{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,2]],"date-time":"2026-07-02T17:41:23Z","timestamp":1783014083635,"version":"3.54.6"},"reference-count":49,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2022,2,17]],"date-time":"2022-02-17T00:00:00Z","timestamp":1645056000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["31771664"],"award-info":[{"award-number":["31771664"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["31900601"],"award-info":[{"award-number":["31900601"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100012166","name":"National Key Research and Development Program of China","doi-asserted-by":"publisher","award":["2018YFC1004400"],"award-info":[{"award-number":["2018YFC1004400"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Vet. Sci."],"abstract":"<jats:p>The endometrial gland is one of the most important components of the mammalian uterus. However, few studies have been conducted on the regulatory mechanisms of adenogenesis during the development of endometrium. In the present study, we detected the genes expression of 35 different prolactin family members (PRLs) together with the prolactin receptor (PRL-R) in the endometrium of neonatal mice along with the adenogenesis process, to address which prolactin-like genes play a key role during gland development in mice. We found that: (1) The expression of <jats:italic>Prl1a1, Prl3d1, Prl5a1, Prl7a1, Prl7a2, Prl7d1, Prl8a6, Prl8a8<\/jats:italic>, and <jats:italic>Prl8a9<\/jats:italic> genes were significantly increased along with the development of uterine glands. <jats:italic>Prl7c1<\/jats:italic> and <jats:italic>Prl8a1<\/jats:italic> were observably up-regulated on Postnatal day 5 (PND5) when the uterine glandular bud invagination begins. <jats:italic>Prl3a1, Prl3b1<\/jats:italic>, and <jats:italic>Prl7b1<\/jats:italic> suddenly increased significantly on PND9. But, <jats:italic>Prl3c1<\/jats:italic> and <jats:italic>Prl8a2<\/jats:italic> were markedly down-regulated on PND5 and the expression of <jats:italic>Prl6a1<\/jats:italic> and <jats:italic>Prlr<\/jats:italic> were stable extremely. (2) After continuous injection of Progesterone (P4), a well-known method to suppress the endometrial adenogenesis, the expression of <jats:italic>Prl1a1, Prl3d1, Prl5a1, Prl7a1, Prl7a2, Prl7d1, Prl8a6, Prl8a8, Prl8a9<\/jats:italic>, and <jats:italic>Prlr<\/jats:italic> were suppressed on PND7. And on PND9, <jats:italic>Prl1a1, Prl3d1, Prl8a6, Prl8a8<\/jats:italic>, and <jats:italic>Prl8a9<\/jats:italic> were significantly inhibited. (3) Further analysis of the epithelial and stroma showed that these PRLs were mainly expressed in the endometrial stroma of neonatal mice. Our results indicate that multiple PRLs are involved in uterine development and endometrial adenogenesis. Continued progesterone therapy may alter the expression pattern of these PRLs in endometrial stromal cells, thereby altering the interaction and communication between stroma and epithelium, and ultimately leading to complete suppression of endometrial adenogenesis.<\/jats:p>","DOI":"10.3389\/fvets.2022.818827","type":"journal-article","created":{"date-parts":[[2022,2,17]],"date-time":"2022-02-17T10:00:33Z","timestamp":1645092033000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":4,"title":["The Influence of the Prolactins on the Development of the Uterus in Neonatal Mice"],"prefix":"10.3389","volume":"9","author":[{"given":"Jinwen","family":"Kang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yingnan","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yu","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wankun","family":"Yan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yao","family":"Wu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Renwei","family":"Su","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2022,2,17]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"34","DOI":"10.1016\/j.mce.2011.09.035","article-title":"Comparative developmental biology of the uterus: insights into mechanisms and developmental disruption","volume":"354","author":"Spencer","year":"2012","journal-title":"Mol Cell Endocrinol."},{"key":"B2","first-page":"99","article-title":"Early uterine development in pigs","volume":"48","author":"Bartol","year":"1993","journal-title":"J Reprod Fertil Suppl."},{"key":"B3","first-page":"287","article-title":"Uterine differentiation as a foundation for subsequent fertility","volume":"54","author":"Bartol","year":"1999","journal-title":"J Reprod Fertil Suppl."