Tobacco Smoking Leads to Extensive Genome-Wide Changes in DNA Methylation

Environmental factors such as tobacco smoking may have long-lasting effects on DNA methylation patterns, which might lead to changes in gene expression and in a broader context to the development or progression of various diseases. We conducted an epigenome-wide association study (EWAs) comparing cu...

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Veröffentlicht in:	PloS one Jg. 8; H. 5; S. e63812
Hauptverfasser:	Zeilinger, Sonja, Kühnel, Brigitte, Klopp, Norman, Baurecht, Hansjörg, Kleinschmidt, Anja, Gieger, Christian, Weidinger, Stephan, Lattka, Eva, Adamski, Jerzy, Peters, Annette, Strauch, Konstantin, Waldenberger, Melanie, Illig, Thomas
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	United States Public Library of Science 17.05.2013 Public Library of Science (PLoS)
Schlagworte:	Adult Aged Alkaline Phosphatase - genetics Analysis of Variance Basic Helix-Loop-Helix Transcription Factors - genetics Bioinformatics Biology Cancer Cardiovascular disease Change detection CpG Islands - genetics Deoxyribonucleic acid Dermatology Development and progression DNA DNA methylation DNA Methylation - drug effects Electrophoretic Mobility Shift Assay Environmental changes Environmental factors Environmental health Epidemiology Epigenetics Epigenomics - methods Female Gene expression Gene Expression Regulation - drug effects Gene Expression Regulation - genetics Genes Genetic research Genetics Genome, Human - drug effects Genome, Human - genetics Genomes Genomics GPI-Linked Proteins - genetics Humans Isoenzymes - genetics Linear Models Male Medical research Medicine Methylation Middle Aged Oligonucleotide Array Sequence Analysis Phosphatase Population Protein binding Receptors, Thrombin - genetics Repressor Proteins - genetics Sex Factors Smokers Smoking Smoking - adverse effects Smoking Cessation - statistics & numerical data Studies Time Factors Tobacco Tobacco smoking Germany
ISSN:	1932-6203, 1932-6203
Online-Zugang:	Volltext
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Abstract	Environmental factors such as tobacco smoking may have long-lasting effects on DNA methylation patterns, which might lead to changes in gene expression and in a broader context to the development or progression of various diseases. We conducted an epigenome-wide association study (EWAs) comparing current, former and never smokers from 1793 participants of the population-based KORA F4 panel, with replication in 479 participants from the KORA F3 panel, carried out by the 450K BeadChip with genomic DNA obtained from whole blood. We observed wide-spread differences in the degree of site-specific methylation (with p-values ranging from 9.31E-08 to 2.54E-182) as a function of tobacco smoking in each of the 22 autosomes, with the percent of variance explained by smoking ranging from 1.31 to 41.02. Depending on cessation time and pack-years, methylation levels in former smokers were found to be close to the ones seen in never smokers. In addition, methylation-specific protein binding patterns were observed for cg05575921 within AHRR, which had the highest level of detectable changes in DNA methylation associated with tobacco smoking (-24.40% methylation; p = 2.54E-182), suggesting a regulatory role for gene expression. The results of our study confirm the broad effect of tobacco smoking on the human organism, but also show that quitting tobacco smoking presumably allows regaining the DNA methylation state of never smokers.
