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Influence of Maternal Lifestyle and Diet on Perinatal DNA Methylation Signatures Associated With Childhood Arterial Stiffness at 8 to 9 Years

Robert Murray, Negusse Kitaba, Elie Antoun, Philip Titcombe, Sheila Barton, Cyrus Cooper, Hazel M. Inskip, Graham C. Burdge, Pamela A. Mahon, John Deanfield, Julian Halcox Orcid Logo, Libby Ellins Orcid Logo, Jennifer Bryant, Charles Peebles, Karen Lillycrop, Keith M. Godfrey, Mark A. Hanson, (EpiGen Consortium)

Hypertension, Volume: 78, Issue: 3, Pages: 787 - 800

Swansea University Authors: Julian Halcox Orcid Logo, Libby Ellins Orcid Logo

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DOI (Published version): 10.1161/hypertensionaha.121.17396

Abstract

Increases in aortic pulse wave velocity, a measure of arterial stiffness, can lead to elevated systolic blood pressure and increased cardiac afterload in adulthood. These changes are detectable in childhood and potentially originate in utero, where an adverse early life environment can alter DNA met...

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Published in: Hypertension
ISSN: 0194-911X 1524-4563
Published: Ovid Technologies (Wolters Kluwer Health) 2021
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These changes are detectable in childhood and potentially originate in utero, where an adverse early life environment can alter DNA methylation patterns detectable at birth. Here, analysis of epigenome-wide methylation patterns using umbilical cord blood DNA from 470 participants in the Southampton&#x2019;s Women&#x2019;s Survey identified differential methylation patterns associated with systolic blood pressure, pulse pressure, arterial distensibility, and descending aorta pulse wave velocity measured by magnetic resonance imaging at 8 to 9 years. Perinatal methylation levels at 16 CpG loci were associated with descending aorta pulse wave velocity, with identified CpG sites enriched in pathways involved in DNA repair (P=9.03&#xD7;10&#x2212;11). The most significant association was with cg20793626 methylation (within protein phosphatase, Mg2+/Mn2+ dependent 1D; &#x3B2;=&#x2212;0.05 m/s/1% methylation change, [95% CI, &#x2212;0.09 to &#x2212;0.02]). Genetic variation was also examined but had a minor influence on these observations. Eight pulse wave velocity-linked dmCpGs were associated with prenatal modifiable risk factors, with cg08509237 methylation (within palmitoyl-protein thioesterase-2) associated with maternal oily fish consumption in early and late pregnancy. Lower oily fish consumption in early pregnancy modified the relationship between methylation and pulse wave velocity, with lower consumption strengthening the association between cg08509237 methylation and increased pulse wave velocity. 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The Southampton Women&#x2019;s Survey has received funding from the Medical Research Council, Dunhill Medical Trust, British Heart Foundation, Arthritis Research UK, Food Standards Agency, National Institute for Health Research (NIHR) Southampton Biomedical Research Centre, and the European Union&#x2019;s Seventh Framework Programme (FP7/2007&#x2013;2013), project EarlyNutrition, under grant agreement 289346 and the European Union&#x2019;s Horizon 2020 research and innovation programme (LIFECYCLE, grant agreement No. 733206). K.M. Godfrey is supported by the UK Medical Research Council (MC_UU_12011/4), the National Institute for Health Research (NIHR Senior Investigator [NF-SI-0515-10042], NIHR Southampton 1000DaysPlus Global Nutrition Research Group [17/63/154] and NIHR Southampton Biomedical Research Centre [IS-BRC-1215-20004]), and the European Union (Erasmus+ Programme ImpENSA 598488-EPP-1-2018-1-DE-EPPKA2-CBHE-JP).