{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,24]],"date-time":"2026-09-24T07:03:26Z","timestamp":1790233406975,"version":"4.1.0"},"reference-count":63,"publisher":"Wiley","issue":"6","license":[{"start":{"date-parts":[[2013,3,27]],"date-time":"2013-03-27T00:00:00Z","timestamp":1364342400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"}],"funder":[{"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":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Intl J of Devlp Neuroscience"],"published-print":{"date-parts":[[2013,10]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Fetal alcohol spectrum disorders represent a wide range of symptoms associated with <jats:italic>in utero<\/jats:italic> alcohol exposure. Animal models of FASD have been useful in determining the specific neurological consequences of developmental alcohol exposure, but the mechanisms of those consequences are unclear. Long\u2010lasting changes to the epigenome are proposed as a mechanism of alcohol\u2010induced teratogenesis in the hippocampus. The current study utilized a three\u2010trimester rodent model of FASD to examine changes to some of the enzymatic regulators of the epigenome in adolescence. Combined pre\u2010 and post\u2010natal alcohol exposureresulted in a significant increase in DNA methyltransferase activity (DNMT), without affecting histone deacetylase activity (HDAC). Developmental alcohol exposure also caused a change in gene expression of regulators of the epigenome, in particular, DNMT1, DNMT3a, and methyl CpG binding protein 2 (MeCP2). The modifications of the activity and expression of epigenetic regulators in the hippocampus of rodents perinatally exposed to alcohol suggest that alcohol's impact on the epigenome and its regulators may be one of the underlying mechanisms of alcohol teratogenesis.<\/jats:p>","DOI":"10.1016\/j.ijdevneu.2013.03.010","type":"journal-article","created":{"date-parts":[[2013,3,27]],"date-time":"2013-03-27T06:31:54Z","timestamp":1364365914000},"page":"391-397","update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":85,"title":["Alcohol exposure during development: Impact on the epigenome"],"prefix":"10.1002","volume":"31","author":[{"given":"Amy","family":"Perkins","sequence":"first","affiliation":[{"name":"Department of Psychology University of South Carolina Columbia SC 29208 United States"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Claudia","family":"Lehmann","sequence":"additional","affiliation":[{"name":"Department of Psychology University of South Carolina Columbia SC 29208 United States"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"R. Charles","family":"Lawrence","sequence":"additional","affiliation":[{"name":"Department of Psychology University of South Carolina Columbia SC 29208 United States"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sandra J.","family":"Kelly","sequence":"additional","affiliation":[{"name":"Department of Psychology University of South Carolina Columbia SC 29208 United States"},{"name":"Department of Pharmacology, Physiology, and Neuroscience University of South Carolina School of Medicine Columbia 29208 United States"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2013,3,27]]},"reference":[{"issue":"34","key":"e_1_2_8_2_1","doi-asserted-by":"crossref","first-page":"32282","DOI":"10.1074\/jbc.M104661200","article-title":"Dnmt3a and Dnmt3b are transcriptional repressors that exhibit unique localization properties to heterochromatin","volume":"276","author":"Bachman K.E.","year":"2001","journal-title":"Journal of Biological