{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,26]],"date-time":"2026-09-26T09:37:58Z","timestamp":1790415478035,"version":"4.1.0"},"reference-count":50,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2020,6,3]],"date-time":"2020-06-03T00:00:00Z","timestamp":1591142400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000027","name":"National Institute on Alcohol Abuse and Alcoholism","doi-asserted-by":"publisher","award":["AA017068"],"award-info":[{"award-number":["AA017068"]}],"id":[{"id":"10.13039\/100000027","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000027","name":"National Institute on Alcohol Abuse and Alcoholism","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000027","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Neurosci."],"DOI":"10.3389\/fnins.2020.00519","type":"journal-article","created":{"date-parts":[[2020,6,3]],"date-time":"2020-06-03T05:24:10Z","timestamp":1591161850000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":9,"title":["Ethanol-Induced Alterations in Placental and Fetal Cerebrocortical Annexin-A4 and Cerebral Cavernous Malformation Protein 3 Are Associated With Reductions in Fetal Cortical VEGF Receptor Binding and Microvascular Density"],"prefix":"10.3389","volume":"14","author":[{"given":"Daniel D.","family":"Savage","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Martina J.","family":"Rosenberg","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laurent","family":"Coquet","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Morgan W.","family":"Porch","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nyika A.","family":"Allen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christian","family":"Roux","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Caroline","family":"Aligny","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Thierry","family":"Jouenne","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bruno J.","family":"Gonzalez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2020,6,3]]},"reference":[{"key":"B1","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/0376-8716(84)90012-7","article-title":"Prenatal effects of alcohol.","volume":"14","author":"Abel","year":"1984","journal-title":"Drug Alcohol Depend"},{"key":"B2","author":"Altman","year":"1995","journal-title":"Atlas of Prenatal Rat Brain."},{"key":"B3","doi-asserted-by":"publisher","first-page":"1390","DOI":"10.1111\/acer.12378","article-title":"Maternal and neonatal plasma microrna biomarkers for fetal alcohol exposure in an ovine model.","volume":"38","author":"Balaraman","year":"2014","journal-title":"Alcohol Clin. Exp. Res."},{"key":"B4","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0165081","article-title":"Plasma mirna profiles in pregnant women predict infant outcomes following prenatal alcohol exposure.","volume":"11","author":"Balaraman","year":"2016","journal-title":"PLoS One"},{"key":"B5","doi-asserted-by":"publisher","first-page":"205","DOI":"10.1016\/j.neuron.2010.04.006","article-title":"Vegfr2 (KDR\/Flk1) signaling mediates axon growth in response to semaphorin 3E in the developing brain.","volume":"66","author":"Bellon","year":"2010","journal-title":"Neuron"},{"key":"B6","doi-asserted-by":"publisher","first-page":"253","DOI":"10.1038\/nn.4213","article-title":"KIF1A inhibition immortalizes brain stem cells but blocks BDNF-mediated neuronal migration.","volume":"19","author":"Carabalona","year":"2016","journal-title":"Nat. Neurosci."},{"key":"B7","doi-asserted-by":"publisher","first-page":"1431","DOI":"10.1111\/acer.13808","article-title":"Alcohol-related alterations in placental imprinted gene expression in humans mediate effects of prenatal alcohol exposure on postnatal growth.","volume":"42","author":"Carter","year":"2018","journal-title":"Alcohol Clin. Exp. Res."},{"key":"B8","doi-asserted-by":"publisher","first-page":"264","DOI":"10.1542\/peds.2014-2171","article-title":"Misdiagnosis and missed diagnoses in foster and adopted children with prenatal alcohol exposure.","volume":"135","author":"Chasnoff","year":"2015","journal-title":"Pediatrics"},{"key":"B9","doi-asserted-by":"publisher","first-page":"650","DOI":"10.1111\/j.1530-0277.1990.tb01222.x","article-title":"Neuropsychological deficits in fetal alcohol syndrome and fetal alcohol effects.","volume":"14","author":"Conry","year":"1990","journal-title":"Alcohol Clin. Exp. Res."