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Newborn DNA-methylation, childhood lung function, and the risks of asthma and COPD across the life course

Herman T. den Dekker, Kimberley Burrows, Janine F. Felix, Lucas A. Salas, Ivana Nedeljkovic, Jin Yao, Sheryl L. Rifas-Shiman, Carlos Ruiz-Arenas, N. Amin, Mariona Bustamante, Dawn L. DeMeo, A. John Henderson, Caitlin G. Howe, Marie-France Hivert, M. Arfan Ikram, Johan C. de Jongste, Lies Lahousse, Pooja R. Mandaviya, Joyce B. van Meurs, Mariona Pinart, Gemma C. Sharp, Lisette Stolk, André G. Uitterlinden, Josep M. Anto, Augusto A. Litonjua, Carrie V. Breton, Guy G. Brusselle, Jordi Sunyer, George Davey Smith, Caroline L. Relton, Vincent W.V. Jaddoe, Liesbeth Duijts
European Respiratory Journal 2019; DOI: 10.1183/13993003.01795-2018
Herman T. den Dekker
1The Generation R Study Group, Erasmus MC, University Medical Center Rotterdam, Rotterdam, the Netherlands
2Department of Pediatrics, Division of Respiratory Medicine and Allergology, Erasmus MC, University Medical Center Rotterdam, Rotterdam, the Netherlands
3Department of Epidemiology, Erasmus MC, University Medical Center Rotterdam, Rotterdam, the Netherlands
*These authors contributed equally
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Kimberley Burrows
4MRC Integrative Epidemiology Unit, University of Bristol, UK School of Social and Community Medicine, University of Bristol, UK
*These authors contributed equally
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Janine F. Felix
1The Generation R Study Group, Erasmus MC, University Medical Center Rotterdam, Rotterdam, the Netherlands
3Department of Epidemiology, Erasmus MC, University Medical Center Rotterdam, Rotterdam, the Netherlands
5Department of Pediatrics, Erasmus MC, University Medical Center Rotterdam, Rotterdam, the Netherlands
*These authors contributed equally
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Lucas A. Salas
6ISGLobal, Centre for Research in Environmental Epidemiology (CREAL), Barcelona, Spain
7Department of Epidemiology, Geisel School of Medicine at Dartmouth, Lebanon, NH, USA
8Universitat Pompeu Fabra (UPF), Barcelona, Spain
9CIBER Epidemiología y Salud Pública (CIBERESP), Barcelona, Spain
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Ivana Nedeljkovic
3Department of Epidemiology, Erasmus MC, University Medical Center Rotterdam, Rotterdam, the Netherlands
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  • ORCID record for Ivana Nedeljkovic
Jin Yao
10Department of Preventive Medicine, University of Southern California, Los Angeles, CA
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Sheryl L. Rifas-Shiman
11Obesity Prevention Program, Department of Population Medicine, Harvard Medical School and Harvard Pilgrim Health Care Institute, Boston, MA , USA
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Carlos Ruiz-Arenas
6ISGLobal, Centre for Research in Environmental Epidemiology (CREAL), Barcelona, Spain
8Universitat Pompeu Fabra (UPF), Barcelona, Spain
9CIBER Epidemiología y Salud Pública (CIBERESP), Barcelona, Spain
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N. Amin
3Department of Epidemiology, Erasmus MC, University Medical Center Rotterdam, Rotterdam, the Netherlands
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Mariona Bustamante
6ISGLobal, Centre for Research in Environmental Epidemiology (CREAL), Barcelona, Spain
8Universitat Pompeu Fabra (UPF), Barcelona, Spain
9CIBER Epidemiología y Salud Pública (CIBERESP), Barcelona, Spain
12Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Barcelona, Spain
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Dawn L. DeMeo
13Channing Division of Network Medicine, Brigham and Women's Hospital, Boston, MA , USA
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A. John Henderson
4MRC Integrative Epidemiology Unit, University of Bristol, UK School of Social and Community Medicine, University of Bristol, UK
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Caitlin G. Howe
10Department of Preventive Medicine, University of Southern California, Los Angeles, CA
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Marie-France Hivert
11Obesity Prevention Program, Department of Population Medicine, Harvard Medical School and Harvard Pilgrim Health Care Institute, Boston, MA , USA
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M. Arfan Ikram
3Department of Epidemiology, Erasmus MC, University Medical Center Rotterdam, Rotterdam, the Netherlands
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Johan C. de Jongste
