Shared DNA methylation signatures in childhood allergy: The MeDALL study.


Journal

The Journal of allergy and clinical immunology
ISSN: 1097-6825
Titre abrégé: J Allergy Clin Immunol
Pays: United States
ID NLM: 1275002

Informations de publication

Date de publication:
03 2021
Historique:
received: 07 05 2020
revised: 14 10 2020
accepted: 19 11 2020
pubmed: 19 12 2020
medline: 23 9 2021
entrez: 18 12 2020
Statut: ppublish

Résumé

Differential DNA methylation associated with allergy might provide novel insights into the shared or unique etiology of asthma, rhinitis, and eczema. We sought to identify DNA methylation profiles associated with childhood allergy. Within the European Mechanisms of the Development of Allergy (MeDALL) consortium, we performed an epigenome-wide association study of whole blood DNA methylation by using a cross-sectional design. Allergy was defined as having symptoms from at least 1 allergic disease (asthma, rhinitis, or eczema) and positive serum-specific IgE to common aeroallergens. The discovery study included 219 case patients and 417 controls at age 4 years and 228 case patients and 593 controls at age 8 years from 3 birth cohorts, with replication analyses in 325 case patients and 1111 controls. We performed additional analyses on 21 replicated sites in 785 case patients and 2124 controls by allergic symptoms only from 8 cohorts, 3 of which were not previously included in analyses. We identified 80 differentially methylated CpG sites that showed a 1% to 3% methylation difference in the discovery phase, of which 21 (including 5 novel CpG sites) passed genome-wide significance after meta-analysis. All 21 CpG sites were also significantly differentially methylated with allergic symptoms and shared between asthma, rhinitis, and eczema. The 21 CpG sites mapped to relevant genes, including ACOT7, LMAN3, and CLDN23. All 21 CpG sties were differently methylated in asthma in isolated eosinophils, and 10 were replicated in respiratory epithelium. Reduced whole blood DNA methylation at 21 CpG sites was significantly associated with childhood allergy. The findings provide novel insights into the shared molecular mechanisms underlying asthma, rhinitis, and eczema.

Sections du résumé

BACKGROUND
Differential DNA methylation associated with allergy might provide novel insights into the shared or unique etiology of asthma, rhinitis, and eczema.
OBJECTIVE
We sought to identify DNA methylation profiles associated with childhood allergy.
METHODS
Within the European Mechanisms of the Development of Allergy (MeDALL) consortium, we performed an epigenome-wide association study of whole blood DNA methylation by using a cross-sectional design. Allergy was defined as having symptoms from at least 1 allergic disease (asthma, rhinitis, or eczema) and positive serum-specific IgE to common aeroallergens. The discovery study included 219 case patients and 417 controls at age 4 years and 228 case patients and 593 controls at age 8 years from 3 birth cohorts, with replication analyses in 325 case patients and 1111 controls. We performed additional analyses on 21 replicated sites in 785 case patients and 2124 controls by allergic symptoms only from 8 cohorts, 3 of which were not previously included in analyses.
RESULTS
We identified 80 differentially methylated CpG sites that showed a 1% to 3% methylation difference in the discovery phase, of which 21 (including 5 novel CpG sites) passed genome-wide significance after meta-analysis. All 21 CpG sites were also significantly differentially methylated with allergic symptoms and shared between asthma, rhinitis, and eczema. The 21 CpG sites mapped to relevant genes, including ACOT7, LMAN3, and CLDN23. All 21 CpG sties were differently methylated in asthma in isolated eosinophils, and 10 were replicated in respiratory epithelium.
CONCLUSION
Reduced whole blood DNA methylation at 21 CpG sites was significantly associated with childhood allergy. The findings provide novel insights into the shared molecular mechanisms underlying asthma, rhinitis, and eczema.

Identifiants

pubmed: 33338541
pii: S0091-6749(20)31766-8
doi: 10.1016/j.jaci.2020.11.044
pmc: PMC8238013
mid: NIHMS1708910
pii:
doi:

Substances chimiques

Immunoglobulin E 37341-29-0

Types de publication

Journal Article Meta-Analysis Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1031-1040

Subventions

Organisme : NIEHS NIH HHS
ID : P30 ES007048
Pays : United States

Informations de copyright

Copyright © 2020 The Authors. Published by Elsevier Inc. All rights reserved.

