{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,30]],"date-time":"2026-10-30T21:09:12Z","timestamp":1793394552702,"version":"4.5.0"},"reference-count":98,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2024,3,16]],"date-time":"2024-03-16T00:00:00Z","timestamp":1710547200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"National Natural Science Foundation of China","award":["NSFC 82301857"],"award-info":[{"award-number":["NSFC 82301857"]}]},{"name":"National Natural Science Foundation of China","award":["32370914"],"award-info":[{"award-number":["32370914"]}]},{"name":"National Natural Science Foundation of China","award":["92057119"],"award-info":[{"award-number":["92057119"]}]},{"name":"National Natural Science Foundation of China","award":["31970798"],"award-info":[{"award-number":["31970798"]}]},{"name":"National Natural Science Foundation of China","award":["2023YFC2705403"],"award-info":[{"award-number":["2023YFC2705403"]}]},{"name":"National Natural Science Foundation of China","award":["23ZR1408200"],"award-info":[{"award-number":["23ZR1408200"]}]},{"DOI":"10.13039\/501100012166","name":"National Key Research and Development Program of China","doi-asserted-by":"publisher","award":["NSFC 82301857"],"award-info":[{"award-number":["NSFC 82301857"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100012166","name":"National Key Research and Development Program of China","doi-asserted-by":"publisher","award":["32370914"],"award-info":[{"award-number":["32370914"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100012166","name":"National Key Research and Development Program of China","doi-asserted-by":"publisher","award":["92057119"],"award-info":[{"award-number":["92057119"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100012166","name":"National Key Research and Development Program of China","doi-asserted-by":"publisher","award":["31970798"],"award-info":[{"award-number":["31970798"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100012166","name":"National Key Research and Development Program of China","doi-asserted-by":"publisher","award":["2023YFC2705403"],"award-info":[{"award-number":["2023YFC2705403"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100012166","name":"National Key Research and Development Program of China","doi-asserted-by":"publisher","award":["23ZR1408200"],"award-info":[{"award-number":["23ZR1408200"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100007219","name":"Shanghai Natural Science Foundation","doi-asserted-by":"publisher","award":["NSFC 82301857"],"award-info":[{"award-number":["NSFC 82301857"]}],"id":[{"id":"10.13039\/100007219","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100007219","name":"Shanghai Natural Science Foundation","doi-asserted-by":"publisher","award":["32370914"],"award-info":[{"award-number":["32370914"]}],"id":[{"id":"10.13039\/100007219","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100007219","name":"Shanghai Natural Science Foundation","doi-asserted-by":"publisher","award":["92057119"],"award-info":[{"award-number":["92057119"]}],"id":[{"id":"10.13039\/100007219","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100007219","name":"Shanghai Natural Science Foundation","doi-asserted-by":"publisher","award":["31970798"],"award-info":[{"award-number":["31970798"]}],"id":[{"id":"10.13039\/100007219","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100007219","name":"Shanghai Natural Science Foundation","doi-asserted-by":"publisher","award":["2023YFC2705403"],"award-info":[{"award-number":["2023YFC2705403"]}],"id":[{"id":"10.13039\/100007219","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100007219","name":"Shanghai Natural Science Foundation","doi-asserted-by":"publisher","award":["23ZR1408200"],"award-info":[{"award-number":["23ZR1408200"]}],"id":[{"id":"10.13039\/100007219","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Shanghai Oriental Talent Plan","award":["NSFC 82301857"],"award-info":[{"award-number":["NSFC 82301857"]}]},{"name":"Shanghai Oriental Talent Plan","award":["32370914"],"award-info":[{"award-number":["32370914"]}]},{"name":"Shanghai Oriental Talent Plan","award":["92057119"],"award-info":[{"award-number":["92057119"]}]},{"name":"Shanghai Oriental Talent Plan","award":["31970798"],"award-info":[{"award-number":["31970798"]}]},{"name":"Shanghai Oriental Talent Plan","award":["2023YFC2705403"],"award-info":[{"award-number":["2023YFC2705403"]}]},{"name":"Shanghai Oriental Talent Plan","award":["23ZR1408200"],"award-info":[{"award-number":["23ZR1408200"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Endometriosis