{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,4]],"date-time":"2026-03-04T05:10:52Z","timestamp":1772601052207,"version":"3.50.1"},"reference-count":96,"publisher":"MDPI AG","issue":"20","license":[{"start":{"date-parts":[[2022,10,15]],"date-time":"2022-10-15T00:00:00Z","timestamp":1665792000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>The endothelial cells of the blood-brain barrier adhere closely, which is provided by tight junctions (TJs). The aim of the study was to assess the damage to the endothelial TJs in pregnancy, complicated by fetal growth restriction (FGR) and circulatory centralization (brain-sparing effect, BS). The serum concentrations of NR1 subunit of the N-methyl-D-aspartate receptor (NR1), nucleoside diphosphate kinase A (NME1), S100 calcium-binding protein B (S100B), occludin (OCLN), claudin-5 (CLN5), and zonula occludens protein \u2013 1 (zo-1), and the placental expressions of OCLN, claudin-4 (CLN4), CLN5, and zo-1 were assessed with ELISA. The significantly higher serum NME1 concentrations and the serum CLN5\/zo-1 index were observed in FGR pregnancy with BS, as compared to the FGR group without BS. The FGR newborns with BS were about 20 times more likely to develop an intraventricular hemorrhage (IVH) than the FGR infants without BS. The cerebroplacental ratio (CPR) allowed to predict the IVH in growth-restricted fetuses. The significantly lower placental CLN4 expression was observed in the FGR group with BS and who postnatally developed an IVH, as compared to the growth-restricted infants with BS without IVH signs. Pregnancy complicated by FGR and BS is associated with the destabilization of the fetal blood-brain barrier. The IVH in newborns is reflected in the inhibition of the placental CLN4 expression, which may be a useful marker in the prediction of an IVH among growth-restricted fetuses.<\/jats:p>","DOI":"10.3390\/ijms232012349","type":"journal-article","created":{"date-parts":[[2022,10,17]],"date-time":"2022-10-17T02:29:46Z","timestamp":1665973786000},"page":"12349","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":13,"title":["Blood-Brain Barrier Disintegration in Growth-Restricted Fetuses with Brain Sparing Effect"],"prefix":"10.3390","volume":"23","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-3185-5020","authenticated-orcid":false,"given":"Natalia","family":"Misan","sequence":"first","affiliation":[{"name":"Department of Perinatology and Gynecology, Poznan University of Medical Sciences, 33 Polna Street, 60-535 Poznan, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"S\u0142awomir","family":"Michalak","sequence":"additional","affiliation":[{"name":"Department of Neurochemistry and Neuropathology, Chair of Neurology, Poznan University of Medical Sciences, 49 Przybyszewskiego Street, 60-355 Poznan, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Katarzyna","family":"Kapska","sequence":"additional","affiliation":[{"name":"Department of Perinatology and Gynecology, Poznan University of Medical Sciences, 33 Polna Street, 60-535 Poznan, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Krystyna","family":"Osztynowicz","sequence":"additional","affiliation":[{"name":"Department of Neurochemistry and Neuropathology, Chair of Neurology, Poznan University of Medical Sciences, 49 Przybyszewskiego Street, 60-355 Poznan, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mariola","family":"Ropacka-Lesiak","sequence":"additional","affiliation":[{"name":"Department of Perinatology and Gynecology, Poznan University of Medical Sciences, 33 Polna Street, 60-535 Poznan, Poland"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2022,10,15]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1159\/000357592","article-title":"Update on the diagnosis and classification of fetal growth restriction and proposal of a stage-based management protocol","volume":"36","author":"Figueras","year":"2014","journal-title":"Fetal Diagn. Ther."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"67","DOI":"10.4137\/CMPed.S40070","article-title":"Intrauterine Growth Restriction: Antenatal and Postnatal Aspects","volume":"10","author":"Sharma","year":"2016","journal-title":"Clin. Med. Insights Pediatr."