{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,20]],"date-time":"2026-05-20T23:15:05Z","timestamp":1779318905593,"version":"3.51.4"},"reference-count":29,"publisher":"Oxford University Press (OUP)","issue":"2","license":[{"start":{"date-parts":[[2023,5,27]],"date-time":"2023-05-27T00:00:00Z","timestamp":1685145600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/pages\/standard-publication-reuse-rights"}],"funder":[{"name":"Government of the Russian Federation","award":["14.W03.31.0009"],"award-info":[{"award-number":["14.W03.31.0009"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2023,7,21]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Passive transfer of antithyroid antibodies in mice leads to reproductive disorders. The purpose was to assess the placental tissue of experimental animals under the influence of the circulating thyroperoxidase antibodies. We performed an immunohistochemical examination of murine placentae after a passive transfer of thyroperoxidase antibodies. Placentae of mice that passively transferred IgG from healthy donors were used as control samples. For histological examination, 30 placental samples were selected from mice from the anti-TPO group and 40 placental samples were taken from mice from the IgG group. Immunostaining for VEGFR1, THBS 1, Laminin, CD31, CD34, FGF-\u03b2, CD56, CD14, TNF-\u03b1, kisspeptin, MCL 1, and Annexin V was performed. There is a significant decrease in the relative area of the expression of VEGFR1 (23.42 \u00b1 0.85 vs. 33.44 \u00b1 0.35, P &amp;lt; 0.01), thrombospondin 1 (31.29 \u00b1 0.83 vs. 34.51 \u00b1 0.75, P &amp;lt; 0.01), CD14 (25.80 \u00b1 0.57 vs. 32.07 \u00b1 0.36, P &amp;lt; .01), CD56 (30.08 \u00b1 0.90 vs. 34.92 \u00b1 0.15, P &amp;lt; 0.01), kisspeptin (25.94 \u00b1 0.47 vs. 31.27 \u00b1 0.57, P &amp;lt; 0.01), MCL 1 (29.24 \u00b1 1.06 vs. 38.57 \u00b1 0.79, P &amp;lt; 0.01) in the labyrinth zone of the placentae of mice from the anti-TPO group compared with control group. A significant increase in the relative expression of laminin and FGF-\u03b2 was noted in the group of mice to which antibodies to thyroperoxidase were transferred, compared with the control group (36.73 \u00b1 1.38 vs. 29.83 \u00b1 0.94, P &amp;lt; 0.01 and 23.26 \u00b1 0.61 vs. 16.38 \u00b1 1.01, P &amp;lt; 0.01respectively). Our study exposed an imbalance of pro- and anti-angiogenic factors, decreased representation of placental macrophages and NK cells, abnormal trophoblast invasion processes, and insufficient expression of antiapoptotic factors in the placentae of mice in which anti-TPO antibodies were passively transferred.<\/jats:p>","DOI":"10.1093\/cei\/uxad057","type":"journal-article","created":{"date-parts":[[2023,5,27]],"date-time":"2023-05-27T06:03:11Z","timestamp":1685167391000},"page":"235-242","source":"Crossref","is-referenced-by-count":2,"title":["Anti-TPO-mediated specific features of the placenta immunohistochemical profile and possible mechanisms for fetal loss"],"prefix":"10.1093","volume":"213","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-7801-7123","authenticated-orcid":false,"given":"Elena","family":"Borodina","sequence":"first","affiliation":[{"name":"Medical Faculty, Saint Petersburg State University , Saint Petersburg , Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Alexander M","family":"Gzgzyan","sequence":"additional","affiliation":[{"name":"Medical Faculty, Saint Petersburg State University , Saint Petersburg , Russia"},{"name":"D.O. Ott Research Institute of Obstetrics, Gynecology and Reproductive Medicine , Saint Petersburg , Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Liailia Kh","family":"Dzhemlikhanova","sequence":"additional","affiliation":[{"name":"Medical Faculty, Saint Petersburg State University , Saint Petersburg , Russia"},{"name":"D.O. Ott Research Institute of Obstetrics, Gynecology and Reproductive Medicine , Saint Petersburg , Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Dariko A","family":"Niauri","sequence":"additional","affiliation":[{"name":"Medical Faculty, Saint Petersburg State University , Saint Petersburg , Russia"},{"name":"D.O. Ott Research Institute of Obstetrics, Gynecology