},{"key":"B4","doi-asserted-by":"publisher","first-page":"2435","DOI":"10.1038\/s41467-018-04848-8","article-title":"Uterine glands coordinate on-time embryo implantation and impact endometrial decidualization for pregnancy success","volume":"9","author":"Kelleher","year":"2018","journal-title":"Nat Commun."},{"key":"B5","doi-asserted-by":"publisher","first-page":"217","DOI":"10.1006\/dbio.2000.9767","article-title":"Embryo implantation","volume":"223","author":"Carson","year":"2000","journal-title":"Dev Biol."},{"key":"B6","doi-asserted-by":"publisher","first-page":"4365","DOI":"10.1210\/endo.141.12.7855","article-title":"Leukemia inhibitory factor can substitute for nidatory estrogen and is essential to inducing a receptive uterus for implantation but is not essential for subsequent embryogenesis","volume":"141","author":"Chen","year":"2000","journal-title":"Endocrinology."},{"key":"B7","doi-asserted-by":"publisher","first-page":"655","DOI":"10.1016\/S8756-3282(02)00688-9","article-title":"Forty years of calcitonin\u2013where are we now? A tribute to the work of Iain Macintyre, FRS","volume":"30","author":"Zaidi","year":"2002","journal-title":"Bone."},{"key":"B8","doi-asserted-by":"publisher","first-page":"46447","DOI":"10.1074\/jbc.M203555200","article-title":"Calcitonin down-regulates E-cadherin expression in rodent uterine epithelium during implantation","volume":"277","author":"Li","year":"2002","journal-title":"J Biol Chem."},{"key":"B9","doi-asserted-by":"publisher","first-page":"1311","DOI":"10.1095\/biolreprod65.5.1311","article-title":"Developmental biology of uterine glands","volume":"65","author":"Gray","year":"2001","journal-title":"Biol Reprod."},{"key":"B10","doi-asserted-by":"publisher","first-page":"1424","DOI":"10.1210\/er.2018-00281","article-title":"Uterine glands: developmental biology and functional roles in pregnancy","volume":"40","author":"Kelleher","year":"2019","journal-title":"Endocr Rev."},{"key":"B11","doi-asserted-by":"publisher","first-page":"125","DOI":"10.1146\/annurev-animal-020518-115321","article-title":"Development and function of uterine glands in domestic animals","volume":"7","author":"Spencer","year":"2019","journal-title":"Annu Rev Anim Biosci."},{"key":"B12","doi-asserted-by":"publisher","first-page":"199","DOI":"10.1007\/s12020-017-1346-x","article-title":"Prolactin function and putative expression in the brain","volume":"57","author":"Cabrera-Reyes","year":"2017","journal-title":"Endocrine."},{"key":"B13","doi-asserted-by":"publisher","first-page":"625","DOI":"10.1530\/REP-15-0107","article-title":"Identification of target genes for a prolactin family paralog in mouse decidua","volume":"149","author":"Alam","year":"2015","journal-title":"Reproduction."},{"key":"B14","doi-asserted-by":"publisher","first-page":"16543","DOI":"10.1073\/pnas.0406185101","article-title":"A prolactin family paralog regulates reproductive adaptations to a physiological stressor","volume":"101","author":"Ain","year":"2004","journal-title":"Proc Natl Acad Sci U S A."},{"key":"B15","doi-asserted-by":"publisher","first-page":"107","DOI":"10.1095\/biolreprod.115.138032","article-title":"A prolactin family paralog regulates placental adaptations to a physiological stressor","volume":"94","author":"Bu","year":"2016","journal-title":"Biol Reprod."},{"key":"B16","doi-asserted-by":"publisher","first-page":"622","DOI":"10.1210\/me.2013-1349","article-title":"Minireview: extrapituitary prolactin: an update on the distribution, regulation, and functions","volume":"28","author":"Marano","year":"2014","journal-title":"Mol Endocrinol."},{"key":"B17","doi-asserted-by":"publisher","first-page":"1523","DOI":"10.1152\/physrev.2000.80.4.1523","article-title":"Prolactin: structure, function, and regulation of secretion","volume":"80","author":"Freeman","year":"2000","journal-title":"Physiol Rev."},{"key":"B18","doi-asserted-by":"publisher","first-page":"265","DOI":"10.1038\/nrendo.2015.36","article-title":"New insights in prolactin: pathological implications","volume":"11","author":"Bernard","year":"2015","journal-title":"Nat Rev Endocrinol."},{"key":"B19","doi-asserted-by":"publisher","first-page":"313","DOI":"10.1210\/en.2002-220724","article-title":"The mouse prolactin gene family locus","volume":"144","author":"Wiemers","year":"2003","journal-title":"Endocrinology."