Epigenome-wide association study of lung cancer among never smokers in two prospective cohorts in Shanghai, China

BackgroundThe aetiology of lung cancer among individuals who never smoked remains elusive, despite 15% of lung cancer cases in men and 53% in women worldwide being unrelated to smoking. Epigenetic alterations, particularly DNA methylation (DNAm) changes, have emerged as potential drivers. Yet, few p...

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Published in	Thorax Vol. 79; no. 8; pp. 735 - 744
Main Authors	Rahman, Mohammad L, Breeze, Charles E, Shu, Xiao-Ou, Wong, Jason Y Y, Blechter, Batel, Cardenas, Andres, Wang, Xuting, Ji, Bu-Tian, Hu, Wei, Cai, Qiuyin, Hosgood, H Dean, Yang, Gong, Shi, Jianxin, Long, Jirong, Gao, Yu-Tang, Bell, Douglas A, Zheng, Wei, Rothman, Nathaniel, Lan, Qing
Format	Journal Article
Language	English
Published	England BMJ Publishing Group Ltd and British Thoracic Society 01.08.2024 BMJ Publishing Group LTD
Subjects	Age Aged Aging Biomarkers Blood Body fluids Carcinogens Case-Control Studies China - epidemiology DNA Methylation Environmental aspects Epidemiology Epigenesis, Genetic Epigenetics Epigenome Female Genome-Wide Association Study Health risks Human exposure Humans Lung cancer Lung Neoplasms - genetics Male Medical diagnosis Medical prognosis Middle Aged non-small cell lung cancer Prospective Studies Sample size Signal transduction Smoking tobacco and the lung Womens health China Shanghai China United States > US lung cancer non-small cell lung cancer tobacco and the lung smoking
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ISSN	0040-6376 1468-3296 1468-3296
DOI	10.1136/thorax-2023-220352

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Abstract	BackgroundThe aetiology of lung cancer among individuals who never smoked remains elusive, despite 15% of lung cancer cases in men and 53% in women worldwide being unrelated to smoking. Epigenetic alterations, particularly DNA methylation (DNAm) changes, have emerged as potential drivers. Yet, few prospective epigenome-wide association studies (EWAS), primarily focusing on peripheral blood DNAm with limited representation of never smokers, have been conducted.MethodsWe conducted a nested case-control study of 80 never-smoking incident lung cancer cases and 83 never-smoking controls within the Shanghai Women’s Health Study and Shanghai Men’s Health Study. DNAm was measured in prediagnostic oral rinse samples using Illumina MethylationEPIC array. Initially, we conducted an EWAS to identify differentially methylated positions (DMPs) associated with lung cancer in the discovery sample of 101 subjects. The top 50 DMPs were further evaluated in a replication sample of 62 subjects, and results were pooled using fixed-effect meta-analysis.ResultsOur study identified three DMPs significantly associated with lung cancer at the epigenome-wide significance level of p<8.22×10−8. These DMPs were identified as cg09198866 (MYH9; TXN2), cg01411366 (SLC9A10) and cg12787323. Furthermore, examination of the top 1000 DMPs indicated significant enrichment in epithelial regulatory regions and their involvement in small GTPase-mediated signal transduction pathways. Additionally, GrimAge acceleration was identified as a risk factor for lung cancer (OR=1.19 per year; 95% CI 1.06 to 1.34).ConclusionsWhile replication in a larger sample size is necessary, our findings suggest that DNAm patterns in prediagnostic oral rinse samples could provide novel insights into the underlying mechanisms of lung cancer in never smokers.
