{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,4]],"date-time":"2026-05-04T06:25:00Z","timestamp":1777875900941,"version":"3.51.4"},"reference-count":41,"publisher":"SAGE Publications","issue":"3","license":[{"start":{"date-parts":[[2023,3,1]],"date-time":"2023-03-01T00:00:00Z","timestamp":1677628800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/journals.sagepub.com\/page\/policies\/text-and-data-mining-license"}],"content-domain":{"domain":["journals.sagepub.com"],"crossmark-restriction":true},"short-container-title":["Thyroid\u00ae"],"published-print":{"date-parts":[[2023,3]]},"abstract":"<jats:sec>\n                    <jats:title>Background:<\/jats:title>\n                    <jats:p>Thyroid hormones play a key role in differentiation and metabolism and are known regulators of gene expression through both genomic and epigenetic processes including DNA methylation. The aim of this study was to examine associations between thyroid hormones and DNA methylation.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods:<\/jats:title>\n                    <jats:p>We carried out a fixed-effect meta-analysis of epigenome-wide association study (EWAS) of blood DNA methylation sites from 8 cohorts from the ThyroidOmics Consortium, incorporating up to 7073 participants of both European and African ancestry, implementing a discovery and replication stage. Statistical analyses were conducted using normalized beta CpG values as dependent and log-transformed thyrotropin (TSH), free thyroxine, and free triiodothyronine levels, respectively, as independent variable in a linear model. The replicated findings were correlated with gene expression levels in whole blood and tested for causal influence of TSH and free thyroxine by two-sample Mendelian randomization (MR).<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results:<\/jats:title>\n                    <jats:p>\n                      Epigenome-wide significant associations (\n                      <jats:italic toggle=\"yes\">p<\/jats:italic>\n                      -value &lt;1.1E-7) of three CpGs for free thyroxine, five for free triiodothyronine, and two for TSH concentrations were discovered and replicated (combined\n                      <jats:italic toggle=\"yes\">p<\/jats:italic>\n                      -values\u2009=\u20091.5E-9 to 4.3E-28). The associations included CpG sites annotated to\n                      <jats:italic toggle=\"yes\">KLF9<\/jats:italic>\n                      (cg00049440) and\n                      <jats:italic toggle=\"yes\">DOT1L<\/jats:italic>\n                      (cg04173586) that overlap with all three traits, consistent with hypothalamic\u2013pituitary\u2013thyroid axis physiology. Significant associations were also found for CpGs in\n                      <jats:italic toggle=\"yes\">FKBP5<\/jats:italic>\n                      for free thyroxine, and at\n                      <jats:italic toggle=\"yes\">CSNK1D\/LINCO1970<\/jats:italic>\n                      and\n                      <jats:italic toggle=\"yes\">LRRC8D<\/jats:italic>\n                      for free triiodothyronine. MR analyses supported a causal effect of thyroid status on DNA methylation of\n                      <jats:italic toggle=\"yes\">KLF9<\/jats:italic>\n                      . DNA methylation of cg00049440 in\n                      <jats:italic toggle=\"yes\">KLF9<\/jats:italic>\n                      was inversely correlated with\n                      <jats:italic toggle=\"yes\">KLF9<\/jats:italic>\n                      gene expression in blood. The CpG at\n                      <jats:italic toggle=\"yes\">CSNK1D\/LINC01970<\/jats:italic>\n                      overlapped with thyroid hormone receptor alpha binding peaks in liver cells. The total additive heritability of the methylation levels of the six significant CpG sites was between 25% and 57%. Significant methylation QTLs were identified for CpGs at\n                      <jats:italic toggle=\"yes\">KLF9<\/jats:italic>\n                      ,\n                      <jats:italic toggle=\"yes\">FKBP5<\/jats:italic>\n                      ,\n                      <jats:italic toggle=\"yes\">LRRC8D<\/jats:italic>\n                      , and\n                      <jats:italic toggle=\"yes\">CSNK1D\/LINC01970<\/jats:italic>\n                      .\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusions:<\/jats:title>\n                    <jats:p>\n                      We report novel associations between TSH, thyroid hormones, and blood-based DNA methylation. This study advances our understanding of thyroid hormone action particularly related to\n                      <jats:italic toggle=\"yes\">KLF9<\/jats:italic>\n                      and serves as a proof-of-concept that integrations of EWAS with other -omics data can provide a valuable tool for unraveling thyroid hormone signaling in humans by complementing and feeding classical\n                      <jats:italic toggle=\"yes\">in vitro<\/jats:italic>\n                      and animal studies.