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1106","DOI":"10.1016\/S0140-6736(03)14466-2","article-title":"Cerebral palsy and intrauterine growth in single births: European collaborative study","volume":"362","author":"Jarvis","year":"2003","journal-title":"Lancet"},{"key":"ref_4","first-page":"332","article-title":"Intrauterine growth retardation (IUGR): Epidemiology and etiology","volume":"6","author":"Romo","year":"2009","journal-title":"Pediatr. Endocrinol. Rev."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"5675","DOI":"10.1113\/JP275428","article-title":"Therapeutic potential to reduce brain injury in growth restricted newborns","volume":"596","author":"Wixey","year":"2018","journal-title":"J. Physiol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"807","DOI":"10.1113\/JP271402","article-title":"The consequences of fetal growth restriction on brain structure and neurodevelopmental outcome","volume":"594","author":"Miller","year":"2016","journal-title":"J. Physiol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"551","DOI":"10.1016\/j.ijdevneu.2011.04.004","article-title":"The biological basis of injury and neuroprotection in the fetal and neonatal brain","volume":"29","author":"Rees","year":"2011","journal-title":"Int. J. Dev. Neurosci."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"R151","DOI":"10.1152\/ajpregu.00036.2014","article-title":"Impact of chronic hypoxemia on blood flow to the brain, heart, and adrenal gland in the late-gestation IUGR sheep fetus","volume":"308","author":"Poudel","year":"2015","journal-title":"Am. J. Physiol. Regul. Integr. Comp. Physiol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"212","DOI":"10.2174\/1573396314666180712114531","article-title":"Neonatal and Long-Term Consequences of Fetal Growth Restriction","volume":"14","author":"Colella","year":"2018","journal-title":"Curr. Pediatr. Rev."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1215","DOI":"10.1113\/JP271099","article-title":"The fetal brain sparing response to hypoxia: Physiological mechanisms","volume":"594","author":"Giussani","year":"2016","journal-title":"J. Physiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"649","DOI":"10.1161\/CIRCULATIONAHA.107.709717","article-title":"Fetal hemodynamic adaptive changes related to intrauterine growth: The Generation R Study","volume":"117","author":"Verburg","year":"2008","journal-title":"Circulation"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Garcia-Canadilla, P., Rudenick, P.A., Crispi, F., Cruz-Lemini, M., Palau, G., Camara, O., Gratacos, E., and Bijnens, B.H. (2014). A computational model of the fetal circulation to quantify blood redistribution in intrauterine growth restriction. PLoS Comput. Biol., 10.","DOI":"10.1371\/journal.pcbi.1003667"},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"MacDonald, T.M., Hui, L., and Tong, S. (2017). Reduced growth velocity across the third trimester is associated with placental insufficiency in fetuses born at a normal birthweight: A prospective cohort study. BMC Med., 15.","DOI":"10.1186\/s12916-017-0928-z"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"821","DOI":"10.1038\/pr.2016.24","article-title":"Intrauterine growth restriction: Impact on cardiovascular development and function throughout infancy","volume":"79","author":"Cohen","year":"2016","journal-title":"Pediatr. Res."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1002\/uog.5377","article-title":"Changes in regional fetal cerebral blood flow perfusion in relation to hemodynamic deterioration in severely growth-restricted fetuses","volume":"32","author":"Jansson","year":"2008","journal-title":"Ultrasound Obstet. Gynecol."},{"key":"ref_16","first-page":"79","article-title":"Intrauterine hypoxia: Clinical consequences and therapeutic perspectives","volume":"5","author":"Thompson","year":"2015","journal-title":"Res. Rep. Neonatol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"184","DOI":"10.1038\/pr.2017.37","article-title":"Detection and assessment of brain injury in the growth-restricted fetus and neonate","volume":"82","author":"Malhotra","year":"2017","journal-title":"Pediatr. Res."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1225","DOI":"10.1016\/j.neuroimage.2010.07.019","article-title":"Fractal-dimension analysis detects cerebral changes in preterm infants with and without intrauterine growth restriction","volume":"53","author":"Esteban","year":"2010","journal-title":"Neuroimage"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1016\/j.brainres.2011.01.032","article-title":"Differential effects of intrauterine growth restriction on brain structure and development in preterm infants: A magnetic resonance imaging study","volume":"1382","author":"Padilla","year":"2011","journal-title":"Brain Res."