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Epigenome-wide meta-analysis of blood DNA methylation in newborns and children identifies numerous loci related to gestational age

Epigenome-wide meta-analysis of blood DNA methylation in newborns and children identifies numerous loci related to gestational age
Epigenome-wide meta-analysis of blood DNA methylation in newborns and children identifies numerous loci related to gestational age
Background

Preterm birth and shorter duration of pregnancy are associated with increased morbidity in neonatal and later life. As the epigenome is known to have an important role during fetal development, we investigated associations between gestational age and blood DNA methylation in children.

Methods

We performed meta-analysis of Illumina’s HumanMethylation450-array associations between gestational age and cord blood DNA methylation in 3648 newborns from 17 cohorts without common pregnancy complications, induced delivery or caesarean section. We also explored associations of gestational age with DNA methylation measured at 4–18 years in additional pediatric cohorts. Follow-up analyses of DNA methylation and gene expression correlations were performed in cord blood. DNA methylation profiles were also explored in tissues relevant for gestational age health effects: fetal brain and lung.

Results

We identified 8899 CpGs in cord blood that were associated with gestational age (range 27–42 weeks), at Bonferroni significance, P < 1.06 × 10− 7, of which 3343 were novel. These were annotated to 4966 genes. After restricting findings to at least three significant adjacent CpGs, we identified 1276 CpGs annotated to 325 genes. Results were generally consistent when analyses were restricted to term births. Cord blood findings tended not to persist into childhood and adolescence. Pathway analyses identified enrichment for biological processes critical to embryonic development. Follow-up of identified genes showed correlations between gestational age and DNA methylation levels in fetal brain and lung tissue, as well as correlation with expression levels.

Conclusions

We identified numerous CpGs differentially methylated in relation to gestational age at birth that appear to reflect fetal developmental processes across tissues. These findings may contribute to understanding mechanisms linking gestational age to health effects.

Development, Epigenetics, Gestational age, Preterm birth, Transcriptomics
1756-994X
1-17
Merid, Simon Kebede
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Novoloaca, Alexei
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Merid, Simon Kebede, Novoloaca, Alexei, Sharp, Gemma C., Küpers, Leanne K., Kho, Alvin T., Roy, Ritu, Gao, Lu, Annesi-Maesano, Isabella, Jain, Pooja, Plusquin, Michelle, Kogevinas, Manolis, Allard, Catherine, Vehmeijer, Florianne O., Kazmi, Nabila, Salas, Lucas A., Rezwan, Faisal I., Zhang, Hongmei, Sebert, Sylvain, Czamara, Darina, Rifas-Shiman, Sheryl L., Melton, Phillip E., Lawlor, Debbie A., Pershagen, Göran, Breton, Carrie V., Huen, Karen, Baiz, Nour, Gagliardi, Luigi, Nawrot, Tim S., Corpeleijn, Eva, Perron, Patrice, Duijts, Liesbeth, Nohr, Ellen Aagaard, Bustamante, Mariona, Ewart, Susan L., Karmaus, Wilfried, Zhao, Shanshan, Page, Christian M., Herceg, Zdenko, Jarvelin, Marjo-Riitta, Lahti, Jari, Baccarelli, Andrea A., Anderson, Denise, Kachroo, Priyadarshini, Relton, Caroline L., Bergström, Anna, Eskenazi, Brenda, Soomro, Munawar Hussain, Vineis, Paolo, Snieder, Harold, Bouchard, Luigi, Jaddoe, Vincent W., Sørensen, Thorkild I.A., Vrijheid, Martine, Arshad, Syed, Holloway, John W., Håberg, Siri E., Magnus, Per, Dwyer, Terence, Binder, Elisabeth B., Demeo, Dawn L., Vonk, Judith M., Newnham, John, Tantisira, Kelan G., Kull, Inger, Wiemels, Joseph L., Heude, Barbara, Sunyer, Jordi, Nystad, Wenche, Munthe-kaas, Monica C., Räikkönen, Katri, Oken, Emily, Huang, Rae-Chi, Weiss, Scott T., Antó, Josep Maria, Bousquet, Jean, Kumar, Ashish, Söderhäll, Cilla, Almqvist, Catarina, Cardenas, Andres, Gruzieva, Olena, Xu, Cheng-Jian, Reese, Sarah E., Kere, Juha, Brodin, Petter, Solomon, Olivia, Wielscher, Matthias, Holland, Nina, Ghantous, Akram, Hivert, Marie-France, Felix, Janine F., Koppelman, Gerard H., London, Stephanie J. and Melén, Erik (2020) Epigenome-wide meta-analysis of blood DNA methylation in newborns and children identifies numerous loci related to gestational age. Genome Medicine, 12 (1), 1-17, [25]. (doi:10.1186/s13073-020-0716-9).

Record type: Article

Abstract

Background

Preterm birth and shorter duration of pregnancy are associated with increased morbidity in neonatal and later life. As the epigenome is known to have an important role during fetal development, we investigated associations between gestational age and blood DNA methylation in children.