is a common estrogen-dependent condition that impacts 8\u201310% of women in their reproductive age, resulting in notable pain, morbidity, and infertility. Despite extensive research endeavors, the precise cause of endometriosis remains elusive, and the mechanisms contributing to its associated infertility are still not well comprehended. Natural killer (NK) cells, vital innate immune cells crucial for successful pregnancy, have been investigated for their potential involvement in the pathogenesis of endometriosis. Prior research has mainly concentrated on the diminished cytotoxicity of NK cells in endometrial fragments that evade the uterus. Interestingly, accumulating evidence suggests that NK cells play multifaceted roles in regulating the biology of endometrial stromal cells (ESCs), promoting local immune tolerance, influencing endometrial receptivity, oocyte development, and embryo implantation, thereby contributing to infertility and miscarriage in patients with endometriosis. In this comprehensive review, our goal is to summarize the current literature and provide an overview of the implications of NK cells in endometriosis, especially concerning infertility and pregnancy loss, under the influence of estrogen.<\/jats:p>","DOI":"10.3390\/ijms25063362","type":"journal-article","created":{"date-parts":[[2024,3,18]],"date-time":"2024-03-18T05:14:07Z","timestamp":1710738847000},"page":"3362","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":41,"title":["An Estrogen\u2013NK Cells Regulatory Axis in Endometriosis, Related Infertility, and Miscarriage"],"prefix":"10.3390","volume":"25","author":[{"given":"Shaoliang","family":"Yang","sequence":"first","affiliation":[{"name":"Lab of Reproductive Immunology, Hospital of Obstetrics and Gynecology, Fudan University, Shanghai 200011, China"},{"name":"Department of Gynecology of Integrated Traditional Chinese and Western Medicine, Hospital of Obstetrics and Gynecology, Fudan University, Shanghai 200011, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Haiyan","family":"Wang","sequence":"additional","affiliation":[{"name":"Department of Gynecology of Integrated Traditional Chinese and Western Medicine, Hospital of Obstetrics and Gynecology, Fudan University, Shanghai 200011, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2280-9727","authenticated-orcid":false,"given":"Dajin","family":"Li","sequence":"additional","affiliation":[{"name":"Lab of Reproductive Immunology, Hospital of Obstetrics and Gynecology, Fudan University, Shanghai 200011, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9276-0722","authenticated-orcid":false,"given":"Mingqing","family":"Li","sequence":"additional","affiliation":[{"name":"Lab of Reproductive Immunology, Hospital of Obstetrics and Gynecology, Fudan University, Shanghai 200011, China"},{"name":"Shanghai Key Laboratory of Female Reproductive Endocrine Related Diseases, Hospital of Obstetrics and Gynecology, Fudan University, Shanghai 200011, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,3,16]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"408","DOI":"10.1007\/s12325-018-0667-3","article-title":"Real-World Evaluation of Direct and Indirect Economic Burden among Endometriosis Patients in the United States","volume":"35","author":"Soliman","year":"2018","journal-title":"Adv. Ther."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.bpobgyn.2018.06.001","article-title":"Risk for and consequences of endometriosis: A critical epidemiologic review","volume":"51","author":"Shafrir","year":"2018","journal-title":"Best Pract. Res. Clin. Obstet. Gynaecol."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Marquardt, R.M., Kim, T.H., Shin, J.H., and Jeong, J.W. (2019). Progesterone and Estrogen Signaling in the Endometrium: What Goes Wrong in Endometriosis?. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20153822"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1048","DOI":"10.1210\/er.2018-00242","article-title":"Endometriosis","volume":"40","author":"Bulun","year":"2019","journal-title":"Endocr. Rev."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1351","DOI":"10.1016\/j.fertnstert.2003.09.076","article-title":"Estrogen up-regulates cyclooxygenase-2 via estrogen receptor in human uterine microvascular endothelial cells","volume":"81","author":"Tamura","year":"2004","journal-title":"Fertil. Steril."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"748","DOI":"10.1016\/j.molmed.2018.07.004","article-title":"The Immunopathophysiology of Endometriosis","volume":"24","author":"Symons","year":"2018","journal-title":"Trends Mol. Med."