{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,2]],"date-time":"2026-10-02T13:39:56Z","timestamp":1790948396145,"version":"4.1.0"},"reference-count":40,"publisher":"MDPI AG","issue":"24","license":[{"start":{"date-parts":[[2021,12,13]],"date-time":"2021-12-13T00:00:00Z","timestamp":1639353600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004166","name":"Medical University of Warsaw","doi-asserted-by":"publisher","award":["1W51\/M\/MB1\/N\/20"],"award-info":[{"award-number":["1W51\/M\/MB1\/N\/20"]}],"id":[{"id":"10.13039\/501100004166","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JCM"],"abstract":"<jats:p>Placental transfer of glucose constitutes one of the major determinants of the intrauterine foetal growth. The objective of the present study was to evaluate the expression of glucose transporter proteins GLUT-1, GLUT-3, GLUT-8 and GLUT-12 in the placenta of macrosomic, small-for-gestational-age (SGA) and growth-restricted foetuses (FGR). A total of 70 placental tissue samples were collected from women who delivered macrosomic \u22654000 g (n = 26), SGA (n = 11), growth-restricted (n = 13) and healthy control neonates (n = 20). Computer-assisted quantitative morphometry of stained placental sections was performed to determine the expression of selected GLUT proteins. Immunohistochemical staining identified the presence of all glucose transporters in the placental tissue. Quantitative morphometric analysis performed for the vascular density-matched placental samples revealed a significant decrease in GLUT-1 and increase in GLUT-3 protein expression in pregnancies complicated by FGR as compared to other groups (p &lt; 0.05). In addition, expression of GLUT-8 was significantly decreased among SGA foetuses (p &lt; 0.05). No significant differences in GLUTs expression were observed in women delivering macrosomic neonates. In the SGA group foetal birth weight (FBW) was negatively correlated with GLUT-3 (rho = \u22120.59, p &lt; 0.05) and positively with GLUT-12 (rho = 0.616, p &lt; 0.05) placental expression. In addition, a positive correlation between FBW and GLUT-12 expression in the control group (rho = 0.536, p &lt; 0.05) was noted. In placentas derived from FGR-complicated pregnancies the expression of two major glucose transporters GLUT-1 and GLUT-3 is altered. On the contrary, idiopathic foetal macrosomia is not associated with changes in the placental expression of GLUT-1, GLUT-3, GLUT-8 and GLUT-12 proteins.<\/jats:p>","DOI":"10.3390\/jcm10245833","type":"journal-article","created":{"date-parts":[[2021,12,14]],"date-time":"2021-12-14T01:20:41Z","timestamp":1639444841000},"page":"5833","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":20,"title":["Differential Expression of Glucose Transporter Proteins GLUT-1, GLUT-3, GLUT-8 and GLUT-12 in the Placenta of Macrosomic, Small-for-Gestational-Age and Growth-Restricted Foetuses"],"prefix":"10.3390","volume":"10","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-7445-7546","authenticated-orcid":false,"given":"Pawe\u0142 Jan","family":"Stanirowski","sequence":"first","affiliation":[{"name":"1st Department of Obstetrics and Gynecology, Medical University of Warsaw, 02-015 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0124-060X","authenticated-orcid":false,"given":"Dariusz","family":"Szukiewicz","sequence":"additional","affiliation":[{"name":"Department of Biophysics, Physiology and Pathophysiology, Faculty of Health Sciences, Medical University of Warsaw, 02-004 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8071-0368","authenticated-orcid":false,"given":"Agata","family":"Majewska","sequence":"additional","affiliation":[{"name":"1st Department of Obstetrics and Gynecology, Medical University of Warsaw, 02-015 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mateusz","family":"W\u0105troba","sequence":"additional","affiliation":[{"name":"Department of Biophysics, Physiology and Pathophysiology, Faculty of Health Sciences, Medical University of Warsaw, 02-004 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Micha\u0142","family":"Pyzlak","sequence":"additional","affiliation":[{"name":"Department of Biophysics, Physiology and Pathophysiology, Faculty of Health Sciences, Medical University of Warsaw, 