AbstractList	Environmental factors such as tobacco smoking may have long-lasting effects on DNA methylation patterns, which might lead to changes in gene expression and in a broader context to the development or progression of various diseases. We conducted an epigenome-wide association study (EWAs) comparing current, former and never smokers from 1793 participants of the population-based KORA F4 panel, with replication in 479 participants from the KORA F3 panel, carried out by the 450K BeadChip with genomic DNA obtained from whole blood. We observed wide-spread differences in the degree of site-specific methylation (with p-values ranging from 9.31E-08 to 2.54E-182) as a function of tobacco smoking in each of the 22 autosomes, with the percent of variance explained by smoking ranging from 1.31 to 41.02. Depending on cessation time and pack-years, methylation levels in former smokers were found to be close to the ones seen in never smokers. In addition, methylation-specific protein binding patterns were observed for cg05575921 within AHRR, which had the highest level of detectable changes in DNA methylation associated with tobacco smoking (–24.40% methylation; p = 2.54E-182), suggesting a regulatory role for gene expression. The results of our study confirm the broad effect of tobacco smoking on the human organism, but also show that quitting tobacco smoking presumably allows regaining the DNA methylation state of never smokers. Environmental factors such as tobacco smoking may have long-lasting effects on DNA methylation patterns, which might lead to changes in gene expression and in a broader context to the development or progression of various diseases. We conducted an epigenome-wide association study (EWAs) comparing current, former and never smokers from 1793 participants of the population-based KORA F4 panel, with replication in 479 participants from the KORA F3 panel, carried out by the 450K BeadChip with genomic DNA obtained from whole blood. We observed wide-spread differences in the degree of site-specific methylation (with p-values ranging from 9.31E-08 to 2.54E-182) as a function of tobacco smoking in each of the 22 autosomes, with the percent of variance explained by smoking ranging from 1.31 to 41.02. Depending on cessation time and pack-years, methylation levels in former smokers were found to be close to the ones seen in never smokers. In addition, methylation-specific protein binding patterns were observed for cg05575921 within AHRR, which had the highest level of detectable changes in DNA methylation associated with tobacco smoking (-24.40% methylation; p = 2.54E-182), suggesting a regulatory role for gene expression. The results of our study confirm the broad effect of tobacco smoking on the human organism, but also show that quitting tobacco smoking presumably allows regaining the DNA methylation state of never smokers.Environmental factors such as tobacco smoking may have long-lasting effects on DNA methylation patterns, which might lead to changes in gene expression and in a broader context to the development or progression of various diseases. We conducted an epigenome-wide association study (EWAs) comparing current, former and never smokers from 1793 participants of the population-based KORA F4 panel, with replication in 479 participants from the KORA F3 panel, carried out by the 450K BeadChip with genomic DNA obtained from whole blood. We observed wide-spread differences in the degree of site-specific methylation (with p-values ranging from 9.31E-08 to 2.54E-182) as a function of tobacco smoking in each of the 22 autosomes, with the percent of variance explained by smoking ranging from 1.31 to 41.02. Depending on cessation time and pack-years, methylation levels in former smokers were found to be close to the ones seen in never smokers. In addition, methylation-specific protein binding patterns were observed for cg05575921 within AHRR, which had the highest level of detectable changes in DNA methylation associated with tobacco smoking (-24.40% methylation; p = 2.54E-182), suggesting a regulatory role for gene expression. The results of our study confirm the broad effect of tobacco smoking on the human organism, but also show that quitting tobacco smoking presumably allows regaining the DNA methylation state of never smokers.
Audience	Academic
Author	Kühnel, Brigitte Waldenberger, Melanie Zeilinger, Sonja Peters, Annette Illig, Thomas Lattka, Eva Adamski, Jerzy Baurecht, Hansjörg Klopp, Norman Strauch, Konstantin Gieger, Christian Weidinger, Stephan Kleinschmidt, Anja
AuthorAffiliation	7 Chair of Experimental Genetics, Technische Universität München, Munich, Germany 8 Institute of Epidemiology II, Helmholtz Zentrum München, German Research Center for Environmental Health, Neuherberg, Germany 1 Research Unit of Molecular Epidemiology, Helmholtz Zentrum München, German Research Center for Environmental Health, Neuherberg, Germany 2 Institute of Genetic Epidemiology, Helmholtz Zentrum München, German Research Center for Environmental Health, Neuherberg, Germany 9 Institute of Medical Informatics, Biometry and Epidemiology, Chair of Genetic Epidemiology, Ludwig-Maximilians-Universität, Munich, Germany 6 Institute of Experimental Genetics, Genome Analysis Center, Helmholtz Zentrum München, Neuherberg, Germany University of Cincinnati, United States of America 3 Hannover Unified Biobank, Hannover Medical School, Hannover, Germany 5 Graduate School of Information Science in Health (GSISH), Technische Universität München, Munich, Germany 4 Department of Dermatology, Allergology, and
