A novel whole blood gene expression signature for asthma, dermatitis, and rhinitis multimorbidity in children and adolescents.


Journal

Allergy
ISSN: 1398-9995
Titre abrégé: Allergy
Pays: Denmark
ID NLM: 7804028

Informations de publication

Date de publication:
12 2020
Historique:
received: 12 02 2020
revised: 25 03 2020
accepted: 30 03 2020
pubmed: 12 4 2020
medline: 15 5 2021
entrez: 12 4 2020
Statut: ppublish

Résumé

Allergic diseases often occur in combination (multimorbidity). Human blood transcriptome studies have not addressed multimorbidity. Large-scale gene expression data were combined to retrieve biomarkers and signaling pathways to disentangle allergic multimorbidity phenotypes. Integrated transcriptomic analysis was conducted in 1233 participants with a discovery phase using gene expression data (Human Transcriptome Array 2.0) from whole blood of 786 children from three European birth cohorts (MeDALL), and a replication phase using RNA Sequencing data from an independent cohort (EVA-PR, n = 447). Allergic diseases (asthma, atopic dermatitis, rhinitis) were considered as single disease or multimorbidity (at least two diseases), and compared with no disease. Fifty genes were differentially expressed in allergic diseases. Thirty-two were not previously described in allergy. Eight genes were consistently overexpressed in all types of multimorbidity for asthma, dermatitis, and rhinitis (CLC, EMR4P, IL5RA, FRRS1, HRH4, SLC29A1, SIGLEC8, IL1RL1). All genes were replicated the in EVA-PR cohort. RT-qPCR validated the overexpression of selected genes. In MeDALL, 27 genes were differentially expressed in rhinitis alone, but none was significant for asthma or dermatitis alone. The multimorbidity signature was enriched in eosinophil-associated immune response and signal transduction. Protein-protein interaction network analysis identified IL5/JAK/STAT and IL33/ST2/IRAK/TRAF as key signaling pathways in multimorbid diseases. Synergistic effect of multimorbidity on gene expression levels was found. A signature of eight genes identifies multimorbidity for asthma, rhinitis, and dermatitis. Our results have clinical and mechanistic implications, and suggest that multimorbidity should be considered differently than allergic diseases occurring alone.

Sections du résumé

BACKGROUND
Allergic diseases often occur in combination (multimorbidity). Human blood transcriptome studies have not addressed multimorbidity. Large-scale gene expression data were combined to retrieve biomarkers and signaling pathways to disentangle allergic multimorbidity phenotypes.
METHODS
Integrated transcriptomic analysis was conducted in 1233 participants with a discovery phase using gene expression data (Human Transcriptome Array 2.0) from whole blood of 786 children from three European birth cohorts (MeDALL), and a replication phase using RNA Sequencing data from an independent cohort (EVA-PR, n = 447). Allergic diseases (asthma, atopic dermatitis, rhinitis) were considered as single disease or multimorbidity (at least two diseases), and compared with no disease.
RESULTS
Fifty genes were differentially expressed in allergic diseases. Thirty-two were not previously described in allergy. Eight genes were consistently overexpressed in all types of multimorbidity for asthma, dermatitis, and rhinitis (CLC, EMR4P, IL5RA, FRRS1, HRH4, SLC29A1, SIGLEC8, IL1RL1). All genes were replicated the in EVA-PR cohort. RT-qPCR validated the overexpression of selected genes. In MeDALL, 27 genes were differentially expressed in rhinitis alone, but none was significant for asthma or dermatitis alone. The multimorbidity signature was enriched in eosinophil-associated immune response and signal transduction. Protein-protein interaction network analysis identified IL5/JAK/STAT and IL33/ST2/IRAK/TRAF as key signaling pathways in multimorbid diseases. Synergistic effect of multimorbidity on gene expression levels was found.
CONCLUSION
A signature of eight genes identifies multimorbidity for asthma, rhinitis, and dermatitis. Our results have clinical and mechanistic implications, and suggest that multimorbidity should be considered differently than allergic diseases occurring alone.

Identifiants

pubmed: 32277847
doi: 10.1111/all.14314
pmc: PMC9302020
mid: NIHMS1821821
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

3248-3260

Subventions

Organisme : NHLBI NIH HHS
ID : R01 HL117191
Pays : United States
Organisme : NIH HHS
ID : MD011764
Pays : United States
Organisme : NIMHD NIH HHS
ID : U54 MD007587
Pays : United States
Organisme : NIH HHS
ID : U54MD007587
Pays : United States
Organisme : NIMHD NIH HHS
ID : R01 MD011764
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL079966
Pays : United States

Informations de copyright

© 2020 EAACI and John Wiley and Sons A/S. Published by John Wiley and Sons Ltd.

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Auteurs

Nathanaël Lemonnier (N)

Institute for Advanced Biosciences, UGA-INSERM U1209-CNRS UMR5309, Allée des Alpes, France.

Erik Melén (E)

Department of Clinical Science and Education Södersjukhuset, Karolinska Institutet, Sachs' Children's Hospital, Stockholm, Sweden.
Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden.

Yale Jiang (Y)

Division of Pediatric Pulmonary Medicine, UPMC Children's Hospital of Pittsburgh, University of Pittsburgh, Pittsburgh, PA, USA.
School of Medicine, Tsinghua University, Beijing, China.

Stéphane Joly (S)

CIRI, International Center for Infectiology Research, Inserm, Lyon, France.

Camille Ménard (C)

CIRI, International Center for Infectiology Research, Inserm, Lyon, France.

