{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,4]],"date-time":"2026-08-04T15:05:15Z","timestamp":1785855915890,"version":"3.56.0"},"reference-count":23,"publisher":"MDPI AG","issue":"19","license":[{"start":{"date-parts":[[2020,9,30]],"date-time":"2020-09-30T00:00:00Z","timestamp":1601424000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100003725","name":"National Research Foundation of Korea","doi-asserted-by":"publisher","award":["2016R1A2B4010043, 2019R1A2C1003398"],"award-info":[{"award-number":["2016R1A2B4010043, 2019R1A2C1003398"]}],"id":[{"id":"10.13039\/501100003725","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>The placenta undergoes reconstruction at different times during fetal development to supply oxygen and nutrients required throughout pregnancy. To accommodate the rapid growth of the fetus, small spiral arteries undergo remodeling in the placenta. This remodeling includes apoptosis of endothelial cells that line spiral arteries, which are replaced by trophoblasts of fetal origin. Removal of dead cells is critical during this process. Stabilin-1 (Stab1) and stabilin-2 (Stab2) are important receptors expressed on scavenger cells that absorb and degrade apoptotic cells, and Stab1 is expressed in specific cells of the placenta. However, the role of Stab1 and Stab2 in placental development and maintenance remain unclear. In this study, we assessed Stab1 and Stab2 expression in the placenta and examined the reproductive capacity and placental development using a double-knockout mouse strain lacking both Stab1 and Stab2 (Stab1\/2 dKO mice). Most pregnant Stab1\/2 dKO female mice did not produce offspring and exhibited placental defects, including decidual hemorrhage and necrosis. Findings of this study offer the first description of the phenotypic characteristics of placentas and embryos of Stab1\/2 dKO females during pregnancy, suggesting that Stab1 and Stab2 are involved in placental development and maintenance.<\/jats:p>","DOI":"10.3390\/ijms21197235","type":"journal-article","created":{"date-parts":[[2020,10,1]],"date-time":"2020-10-01T09:04:12Z","timestamp":1601543052000},"page":"7235","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":7,"title":["Identifying Stabilin-1 and Stabilin-2 Double Knockouts in Reproduction and Placentation: A Descriptive Study"],"prefix":"10.3390","volume":"21","author":[{"given":"Soon-Young","family":"Kim","sequence":"first","affiliation":[{"name":"Department of Molecular Medicine, Cell and Matrix Research Institute, School of Medicine, Kyungpook National University, Daegu 41944, Korea"},{"name":"BK21 Plus KNU Biomedical Convergence Program, Department of Biomedical Science, Kyungpook National University, Daegu 41944, Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eun-Hye","family":"Lee","sequence":"additional","affiliation":[{"name":"Department of Molecular Medicine, Cell and Matrix Research Institute, School of Medicine, Kyungpook National University, Daegu 41944, Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eun Na","family":"Kim","sequence":"additional","affiliation":[{"name":"Department of Pathology, Asan Medical Center, University of Ulsan College of Medicine, Seoul 05505, Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Woo-Chan","family":"Son","sequence":"additional","affiliation":[{"name":"Department of Pathology, Asan Medical Center, University of Ulsan College of Medicine, Seoul 05505, Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1631-574X","authenticated-orcid":false,"given":"Yeo Hyang","family":"Kim","sequence":"additional","affiliation":[{"name":"Department of Pediatrics, School of Medicine, Kyungpook National University, Daegu 41944, Korea"},{"name":"Division of Pediatric Cardiology, Kyungpook National University Children\u2019s Hospital, Daegu 41404, Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Seung-Yoon","family":"Park","sequence":"additional","affiliation":[{"name":"Department of Biochemistry, School of Medicine, Dongguk University, Gyeongju 38066, Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"In-San","family":"Kim","sequence":"additional","affiliation":[{"name":"Center for Theragnosis, Biomedical Research Institute, Korea Institute of Science and Technology, Seoul 02792, Korea"},{"name":"KU-KIST Graduate School of Converging Science and Technology, Korea University, Seoul 02841, Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jung-Eun","family":"Kim","sequence":"additional","affiliation":[{"name":"Department of Molecular Medicine, Cell and Matrix Research Institute, School of Medicine, Kyungpook National University, Daegu 41944, Korea"},{"name":"BK21 Plus KNU Biomedical Convergence Program, Department of Biomedical Science, Kyungpook National University, Daegu 41944, Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,9,30]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"2039","DOI":"10.1100\/tsw.2010.189","article-title":"Multifunctional receptor stabilin-1 in homeostasis and disease","volume":"10","author":"Kzhyshkowska","year":"2010","journal-title":"Sci. World J."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1042\/bj3620155","article-title":"Stabilin-1 and -2 constitute a novel family of fasciclin-like hyaluronan receptor homologues","volume":"362","author":"Politz","year":"2002","journal-title":"Biochem. J."