</funders><lastEdited>2021-09-07T15:00:31.7601062</lastEdited><Created>2021-06-01T10:05:29.4227487</Created><path><level id="1">Faculty of Medicine, Health and Life Sciences</level><level id="2">Swansea University Medical School - Medicine</level></path><authors><author><firstname>Robert</firstname><surname>Murray</surname><order>1</order></author><author><firstname>Negusse</firstname><surname>Kitaba</surname><order>2</order></author><author><firstname>Elie</firstname><surname>Antoun</surname><order>3</order></author><author><firstname>Philip</firstname><surname>Titcombe</surname><order>4</order></author><author><firstname>Sheila</firstname><surname>Barton</surname><order>5</order></author><author><firstname>Cyrus</firstname><surname>Cooper</surname><order>6</order></author><author><firstname>Hazel M.</firstname><surname>Inskip</surname><order>7</order></author><author><firstname>Graham C.</firstname><surname>Burdge</surname><order>8</order></author><author><firstname>Pamela A.</firstname><surname>Mahon</surname><order>9</order></author><author><firstname>John</firstname><surname>Deanfield</surname><order>10</order></author><author><firstname>Julian</firstname><surname>Halcox</surname><orcid>0000-0001-6926-2947</orcid><order>11</order></author><author><firstname>Libby</firstname><surname>Ellins</surname><orcid>0000-0001-5164-6416</orcid><order>12</order></author><author><firstname>Jennifer</firstname><surname>Bryant</surname><order>13</order></author><author><firstname>Charles</firstname><surname>Peebles</surname><order>14</order></author><author><firstname>Karen</firstname><surname>Lillycrop</surname><order>15</order></author><author><firstname>Keith M.</firstname><surname>Godfrey</surname><order>16</order></author><author><firstname>Mark A.</firstname><surname>Hanson</surname><order>17</order></author><author><firstname>(EpiGen</firstname><surname>Consortium)</surname><order>18</order></author></authors><documents><document><filename>56995__20606__6fb25a0f8b4b4d6983402bdc5daef7b2.pdf</filename><originalFilename>56995.pdf</originalFilename><uploaded>2021-08-10T17:16:09.1112318</uploaded><type>Output</type><contentLength>1556662</contentLength><contentType>application/pdf</contentType><version>Version of Record</version><cronfaStatus>true</cronfaStatus><documentNotes>&#xA9; 2021 The Authors. 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spelling 2021-09-07T15:00:31.7601062 v2 56995 2021-06-01 Influence of Maternal Lifestyle and Diet on Perinatal DNA Methylation Signatures Associated With Childhood Arterial Stiffness at 8 to 9 Years 3676f695eeda169d0f8c618adf27c04b 0000-0001-6926-2947 Julian Halcox Julian Halcox true false 553ce2abe05a6396e7dd6eadb6b90a6d 0000-0001-5164-6416 Libby Ellins Libby Ellins true false 2021-06-01 HDAT Increases in aortic pulse wave velocity, a measure of arterial stiffness, can lead to elevated systolic blood pressure and increased cardiac afterload in adulthood. These changes are detectable in childhood and potentially originate in utero, where an adverse early life environment can alter DNA methylation patterns detectable at birth. Here, analysis of epigenome-wide methylation patterns using umbilical cord blood DNA from 470 participants in the Southampton’s Women’s Survey identified differential methylation patterns associated with systolic blood pressure, pulse pressure, arterial distensibility, and descending aorta pulse wave velocity measured by magnetic resonance imaging at 8 to 9 years. Perinatal methylation levels at 16 CpG loci were associated with descending aorta pulse wave velocity, with identified CpG sites enriched in pathways involved in DNA repair (P=9.03×10−11). The most significant association was with cg20793626 methylation (within protein phosphatase, Mg2+/Mn2+ dependent 1D; β=−0.05 m/s/1% methylation change, [95% CI, −0.09 