Références

Prostaglandins Other Lipid Mediat. 2006 May;79(3-4):271-7
pubmed: 16647640
J Allergy Clin Immunol. 2016 Jun;137(6):1841-1851.e2
pubmed: 26703454
J Allergy Clin Immunol. 2017 Aug;140(2):571-577
pubmed: 28069425
Clin Epigenetics. 2018 Apr 17;10:55
pubmed: 29692868
Bioinformatics. 2012 Nov 15;28(22):2986-8
pubmed: 22954632
Nature. 2015 Feb 19;518(7539):317-30
pubmed: 25693563
Clin Epigenetics. 2015 Jul 21;7:68
pubmed: 26199674
Allergy. 2011 Jul;66 Suppl 95:1-3
pubmed: 21668839
Lancet. 2006 Aug 26;368(9537):733-43
pubmed: 16935684
BMC Genomics. 2017 Jan 5;18(1):25
pubmed: 28056824
Am J Respir Crit Care Med. 2017 May 15;195(10):1311-1320
pubmed: 27925796
J Allergy Clin Immunol. 2018 Sep;142(3):715-726
pubmed: 30195377
J Allergy Clin Immunol. 2015 Jul;136(1):69-80
pubmed: 25769910
Expert Rev Clin Immunol. 2019 Dec;15(12):1287-1302
pubmed: 31674254
Nat Genet. 2015 Dec;47(12):1449-1456
pubmed: 26482879
BMC Bioinformatics. 2012 May 08;13:86
pubmed: 22568884
Front Immunol. 2016 Jun 08;7:222
pubmed: 27375620
Nature. 2015 Apr 30;520(7549):670-674
pubmed: 25707804
JCI Insight. 2016 May 19;1(7):e86689
pubmed: 27699264
J Allergy Clin Immunol. 2019 Jun;143(6):2062-2074
pubmed: 30579849
Clin Epigenetics. 2017 Oct 13;9:112
pubmed: 29046734
Nat Genet. 2017 Jan;49(1):131-138
pubmed: 27918535
Sci Rep. 2019 Feb 26;9(1):2828
pubmed: 30808949
Nat Genet. 2003 Aug;34(4):395-402
pubmed: 12833157
Nat Commun. 2017 Dec 5;8(1):1943
pubmed: 29203772
Nat Genet. 2018 Jan;50(1):42-53
pubmed: 29273806
Genome Med. 2015 Aug 21;7:89
pubmed: 26292806
J Allergy Clin Immunol. 2020 Jun;145(6):1655-1663
pubmed: 31953105
Allergy. 2019 Jun;74(6):1166-1175
pubmed: 30762239
Cell. 2016 Nov 17;167(5):1415-1429.e19
pubmed: 27863252
Lancet Respir Med. 2019 Apr;7(4):336-346
pubmed: 30584054
J Allergy Clin Immunol. 2013 Mar;131(3):856-65
pubmed: 23380221
Genes Immun. 2014 Apr;15(4):247-55
pubmed: 24646526
Nat Commun. 2019 Jul 12;10(1):3095
pubmed: 31300640
Bioinformatics. 2010 Sep 1;26(17):2190-1
pubmed: 20616382
J Allergy Clin Immunol. 2017 May;139(5):1478-1488
pubmed: 27745942
Allergy. 2020 Dec;75(12):3248-3260
pubmed: 32277847
Epigenetics. 2019 May;14(5):445-466
pubmed: 30876376
Epigenetics. 2020 May;15(5):454-461
pubmed: 31818188
Nat Genet. 2017 Dec;49(12):1752-1757
pubmed: 29083406
J Transl Med. 2015 Aug 20;13:273
pubmed: 26289446
Cell Rep. 2016 Nov 22;17(9):2474-2487
pubmed: 27818087
J Allergy Clin Immunol. 2013 Jun;131(6):1644-52
pubmed: 23632297
Nat Biotechnol. 2010 May;28(5):495-501
pubmed: 20436461
Cell. 2016 Nov 3;167(4):1099-1110.e14
pubmed: 27814507
Lancet Respir Med. 2014 Feb;2(2):131-40
pubmed: 24503268
Lancet Respir Med. 2018 May;6(5):379-388
pubmed: 29496485

