{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,17]],"date-time":"2026-06-17T15:09:38Z","timestamp":1781708978912,"version":"3.54.5"},"reference-count":39,"publisher":"MDPI AG","issue":"12","license":[{"start":{"date-parts":[[2024,6,8]],"date-time":"2024-06-08T00:00:00Z","timestamp":1717804800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Albert Szent-Gyorgyi Medical School of the University of Szeged","award":["5S 724 (A202)"],"award-info":[{"award-number":["5S 724 (A202)"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Galectin-13 (Gal-13) is predominantly produced by the syncytiotrophoblast, while laeverin is expressed on the outgrowing extravillous trophoblast, and both are thought to be biomarkers of preeclampsia. The aim of this study was to assess the correlation between concentrations of Gal-13 and laeverin measured in maternal serum and amniotic fluid at 16\u201322 weeks of gestation and the sonographic assessment of the fetoplacental measurements. Fetal biometric data and placental volume and perfusion indices were measured in 62 singleton pregnancies. Serum and amniotic levels of Gal-13 and laeverin levels were measured using a sandwich ELISA. Both amniotic fluid and serum Gal-13 levels expressed a negative correlation to the plasma laeverin level in mid-pregnancy. Serum laeverin level correlated positively with the gestational length at delivery (\u03b2 = 0.39, p &lt; 0.05), while the amniotic laeverin level correlated well with the abdominal circumference of the fetus (\u03b2 = 0.44, p &lt; 0.05). Furthermore, laeverin level in the amnion correlated positively with the estimated fetal weight (\u03b2 = 0.48, p &lt; 0.05) and with the placental volume (\u03b2 = 0.32, p &lt; 0.05). Logistic regression analyses revealed that a higher circulating Gal-13 level represents a slightly significant risk factor (OR: 1.01) for hypertension-related diseases during pregnancy. It is a novelty that laeverin can be detected in the amniotic fluid, and amnion laeverin concentration represents a potential biomarker of fetoplacental growth.<\/jats:p>","DOI":"10.3390\/ijms25126347","type":"journal-article","created":{"date-parts":[[2024,6,10]],"date-time":"2024-06-10T10:08:43Z","timestamp":1718014123000},"page":"6347","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Galectin-13 and Laeverin Levels Interfere with Human Fetoplacental Growth"],"prefix":"10.3390","volume":"25","author":[{"given":"M\u00e1ri\u00f3","family":"Vincze","sequence":"first","affiliation":[{"name":"Department of Obstetrics and Gynecology, University of Szeged, H-6725 Szeged, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"suffix":"Jr.","given":"J\u00e1nos","family":"Sikovanyecz","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, University of Szeged, H-6725 Szeged, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Imre","family":"F\u00f6ldesi","sequence":"additional","affiliation":[{"name":"Department of Laboratory Medicine, University of Szeged, H-6720 Szeged, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1168-7261","authenticated-orcid":false,"given":"Andrea","family":"Sur\u00e1nyi","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, University of Szeged, H-6725 Szeged, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Szabolcs","family":"V\u00e1rb\u00edr\u00f3","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, University of Szeged, H-6725 Szeged, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"G\u00e1bor","family":"N\u00e9meth","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, University of Szeged, H-6725 Szeged, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"J\u00e1nos","family":"Sikovanyecz","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, University of Szeged, H-6725 Szeged, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7485-9895","authenticated-orcid":false,"given":"Zoltan","family":"Kozinszky","sequence":"additional","affiliation":[{"name":"Capio Specialized Center for Gynecology, Solna, 182 88 Stockholm, Sweden"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,6,8]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1296","DOI":"10.1136\/jcp.2008.055277","article-title":"The anatomy of the normal placenta","volume":"61","author":"Huppertz","year":"2008","journal-title":"J. Clin. Pathol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1088024","DOI":"10.3389\/fimmu.2022.1088024","article-title":"Placental galectins regulate innate and adaptive immune responses in pregnancy","volume":"13","author":"Oravecz","year":"2022","journal-title":"Front. Immunol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1240","DOI":"10.3389\/fimmu.2019.01240","article-title":"Placental galectins are key players in regulating the maternal adaptive immune response","volume":"10","author":"Balogh","year":"2019","journal-title":"Front. Immunol."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Sammar, M., Drobnjak, T., Mandala, M., Gizurarson, S., Huppertz, B., and Meiri, H. (2019). Galectin 13 (PP13) facilitates remodeling and structural stabilization of maternal vessels during pregnancy. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20133192"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1065","DOI":"10.1111\/j.1432-1033.2004.04004.x","article-title":"Functional analyses of placental protein 13\/galectin-13","volume":"271","author":"Than","year":"2004","journal-title":"Eur. J. Biochem."