02-004 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dorota","family":"Bomba-Opo\u0144","sequence":"additional","affiliation":[{"name":"1st Department of Obstetrics and Gynecology, Medical University of Warsaw, 02-015 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Miros\u0142aw","family":"Wielgo\u015b","sequence":"additional","affiliation":[{"name":"1st Department of Obstetrics and Gynecology, Medical University of Warsaw, 02-015 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,12,13]]},"reference":[{"key":"ref_1","first-page":"332","article-title":"Intrauterine growth retardation (IUGR): Epidemiology and etiology","volume":"6","author":"Romo","year":"2009","journal-title":"Pediatric Endocrinol. Rev."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1007\/s00404-019-05400-9","article-title":"Trends in the incidence of fetal macrosomia and its phenotypes in the United States, 1971\u20132017","volume":"301","author":"Salihu","year":"2020","journal-title":"Arch. Gynecol. Obstet."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"15016","DOI":"10.1038\/s41598-021-94375-2","article-title":"Prevalence of low birth weight and macrosomia estimates based on heaping adjustment method in China","volume":"11","author":"Shen","year":"2021","journal-title":"Sci. Rep."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1061","DOI":"10.1007\/s00404-017-4341-9","article-title":"Fetal growth restriction: Current knowledge","volume":"295","author":"Nardozza","year":"2017","journal-title":"Arch. Gynecol. Obstet."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1372","DOI":"10.1067\/mob.2003.302","article-title":"Macrosomic births in the United States: Determinants, outcomes, and proposed grades of risk","volume":"188","author":"Boulet","year":"2003","journal-title":"Am. J. Obs. Gynecol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"521","DOI":"10.2174\/157016109789043982","article-title":"The role of trophoblast nutrient and ion transporters in the development of pregnancy complications and adult disease","volume":"7","author":"Jansson","year":"2009","journal-title":"Curr. Vasc. Pharmacol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"12","DOI":"10.3389\/fphys.2016.00012","article-title":"Placental Responses to Changes in the Maternal Environment Determine Fetal Growth","volume":"7","author":"Dimasuay","year":"2016","journal-title":"Front. Physiol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"165373","DOI":"10.1016\/j.bbadis.2018.12.024","article-title":"Complex, coordinated and highly regulated changes in placental signaling and nutrient transport capacity in IUGR","volume":"1866","author":"Chassen","year":"2020","journal-title":"Biochim. Biophys. Acta Mol. Basis Dis."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"S109","DOI":"10.1016\/j.placenta.2006.01.017","article-title":"Placental transport and metabolism in fetal overgrowth -- a workshop report","volume":"27","author":"Jansson","year":"2006","journal-title":"Placenta"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"165359","DOI":"10.1016\/j.bbadis.2018.12.010","article-title":"Human placental glucose transport in fetoplacental growth and metabolism","volume":"1866","author":"Illsley","year":"2020","journal-title":"Biochim. Biophys. Acta Mol. Basis Dis."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1016\/j.mam.2012.07.001","article-title":"The SLC2 (GLUT) family of membrane transporters","volume":"34","author":"Mueckler","year":"2013","journal-title":"Mol. Asp. Med."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/bs.apcsb.2019.12.003","article-title":"Expression of placental glucose transporter proteins in pregnancies complicated by fetal growth disorders","volume":"123","author":"Stanirowski","year":"2021","journal-title":"Adv. Protein Chem. Struct. Biol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"206","DOI":"10.1530\/eje.0.1320206","article-title":"Increase in human placental glucose transporter-1 during pregnancy","volume":"132","author":"Sakata","year":"1995","journal-title":"Eur. J. Endocrinol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1041","DOI":"10.1016\/j.placenta.2011.09.014","article-title":"Glucose transporter 3 (GLUT3) protein expression in human placenta