Auteurs

Cheng-Jian Xu (CJ)

Department of Pediatric Pulmonology and Pediatric Allergy, Beatrix Children's Hospital, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands; GRIAC Research Institute, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands; Centre for Individualized Infection Medicine, CiiM, a joint venture between Hannover Medical School and the Helmholtz Centre for Infection Research, Hannover, Germany; TWINCORE, Centre for Experimental and Clinical Infection Research, a joint venture between the Hannover Medical School and the Helmholtz Centre for Infection Research, Hannover, Germany; Department of Internal Medicine and Radboud Center for Infectious Diseases, Radboud University Medical Center, Nijmegen, The Netherlands. Electronic address: Xu.Chengjian@mh-hannover.de.

Olena Gruzieva (O)

Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden; Centre for Occupational and Environmental Medicine, Region Stockholm, Stockholm, Sweden.

Cancan Qi (C)

Department of Pediatric Pulmonology and Pediatric Allergy, Beatrix Children's Hospital, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands; GRIAC Research Institute, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands.

Ana Esplugues (A)

Nursing Department, Faculty of Nursing and Chiropody, Universitat de València, València, Spain; FISABIO-Universitat Jaume I-Universitat de València Joint Research Unit of Epidemiology and Environmental Health, València, Spain; CIBER Epidemiología y Salud Pública (CIBERESP), Madrid, Spain.

Ulrike Gehring (U)

Institute for Risk Assessment Sciences, Utrecht University, Utrecht, The Netherlands.

Anna Bergström (A)

Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden.

Dan Mason (D)

Bradford Institute for Health Research, Bradford, United Kingdom.

Leda Chatzi (L)

Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles.

Daniela Porta (D)

Department of Epidemiology, Lazio Regional Health Service, Rome, Italy.

Karin C Lodrup Carlsen (KC)

Division of Paediatric and Adolescent Medicine, The Faculty of Medicine, University of Oslo, Oslo, Norway; Division of Paediatric and Adolescent Medicine, Oslo University Hospital, Oslo, Norway.

Nour Baïz (N)

Sorbonne University and INSERM, Epidemiology of Allergic and Respiratory Diseases (EPAR) Department, IPLESP, Medical School Saint Antoine, Paris, France.

Anne-Marie Madore (AM)

Département des sciences fondamentales, Université du Québec à Chicoutimi, Saguenay, Québec City, Canada.

Harri Alenius (H)

Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden.

Bianca van Rijkom (B)

Department of Genetics, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands.

Soesma A Jankipersadsing (SA)

Department of Genetics, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands.

Pieter van der Vlies (P)

Department of Genetics, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands; HZPC Research BV, Metslawier, The Netherlands.

Inger Kull (I)

Department of Clinical Sciences and Education, Karolinska Institutet, Södersjukhuset, Stockholm, Sweden.

Marianne van Hage (M)

Division of Immunology and Allergy, Department of Medicine Solna, Karolinska Institutet, Stockholm, Sweden; Karolinska University Hospital, Stockholm, Sweden.

Mariona Bustamante (M)

CIBER Epidemiología y Salud Pública (CIBERESP), Madrid, Spain; ISGlobal, Institute of Global Health, Barcelona, Spain; Universitat Pompeu Fabra, Barcelona, Spain.

Aitana Lertxundi (A)

CIBER Epidemiología y Salud Pública (CIBERESP), Madrid, Spain; Preventive Medicine and Public Health Department, University of Basque Country (UPV/EHU), Leioa, Bizkaia, Spain; Health Research institute Biodonostia, Donostia-San Sebastian, Gipuzkoa, Spain.

Matias Torrent (M)

Health Research Institute of the Balearic Islands, Spain; ib-salut, Area de Salut de Menorca, Spain.

Gillian Santorelli (G)

Bradford Institute for Health Research, Bradford, United Kingdom.

Maria Pia Fantini (MP)

Department of Biomedical and Neuromotor Sciences, University of Bologna, Bologna, Italy.

Vegard Hovland (V)

Division of Paediatric and Adolescent Medicine, Oslo University Hospital, Oslo, Norway.