AbstractList	BackgroundThe aetiology of lung cancer among individuals who never smoked remains elusive, despite 15% of lung cancer cases in men and 53% in women worldwide being unrelated to smoking. Epigenetic alterations, particularly DNA methylation (DNAm) changes, have emerged as potential drivers. Yet, few prospective epigenome-wide association studies (EWAS), primarily focusing on peripheral blood DNAm with limited representation of never smokers, have been conducted.MethodsWe conducted a nested case-control study of 80 never-smoking incident lung cancer cases and 83 never-smoking controls within the Shanghai Women’s Health Study and Shanghai Men’s Health Study. DNAm was measured in prediagnostic oral rinse samples using Illumina MethylationEPIC array. Initially, we conducted an EWAS to identify differentially methylated positions (DMPs) associated with lung cancer in the discovery sample of 101 subjects. The top 50 DMPs were further evaluated in a replication sample of 62 subjects, and results were pooled using fixed-effect meta-analysis.ResultsOur study identified three DMPs significantly associated with lung cancer at the epigenome-wide significance level of p<8.22×10−8. These DMPs were identified as cg09198866 (MYH9; TXN2), cg01411366 (SLC9A10) and cg12787323. Furthermore, examination of the top 1000 DMPs indicated significant enrichment in epithelial regulatory regions and their involvement in small GTPase-mediated signal transduction pathways. Additionally, GrimAge acceleration was identified as a risk factor for lung cancer (OR=1.19 per year; 95% CI 1.06 to 1.34).ConclusionsWhile replication in a larger sample size is necessary, our findings suggest that DNAm patterns in prediagnostic oral rinse samples could provide novel insights into the underlying mechanisms of lung cancer in never smokers. The aetiology of lung cancer among individuals who never smoked remains elusive, despite 15% of lung cancer cases in men and 53% in women worldwide being unrelated to smoking. Epigenetic alterations, particularly DNA methylation (DNAm) changes, have emerged as potential drivers. Yet, few prospective epigenome-wide association studies (EWAS), primarily focusing on peripheral blood DNAm with limited representation of never smokers, have been conducted. We conducted a nested case-control study of 80 never-smoking incident lung cancer cases and 83 never-smoking controls within the Shanghai Women's Health Study and Shanghai Men's Health Study. DNAm was measured in prediagnostic oral rinse samples using Illumina MethylationEPIC array. Initially, we conducted an EWAS to identify differentially methylated positions (DMPs) associated with lung cancer in the discovery sample of 101 subjects. The top 50 DMPs were further evaluated in a replication sample of 62 subjects, and results were pooled using fixed-effect meta-analysis. Our study identified three DMPs significantly associated with lung cancer at the epigenome-wide significance level of p<8.22×10 . These DMPs were identified as cg09198866 ( ; ), cg01411366 ( ) and cg12787323. Furthermore, examination of the top 1000 DMPs indicated significant enrichment in epithelial regulatory regions and their involvement in small GTPase-mediated signal transduction pathways. Additionally, GrimAge acceleration was identified as a risk factor for lung cancer (OR=1.19 per year; 95% CI 1.06 to 1.34). While replication in a larger sample size is necessary, our findings suggest that DNAm patterns in prediagnostic oral rinse samples could provide novel insights into the underlying mechanisms of lung cancer in never smokers. The aetiology of lung cancer among individuals who never smoked remains elusive, despite 15% of lung cancer cases in men and 53% in women worldwide being unrelated to smoking. Epigenetic alterations, particularly DNA methylation (DNAm) changes, have emerged as potential drivers. Yet, few prospective epigenome-wide association studies (EWAS), primarily focusing on peripheral blood DNAm with limited representation of never smokers, have been conducted.BACKGROUNDThe aetiology of lung cancer among individuals who never smoked remains elusive, despite 15% of lung cancer cases in men and 53% in women worldwide being unrelated to smoking. Epigenetic alterations, particularly DNA methylation (DNAm) changes, have emerged as potential drivers. Yet, few prospective epigenome-wide association studies (EWAS), primarily focusing on peripheral blood DNAm with limited representation of never smokers, have been conducted.We conducted a nested case-control study of 80 never-smoking incident lung cancer cases and 83 never-smoking controls within the Shanghai Women's Health Study and Shanghai Men's Health Study. DNAm was measured in prediagnostic oral rinse samples using Illumina MethylationEPIC array. Initially, we conducted an EWAS to identify differentially methylated positions (DMPs) associated with lung cancer in the discovery sample of 101 subjects. The top 50 DMPs were further evaluated in a replication sample of 62 subjects, and results were pooled using fixed-effect meta-analysis.METHODSWe conducted a nested case-control study of 80 never-smoking incident lung cancer cases and 83 never-smoking controls within the Shanghai Women's Health Study and Shanghai Men's Health Study. DNAm was measured in prediagnostic oral rinse samples using Illumina MethylationEPIC array. Initially, we conducted an EWAS to identify differentially methylated positions (DMPs) associated with lung cancer in the discovery sample of 101 subjects. The top 50 DMPs were further evaluated in a replication sample of 62 subjects, and results were pooled using fixed-effect meta-analysis.Our study identified three DMPs significantly associated with lung cancer at the epigenome-wide significance level of p<8.22×10-8. These DMPs were identified as cg09198866 (MYH9; TXN2), cg01411366 (SLC9A10) and cg12787323. Furthermore, examination of the top 1000 DMPs indicated significant enrichment in epithelial regulatory regions and their involvement in small GTPase-mediated signal transduction pathways. Additionally, GrimAge acceleration was identified as a risk factor for lung cancer (OR=1.19 per year; 95% CI 1.06 to 1.34).RESULTSOur study identified three DMPs significantly associated with lung cancer at the epigenome-wide significance level of p<8.22×10-8. These DMPs were identified as cg09198866 (MYH9; TXN2), cg01411366 (SLC9A10) and cg12787323. Furthermore, examination of the top 1000 DMPs indicated significant enrichment in epithelial regulatory regions and their involvement in small GTPase-mediated signal transduction pathways. Additionally, GrimAge acceleration was identified as a risk factor for lung cancer (OR=1.19 per year; 95% CI 1.06 to 1.34).While replication in a larger sample size is necessary, our findings suggest that DNAm patterns in prediagnostic oral rinse samples could provide novel insights into the underlying mechanisms of lung cancer in never smokers.CONCLUSIONSWhile replication in a larger sample size is necessary, our findings suggest that DNAm patterns in prediagnostic oral rinse samples could provide novel insights into the underlying mechanisms of lung cancer in never smokers.
