Prenatal Particulate Air Pollution and DNA Methylation in Newborns: An Epigenome-Wide Meta-Analysis

doi:10.1289/EHP4522

Meta-Analysis

. 2019 May;127(5):57012.

doi: 10.1289/EHP4522. Epub 2019 May 31.

Prenatal Particulate Air Pollution and DNA Methylation in Newborns: An Epigenome-Wide Meta-Analysis

Olena Gruzieva^{1

2}, Cheng-Jian Xu^{3

4

5}, Paul Yousefi^{6

7}, Caroline Relton^{6

7}, Simon Kebede Merid¹, Carrie V Breton⁸, Lu Gao⁸, Heather E Volk^{9

10}, Jason I Feinberg⁹, Christine Ladd-Acosta¹¹, Kelly Bakulski¹¹, Charles Auffray¹², Nathanaël Lemonnier^{12

13}, Michelle Plusquin^{14

15}, Akram Ghantous¹⁶, Zdenko Herceg¹⁶, Tim S Nawrot^{14

17}, Costanza Pizzi¹⁸, Lorenzo Richiardi¹⁸, Franca Rusconi¹⁹, Paolo Vineis¹⁵, Manolis Kogevinas^{20

21}, Janine F Felix^{22

23}, Liesbeth Duijts^{22

24}, Herman T den Dekker^{22

23}, Vincent W V Jaddoe^{22

23}, José L Ruiz^{25

26}, Mariona Bustamante^{20

21

25}, Josep Maria Antó^{20

21

27}, Jordi Sunyer^{20

21

27}, Martine Vrijheid^{20

21}, Kristine B Gutzkow²⁸, Regina Grazuleviciene²⁹, Carles Hernandez-Ferrer^{20

30}, Isabella Annesi-Maesano³¹, Johanna Lepeule³², Jean Bousquet^{33

34}, Anna Bergström^{1

2}, Inger Kull^{1

35

36}, Cilla Söderhäll^{37

38}, Juha Kere^{38

39}, Ulrike Gehring⁴⁰, Bert Brunekreef^{40

41}, Allan C Just⁴², Rosalind J Wright⁴³, Cheng Peng⁴⁴, Diane R Gold^{44

45}, Itai Kloog⁴⁶, Dawn L DeMeo⁴⁴, Göran Pershagen^{1

2}, Gerard H Koppelman^{3

4}, Stephanie J London⁴⁷, Andrea A Baccarelli⁴⁸, Erik Melén^{1

36}

Affiliations

¹ 1 Institute of Environmental Medicine, Karolinska Institutet , Stockholm, Sweden.
² 2 Centre for Occupational and Environmental Medicine, Stockholm County Council , Stockholm, Sweden.
³ 3 Groningen Research Institute for Asthma and COPD, University Medical Center Groningen, University of Groningen , Netherlands.
⁴ 4 Department of Pediatric Pulmonology and Pediatric Allergology, University Medical Center Groningen, Beatrix Children's Hospital, University of Groningen , Netherlands.
⁵ 5 Department of Genetics, University Medical Center Groningen, University of Groningen , Netherlands.
⁶ 6 MRC Integrative Epidemiology Unit, University of Bristol , Bristol, UK.
⁷ 7 Population Health Sciences, Bristol Medical School, University of Bristol , Bristol, UK.
⁸ 8 Department of Preventive Medicine, University of Southern California Los Angeles , Los Angeles, California, USA.
⁹ 9 Department of Mental Health, Johns Hopkins Bloomberg School of Public Health , Baltimore, Maryland, USA.
¹⁰ 10 Department of Environmental Health and Engineering, Johns Hopkins Bloomberg School of Public Health , Baltimore, Maryland, USA.
¹¹ 11 Department of Epidemiology, School of Public Health, University of Michigan , Ann Arbor, Michigan, USA.
¹² 12 European Institute for Systems Biology and Medicine (EISBM), CNRS-ENS-UCBL, Université de Lyon , Lyon, France.
¹³ 13 Institute for Advanced Biosciences, UGA-Institut national de la santé et de la recherché médicale (Inserm) , La Tronche, France.
¹⁴ 14 Centre for Environmental Sciences, Hasselt University , Diepenbeek, Belgium.
¹⁵ 15 MRC-PHE Centre for Environment and Health, School of Public Health, Imperial College London , London, UK.
¹⁶ 16 Epigenetics Group, International Agency for Research on Cancer, Lyon, France.
¹⁷ 17 Department of Public Health & Primary Care, Leuven University , Leuven, Belgium.