across gestation","volume":"32","author":"Brown","year":"2011","journal-title":"Placenta"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1072","DOI":"10.1016\/j.placenta.2013.08.010","article-title":"Placental glucose transporter 3 (GLUT3) is up-regulated in human pregnancies complicated by late-onset intrauterine growth restriction","volume":"34","author":"Janzen","year":"2013","journal-title":"Placenta"},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Jones, H.N., Crombleholme, T., and Habli, M. (2013). Adenoviral-Mediated Placental Gene Transfer of IGF-1 Corrects Placental Insufficiency via Enhanced Placental Glucose Transport Mechanisms. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0074632"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Janzen, C., Lei, M.Y.Y., Jeong, I.S.D., Ganguly, A., Sullivan, P., Paharkova, V., Capodanno, G., Nakamura, H., Perry, A., and Shin, B.C. (2018). Humanin (HN) and glucose transporter 8 (GLUT8) in pregnancies complicated by intrauterine growth restriction. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0193583"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"566","DOI":"10.1053\/plac.2002.0925","article-title":"GLUT12 expression in human placenta in first trimester and term","volume":"24","author":"Gude","year":"2003","journal-title":"Placenta"},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Stanirowski, P.J., Szukiewicz, D., Majewska, A., W\u0105troba, M., Pyzlak, M., Bomba-Opo\u0144, D., and Wielgo\u015b, M. (2021). Placental expression of glucose transporters GLUT-1, GLUT-3, GLUT-8 and GLUT-12 in pregnancies complicated by gestational and type 1 diabetes mellitus. J. Diabetes Investig.","DOI":"10.1111\/jdi.13680"},{"key":"ref_20","first-page":"1554","article-title":"Glucose transporter expression and distribution in the human placenta throughout gestation and in intrauterine growth retardation","volume":"77","author":"Jansson","year":"1993","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"392","DOI":"10.1053\/plac.2002.0826","article-title":"Glucose transport and system A activity in syncytiotrophoblast microvillous and basal plasma membranes in intrauterine growth restriction","volume":"23","author":"Jansson","year":"2002","journal-title":"Placenta"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1159\/000291493","article-title":"Placental glucose transporters in fetal intrauterine growth retardation and macrosomia","volume":"44","author":"Kainulainen","year":"1997","journal-title":"Gynecol. Obstet. Investig."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1002\/uog.15884","article-title":"Consensus definition of fetal growth restriction: A Delphi procedure","volume":"48","author":"Gordijn","year":"2016","journal-title":"Ultrasound Obs. Gynecol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1016\/j.jpeds.2017.12.059","article-title":"Consensus Based Definition of Growth Restriction in the Newborn","volume":"196","author":"Beune","year":"2018","journal-title":"J. Pediatr."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"857","DOI":"10.1016\/S0140-6736(14)60932-6","article-title":"International standards for newborn weight, length, and head circumference by gestational age and sex: The Newborn Cross-Sectional Study of the INTERGROWTH-21st Project","volume":"384","author":"Villar","year":"2014","journal-title":"Lancet"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"799","DOI":"10.1007\/s12020-016-1202-4","article-title":"Impact of pre-gestational and gestational diabetes mellitus on the expression of glucose transporters GLUT-1, GLUT-4 and GLUT-9 in human term placenta","volume":"55","author":"Stanirowski","year":"2017","journal-title":"Endocrine"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1016\/j.placenta.2004.12.010","article-title":"Effects of chronic hypoxia in vivo on the expression of human placental glucose transporters","volume":"27","author":"Zamudio","year":"2006","journal-title":"Placenta"},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Zamudio, S., Torricos, T., Fik, E., Oyala, M., Echalar, L., Pullockaran, J., Tutino, E., Martin, B., Belliappa, S., and Balanza, E. (2010). Hypoglycemia and the origin of hypoxia-induced reduction in human fetal growth. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0008551"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1663","DOI":"10.1093\/infdis\/jit803","article-title":"Insight into the pathogenesis of fetal growth restriction in placental malaria: Decreased placental glucose transporter isoform 1 expression","volume":"209","author":"Chandrasiri","year":"2014","journal-title":"J. Infect. Dis."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1016\/j.placenta.2017.04.023","article-title":"Placental glucose transporter (GLUT)-1 is down-regulated in preeclampsia","volume":"55","author":"Marini","year":"2017","journal-title":"Placenta"},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Chang, Y.L., Chao, A.S., Chang, S.D., and Cheng, P.J. (2021). Placental glucose transporter 1 and 3 gene expression in Monochorionic twin pregnancies with selective fetal growth restriction. BMC Pregnancy Childbirth, 21.","DOI":"10.1186\/s12884-021-03744-2"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1203\/00006450-200003000-00005","article-title":"Glucose metabolism is elevated and vascular resistance and maternofetal transfer is normal in perfused placental cotyledons from severely growth-restricted fetuses","volume":"47","author":"Challis","year":"2000","journal-title":"Pediatr. Res."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"E614","DOI":"10.1152\/ajpendo.91019.2008","article-title":"GLUT8, the enigmatic intracellular hexose transporter","volume":"296","author":"Schmidt","year":"2009","journal-title":"Am. J. Physiol. Endocrinol. Metab."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1095\/biolreprod.111.097675","article-title":"Slc2a8 deficiency in mice results in reproductive and growth impairments","volume":"87","author":"Adastra","year":"2012","journal-title":"Biol. Reprod."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"969","DOI":"10.1006\/bbrc.2001.5866","article-title":"Mouse GLUT8: Genomic organization and regulation of expression in 3T3-L1 adipocytes by glucose","volume":"288","author":"Scheepers","year":"2001","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"R237","DOI":"10.1152\/ajpregu.00093.2014","article-title":"Differential regulation of GLUT1 and GLUT8 expression by hypoxia in mammary epithelial cells","volume":"307","author":"Shao","year":"2014","journal-title":"Am. J. Physiol. Regul. Integr. Comp. Physiol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"650","DOI":"10.1080\/14767058.2017.1387897","article-title":"Analysis of correlations between the placental expression of glucose transporters GLUT-1, GLUT-4 and GLUT-9 and selected maternal and fetal parameters in pregnancies complicated by diabetes mellitus","volume":"32","author":"Stanirowski","year":"2019","journal-title":"J. Matern. Fetal. Neonatal Med."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"227.e1","DOI":"10.1016\/j.ajog.2014.08.009","article-title":"Increased glucose and placental GLUT-1 in large infants of obese nondiabetic mothers","volume":"212","author":"Acosta","year":"2015","journal-title":"Am. J. Obs. Gynecol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"18175","DOI":"10.1073\/pnas.2006958117","article-title":"Identification of GLUT12\/SLC2A12 as a urate transporter that regulates the blood urate level in hyperuricemia model mice","volume":"117","author":"Toyoda","year":"2020","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"S67","DOI":"10.1016\/j.placenta.2007.11.001","article-title":"Uric acid as a pathogenic factor in preeclampsia","volume":"29","author":"Bainbridge","year":"2008","journal-title":"Placenta"}],"container-title":["Journal of Clinical Medicine"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2077-0383\/10\/24\/5833\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T07:46:35Z","timestamp":1760168795000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2077-0383\/10\/24\/5833"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,12,13]]},"references-count":40,"journal-issue":{"issue":"24","published-online":{"date-parts":[[2021,12]]}},"alternative-id":["jcm10245833"],"URL":"https:\/\/doi.org\/10.3390\/jcm10245833","relation":{},"ISSN":["2077-0383"],"issn-type":[{"value":"2077-0383","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,12,13]]}}}