{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,3]],"date-time":"2026-06-03T20:52:01Z","timestamp":1780519921654,"version":"3.54.1"},"reference-count":51,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2020,7,14]],"date-time":"2020-07-14T00:00:00Z","timestamp":1594684800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Immunol."],"DOI":"10.3389\/fimmu.2020.01316","type":"journal-article","created":{"date-parts":[[2020,7,14]],"date-time":"2020-07-14T06:22:40Z","timestamp":1594707760000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":27,"title":["Altered Glycosylation Contributes to Placental Dysfunction Upon Early Disruption of the NK Cell-DC Dynamics"],"prefix":"10.3389","volume":"11","author":[{"given":"Sophia","family":"Borowski","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Irene","family":"Tirado-Gonzalez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nancy","family":"Freitag","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mariana G.","family":"Garcia","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gabriela","family":"Barrientos","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sandra M.","family":"Blois","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2020,7,14]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"584","DOI":"10.1038\/nri1897","article-title":"Immunology of placentation in eutherian mammals","volume":"6","author":"Moffett","year":"2006","journal-title":"Nat Rev Immunol."},{"key":"B2","doi-asserted-by":"publisher","first-page":"192","DOI":"10.1016\/j.mam.2007.02.006","article-title":"The role of the immune system in preeclampsia","volume":"28","author":"Saito","year":"2007","journal-title":"Mol Aspects Med."},{"key":"B3","doi-asserted-by":"publisher","first-page":"262","DOI":"10.1002\/jlb.59.2.262","article-title":"Accounting for the peripartum loss of granulated metrial gland cells, a natural killer cell population, from the pregnant mouse uterus","volume":"59","author":"Delgado","year":"1996","journal-title":"J Leukoc Biol."},{"key":"B4","doi-asserted-by":"publisher","first-page":"2203","DOI":"10.1002\/eji.200838844","article-title":"DC within the pregnant mouse uterus influence growth and functional properties of uterine NK cells","volume":"39","author":"Karsten","year":"2009","journal-title":"Eur J Immunol."},{"key":"B5","doi-asserted-by":"publisher","first-page":"285","DOI":"10.1007\/s004410000198","article-title":"Expression of vascular endothelial growth factor by granulated metrial gland cells in pregnant murine uteri","volume":"300","author":"Wang","year":"2000","journal-title":"Cell Tissue Res."},{"key":"B6","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/cmi.2010.38","article-title":"Natural killer cell-triggered vascular transformation: maternal care before birth?","volume":"8","author":"Zhang","year":"2011","journal-title":"Cell Mol Immunol."},{"key":"B7","doi-asserted-by":"publisher","first-page":"66","DOI":"10.1093\/molehr\/gat060","article-title":"Uterine natural killer cells pace early development of mouse decidua basalis","volume":"20","author":"Hofmann","year":"2014","journal-title":"Mol Hum Reprod."},{"key":"B8","doi-asserted-by":"publisher","first-page":"1018","DOI":"10.1095\/biolreprod.103.022640","article-title":"Lineage, maturity, and phenotype of uterine murine dendritic cells throughout gestation indicate a protective role in maintaining pregnancy","volume":"70","author":"Blois","year":"2004","journal-title":"Biol Reprod."},{"key":"B9","doi-asserted-by":"publisher","first-page":"999","DOI":"10.1007\/s00109-008-0379-2","article-title":"In vivo dendritic cell depletion reduces breeding efficiency, affecting implantation and early placental development in mice","volume":"86","author":"Krey","year":"2008","journal-title":"J Mol Med."},{"key":"B10","doi-asserted-by":"publisher","first-page":"3954","DOI":"10.1172\/JCI36682","article-title":"Uterine DCs are crucial for decidua formation during embryo implantation in mice","volume":"118","author":"Plaks","year":"2008","journal-title":"J Clin Invest."},{"key":"B11","doi-asserted-by":"publisher","first-page":"417","DOI":"10.1007\/s10456-012-9325-6","article-title":"CXCR4(+) dendritic cells promote angiogenesis during embryo implantation in mice","volume":"16","author":"Barrientos","year":"2013","journal-title":"Angiogenesis."