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"132","DOI":"10.1203\/01.PDR.0000128983.54614.7E","article-title":"Early alteration of structural and functional brain development in premature infants born with intrauterine growth restriction","volume":"56","author":"Tolsa","year":"2004","journal-title":"Pediatr. Res."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"2028","DOI":"10.1093\/brain\/awn137","article-title":"Primary cortical folding in the human newborn: An early marker of later functional development","volume":"131","author":"Dubois","year":"2008","journal-title":"Brain"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"56.e1","DOI":"10.1016\/j.ajog.2007.02.011","article-title":"Severe cell reduction in the future brain cortex in human growth-restricted fetuses and infants","volume":"197","author":"Samuelsen","year":"2007","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"238","DOI":"10.1159\/000488904","article-title":"Predictors of Cranial Ultrasound Abnormalities in Intrauterine Growth-Restricted Fetuses Born between 28 and 34 Weeks of Gestation: A Prospective Cohort Study","volume":"45","author":"Khazardoost","year":"2019","journal-title":"Fetal Diagn. Ther."},{"key":"ref_24","first-page":"125","article-title":"The role of Doppler indices in predicting intra ventricular hemorrhage and perinatal mortality in fetal growth restriction","volume":"14","author":"Marsoosi","year":"2012","journal-title":"Med. Ultrason."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"198","DOI":"10.1016\/S0002-9378(00)70513-8","article-title":"Morbidity and mortality among very-low-birth-weight neonates with intrauterine growth restriction. The Vermont Oxford Network","volume":"182","author":"Bernstein","year":"2000","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1596","DOI":"10.1067\/mob.2003.384","article-title":"Pregnancy outcomes associated with intrauterine growth restriction","volume":"188","author":"Gilbert","year":"2003","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"975","DOI":"10.1016\/j.jpeds.2015.08.025","article-title":"Intrauterine Growth Restriction, Head Size at Birth, and Outcome in Very Preterm Infants","volume":"167","author":"Guellec","year":"2015","journal-title":"J. Pediatr."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1498","DOI":"10.1111\/j.1651-2227.2010.01848.x","article-title":"Twelve-month neurodevelopmental outcome in preterm infants with and without intrauterine growth restriction","volume":"99","author":"Padilla","year":"2010","journal-title":"Acta Paediatr."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"469","DOI":"10.1177\/1933719110388847","article-title":"Cerebral maturation in IUGR and appropriate for gestational age preterm babies","volume":"18","author":"Ramenghi","year":"2011","journal-title":"Reprod. Sci."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"438","DOI":"10.1203\/PDR.0b013e318165c005","article-title":"Intrauterine growth restriction affects the preterm infant\u2019s hippocampus","volume":"63","author":"Lodygensky","year":"2008","journal-title":"Pediatr. Res."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1352","DOI":"10.1016\/j.neuroimage.2012.01.059","article-title":"Altered small-world topology of structural brain networks in infants with intrauterine growth restriction and its association with later neurodevelopmental outcome","volume":"60","author":"Batalle","year":"2012","journal-title":"Neuroimage"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"2793","DOI":"10.1093\/cercor\/bhu073","article-title":"Structural Brain Connectivity in School-Age Preterm Infants Provides Evidence for Impaired Networks Relevant for Higher Order Cognitive Skills and Social Cognition","volume":"25","author":"Vasung","year":"2015","journal-title":"Cereb. Cortex"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"e874","DOI":"10.1542\/peds.2010-1821","article-title":"Cognitive function after intrauterine growth restriction and very preterm birth","volume":"127","author":"Morsing","year":"2011","journal-title":"Pediatrics"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1007\/s004310000680","article-title":"Neonatal and neurodevelopmental outcome in infants born before 30 weeks of gestation with absent or reversed end-diastolic flow velocities in the umbilical artery","volume":"160","author":"Vossbeck","year":"2001","journal-title":"Eur. J. Pediatr."