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"2286","DOI":"10.1016\/j.ajpath.2015.04.012","article-title":"Estradiol is a critical mediator of macrophage-nerve cross talk in peritoneal endometriosis","volume":"185","author":"Greaves","year":"2015","journal-title":"Am. J. Pathol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"720","DOI":"10.1093\/humupd\/dmaa062","article-title":"Uterine natural killer cells: From foe to friend in reproduction","volume":"27","author":"Alecsandru","year":"2021","journal-title":"Hum. Reprod. Update"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1111\/aji.12408","article-title":"Natural Killer Cells: Key Players in Endometriosis","volume":"74","author":"Thiruchelvam","year":"2015","journal-title":"Am. J. Reprod. Immunol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"e12817","DOI":"10.1111\/aji.12817","article-title":"Uterine natural killer cell progenitor populations predict successful implantation in women with endometriosis-associated infertility","volume":"79","author":"Glover","year":"2018","journal-title":"Am. J. Reprod. Immunol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"e13556","DOI":"10.1111\/aji.13556","article-title":"Peritoneal natural killer cell chemotaxis is decreased in women with pelvic endometriosis","volume":"88","author":"Ushiwaka","year":"2022","journal-title":"Am. J. Reprod. Immunol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"102615","DOI":"10.1016\/j.jri.2019.102615","article-title":"Expressions of natural cytotoxicity receptor, NKG2D and NKG2D ligands in endometriosis","volume":"136","author":"Xu","year":"2019","journal-title":"J. Reprod. Immunol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1620\/tjem.193.13","article-title":"Involvement of granule-mediated apoptosis in the cyclic changes of the normal human endometrium","volume":"193","author":"Igarashi","year":"2001","journal-title":"Tohoku J. Exp. Med."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"eabb7800","DOI":"10.1126\/sciimmunol.abb7800","article-title":"Continuous human uterine NK cell differentiation in response to endometrial regeneration and pregnancy","volume":"6","author":"Strunz","year":"2021","journal-title":"Sci. Immunol."},{"key":"ref_15","first-page":"564","article-title":"The endometrial immune environment of women with endometriosis","volume":"25","author":"Houshdaran","year":"2019","journal-title":"Hum. Reprod. Update"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"2387","DOI":"10.3389\/fimmu.2019.02387","article-title":"Uterine Immunity and Microbiota: A Shifting Paradigm","volume":"10","author":"Agostinis","year":"2019","journal-title":"Front. Immunol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"322","DOI":"10.1038\/mi.2016.50","article-title":"Composition and dynamics of the uterine NK cell KIR repertoire in menstrual blood","volume":"10","author":"Ivarsson","year":"2017","journal-title":"Mucosal. Immunol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"656","DOI":"10.1038\/nri886","article-title":"Natural killer cells and pregnancy","volume":"2","year":"2002","journal-title":"Nat. Rev. Immunol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"5746","DOI":"10.4049\/jimmunol.180.8.5746","article-title":"NK cells expressing a progesterone receptor are susceptible to progesterone-induced apoptosis","volume":"180","author":"Arruvito","year":"2008","journal-title":"J. Immunol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"633","DOI":"10.1016\/S1471-4906(01)02060-9","article-title":"The biology of human natural killer-cell subsets","volume":"22","author":"Cooper","year":"2001","journal-title":"Trends Immunol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"296","DOI":"10.5603\/FM.a2019.0095","article-title":"Endometrial immunocompetent cells in proliferative and secretory phase of normal menstrual cycle","volume":"79","year":"2020","journal-title":"Folia Morphol."},{"key":"ref_22","first-page":"1823","article-title":"Angiogenic growth factor messenger ribonucleic acids in uterine natural killer cells","volume":"86","author":"Li","year":"2001","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1016\/S0015-0282(16)58391-5","article-title":"Immunohistochemical characterization of stromal leukocytes in ovarian endometriosis: Comparison of eutopic and ectopic endometrium with normal endometrium","volume":"66","author":"Jones","year":"1996","journal-title":"Fertil. Steril."