},{"key":"B10","doi-asserted-by":"publisher","first-page":"2229","DOI":"10.2337\/diabetes.48.11.2229","article-title":"Increased renal expression of vascular endothelial growth factor (VEGF) and its receptor VEGFR-2 in experimental diabetes.","volume":"48","author":"Cooper","year":"1999","journal-title":"Diabetes"},{"key":"B11","author":"Coquet","year":"2006","journal-title":"A Proteomic Approach of Biofilm Cell Physiology. Methods in Biotechnology, Immobilization of Enzymes and Cells"},{"key":"B12","doi-asserted-by":"publisher","first-page":"177","DOI":"10.1002\/bdra.20440","article-title":"Fetal alcohol syndrome (FAS) in C57Bl\/6 mice detected through proteomics screening of the amniotic fluid.","volume":"82","author":"Datta","year":"2008","journal-title":"Birth Defects Res. A Clin. Mol. Teratol."},{"key":"B13","doi-asserted-by":"publisher","first-page":"47","DOI":"10.1016\/j.alcohol.2018.07.007","article-title":"Impact of moderate prenatal alcohol exposure on histaminergic neurons, histidine decarboxylase levels and histamine H2 receptors in adult rat offspring.","volume":"76","author":"Davies","year":"2019","journal-title":"Alcohol"},{"key":"B14","doi-asserted-by":"publisher","first-page":"1551","DOI":"10.1111\/acer.13448","article-title":"Placental proteomics reveal insights into fetal alcohol spectrum disorders.","volume":"41","author":"Davis-Anderson","year":"2017","journal-title":"Alcohol Clin. Exp. Res."},{"key":"B15","doi-asserted-by":"publisher","first-page":"1519","DOI":"10.1111\/j.1530-0277.2012.01757.x","article-title":"Gene expression changes in C57Bl\/6J and DBA\/2J mice following prenatal alcohol exposure.","volume":"36","author":"Downing","year":"2012","journal-title":"Alcohol Clin. Exp. Res."},{"key":"B16","first-page":"640","article-title":"Alterations of annexin expression in pathological neuronal and glial reactions. Immunohistochemical localization of annexins I, II (p36 and p11 subunits), IV, and VI in the human hippocampus.","volume":"145","author":"Eberhard","year":"1994","journal-title":"Am. J. Pathol."},{"key":"B17","doi-asserted-by":"publisher","first-page":"1881","DOI":"10.1007\/s00018-013-1532-9","article-title":"Signaling pathways and the cerebral cavernous malformations proteins: lessons from structural biology.","volume":"71","author":"Fisher","year":"2014","journal-title":"Cell Mol. Life Sci."},{"key":"B18","doi-asserted-by":"publisher","first-page":"826","DOI":"10.1111\/acer.13026","article-title":"Alcohol use during pregnancy is associated with specific alterations in microrna levels in maternal serum.","volume":"40","author":"Gardiner","year":"2016","journal-title":"Alcohol Clin. Exp. Res."},{"key":"B19","doi-asserted-by":"publisher","first-page":"457","DOI":"10.1016\/s0022-3476(78)80449-1","article-title":"The effects of moderate alcohol consumption during pregnancy on fetal growth and morphogenesis.","volume":"92","author":"Hanson","year":"1978","journal-title":"J. Pediatr"},{"key":"B20","doi-asserted-by":"publisher","DOI":"10.1126\/scisignal.2000722","article-title":"Stabilization of VEGFR2 signaling by cerebral cavernous malformation 3 is critical for vascular development.","volume":"3","author":"He","year":"2010","journal-title":"Sci. Signal"},{"key":"B21","doi-asserted-by":"publisher","first-page":"19009","DOI":"10.3390\/ijms160819009","article-title":"Angiogenesis-related biomarkers (sFlt-1\/PLGF) in the prediction and diagnosis of placental dysfunction: an approach for clinical integration.","volume":"16","author":"Herraiz","year":"2015","journal-title":"Int. J. Mol. Sci."},{"key":"B22","doi-asserted-by":"publisher","first-page":"244","DOI":"10.1172\/JCI115568","article-title":"Binding sites for vascular endothelial growth factor are localized on endothelial cells in adult rat tissues.","volume":"89","author":"Jakeman","year":"1992","journal-title":"J. Clin. Invest."},{"key":"B23","doi-asserted-by":"publisher","first-page":"952","DOI":"10.1002\/ana.23699","article-title":"Prenatal alcohol exposure affects vasculature development in the neonatal brain.","volume":"72","author":"Jegou","year":"2012","journal-title":"Ann. Neurol."