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1542\/peds.105.2.385","article-title":"The discrepancy between maturation of visual-evoked potentials and cognitive outcome at five years in very preterm infants with and without hemodynamic signs of fetal brain-sparing","volume":"105","author":"Scherjon","year":"2000","journal-title":"Pediatrics"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1016\/S0378-3782(98)00004-8","article-title":"Neurodevelopmental outcome at three years of age after fetal \u2018brain-sparing\u2019","volume":"52","author":"Scherjon","year":"1998","journal-title":"Early Hum. Dev."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"136","DOI":"10.1159\/000353631","article-title":"Neurodevelopment after fetal growth restriction","volume":"36","author":"Baschat","year":"2014","journal-title":"Fetal Diagn. Ther."},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Herrera, E.A., and Gonz\u00e1lez-Candia, A. (2021). Gestational Hypoxia and Blood-Brain Barrier Permeability: Early Origins of Cerebrovascular Dysfunction Induced by Epigenetic Mechanisms. Front. Physiol., 12.","DOI":"10.3389\/fphys.2021.717550"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1038\/nrn1824","article-title":"Astrocyte-endothelial interactions at the blood-brain barrier","volume":"7","author":"Abbott","year":"2006","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"598","DOI":"10.1016\/j.tins.2015.08.003","article-title":"The molecular constituents of the blood-brain barrier","volume":"38","author":"Chow","year":"2015","journal-title":"Trends Neurosci."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1038\/nrd.2015.21","article-title":"From blood-brain barrier to blood-brain interface: New opportunities for CNS drug delivery","volume":"15","author":"Banks","year":"2016","journal-title":"Nat. Rev. Drug Discov."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Heinbockel, T., and Zhou, Y. (2020). Blood-Brain Barrier Dysfunction in the Detrimental Brain Function. Connectivity and Functional Specialization in the Brain, IntechOpen.","DOI":"10.5772\/intechopen.87662"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1064","DOI":"10.1016\/j.cell.2015.10.067","article-title":"Establishment and Dysfunction of the Blood-Brain Barrier","volume":"163","author":"Zhao","year":"2015","journal-title":"Cell"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1186\/s12987-021-00240-9","article-title":"Circulating tight-junction proteins are potential biomarkers for blood-brain barrier function in a model of neonatal hypoxic\/ischemic brain injury","volume":"18","author":"Andersson","year":"2021","journal-title":"Fluids Barriers CNS"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1080\/08998280.2020.1727706","article-title":"Exploring blood-brain barrier hyperpermeability and potential biomarkers in traumatic brain injury","volume":"33","author":"Robinson","year":"2020","journal-title":"Proc. Bayl. Univ. Med. Cent."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1089\/neu.2014.3811","article-title":"A New Panel of Blood Biomarkers for the Diagnosis of Mild Traumatic Brain Injury\/Concussion in Adults","volume":"33","author":"Shan","year":"2016","journal-title":"J. Neurotrauma"},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Jiao, X., He, P., Li, Y., Fan, Z., Si, M., Xie, Q., Chang, X., and Huang, D. (2015). The role of circulating tight junction proteins in evaluating blood brain barrier disruption following intracranial hemorrhage. Dis. Markers, 2015.","DOI":"10.1155\/2015\/860120"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"277","DOI":"10.4103\/1673-5374.265562","article-title":"Neuroprotective mechanism of TMP269, a selective class IIA histone deacetylase inhibitor, after cerebral ischemia\/reperfusion injury","volume":"15","author":"Su","year":"2020","journal-title":"Neural Regen. Res."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"1139","DOI":"10.1111\/jcmm.12803","article-title":"DAC9 exacerbates endothelial injury in cerebral ischaemia\/reperfusion injury","volume":"20","author":"Shi","year":"2016","journal-title":"J. Cell Mol. Med."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1677","DOI":"10.1212\/WNL.0b013e31826e9a83","article-title":"Serum tight-junction proteins predict hemorrhagic transformation in ischemic stroke patients","volume":"79","author":"Kazmierski","year":"2012","journal-title":"Neurology"},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Pan, R., Yu, K., Weatherwax, T., Zheng, H., Liu, W., and Liu, K.J. (2017). Blood Occludin Level as a Potential Biomarker for Early Blood Brain Barrier Damage Following Ischemic Stroke. Sci. Rep., 7.","DOI":"10.1038\/srep40331"},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Ma, F., Zhang, X., and Yin, K.J. (2020). MicroRNAs in central nervous system diseases: A prospective role in regulating blood-brain barrier integrity. Exp. Neurol., 323.","DOI":"10.1016\/j.expneurol.2019.113094"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"744","DOI":"10.2174\/1567201813666160830124627","article-title":"Role of microRNAs on Blood Brain Barrier Dysfunction in Vascular Cognitive Impairment","volume":"14","author":"Toyama","year":"2017","journal-title":"Curr. Drug Deliv."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1016\/j.arr.2016.09.006","article-title":"Dysfunction of the neurovascular unit in ischemic stroke and neurodegenerative diseases: An aging effect","volume":"34","author":"Cai","year":"2017","journal-title":"Ageing Res. Rev."},{"key":"ref_55","doi-asserted-by":"crossref","unstructured":"Anantha, J., Goulding, S.R., Wyatt, S.L., Concannon, R.M., Collins, L.M., Sullivan, A.M., and O\u2019Keeffe, G.W. (2020). STRAP and NME1 Mediate the Neurite Growth-Promoting Effects of the Neurotrophic Factor GDF5. iScience, 23.","DOI":"10.2139\/ssrn.3571299"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1007\/s12035-021-02569-6","article-title":"NME1 Protects Against Neurotoxin-, \u03b1-Synuclein- and LRRK2-Induced Neurite Degeneration in Cell Models of Parkinson\u2019s Disease","volume":"59","author":"Anantha","year":"2022","journal-title":"Mol. Neurobiol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1006\/excr.1995.1086","article-title":"The association of the Nm23-M1 protein and beta-tubulin correlates with cell differentiation","volume":"217","author":"Lombardi","year":"1995","journal-title":"Exp. Cell Res."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1023\/A:1005589029959","article-title":"NM23\/nucleoside diphosphate kinase and signal transduction","volume":"32","author":"Otero","year":"2000","journal-title":"J. Bioenerg. Biomembr."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1006\/excr.2000.5037","article-title":"Nucleoside diphosphate kinase beta (Nm23-R1\/NDPKbeta) is associated with intermediate filaments and becomes upregulated upon cAMP-induced differentiation of rat C6 glioma","volume":"261","author":"Roymans","year":"2000","journal-title":"Exp. Cell Res."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1038\/labinvest.2017.102","article-title":"Extracellular NME proteins: A player or a bystander?","volume":"98","author":"Romani","year":"2018","journal-title":"Lab. Investig."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1016\/j.bbrc.2010.06.039","article-title":"Extracellular Nm23H1 stimulates neurite outgrowth from dorsal root ganglia neurons in vitro independently of nerve growth factor supplementation or its nucleoside diphosphate kinase activity","volume":"398","author":"Wright","year":"2010","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_62","doi-asserted-by":"crossref","unstructured":"L\u00f6\u00f6v, C., Shevchenko, G., and Geeyarpuram Nadadhur, A. (2013). Identification of injury specific proteins in a cell culture model of traumatic brain injury. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0055983"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"2234","DOI":"10.1002\/pmic.200300822","article-title":"Identification of post-mortem cerebrospinal fluid proteins as potential biomarkers of ischemia and neurodegeneration","volume":"4","author":"Lescuyer","year":"2004","journal-title":"Proteomics"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"2043","DOI":"10.1373\/clinchem.2005.053942","article-title":"PARK7 and nucleoside diphosphate kinase A as plasma markers for the early diagnosis of stroke","volume":"51","author":"Allard","year":"2005","journal-title":"Clin. Chem."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"338","DOI":"10.5604\/17322693.946637","article-title":"Glutamate NMDA receptors in pathophysiology and pharmacotherapy of selected nervous system diseases","volume":"65","author":"Dobrek","year":"2011","journal-title":"Postepy Hig. Med. Dosw."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"1039","DOI":"10.1038\/nn936","article-title":"NMDA receptor pathways as drug targets","volume":"5","author":"Kemp","year":"2002","journal-title":"Nat. Neurosci."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1016\/j.coph.2005.12.002","article-title":"Glutamate-based therapeutic approaches: Clinical trials with NMDA antagonists","volume":"6","author":"Muir","year":"2006","journal-title":"Curr. Opin. Pharmacol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"567","DOI":"10.2174\/18715273113126660196","article-title":"Novel approach to the role of NMDA receptors in traumatic brain injury","volume":"13","author":"Shohami","year":"2014","journal-title":"CNS Neurol. Disord. Drug Targets"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"131","DOI":"10.2174\/1566524043479248","article-title":"The rise and fall of NMDA antagonists for ischemic stroke","volume":"4","author":"Hoyte","year":"2004","journal-title":"Curr. Mol. Med."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"621","DOI":"10.2174\/138945007780618472","article-title":"Pathologically-activated therapeutics for neuroprotection: Mechanism of NMDA receptor block by memantine and S-nitrosylation","volume":"8","author":"Lipton","year":"2007","journal-title":"Curr. Drug Targets"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"162","DOI":"10.1159\/000077523","article-title":"NMDA receptors in the developing brain and effects of noxious insults","volume":"13","author":"Waters","year":"2004","journal-title":"Neurosignals"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"5157","DOI":"10.1074\/jbc.272.8.5157","article-title":"Characterization of protein kinase A and protein kinase C phosphorylation of the N-methyl-D-aspartate receptor NR1 subunit using phosphorylation site-specific antibodies","volume":"272","author":"Tingley","year":"1997","journal-title":"J. Biol. Chem."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"1223","DOI":"10.1007\/BF00968404","article-title":"Modification of modulatory sites of NMDA receptor in the fetal guinea pig brain during development","volume":"17","author":"Mishra","year":"1992","journal-title":"Neurochem. Res."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"R681","DOI":"10.1152\/ajpregu.90396.2008","article-title":"Intrauterine growth restriction due to uteroplacental insufficiency decreased white matter and altered NMDAR subunit composition in juvenile rat hippocampi","volume":"296","author":"Schober","year":"2009","journal-title":"Am. J. Physiol. Regul. Integr. Comp. Physiol."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"9079","DOI":"10.1038\/s41598-017-06300-1","article-title":"Treating the placenta to prevent adverse effects of gestational hypoxia on fetal brain development","volume":"7","author":"Phillips","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"819","DOI":"10.1373\/clinchem.2005.060665","article-title":"High maternal blood S100B concentrations in pregnancies complicated by intrauterine growth restriction and intraventricular hemorrhage","volume":"52","author":"Gazzolo","year":"2006","journal-title":"Clin. Chem."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1203\/00006450-200202000-00015","article-title":"Circulating S100beta protein is increased in intrauterine growth-retarded fetuses","volume":"51","author":"Gazzolo","year":"2002","journal-title":"Pediatr. Res."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1093\/molehr\/7.3.279","article-title":"Expression of ZO-1 and occludin in normal human placenta and in hydatidiform moles","volume":"7","author":"Marzioni","year":"2001","journal-title":"Mol. Hum. Reprod."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"433","DOI":"10.1007\/s00441-005-0135-7","article-title":"Endothelia of term human placentae display diminished expression of tight junction proteins during preeclampsia","volume":"324","year":"2006","journal-title":"Cell Tissue Res."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1083\/jcb.138.1.181","article-title":"Involvement of ZO-1 in cadherin-based cell adhesion through its direct binding to alpha catenin and actin filaments","volume":"138","author":"Itoh","year":"1997","journal-title":"J. Cell Biol."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"C1517","DOI":"10.1152\/ajpcell.00484.2008","article-title":"ZO-1 is involved in trophoblastic cell differentiation in human placenta","volume":"298","author":"Pidoux","year":"2010","journal-title":"Am. J. Physiol. Cell Physiol."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"1375","DOI":"10.2174\/1570159X16666180222164809","article-title":"The Role of VE-cadherin in Blood-brain Barrier Integrity under Central Nervous System Pathological Conditions","volume":"16","author":"Li","year":"2018","journal-title":"Curr. Neuropharmacol."},{"key":"ref_83","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 Obstet. Gynecol."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1148\/radiology.181.1.1887021","article-title":"In utero analysis of fetal growth: A sonographic weight standard","volume":"181","author":"Hadlock","year":"1991","journal-title":"Radiology"},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"497","DOI":"10.1148\/radiology.152.2.6739822","article-title":"Estimating fetal age: Computer-assisted analysis of multiple fetal growth parameters","volume":"152","author":"Hadlock","year":"1984","journal-title":"Radiology"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"1581","DOI":"10.1067\/mob.2000.107325","article-title":"The amniotic fluid index, single deepest poecket and two diameter poeket in normal pregnancy","volume":"182","author":"Magann","year":"2000","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"124","DOI":"10.1002\/uog.20","article-title":"The cerebroplacental Doppler ratio revisited","volume":"21","author":"Baschat","year":"2003","journal-title":"Ultrasound Obstet. Gynecol."},{"key":"ref_88","first-page":"197","article-title":"Scoring of uterine artery flow velocity waveform in the assessment of fetal growth restriction and\/or pregnancy induced hypertension","volume":"7","author":"Sekizuka","year":"1997","journal-title":"J. Matern. Fetal Investig."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"807","DOI":"10.1034\/j.1600-0412.2003.00203.x","article-title":"New score indicating placental vascular resistance","volume":"82","author":"Gudmundsson","year":"2003","journal-title":"Acta Obstet. Gynecol. Scand."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"655","DOI":"10.1002\/pd.4412","article-title":"Stage-based approach to the management of fetal growth restriction","volume":"34","author":"Figueras","year":"2014","journal-title":"Prenat. Diagn."},{"key":"ref_91","unstructured":"Dobrza\u0144ska, A., and Ry\u017cko, J. (2014). Wcze\u015bniactwo. Pediatria. Podr\u0119cznik do Lekarskiego Egzaminu Ko\u0144cowego i Pa\u0144stwowego Egzaminu Specjalizacyjnego, Elsevier Urban & Partner."},{"key":"ref_92","unstructured":"Korones, S.B. (1981). High Risk Newborn Infants. The Basis for Intensive Nursing Care, C.V. Mosby Co."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1016\/S0021-9258(19)52451-6","article-title":"Protein measurement with the Folin phenol reagent","volume":"193","author":"Lowry","year":"1951","journal-title":"J. Biol. Chem."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"529","DOI":"10.1016\/S0022-3476(78)80282-0","article-title":"Incidence and evolution of subependymal and intraventricular hemorrhage: A study of infants with birth weights less than 1500 gm","volume":"92","author":"Papile","year":"1978","journal-title":"J. Pediatr."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"809","DOI":"10.1148\/radiology.168.3.3406411","article-title":"End-stage periventricular leukomalacia: MR evaluation","volume":"168","author":"Baker","year":"1988","journal-title":"Radiology"},{"key":"ref_96","first-page":"1087","article-title":"Brain damage from perinatal asphyxia: Correlation of MR findings with gestational age","volume":"11","author":"Barkovich","year":"1990","journal-title":"AJNR Am. J. Neuroradiol."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/20\/12349\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T00:54:47Z","timestamp":1760144087000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/20\/12349"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,10,15]]},"references-count":96,"journal-issue":{"issue":"20","published-online":{"date-parts":[[2022,10]]}},"alternative-id":["ijms232012349"],"URL":"https:\/\/doi.org\/10.3390\/ijms232012349","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,10,15]]}}}