},{"key":"B20","doi-asserted-by":"publisher","first-page":"51","DOI":"10.1186\/1477-7827-2-51","article-title":"The prolactin and growth hormone families: pregnancy-specific hormones\/cytokines at the maternal-fetal interface","volume":"2","author":"Soares","year":"2004","journal-title":"Reprod Biol Endocrinol."},{"key":"B21","doi-asserted-by":"publisher","first-page":"154","DOI":"10.1007\/s00335-007-9003-y","article-title":"A standardized nomenclature for the mouse and rat prolactin superfamilies","volume":"18","author":"Soares","year":"2007","journal-title":"Mamm Genome."},{"key":"B22","doi-asserted-by":"publisher","first-page":"1888","DOI":"10.1101\/gr.2478604","article-title":"et al. Organization and evolution of a gene-rich region of the mouse genome: a 127-Mb region deleted in the Del(13)Svea36H mouse","volume":"14","author":"Mallon","year":"2004","journal-title":"Genome Res."},{"key":"B23","doi-asserted-by":"publisher","first-page":"414","DOI":"10.1080\/07853890410033892","article-title":"Prolactin and the prolactin receptor: new targets of an old hormone","volume":"36","author":"Harris","year":"2004","journal-title":"Ann Med."},{"key":"B24","doi-asserted-by":"publisher","first-page":"4777","DOI":"10.1210\/en.2013-1476","article-title":"Completely humanizing prolactin rescues infertility in prolactin knockout mice and leads to human prolactin expression in extrapituitary mouse tissues","volume":"154","author":"Christensen","year":"2013","journal-title":"Endocrinology."},{"key":"B25","doi-asserted-by":"publisher","first-page":"696","DOI":"10.1002\/mrd.23148","article-title":"Deletion of Prl7d1 causes placental defects at mid-pregnancy in mice","volume":"86","author":"Zhang","year":"2019","journal-title":"Mol Reprod Dev."},{"key":"B26","doi-asserted-by":"publisher","first-page":"103","DOI":"10.1016\/S0896-6273(00)80351-7","article-title":"Pituitary lactotroph hyperplasia and chronic hyperprolactinemia in dopamine D2 receptor-deficient mice","volume":"19","author":"Kelly","year":"1997","journal-title":"Neuron."},{"key":"B27","doi-asserted-by":"publisher","first-page":"110","DOI":"10.1210\/en.2002-220627","article-title":"Prolactin regulation of neonatal ovine uterine gland morphogenesis","volume":"144","author":"Carpenter","year":"2003","journal-title":"Endocrinology."},{"key":"B28","doi-asserted-by":"publisher","first-page":"1236","DOI":"10.1095\/biolreprod64.4.1236","article-title":"Expression of messenger ribonucleic acids for fibroblast growth factors 7 and 10, hepatocyte growth factor, and insulin-like growth factors and their receptors in the neonatal ovine uterus","volume":"64","author":"Taylor","year":"2001","journal-title":"Biol Reprod."},{"key":"B29","doi-asserted-by":"publisher","first-page":"55168","DOI":"10.3791\/55168","article-title":"Isolation of mouse endometrial epithelial and stromal cells for in vitro decidualization","volume":"121","author":"De Clercq","year":"2017","journal-title":"J Vis Exp."},{"key":"B30","doi-asserted-by":"publisher","first-page":"1192","DOI":"10.1095\/biolreprod63.4.1192","article-title":"Neonatal ovine uterine development involves alterations in expression of receptors for estrogen, progesterone, and prolactin","volume":"63","author":"Taylor","year":"2000","journal-title":"Biol Reprod."},{"key":"B31","doi-asserted-by":"publisher","first-page":"z29","DOI":"10.1210\/jendso\/bvz029","article-title":"Prolactin enhances the proliferation of proliferative endometrial glandular cells and endometrial cancer cells","volume":"4","author":"Yamaguchi","year":"2020","journal-title":"J Endocr Soc."},{"key":"B32","doi-asserted-by":"publisher","first-page":"114","DOI":"10.1093\/humupd\/dmy035","article-title":"The role of mesenchymal-epithelial transition in endometrial function","volume":"25","author":"Owusu-Akyaw","year":"2019","journal-title":"Hum Reprod Update."},{"key":"B33","doi-asserted-by":"publisher","first-page":"141","DOI":"10.1095\/biolreprod.112.098871","article-title":"CDH1 is essential for endometrial differentiation, gland development, and adult function in the mouse uterus","volume":"86","author":"Reardon","year":"2012","journal-title":"Biol Reprod."},{"key":"B34","doi-asserted-by":"publisher","first-page":"547","DOI":"10.1093\/molehr\/gat031","article-title":"Uterine glands: development, function and experimental model systems","volume":"19","author":"Cooke","year":"2013","journal-title":"Mol Hum Reprod."},{"key":"B35","first-page":"417","article-title":"Extracellular matrix signaling from the cellular membrane skeleton to the nuclear skeleton: a model of gene regulation","volume":"51","author":"Lelievre","year":"1996","journal-title":"Recent Prog Horm Res."