2Department of Pediatrics, Division of Respiratory Medicine and Allergology, Erasmus MC, University Medical Center Rotterdam, Rotterdam, the Netherlands
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Lies Lahousse
3Department of Epidemiology, Erasmus MC, University Medical Center Rotterdam, Rotterdam, the Netherlands
14Department of Respiratory Medicine, Ghent University Hospital, Ghent, Belgium
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  • ORCID record for Lies Lahousse
Pooja R. Mandaviya
15Department of Clinical Chemistry, Erasmus MC, University Medical Center Rotterdam, The Netherlands
16Department of Internal Medicine, Erasmus MC, University Medical Center Rotterdam, the Netherlands
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Joyce B. van Meurs
16Department of Internal Medicine, Erasmus MC, University Medical Center Rotterdam, the Netherlands
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Mariona Pinart
6ISGLobal, Centre for Research in Environmental Epidemiology (CREAL), Barcelona, Spain
8Universitat Pompeu Fabra (UPF), Barcelona, Spain
9CIBER Epidemiología y Salud Pública (CIBERESP), Barcelona, Spain
17IMIM (Hospital del Mar Medical Research Institute)
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Gemma C. Sharp
4MRC Integrative Epidemiology Unit, University of Bristol, UK School of Social and Community Medicine, University of Bristol, UK
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Lisette Stolk
16Department of Internal Medicine, Erasmus MC, University Medical Center Rotterdam, the Netherlands
18Netherlands Consortium for Healthy Ageing (NCHA), Erasmus MC, University Medical Center Rotterdam, The Netherlands
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André G. Uitterlinden
3Department of Epidemiology, Erasmus MC, University Medical Center Rotterdam, Rotterdam, the Netherlands
16Department of Internal Medicine, Erasmus MC, University Medical Center Rotterdam, the Netherlands
18Netherlands Consortium for Healthy Ageing (NCHA), Erasmus MC, University Medical Center Rotterdam, The Netherlands
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Josep M. Anto
6ISGLobal, Centre for Research in Environmental Epidemiology (CREAL), Barcelona, Spain
8Universitat Pompeu Fabra (UPF), Barcelona, Spain
9CIBER Epidemiología y Salud Pública (CIBERESP), Barcelona, Spain
17IMIM (Hospital del Mar Medical Research Institute)
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Augusto A. Litonjua
13Channing Division of Network Medicine, Brigham and Women's Hospital, Boston, MA , USA
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Carrie V. Breton
10Department of Preventive Medicine, University of Southern California, Los Angeles, CA
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Guy G. Brusselle
3Department of Epidemiology, Erasmus MC, University Medical Center Rotterdam, Rotterdam, the Netherlands
10Department of Preventive Medicine, University of Southern California, Los Angeles, CA
19Department of Respiratory Medicine, Erasmus MC, University Medical Center Rotterdam, Netherlands
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Jordi Sunyer
6ISGLobal, Centre for Research in Environmental Epidemiology (CREAL), Barcelona, Spain
8Universitat Pompeu Fabra (UPF), Barcelona, Spain
9CIBER Epidemiología y Salud Pública (CIBERESP), Barcelona, Spain
17IMIM (Hospital del Mar Medical Research Institute)
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George Davey Smith
4MRC Integrative Epidemiology Unit, University of Bristol, UK School of Social and Community Medicine, University of Bristol, UK
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Caroline L. Relton
4MRC Integrative Epidemiology Unit, University of Bristol, UK School of Social and Community Medicine, University of Bristol, UK
†These authors contributed equally
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Vincent W.V. Jaddoe
1The Generation R Study Group, Erasmus MC, University Medical Center Rotterdam, Rotterdam, the Netherlands
3Department of Epidemiology, Erasmus MC, University Medical Center Rotterdam, Rotterdam, the Netherlands
5Department of Pediatrics, Erasmus MC, University Medical Center Rotterdam, Rotterdam, the Netherlands
†These authors contributed equally
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Liesbeth Duijts
2Department of Pediatrics, Division of Respiratory Medicine and Allergology, Erasmus MC, University Medical Center Rotterdam, Rotterdam, the Netherlands
20Department of Pediatrics, Division of Neonatology, Erasmus MC, University Medical Center Rotterdam, Rotterdam, the Netherlands
†These authors contributed equally
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Abstract

