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Fathers’ preconception smoking and offspring DNA methylation

Fathers’ preconception smoking and offspring DNA methylation
Fathers’ preconception smoking and offspring DNA methylation
Background: experimental studies suggest that exposures may impact respiratory health across generations via epigenetic changes transmitted specifically through male germ cells. Studies in humans are, however, limited. We aim to identify epigenetic marks in offspring associated with father’s preconception smoking.

Methods: we conducted epigenome-wide association studies (EWAS) in the RHINESSA cohort (7–50 years) on father’s any preconception smoking (n = 875 offspring) and father’s pubertal onset smoking < 15 years (n = 304), using Infinium MethylationEPIC Beadchip arrays, adjusting for offspring age, own smoking and maternal smoking. EWAS of maternal and offspring personal smoking were performed for comparison. Father’s smoking-associated dmCpGs were checked in subpopulations of offspring who reported no personal smoking and no maternal smoking exposure.

Results: father’s smoking commencing preconception was associated with methylation of blood DNA in offspring at two cytosine-phosphate-guanine sites (CpGs) (false discovery rate (FDR) < 0.05) in PRR5 and CENPP. Father’s pubertal onset smoking was associated with 19 CpGs (FDR < 0.05) mapped to 14 genes (TLR9, DNTT, FAM53B, NCAPG2, PSTPIP2, MBIP, C2orf39, NTRK2, DNAJC14, CDO1, PRAP1, TPCN1, IRS1 and CSF1R). These differentially methylated sites were hypermethylated and associated with promoter regions capable of gene silencing. Some of these sites were associated with offspring outcomes in this cohort including ever-asthma (NTRK2), ever-wheezing (DNAJC14, TPCN1), weight (FAM53B, NTRK2) and BMI (FAM53B, NTRK2) (p < 0.05). Pathway analysis showed enrichment for gene ontology pathways including regulation of gene expression, inflammation and innate immune responses. Father’s smoking-associated sites did not overlap with dmCpGs identified in EWAS of personal and maternal smoking (FDR < 0.05), and all sites remained significant (p < 0.05) in analyses of offspring with no personal smoking and no maternal smoking exposure.

Conclusion: father’s preconception smoking, particularly in puberty, is associated with offspring DNA methylation, providing evidence that epigenetic mechanisms may underlie epidemiological observations that pubertal paternal smoking increases risk of offspring asthma, low lung function and obesity.
Asthma, Chromosomal Proteins, Non-Histone, Cytosine, DNA Methylation, Epigenesis, Genetic, Guanine, Humans, Male, Smoking/adverse effects, Tobacco Smoking
1868-7075
131
Kitaba, Negusse Tadesse
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Knudsen, Gerd Toril Mørkve
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Johannessen, Ane
aa3ea773-3c29-45bf-a81f-d6cba2444542
Rezwan, Faisal I.
203f8f38-1f5d-485b-ab11-c546b4276338
Malinovschi, Andrei
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Oudin, Anna
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Benediktsdottir, Bryndis
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Martino, David
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González, Francisco Javier Callejas
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Gómez, Leopoldo Palacios
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Holm, Mathias
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Jõgi, Nils Oskar
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Dharmage, Shyamali C.
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Skulstad, Svein Magne
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Watkins, Sarah H.
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Suderman, Matthew
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Gómez-real, Francisco
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Schlünssen, Vivi
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Svanes, Cecilie
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Holloway, John W.
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Kitaba, Negusse Tadesse
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Knudsen, Gerd Toril Mørkve
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Johannessen, Ane
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Rezwan, Faisal I.
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Malinovschi, Andrei
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Oudin, Anna
972f3b26-a8a1-4823-94e1-7a77fe394745
Benediktsdottir, Bryndis
bbe7acea-70d4-4611-b8d8-b416aa8bc375
Martino, David
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González, Francisco Javier Callejas
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Gómez, Leopoldo Palacios
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Holm, Mathias
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Jõgi, Nils Oskar
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Dharmage, Shyamali C.
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Skulstad, Svein Magne
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Watkins, Sarah H.
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Suderman, Matthew
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Gómez-real, Francisco
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Schlünssen, Vivi
872b391d-a114-4392-9701-265792601c79
Svanes, Cecilie
a3a19113-69d6-419f-8f28-e1a6c8479142
Holloway, John W.
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Kitaba, Negusse Tadesse, Knudsen, Gerd Toril Mørkve, Johannessen, Ane, Rezwan, Faisal I., Malinovschi, Andrei, Oudin, Anna, Benediktsdottir, Bryndis, Martino, David, González, Francisco Javier Callejas, Gómez, Leopoldo Palacios, Holm, Mathias, Jõgi, Nils Oskar, Dharmage, Shyamali C., Skulstad, Svein Magne, Watkins, Sarah H., Suderman, Matthew, Gómez-real, Francisco, Schlünssen, Vivi, Svanes, Cecilie and Holloway, John W. (2023) Fathers’ preconception smoking and offspring DNA methylation. Clinical Epigenetics, 15 (1), 131, [131]. (doi:10.1101/2023.01.13.523912).