¹⁸ 18 Cancer Epidemiology Unit, Department of Medical Sciences, University of Turin and CPO-Piemonte , Turin, Italy.
¹⁹ 19 Unit of Epidemiology, Meyer Children's University Hospital , Florence, Italy.
²⁰ 20 Barcelona Institute for Global Health (ISGlobal) , Barcelona, Spain.
²¹ 22 CIBER Epidemiología y Salud Pública (CIBERESP) , Madrid, Spain.
²² 23 Generation R Study Group, Erasmus MC (Medical Centre) , University Medical Center Rotterdam , Rotterdam, Netherlands.
²³ 25 Department of Pediatrics, Erasmus MC, University Medical Center Rotterdam , Rotterdam, Netherlands.
²⁴ 26 Department of Pediatrics, Divisions of Respiratory Medicine and Allergology, and Neonatology, Erasmus MC, University Medical Center , Rotterdam, Netherlands.
²⁵ 27 Center for Genomic Regulation (CRG) , Barcelona, Spain.
²⁶ 28 Instituto de Parasitología y Biomedicina López-Neyra (IPBLN), Spanish National Research Council (CSIC) , Armilla, Granada, Spain.
²⁷ 29 Hospital de Mar Medical Research Institute (IMIM) , Barcelona, Spain.
²⁸ 30 Norwegian Institute of Public Health , Oslo, Norway.
²⁹ 31 Department of Environmental Sciences, Vytauto Didziojo Universitetas , Kaunas, Lithuania.
³⁰ 32 Computational Health Informatics Program , Boston Children's Hospital , Boston, Massachusetts, USA.
³¹ 33 Epidemiology of Allergic and Respiratory Diseases Department, IPLESP, Inserm and Sorbonne University Medical School Saint-Antoine , Paris, France.
³² 34 Université Grenoble Alpes, Inserm, National Institute of Health & Medical Research, CNRS, IAB , Grenoble, France.
³³ 35 Innovation Partnership on Active and Healthy Ageing Reference Site, MACVIA-France (Contre les Maladies Chroniques pour un Vieillissement Actif en France European) , Montpellier, France.
³⁴ 36 U 1168, VIMA: Ageing and Chronic Diseases Epidemiological and Public Health Approaches, Inserm Villejuif, Université Versailles St-Quentin-en-Yvelines , Montigny le Bretonneux, France.
³⁵ 37 Department of Clinical Science and Education, Södersjukhuset, Karolinska Institutet , Stockholm, Sweden.
³⁶ 38 Sachs Children's Hospital , Stockholm, Sweden.
³⁷ 39 Department of Women's and Children's Health, Karolinska Institutet , Stockholm, Sweden.
³⁸ 40 Department of Biosciences and Nutrition, Karolinska Institutet , Stockholm, Sweden.
³⁹ 42 School of Basic and Medical Biosciences, King's College London, Guy's Hospital , London, UK.
⁴⁰ 44 Institute for Risk Assessment Sciences, Utrecht University , Utrecht, Netherlands.
⁴¹ 45 Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Utrecht University , Utrecht, Netherlands.
⁴² 46 Department of Environmental Medicine and Public Health, Icahn School of Medicine at Mount Sinai , New York, USA.
⁴³ 47 Department of Pediatrics, Icahn School of Medicine at Mount Sinai , New York, USA.
⁴⁴ 48 Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School , Boston, Massachusetts, USA.
⁴⁵ 49 Department of Environmental Health, Harvard T.H. Chan School of Public Health , Boston, Massachusetts, USA.
⁴⁶ 50 Department of Geography and Environmental Development, Ben-Gurion University of the Negev , Beer Sheva, Israel.
⁴⁷ 51 National Institute of Environmental Health Sciences (NIEHS), National Institutes of Health (NIH), U.S. Department of Health and Human Services , Research Triangle Park, North Carolina, USA.
⁴⁸ 52 Department of Environmental Health Sciences, Columbia University Mailman School of Public Health , New York, USA.