},{"key":"B36","first-page":"S68","article-title":"Extracellular matrix remodeling and the regulation of epithelial-stromal interactions during differentiation and involution","volume":"54","author":"Werb","year":"1996","journal-title":"Kidney Int Suppl."},{"key":"B37","doi-asserted-by":"publisher","first-page":"1037","DOI":"10.1095\/biolreprod.109.079772","article-title":"Hepatocyte growth factor system in the mouse uterus: variation across the estrous cycle and regulation by 17-beta-estradiol and progesterone","volume":"82","author":"Zhang","year":"2010","journal-title":"Biol Reprod."},{"key":"B38","doi-asserted-by":"publisher","first-page":"337","DOI":"10.1530\/rep.1.00342","article-title":"The IGF system in the neonatal ovine uterus","volume":"129","author":"Hayashi","year":"2005","journal-title":"Reproduction."},{"key":"B39","doi-asserted-by":"publisher","first-page":"7","DOI":"10.1095\/biolreprod.113.114496","article-title":"Fibroblast growth factor receptor two (FGFR2) regulates uterine epithelial integrity and fertility in mice","volume":"90","author":"Filant","year":"2014","journal-title":"Biol Reprod."},{"key":"B40","first-page":"2865","volume":"55","author":"Kamada","year":"1997","journal-title":"Nihon Rinsho."},{"key":"B41","doi-asserted-by":"publisher","first-page":"265","DOI":"10.1016\/j.bpobgyn.2004.01.006","article-title":"Steroid receptor action","volume":"18","author":"Brosens","year":"2004","journal-title":"Best Pract Res Clin Obstet Gynaecol."},{"key":"B42","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.domaniend.2016.07.003","article-title":"Prolactin role in the bovine uterus during adenomyosis","volume":"58","author":"Lupicka","year":"2017","journal-title":"Domest Anim Endocrinol."},{"key":"B43","doi-asserted-by":"publisher","first-page":"207","DOI":"10.1016\/S0014-5793(99)00052-6","article-title":"Cellular localization and evolution of prolactin receptor mRNA in ovine endometrium during pregnancy","volume":"445","author":"Cassy","year":"1999","journal-title":"FEBS Lett."},{"key":"B44","doi-asserted-by":"publisher","first-page":"2326","DOI":"10.1210\/en.2006-1643","article-title":"Decidual prolactin silences the expression of genes detrimental to pregnancy","volume":"148","author":"Bao","year":"2007","journal-title":"Endocrinology."},{"key":"B45","doi-asserted-by":"publisher","first-page":"2691","DOI":"10.1210\/endo.141.7.7568","article-title":"Rescue of preimplantatory egg development and embryo implantation in prolactin receptor-deficient mice after progesterone administration","volume":"141","author":"Binart","year":"2000","journal-title":"Endocrinology."},{"key":"B46","doi-asserted-by":"publisher","first-page":"185","DOI":"10.1159\/000068380","article-title":"Metoclopramide-induced hyperprolactinemia affects mouse endometrial morphology","volume":"54","author":"Rossi","year":"2002","journal-title":"Gynecol Obstet Invest."},{"key":"B47","doi-asserted-by":"publisher","first-page":"1169","DOI":"10.1210\/mend-2-12-1169","article-title":"Servomechanism of prolactin and progesterone in regulating uterine gene expression","volume":"2","author":"Chilton","year":"1988","journal-title":"Mol Endocrinol."},{"key":"B48","doi-asserted-by":"publisher","first-page":"713","DOI":"10.1530\/jrf.0.0860713","article-title":"Effects of prolactin on conceptus survival and uterine secretory activity in pigs","volume":"86","author":"Young","year":"1989","journal-title":"J Reprod Fertil."},{"key":"B49","doi-asserted-by":"publisher","first-page":"148","DOI":"10.3109\/09513590.2014.967204","article-title":"The progesterone and estrogen modify the uterine prolactin and prolactin receptor expression of hyperprolactinemic mice","volume":"31","author":"Do","year":"2015","journal-title":"Gynecol Endocrinol."}],"container-title":["Frontiers in Veterinary Science"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fvets.2022.818827\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,2,17]],"date-time":"2022-02-17T10:00:42Z","timestamp":1645092042000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fvets.2022.818827\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,2,17]]},"references-count":49,"alternative-id":["10.3389\/fvets.2022.818827"],"URL":"https:\/\/doi.org\/10.3389\/fvets.2022.818827","relation":{},"ISSN":["2297-1769"],"issn-type":[{"value":"2297-1769","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,2,17]]},"article-number":"818827"}}