{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,24]],"date-time":"2026-09-24T23:37:39Z","timestamp":1790293059965,"version":"4.1.0"},"reference-count":51,"publisher":"Oxford University Press (OUP)","issue":"2","license":[{"start":{"date-parts":[[2022,11,19]],"date-time":"2022-11-19T00:00:00Z","timestamp":1668816000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["31730089"],"award-info":[{"award-number":["31730089"]}],"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":["31972538"],"award-info":[{"award-number":["31972538"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Wuhan Applied Foundational Frontier Project","award":["2020020601012255"],"award-info":[{"award-number":["2020020601012255"]}]},{"name":"March of Dimes Prematurity Research Center","award":["22-FY18-821"],"award-info":[{"award-number":["22-FY18-821"]}]},{"name":"Wellcome Trust Biomedical Resource","award":["218304\/Z\/19\/Z"],"award-info":[{"award-number":["218304\/Z\/19\/Z"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2023,2,13]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Successful attachment of conceptus to the uterine luminal epithelium (LE) is crucial for establishing a functional placenta in pigs. However, the underlying mechanisms are yet to be elucidated. The uterine LE-conceptus interface is enriched in various glycoconjugates essential to implantation. Using MALDI-MS profiling, we identified for the first time the O-glycan repertoire of pig endometrium during the conceptus attachment stage. The expression pattern of blood group A, O(H), Lewis x, y, a, b (Lex, Ley, Lea, and Leb), the sialylated and sulfated Lex antigens in the uterine LE-conceptus interface was assessed using immunofluorescence assays. Notably, the Lex-carrying O-glycans exhibited a temporal\u2013spatial expression pattern. They were absent in the endometrium on estrous cycle days but strongly and spatially presented in the conceptus and uterine LE to which the conceptus apposes during the early conceptus attachment stage. In addition, Lex-carrying O-glycans were co-localized with secreted phosphoprotein 1 (SPP1), a well-characterized factor that plays a role in promoting conceptus attachment through interacting with integrin \u03b1V\u03b23 and integrin \u03b1V\u03b26. Meanwhile, the immunoprecipitation assays revealed an interaction between the Lex-carrying O-glycans and SPP1, integrin \u03b1V, and integrin \u03b26. Furthermore, we provided evidence that the \u03b21,4-galactosyltransferase 1 (B4GALT1) gene is a potential regulator for Lex antigen expression in the uterine LE-conceptus interface during the early conceptus attachment stage. In conclusion, our findings show that Lex-carrying O-glycans, presumably dependent on B4GALT1 gene expression, might modulate conceptus attachment by interacting with the SPP1-integrin receptor complex in pigs.<\/jats:p>","DOI":"10.1093\/biolre\/ioac204","type":"journal-article","created":{"date-parts":[[2022,11,19]],"date-time":"2022-11-19T22:39:45Z","timestamp":1668897585000},"page":"292-303","source":"Crossref","is-referenced-by-count":2,"title":["Lewis x-carrying O-glycans are candidate modulators for conceptus attachment in pigs"],"prefix":"10.1093","volume":"108","author":[{"given":"Kun","family":"Han","sequence":"first","affiliation":[{"name":"Key Lab of Agricultural Animal Genetics, Breeding and Reproduction of Ministry of Education, College of Animal Science and Technology, Huazhong Agricultural University , Wuhan , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yulu","family":"Yue","sequence":"additional","affiliation":[{"name":"Key Lab of Agricultural Animal Genetics, Breeding and Reproduction of Ministry of Education, College of Animal Science and Technology, Huazhong Agricultural University , Wuhan , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Weiwei","family":"Wang","sequence":"additional","affiliation":[{"name":"Key Lab of Agricultural Animal Genetics, Breeding and Reproduction of Ministry of Education, College of Animal Science and Technology, Huazhong Agricultural University , Wuhan , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Feiyu","family":"Wang","sequence":"additional","affiliation":[{"name":"Key Lab of Agricultural Animal Genetics, Breeding and Reproduction of Ministry of Education, College of Animal Science and Technology, Huazhong Agricultural University , Wuhan , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wengang","family":"Chai","sequence":"additional","affiliation":[{"name":"Glycosciences Laboratory, Faculty of Medicine, Imperial College London , London , UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shuhong","family":"Zhao","sequence":"additional","affiliation":[{"name":"Key Lab of Agricultural Animal Genetics, Breeding and Reproduction of Ministry of Education, College of Animal Science and Technology, Huazhong Agricultural University , Wuhan , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mei","family":"Yu","sequence":"additional","affiliation":[{"name":"Key Lab of Agricultural Animal Genetics, Breeding and Reproduction of Ministry of Education, College of Animal Science and Technology, Huazhong Agricultural University , Wuhan , China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2022,11,19]]},"reference":[{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1186\/2049-1891-5-51","article-title":"Cytokines from the pig conceptus: roles in conceptus development in pigs","volume":"5","author":"Geisert","year":"2014","journal-title":"J Anim Sci Biotechnol"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1016\/j.diff.2013.11.005","article-title":"Pig blastocyst-uterine interactions","volume":"87","author":"Bazer","year":"2014","journal-title":"Differentiation"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"895","DOI":"10.1186\/s12864-019-6264-2","article-title":"Spatial organization of endometrial gene expression at the onset of embryo attachment in pigs","volume":"20","author":"Zeng","year":"2019","journal-title":"BMC Genomics"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"1248","DOI":"10.3390\/ijms22031248","article-title":"Integrating LCM-based spatio-temporal transcriptomics uncovers conceptus and endometrial luminal epithelium communication that coordinates the conceptus attachment in pigs","volume":"22","author":"Wang","year":"2021","journal-title":"Int J Mol Sci"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1186\/2049-1891-5-56","article-title":"Osteopontin: a leading candidate adhesion molecule for implantation in pigs and sheep","volume":"5","author":"Johnson","year":"2014","journal-title":"J Anim Sci Biotechnol"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1007\/978-3-030-77360-1_5","article-title":"The early stages of implantation and placentation in the pig","volume":"234","author":"Johnson","year":"2021","journal-title":"Adv Anat Embryol Cell Biol"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1186\/s40738-015-0007-0","article-title":"Functional glycosylation in the human and mammalian uterus","volume":"1","author":"Clark","year":"2015","journal-title":"Fertil Res Pract"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"346","DOI":"10.1038\/s41581-019-0129-4","article-title":"Glycosylation in health and disease","volume":"15","author":"Reily","year":"2019","journal-title":"Nat Rev Nephrol"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"788","DOI":"10.1016\/j.chembiol.2021.01.024","article-title":"Quantitative chemoproteomics reveals O-GlcNAcylation of cystathionine \u03b3-lyase (CSE) represses trophoblast syncytialization","volume":"28","author":"Liu","year":"2021","journal-title":"Cell Chem Biol"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1038\/s41467-021-27781-9","article-title":"Mammalian brain glycoproteins exhibit diminished glycan complexity compared to other tissues","volume":"13","author":"Williams","year":"2022","journal-title":"Nat Commun"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1126\/science.1079546","article-title":"Trophoblast L-selectin-mediated adhesion at the maternal-fetal interface","volume":"299","author":"Genbacev","year":"2003","journal-title":"Science"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1095\/biolreprod.115.128652","article-title":"The role of endometrial selectins and their ligands on bovine conceptus attachment to the uterine epithelium during peri-implantation period","volume":"93","author":"Bai","year":"2015","journal-title":"Biol Reprod"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"7982","DOI":"10.1073\/pnas.0402669101","article-title":"Discovery and characterization of an epithelial-specific galectin in the endometrium that forms crystals in the trophectoderm","volume":"101","author":"Gray","year":"2004","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"557","DOI":"10.1038\/nature10656","article-title":"GlcNAcylation of histone H2B facilitates its monoubiquitination","volume":"480","author":"Fujiki","year":"2011","journal-title":"Nature"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"7183","DOI":"10.1111\/febs.16148","article-title":"Global functions of O-glycosylation: promises and challenges in O-glycobiology","volume":"288","author":"Wandall","year":"2021","journal-title":"FEBS J"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"100","DOI":"10.1002\/(SICI)1097-0029(19970701\/15)38:1\/2<100::AID-JEMT11>3.0.CO;2-T","article-title":"Localisation of glycans in the placenta: a comparative study of epitheliochorial, endotheliochorial, and haemomonochorial placentation","volume":"38","author":"Jones","year":"1997","journal-title":"Microsc Res Tech"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"551","DOI":"10.1007\/BF00318167","article-title":"Changes in glycan distribution within the porcine interhaemal barrier during gestation","volume":"279","author":"Jones","year":"1995","journal-title":"Cell Tissue Res"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"485","DOI":"10.1007\/s10719-020-09931-1","article-title":"Identification by mass spectrometry and immunoblotting of xenogeneic antigens in the N- and O-glycomes of porcine, bovine and equine heart tissues","volume":"37","author":"Jin","year":"2020","journal-title":"Glycoconj J"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"242","DOI":"10.1038\/s41598-017-18299-6","article-title":"Sample handling of gastric tissue and O-glycan alterations in