},{"key":"B24","doi-asserted-by":"publisher","first-page":"236","DOI":"10.1002\/neu.20215","article-title":"Vascular endothelial growth factor stimulates neurite outgrowth from cerebral cortical neurons via Rho kinase signaling.","volume":"66","author":"Jin","year":"2006","journal-title":"J. Neurobiol."},{"key":"B25","doi-asserted-by":"publisher","first-page":"19230","DOI":"10.1074\/jbc.M312025200","article-title":"Intercellular adhesion molecule-1 (ICAM-1) regulates endothelial cell motility through a nitric oxide-dependent pathway.","volume":"279","author":"Kevil","year":"2004","journal-title":"J. Biol. Chem."},{"key":"B26","doi-asserted-by":"publisher","DOI":"10.1186\/s40478-017-0444-6","article-title":"Plgf, a placental marker of fetal brain defects after in utero alcohol exposure.","volume":"5","author":"Lecuyer","year":"2017","journal-title":"Acta Neuropathol. Commun."},{"key":"B27","doi-asserted-by":"publisher","DOI":"10.1007\/s00018-019-03248-5","article-title":"Glutamate controls vessel-associated migration of GABA interneurons from the pial migratory route via NMDA receptors and endothelial protease activation.","author":"Leger","year":"2019","journal-title":"Cell Mol. Life Sci."},{"key":"B28","doi-asserted-by":"publisher","first-page":"339","DOI":"10.1007\/978-1-59745-281-6_21","article-title":"Silver staining of proteins in 2DE gels.","volume":"519","author":"Lelong","year":"2009","journal-title":"Methods Mol. Biol."},{"key":"B29","doi-asserted-by":"publisher","first-page":"14809","DOI":"10.1523\/JNEUROSCI.1368-13.2013","article-title":"Endothelial VEGF sculpts cortical cytoarchitecture.","volume":"33","author":"Li","year":"2013","journal-title":"J. Neurosci."},{"key":"B30","doi-asserted-by":"publisher","first-page":"1404","DOI":"10.1242\/dev.093526","article-title":"Ccm3, a gene associated with cerebral cavernous malformations, is required for neuronal migration.","volume":"141","author":"Louvi","year":"2014","journal-title":"Development"},{"key":"B31","doi-asserted-by":"publisher","first-page":"130","DOI":"10.1093\/molehr\/gav069","article-title":"Placental growth factor deficiency is associated with impaired cerebral vascular development in mice.","volume":"22","author":"Luna","year":"2016","journal-title":"Mol. Hum. Reprod."},{"key":"B32","doi-asserted-by":"publisher","first-page":"784","DOI":"10.3109\/00365516009062448","article-title":"Quantitative determination of amino acids by combined displacement and paper chromatography.","volume":"4","author":"Lundquist","year":"1959","journal-title":"Clin. Chim. Acta"},{"key":"B33","doi-asserted-by":"publisher","DOI":"10.1186\/s13148-018-0439-6","article-title":"DNA methylation as a predictor of fetal alcohol spectrum disorder.","volume":"10","author":"Lussier","year":"2018","journal-title":"Clin. Epigenetics"},{"key":"B34","doi-asserted-by":"publisher","DOI":"10.1101\/cshperspect.a001834","article-title":"Guiding neuronal cell migrations.","volume":"2","author":"Mar\u00edn","year":"2010","journal-title":"Cold Spring Harb. Perspect Biol."},{"key":"B35","doi-asserted-by":"publisher","first-page":"1129","DOI":"10.1160\/TH03-12-0778","article-title":"Levels of annexin IV and V in the plasma of pregnant and postpartum women.","volume":"91","author":"Masuda","year":"2004","journal-title":"Thromb. Haemost"},{"key":"B36","doi-asserted-by":"publisher","first-page":"217","DOI":"10.1016\/s0925-4439(02)00168-0","article-title":"Ethanol-induced augmentation of annexin IV in cultured cells and the enhancement of cytotoxicity by overexpression of annexin IV by ethanol.","volume":"1588","author":"Ohkawa","year":"2002","journal-title":"Biochim. Biophys. Acta"},{"key":"B37","doi-asserted-by":"publisher","first-page":"495","DOI":"10.1016\/j.modgep.2005.11.001","article-title":"Patterns of expression of the three cerebral cavernous malformation (CCM) genes during embryonic and postnatal brain development.","volume":"6","author":"Petit","year":"2006","journal-title":"Gene Expr. Patterns"},{"key":"B38","doi-asserted-by":"publisher","first-page":"538","DOI":"10.1016\/j.reprotox.2012.08.008","article-title":"Alcohol-induced alterations in maternal uterine endothelial proteome: a quantitative ITRAQ mass spectrometric approach.","volume":"34","author":"Ramadoss","year":"2012","journal-title":"Reprod. Toxicol."