\n                    <\/jats:p>\n                  <\/jats:sec>","DOI":"10.1089\/thy.2022.0373","type":"journal-article","created":{"date-parts":[[2023,1,31]],"date-time":"2023-01-31T12:05:58Z","timestamp":1675166758000},"page":"301-311","update-policy":"https:\/\/doi.org\/10.1177\/sage-journals-update-policy","source":"Crossref","is-referenced-by-count":9,"title":["Epigenome-Wide Association Study Reveals CpG Sites Associated with Thyroid Function and Regulatory Effects on\n                    <i>KLF9<\/i>"],"prefix":"10.1177","volume":"33","author":[{"given":"Antoine","family":"Weihs","sequence":"first","affiliation":[{"name":"Department of Psychiatry and Psychotherapy, University Medicine Greifswald, Greifswald, Germany."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Layal","family":"Chaker","sequence":"additional","affiliation":[{"name":"Erasmus MC Academic Center for Thyroid Diseases, Department of Internal Medicine, Erasmus Medical Center, Rotterdam, The Netherlands."},{"name":"Erasmus MC Academic Center for Thyroid Diseases, Department of Epidemiology, Erasmus Medical Center, Rotterdam, The Netherlands."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Tiphaine C.","family":"Martin","sequence":"additional","affiliation":[{"name":"Department of Oncological Sciences, Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, New York, USA."},{"name":"Department of Twin Research and Genetic Epidemiology, St Thomas' Hospital Campus, King's College London, London, United Kingdom."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kim V.E.","family":"Braun","sequence":"additional","affiliation":[{"name":"Department of Epidemiology, Erasmus Medical Center, Rotterdam, The Netherlands."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Purdey J.","family":"Campbell","sequence":"additional","affiliation":[{"name":"Department of Endocrinology and Diabetes, Sir Charles Gairdner Hospital, Nedlands, Australia."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Simon R.","family":"Cox","sequence":"additional","affiliation":[{"name":"Lothian Birth Cohorts, Department of Psychology; Institute of Genetics and Cancer; University of Edinburgh, Edinburgh, United Kingdom."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Myriam","family":"Fornage","sequence":"additional","affiliation":[{"name":"Brown Foundation Institute of Molecular Medicine, McGovern Medical School, Houston, Texas, USA."},{"name":"Human Genetics Center, School of Public Health, The University of Texas Health Science Center at Houston, Houston, Texas, USA."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Christian","family":"Gieger","sequence":"additional","affiliation":[{"name":"Research Unit Molecular Epidemiology, Computational Health Center, Helmholtz Munich, Neuherberg, Germany."},{"name":"Institute of Epidemiology, Computational Health Center, Helmholtz Munich, Neuherberg, Germany."},{"name":"German Center for Cardiovascular Research (DZHK), Partner Site Munich Heart Alliance, Munich, Germany."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hans J.","family":"Grabe","sequence":"additional","affiliation":[{"name":"Department of Psychiatry and Psychotherapy, University Medicine Greifswald, Greifswald, Germany."},{"name":"German Centre for Neurodegenerative Diseases (DZNE), Site Rostock, Greifswald, Germany."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Harald","family":"Grallert","sequence":"additional","affiliation":[{"name":"Research Unit Molecular Epidemiology, Computational Health Center, Helmholtz Munich, Neuherberg, Germany."},{"name":"Institute of Epidemiology, Computational Health Center, Helmholtz Munich, Neuherberg, Germany."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sarah E.","family":"Harris","sequence":"additional","affiliation":[{"name":"Lothian Birth Cohorts, Department of Psychology; Institute of Genetics and Cancer; University of Edinburgh, Edinburgh, United Kingdom."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Brigitte","family":"K\u00fchnel","sequence":"additional","affiliation":[{"name":"Research Unit Molecular Epidemiology, Computational Health Center, Helmholtz Munich, Neuherberg, Germany."},{"name":"Institute of Epidemiology, Computational Health Center, Helmholtz Munich, Neuherberg, Germany."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Riccardo E.","family":"Marioni","sequence":"additional","affiliation":[{"name":"Centre for Genomic and Experimental Medicine, Institute of Genetics and Cancer; University of Edinburgh, Edinburgh, United Kingdom."