to −0.02]). Genetic variation was also examined but had a minor influence on these observations. Eight pulse wave velocity-linked dmCpGs were associated with prenatal modifiable risk factors, with cg08509237 methylation (within palmitoyl-protein thioesterase-2) associated with maternal oily fish consumption in early and late pregnancy. Lower oily fish consumption in early pregnancy modified the relationship between methylation and pulse wave velocity, with lower consumption strengthening the association between cg08509237 methylation and increased pulse wave velocity. In conclusion, measurement of perinatal DNA methylation signatures has utility in identifying infants who might benefit from preventive interventions to reduce risk of later cardiovascular disease, and modifiable maternal factors can reduce this risk in the child. Journal Article Hypertension 78 3 787 800 Ovid Technologies (Wolters Kluwer Health) 0194-911X 1524-4563 1 9 2021 2021-09-01 10.1161/hypertensionaha.121.17396 http://dx.doi.org/10.1161/hypertensionaha.121.17396 COLLEGE NANME Health Data Science COLLEGE CODE HDAT Swansea University Other This work was funded by the British Heart Foundation (RG/15/17/31749). The Southampton Women’s Survey has received funding from the Medical Research Council, Dunhill Medical Trust, British Heart Foundation, Arthritis Research UK, Food Standards Agency, National Institute for Health Research (NIHR) Southampton Biomedical Research Centre, and the European Union’s Seventh Framework Programme (FP7/2007–2013), project EarlyNutrition, under grant agreement 289346 and the European Union’s Horizon 2020 research and innovation programme (LIFECYCLE, grant agreement No. 733206). K.M. Godfrey is supported by the UK Medical Research Council (MC_UU_12011/4), the National Institute for Health Research (NIHR Senior Investigator [NF-SI-0515-10042], NIHR Southampton 1000DaysPlus Global Nutrition Research Group [17/63/154] and NIHR Southampton Biomedical Research Centre [IS-BRC-1215-20004]), and the European Union (Erasmus+ Programme ImpENSA 598488-EPP-1-2018-1-DE-EPPKA2-CBHE-JP). 2021-09-07T15:00:31.7601062 2021-06-01T10:05:29.4227487 Faculty of Medicine, Health and Life Sciences Swansea University Medical School - Medicine Robert Murray 1 Negusse Kitaba 2 Elie Antoun 3 Philip Titcombe 4 Sheila Barton 5 Cyrus Cooper 6 Hazel M. Inskip 7 Graham C. Burdge 8 Pamela A. Mahon 9 John Deanfield 10 Julian Halcox 0000-0001-6926-2947 11 Libby Ellins 0000-0001-5164-6416 12 Jennifer Bryant 13 Charles Peebles 14 Karen Lillycrop 15 Keith M. Godfrey 16 Mark A. Hanson 17 (EpiGen Consortium) 18 56995__20606__6fb25a0f8b4b4d6983402bdc5daef7b2.pdf 56995.pdf 2021-08-10T17:16:09.1112318 Output 1556662 application/pdf Version of Record true © 2021 The Authors. Hypertension is published on behalf of the American Heart Association, Inc., by Wolters Kluwer Health, Inc. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution, and reproduction in any medium, provided that the original work is properly cited. true eng https://creativecommons.org/licenses/by/4.0/
title Influence of Maternal Lifestyle and Diet on Perinatal DNA Methylation Signatures Associated With Childhood Arterial Stiffness at 8 to 9 Years
spellingShingle Influence of Maternal Lifestyle and Diet on Perinatal DNA Methylation Signatures Associated With Childhood Arterial Stiffness at 8 to 9 Years
Julian Halcox
Libby Ellins
title_short Influence of Maternal Lifestyle and Diet on Perinatal DNA Methylation Signatures Associated With Childhood Arterial Stiffness at 8 to 9 Years
title_full Influence of Maternal Lifestyle and Diet on Perinatal DNA Methylation Signatures Associated With Childhood Arterial Stiffness at 8 to 9 Years
title_fullStr Influence of Maternal Lifestyle and Diet on Perinatal DNA Methylation Signatures Associated With Childhood Arterial Stiffness at 8 to 9 Years