Chemistry"},{"key":"e_1_2_8_3_1","doi-asserted-by":"publisher","DOI":"10.1016\/0165-3806(81)90071-7"},{"key":"e_1_2_8_4_1","doi-asserted-by":"publisher","DOI":"10.1002\/cne.22009"},{"issue":"2","key":"e_1_2_8_5_1","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1016\/0741-8329(95)02049-7","article-title":"Prenatal alcohol exposure and the effects of environmental enrichment on hippocampal dendritic spine density","volume":"13","author":"Berman R.F.","year":"1996","journal-title":"Alcohol"},{"key":"e_1_2_8_6_1","doi-asserted-by":"publisher","DOI":"10.1002\/(SICI)1098-1063(2000)10:1<94::AID-HIPO11>3.0.CO;2-T"},{"issue":"1","key":"e_1_2_8_7_1","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1111\/j.1530-0277.1990.tb00455.x","article-title":"Alcohol\u2010induced neuronal loss in rats: increased brain damage with binge exposure","volume":"14","author":"Bonthius D.J.","year":"1990","journal-title":"Alcoholism: Clinical and Experimental Research"},{"issue":"2","key":"e_1_2_8_8_1","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1002\/tera.1420440203","article-title":"Permanent neuronal deficits in rats exposed to alcohol during the brain growth spurt","volume":"44","author":"Bonthius D.J.","year":"1991","journal-title":"Teratology"},{"issue":"4","key":"e_1_2_8_9_1","doi-asserted-by":"crossref","first-page":"614","DOI":"10.1016\/j.pbb.2008.05.004","article-title":"Fetal alcohol spectrum disorder\u2010associated depression: evidence for reductions in the levels of brain\u2010derived neurotrophic factor in a mouse model","volume":"90","author":"Caldwell K.K.","year":"2008","journal-title":"Pharmacology, Biochemistry, and Behavior"},{"issue":"1","key":"e_1_2_8_10_1","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1038\/5047","article-title":"Synergy of demethylation and histone deacetylase inhibition in the re\u2010expression of genes silenced in cancer","volume":"21","author":"Cameron E.E.","year":"1999","journal-title":"Nature Genetics"},{"issue":"6","key":"e_1_2_8_11_1","doi-asserted-by":"crossref","first-page":"795","DOI":"10.1111\/j.1365-2826.2008.01725.x","article-title":"Epigenetic programming of phenotypic variations in reproductive strategies in the rat through maternal care","volume":"20","author":"Cameron N.","year":"2008","journal-title":"Journal of Neuroendocrinology"},{"issue":"2","key":"e_1_2_8_12_1","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1016\/j.nbd.2009.05.001","article-title":"Dendritic spine pathologies in hippocampal pyramidal neurons from Rett syndrome brain and after expression of Rett\u2010associated MECP2 mutations","volume":"35","author":"Chapleau C.A.","year":"2009","journal-title":"Neurobiology of Disease"},{"issue":"5646","key":"e_1_2_8_13_1","doi-asserted-by":"crossref","first-page":"885","DOI":"10.1126\/science.1086446","article-title":"Depression of BDNF transcription involves calcium\u2010dependent phosphorylation of MeCP2","volume":"302","author":"Chen W.G.","year":"2003","journal-title":"Science"},{"issue":"2","key":"e_1_2_8_14_1","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1007\/s11065-011-9165-y","article-title":"Functional neuroimaging in the examination of effects of prenatal alcohol exposure","volume":"21","author":"Coles C.D.","year":"2011","journal-title":"Neuropsychological Review"},{"key":"e_1_2_8_15_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF01066065"},{"issue":"4","key":"e_1_2_8_16_1","doi-asserted-by":"crossref","first-page":"423","DOI":"10.1038\/nn.2514","article-title":"Dnmt1 and Dnmt3a maintain DNA methylation and regulate synaptic function in adult forebrain neurons","volume":"13","author":"Feng J.","year":"2010","journal-title":"Nature Neuroscience"},{"issue":"11","key":"e_1_2_8_17_1","doi-asserted-by":"crossref","first-page":"642","DOI":"10.1111\/j.1753-4887.2011.00417.x","article-title":"Effect of alcohol