paired gastric cancer and non-tumorigenic tissues","volume":"8","author":"Adamczyk","year":"2018","journal-title":"Sci Rep"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1016\/j.carres.2012.12.024","article-title":"Structural characterization of \u03b1-galactosylated O-glycans from miniature pig kidney and endothelial cells","volume":"369","author":"Park","year":"2013","journal-title":"Carbohydr Res"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"e13169","DOI":"10.1111\/cpr.13169","article-title":"Glycomics reveal that ST6GAL1-mediated sialylation regulates uterine lumen closure during implantation","volume":"55","author":"Han","year":"2022","journal-title":"Cell Prolif"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1016\/0003-9861(71)90263-3","article-title":"Alkaline borohydride degradation of blood group H substance","volume":"142","author":"Iyer","year":"1971","journal-title":"Arch Biochem Biophys"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1016\/S0076-6879(06)15005-3","article-title":"Glycomic profiling of cells and tissues by mass spectrometry: fingerprinting and sequencing methodologies","volume":"415","author":"Jang-Lee","year":"2006","journal-title":"Methods Enzymol"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"1650","DOI":"10.1021\/pr7008252","article-title":"GlycoWorkbench: a tool for the computer-assisted annotation of mass spectra of glycans","volume":"7","author":"Ceroni","year":"2008","journal-title":"J Proteome Res"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1095\/biolreprod.113.114181","article-title":"Expression of heparanase is associated with breed-specific morphological characters of placental folded bilayer between Yorkshire and Meishan pigs","volume":"90","author":"Hong","year":"2014","journal-title":"Biol Reprod"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"2217","DOI":"10.1038\/s41467-021-22448-x","article-title":"A compendium and comparative epigenomics analysis of cis-regulatory elements in the pig genome","volume":"12","author":"Zhao","year":"2021","journal-title":"Nat Commun"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"3308","DOI":"10.1182\/blood.V97.10.3308","article-title":"Molecular genetic basis of porcine histo-blood group AO system","volume":"97","author":"Yamamoto","year":"2001","journal-title":"Blood"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1007\/s10719-021-10014-y","article-title":"Highly sialylated mucin-type glycopeptide from porcine intestinal mucosa after heparin extraction: O-glycan profiling and immunological activity evaluation","volume":"38","author":"Zhang","year":"2021","journal-title":"Glycoconj J"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"814","DOI":"10.1095\/biolreprod.109.078600","article-title":"Secreted phosphoprotein 1 (SPP1, osteopontin) binds to integrin alpha v beta 6 on porcine trophectoderm cells and integrin alpha v beta 3 on uterine luminal epithelial cells, and promotes trophectoderm cell adhesion and migration","volume":"81","author":"Erikson","year":"2009","journal-title":"Biol Reprod"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1038\/s41385-021-00466-8","article-title":"Finding the sweet spot: glycosylation mediated regulation of intestinal inflammation","volume":"15","author":"Brazil","year":"2022","journal-title":"Mucosal Immunol"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1186\/s12865-021-00456-2","article-title":"Highly individual- and tissue-specific expression of glycoprotein group A and B blood antigens in the human kidney and liver","volume":"22","author":"Wang","year":"2021","journal-title":"BMC Immunol"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"140","DOI":"10.1095\/biolreprod.114.119503","article-title":"LewisX-containing glycans on the porcine oviductal epithelium contribute to formation of the sperm reservoir","volume":"91","author":"Machado","year":"2014","journal-title":"Biol Reprod"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1095\/biolreprod62.2.277","article-title":"Expression of carbohydrate antigens in the goat uterus during early pregnancy and on steroid-treated polarized uterine epithelial cells in vitro","volume":"62","author":"Powell","year":"2000","journal-title":"Biol Reprod"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"1298","DOI":"10.1182\/blood-2006-06-030551","article-title":"Nonhematopoietic\/endothelial SSEA-1+ cells define the most primitive progenitors in the adult murine bone marrow mesenchymal compartment","volume":"109","author":"Anjos-Afonso","year":"2007","journal-title":"Blood"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"1057","DOI":"10.1016\/S0301-472X(03)00237-6","article-title":"Selectins and anti-CD15 (Lewis x\/a) antibodies transmit activation signals in Hodgkin's lymphoma-derived cell lines","volume":"31","author":"Ohana-Malka","year":"2003","journal-title":"Exp Hematol"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1186\/s12951-021-00793-9","article-title":"Highly glycosylated MUC1 mediates high affinity L-selectin binding at the human endometrial surface","volume":"19","author":"Francis","year":"2021","journal-title":"J