title_full_unstemmed Influence of Maternal Lifestyle and Diet on Perinatal DNA Methylation Signatures Associated With Childhood Arterial Stiffness at 8 to 9 Years
title_sort Influence of Maternal Lifestyle and Diet on Perinatal DNA Methylation Signatures Associated With Childhood Arterial Stiffness at 8 to 9 Years
author_id_str_mv 3676f695eeda169d0f8c618adf27c04b
553ce2abe05a6396e7dd6eadb6b90a6d
author_id_fullname_str_mv 3676f695eeda169d0f8c618adf27c04b_***_Julian Halcox
553ce2abe05a6396e7dd6eadb6b90a6d_***_Libby Ellins
author Julian Halcox
Libby Ellins
author2 Robert Murray
Negusse Kitaba
Elie Antoun
Philip Titcombe
Sheila Barton
Cyrus Cooper
Hazel M. Inskip
Graham C. Burdge
Pamela A. Mahon
John Deanfield
Julian Halcox
Libby Ellins
Jennifer Bryant
Charles Peebles
Karen Lillycrop
Keith M. Godfrey
Mark A. Hanson
(EpiGen Consortium)
format Journal article
container_title Hypertension
container_volume 78
container_issue 3
container_start_page 787
publishDate 2021
institution Swansea University
issn 0194-911X
1524-4563
doi_str_mv 10.1161/hypertensionaha.121.17396
publisher Ovid Technologies (Wolters Kluwer Health)
college_str Faculty of Medicine, Health and Life Sciences
hierarchytype
hierarchy_top_id facultyofmedicinehealthandlifesciences
hierarchy_top_title Faculty of Medicine, Health and Life Sciences
hierarchy_parent_id facultyofmedicinehealthandlifesciences
hierarchy_parent_title Faculty of Medicine, Health and Life Sciences
department_str Swansea University Medical School - Medicine{{{_:::_}}}Faculty of Medicine, Health and Life Sciences{{{_:::_}}}Swansea University Medical School - Medicine
url http://dx.doi.org/10.1161/hypertensionaha.121.17396
document_store_str 1
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description Increases in aortic pulse wave velocity, a measure of arterial stiffness, can lead to elevated systolic blood pressure and increased cardiac afterload in adulthood. These changes are detectable in childhood and potentially originate in utero, where an adverse early life environment can alter DNA methylation patterns detectable at birth. Here, analysis of epigenome-wide methylation patterns using umbilical cord blood DNA from 470 participants in the Southampton’s Women’s Survey identified differential methylation patterns associated with systolic blood pressure, pulse pressure, arterial distensibility, and descending aorta pulse wave velocity measured by magnetic resonance imaging at 8 to 9 years. Perinatal methylation levels at 16 CpG loci were associated with descending aorta pulse wave velocity, with identified CpG sites enriched in pathways involved in DNA repair (P=9.03×10−11). The most significant association was with cg20793626 methylation (within protein phosphatase, Mg2+/Mn2+ dependent 1D; β=−0.05 m/s/1% methylation change, [95% CI, −0.09 to −0.02]). Genetic variation was also examined but had a minor influence on these observations. Eight pulse wave velocity-linked dmCpGs were associated with prenatal modifiable risk factors, with cg08509237 methylation (within palmitoyl-protein thioesterase-2) associated with maternal oily fish consumption in early and late pregnancy. Lower oily fish consumption in early pregnancy modified the relationship between methylation and pulse wave velocity, with lower consumption strengthening the association between cg08509237 methylation and increased pulse wave velocity. In conclusion, measurement of perinatal DNA methylation signatures has utility in identifying infants who might benefit from preventive interventions to reduce risk of later cardiovascular disease, and modifiable maternal factors can reduce this risk in the child.
published_date 2021-09-01T04:12:23Z
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