consumption in prenatal life, childhood, and adolescence on child development","volume":"69","author":"Foltran F.","year":"2011","journal-title":"Nutrition Reviews"},{"issue":"10","key":"e_1_2_8_18_1","doi-asserted-by":"crossref","first-page":"2536","DOI":"10.1093\/emboj\/20.10.2536","article-title":"Dnmt3a binds deacetylases and is recruited by a sequence\u2010specific repressor to silence transcription","volume":"20","author":"Fuks F.","year":"2001","journal-title":"EMBO Journal"},{"issue":"4","key":"e_1_2_8_19_1","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/gb-2001-2-4-reviews0003","article-title":"A tale of histone modifications","volume":"2","author":"Grant P.A.","year":"2001","journal-title":"Genome Biology"},{"key":"e_1_2_8_20_1","doi-asserted-by":"publisher","DOI":"10.1038\/nature07925"},{"issue":"4","key":"e_1_2_8_21_1","doi-asserted-by":"crossref","first-page":"703","DOI":"10.1016\/j.clp.2011.08.005","article-title":"Epigenetic effects of early developmental experiences","volume":"38","author":"Gudsnuk K.M.","year":"2011","journal-title":"Clinics in perinatology"},{"key":"e_1_2_8_22_1","doi-asserted-by":"publisher","DOI":"10.1016\/0014-4886(86)90203-7"},{"key":"e_1_2_8_23_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.brainres.2011.07.027"},{"issue":"10","key":"e_1_2_8_24_1","first-page":"732","article-title":"Binding of the Rett syndrome protein, MeCP2, to methylated and unmethylated DNA and chromatin","volume":"62","author":"Hansen J.C.","year":"2010","journal-title":"International Union of Biochemistry and Molecular Biology"},{"key":"e_1_2_8_25_1","doi-asserted-by":"publisher","DOI":"10.1095\/biolreprod.108.074682"},{"key":"e_1_2_8_26_1","doi-asserted-by":"publisher","DOI":"10.1095\/biolreprod.108.074690"},{"issue":"4","key":"e_1_2_8_27_1","doi-asserted-by":"crossref","first-page":"278","DOI":"10.1007\/s13238-012-2916-6","article-title":"Epigenetic control on cell fate choice in neural stem cells","volume":"3","author":"Hu X.\u2010L.","year":"2012","journal-title":"Protein Cell"},{"key":"e_1_2_8_28_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1471-4159.2010.06886.x"},{"issue":"2","key":"e_1_2_8_29_1","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1038\/561","article-title":"Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription","volume":"19","author":"Jones P.L.","year":"1998","journal-title":"Nature Genetics"},{"key":"e_1_2_8_30_1","doi-asserted-by":"publisher","DOI":"10.1007\/978-1-59745-242-7_8"},{"key":"e_1_2_8_31_1","doi-asserted-by":"publisher","DOI":"10.1002\/ddrr.69"},{"key":"e_1_2_8_32_1","doi-asserted-by":"publisher","DOI":"10.1002\/dvdy.21094"},{"issue":"12","key":"e_1_2_8_33_1","doi-asserted-by":"crossref","first-page":"1513","DOI":"10.1038\/nn2010","article-title":"Homeostatic regulation of MeCP2 expression by a CREB\u2010induced microRNA","volume":"10","author":"Klein M.E.","year":"2007","journal-title":"Nature Neuroscience"},{"issue":"12","key":"e_1_2_8_34_1","doi-asserted-by":"crossref","first-page":"2073","DOI":"10.1111\/j.1530-0277.2007.00528.x","article-title":"Persistent impairment of hippocampal neurogenesis in young adult rats following early postnatal alcohol exposure","volume":"31","author":"Klintsova A.Y.","year":"2007","journal-title":"Alcoholism: Clinical and Experimental Research"},{"key":"e_1_2_8_35_1","doi-asserted-by":"publisher","DOI":"10.3389\/fgene.2012.00010"},{"issue":"7","key":"e_1_2_8_36_1","doi-asserted-by":"crossref","first-page":"500","DOI":"10.4161\/epi.4.7.9925","article-title":"Alcohol exposure alters DNA methylation profiles in mouse embryos at early neurulation","volume":"4","author":"Liu