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Drury, J.A., Parkin, K.L., Coyne, L., Giuliani, E., Fazleabas, A.T., and Hapangama, D.K. (2018). The dynamic changes in the number of uterine natural killer cells are specific to the eutopic but not to the ectopic endometrium in women and in a baboon model of endometriosis. Reprod. Biol. Endocrinol. RB&E, 16.","DOI":"10.1186\/s12958-018-0385-3"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"262","DOI":"10.1111\/aji.12259","article-title":"Characterization of uterine NK cells in women with infertility or recurrent pregnancy loss and associated endometriosis","volume":"72","author":"Giuliani","year":"2014","journal-title":"Am. J. Reprod. Immunol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"493","DOI":"10.1111\/aji.12486","article-title":"Increased uNK Progenitor Cells in Women with Endometriosis and Infertility are Associated with Low Levels of Endometrial Stem Cell Factor","volume":"75","author":"Thiruchelvam","year":"2016","journal-title":"Am. J. Reprod. Immunol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1002\/path.6178","article-title":"Single-cell profiling identifies distinct hormonal, immunologic, and inflammatory signatures of endometriosis-constituting cells","volume":"261","author":"Shin","year":"2023","journal-title":"J. Pathol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"756","DOI":"10.4049\/jimmunol.0904192","article-title":"Fluctuation of peripheral blood T, B, and NK cells during a menstrual cycle of normal healthy women","volume":"185","author":"Lee","year":"2010","journal-title":"J. Immunol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1111\/j.1600-0897.1994.tb00843.x","article-title":"Flow cytometry analysis of lymphocyte subpopulations in peritoneal fluid of women with endometriosis","volume":"31","author":"Oosterlynck","year":"1994","journal-title":"Am. J. Reprod. Immunol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"157","DOI":"10.3109\/00016349309013364","article-title":"Changes of peripheral blood lymphocyte subsets before and after operation of patients with endometriosis","volume":"72","author":"Kikuchi","year":"1993","journal-title":"Acta Obstet. Gynecol. Scand."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1016\/j.jmig.2011.12.021","article-title":"Patients with endometriosis of the rectosigmoid have a higher percentage of natural killer cells in peripheral blood","volume":"19","author":"Dias","year":"2012","journal-title":"J. Minim. Invasive Gynecol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"711231","DOI":"10.3389\/fimmu.2021.711231","article-title":"A History of Endometriosis Is Associated with Decreased Peripheral NK Cytotoxicity and Increased Infiltration of Uterine CD68+ Macrophages","volume":"12","author":"Wang","year":"2021","journal-title":"Front. Immunol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1016\/S0015-0282(16)55224-8","article-title":"The natural killer activity of peritoneal fluid lymphocytes is decreased in women with endometriosis","volume":"58","author":"Oosterlynck","year":"1992","journal-title":"Fertil. Steril."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"18598","DOI":"10.1038\/s41598-020-75570-z","article-title":"Circulating CD56+ NKG2D+ NK cells and postoperative fertility in ovarian endometrioma","volume":"10","author":"Liu","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Meggyes, M., Szereday, L., Bohonyi, N., Koppan, M., Szegedi, S., Marics-Kutas, A., Marton, M., Totsimon, A., and Polgar, B. (2020). Different Expression Pattern of TIM-3 and Galectin-9 Molecules by Peripheral and Peritoneal Lymphocytes in Women with and without Endometriosis. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21072343"},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Zou, G., Wang, J., Xu, X., Xu, P., Zhu, L., Yu, Q., Peng, Y., Guo, X., Li, T., and Zhang, X. (2021). Cell subtypes and immune dysfunction in peritoneal fluid of endometriosis revealed by single-cell RNA-sequencing. Cell Biosci., 11.","DOI":"10.1186\/s13578-021-00613-5"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"103765","DOI":"10.1016\/j.jri.2022.103765","article-title":"Co-expression of activating and inhibitory receptors on peritoneal fluid NK cells in women with endometriosis","volume":"155","author":"Saeki","year":"2023","journal-title":"J. Reprod. Immunol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1134663","DOI":"10.3389\/fimmu.2023.1134663","article-title":"Peritoneal immune microenvironment of endometriosis: Role and therapeutic perspectives","volume":"14","author":"Chen","year":"2023","journal-title":"Front. Immunol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"930","DOI":"10.3389\/fimmu.2017.00930","article-title":"Developmental and Functional Control of Natural Killer Cells by Cytokines","volume":"8","author":"Wu","year":"2017","journal-title":"Front. Immunol."