AuthorAffiliation_xml	– name: 8 Institute of Epidemiology II, Helmholtz Zentrum München, German Research Center for Environmental Health, Neuherberg, Germany – name: 1 Research Unit of Molecular Epidemiology, Helmholtz Zentrum München, German Research Center for Environmental Health, Neuherberg, Germany – name: 5 Graduate School of Information Science in Health (GSISH), Technische Universität München, Munich, Germany – name: University of Cincinnati, United States of America – name: 3 Hannover Unified Biobank, Hannover Medical School, Hannover, Germany – name: 9 Institute of Medical Informatics, Biometry and Epidemiology, Chair of Genetic Epidemiology, Ludwig-Maximilians-Universität, Munich, Germany – name: 2 Institute of Genetic Epidemiology, Helmholtz Zentrum München, German Research Center for Environmental Health, Neuherberg, Germany – name: 4 Department of Dermatology, Allergology, and Venerology, University Hospital Schleswig-Holstein, Campus Kiel, Kiel, Germany – name: 6 Institute of Experimental Genetics, Genome Analysis Center, Helmholtz Zentrum München, Neuherberg, Germany – name: 7 Chair of Experimental Genetics, Technische Universität München, Munich, Germany
Author_xml	– sequence: 1 givenname: Sonja surname: Zeilinger fullname: Zeilinger, Sonja – sequence: 2 givenname: Brigitte surname: Kühnel fullname: Kühnel, Brigitte – sequence: 3 givenname: Norman surname: Klopp fullname: Klopp, Norman – sequence: 4 givenname: Hansjörg surname: Baurecht fullname: Baurecht, Hansjörg – sequence: 5 givenname: Anja surname: Kleinschmidt fullname: Kleinschmidt, Anja – sequence: 6 givenname: Christian surname: Gieger fullname: Gieger, Christian – sequence: 7 givenname: Stephan surname: Weidinger fullname: Weidinger, Stephan – sequence: 8 givenname: Eva surname: Lattka fullname: Lattka, Eva – sequence: 9 givenname: Jerzy surname: Adamski fullname: Adamski, Jerzy – sequence: 10 givenname: Annette surname: Peters fullname: Peters, Annette – sequence: 11 givenname: Konstantin surname: Strauch fullname: Strauch, Konstantin – sequence: 12 givenname: Melanie surname: Waldenberger fullname: Waldenberger, Melanie – sequence: 13 givenname: Thomas surname: Illig fullname: Illig, Thomas
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/23691101$$D View this record in MEDLINE/PubMed
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Copyright	COPYRIGHT 2013 Public Library of Science 2013 Zeilinger et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2013 Zeilinger et al 2013 Zeilinger et al
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Competing Interests: The authors have declared that no competing interests exist. Conceived and designed the experiments: SZ NK TI KS MW. Performed the experiments: SZ. Analyzed the data: SZ BK HB KS CG. Contributed reagents/materials/analysis tools: AP JA. Wrote the paper: SZ MW NK EL KS TI. Pre-processed the Illumina 450K data: SZ HB. Designed and performed EMSA experiments: AK EL. Critically reviewed the paper: AP SW JA. Discussed the results and implications and commented on the manuscript at all stages: MW SZ BK NK HB AK CG SW EL JA AP KS TI.
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Snippet	Environmental factors such as tobacco smoking may have long-lasting effects on DNA methylation patterns, which might lead to changes in gene expression and in...
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SubjectTerms	Adult Aged Alkaline Phosphatase - genetics Analysis of Variance Basic Helix-Loop-Helix Transcription Factors - genetics Bioinformatics Biology Cancer Cardiovascular disease Change detection CpG Islands - genetics Deoxyribonucleic acid Dermatology Development and progression DNA DNA methylation DNA Methylation - drug effects Electrophoretic Mobility Shift Assay Environmental changes Environmental factors Environmental health Epidemiology Epigenetics Epigenomics - methods Female Gene expression Gene Expression Regulation - drug effects Gene Expression Regulation - genetics Genes Genetic research Genetics Genome, Human - drug effects Genome, Human - genetics Genomes Genomics GPI-Linked Proteins - genetics Humans Isoenzymes - genetics Linear Models Male Medical research Medicine Methylation Middle Aged Oligonucleotide Array Sequence Analysis Phosphatase Population Protein binding Receptors, Thrombin - genetics Repressor Proteins - genetics Sex Factors Smokers Smoking Smoking - adverse effects Smoking Cessation - statistics & numerical data Studies Time Factors Tobacco Tobacco smoking
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Title	Tobacco Smoking Leads to Extensive Genome-Wide Changes in DNA Methylation
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Volume	8
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