Y.","year":"2009","journal-title":"Epigenetics"},{"key":"e_1_2_8_37_1","doi-asserted-by":"publisher","DOI":"10.1002\/dvdy.21626"},{"issue":"4","key":"e_1_2_8_38_1","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1002\/dev.10077","article-title":"Ultrasonic vocalizations and maternal\u2010infant interactions in a rat model of fetal alcohol syndrome","volume":"41","author":"Marino M.D.","year":"2002","journal-title":"Developmental Psychobiology"},{"issue":"3","key":"e_1_2_8_39_1","doi-asserted-by":"crossref","first-page":"284","DOI":"10.1002\/1098-1063(2000)10:3<284::AID-HIPO9>3.0.CO;2-K","article-title":"Neurons in the hilus region of the rat hippocampus are depleted in number by exposure to alcohol during early postnatal life","volume":"10","author":"Miki T.","year":"2000","journal-title":"Hippocampus"},{"issue":"1","key":"e_1_2_8_40_1","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1002\/neu.20009","article-title":"Ethanol exposure alters neurotrophin receptor expression in the rat central nervous system: Effects of prenatal exposure","volume":"60","author":"Moore D.B.","year":"2004","journal-title":"Journal of Neurobiology"},{"issue":"1","key":"e_1_2_8_41_1","doi-asserted-by":"crossref","first-page":"114","DOI":"10.1002\/neu.20010","article-title":"Ethanol exposure alters neurotrophin receptor expression in the rat central nervous system: effects of neonatal exposure","volume":"60","author":"Moore D.B.","year":"2004","journal-title":"Journal of Neurobiology"},{"issue":"10","key":"e_1_2_8_42_1","doi-asserted-by":"crossref","first-page":"1701","DOI":"10.1111\/j.1530-0277.2012.01784.x","article-title":"Choline supplementation and DNA methylation in the hippocampus and prefrontal cortex of rats exposed to alcohol during development","volume":"36","author":"Otero N.K.","year":"2012","journal-title":"Alcoholism: Clinical and Experimental Research"},{"key":"e_1_2_8_43_1","volume-title":"The Rat Brain: In Stereotaxic Coordinates","author":"Paxinos G.","year":"2005"},{"issue":"8","key":"e_1_2_8_44_1","doi-asserted-by":"crossref","first-page":"985","DOI":"10.1001\/archneurol.2011.149","article-title":"Rett syndrome: Exploring the autism link","volume":"68","author":"Percy A.K.","year":"2011","journal-title":"Archives in Neurology"},{"issue":"9","key":"e_1_2_8_45_1","doi-asserted-by":"crossref","first-page":"2002","DOI":"10.1093\/nar\/29.9.e45","article-title":"A new mathematical model for relative quantification in real\u2010time RT\u2010PCR","volume":"29","author":"Pfaffl M.W.","year":"2001","journal-title":"Nucleic Acids Research"},{"key":"e_1_2_8_46_1","doi-asserted-by":"publisher","DOI":"10.1007\/s11065-011-9166-x"},{"key":"e_1_2_8_47_1","doi-asserted-by":"publisher","DOI":"10.1038\/sj.onc.1205609"},{"key":"e_1_2_8_48_1","doi-asserted-by":"publisher","DOI":"10.1038\/nrg1655"},{"issue":"5","key":"e_1_2_8_49_1","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1002\/(SICI)1096-9926(199711)56:5<317::AID-TERA5>3.0.CO;2-U","article-title":"Incidence of fetal alcohol syndrome and prevalence of alcohol\u2010related neurodevelopmental disorder","volume":"56","author":"Sampson P.D.","year":"1997","journal-title":"Teratology"},{"key":"e_1_2_8_50_1","doi-asserted-by":"publisher","DOI":"10.1155\/2012\/179159"},{"issue":"10","key":"e_1_2_8_51_1","doi-asserted-by":"crossref","first-page":"1197","DOI":"10.3727\/096368909X12483162197204","article-title":"Cellular epigenetic modifications of neural stem cell differentiation","volume":"18","author":"Singh R.P.","year":"2009","journal-title":"Cell Transplantation"},{"key":"e_1_2_8_52_1","doi-asserted-by":"publisher","DOI":"10.1016\/0741-8329(88)90008-0"},{"issue":"1","key":"e_1_2_8_53_1","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1016\/j.reprotox.2007.05.001","article-title":"Maternal care, the