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Maternal smoking during pregnancy induces persistent epigenetic changes into adolescence, independent of postnatal smoke exposure and is associated with cardiometabolic risk

Maternal smoking during pregnancy induces persistent epigenetic changes into adolescence, independent of postnatal smoke exposure and is associated with cardiometabolic risk
Maternal smoking during pregnancy induces persistent epigenetic changes into adolescence, independent of postnatal smoke exposure and is associated with cardiometabolic risk
Background: Several studies have shown effects of current and maternal smoking during pregnancy on DNA methylation of CpG sites in newborns and later in life. Here, we hypothesized that there are long-term and persistent epigenetic effects following maternal smoking during pregnancy on adolescent offspring DNA methylation, independent of paternal and postnatal smoke exposure. Furthermore, we explored the association between DNA methylation and cardiometabolic risk factors at 17 years of age.

Materials and Methods: DNA methylation was measured using the Illumina HumanMethylation450K BeadChip in whole blood from 995 participants attending the 17-year follow-up of the Raine Study. Linear mixed effects models were used to identify differential methylated CpGs, adjusting for parental smoking during pregnancy, and paternal, passive, and adolescent smoke exposure. Additional models examined the association between DNA methylation and paternal, adolescent, and passive smoking over the life course. Offspring CpGs identified were analyzed against cardiometabolic risk factors (blood pressure, triacylglycerols (TG), high-density lipoproteins cholesterol (HDL-C), and body mass index).

Results: We identified 23 CpGs (genome-wide p level: 1.06 × 10−7) that were associated with maternal smoking during pregnancy, including associated genes AHRR (cancer development), FTO (obesity), CNTNAP2 (developmental processes), CYP1A1 (detoxification), MYO1G (cell signalling), and FRMD4A (nicotine dependence). A sensitivity analysis showed a dose-dependent relationship between maternal smoking and offspring methylation. These results changed little following adjustment for paternal, passive, or offspring smoking, and there were no CpGs identified that associated with these variables. Two of the 23 identified CpGs [cg00253568 (FTO) and cg00213123 (CYP1A1)] were associated with either TG (male and female), diastolic blood pressure (female only), or HDL-C (male only), after Bonferroni correction.

Discussion: This study demonstrates a critical timing of cigarette smoke exposure over the life course for establishing persistent changes in DNA methylation into adolescence in a dose-dependent manner. There were significant associations between offspring CpG methylation and adolescent cardiovascular risk factors, namely, TG, HDL-C, and diastolic blood pressure. Future studies on current smoking habits and DNA methylation should consider the importance of maternal smoking during pregnancy and explore how the persistent DNA methylation effects of in utero smoke exposure increase cardiometabolic risk.
1664-8021
1-15
Rauschert, Sebastian
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Melton, Phillip
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Burdge, Graham
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Craig, Jeffrey
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Godfrey, Keith
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Holbrook, Joanna D
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Lillycrop, Karen
eeaaa78d-0c4d-4033-a178-60ce7345a2cc
Mori, Trevor
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Beilin, Lawrence J
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Oddy, Wendy H.
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Pennell, Craig
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Huang, Rae-Chi
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Rauschert, Sebastian
4d4cf3e0-3a95-4223-a49c-c3c5227785d0
Melton, Phillip
e6c4b581-a884-431c-b431-405ed8b29a22
Burdge, Graham
09d60a07-8ca1-4351-9bf1-de6ffcfb2159
Craig, Jeffrey
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Godfrey, Keith
0931701e-fe2c-44b5-8f0d-ec5c7477a6fd
Holbrook, Joanna D
69989b79-2710-4f12-946e-c6214e1b6513
Lillycrop, Karen
eeaaa78d-0c4d-4033-a178-60ce7345a2cc
Mori, Trevor
0490a692-1d94-4420-8e44-f2d803556c98
Beilin, Lawrence J
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Oddy, Wendy H.
1117306e-e383-424f-8525-13b0e493a2e7
Pennell, Craig
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Huang, Rae-Chi
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Rauschert, Sebastian, Melton, Phillip, Burdge, Graham, Craig, Jeffrey, Godfrey, Keith, Holbrook, Joanna D, Lillycrop, Karen, Mori, Trevor, Beilin, Lawrence J, Oddy, Wendy H., Pennell, Craig and Huang, Rae-Chi (2019) Maternal smoking during pregnancy induces persistent epigenetic changes into adolescence, independent of postnatal smoke exposure and is associated with cardiometabolic risk. Frontiers in Genetics, 10, 1-15, [770]. (doi:10.3389/fgene.2019.00770).

Record type: Article

Abstract

Background: Several studies have shown effects of current and maternal smoking during pregnancy on DNA methylation of CpG sites in newborns and later in life. Here, we hypothesized that there are long-term and persistent epigenetic effects following maternal smoking during pregnancy on adolescent offspring DNA methylation, independent of paternal and postnatal smoke exposure. Furthermore, we explored the association between DNA methylation and cardiometabolic risk factors at 17 years of age.

Materials and Methods: DNA methylation was measured using the Illumina HumanMethylation450K BeadChip in whole blood from 995 participants attending the 17-year follow-up of the Raine Study. Linear mixed effects models were used to identify differential methylated CpGs, adjusting for parental smoking during pregnancy, and paternal, passive, and adolescent smoke exposure. Additional models examined the association between DNA methylation and paternal, adolescent, and passive smoking over the life course. Offspring CpGs identified were analyzed against cardiometabolic risk factors (blood pressure, triacylglycerols (TG), high-density lipoproteins cholesterol (HDL-C), and body mass index).

Results: We identified 23 CpGs (genome-wide p level: 1.06 × 10−7) that were associated with maternal smoking during pregnancy, including associated genes AHRR (cancer development), FTO (obesity), CNTNAP2 (developmental processes), CYP1A1 (detoxification), MYO1G (cell signalling), and FRMD4A (nicotine dependence). A sensitivity analysis showed a dose-dependent relationship between maternal smoking and offspring methylation. These results changed little following adjustment for paternal, passive, or offspring smoking, and there were no CpGs identified that associated with these variables. Two of the 23 identified CpGs [cg00253568 (FTO) and cg00213123 (CYP1A1)] were associated with either TG (male and female), diastolic blood pressure (female only), or HDL-C (male only), after Bonferroni correction.

Discussion: This study demonstrates a critical timing of cigarette smoke exposure over the life course for establishing persistent changes in DNA methylation into adolescence in a dose-dependent manner. There were significant associations between offspring CpG methylation and adolescent cardiovascular risk factors, namely, TG, HDL-C, and diastolic blood pressure. Future studies on current smoking habits and DNA methylation should consider the importance of maternal smoking during pregnancy and explore how the persistent DNA methylation effects of in utero smoke exposure increase cardiometabolic risk.

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More information

Accepted/In Press date: 22 July 2019
Published date: 5 September 2019

Identifiers

Local EPrints ID: 433961
URI: http://eprints.soton.ac.uk/id/eprint/433961
ISSN: 1664-8021
PURE UUID: c4ad8ffb-d9eb-4575-a5cd-fed7db31e3ed
ORCID for Graham Burdge: ORCID iD orcid.org/0000-0002-7665-2967
ORCID for Keith Godfrey: ORCID iD orcid.org/0000-0002-4643-0618
ORCID for Joanna D Holbrook: ORCID iD orcid.org/0000-0003-1791-6894
ORCID for Karen Lillycrop: ORCID iD orcid.org/0000-0001-7350-5489

Catalogue record

Date deposited: 09 Sep 2019 16:30
Last modified: 17 Mar 2024 02:42

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Contributors

Author: Sebastian Rauschert
Author: Phillip Melton
Author: Graham Burdge ORCID iD
Author: Jeffrey Craig
Author: Keith Godfrey ORCID iD
Author: Joanna D Holbrook ORCID iD
Author: Karen Lillycrop ORCID iD
Author: Trevor Mori
Author: Lawrence J Beilin
Author: Wendy H. Oddy
Author: Craig Pennell
Author: Rae-Chi Huang

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