Rationale We aimed to identify differentially methylated regions (DMRs) in cord blood DNA associated with childhood lung function, asthma and chronic obstructive pulmonary disease (COPD) across the life course.

Methods We meta-analyzed epigenome-wide data of 1688 children from five cohorts to identify cord blood DMRs and their annotated genes, in relation to Forced Expiratory Volume in 1 s (FEV1), FEV1/Forced Vital Capacity (FVC), and Forced Expiratory Flow at 75% of FVC (FEF75) at ages 7–13 years. Identified DMRs were explored for associations with childhood asthma, adult lung function and COPD, gene expression and involvement in biological processes.

Results We identified 59 DMRs associated with childhood lung function, of which 18 were associated with childhood asthma and 9 with COPD in adulthood. Genes annotated to the top ten identified DMRs were HOXA5, PAOX, LINC00602, ABCA7, PER3, CLCA1, VENTX, NUDT12, PTPRN2 and TCL1A. Differential gene expression in blood was observed for 32 DMRs in childhood and 18 in adulthood. Genes related with 16 identified DMRs were associated with respiratory developmental or pathogenic pathways.

Interpretation Our findings suggest that the epigenetic status of the newborn affects respiratory health and disease across the life course.

Footnotes

This manuscript has recently been accepted for publication in the European Respiratory Journal. It is published here in its accepted form prior to copyediting and typesetting by our production team. After these production processes are complete and the authors have approved the resulting proofs, the article will move to the latest issue of the ERJ online. Please open or download the PDF to view this article.

Conflict of interest: Dr. den Dekker has nothing to disclose.

Conflict of interest: Dr. Burrows has nothing to disclose.

Conflict of interest: Dr. Felix reports grants from European Union's Horizon 2020 research and innovation programme, during the conduct of the study.

Conflict of interest: Dr. Salas has nothing to disclose.

Conflict of interest: Dr. Nedeljkovic has nothing to disclose.

Conflict of interest: Dr. Yao has nothing to disclose.

Conflict of interest: Dr. Rifas-Shiman has nothing to disclose.

Conflict of interest: Dr. Amin has nothing to disclose.

Conflict of interest: Dr. Bustamante has nothing to disclose.

Conflict of interest: Dr. DeMeo reports grants from National Institutes of Health, and personal fees from Novartis for efforts outside the submitted work .

Conflict of interest: Dr. Howe has nothing to disclose.

Conflict of interest: Dr. Hivert has nothing to disclose.

Conflict of interest: Dr. de Jongste has nothing to disclose.

Conflict of interest: Dr. Lahousse has nothing to disclose.

Conflict of interest: Dr. Mandaviya has nothing to disclose.

Conflict of interest: Dr. van Meurs has nothing to disclose.

Conflict of interest: Dr. Pinart has nothing to disclose.

Conflict of interest: Dr. Sharp has nothing to disclose.

Conflict of interest: Dr. stolk has nothing to disclose.

Conflict of interest: Dr. Uitterlinden has nothing to disclose.

Conflict of interest: Dr. Antó has nothing to disclose.

Conflict of interest: Dr. Litonjua has nothing to disclose.

Conflict of interest: Dr. Breton has nothing to disclose.

Conflict of interest: Dr. Brusselle has nothing to disclose.

Conflict of interest: Dr. Sunyer has nothing to disclose.

Conflict of interest: Dr. Relton has nothing to disclose.

Conflict of interest: Dr. Jaddoe reports grants from European Union's Horizon 2020 research and innovation programme, during the conduct of the study.

Conflict of interest: Dr. Duijts reports grants from Lung Foundation, grants from Horizon 2020, personal fees from Abbvie, during the conduct of the study.

Conflict of interest: Dr. Ikram has nothing to disclose.

Conflict of interest: Dr. Ruiz Arenas has nothing to disclose.

Conflict of interest: Dr. Davey-Smith has nothing to disclose.

Conflict of interest: Dr. Henderson reports grants from Medical Research Council, grants from Wellcome, during the conduct of the study.

This is a PDF-only article. Please click on the PDF link above to read it.

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Newborn DNA-methylation, childhood lung function, and the risks of asthma and COPD across the life course
Herman T. den Dekker, Kimberley Burrows, Janine F. Felix, Lucas A. Salas, Ivana Nedeljkovic, Jin Yao, Sheryl L. Rifas-Shiman, Carlos Ruiz-Arenas, N. Amin, Mariona Bustamante, Dawn L. DeMeo, A. John Henderson, Caitlin G. Howe, Marie-France Hivert, M. Arfan Ikram, Johan C. de Jongste, Lies Lahousse, Pooja R. Mandaviya, Joyce B. van Meurs, Mariona Pinart, Gemma C. Sharp, Lisette Stolk, André G. Uitterlinden, Josep M. Anto, Augusto A. Litonjua, Carrie V. Breton, Guy G. Brusselle, Jordi Sunyer, George Davey Smith, Caroline L. Relton, Vincent W.V. Jaddoe, Liesbeth Duijts
European Respiratory Journal Jan 2019, 1801795; DOI: 10.1183/13993003.01795-2018

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Newborn DNA-methylation, childhood lung function, and the risks of asthma and COPD across the life course
Herman T. den Dekker, Kimberley Burrows, Janine F. Felix, Lucas A. Salas, Ivana Nedeljkovic, Jin Yao, Sheryl L. Rifas-Shiman, Carlos Ruiz-Arenas, N. Amin, Mariona Bustamante, Dawn L. DeMeo, A. John Henderson, Caitlin G. Howe, Marie-France Hivert, M. Arfan Ikram, Johan C. de Jongste, Lies Lahousse, Pooja R. Mandaviya, Joyce B. van Meurs, Mariona Pinart, Gemma C. Sharp, Lisette Stolk, André G. Uitterlinden, Josep M. Anto, Augusto A. Litonjua, Carrie V. Breton, Guy G. Brusselle, Jordi Sunyer, George Davey Smith, Caroline L. Relton, Vincent W.V. Jaddoe, Liesbeth Duijts
European Respiratory Journal Jan 2019, 1801795; DOI: 10.1183/13993003.01795-2018
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