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1016\/j.placenta.2023.04.015","article-title":"Galectins are critical regulators of cytokine signalling at feto-maternal interface in infection-associated spontaneous preterm birth","volume":"138","author":"Bhati","year":"2023","journal-title":"Placenta"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"145","DOI":"10.3389\/fimmu.2020.00145","article-title":"Placental Protein 13 (Galectin-13) Polarizes Neutrophils toward an Immune Regulatory Phenotype","volume":"11","author":"Vokalova","year":"2020","journal-title":"Front. Immunol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1177\/1933719111424445","article-title":"Placental protein 13 and decidual zones of necrosis: An immunologic diversion that may be linked to preeclampsia","volume":"19","author":"Kliman","year":"2012","journal-title":"Reprod. Sci."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"230","DOI":"10.1159\/000151344","article-title":"Longitudinal determination of serum placental protein 13 during development of preeclampsia","volume":"24","author":"Huppertz","year":"2008","journal-title":"Fetal Diagn. Ther."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Kazatsker, M.M., Sharabi-Nov, A., Meiri, H., Sammour, R., and Sammar, M. (2023). Augmented Placental Protein 13 in Placental-Associated Extracellular Vesicles in Term and Preterm Preeclampsia Is Further Elevated by Corticosteroids. Int. J. Mol. Sci., 24.","DOI":"10.3390\/ijms241512051"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"962","DOI":"10.1016\/j.bbrc.2003.12.024","article-title":"Human extravillous trophoblasts express laeverin, a novel protein that belongs to membrane-bound gluzincin metallopeptidases","volume":"313","author":"Fujiwara","year":"2004","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"12051","DOI":"10.1016\/S0143-4004(83)80043-5","article-title":"Uteroplacental arterial changes related to interstitial trophoblast migration in early human pregnancy","volume":"4","author":"Pijnenborg","year":"1983","journal-title":"Placenta"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"107692","DOI":"10.1016\/j.isci.2023.107692","article-title":"Laeverin\/aminopeptidase Q induces indoleamine 2,3-dioxygenase-1 in human monocytes","volume":"26","author":"Suzuki","year":"2023","journal-title":"iScience"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Fujiwara, H., Ono, M., Sato, Y., Imakawa, K., Iizuka, T., Kagami, K., Fujiwara, T., Horie, A., Tani, H., and Hattori, A. (2020). Promoting roles of embryonic signals in embryo implantation and placentation in cooperation with endocrine and immune systems. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21051885"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"20088","DOI":"10.1074\/jbc.M702650200","article-title":"Laeverin\/aminopeptidase Q, a novel bestatin-sensitive leucine aminopeptidase belonging to the M1 family of aminopeptidases","volume":"282","author":"Maruyama","year":"2007","journal-title":"J. Biol. Chem."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"S70","DOI":"10.1016\/j.placenta.2007.01.005","article-title":"Membrane-Bound Peptidases Regulate Human Extravillous Trophoblast Invasion","volume":"28","author":"Fujiwara","year":"2007","journal-title":"Placenta"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"686.e1","DOI":"10.1016\/j.ajog.2014.06.047","article-title":"Placental expression of aminopeptidase-Q (laeverin) and its role in the pathophysiology of preeclampsia","volume":"211","author":"Nystad","year":"2014","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"424","DOI":"10.1016\/j.placenta.2009.01.012","article-title":"Differential Placental Gene Expression in Severe Preeclampsia","volume":"30","author":"Sitras","year":"2009","journal-title":"Placenta"},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Nystad, M., Sitras, V., Flo, K., Widnes, C., V\u00e5rtun, \u00c5., Wilsgaard, T., and Acharya, G. (2016). Longitudinal reference ranges for maternal plasma laeverin, and its role as a potential biomarker of preeclampsia. BMC Pregnancy Childbirth, 16.","DOI":"10.1186\/s12884-016-1156-9"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"536","DOI":"10.1111\/aogs.13304","article-title":"Laeverin protein expression in normal and preeclamptic placentas using tissue microarray analysis","volume":"97","author":"Nystad","year":"2018","journal-title":"Acta Obstet. Gynecol. Scand."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"3348","DOI":"10.1080\/14767058.2018.1463368","article-title":"Maternal serum laeverin (aminopeptidase Q) measured in the first trimester of pregnancy does not predict preeclampsia","volume":"32","author":"Pihl","year":"2019","journal-title":"J. Matern. Fetal Neonatal Med."