epigenome, and phenotypic differences in behavior","volume":"24","author":"Szyf M.","year":"2007","journal-title":"Reproductive Toxicology"},{"key":"e_1_2_8_54_1","doi-asserted-by":"publisher","DOI":"10.1016\/0741-8329(90)90040-J"},{"key":"e_1_2_8_55_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0304-3940(00)01075-2"},{"issue":"5","key":"e_1_2_8_56_1","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1016\/S0892-0362(03)00074-6","article-title":"Critical periods for ethanol\u2010induced cell loss in the hippocampal formation","volume":"25","author":"Tran T.D.","year":"2003","journal-title":"Neurotoxicology & Teratology"},{"key":"e_1_2_8_57_1","doi-asserted-by":"publisher","DOI":"10.1038\/nrn2132"},{"key":"e_1_2_8_58_1","first-page":"631","article-title":"The role of mammalian DNA methyltransferases in the regulation of gene expression","volume":"10","author":"Turek\u2010Plewa J.","year":"2005","journal-title":"Cellular and Molecular Biology Letters"},{"issue":"3","key":"e_1_2_8_59_1","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1016\/0741-8329(84)90101-0","article-title":"Delay in brain growth induced by alcohol in artificially reared rat pups","volume":"1","author":"West J.R.","year":"1984","journal-title":"Alcohol"},{"key":"e_1_2_8_60_1","volume-title":"Alcohol & Brain Development","author":"West J.R.","year":"1990"},{"issue":"5","key":"e_1_2_8_61_1","doi-asserted-by":"crossref","first-page":"1488S","DOI":"10.3945\/ajcn.2009.27113B","article-title":"Epigenetic mechanisms for nutrition determinants of later health outcomes","volume":"89","author":"Zeisel S.H.","year":"2009","journal-title":"American Journal of Clinical Nutrition"},{"key":"e_1_2_8_62_1","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.psych.60.110707.163625"},{"issue":"4","key":"e_1_2_8_63_1","doi-asserted-by":"crossref","first-page":"735","DOI":"10.1111\/j.1530-0277.2010.01391.x","article-title":"Alcohol alters DNA methylation patterns and inhibits neural stem cell differentiation","volume":"35","author":"Zhou F.C.","year":"2011","journal-title":"Alcoholism: Clinical and Experimental Research"},{"key":"e_1_2_8_64_1","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2164-12-124"}],"container-title":["International Journal of Developmental Neuroscience"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0736574813000464?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0736574813000464?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.wiley.com\/onlinelibrary\/tdm\/v1\/articles\/10.1016%2Fj.ijdevneu.2013.03.010","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1016\/j.ijdevneu.2013.03.010","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/full-xml\/10.1016\/j.ijdevneu.2013.03.010","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1016\/j.ijdevneu.2013.03.010","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,9,6]],"date-time":"2023-09-06T15:18:51Z","timestamp":1694013531000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1016\/j.ijdevneu.2013.03.010"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2013,3,27]]},"references-count":63,"journal-issue":{"issue":"6","published-print":{"date-parts":[[2013,10]]}},"alternative-id":["10.1016\/j.ijdevneu.2013.03.010"],"URL":"https:\/\/doi.org\/10.1016\/j.ijdevneu.2013.03.010","archive":["Portico"],"relation":{},"ISSN":["0736-5748","1873-474X"],"issn-type":[{"value":"0736-5748","type":"print"},{"value":"1873-474X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2013,3,27]]},"assertion":[{"value":"2012-08-31","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2013-03-16","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2013-03-27","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}