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Abnormal M1\/M2 polarization of decidual macrophages might predispose immune maladaptation in recurrent pregnancy loss (RPL). However, the mechanism of decidual macrophage polarization is unclear. We explored the role of Estradiol (E<jats:sub>2<\/jats:sub>)-sensitive serum-glucocorticoid regulated kinase (SGK) 1 in promoting macrophage polarization and suppressing inflammation at the maternal\u2013fetal interface.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Methods<\/jats:title>\n                <jats:p>We assessed serum levels of E<jats:sub>2<\/jats:sub> and progesterone during first trimester of pregnancy in women with or without threatened miscarriages (ended in live birth, <jats:italic>n<\/jats:italic>\u2009=\u2009448; or early miscarriages, <jats:italic>n<\/jats:italic>\u2009=\u200968). For detection of SGK1 in decidual macrophages, we performed immunofluorescence labeling and western blot analysis applying decidual samples from RPL (<jats:italic>n<\/jats:italic>\u2009=\u200993) and early normal pregnancy (<jats:italic>n<\/jats:italic>\u2009=\u200966). Human monocytic THP-1 cells were differentiated into macrophages and treated with Toll-like receptor (TLR) 4 ligand lipopolysaccharide (LPS), E<jats:sub>2<\/jats:sub>, inhibitors or siRNA for in vitro analysis. Flow cytometry analysis were conducted to detect macrophages polarization. We also applied ovariectomized (OVX) mice with hormones exploring the mechanisms underlying the regulation of SGK1 activation by E<jats:sub>2<\/jats:sub> in the decidual macrophages in vivo.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Results<\/jats:title>\n                <jats:p>SGK1 expression down regulation in the decidual macrophages of RPL was consistent with the lower concentration and slower increment of serum E<jats:sub>2<\/jats:sub> from 4 to 12\u00a0weeks of gestation seen in these compromised pregnancies. LPS reduced SGK1 activities, but induced the pro-inflammatory M1 phenotype of THP-1 monocyte-derived macrophages and T helper (Th) 1 cytokines that favored pregnancy loss. E<jats:sub>2<\/jats:sub> pretreatment promoted SGK1 activation in the decidual macrophages of OVX mice in vivo. E<jats:sub>2<\/jats:sub> pretreatment amplified SGK1 activation in TLR4-stimulated THP-1 macrophages in vitro through the estrogen receptor beta (ER\u03b2) and PI3K pathway. E<jats:sub>2<\/jats:sub>-sensitive activation of SGK1 increased M2 macrophages and Th2 immune responses, which were beneficial to successful pregnancy, by inducing <jats:italic>ARG1<\/jats:italic> and <jats:italic>IRF4<\/jats:italic> transcription, which are implicated in normal pregnancy. The experiments on OVX mice have shown that pharmacological inhibition of E<jats:sub>2<\/jats:sub> promoted nuclear translocation of NF-\u03baB in the decidual macrophages. Further more, pharmacological inhibition or knockdown of SGK1 in TLR4-stimulated THP-1 macrophages activated NF-\u03baB by promoting its nuclear translocation, leading to increased secretion of pro-inflammatory cytokines involved in pregnancy loss.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Conclusion<\/jats:title>\n                <jats:p>Our findings highlighted the immunomodulatory roles of E<jats:sub>2<\/jats:sub>-activated SGK1 in Th2 immune responses by priming anti-inflammatory M2 macrophages at the maternal\u2013fetal interface, resulting in a balanced immune microenvironment during pregnancy. Our results suggest new perspectives on future preventative strategies for RPL.<\/jats:p>\n              <\/jats:sec>","DOI":"10.1186\/s12958-023-01102-9","type":"journal-article","created":{"date-parts":[[2023,5,24]],"date-time":"2023-05-24T07:02:52Z","timestamp":1684911772000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":28,"title":["Estrogen-sensitive activation of SGK1 induces M2 macrophages with anti-inflammatory properties and a Th2 response at the maternal\u2013fetal interface"],"prefix":"10.1186","volume":"21","author":[{"given":"Yiyun","family":"Lou","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhujing","family":"Fu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ye","family":"Tian","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Minhao","family":"Hu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qijing","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuanyuan","family":"Zhou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ning","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qin","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fan","family":"Jin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2023,5,24]]},"reference":[{"key":"1102_CR1","doi-asserted-by":"publisher","first-page":"533","DOI":"10.1016\/j.fertnstert.2019.11.025","volume":"113","author":"Practice Committee of the American Society for Reproductive Medicine","year":"2020","unstructured":"Practice Committee of the American Society for Reproductive Medicine. 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The animal study protocol was approved by the Animal Ethics Committee of Zhejiang Chinese Medical University (protocol code 20211018\u201307, 20211129\u201319).","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare that they have no competing interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"50"}}