PMID: 31148503
PMCID: PMC6792178
DOI: 10.1289/EHP4522

Meta-Analysis

Prenatal Particulate Air Pollution and DNA Methylation in Newborns: An Epigenome-Wide Meta-Analysis

Olena Gruzieva et al. Environ Health Perspect. 2019 May.

. 2019 May;127(5):57012.

doi: 10.1289/EHP4522. Epub 2019 May 31.

Authors

Affiliations

¹ 1 Institute of Environmental Medicine, Karolinska Institutet , Stockholm, Sweden.
² 2 Centre for Occupational and Environmental Medicine, Stockholm County Council , Stockholm, Sweden.
³ 3 Groningen Research Institute for Asthma and COPD, University Medical Center Groningen, University of Groningen , Netherlands.
⁴ 4 Department of Pediatric Pulmonology and Pediatric Allergology, University Medical Center Groningen, Beatrix Children's Hospital, University of Groningen , Netherlands.
⁵ 5 Department of Genetics, University Medical Center Groningen, University of Groningen , Netherlands.
⁶ 6 MRC Integrative Epidemiology Unit, University of Bristol , Bristol, UK.
⁷ 7 Population Health Sciences, Bristol Medical School, University of Bristol , Bristol, UK.
⁸ 8 Department of Preventive Medicine, University of Southern California Los Angeles , Los Angeles, California, USA.
⁹ 9 Department of Mental Health, Johns Hopkins Bloomberg School of Public Health , Baltimore, Maryland, USA.
¹⁰ 10 Department of Environmental Health and Engineering, Johns Hopkins Bloomberg School of Public Health , Baltimore, Maryland, USA.
¹¹ 11 Department of Epidemiology, School of Public Health, University of Michigan , Ann Arbor, Michigan, USA.
¹² 12 European Institute for Systems Biology and Medicine (EISBM), CNRS-ENS-UCBL, Université de Lyon , Lyon, France.
¹³ 13 Institute for Advanced Biosciences, UGA-Institut national de la santé et de la recherché médicale (Inserm) , La Tronche, France.
¹⁴ 14 Centre for Environmental Sciences, Hasselt University , Diepenbeek, Belgium.
¹⁵ 15 MRC-PHE Centre for Environment and Health, School of Public Health, Imperial College London , London, UK.
¹⁶ 16 Epigenetics Group, International Agency for Research on Cancer, Lyon, France.
¹⁷ 17 Department of Public Health & Primary Care, Leuven University , Leuven, Belgium.
¹⁸ 18 Cancer Epidemiology Unit, Department of Medical Sciences, University of Turin and CPO-Piemonte , Turin, Italy.
¹⁹ 19 Unit of Epidemiology, Meyer Children's University Hospital , Florence, Italy.
²⁰ 20 Barcelona Institute for Global Health (ISGlobal) , Barcelona, Spain.
²¹ 22 CIBER Epidemiología y Salud Pública (CIBERESP) , Madrid, Spain.
²² 23 Generation R Study Group, Erasmus MC (Medical Centre) , University Medical Center Rotterdam , Rotterdam, Netherlands.
²³ 25 Department of Pediatrics, Erasmus MC, University Medical Center Rotterdam , Rotterdam, Netherlands.