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Gong, H., Chen, Y., Xu, J., Xie, X., Yu, D., Yang, B., and Kuang, H. (2017). The regulation of ovary and conceptus on the uterine natural killer cells during early pregnancy. Reprod. Biol. Endocrinol. RB&E, 15.","DOI":"10.1186\/s12958-017-0290-1"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"5444","DOI":"10.4049\/jimmunol.1303400","article-title":"X-Chromosome complement and estrogen receptor signaling independently contribute to the enhanced TLR7-mediated IFN-\u03b1 production of plasmacytoid dendritic cells from women","volume":"193","author":"Laffont","year":"2014","journal-title":"J. Immunol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"405","DOI":"10.3389\/fimmu.2019.00405","article-title":"Physiological Regulation of Innate Lymphoid Cells","volume":"10","author":"Jacquelot","year":"2019","journal-title":"Front. Immunol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1006\/cimm.2002.1886","article-title":"Natural killer cells express estrogen receptor-alpha and estrogen receptor-beta and can respond to estrogen via a non-estrogen receptor-alpha-mediated pathway","volume":"214","author":"Curran","year":"2001","journal-title":"Cell. Immunol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"440","DOI":"10.1210\/jc.2002-021174","article-title":"Steroid receptor expression in uterine natural killer cells","volume":"88","author":"Henderson","year":"2003","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"ref_45","first-page":"1502","article-title":"Progesterone stimulates the induction of human endometrial CD56+ lymphocytes in an in vitro culture system","volume":"81","author":"Inoue","year":"1996","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1016\/0165-2478(93)90065-A","article-title":"Enhancing effect of 17 beta-estradiol on human NK cell activity","volume":"36","author":"Sorachi","year":"1993","journal-title":"Immunol. Lett."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"4011","DOI":"10.4049\/jimmunol.171.8.4011","article-title":"Coordinate regulation of lymphocyte-endothelial interactions by pregnancy-associated hormones","volume":"171","author":"Chantakru","year":"2003","journal-title":"J. Immunol."},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Ma, R., Jin, N., Lei, H., Dong, J., Xiong, Y., Qian, C., Chen, S., and Wang, X. (2023). Ovarian Stimulation in Mice Resulted in Abnormal Placentation through Its Effects on Proliferation and Cytokine Production of Uterine NK Cells. Int. J. Mol. Sci., 24.","DOI":"10.3390\/ijms24065907"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"308","DOI":"10.1007\/s12016-017-8648-x","article-title":"Sexual Dimorphism in Innate Immunity","volume":"56","author":"Jaillon","year":"2019","journal-title":"Clin. Rev. Allergy Immunol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"298","DOI":"10.1016\/j.phrs.2006.06.006","article-title":"Effects of hormone replacement therapy on plasma pro-inflammatory and anti-inflammatory cytokines and some bone turnover markers in postmenopausal women","volume":"54","author":"Vural","year":"2006","journal-title":"Pharmacol. Res."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1111\/acel.12326","article-title":"How sex and age affect immune responses, susceptibility to infections, and response to vaccination","volume":"14","author":"Berger","year":"2015","journal-title":"Aging Cell"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"1765","DOI":"10.1016\/j.intimp.2007.09.017","article-title":"Modulation of 17beta-estradiol on the number and cytotoxicity of NK cells in vivo related to MCM and activating receptors","volume":"7","author":"Hao","year":"2007","journal-title":"Int. Immunopharmacol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"1290","DOI":"10.1093\/humrep\/dev067","article-title":"Estrogen-dependent regulation of human uterine natural killer cells promotes vascular remodelling via secretion of CCL2","volume":"30","author":"Gibson","year":"2015","journal-title":"Hum. Reprod."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"6760","DOI":"10.4049\/jimmunol.173.11.6760","article-title":"Recruitment of uterine NK cells: Induction of CXC chemokine ligands 10 and 11 in human endometrium by estradiol and progesterone","volume":"173","author":"Sentman","year":"2004","journal-title":"J. Immunol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"9596","DOI":"10.1074\/jbc.RA120.012753","article-title":"The transcription factor HAND2 up-regulates transcription of the IL15 gene in human endometrial stromal cells","volume":"295","author":"Murata","year":"2020","journal-title":"J. Biol. Chem."