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Uterine PGR responds to the heightened levels of ovarian progesterone (P4) after ovulation and regulates uterine gene transcription for successful embryo implantation. Although epithelial and stromal P4-PGR signaling may interact with each other to form appropriate endometrial milieu for uterine receptivity and the subsequent embryo attachment, it remains unclear what the specific roles of epithelial P4-PGR signaling in the adult uterus are. Here we generated mice with epithelial deletion of Pgr in the adult uterus (Pgrfl\/flLtfCre\/+ mice) by crossing Pgr-floxed and Ltf-Cre mice. Pgrfl\/flLtfCre\/+ mice are infertile due to the impairment of embryo attachment. Pgrfl\/flLtfCre\/+ uteri did not exhibit epithelial growth arrest, suggesting compromised uterine receptivity. Both epithelial and stromal expressions of P4-responsive genes decreased in Pgrfl\/flLtfCre\/+ mice during the peri-implantation period, indicating that epithelial Pgr deletion affects not only epithelial but stromal P4 responsiveness. In addition, uterine LIF, an inducer of embryo attachment, was decreased in Pgrfl\/flLtfCre\/+ mice. The RNA-seq analysis using luminal epithelial specimens dissected out by laser capture microdissection revealed that the signaling pathways related to extracellular matrix, cell adhesion, and cell proliferation are altered in Pgr\u2009fl\/flLtf\u2009Cre\/+ mice. These findings suggest that epithelial PGR controls both epithelial and stromal P4 responsiveness and epithelial cell differentiation, which provides normal uterine receptivity and subsequent embryo attachment.<\/jats:p>","DOI":"10.1210\/endocr\/bqaa195","type":"journal-article","created":{"date-parts":[[2020,10,24]],"date-time":"2020-10-24T22:40:41Z","timestamp":1603579241000},"source":"Crossref","is-referenced-by-count":38,"title":["Uterine Epithelial Progesterone Receptor Governs Uterine Receptivity Through Epithelial Cell Differentiation"],"prefix":"10.1210","volume":"161","author":[{"given":"Mona","family":"Gebril","sequence":"first","affiliation":[{"name":"Department of Obstetrics and Gynecology, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan"},{"name":"Reproductive Health Department, National Research Center of Egypt, Cairo, Egypt"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0241-9780","authenticated-orcid":false,"given":"Yasushi","family":"Hirota","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shizu","family":"Aikawa","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yamato","family":"Fukui","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tetsuaki","family":"Kaku","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mitsunori","family":"Matsuo","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tomoyuki","family":"Hirata","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shun","family":"Akaeda","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Takehiro","family":"Hiraoka","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ryoko","family":"Shimizu-Hirota","sequence":"additional","affiliation":[{"name":"Department of Internal Medicine, Center for Preventive Medicine, School of Medicine, Keio University, Tokyo, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Norihiko","family":"Takeda","sequence":"additional","affiliation":[{"name":"Center for Molecular Medicine, Jichi Medical University, Shimotuke, Tochigi, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tamer","family":"Taha","sequence":"additional","affiliation":[{"name":"Reproductive Health Department, National Research Center of Egypt, Cairo, Egypt"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Osama Al","family":"Balah","sequence":"additional","affiliation":[{"name":"Department of Medical Application of Laser, National Institute of Laser Enhanced Sciences, Cairo University, Giza, Egypt"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mohamed Amr H","family":"Elnoury","sequence":"additional","affiliation":[{"name":"Department of Medical Application of Laser, National Institute of Laser Enhanced Sciences, Cairo University, Giza, Egypt"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tomoyuki","family":"Fujii","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yutaka","family":"Osuga","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"80","published-online":{"date-parts":[[2020,10,24]]},"reference":[{"issue":"12","key":"2021121718174412300_CIT0001","doi-asserted-by":"crossref","first-page":"1754","DOI":"10.1038\/nm.3012","article-title":"Mechanisms of implantation: strategies for successful pregnancy","volume":"18","author":"Cha","year":"2012","journal-title":"Nat Med."},{"issue":"4","key":"2021121718174412300_CIT0002","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1007\/s12522-013-0153-1","article-title":"Uterine receptivity and embryo-uterine interactions in embryo implantation: lessons from mice","volume":"12","author":"Egashira","year":"2013","journal-title":"Reprod Med Biol."},{"issue":"3","key":"2021121718174412300_CIT0003","doi-asserted-by":"crossref","first-page":"234","DOI":"10.1002\/rmb2.12280","article-title":"Uterine receptivity, embryo attachment, and embryo invasion: multistep processes in embryo implantation","volume":"18","author":"Fukui","year":"2019","journal-title":"Reprod Med Biol."},{"issue":"3","key":"2021121718174412300_CIT0004","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1507\/endocrj.EJ18-0431","article-title":"Progesterone governs endometrial proliferation-differentiation switching and blastocyst implantation","volume":"66","author":"Hirota","year":"2019","journal-title":"Endocr J."