²⁴ 26 Department of Pediatrics, Divisions of Respiratory Medicine and Allergology, and Neonatology, Erasmus MC, University Medical Center , Rotterdam, Netherlands.
²⁵ 27 Center for Genomic Regulation (CRG) , Barcelona, Spain.
²⁶ 28 Instituto de Parasitología y Biomedicina López-Neyra (IPBLN), Spanish National Research Council (CSIC) , Armilla, Granada, Spain.
²⁷ 29 Hospital de Mar Medical Research Institute (IMIM) , Barcelona, Spain.
²⁸ 30 Norwegian Institute of Public Health , Oslo, Norway.
²⁹ 31 Department of Environmental Sciences, Vytauto Didziojo Universitetas , Kaunas, Lithuania.
³⁰ 32 Computational Health Informatics Program , Boston Children's Hospital , Boston, Massachusetts, USA.
³¹ 33 Epidemiology of Allergic and Respiratory Diseases Department, IPLESP, Inserm and Sorbonne University Medical School Saint-Antoine , Paris, France.
³² 34 Université Grenoble Alpes, Inserm, National Institute of Health & Medical Research, CNRS, IAB , Grenoble, France.
³³ 35 Innovation Partnership on Active and Healthy Ageing Reference Site, MACVIA-France (Contre les Maladies Chroniques pour un Vieillissement Actif en France European) , Montpellier, France.
³⁴ 36 U 1168, VIMA: Ageing and Chronic Diseases Epidemiological and Public Health Approaches, Inserm Villejuif, Université Versailles St-Quentin-en-Yvelines , Montigny le Bretonneux, France.
³⁵ 37 Department of Clinical Science and Education, Södersjukhuset, Karolinska Institutet , Stockholm, Sweden.
³⁶ 38 Sachs Children's Hospital , Stockholm, Sweden.
³⁷ 39 Department of Women's and Children's Health, Karolinska Institutet , Stockholm, Sweden.
³⁸ 40 Department of Biosciences and Nutrition, Karolinska Institutet , Stockholm, Sweden.
³⁹ 42 School of Basic and Medical Biosciences, King's College London, Guy's Hospital , London, UK.
⁴⁰ 44 Institute for Risk Assessment Sciences, Utrecht University , Utrecht, Netherlands.
⁴¹ 45 Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Utrecht University , Utrecht, Netherlands.
⁴² 46 Department of Environmental Medicine and Public Health, Icahn School of Medicine at Mount Sinai , New York, USA.
⁴³ 47 Department of Pediatrics, Icahn School of Medicine at Mount Sinai , New York, USA.
⁴⁴ 48 Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School , Boston, Massachusetts, USA.
⁴⁵ 49 Department of Environmental Health, Harvard T.H. Chan School of Public Health , Boston, Massachusetts, USA.
⁴⁶ 50 Department of Geography and Environmental Development, Ben-Gurion University of the Negev , Beer Sheva, Israel.
⁴⁷ 51 National Institute of Environmental Health Sciences (NIEHS), National Institutes of Health (NIH), U.S. Department of Health and Human Services , Research Triangle Park, North Carolina, USA.
⁴⁸ 52 Department of Environmental Health Sciences, Columbia University Mailman School of Public Health , New York, USA.

