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Role of Thyroid Dysimmunity and Thyroid Hormones in Endometriosis

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Role of Thyroid Dysimmunity and Thyroid Hormones in Endometriosis Role of thyroid dysimmunity and thyroid hormones in endometriosis Marine Peyneaua, Niloufar Kaviana,b,c,d, Sandrine Chouzenouxa, Carole Niccoa, Mohamed Jeljelia,b,c, Laurie Toulleca, Jeanne Reboul-Martyb,e, Camille Chenevier-Gobeauxb,f, Fernando M. Reisa, Pietro Santullia,b,g, Ludivine Doridota,1, Charles Chaprona,b,g,1, and Frédéric Batteuxa,b,c,1,2 aInstitut Cochin, INSERM U1016, Université Paris Descartes, Sorbonne Paris Cité, 75679 Paris, France; bAssistance Publique–Hôpitaux de Paris, Hôpital Universitaire Paris Centre, Centre Hospitalier Universitaire Cochin, 75679 Paris, France; cService d’immunologie biologique, Université Paris Descartes, Sorbonne Paris Cité, 75679 Paris, France; dHKU Pasteur Research Pole, School of Public Health, The University of Hong Kong, Hong Kong, China; eDépartement d’Information Médicale, Université Paris Descartes, Sorbonne Paris Cité, 75679 Paris, France; fService de Diagnostic Biologique Automatisé, Université Paris Descartes, Sorbonne Paris Cité, 75679 Paris, France; and gDépartement de Gynécologie Obstétrique II et Médecine de la Reproduction, Université Paris Descartes, Sorbonne Paris Cité, 75679 Paris, France Edited by Lawrence Steinman, Stanford University School of Medicine, Stanford, CA, and approved April 29, 2019 (received for review December 4, 2018) Endometriosis is characterized by the presence of ectopic endo- thyroid-stimulating hormone (TSH) receptor Abs causing hy- metrial cells outside the uterine cavity. Thyroid autoimmunity has perthyroidism (16). Many studies have shown an association been associated with endometriosis. This work investigated the between the presence of thyroid Abs and endometriosis (11–13, potential pathophysiological link between endometriosis and 17), with AITD leading either to hypothyroidism or hyperthy- thyroid disorders. Transcripts and proteins involved in thyroid roidism (13). With endometriosis being characterized by a metabolism are dysregulated in eutopic and ectopic endometrium chronic inflammatory process, the high prevalence of AITD in of endometriotic patients, leading to resistance of ectopic endo- endometriosis patients could be the result of the immune dys- metrium to triiodothyronine (T3) action and local accumulation of regulation observed in women with endometriosis (6, 8). On the thyroxine (T4). Thyroid-stimulating hormone (TSH) acts as a pro- other hand, although no pathophysiological link has been dem- liferative and prooxidative hormone on all endometria of endometriosis onstrated so far, AITD and, more generally, thyroid dysfunction patients and controls, whereas T3 and T4 act to specifically increase may also have consequences on endometriosis progression. ectopic endometrial cell proliferation and reactive oxygen species (ROS) Thyroid involvement in endometrium and ovary physiology has production. Mouse studies confirmed the data gained in vitro since already been described (18, 19), and thyroid diseases are fre- endometriotic implants were found to be bigger when thyroid hor- quently associated with gynecological and obstetrical disorders mones increased. A retrospective analysis of endometriosis patients such as infertility, miscarriages, or preterm births (20). More- with or without a thyroid disorder revealed an increased chronic pelvic over, there are structural similarities and cross-reactions between pain and disease score in endometriotic patients with a thyroid disorder. TSH and the luteinizing hormone (LH), whose receptors are present on the uterus and ovaries and are implicated in endo- thyroid | thyroid hormones | endometriosis | oxidative stress | metriotic lesion growth (21). The aim of this study was to in- autoimmunity vestigate the interplay between endometriosis and AITD and, more precisely, to explore the consequences of thyroid disorders ndometriosis is a benign gynecological disorder affecting up on endometriosis evolution in vitro using endometrial and Eto 10% of women of reproductive age (1). Its characteristic endometriotic primary cell lines and tissue and in vivo using feature is the presence of ectopic endometrium outside the uterine cavity (2), which is responsible for severe inflammation Significance leading to pelvic pain and infertility (3, 4). The pathophysiology of endometriosis is still unclear, but the release of endometrial Endometriosis is a common gynecological disorder whose cells in the peritoneal cavity by retrograde menstrual reflux is physiopathology is still unclear. Thyroid autoimmunity has probably the most commonly accepted theory to explain the long been associated with endometriosis, without a mecha- presence of ectopic endometrium (5). However, menstrual