{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,7]],"date-time":"2026-10-07T01:54:56Z","timestamp":1791338096329,"version":"4.3.1"},"reference-count":78,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2022,11,7]],"date-time":"2022-11-07T00:00:00Z","timestamp":1667779200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000025","name":"National Institute of Mental Health","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000025","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Neurosci."],"abstract":"<jats:p>Genetic mutations identified in genome-wide association studies can only explain a small percentage of the cases of complex, highly heritable human conditions, including neurological and neurodevelopmental disorders. This suggests that intergenerational epigenetic effects, possibly triggered by environmental circumstances, may contribute to their etiology. We previously described altered DNA methylation signatures in the sperm of mice that experienced developmental overexposure to thyroid hormones as a result of a genetic defect in hormone clearance (DIO3 deficiency). Here we studied fetal brain gene expression and adult social behavior in genetically normal F2 generation descendants of overexposed mice. The brain of F2 generation E13.5 fetuses exhibited abnormal expression of genes associated with autism in humans, including <jats:italic>Auts2, Disc1, Ldlr<\/jats:italic>, <jats:italic>Per2<\/jats:italic>, <jats:italic>Shank3<\/jats:italic>, <jats:italic>Oxtr<\/jats:italic>, <jats:italic>Igf1<\/jats:italic>, <jats:italic>Foxg1<\/jats:italic>, <jats:italic>Cd38<\/jats:italic>, <jats:italic>Grid2<\/jats:italic>, <jats:italic>Nrxn3<\/jats:italic>, and <jats:italic>Reln<\/jats:italic>. These abnormal gene expression profiles differed depending on the sex of the exposed ancestor. In the three-chamber social box test, adult F2 generation males manifested significantly decreased interest in social interaction and social novelty, as revealed by decrease total time, distance traveled and time immobile in the area of interaction with novel strangers. F1 generation mice, compared to appropriate controls also exhibited altered profiles in fetal brain gene expression, although these profiles were substantially different to those in the F2 generation. Likewise adult F1 generation mice showed some abnormalities in social behavior that were sexually dimorphic and milder than those in F2 generation mice. Our results indicate that developmental overexposure to thyroid hormone causes intergenerational epigenetic effects impacting social behavior and the expression of autism-related genes during early brain development. Our results open the possibility that altered thyroid hormone states, by eliciting changes in the epigenetic information of the germ line, contribute to the susceptibility and the missing\u2014but heriTables\u2014etiology of complex neurodevelopmental conditions characterized by social deficits, including autism and schizophrenia.<\/jats:p>","DOI":"10.3389\/fnins.2022.1055116","type":"journal-article","created":{"date-parts":[[2022,11,7]],"date-time":"2022-11-07T06:51:03Z","timestamp":1667803863000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":12,"title":["Thyroid hormone elicits intergenerational epigenetic effects on adult social behavior and fetal brain expression of autism susceptibility genes"],"prefix":"10.3389","volume":"16","author":[{"given":"Maria Elena","family":"Martinez","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Julia Patrizia","family":"Stohn","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elizabeth M.","family":"Mutina","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rayne J.","family":"Whitten","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Arturo","family":"Hernandez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2022,11,7]]},"reference":[{"key":"B1","doi-asserted-by":"crossref","first-page":"1365","DOI":"10.1111\/1471-0528.12681","article-title":"Attention deficit hyperactivity disorder and autism spectrum disorder in children born to mothers with thyroid dysfunction: A Danish nationwide cohort study.","volume":"121","author":"Andersen","year":"2014","journal-title":"BJOG"},{"key":"B2","doi-asserted-by":"crossref","first-page":"691","DOI":"10.1001\/jama.292.6.691","article-title":"Fetal loss associated with excess thyroid hormone exposure.","volume":"292","author":"Anselmo","year":"2004","journal-title":"JAMA"},{"key":"B3","doi-asserted-by":"crossref","first-page":"778","DOI":"10.1089\/thy.2019.0080","article-title":"Reduced sensitivity to thyroid hormone as a transgenerational epigenetic marker transmitted along the human male line.","volume":"29","author":"Anselmo","year":"2019","journal-title":"Thyroid"},{"key":"B4","doi-asserted-by":"crossref","first-page":"1466","DOI":"10.1126\/science.1108190","article-title":"Epigenetic transgenerational actions of endocrine disruptors and male fertility.","volume":"308","author":"Anway","year":"2006","journal-title":"Science"},{"key":"B5","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1159\/000240946","article-title":"Endocrine studies in the untreated F1 and F2 progeny of rats treated neonatally with thyroxine Biol.","volume":"31","author":"Bakke","year":"1977","journal-title":"Neonate"},{"key":"B6","doi-asserted-by":"publisher","first-page":"437","DOI":"10.1016\/0026-0495(76)90076-7","article-title":"Observations on the untreated progeny of hypothyroid male rats.","volume":"25","author":"Bakke","year":"1976","journal-title":"Metabolism"},{"key":"B7","doi-asserted-by":"crossref","first-page":"819","DOI":"10.1126\/science.1115455","article-title":"Sex differences in the brain: Implications for explaining autism.","volume":"310","author":"Baron-Cohen","year":"2005","journal-title":"Science"},{"key":"B8","doi-asserted-by":"publisher","first-page":"788","DOI":"10.1093\/schbul\/sbw146","article-title":"Heritability of neuropsychological measures in schizophrenia and nonpsychiatric populations: A systematic review and meta-analysis.","volume":"43","author":"Blokland","year":"2017","journal-title":"Schizophr. 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