Daniel Aguilar (D)

Biomedical Research Networking Center in Hepatic and Digestive Diseases (CIBEREHD), Barcelona, Spain.

Edna Acosta-Perez (E)

Behavioral Sciences Research Institute, University of Puerto Rico, San Juan, Puerto Rico.

Anna Bergström (A)

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

Nadia Boutaoui (N)

Division of Pediatric Pulmonary Medicine, UPMC Children's Hospital of Pittsburgh, University of Pittsburgh, Pittsburgh, PA, USA.

Mariona Bustamante (M)

ISGlobal, Barcelona Institute for Global Health, Barcelona, Spain.
Universitat Pompeu Fabra (UPF), Barcelona, Spain.
Instituto de Salud Carlos III, Spanish Consortium for Research on Epidemiology and Public Health (CIBERESP), Madrid, Spain.

Glorisa Canino (G)

Behavioral Sciences Research Institute, University of Puerto Rico, San Juan, Puerto Rico.

Erick Forno (E)

Division of Pediatric Pulmonary Medicine, UPMC Children's Hospital of Pittsburgh, University of Pittsburgh, Pittsburgh, PA, USA.

Juan Ramon González (J)

ISGlobal, Barcelona Institute for Global Health, Barcelona, Spain.

Judith Garcia-Aymerich (J)

ISGlobal, Barcelona Institute for Global Health, Barcelona, Spain.

Olena Gruzieva (O)

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

Stefano Guerra (S)

ISGlobal, Barcelona Institute for Global Health, Barcelona, Spain.
Asthma and Airway Disease Research Center, University of Arizona, Tucson, AZ, USA.

Joachim Heinrich (J)

Institute of Epidemiology, Helmholtz Zentrum München, German Research Center for Environmental Health, Munich, Germany.
Institute and Outpatient Clinic for Occupational, Social and Environmental Medicine, Inner City Clinic, University Hospital of Munich (LMU), Munich, Germany.

Inger Kull (I)

Department of Clinical Science and Education, Sodersjukhuset, Karolinska Institute, Stockholm, Sweden.

Jesús Ibarluzea Maurolagoitia (J)

Instituto de Salud Carlos III, Spanish Consortium for Research on Epidemiology and Public Health (CIBERESP), Madrid, Spain.
BIODONOSTIA, Instituto de Investigación Sanitaria, Donostia-San Sebastián, Spain.

Loreto Santa-Marina Rodriguez (L)

Instituto de Salud Carlos III, Spanish Consortium for Research on Epidemiology and Public Health (CIBERESP), Madrid, Spain.

Elisabeth Thiering (E)

Institute of Epidemiology, Helmholtz Zentrum München, German Research Center for Environmental Health, Munich, Germany.
Division of Metabolic Diseases and Nutritional Medicine, Dr. von Hauner Children's Hospital, Ludwig-Maximilians-University of Munich, Munich, Germany.

Magnus Wickman (M)

Centre for Clinical Research Sörmland, Uppsala University, Eskilstuna, Sweden.

Cezmi Akdis (C)

Swiss Institute of Allergy and Asthma Research (SIAF), University of Zurich, Davos, Switzerland.

Mübeccel Akdis (M)

Swiss Institute of Allergy and Asthma Research (SIAF), University of Zurich, Davos, Switzerland.

Wei Chen (W)

Division of Pediatric Pulmonary Medicine, UPMC Children's Hospital of Pittsburgh, University of Pittsburgh, Pittsburgh, PA, USA.
Department of Biostatistics, University of Pittsburgh, Pittsburgh, PA, USA.

Thomas Keil (T)

Institute of Social Medicine, Epidemiology and Health Economics, Charité - Universitätsmedizin Berlin, Berlin, Germany.
Institute for Clinical Epidemiology and Biometry, University of Würzburg, Würzburg, Germany.
Institute for Health Resort Medicine and Health Promotion, Bavarian Health and Food Safety Authority, Bad Kissingen, Germany.

Gerard H Koppelman (GH)

Department of Pediatric Pulmonology and Pediatric Allergology, 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.

Valérie Siroux (V)

Institute for Advanced Biosciences, UGA-INSERM U1209-CNRS UMR5309, Allée des Alpes, France.

Cheng-Jian Xu (CJ)

Department of Pediatric Pulmonology and Pediatric Allergology, 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.

Pierre Hainaut (P)

Institute for Advanced Biosciences, UGA-INSERM U1209-CNRS UMR5309, Allée des Alpes, France.

Marie Standl (M)

Institute of Epidemiology, Helmholtz Zentrum München, German Research Center for Environmental Health, Munich, Germany.

Jordi Sunyer (J)

ISGlobal, Barcelona Institute for Global Health, Barcelona, Spain.

Juan C Celedón (JC)

Division of Pediatric Pulmonary Medicine, UPMC Children's Hospital of Pittsburgh, University of Pittsburgh, Pittsburgh, PA, USA.

Josep Maria Antó (J)

ISGlobal, Barcelona Institute for Global Health, Barcelona, Spain.

Jean Bousquet (J)

MACVIA-France, Fondation partenariale FMC VIA-LR, Montpellier, France.
Ageing and Chronic Diseases, Epidemiological and Public Health Approaches, Université Versailles St-Quentin-en-Yvelines, UMR-S 1168, Montigny le Bretonneux, France.
Euforea, Brussels, Belgium.
Department of Dermatology and Allergy, Charité - Universitätsmedizin Berlin, Comprehensive Allergy Center, Berlin, Germany.

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