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Nicholas G.","family":"Martin","sequence":"additional","affiliation":[{"name":"QIMR Berghofer Medical Research Institute, Brisbane, Australia."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Daniel L.","family":"McCartney","sequence":"additional","affiliation":[{"name":"Centre for Genomic and Experimental Medicine, Institute of Genetics and Cancer; University of Edinburgh, Edinburgh, United Kingdom."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Allan F.","family":"McRae","sequence":"additional","affiliation":[{"name":"Institute for Molecular Bioscience, The University of Queensland, St Lucia, Australia."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Christa","family":"Meisinger","sequence":"additional","affiliation":[{"name":"Epidemiology, Medical Faculty, University of Augsburg, Augsburg, Germany."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Joyce B.J.","family":"van Meurs","sequence":"additional","affiliation":[{"name":"Department of Internal Medicine, Erasmus Medical Center, Rotterdam, The Netherlands."},{"name":"Department of Orthopeadics and Sports Medicine, Erasmus Medical Center, Rotterdam, The Netherlands."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jana","family":"Nano","sequence":"additional","affiliation":[{"name":"Institute of Epidemiology, Computational Health Center, Helmholtz Munich, Neuherberg, Germany."},{"name":"Institute for Medical Informatics, Biometrics and Epidemiology, Ludwig-Maximilians-Universit\u00e4t (LMU) Munich, Munich, Germany."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Matthias","family":"Nauck","sequence":"additional","affiliation":[{"name":"Institute of Clinical Chemistry and Laboratory Medicine, University Medicine Greifswald, Greifswald, Germany."},{"name":"DZHK (German Centre for Cardiovascular Research), Partner Site Greifswald, Greifswald, Germany."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Annette","family":"Peters","sequence":"additional","affiliation":[{"name":"Research Unit Molecular Epidemiology, Computational Health Center, Helmholtz Munich, Neuherberg, Germany."},{"name":"Institute of Epidemiology, Computational Health Center, Helmholtz Munich, Neuherberg, Germany."},{"name":"German Center for Cardiovascular Research (DZHK), Partner Site Munich Heart Alliance, Munich, Germany."},{"name":"Institute for Medical Informatics, Biometrics and Epidemiology, Ludwig-Maximilians-Universit\u00e4t (LMU) Munich, Munich, Germany."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Holger","family":"Prokisch","sequence":"additional","affiliation":[{"name":"Institute of Neurogenomics, Computational Health Center; Helmholtz Munich, Neuherberg, Germany."},{"name":"Institute of Human Genetics, School of Medicine, Technical University Munich, Munich, Germany."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Michael","family":"Roden","sequence":"additional","affiliation":[{"name":"Institute for Clinical Diabetology, German Diabetes Center, Leibniz Center for Diabetes Research, Medical Faculty; Heinrich Heine University D\u00fcsseldorf, D\u00fcsseldorf, Germany."},{"name":"Division of Endocrinology and Diabetology, Medical Faculty; Heinrich Heine University D\u00fcsseldorf, D\u00fcsseldorf, Germany."},{"name":"German Center for Diabetes Research (DZD), Munich-Neuherberg, Germany."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Elizabeth","family":"Selvin","sequence":"additional","affiliation":[{"name":"Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, USA."},{"name":"Welch Center for Prevention, Epidemiology and Clinical Research, Johns Hopkins School of Medicine, Baltimore, Maryland, USA."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Marian","family":"Beekman","sequence":"additional","affiliation":[{"name":"Section of Molecular Epidemiology, Department of Biomedical Data Sciences, Department of Internal Medicine, Leiden University Medical Center, Leiden, Netherlands."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Diana","family":"van Heemst","sequence":"additional","affiliation":[{"name":"Section of Gerontology and Geriatrics, Department of Internal Medicine; Leiden University Medical Center, Leiden, Netherlands."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Eline P.","family":"Slagboom","sequence":"additional","affiliation":[{"name":"Section of Molecular Epidemiology, Department of Biomedical Data Sciences, Department of Internal Medicine, Leiden University Medical Center, Leiden, Netherlands."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4176-8273","authenticated-orcid":false,"given":"Brenton R.","family":"Swenson","sequence":"additional","affiliation":[{"name":"Cardiovascular Health Research Unit, University of Washington, Seattle, Washington, USA."