Author	Breeze, Charles E Wong, Jason Y Y Yang, Gong Shi, Jianxin Wang, Xuting Hosgood, H Dean Ji, Bu-Tian Gao, Yu-Tang Lan, Qing Cai, Qiuyin Shu, Xiao-Ou Zheng, Wei Bell, Douglas A Hu, Wei Long, Jirong Cardenas, Andres Rothman, Nathaniel Rahman, Mohammad L Blechter, Batel
AuthorAffiliation	1 Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, USA 5 Albert Einstein College of Medicine, Bronx, New York, USA 6 Shanghai Cancer Institute, Shanghai, China 2 Division of Epidemiology, Department of Medicine, Vanderbilt University Medical Center and Vanderbilt-Ingram Cancer Center, Nashville, Tennessee, USA 4 Immunity, Inflammation and Disease Laboratory, National Institute of Environmental Health Sciences, National Institutes of Health, Research Triangle Park, NC 27709, USA 3 Department of Epidemiology and Population Health, Stanford University, Stanford, CA
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CitedBy_id	crossref_primary_10_1111_resp_14768 crossref_primary_10_4103_jpbs_jpbs_1214_24 crossref_primary_10_1136_thorax_2024_221393
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Keywords	lung cancer non-small cell lung cancer tobacco and the lung smoking
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Notes	Original research ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 This author is currently at the Epidemiology and Community Health Branch, National Heart Lung and Blood Institute. This work was conducted while formerly at the Division of Cancer Epidemiology and Genetics, National Cancer Institute. These authors co-supervised this work. Legends: MLR - Mohammad L. Rahman; CEB - Charles E. Breeze; XOU - Xiao-Ou Shu; JYYW - Jason Y.Y. Wong; BB - Batel Blechter; AC - Andres Cardenas; XW - Xuting Wang; BTJ - Bu-Tian Ji; WH - Wei Hu; QC - Qiuyin Cai; HDH - H. Dean Hosgood; GY - Gong Yang; JS - Jianxin Shi; JL - Jirong Long; YTG - Yu-Tang Gao; DAB - Douglas A. Bell; WZ - Wei Zheng; NR - Nathaniel Rothman; QL - Qing Lan These authors contributed equally Contributors: NR, QL, WZ and XOS designed the study and supervised data collection. MLR, CEB, JYYW, and DB prepared the analysis plan. MLR and CEB analyzed the data and drafted the manuscript. MLR, CEB, XOU, JYYW, BB, AC, XW, BTJ, WH, QC, HDH, GY, JS, JL, YTG, DAB, WZ, NR, QL contributed to the interpretation of the results and revision of the manuscript for important intellectual content and approved the final version of the manuscript. MLR and QL are the guarantors of this work and, as such, had full access to all the data in the study and take responsibility for the integrity of the data. The work reported in the paper has been performed by the authors, unless clearly specified in the text.
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Snippet	BackgroundThe aetiology of lung cancer among individuals who never smoked remains elusive, despite 15% of lung cancer cases in men and 53% in women worldwide... The aetiology of lung cancer among individuals who never smoked remains elusive, despite 15% of lung cancer cases in men and 53% in women worldwide being...
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SubjectTerms	Age Aged Aging Biomarkers Blood Body fluids Carcinogens Case-Control Studies China - epidemiology DNA Methylation Environmental aspects Epidemiology Epigenesis, Genetic Epigenetics Epigenome Female Genome-Wide Association Study Health risks Human exposure Humans Lung cancer Lung Neoplasms - genetics Male Medical diagnosis Medical prognosis Middle Aged non-small cell lung cancer Prospective Studies Sample size Signal transduction Smoking tobacco and the lung Womens health
Title	Epigenome-wide association study of lung cancer among never smokers in two prospective cohorts in Shanghai, China
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