PMID: 31148503
PMCID: PMC6792178
DOI: 10.1289/EHP4522

Abstract

Background: Prenatal exposure to air pollution has been associated with childhood respiratory disease and other adverse outcomes. Epigenetics is a suggested link between exposures and health outcomes.

Objectives: We aimed to investigate associations between prenatal exposure to particulate matter (PM) with diameter [Formula: see text] ([Formula: see text]) or [Formula: see text] ([Formula: see text]) and DNA methylation in newborns and children.

Methods: We meta-analyzed associations between exposure to [Formula: see text] ([Formula: see text]) and [Formula: see text] ([Formula: see text]) at maternal home addresses during pregnancy and newborn DNA methylation assessed by Illumina Infinium HumanMethylation450K BeadChip in nine European and American studies, with replication in 688 independent newborns and look-up analyses in 2,118 older children. We used two approaches, one focusing on single cytosine-phosphate-guanine (CpG) sites and another on differentially methylated regions (DMRs). We also related PM exposures to blood mRNA expression.

Results: Six CpGs were significantly associated [false discovery rate (FDR) [Formula: see text]] with prenatal [Formula: see text] and 14 with [Formula: see text] exposure. Two of the [Formula: see text] CpGs mapped to FAM13A (cg00905156) and NOTCH4 (cg06849931) previously associated with lung function and asthma. Although these associations did not replicate in the smaller newborn sample, both CpGs were significant ([Formula: see text]) in 7- to 9-y-olds. For cg06849931, however, the direction of the association was inconsistent. Concurrent [Formula: see text] exposure was associated with a significantly higher NOTCH4 expression at age 16 y. We also identified several DMRs associated with either prenatal [Formula: see text] and or [Formula: see text] exposure, of which two [Formula: see text] DMRs, including H19 and MARCH11, replicated in newborns.

Conclusions: Several differentially methylated CpGs and DMRs associated with prenatal PM exposure were identified in newborns, with annotation to genes previously implicated in lung-related outcomes. https://doi.org/10.1289/EHP4522.

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Figures

Figure 1 A and B are Manhattan plots plotting negative log sub 10 with p values ranging between 0 and 8 (y-axis) across chromosome (from 1 to 22) (x-axis) for prenatal PM sub 10 and prenatal PM sub 2.5, respectively. — **Figure 1.**
Manhattan plot for epigenome-wide meta-analysis of the association between (A) prenatal ${PM}_{10}$ ( $n = 1,949$ ) and (B) prenatal ${PM}_{2.5}$ exposure ( $n = 1,551$ ) and cord blood DNA methylation. Note: The solid horizontal line corresponds to an FDR rate of 0.05. Manhattan plot for ${PM}_{10}$ : Six CpGs were considered statistically significant using FDR correction (red squares): cg15082635 in *GNB2L1;SNORD96A*, cg20340716 in *USP43*, cg00905156 in *FAM13A*, cg24127244 in *SRPRB*, cg06849931 in *NOTCH4*, and cg18640183 in *P4HA2*. Manhattan plot for ${PM}_{2.5}$ : Fourteen CpGs were considered statistically significant using FDR correction (red squares): cg16811875 in *PLXNA4*, cg12193649 in *ZNF705A*, cg11886880 $2,5 kb$ upstream of *C14orf2*, cg16253537 in *FNIP1*, cg12044654 in *COL22A1*, cg19120073 in *TMCO3*, cg05479174 in *SFRS8*, cg06846669 $8.1 kb$ downstream of *NEUROG1*, cg23270359 in *MRI1*, cg01011943 in *PSG5*, cg00348551 in *C7orf50*, cg24709511 $1,1 kb$ downstream of *MORN1*, cg22038738 in *PLAT*, and cg02236896 in *ZNF695*.

See this image and copyright information in PMC

Comment in

Effects of the Environment and Its Interplay with Genetics in Lung Function throughout Life.
Fuertes E, van der Plaat DA, Portas L, Minelli C. Fuertes E, et al. Am J Respir Crit Care Med. 2020 Jun 1;201(11):1425-1427. doi: 10.1164/rccm.201910-1937RR. Am J Respir Crit Care Med. 2020. PMID: 32293903 No abstract available.

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References

1. Abraham E, Rousseaux S, Agier L, Giorgis-Allemand L, Tost J, Galineau J, et al. . 2018. Pregnancy exposure to atmospheric pollution and meteorological conditions and placental DNA methylation. Environ Int 118:334–347, PMID: 29935799, 10.1016/j.envint.2018.05.007. - DOI - PubMed
1. Bakulski KM, Fallin MD. 2014. Epigenetic epidemiology: promises for public health research. Environ Mol Mutagen 55(3):171–183, PMID: 24449392, 10.1002/em.21850. - DOI - PMC - PubMed
1. Bakulski KM, Feinberg JI, Andrews SV, Yang J, Brown S, McKenney SL, et al. . 2016. DNA methylation of cord blood cell types: applications for mixed cell birth studies. Epigenetics 11(5):354–362, PMID: 27019159, 10.1080/15592294.2016.1161875. - DOI - PMC - PubMed
1. Barouki R, Melén E, Herceg Z, Beckers J, Chen J, Karagas M, et al. . 2018. Epigenetics as a mechanism linking developmental exposures to long-term toxicity. Environ Int 114:77–86, PMID: 29499450, 10.1016/j.envint.2018.02.014. - DOI - PMC - PubMed
1. Barrett T, Wilhite SE, Ledoux P, Evangelista C, Kim IF, Tomashevsky M, et al. . 2013. NCBI GEO: archive for functional genomics data sets–update. Nucleic Acids Res 41(Database issue):D991–D995, PMID: 23193258, 10.1093/nar/gks1193. - DOI - PMC - PubMed