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"1227","DOI":"10.1080\/13543784.2022.2152325","article-title":"Advances in targeting estrogen synthesis and receptors in patients with endometriosis","volume":"31","author":"Clemenza","year":"2022","journal-title":"Expert Opin. Investig. Drugs"},{"key":"ref_57","doi-asserted-by":"crossref","unstructured":"\u015acie\u017cy\u0144ska, A., Komorowski, M., Soszy\u0144ska, M., and Malejczyk, J. (2019). NK Cells as Potential Targets for Immunotherapy in Endometriosis. J. Clin. Med., 8.","DOI":"10.3390\/jcm8091468"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"574","DOI":"10.1038\/s41419-018-0581-2","article-title":"The ginsenoside PPD exerts anti-endometriosis effects by suppressing estrogen receptor-mediated inhibition of endometrial stromal cell autophagy and NK cell cytotoxicity","volume":"9","author":"Zhang","year":"2018","journal-title":"Cell Death Dis."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"1878","DOI":"10.7150\/ijbs.58657","article-title":"Protopanaxadiol improves endometriosis associated infertility and miscarriage in sex hormones receptors-dependent and independent manners","volume":"17","author":"Lai","year":"2021","journal-title":"Int. J. Biol. Sci."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"1376","DOI":"10.1080\/15548627.2018.1476809","article-title":"Suppression of autophagy and HCK signaling promotes PTGS2(high) FCGR3(-) NK cell differentiation triggered by ectopic endometrial stromal cells","volume":"14","author":"Mei","year":"2018","journal-title":"Autophagy"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1530\/REP-16-0089","article-title":"IL15 promotes growth and invasion of endometrial stromal cells and inhibits killing activity of NK cells in endometriosis","volume":"152","author":"Yu","year":"2016","journal-title":"Reproduction"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"751","DOI":"10.1093\/molehr\/gah233","article-title":"Differential regulation of interleukins IL-13 and IL-15 by ovarian steroids, TNF-alpha and TGF-beta in human endometrial epithelial and stromal cells","volume":"11","author":"Roberts","year":"2005","journal-title":"Mol. Hum. Reprod."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"785","DOI":"10.1007\/s40618-016-0435-7","article-title":"Aberrant expression and hormonal regulation of Galectin-3 in endometriosis women with infertility","volume":"39","author":"Yang","year":"2016","journal-title":"J. Endocrinol. Investig."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"e13533","DOI":"10.1111\/aji.13533","article-title":"Endometrial galectin-3 causes endometriosis by supporting eutopic endometrial cell survival and engraftment in the peritoneal cavity","volume":"87","author":"Yamashita","year":"2022","journal-title":"Am. J. Reprod. Immunol."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"e14","DOI":"10.4110\/in.2023.23.e14","article-title":"IL-17A and Th17 Cells Contribute to Endometrial Cell Survival by Inhibiting Apoptosis and NK Cell Mediated Cytotoxicity of Endometrial Cells via ERK1\/2 Pathway","volume":"23","author":"Kang","year":"2023","journal-title":"Immune Netw."},{"key":"ref_66","doi-asserted-by":"crossref","unstructured":"Lagan\u00e0, A.S., Garzon, S., G\u00f6tte, M., Vigan\u00f2, P., Franchi, M., Ghezzi, F., and Martin, D.C. (2019). The Pathogenesis of Endometriosis: Molecular and Cell Biology Insights. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20225615"},{"key":"ref_67","doi-asserted-by":"crossref","unstructured":"Radomska-Le\u015bniewska, D.M., Bia\u0142oszewska, A., and Kami\u0144ski, P. (2021). Angiogenic Properties of NK Cells in Cancer and Other Angiogenesis-Dependent Diseases. Cells, 10.","DOI":"10.3390\/cells10071621"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"106932","DOI":"10.1016\/j.vph.2021.106932","article-title":"17\u03b2-estradiol promotes angiogenesis through non-genomic activation of Smad1 signaling in endometriosis","volume":"142","author":"Zhao","year":"2022","journal-title":"Vascul. Pharmacol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"820","DOI":"10.1016\/j.immuni.2017.10.008","article-title":"The Broad Spectrum of Human Natural Killer Cell Diversity","volume":"47","author":"Freud","year":"2017","journal-title":"Immunity"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"e13166","DOI":"10.1111\/aji.13166","article-title":"Interleukin-22 secreted by ectopic endometrial stromal cells and natural killer cells promotes the recruitment of macrophages through promoting CCL2 secretion","volume":"82","author":"Mei","year":"2019","journal-title":"Am. J. Reprod. Immunol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"2783","DOI":"10.7150\/ijbs.35128","article-title":"Cyclooxygenase-2 in Endometriosis","volume":"15","author":"Lai","year":"2019","journal-title":"Int. J. Biol. Sci."