reflux nistic explanation to link the two pathologies. First, we occurs in up to 90% of women, while endometriosis affects only showed that thyroid hormone metabolism is altered in endo- around 10%. Thus, additional factors must explain endometri- metriotic cells. Our in vitro study further revealed the pro- osis development (6, 7). Hormonal dysregulation with ectopic liferative and prooxidative roles of thyroid hormones in expression of aromatase leading to local production of estrogen, endometriotic cells. Finally, we confirmed the aggravating role along with progesterone resistance of ectopic tissue, is a hall- of thyroid hormones in endometriosis evolution in three dif- mark of endometriosis and contributes to lesion growth. Among ferent mouse models. In humans, thyroid disorders are asso- inflammatory factors, some authors have suggested autoimmu- ciated with more severe forms of endometriosis. Thus, thyroid nity as a major factor in endometriosis development (8). Indeed, function and thyroid hormone medication should be taken into endometriosis recapitulates some characteristics of autoimmune account for the care of women with endometriosis. disorders, such as chronic local inflammation associated with the presence of autoantibodies (Abs) (9, 10). Moreover, endome- Author contributions: N.K., F.M.R., C.C., and F.B. designed research; M.P., S.C., C.N., M.J., triosis is frequently associated with several other organ-specific L.T., C.C.-G., and L.D. performed research; J.R.-M., P.S., and C.C. contributed new reagents/ autoimmune diseases (11). Among them, autoimmune thyroid analytic tools; M.P., N.K., S.C., P.S., L.D., C.C., and F.B. analyzed data; and M.P., N.K., disorder(s) (AITD) have long been highlighted in endometriosis F.M.R., L.D., and F.B. wrote the paper. patients (11–13) suggesting a pathogenic association between The authors declare no conflict of interest. these two pathologies. Grave’s disease and Hashimoto’s thy- Published under the PNAS license. roiditis are the two main clinical presentations (14), resulting 1L.D., C.C., and F.B. contributed equally to this work. from a breach of tolerance against thyroid-specific antigens. 2To whom correspondence may be addressed. Email: [email protected]. Hashimoto’s thyroiditis is a chronic lymphocytic thyroiditis with This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. progressive destruction of the gland leading to hypothyroidism 1073/pnas.1820469116/-/DCSupplemental. (15). Grave’s disease is characterized by the presence of anti– Published online May 29, 2019. 11894–11899 | PNAS | June 11, 2019 | vol. 116 | no. 24 www.pnas.org/cgi/doi/10.1073/pnas.1820469116 Downloaded by guest on September 28, 2021 relevant mouse models of thyroiditis and endometriosis. Finally, patients compared with the endometrium of endometriosis-free a retrospective analysis of clinical features in endometriosis pa- patients (Fig. 1, 2). THRA2 encodes a truncated isoform of thy- tients with or without thyroid disorder was conducted. roid receptor, which is thus unable to bind triiodothyronine (T3) and acts as a competitive inhibitor of transcriptional activity of T3 (23). Results DIO2 is an enzyme responsible for the deiodination of the pro- Transcripts and Proteins Involved in Thyroid Hormone Signaling and hormone thyroxine (T4) into the bioactive T3, while DIO3 is re- Metabolism Are Dysregulated in Eutopic and Ectopic Endometrium of sponsible for deiodination of T4 and T3 into triiodothyronine inverse Endometriotic Patients. Clinical characteristics of the patients and diiodothyronine, two inactive metabolites of T3 and T4. We found 31.2-fold and 21.3-fold decreased DIO2 expression in ectopic whose biopsies were used for the qRT-PCR analysis are sum- P < P < marized in SI Appendix,S1. We confirmed that TSHR, THRA1, endometrium ( 0.01) and eutopic endometrium ( 0.05) from THRA2, THRB, and THRB1 were expressed in human endo- endometriotic patients compared with control endometrium, re- metrium at the messenger RNA (mRNA) and protein levels (19, spectively. This decreased expression was confirmed by Western blot TSHR analysis, especially in epithelial cells of ectopic lesions compared with 22). We found an increased expression of in ectopic en- P < 2 dometrium by a mean of 2.5-fold (P < 0.001) and of THRA2 by a controls ( 0.05) (Fig. 1, ); meanwhile, no difference was found P < for DIO3 expression in qRT-PCR and Western blot analysis. Al- mean of 3.3-fold compared with controls ( 0.01). There was THRA1 THRA2 DIO2 DIO3 no difference for these transcripts in eutopic endometrium of together, mRNA expression of , , ,and endometriosis patients compared with control endometrium suggests that ectopic endometrium of endometriotic biopsies may (Fig. 1, 1). An increased expression of LH receptors LHRa display decreased production of T3 and may be resistant
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