},{"key":"B12","doi-asserted-by":"publisher","first-page":"e46755","DOI":"10.1371\/annotation\/9c332046-387a-4bbc-9549-2bcff73afd9a","article-title":"Uterine NK cells are critical in shaping DC immunogenic functions compatible with pregnancy progression","volume":"7","author":"Tirado-Gonzalez","year":"2012","journal-title":"PLoS ONE."},{"key":"B13","doi-asserted-by":"publisher","first-page":"e1392","DOI":"10.1038\/cddis.2014.353","article-title":"Influence of relative NK-DC abundance on placentation and its relation to epigenetic programming in the offspring","volume":"5","author":"Freitag","year":"2014","journal-title":"Cell Death Dis."},{"key":"B14","doi-asserted-by":"publisher","first-page":"2189","DOI":"10.1038\/s41598-017-02333-8","article-title":"NK cell-derived IL-10 is critical for DC-NK cell dialogue at the maternal-fetal interface","volume":"7","author":"Blois","year":"2017","journal-title":"Sci Rep."},{"key":"B15","doi-asserted-by":"publisher","first-page":"165","DOI":"10.1016\/S0304-4165(02)00306-9","article-title":"The sugar code: functional lectinomics","volume":"1572","author":"Gabius","year":"2002","journal-title":"Biochim Biophys Acta."},{"key":"B16","doi-asserted-by":"publisher","first-page":"2064","DOI":"10.1093\/humrep\/dev153","article-title":"Altered beta1,6-GlcNAc and bisecting GlcNAc-branched N-glycan on integrin beta1 are associated with early spontaneous miscarriage in humans","volume":"30","author":"Zhang","year":"2015","journal-title":"Hum Reprod."},{"key":"B17","doi-asserted-by":"publisher","first-page":"503","DOI":"10.1053\/plac.2002.0793","article-title":"Lectin histochemistry in the human placenta of pregnancies complicated by intrauterine growth retardation based on absent or reversed diastolic flow","volume":"23","author":"Sgambati","year":"2002","journal-title":"Placenta."},{"key":"B18","doi-asserted-by":"publisher","first-page":"815","DOI":"10.1016\/j.acthis.2010.12.001","article-title":"Distribution of sugar residues in human placentas from pregnancies complicated by hypertensive disorders","volume":"113","author":"Marini","year":"2011","journal-title":"Acta Histochem."},{"key":"B19","doi-asserted-by":"publisher","first-page":"98","DOI":"10.1016\/j.jri.2016.08.008","article-title":"Update of syncytiotrophoblast derived extracellular vesicles in normal pregnancy and preeclampsia","volume":"119","author":"Tannetta","year":"2017","journal-title":"J Reprod Immunol."},{"key":"B20","doi-asserted-by":"publisher","first-page":"1450","DOI":"10.1038\/nm1680","article-title":"A pivotal role for galectin-1 in fetomaternal tolerance","volume":"13","author":"Blois","year":"2007","journal-title":"Nat Med."},{"key":"B21","doi-asserted-by":"publisher","first-page":"1166","DOI":"10.3389\/fimmu.2019.01166","article-title":"Pregnancy galectinology: insights into a complex network of glycan binding proteins","volume":"10","author":"Blois","year":"2019","journal-title":"Front Immunol."},{"key":"B22","doi-asserted-by":"publisher","first-page":"213","DOI":"10.1002\/SICI1526-968X20000326:3<213::AID-GENE7>3.0.CO;2-M","article-title":"Differential expression of VEGF isoforms and VEGF(164)-specific receptor neuropilin-1 in the mouse uterus suggests a role for VEGF(164) in vascular permeability and angiogenesis during implantation","volume":"26","author":"Halder","year":"2000","journal-title":"Genesis."},{"key":"B23","doi-asserted-by":"publisher","first-page":"3845","DOI":"10.1210\/en.2008-1207","article-title":"Vascular endothelial growth factor receptor 2 (VEGFR-2) functions to promote uterine decidual angiogenesis during early pregnancy in the mouse","volume":"150","author":"Douglas","year":"2009","journal-title":"Endocrinology."},{"key":"B24","doi-asserted-by":"publisher","first-page":"737","DOI":"10.1074\/jbc.M110.177006","article-title":"Heparan sulfate regulates VEGF165- and VEGF121-mediated vascular hyperpermeability","volume":"286","author":"Xu","year":"2011","journal-title":"J Biol Chem."},{"key":"B25","doi-asserted-by":"publisher","first-page":"744","DOI":"10.1016\/j.cell.2014.01.043","article-title":"Glycosylation-dependent lectin-receptor interactions preserve angiogenesis in anti-VEGF refractory tumors","volume":"156","author":"Croci","year":"2014","journal-title":"Cell."