},{"key":"B39","doi-asserted-by":"publisher","first-page":"673","DOI":"10.1016\/j.alcohol.2009.10.002","article-title":"Effects of moderate drinking during pregnancy on placental gene expression.","volume":"44","author":"Rosenberg","year":"2010","journal-title":"Alcohol"},{"key":"B40","doi-asserted-by":"publisher","first-page":"1793","DOI":"10.1111\/j.1530-0277.2010.01266.x","article-title":"Effects of a novel cognition-enhancing agent on fetal ethanol-induced learning deficits.","volume":"34","author":"Savage","year":"2010","journal-title":"Alcohol Clin. Exp. Res."},{"key":"B41","doi-asserted-by":"publisher","first-page":"978","DOI":"10.1016\/s0022-3476(80)80621-4","article-title":"Behavior and learning difficulties in children of normal intelligence born to alcoholic mothers.","volume":"96","author":"Shaywitz","year":"1980","journal-title":"J. Pediatr."},{"key":"B42","doi-asserted-by":"publisher","first-page":"44S","DOI":"10.1097\/01.ALC.0000026975.39372.A5","article-title":"Ethanol-induced augmentation of annexin IV expression in rat C6 glioma and human A549 adenocarcinoma cells.","volume":"26","author":"Sohma","year":"2002","journal-title":"Alcohol. Clin. Exp. Res."},{"key":"B43","doi-asserted-by":"publisher","first-page":"55S","DOI":"10.1097\/00000374-200106001-00013","article-title":"Alteration of annexin IV expression in alcoholics.","volume":"25","author":"Sohma","year":"2001","journal-title":"Alcohol. Clin. Exp. Res."},{"key":"B44","doi-asserted-by":"publisher","first-page":"662","DOI":"10.1111\/j.1530-0277.1990.tb01224.x","article-title":"Moderate prenatal alcohol exposure: effects on child IQ and learning problems at age 7 1\/2 years.","volume":"14","author":"Streissguth","year":"1990","journal-title":"Alcohol. Clin Exp. Res."},{"key":"B45","doi-asserted-by":"publisher","first-page":"379","DOI":"10.1126\/science.aad3839","article-title":"Oligodendrocyte precursors migrate along vasculature in the developing nervous system.","volume":"351","author":"Tsai","year":"2016","journal-title":"Science"},{"key":"B46","doi-asserted-by":"publisher","first-page":"191","DOI":"10.1124\/jpet.109.165027","article-title":"Effects of the cognition-enhancing agent ABT-239 on fetal ethanol-induced deficits in dentate gyrus synaptic plasticity.","volume":"334","author":"Varaschin","year":"2010","journal-title":"J. Pharmacol. Exp. Ther."},{"key":"B47","doi-asserted-by":"publisher","DOI":"10.3389\/fnint.2015.00065","article-title":"Fetal alcohol spectrum disorders: an overview from the glia perspective.","volume":"9","author":"Wilhelm","year":"2015","journal-title":"Front. Integr. Neurosci."},{"key":"B48","doi-asserted-by":"publisher","DOI":"10.1038\/ncomms3149","article-title":"Autonomous vascular networks synchronize GABA neuron migration in the embryonic forebrain.","volume":"4","author":"Won","year":"2013","journal-title":"Nat. Commun."},{"key":"B49","doi-asserted-by":"publisher","first-page":"62","DOI":"10.1111\/j.1471-4159.1990.tb13283.x","article-title":"Characterization of annexins in mammalian brain.","volume":"54","author":"Woolgar","year":"1990","journal-title":"J. Neurochem."},{"key":"B50","doi-asserted-by":"publisher","first-page":"407","DOI":"10.1111\/jcmm.12022","article-title":"Loss of CCM3 impairs DLL4-Notch signalling: implication in endothelial angiogenesis and in inherited cerebral cavernous malformations.","volume":"17","author":"You","year":"2013","journal-title":"J. Cell Mol. Med."}],"container-title":["Frontiers in Neuroscience"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/article\/10.3389\/fnins.2020.00519\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,6,3]],"date-time":"2020-06-03T05:24:13Z","timestamp":1591161853000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/article\/10.3389\/fnins.2020.00519\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,6,3]]},"references-count":50,"alternative-id":["10.3389\/fnins.2020.00519"],"URL":"https:\/\/doi.org\/10.3389\/fnins.2020.00519","relation":{},"ISSN":["1662-453X"],"issn-type":[{"value":"1662-453X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,6,3]]},"article-number":"519"}}