and Reproductive Medicine , Saint Petersburg , Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Gulrukhsor Kh","family":"Tolibova","sequence":"additional","affiliation":[{"name":"D.O. Ott Research Institute of Obstetrics, Gynecology and Reproductive Medicine , Saint Petersburg , Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Tatiana G","family":"Tral","sequence":"additional","affiliation":[{"name":"D.O. Ott Research Institute of Obstetrics, Gynecology and Reproductive Medicine , Saint Petersburg , Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Igor Y","family":"Kogan","sequence":"additional","affiliation":[{"name":"Medical Faculty, Saint Petersburg State University , Saint Petersburg , Russia"},{"name":"D.O. Ott Research Institute of Obstetrics, Gynecology and Reproductive Medicine , Saint Petersburg , Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Galina Kh","family":"Safarian","sequence":"additional","affiliation":[{"name":"Medical Faculty, Saint Petersburg State University , Saint Petersburg , Russia"},{"name":"D.O. Ott Research Institute of Obstetrics, Gynecology and Reproductive Medicine , Saint Petersburg , Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yuri","family":"Ostrinski","sequence":"additional","affiliation":[{"name":"Zabludowicz Center for Autoimmune Diseases, Sheba Medical Center, Affiliated with the Sackler Faculty of Medicine, Tel-Aviv University , Tel-Aviv , Israel"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Leonid P","family":"Churilov","sequence":"additional","affiliation":[{"name":"Medical Faculty, Saint Petersburg State University , Saint Petersburg , Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5406-7716","authenticated-orcid":false,"given":"Howard","family":"Amital","sequence":"additional","affiliation":[{"name":"Zabludowicz Center for Autoimmune Diseases, Sheba Medical Center, Affiliated with the Sackler Faculty of Medicine, Tel-Aviv University , Tel-Aviv , Israel"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Miri","family":"Blank","sequence":"additional","affiliation":[{"name":"Zabludowicz Center for Autoimmune Diseases, Sheba Medical Center, Affiliated with the Sackler Faculty of Medicine, Tel-Aviv University , Tel-Aviv , Israel"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yehuda","family":"Shoenfeld","sequence":"additional","affiliation":[{"name":"Zabludowicz Center for Autoimmune Diseases, Sheba Medical Center, Affiliated with the Sackler Faculty of Medicine, Tel-Aviv University , Tel-Aviv , Israel"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2023,5,27]]},"reference":[{"key":"2023072415482210300_CIT0001","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1089\/thy.2016.0457","article-title":"Guidelines of the American Thyroid Association for the Diagnosis and Management of Thyroid Disease During Pregnancy and the Postpartum","volume":"27","author":"Alexander","year":"2017","journal-title":"Thyroid"},{"key":"2023072415482210300_CIT0002","doi-asserted-by":"crossref","first-page":"101433","DOI":"10.1016\/j.beem.2020.101433","article-title":"TPO antibody positivity and adverse pregnancy outcomes","volume":"34","author":"Dhillon-Smith","year":"2020","journal-title":"Best Pract Res Clin Endocrinol Metab"},{"key":"2023072415482210300_CIT0003","doi-asserted-by":"crossref","first-page":"2104","DOI":"10.1016\/j.fertnstert.2008.07.1704","article-title":"Increased fetal abortion rate in autoimmune thyroid disease is related to circulating TPO autoantibodies in an autoimmune thyroiditis animal model","volume":"91","author":"Lee","year":"2009","journal-title":"Fertil Steril"},{"key":"2023072415482210300_CIT0004","doi-asserted-by":"crossref","first-page":"1094","DOI":"10.1093\/humrep\/deg210","article-title":"The pathogenic role of anti-thyroglobulin antibody on pregnancy: evidence from an active immunization model in mice","volume":"18","author":"Matalon","year":"2003","journal-title":"Hum Reprod"},{"key":"2023072415482210300_CIT0005","doi-asserted-by":"crossref","first-page":"e13331","DOI":"10.1111\/aji.13331","article-title":"The pathogenic role of circulating Hashimoto\u2019s thyroiditis-derived TPO-positive IgG on fetal loss in na\u00efve mice","volume":"85","author":"Borodina","year":"2021","journal-title":"Am J Reprod Immunol"},{"key":"2023072415482210300_CIT0006","first-page":"54","article-title":"Structure of rat placenta in different terms of normal pregnancy","volume":"1","author":"Matsyuk","year":"2012","journal-title":"J Grodno State Medical Univ"},{"key":"2023072415482210300_CIT0007","first-page":"73","article-title":"Structural and functional comparison of human and mouse placenta as justification for modeling miscarriage","volume":"1","author":"Boltovskaya","year":"2014","journal-title":"Clin. Exp. Morphol."