},{"key":"B26","doi-asserted-by":"publisher","first-page":"825","DOI":"10.1038\/ni1482","article-title":"Differential glycosylation of TH1, TH2 and TH-17 effector cells selectively regulates susceptibility to cell death","volume":"8","author":"Toscano","year":"2007","journal-title":"Nat Immunol."},{"key":"B27","doi-asserted-by":"publisher","first-page":"H2815","DOI":"10.1152\/ajpheart.2000.279.6.H2815","article-title":"TNF-alpha increases entry of macromolecules into luminal endothelial cell glycocalyx","volume":"279","author":"Henry","year":"2000","journal-title":"Am J Physiol Heart Circ Physiol."},{"key":"B28","doi-asserted-by":"publisher","first-page":"3029","DOI":"10.1074\/mcp.M114.039537","article-title":"Immunoglobulin G (IgG) Fab glycosylation analysis using a new mass spectrometric high-throughput profiling method reveals pregnancy-associated changes","volume":"13","author":"Bondt","year":"2014","journal-title":"Mol Cell Proteomics."},{"key":"B29","doi-asserted-by":"publisher","first-page":"356","DOI":"10.1038\/s41467-019-14178-y","article-title":"beta4GALT1 controls beta1 integrin function to govern thrombopoiesis and hematopoietic stem cell homeostasis","volume":"11","author":"Giannini","year":"2020","journal-title":"Nat Commun."},{"key":"B30","doi-asserted-by":"publisher","first-page":"682","DOI":"10.1096\/fj.07-9268com","article-title":"Inhibitory control of endothelial galectin-1 on in vitro and in vivo lymphocyte trafficking","volume":"22","author":"Norling","year":"2008","journal-title":"FASEB J."},{"key":"B31","doi-asserted-by":"publisher","first-page":"1857","DOI":"10.1074\/mcp.M115.055798","article-title":"Evidence for differential glycosylation of trophoblast cell types","volume":"15","author":"Chen","year":"2016","journal-title":"Mol Cell Proteomics."},{"key":"B32","doi-asserted-by":"publisher","first-page":"2114","DOI":"10.1038\/s41598-018-19263-8","article-title":"Periconception onset diabetes is associated with embryopathy and fetal growth retardation, reproductive tract hyperglycosylation and impaired immune adaptation to pregnancy","volume":"8","author":"Brown","year":"2018","journal-title":"Sci Rep."},{"key":"B33","doi-asserted-by":"publisher","first-page":"53","DOI":"10.1016\/bs.acr.2014.11.002","article-title":"Simple sugars to complex disease\u2013mucin-type O-glycans in cancer","volume":"126","author":"Kudelka","year":"2015","journal-title":"Adv Cancer Res."},{"key":"B34","doi-asserted-by":"publisher","first-page":"4875","DOI":"10.1111\/jcmm.13752","article-title":"Aberrant O-glycosylation contributes to tumorigenesis in human colorectal cancer","volume":"22","author":"Jiang","year":"2018","journal-title":"J Cell Mol Med."},{"key":"B35","doi-asserted-by":"publisher","first-page":"2083","DOI":"10.1111\/jcmm.14117","article-title":"Tn antigen promotes human colorectal cancer metastasis via H-Ras mediated epithelial-mesenchymal transition activation","volume":"23","author":"Liu","year":"2019","journal-title":"J Cell Mol Med."},{"key":"B36","doi-asserted-by":"publisher","first-page":"10661","DOI":"10.1128\/MCB.24.24.10661-10669.2004","article-title":"Peroxisome proliferator-activated receptor gamma controls Muc1 transcription in trophoblasts","volume":"24","author":"Shalom-Barak","year":"2004","journal-title":"Mol Cell Biol."},{"key":"B37","doi-asserted-by":"publisher","first-page":"1007","DOI":"10.1016\/j.bbamcr.2007.04.006","article-title":"MUC1 is involved in trophoblast transendothelial migration","volume":"1773","author":"Thirkill","year":"2007","journal-title":"Biochim Biophys Acta."},{"key":"B38","doi-asserted-by":"publisher","first-page":"233","DOI":"10.1095\/biolreprod.108.067629","article-title":"MUC1 expression is increased during human placental development and suppresses trophoblast-like cell invasion in vitro","volume":"79","author":"Shyu","year":"2008","journal-title":"Biol Reprod."},{"key":"B39","doi-asserted-by":"publisher","first-page":"1831","DOI":"10.3892\/ij.2012.1411","article-title":"MUC1 carrying core 2 O-glycans functions as a molecular shield against NK cell attack, promoting bladder tumor metastasis","volume":"40","author":"Suzuki","year":"2012","journal-title":"Int J Oncol."