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[1] Abraham E, Rousseaux S, Agier L, Giorgis-Allemand L, Tost J, Galineau J, et al. . 2018. Pregnancy exposure to atmospheric pollution and meteorological conditions and placental DNA methylation. Environ Int 118:334–347, PMID: 29935799, 10.1016/j.envint.2018.05.007. - DOI - PubMed

[2] Abraham E, Rousseaux S, Agier L, Giorgis-Allemand L, Tost J, Galineau J, et al. . 2018. Pregnancy exposure to atmospheric pollution and meteorological conditions and placental DNA methylation. Environ Int 118:334–347, PMID: 29935799, 10.1016/j.envint.2018.05.007. - DOI - PubMed

[3] Bakulski KM, Fallin MD. 2014. Epigenetic epidemiology: promises for public health research. Environ Mol Mutagen 55(3):171–183, PMID: 24449392, 10.1002/em.21850. - DOI - PMC - PubMed

[4] Bakulski KM, Fallin MD. 2014. Epigenetic epidemiology: promises for public health research. Environ Mol Mutagen 55(3):171–183, PMID: 24449392, 10.1002/em.21850. - DOI - PMC - PubMed

[5] Bakulski KM, Feinberg JI, Andrews SV, Yang J, Brown S, McKenney SL, et al. . 2016. DNA methylation of cord blood cell types: applications for mixed cell birth studies. Epigenetics 11(5):354–362, PMID: 27019159, 10.1080/15592294.2016.1161875. - DOI - PMC - PubMed

[6] Bakulski KM, Feinberg JI, Andrews SV, Yang J, Brown S, McKenney SL, et al. . 2016. DNA methylation of cord blood cell types: applications for mixed cell birth studies. Epigenetics 11(5):354–362, PMID: 27019159, 10.1080/15592294.2016.1161875. - DOI - PMC - PubMed

[7] Barouki R, Melén E, Herceg Z, Beckers J, Chen J, Karagas M, et al. . 2018. Epigenetics as a mechanism linking developmental exposures to long-term toxicity. Environ Int 114:77–86, PMID: 29499450, 10.1016/j.envint.2018.02.014. - DOI - PMC - PubMed

[8] Barouki R, Melén E, Herceg Z, Beckers J, Chen J, Karagas M, et al. . 2018. Epigenetics as a mechanism linking developmental exposures to long-term toxicity. Environ Int 114:77–86, PMID: 29499450, 10.1016/j.envint.2018.02.014. - DOI - PMC - PubMed

[9] Barrett T, Wilhite SE, Ledoux P, Evangelista C, Kim IF, Tomashevsky M, et al. . 2013. NCBI GEO: archive for functional genomics data sets–update. Nucleic Acids Res 41(Database issue):D991–D995, PMID: 23193258, 10.1093/nar/gks1193. - DOI - PMC - PubMed

[10] Barrett T, Wilhite SE, Ledoux P, Evangelista C, Kim IF, Tomashevsky M, et al. . 2013. NCBI GEO: archive for functional genomics data sets–update. Nucleic Acids Res 41(Database issue):D991–D995, PMID: 23193258, 10.1093/nar/gks1193. - DOI - PMC - PubMed

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Prenatal Particulate Air Pollution and DNA Methylation in Newborns: An Epigenome-Wide Meta-Analysis

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Prenatal Particulate Air Pollution and DNA Methylation in Newborns: An Epigenome-Wide Meta-Analysis

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