},{"key":"2023072415482210300_CIT0008","first-page":"180","article-title":"Development of structures and transport functions in the mouse placenta","volume":"20","author":"Watson","year":"2005","journal-title":"Physiology (Bethesda)"},{"key":"2023072415482210300_CIT0009","first-page":"129","article-title":"Vasculogenesis and angiogenesis in placental development","volume":"LVI","author":"Sokolov","year":"2007","journal-title":"J. Obstetrics Women\u2019s Dis."},{"key":"2023072415482210300_CIT0010","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1007\/s10456-019-09694-w","article-title":"Reconciling the distinct roles of angiogenic\/anti-angiogenic factors in the placenta and maternal circulation of normal and pathological pregnancies","volume":"23","author":"Umapathy","year":"2020","journal-title":"Angiogenesis."},{"key":"2023072415482210300_CIT0011","doi-asserted-by":"crossref","first-page":"2543","DOI":"10.1080\/14767058.2018.1441279","article-title":"Maternal serum thrombospondin-1 is significantly altered in cases with established preeclampsia","volume":"32","author":"Ulu","year":"2019","journal-title":"J Matern Fetal Neonatal Med"},{"key":"2023072415482210300_CIT0012","doi-asserted-by":"crossref","first-page":"19588","DOI":"10.1038\/srep19588","article-title":"Hypoxia-inducible miR-210 contributes to preeclampsia via targeting thrombospondin type I domain containing 7A","volume":"6","author":"Luo","year":"2016","journal-title":"Sci Rep"},{"key":"2023072415482210300_CIT0013","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1007\/s10517-011-1292-1","article-title":"Expression of thrombospondin-1 gene mRNA and protein in the placenta in gestosis","volume":"151","author":"Ostankova","year":"2011","journal-title":"Bull Exp Biol Med"},{"key":"2023072415482210300_CIT0014","doi-asserted-by":"crossref","first-page":"61","DOI":"10.3109\/10641955.2013.837173","article-title":"The comparison of endogenous angiogenesis inhibitors in normotensive and preeclamptic placentas: an immunohistochemical study","volume":"33","author":"Ayaz","year":"2014","journal-title":"Hypertens Pregnancy"},{"key":"2023072415482210300_CIT0015","doi-asserted-by":"crossref","first-page":"e201900515","DOI":"10.26508\/lsa.201900515","article-title":"Laminin is the ECM niche for trophoblast stem cells","volume":"3","author":"Kiyozumi","year":"2020","journal-title":"Life Sci Alliance"},{"key":"2023072415482210300_CIT0016","doi-asserted-by":"crossref","first-page":"1476","DOI":"10.1002\/jbm.a.36350","article-title":"Placental basement membrane proteins are required for effective cytotrophoblast invasion in a three-dimensional bioprinted placenta model","volume":"106","author":"Kuo","year":"2018","journal-title":"J Biomed Mater Res A"},{"key":"2023072415482210300_CIT0017","doi-asserted-by":"crossref","first-page":"754","DOI":"10.3389\/fcell.2020.00754","article-title":"Laminins regulate placentation and pre-eclampsia: focus on trophoblasts and endothelial cells","volume":"8","author":"Liu","year":"2020","journal-title":"Front Cell Dev Biol"},{"key":"2023072415482210300_CIT0018","doi-asserted-by":"crossref","first-page":"4909","DOI":"10.12659\/MSM.905418","article-title":"Hypoxia-induced activation of JAK\/STAT3 signaling pathway promotes trophoblast cell viability and angiogenesis in preeclampsia","volume":"23","author":"Xu","year":"2017","journal-title":"Med Sci Monit"},{"key":"2023072415482210300_CIT0019","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1186\/1746-1596-5-24","article-title":"Intrauterine growth restriction and placental angiogenesis","volume":"5","author":"Barut","year":"2010","journal-title":"Diagn Pathol"},{"key":"2023072415482210300_CIT0020","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1016\/j.preghy.2019.02.007","article-title":"CD-34+ and VE-cadherin+ endothelial progenitor cells in preeclampsia and normotensive pregnancies","volume":"16","author":"Brown","year":"2019","journal-title":"Pregnancy Hypertens."