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"2111","DOI":"10.1007\/s00018-019-03056-x","article-title":"Anti-inflammatory cytokines in endometriosis","volume":"76","author":"Zhou","year":"2019","journal-title":"Cell. Mol. Life Sci. CMLS"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1111\/aji.12206","article-title":"Expression of natural cytotoxicity receptors on peritoneal fluid natural killer cell and cytokine production by peritoneal fluid natural killer cell in women with endometriosis","volume":"71","author":"Funamizu","year":"2014","journal-title":"Am. J. Reprod. Immunol."},{"key":"ref_74","doi-asserted-by":"crossref","unstructured":"Olkowska-Truchanowicz, J., Bia\u0142oszewska, A., Zwierzchowska, A., Sztokfisz-Ignasiak, A., Janiuk, I., D\u0105browski, F., Korczak-Kowalska, G., Barcz, E., Bocian, K., and Malejczyk, J. (2021). Peritoneal Fluid from Patients with Ovarian Endometriosis Displays Immunosuppressive Potential and Stimulates Th2 Response. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms22158134"},{"key":"ref_75","doi-asserted-by":"crossref","unstructured":"Emori, M.M., and Drapkin, R. (2014). The hormonal composition of follicular fluid and its implications for ovarian cancer pathogenesis. Reprod. Biol. Endocrinol. RB&E, 12.","DOI":"10.1186\/1477-7827-12-60"},{"key":"ref_76","doi-asserted-by":"crossref","unstructured":"Drummond, A.E. (2006). The role of steroids in follicular growth. Reprod. Biol. Endocrinol. RB&E, 4.","DOI":"10.1186\/1477-7827-4-16"},{"key":"ref_77","doi-asserted-by":"crossref","unstructured":"Giacomini, E., Pagliardini, L., Minetto, S., Pinna, M., Kleeman, F., Bonesi, F., Makieva, S., Pavone, V., Reschini, M., and Papaleo, E. (2024). The relationship between CYP19A1 gene expression in luteinized granulosa cells and follicular estradiol output in women with endometriosis. J. Steroid Biochem. Mol. Biol., 237.","DOI":"10.1016\/j.jsbmb.2023.106439"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"1135","DOI":"10.1016\/S0015-0282(16)58327-7","article-title":"Flow cytometric evaluation of leukocyte subpopulations in the follicular fluids of infertile patients","volume":"65","author":"Lachapelle","year":"1996","journal-title":"Fertil. Steril."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"R45","DOI":"10.1530\/REP-19-0050","article-title":"Is there an immune modulating role for follicular fluid in endometriosis? A narrative review","volume":"159","author":"Prins","year":"2020","journal-title":"Reproduction"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1038\/s41420-021-00751-2","article-title":"Iron overload in endometriosis peritoneal fluid induces early embryo ferroptosis mediated by HMOX1","volume":"7","author":"Li","year":"2021","journal-title":"Cell Death Discov."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"777","DOI":"10.1093\/humrep\/17.3.777","article-title":"Embryotoxicity of peritoneal fluid in women with endometriosis. Its relation with cytokines and lymphocyte populations","volume":"17","author":"Campos","year":"2002","journal-title":"Hum. Reprod."},{"key":"ref_82","first-page":"145","article-title":"Effect of peritoneal fluid and serum from patients with endometriosis on mouse embryo in vitro development","volume":"54","author":"Tzeng","year":"1994","journal-title":"Chin. Med. J. Free China Ed"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"2538","DOI":"10.1016\/j.fertnstert.2009.11.011","article-title":"Attenuated oocyte fertilization and embryo development associated with altered growth factor\/signal transduction induced by endometriotic peritoneal fluid","volume":"93","author":"Ding","year":"2010","journal-title":"Fertil. Steril."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1016\/j.jri.2017.12.003","article-title":"Embryotoxic cytokines-Potential roles in embryo loss and fetal programming","volume":"125","author":"Robertson","year":"2018","journal-title":"J. Reprod. Immunol."