Methods

We performed meta-analysis of Illumina’s HumanMethylation450-array associations between gestational age and cord blood DNA methylation in 3648 newborns from 17 cohorts without common pregnancy complications, induced delivery or caesarean section. We also explored associations of gestational age with DNA methylation measured at 4–18 years in additional pediatric cohorts. Follow-up analyses of DNA methylation and gene expression correlations were performed in cord blood. DNA methylation profiles were also explored in tissues relevant for gestational age health effects: fetal brain and lung.

Results

We identified 8899 CpGs in cord blood that were associated with gestational age (range 27–42 weeks), at Bonferroni significance, P < 1.06 × 10− 7, of which 3343 were novel. These were annotated to 4966 genes. After restricting findings to at least three significant adjacent CpGs, we identified 1276 CpGs annotated to 325 genes. Results were generally consistent when analyses were restricted to term births. Cord blood findings tended not to persist into childhood and adolescence. Pathway analyses identified enrichment for biological processes critical to embryonic development. Follow-up of identified genes showed correlations between gestational age and DNA methylation levels in fetal brain and lung tissue, as well as correlation with expression levels.

Conclusions

We identified numerous CpGs differentially methylated in relation to gestational age at birth that appear to reflect fetal developmental processes across tissues. These findings may contribute to understanding mechanisms linking gestational age to health effects.

Text
Epigenome-wide meta-analysis of blood DNA - Version of Record
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More information

Accepted/In Press date: 30 January 2020
Published date: 2 March 2020
Keywords: Development, Epigenetics, Gestational age, Preterm birth, Transcriptomics

Identifiers

Local EPrints ID: 438438
URI: http://eprints.soton.ac.uk/id/eprint/438438
ISSN: 1756-994X
PURE UUID: 4071018b-8209-47d4-8056-e51b47313a58
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: 10 Mar 2020 17:31
Last modified: 22 Nov 2021 03:04

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Contributors

Author: Simon Kebede Merid
Author: Alexei Novoloaca
Author: Gemma C. Sharp
Author: Leanne K. Küpers
Author: Alvin T. Kho
Author: Ritu Roy
Author: Lu Gao
Author: Isabella Annesi-Maesano
Author: Pooja Jain
Author: Michelle Plusquin
Author: Manolis Kogevinas
Author: Catherine Allard
Author: Florianne O. Vehmeijer
Author: Nabila Kazmi
Author: Lucas A. Salas
Author: Faisal I. Rezwan ORCID iD
Author: Hongmei Zhang
Author: Sylvain Sebert
Author: Darina Czamara
Author: Sheryl L. Rifas-Shiman
Author: Phillip E. Melton
Author: Debbie A. Lawlor
Author: Göran Pershagen
Author: Carrie V. Breton
Author: Karen Huen
Author: Nour Baiz
Author: Luigi Gagliardi
Author: Tim S. Nawrot
Author: Eva Corpeleijn
Author: Patrice Perron
Author: Liesbeth Duijts
Author: Ellen Aagaard Nohr
Author: Mariona Bustamante
Author: Susan L. Ewart
Author: Wilfried Karmaus
Author: Shanshan Zhao
Author: Christian M. Page
Author: Zdenko Herceg
Author: Marjo-Riitta Jarvelin
Author: Jari Lahti
Author: Andrea A. Baccarelli
Author: Denise Anderson
Author: Priyadarshini Kachroo
Author: Caroline L. Relton
Author: Anna Bergström
Author: Brenda Eskenazi
Author: Munawar Hussain Soomro
Author: Paolo Vineis
Author: Harold Snieder
Author: Luigi Bouchard
Author: Vincent W. Jaddoe
Author: Thorkild I.A. Sørensen
Author: Martine Vrijheid
Author: Syed Arshad
Author: Siri E. Håberg
Author: Per Magnus
Author: Terence Dwyer
Author: Elisabeth B. Binder
Author: Dawn L. Demeo
Author: Judith M. Vonk
Author: John Newnham
Author: Kelan G. Tantisira
Author: Inger Kull
Author: Joseph L. Wiemels
Author: Barbara Heude
Author: Jordi Sunyer
Author: Wenche Nystad
Author: Monica C. Munthe-kaas
Author: Katri Räikkönen
Author: Emily Oken
Author: Rae-Chi Huang
Author: Scott T. Weiss
Author: Josep Maria Antó
Author: Jean Bousquet
Author: Ashish Kumar
Author: Cilla Söderhäll
Author: Catarina Almqvist
Author: Andres Cardenas
Author: Olena Gruzieva
Author: Cheng-Jian Xu
Author: Sarah E. Reese
Author: Juha Kere
Author: Petter Brodin
Author: Olivia Solomon
Author: Matthias Wielscher
Author: Nina Holland
Author: Akram Ghantous
Author: Marie-France Hivert
Author: Janine F. Felix
Author: Gerard H. Koppelman
Author: Stephanie J. London
Author: Erik Melén

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