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Adrienne","family":"Tin","sequence":"additional","affiliation":[{"name":"Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, USA."},{"name":"Department of Medicine, University of Mississippi Medical Center, Jackson, Mississippi, USA."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Pei-Chien","family":"Tsai","sequence":"additional","affiliation":[{"name":"Department of Twin Research and Genetic Epidemiology, St Thomas' Hospital Campus, King's College London, London, United Kingdom."},{"name":"Department of Biomedical Sciences, Chang Gung University, Taoyuan, Taiwan."},{"name":"Division of Pediatric Infectious Diseases, Department of Pediatrics, Chang Gung Memorial Hospital, Taoyuan City, Taiwan."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Andre","family":"Uitterlinden","sequence":"additional","affiliation":[{"name":"Department of Internal Medicine, Erasmus Medical Center, Rotterdam, The Netherlands."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"W. Edward","family":"Visser","sequence":"additional","affiliation":[{"name":"Erasmus MC Academic Center for Thyroid Diseases, Department of Internal Medicine, Erasmus Medical Center, Rotterdam, The Netherlands."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Henry","family":"V\u00f6lzke","sequence":"additional","affiliation":[{"name":"DZHK (German Centre for Cardiovascular Research), Partner Site Greifswald, Greifswald, Germany."},{"name":"Institute for Community Medicine; University Medicine Greifswald, Greifswald, Germany."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Melanie","family":"Waldenberger","sequence":"additional","affiliation":[{"name":"Research Unit Molecular Epidemiology, Computational Health Center, Helmholtz Munich, Neuherberg, Germany."},{"name":"Institute of Epidemiology, Computational Health Center, Helmholtz Munich, Neuherberg, Germany."},{"name":"German Center for Cardiovascular Research (DZHK), Partner Site Munich Heart Alliance, Munich, Germany."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"John P.","family":"Walsh","sequence":"additional","affiliation":[{"name":"Department of Endocrinology and Diabetes, Sir Charles Gairdner Hospital, Nedlands, Australia."},{"name":"Medical School, University of Western Australia, Crawley, Australia."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Anna","family":"K\u00f6ttgen","sequence":"additional","affiliation":[{"name":"Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, USA."},{"name":"Institute of Genetic Epidemiology, Faculty of Medicine and Medical Center\u2014University of Freiburg, Freiburg, Germany."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Scott G.","family":"Wilson","sequence":"additional","affiliation":[{"name":"Department of Twin Research and Genetic Epidemiology, St Thomas' Hospital Campus, King's College London, London, United Kingdom."},{"name":"Department of Endocrinology and Diabetes, Sir Charles Gairdner Hospital, Nedlands, Australia."},{"name":"School of Biomedical Sciences, University of Western Australia, Perth, Australia."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Robin P.","family":"Peeters","sequence":"additional","affiliation":[{"name":"Erasmus MC Academic Center for Thyroid Diseases, Department of Internal Medicine, Erasmus Medical Center, Rotterdam, The Netherlands."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jordana T.","family":"Bell","sequence":"additional","affiliation":[{"name":"Department of Twin Research and Genetic Epidemiology, St Thomas' Hospital Campus, King's College London, London, United Kingdom."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Marco","family":"Medici","sequence":"additional","affiliation":[{"name":"Erasmus MC Academic Center for Thyroid Diseases, Department of Internal Medicine, Erasmus Medical Center, Rotterdam, The Netherlands."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8309-094X","authenticated-orcid":false,"given":"Alexander","family":"Teumer","sequence":"additional","affiliation":[{"name":"Department of Psychiatry and Psychotherapy, University Medicine Greifswald, Greifswald, Germany."},{"name":"DZHK (German Centre for Cardiovascular Research), Partner Site Greifswald, Greifswald, Germany."},{"name":"Institute for Community Medicine; University Medicine Greifswald, Greifswald, Germany."},{"name":"Department of Population Medicine and Lifestyle Diseases Prevention, Medical University of Bialystok, Bialystok, Poland."}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"179","published-online":{"date-parts":[[2023,3,16]]},"reference":[{"key":"e_1_3_5_2_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0140-6736(11)60276-6"},{"key":"e_1_3_5_3_2","unstructured":"Wondisford Fredric E ; Radovick S (eds). 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