Nanobiotechnology"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"718","DOI":"10.1095\/biolreprod66.3.718","article-title":"Analysis of osteopontin at the maternal-placental interface in pigs","volume":"66","author":"Garlow","year":"2002","journal-title":"Biol Reprod"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"1294","DOI":"10.1095\/biolreprod.105.045153","article-title":"Steroid regulation of cell specific secreted phosphoprotein 1 (osteopontin) expression in the pregnant porcine uterus","volume":"73","author":"White","year":"2005","journal-title":"Biol Reprod"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1177\/10454411000110030101","article-title":"Osteopontin","volume":"11","author":"Sodek","year":"2000","journal-title":"Crit Rev Oral Biol Med"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"1583","DOI":"10.1042\/BCJ20170205","article-title":"Biological role of site-specific O-glycosylation in cell adhesion activity and phosphorylation of osteopontin","volume":"475","author":"Oyama","year":"2018","journal-title":"Biochem J"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"79","DOI":"10.3390\/cancers9070079","article-title":"Roles of Integrin \u03b16\u03b24 Glycosylation in Cancer","volume":"9","author":"Kariya","year":"2017","journal-title":"Cancers (Basel)"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"1218","DOI":"10.1038\/onc.2008.471","article-title":"Contribution of sialidase NEU1 to suppression of metastasis of human colon cancer cells through desialylation of integrin beta4","volume":"28","author":"Uemura","year":"2009","journal-title":"Oncogene"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"1446","DOI":"10.1016\/j.fertnstert.2010.04.036","article-title":"Difucosylated oligosaccharide Lewis Y is contained within integrin \u03b1v\u03b23 on RL95-2 cells and required for endometrial receptivity","volume":"95","author":"Zhang","year":"2011","journal-title":"Fertil Steril"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"78","DOI":"10.1016\/j.sbi.2018.12.005","article-title":"Protein O-fucosylation: structure and function","volume":"56","author":"Holdener","year":"2019","journal-title":"Curr Opin Struct Biol"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"601","DOI":"10.1093\/glycob\/cwx034","article-title":"Biological functions of fucose in mammals","volume":"27","author":"Schneider","year":"2017","journal-title":"Glycobiology"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"773","DOI":"10.1038\/s41417-019-0153-3","article-title":"MyoD1 suppresses cell migration and invasion by inhibiting FUT4 transcription in human gastric cancer cells","volume":"27","author":"Wu","year":"2020","journal-title":"Cancer Gene Ther"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"7300","DOI":"10.1074\/jbc.RA117.000775","article-title":"Distinct human \u03b1(1,3)-fucosyltransferases drive Lewis-X\/sialyl Lewis-X assembly in human cells","volume":"293","author":"Mondal","year":"2018","journal-title":"J Biol Chem"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1038\/s41420-019-0145-y","article-title":"Fucosyltransferase 1 and 2 play pivotal roles in breast cancer cells","volume":"5","author":"Lai","year":"2019","journal-title":"Cell Death Discov"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"356","DOI":"10.1038\/s41467-019-14178-y","article-title":"\u03b24GALT1 controls \u03b21 integrin function to govern thrombopoiesis and hematopoietic stem cell homeostasis","volume":"11","author":"Giannini","year":"2020","journal-title":"Nat Commun"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"1221","DOI":"10.1126\/science.abe0348","article-title":"Genetic and functional evidence links a missense variant in B4GALT1 to lower LDL and fibrinogen","volume":"374","author":"Montasser","year":"2021","journal-title":"Science"},{"key":"2023021512504869100_","doi-asserted-by":"crossref","first-page":"1393","DOI":"10.3892\/ijo.2015.3136","article-title":"Multifaceted roles of 5\u2032-regulatory region of the cancer associated gene B4GALT1 and its comparison with the gene family","volume":"47","author":"Al-Obaide","year":"2015","journal-title":"Int J Oncol"}],"container-title":["Biology of Reproduction"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/biolreprod\/advance-article-pdf\/doi\/10.1093\/biolre\/ioac204\/47816722\/ioac204.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/biolreprod\/article-pdf\/108\/2\/292\/49196924\/ioac204.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/biolreprod\/article-pdf\/108\/2\/292\/49196924\/ioac204.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,3,13]],"date-time":"2023-03-13T03:59:16Z","timestamp":1678679956000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/biolreprod\/article\/108\/2\/292\/6833511"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,11,19]]},"references-count":51,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2022,11,19]]},"published-print":{"date-parts":[[2023,2,13]]}},"URL":"https:\/\/doi.org\/10.1093\/biolre\/ioac204","relation":{},"ISSN":["0006-3363","1529-7268"],"issn-type":[{"value":"0006-3363","type":"print"},{"value":"1529-7268","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2023,2]]},"published":{"date-parts":[[2022,11,19]]}}}