Record type: Article

Abstract

Background: experimental studies suggest that exposures may impact respiratory health across generations via epigenetic changes transmitted specifically through male germ cells. Studies in humans are, however, limited. We aim to identify epigenetic marks in offspring associated with father’s preconception smoking.

Methods: we conducted epigenome-wide association studies (EWAS) in the RHINESSA cohort (7–50 years) on father’s any preconception smoking (n = 875 offspring) and father’s pubertal onset smoking < 15 years (n = 304), using Infinium MethylationEPIC Beadchip arrays, adjusting for offspring age, own smoking and maternal smoking. EWAS of maternal and offspring personal smoking were performed for comparison. Father’s smoking-associated dmCpGs were checked in subpopulations of offspring who reported no personal smoking and no maternal smoking exposure.

Results: father’s smoking commencing preconception was associated with methylation of blood DNA in offspring at two cytosine-phosphate-guanine sites (CpGs) (false discovery rate (FDR) < 0.05) in PRR5 and CENPP. Father’s pubertal onset smoking was associated with 19 CpGs (FDR < 0.05) mapped to 14 genes (TLR9, DNTT, FAM53B, NCAPG2, PSTPIP2, MBIP, C2orf39, NTRK2, DNAJC14, CDO1, PRAP1, TPCN1, IRS1 and CSF1R). These differentially methylated sites were hypermethylated and associated with promoter regions capable of gene silencing. Some of these sites were associated with offspring outcomes in this cohort including ever-asthma (NTRK2), ever-wheezing (DNAJC14, TPCN1), weight (FAM53B, NTRK2) and BMI (FAM53B, NTRK2) (p < 0.05). Pathway analysis showed enrichment for gene ontology pathways including regulation of gene expression, inflammation and innate immune responses. Father’s smoking-associated sites did not overlap with dmCpGs identified in EWAS of personal and maternal smoking (FDR < 0.05), and all sites remained significant (p < 0.05) in analyses of offspring with no personal smoking and no maternal smoking exposure.

Conclusion: father’s preconception smoking, particularly in puberty, is associated with offspring DNA methylation, providing evidence that epigenetic mechanisms may underlie epidemiological observations that pubertal paternal smoking increases risk of offspring asthma, low lung function and obesity.

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Accepted/In Press date: 24 July 2023
Published date: 31 August 2023
Keywords: Asthma, Chromosomal Proteins, Non-Histone, Cytosine, DNA Methylation, Epigenesis, Genetic, Guanine, Humans, Male, Smoking/adverse effects, Tobacco Smoking

Identifiers

Local EPrints ID: 478219
URI: http://eprints.soton.ac.uk/id/eprint/478219
ISSN: 1868-7075
PURE UUID: d7d63783-c87a-4cbd-9552-fd22a845cef4
ORCID for Negusse Tadesse Kitaba: ORCID iD orcid.org/0000-0001-7518-9096
ORCID for Faisal I. Rezwan: ORCID iD orcid.org/0000-0001-9921-222X
ORCID for John W. Holloway: ORCID iD orcid.org/0000-0001-9998-0464

Catalogue record

Date deposited: 23 Jun 2023 17:11
Last modified: 10 Aug 2024 01:51

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Contributors

Author: Gerd Toril Mørkve Knudsen
Author: Ane Johannessen
Author: Faisal I. Rezwan ORCID iD
Author: Andrei Malinovschi
Author: Anna Oudin
Author: Bryndis Benediktsdottir
Author: David Martino
Author: Francisco Javier Callejas González
Author: Leopoldo Palacios Gómez
Author: Mathias Holm
Author: Nils Oskar Jõgi
Author: Shyamali C. Dharmage
Author: Svein Magne Skulstad
Author: Sarah H. Watkins
Author: Matthew Suderman
Author: Francisco Gómez-real
Author: Vivi Schlünssen
Author: Cecilie Svanes

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