},{"key":"B40","doi-asserted-by":"publisher","first-page":"219","DOI":"10.1007\/s00418-002-0383-5","article-title":"Expression of the Thomsen-Friedenreich antigen and of its putative carrier protein mucin 1 in the human placenta and in trophoblast cells in vitro","volume":"117","author":"Jeschke","year":"2002","journal-title":"Histochem Cell Biol."},{"key":"B41","doi-asserted-by":"publisher","first-page":"e28514","DOI":"10.1371\/journal.pone.0028514","article-title":"Galectin-1 is part of human trophoblast invasion machinery\u2013a functional study in vitro","volume":"6","author":"Kolundzic","year":"2011","journal-title":"PLoS ONE."},{"key":"B42","doi-asserted-by":"publisher","first-page":"541","DOI":"10.1007\/s00418-014-1229-7","article-title":"Galectin-1 binds mucin in human trophoblast","volume":"142","author":"Bojic-Trbojevic","year":"2014","journal-title":"Histochem Cell Biol."},{"key":"B43","doi-asserted-by":"publisher","first-page":"999","DOI":"10.1016\/j.bbrc.2005.02.186","article-title":"Elevated expression of N-acetylglucosaminyltransferase V in first trimester human placenta","volume":"330","author":"Tomiie","year":"2005","journal-title":"Biochem Biophys Res Commun."},{"key":"B44","doi-asserted-by":"publisher","first-page":"269","DOI":"10.1159\/000102175","article-title":"Glycosylation at the fetomaternal interface in hemomonochorial placentae from five widely separated species of mammal: is there evidence for convergent evolution?","volume":"185","author":"Jones","year":"2007","journal-title":"Cells Tissues Organs."},{"key":"B45","doi-asserted-by":"publisher","first-page":"1291","DOI":"10.1007\/s00018-014-1794-x","article-title":"Signaling pathways in mouse and human trophoblast differentiation: a comparative review","volume":"72","author":"Soncin","year":"2015","journal-title":"Cell Mol Life Sci."},{"key":"B46","doi-asserted-by":"publisher","first-page":"1773","DOI":"10.1007\/s10753-017-0620-7","article-title":"Increased O-linked N-acetylglucosamine modification of NF-KappaB and augmented cytokine production in the placentas from hyperglycemic rats","volume":"40","author":"Dela Justina","year":"2017","journal-title":"Inflammation."},{"key":"B47","doi-asserted-by":"publisher","first-page":"18","DOI":"10.1016\/j.lfs.2018.05.013","article-title":"O-linked N-acetyl-glucosamine deposition in placental proteins varies according to maternal glycemic levels","volume":"205","author":"Dela Justina","year":"2018","journal-title":"Life Sci."},{"key":"B48","doi-asserted-by":"publisher","first-page":"255","DOI":"10.1016\/j.tibs.2016.11.003","article-title":"Translating the \u201cSugar Code\u201d into immune and vascular signaling programs","volume":"42","author":"Cerliani","year":"2017","journal-title":"Trends Biochem Sci."},{"key":"B49","doi-asserted-by":"publisher","first-page":"11451","DOI":"10.1073\/pnas.1303707110","article-title":"Interfering with Gal-1-mediated angiogenesis contributes to the pathogenesis of preeclampsia","volume":"110","author":"Freitag","year":"2013","journal-title":"Proc Natl Acad Sci USA."},{"key":"B50","doi-asserted-by":"publisher","first-page":"7842","DOI":"10.1021\/bi201121m","article-title":"When galectins recognize glycans: from biochemistry to physiology and back again","volume":"50","author":"Di Lella","year":"2011","journal-title":"Biochemistry."},{"key":"B51","doi-asserted-by":"crossref","first-page":"5922","DOI":"10.4049\/jimmunol.160.12.5922","article-title":"HLA-G isoforms produced by placental cytotrophoblasts and found in amniotic fluid are due to unusual glycosylation","volume":"160","author":"Mcmaster","year":"1998","journal-title":"J Immunol."}],"container-title":["Frontiers in Immunology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/article\/10.3389\/fimmu.2020.01316\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,10,4]],"date-time":"2023-10-04T06:15:41Z","timestamp":1696400141000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/article\/10.3389\/fimmu.2020.01316\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,7,14]]},"references-count":51,"alternative-id":["10.3389\/fimmu.2020.01316"],"URL":"https:\/\/doi.org\/10.3389\/fimmu.2020.01316","relation":{},"ISSN":["1664-3224"],"issn-type":[{"value":"1664-3224","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,7,14]]},"article-number":"1316"}}