},{"key":"2023072415482210300_CIT0021","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1016\/j.placenta.2019.02.001","article-title":"CD34 immunostain increases the sensitivity of placental diagnosis of fetal vascular malperfusion in stillbirth","volume":"77","author":"Stanek","year":"2019","journal-title":"Placenta"},{"key":"2023072415482210300_CIT0022","first-page":"8161","article-title":"Role of kisspeptin\/GPR54 in the first trimester trophoblast of women with a history of recurrent spontaneous abortion","volume":"10","author":"Li","year":"2017","journal-title":"Int J ClinExpPathol"},{"key":"2023072415482210300_CIT0023","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1007\/s00404-019-05408-1","article-title":"Placental protein expression of kisspeptin-1 (KISS1) and the kisspeptin-1 receptor (KISS1R) in pregnancy complicated by diabetes mellitus or preeclampsia","volume":"301","author":"Kapustin","year":"2020","journal-title":"Arch Gynecol Obstet"},{"key":"2023072415482210300_CIT0024","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1016\/j.preghy.2015.11.001","article-title":"Elevated placental expression at the maternal-fetal interface but diminished maternal circulatory kisspeptin in preeclamptic pregnancies","volume":"6","author":"Matjila","year":"2016","journal-title":"Pregnancy Hypertens."},{"key":"2023072415482210300_CIT0025","doi-asserted-by":"crossref","first-page":"960","DOI":"10.3389\/fimmu.2019.00960","article-title":"Uterine natural killer cells","volume":"10","author":"Sojka","year":"2019","journal-title":"Front Immunol"},{"key":"2023072415482210300_CIT0026","doi-asserted-by":"crossref","first-page":"720","DOI":"10.1093\/humupd\/dmaa062","article-title":"Uterine natural killer cells: from foe to friend in reproduction","volume":"27","author":"D\u00edaz-Hern\u00e1ndez","year":"2021","journal-title":"Hum Reprod Update"},{"key":"2023072415482210300_CIT0027","doi-asserted-by":"crossref","first-page":"e0164353","DOI":"10.1371\/journal.pone.0164353","article-title":"Induced human decidual NK-like cells improve utero-placental perfusion in mice","volume":"11","author":"Cavalli","year":"2016","journal-title":"PLoS One"},{"key":"2023072415482210300_CIT0028","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1007\/s00005-019-00552-7","article-title":"Role of macrophages in pregnancy and related complications","volume":"67","author":"Jena","year":"2019","journal-title":"Arch Immunol Ther Exp (Warsz)"},{"key":"2023072415482210300_CIT0029","doi-asserted-by":"crossref","first-page":"2628","DOI":"10.3389\/fimmu.2018.02628","article-title":"Hofbauer cells: their role in healthy and complicated pregnancy","volume":"9","author":"Reyes","year":"2018","journal-title":"Front Immunol"}],"container-title":["Clinical and Experimental Immunology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/cei\/advance-article-pdf\/doi\/10.1093\/cei\/uxad057\/50569129\/uxad057.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/cei\/article-pdf\/213\/2\/235\/50947671\/uxad057.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/cei\/article-pdf\/213\/2\/235\/50947671\/uxad057.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,7,24]],"date-time":"2023-07-24T15:48:44Z","timestamp":1690213724000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/cei\/article\/213\/2\/235\/7180997"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,5,27]]},"references-count":29,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2023,5,27]]},"published-print":{"date-parts":[[2023,7,21]]}},"URL":"https:\/\/doi.org\/10.1093\/cei\/uxad057","relation":{},"ISSN":["0009-9104","1365-2249"],"issn-type":[{"value":"0009-9104","type":"print"},{"value":"1365-2249","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2023,8,1]]},"published":{"date-parts":[[2023,5,27]]}}}