},{"issue":"8","key":"2021121718174412300_CIT0005","doi-asserted-by":"crossref","first-page":"1428","DOI":"10.1210\/me.2011-1355","article-title":"Research resource: genome-wide profiling of progesterone receptor binding in the mouse uterus","volume":"26","author":"Rubel","year":"2012","journal-title":"Mol Endocrinol."},{"issue":"2","key":"2021121718174412300_CIT0006","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1002\/gene.20098","article-title":"Cre-mediated recombination in cell lineages that express the progesterone 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implantation","volume":"102","author":"Tranguch","year":"2005","journal-title":"Proc Natl Acad Sci U S A."},{"issue":"1","key":"2021121718174412300_CIT0010","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1172\/JCI92862","article-title":"Polycomb subunit BMI1 determines uterine progesterone responsiveness essential for normal embryo implantation","volume":"128","author":"Xin","year":"2018","journal-title":"J Clin Invest."},{"issue":"5","key":"2021121718174412300_CIT0011","doi-asserted-by":"crossref","first-page":"1489","DOI":"10.1038\/s41418-019-0429-z","article-title":"Uterine deficiency of high-mobility group box-1 (HMGB1) protein causes implantation defects and adverse pregnancy outcomes","volume":"27","author":"Aikawa","year":"2020","journal-title":"Cell Death Differ."},{"issue":"10","key":"2021121718174412300_CIT0012","doi-asserted-by":"crossref","first-page":"1204","DOI":"10.1038\/ng1874","article-title":"Indian hedgehog is a major mediator of progesterone signaling in the mouse uterus","volume":"38","author":"Lee","year":"2006","journal-title":"Nat Genet."},{"issue":"6019","key":"2021121718174412300_CIT0013","doi-asserted-by":"crossref","first-page":"912","DOI":"10.1126\/science.1197454","article-title":"The antiproliferative action of progesterone in uterine epithelium is mediated by Hand2","volume":"331","author":"Li","year":"2011","journal-title":"Science."},{"issue":"3","key":"2021121718174412300_CIT0014","doi-asserted-by":"crossref","first-page":"1218","DOI":"10.1096\/fj.11-193334","article-title":"Epithelial progesterone receptor exhibits pleiotropic roles in uterine development and function","volume":"26","author":"Franco","year":"2012","journal-title":"Faseb J."},{"issue":"2","key":"2021121718174412300_CIT0015","doi-asserted-by":"crossref","first-page":"386","DOI":"10.1095\/biolreprod.111.091769","article-title":"Postnatal deletion of Wnt7a inhibits uterine gland morphogenesis and compromises adult fertility in mice","volume":"85","author":"Dunlap","year":"2011","journal-title":"Biol Reprod."},{"issue":"5","key":"2021121718174412300_CIT0016","doi-asserted-by":"crossref","first-page":"146","DOI":"10.1095\/biolreprod.111.097089","article-title":"Progesterone inhibits uterine gland development in the neonatal mouse uterus","volume":"86","author":"Filant","year":"2012","journal-title":"Biol Reprod."},{"key":"2021121718174412300_CIT0017","doi-asserted-by":"crossref","first-page":"38078","DOI":"10.1038\/srep38078","article-title":"Uterine glands impact uterine receptivity, luminal fluid homeostasis and blastocyst implantation","volume":"6","author":"Kelleher","year":"2016","journal-title":"Sci Rep."},{"issue":"7","key":"2021121718174412300_CIT0018","doi-asserted-by":"crossref","first-page":"2718","DOI":"10.1210\/en.2014-1265","article-title":"Lactoferrin-iCre: a new mouse line to study uterine epithelial gene 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ligand-dependent manner by the progesterone receptor","volume":"146","author":"Jeong","year":"2005","journal-title":"Endocrinology."},{"issue":"7","key":"2021121718174412300_CIT0046","doi-asserted-by":"crossref","first-page":"1824","DOI":"10.1172\/JCI31622","article-title":"FKBP52 deficiency-conferred uterine progesterone resistance is genetic background and pregnancy stage specific","volume":"117","author":"Tranguch","year":"2007","journal-title":"J Clin Invest."},{"issue":"12","key":"2021121718174412300_CIT0047","doi-asserted-by":"crossref","first-page":"5503","DOI":"10.1210\/en.2006-0040","article-title":"Overlapping and distinct expression of progesterone receptors A and B in mouse uterus and mammary gland during the estrous cycle","volume":"147","author":"Mote","year":"2006","journal-title":"Endocrinology."},{"issue":"2","key":"2021121718174412300_CIT0048","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1095\/biolreprod.116.144410","article-title":"Decreased epithelial progesterone receptor A at the window of receptivity is required for preparation of the endometrium for embryo attachment","volume":"96","author":"Wetendorf","year":"2017","journal-title":"Biol Reprod."}],"container-title":["Endocrinology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/endo\/advance-article-pdf\/doi\/10.1210\/endocr\/bqaa195\/34025519\/bqaa195.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/endo\/article-pdf\/161\/12\/bqaa195\/41812431\/bqaa195.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/endo\/article-pdf\/161\/12\/bqaa195\/41812431\/bqaa195.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,12,17]],"date-time":"2021-12-17T14:44:12Z","timestamp":1639752252000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/endo\/article\/doi\/10.1210\/endocr\/bqaa195\/5939206"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,10,24]]},"references-count":48,"journal-issue":{"issue":"12","published-print":{"date-parts":[[2020,12,1]]}},"URL":"https:\/\/doi.org\/10.1210\/endocr\/bqaa195","relation":{},"ISSN":["0013-7227","1945-7170"],"issn-type":[{"value":"0013-7227","type":"print"},{"value":"1945-7170","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2020,12]]},"published":{"date-parts":[[2020,10,24]]},"article-number":"bqaa195"}}