. The link between immunity, autoimmunity and endometriosis: A literature update. Autoimmun. Rev. 2018;17:945–955. doi: 10.1016/j.autrev.2018.03.017.
    1. Ferlita A., Battaglia R., Andronico F., Caruso S., Cianci A., Purrello M., Pietro C.D. Non-Coding RNAs in Endometrial Physiopathology. Int. J. Mol. Sci. 2018;19:2120. doi: 10.3390/ijms19072120.

Source: PubMed

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