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1071\/RD9930141","article-title":"Expression and regulation of the tumour necrosis factor-alpha gene in the female reproductive tract","volume":"5","author":"Hunt","year":"1993","journal-title":"Reprod. Fertil. Dev."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"1476","DOI":"10.1016\/j.fertnstert.2013.07.1985","article-title":"A tumor necrosis factor-\u03b1 inhibitor reduces the embryotoxic effects of endometriotic peritoneal fluid","volume":"100","author":"Chen","year":"2013","journal-title":"Fertil. Steril."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1016\/S0165-0378(97)00060-0","article-title":"Female steroid hormones regulate production of pro-inflammatory molecules in uterine leukocytes","volume":"35","author":"Hunt","year":"1997","journal-title":"J. Reprod. Immunol."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"728291","DOI":"10.3389\/fimmu.2021.728291","article-title":"Role of Decidual Natural Killer Cells in Human Pregnancy and Related Pregnancy Complications","volume":"12","author":"Zhang","year":"2021","journal-title":"Front. Immunol."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"eaaf7533","DOI":"10.1126\/scitranslmed.aaf7533","article-title":"Loss of HDAC3 results in nonreceptive endometrium and female infertility","volume":"11","author":"Kim","year":"2019","journal-title":"Sci. Transl. Med."},{"key":"ref_90","doi-asserted-by":"crossref","unstructured":"Adamczyk, M., Wender-Ozegowska, E., and Kedzia, M. (2022). Epigenetic Factors in Eutopic Endometrium in Women with Endometriosis and Infertility. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23073804"},{"key":"ref_91","doi-asserted-by":"crossref","unstructured":"Salmeri, N., Gennarelli, G., Vanni, V.S., Ferrari, S., Ruffa, A., Rovere-Querini, P., Pagliardini, L., Candiani, M., and Papaleo, E. (2023). Concomitant Autoimmunity in Endometriosis Impairs Endometrium-Embryo Crosstalk at the Implantation Site: A Multicenter Case-Control Study. J. Clin. Med., 12.","DOI":"10.3390\/jcm12103557"},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1093\/cei\/uxad029","article-title":"Single-cell transcriptome analysis reveals endometrial immune microenvironment in minimal\/mild endometriosis","volume":"212","author":"Huang","year":"2023","journal-title":"Clin. Exp. Immunol."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"826","DOI":"10.1016\/j.fertnstert.2022.12.042","article-title":"Endometriosis is associated with pregnancy loss: A nationwide historical cohort study","volume":"119","author":"Boje","year":"2023","journal-title":"Fertil. Steril."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"727","DOI":"10.1016\/j.fertnstert.2023.03.018","article-title":"Association of endometriosis and adenomyosis with pregnancy and infertility","volume":"119","author":"Vercellini","year":"2023","journal-title":"Fertil. Steril."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"392","DOI":"10.1016\/j.fertnstert.2023.02.030","article-title":"Endometriosis and pregnancy loss: The importance of mitigating sources of bias","volume":"120","author":"Zanardi","year":"2023","journal-title":"Fertil. Steril."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"725","DOI":"10.1093\/oxfordjournals.humrep.a138578","article-title":"Outcome of patients with endometriosis in assisted reproduction: Results from in-vitro fertilization and oocyte donation","volume":"9","author":"Vidal","year":"1994","journal-title":"Hum. Reprod."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"6741","DOI":"10.1038\/s41598-023-34045-7","article-title":"Impact of adenomyosis and endometriosis on IVF\/ICSI pregnancy outcome in patients undergoing gonadotropin-releasing hormone agonist treatment and frozen embryo transfer","volume":"13","author":"Wang","year":"2023","journal-title":"Sci. Rep."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"103477","DOI":"10.1016\/j.jri.2022.103477","article-title":"CD200S-positive granulated lymphoid cells in endometrium appear to be CD56-positive uterine NK cells","volume":"150","author":"Clark","year":"2022","journal-title":"J. Reprod. Immunol."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/25\/6\/3362\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T14:14:32Z","timestamp":1760105672000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/25\/6\/3362"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,3,16]]},"references-count":98,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2024,3]]}},"alternative-id":["ijms25063362"],"URL":"https:\/\/doi.org\/10.3390\/ijms25063362","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,3,16]]}}}