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Vincze, M., Sikovanyecz, J., Moln\u00e1r, A., F\u00f6ldesi, I., Sur\u00e1nyi, A., V\u00e1rb\u00edr\u00f3, S., N\u00e9meth, G., Sikovanyecz, J., and Kozinszky, Z. (2024). Predictive Capabilities of Human Leukocyte Antigen-G and Galectin-13 Levels in the Amniotic Fluid and Maternal Blood for the Pregnancy Outcome. Medicina, 60.","DOI":"10.3390\/medicina60010085"},{"key":"ref_23","first-page":"78","article-title":"PP030. Transmission electron microscopy reveals leakage of laeverin into the villous capillaries and ectopic expression in the cytoplasm instead of cell membrane of the trophoblasts in preeclamptic placentas","volume":"3","author":"Nystad","year":"2013","journal-title":"Pregnancy Hypertens. Int. J. Women\u2019s Cardiovasc. Health"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"S30","DOI":"10.1016\/j.placenta.2010.09.006","article-title":"Placenta-bound and body fluid PP13 and its mRNA in normal pregnancy compared to preeclampsia, HELLP and preterm delivery","volume":"32","author":"Sammar","year":"2011","journal-title":"Placenta"},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Kay, H., Nelson, M., and Wang, Y. (2011). The Placenta: From Development to Disease, Wiley-Blackwell.","DOI":"10.1002\/9781444393927"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1267","DOI":"10.1093\/humrep\/des068","article-title":"Laeverin\/aminopeptidase Q induces trophoblast invasion during human early placentation","volume":"27","author":"Horie","year":"2012","journal-title":"Hum. Reprod."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"952","DOI":"10.1002\/pd.4172","article-title":"Placental three-dimensional power Doppler indices in mid-pregnancy and late pregnancy complicated by gestational diabetes mellitus","volume":"33","author":"Suranyi","year":"2013","journal-title":"Prenat. Diagn."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1016\/j.acthis.2007.02.008","article-title":"Vasculogenesis and angiogenesis in the early human placenta","volume":"109","author":"Demir","year":"2007","journal-title":"Acta Histochem."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1002\/uog.2686","article-title":"A novel approach to first-trimester screening for early pre-eclampsia combining serum PP-13 and Doppler ultrasound","volume":"27","author":"Nicolaides","year":"2006","journal-title":"Ultrasound Obstet. Gynecol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"781","DOI":"10.1002\/pd.2287","article-title":"First trimester maternal serum placental protein 13 for the prediction of pre-eclampsia in women with a priori high risk","volume":"29","author":"Khalil","year":"2009","journal-title":"Prenat. Diagn."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"370","DOI":"10.3892\/etm.2022.11297","article-title":"Predictive performance of first trimester serum galectin-13\/PP-13 in preeclampsia screening: A systematic review and meta-analysis","volume":"23","author":"Vasilache","year":"2022","journal-title":"Exp. Ther. Med."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1016\/j.preghy.2017.03.004","article-title":"Evaluation of placental vascularization by three-dimensional ultrasound examination in second and third trimester of pregnancies complicated by chronic hypertension, gestational hypertension or pre-eclampsia","volume":"8","author":"Suranyi","year":"2017","journal-title":"Pregnancy Hypertens."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"608","DOI":"10.1080\/00016340802056178","article-title":"Placenta weight in pre-eclampsia","volume":"87","author":"Dahlstrom","year":"2008","journal-title":"Acta Obstet. Gynecol. Scand."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1016\/j.placenta.2014.11.019","article-title":"Galectin-13\/PP-13 expression in term placentas of gestational diabetes mellitus pregnancies","volume":"36","author":"Unverdorben","year":"2015","journal-title":"Placenta"},{"key":"ref_35","unstructured":"(2024, May 01). K\u00f6zponti Statisztikai Hivatal (Central Statistical Office H. KSH Database 22.1.1.7. Live Births by Main Characteristics of Mother and Newborn 1980\u20132023). Available online: https:\/\/www.ksh.hu\/stadat_files\/nep\/en\/nep0007.html."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1016\/0002-9378(85)90298-4","article-title":"Estimation of fetal weight with the use of head, body, and femur measurements\u2014A prospective study","volume":"151","author":"Hadlock","year":"1985","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_37","first-page":"155","article-title":"Magyar sz\u00fclet\u00e9skori testt\u00f6meg-\u00e9s testhossz-standardok az 1990\u20131996. \u00e9vi orsz\u00e1gos \u00e9lvesz\u00fclet\u00e9si adatok alapj\u00e1n","volume":"63","author":"Joubert","year":"2000","journal-title":"Magy. N\u00f6orvosok Lapja"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1016\/j.ijgo.2014.10.035","article-title":"Examination of placental three-dimensional power Doppler indices and perinatal outcome in pregnancies complicated by intrauterine growth restriction","volume":"129","author":"Molnar","year":"2015","journal-title":"Int. J. Gynaecol. Obstet."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"202","DOI":"10.1002\/uog.7608","article-title":"Reproducibility of regional placental vascularity\/perfusion measurement using 3D power Doppler","volume":"36","author":"Lai","year":"2010","journal-title":"Ultrasound Obstet. Gynecol."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/25\/12\/6347\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T14:55:44Z","timestamp":1760108144000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/25\/12\/6347"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,6,8]]},"references-count":39,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2024,6]]}},"alternative-id":["ijms25126347"],"URL":"https:\/\/doi.org\/10.3390\/ijms25126347","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,6,8]]}}}