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"2052","DOI":"10.1002\/eji.201041376","article-title":"Stabilin-1\/CLEVER-1, a type 2 macrophage marker, is an adhesion and scavenging molecule on human placental macrophages","volume":"41","author":"Palani","year":"2011","journal-title":"Eur. J. Immunol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"4263","DOI":"10.1073\/pnas.1117560109","article-title":"Inhibition of Stabilin-2 elevates circulating hyaluronic acid levels and prevents tumor metastasis","volume":"109","author":"Hirose","year":"2012","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1007\/s00223-019-00552-x","article-title":"Ablation of Stabilin-1 enhances bone-resorbing activity in osteoclast in vitro","volume":"105","author":"Kim","year":"2019","journal-title":"Calcif. Tissue Int."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"12613","DOI":"10.1074\/jbc.M210211200","article-title":"FEEL-1 and FEEL-2 are endocytic receptors for advanced glycation end products","volume":"278","author":"Tamura","year":"2003","journal-title":"J. Biol. Chem."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1007\/s00418-003-0585-5","article-title":"Expression of stabilin-2, a novel fasciclin-like hyaluronan receptor protein, in murine sinusoidal endothelia, avascular tissues, and at solid\/liquid interfaces","volume":"120","author":"Falkowski","year":"2003","journal-title":"Histochem. Cell Biol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1776","DOI":"10.1055\/s-0038-1669477","article-title":"Macrophagic Stabilin-1 restored disruption of vascular integrity caused by sepsis","volume":"118","author":"Lee","year":"2018","journal-title":"Thromb. Haemost."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"3028","DOI":"10.4049\/jimmunol.180.5.3028","article-title":"Alternatively activated macrophages regulate extracellular levels of the hormone placental lactogen via receptor-mediated uptake and transcytosis","volume":"180","author":"Kzhyshkowska","year":"2008","journal-title":"J. Immunol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"703","DOI":"10.1172\/JCI44740","article-title":"Deficiency of liver sinusoidal scavenger receptors stabilin-1 and -2 mice causes glomerulofibrotic nephropathy via impaired hepatic clearance of noxious blood factors","volume":"121","author":"Schledzewski","year":"2011","journal-title":"J. Clin. Investig."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1016\/j.placenta.2017.01.114","article-title":"Review: Alterations in placental glycogen deposition in complicated pregnancies: Current preclinical and clinical evidence","volume":"54","author":"Akison","year":"2017","journal-title":"Placenta"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1017","DOI":"10.2353\/ajpath.2010.091105","article-title":"Vascular-leukocyte interactions: Mechanisms of human decidual spiral artery remodeling in vitro","volume":"177","author":"Hazan","year":"2010","journal-title":"Am. J. Pathol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1016\/j.ydbio.2014.01.015","article-title":"Development of the hemochorial maternal vascular spaces in the placenta through endothelial and vasculogenic mimicry","volume":"387","author":"Rai","year":"2014","journal-title":"Dev. Biol."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Rost, M.S., and Sumanas, S. (2014). Hyaluronic acid receptor Stabilin-2 regulates Erk phosphorylation and arterial-venous differentiation in zebrafish. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0088614"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"3280","DOI":"10.1002\/dvdy.20981","article-title":"Origin and characteristics of glycogen cells in the developing murine placenta","volume":"235","author":"Coan","year":"2006","journal-title":"Dev. Dyn."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1005","DOI":"10.1097\/01.AOG.0000239439.04364.9a","article-title":"Placental abruption","volume":"108","author":"Oyelese","year":"2006","journal-title":"Obstet. Gynecol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"732","DOI":"10.3109\/00016341003686081","article-title":"Etiology, clinical manifestations, and prediction of placental abruption","volume":"89","author":"Tikkanen","year":"2010","journal-title":"Acta Obstet. Gynecol. Scand."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"635","DOI":"10.1007\/s00281-016-0574-0","article-title":"The decidua-the maternal bed embracing the embryo-maintains the pregnancy","volume":"38","author":"Mori","year":"2016","journal-title":"Semin. Immunopathol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"579","DOI":"10.1095\/biolreprod.106.056630","article-title":"Effect of the conceptus on uterine natural killer cell numbers and function in the mouse uterus during decidualization","volume":"76","author":"Herington","year":"2007","journal-title":"Biol. Reprod."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"567","DOI":"10.1016\/j.ydbio.2007.01.009","article-title":"Diverse subtypes and developmental origins of trophoblast giant cells in the mouse placenta","volume":"304","author":"Simmons","year":"2007","journal-title":"Dev. Biol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"10871","DOI":"10.1038\/ncomms10871","article-title":"Stabilin-2 modulates the efficiency of myoblast fusion during myogenic differentiation and muscle regeneration","volume":"7","author":"Park","year":"2016","journal-title":"Nat. Commun."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"89","DOI":"10.5830\/CVJA-2016-021","article-title":"Physiological changes in pregnancy","volume":"27","author":"Tolppanen","year":"2016","journal-title":"Cardiovasc. J. Afr."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"570","DOI":"10.3389\/fendo.2018.00570","article-title":"Regulation of placental development and its impact on fetal growth\u2014new insights from mouse models","volume":"9","author":"Woods","year":"2018","journal-title":"Front. 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