Giancarlo Pesce (G)

Sorbonne University and INSERM, Epidemiology of Allergic and Respiratory Diseases (EPAR) Department, IPLESP, Medical School Saint Antoine, Paris, France.

Nanna Fyhrquist (N)

Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden; Human Microbiome Program, Medicum, University of Helsinki, Helsinki, Finland.

Tiina Laatikainen (T)

Finnish Institute for Health and Welfare, Helsinki, Finland; Institute of Public Health and Clinical Nutrition, University of Eastern Finland, Kuopio, Finland.

Martijn C Nawijn (MC)

GRIAC Research Institute, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands; Department of Pathology and Medical Biology, Experimental Pulmonology and Inflammation Research, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands.

Yang Li (Y)

Centre for Individualized Infection Medicine, CiiM, a joint venture between Hannover Medical School and the Helmholtz Centre for Infection Research, Hannover, Germany; TWINCORE, Centre for Experimental and Clinical Infection Research, a joint venture between the Hannover Medical School and the Helmholtz Centre for Infection Research, Hannover, Germany; Department of Internal Medicine and Radboud Center for Infectious Diseases, Radboud University Medical Center, Nijmegen, The Netherlands.

Cisca Wijmenga (C)

Department of Genetics, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands.

Mihai G Netea (MG)

Department of Internal Medicine and Radboud Center for Infectious Diseases, Radboud University Medical Center, Nijmegen, The Netherlands; Department for Genomics and Immunoregulation, Life and Medical Sciences Institute (LIMES), University of Bonn, Bonn, Germany.

Jean Bousquet (J)

University Hospital, Montpellier, France; Department of Dermatology, Charité, Berlin, Germany.

Josep M Anto (JM)

CIBER Epidemiología y Salud Pública (CIBERESP), Madrid, Spain; ISGlobal, Institute of Global Health, Barcelona, Spain; Universitat Pompeu Fabra, Barcelona, Spain; IMIM (Hospital del Mar Medical Research Institute), Barcelona, Spain.

Catherine Laprise (C)

Département des sciences fondamentales, Université du Québec à Chicoutimi, Saguenay, Québec City, Canada; Centre intersectoriel en santé durable, Université du Québec à Chicoutimi, Saguenay, Québec City, Canada; Centre de santé et de services sociaux du Saguenay-Lac-Saint-Jean, Saguenay, Québec, Canada.

Tari Haahtela (T)

Skin and Allergy Hospital, Helsinki University Hospital, University of Helsinki, Helsinki, Finland.

Isabella Annesi-Maesano (I)

Sorbonne University and INSERM, Epidemiology of Allergic and Respiratory Diseases (EPAR) Department, IPLESP, Medical School Saint Antoine, Paris, France.

Kai-Håkon Carlsen (KH)

Division of Paediatric and Adolescent Medicine, The Faculty of Medicine, University of Oslo, Oslo, Norway; Division of Paediatric and Adolescent Medicine, Oslo University Hospital, Oslo, Norway.

Davide Gori (D)

Department of Biomedical and Neuromotor Sciences, University of Bologna, Bologna, Italy.

Manolis Kogevinas (M)

ISGlobal, Institute of Global Health, Barcelona, Spain.

John Wright (J)

Bradford Institute for Health Research, Bradford, United Kingdom.

Cilla Söderhäll (C)

Department of Women's and Children's Health, Karolinska Institutet, Stockholm, Sweden; Department of Biosciences and Nutrition, Karolinska Institutet, Stockholm, Sweden.

Judith M Vonk (JM)

GRIAC Research Institute, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands; Department of Epidemiology, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands.

Jordi Sunyer (J)

CIBER Epidemiología y Salud Pública (CIBERESP), Madrid, Spain; ISGlobal, Institute of Global Health, Barcelona, Spain; Universitat Pompeu Fabra, Barcelona, Spain; IMIM (Hospital del Mar Medical Research Institute), Barcelona, Spain.

Erik Melén (E)

Department of Clinical Sciences and Education, Karolinska Institutet, Södersjukhuset, Stockholm, Sweden; Sachs' Children's Hospital, Stockholm, Sweden.

Gerard H Koppelman (GH)

Department of Pediatric Pulmonology and Pediatric Allergy, Beatrix Children's Hospital, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands; GRIAC Research Institute, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH