Respiratory virome profiles reflect antiviral immune responses.


Journal

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

Informations de publication

Date de publication:
05 2023
Historique:
revised: 01 12 2022
received: 02 08 2022
accepted: 11 12 2022
medline: 2 5 2023
pubmed: 4 1 2023
entrez: 3 1 2023
Statut: ppublish

Résumé

From early life, respiratory viruses are implicated in the development, exacerbation and persistence of respiratory conditions such as asthma. Complex dynamics between microbial communities and host immune responses shape immune maturation and homeostasis, influencing health outcomes. We evaluated the hypothesis that the respiratory virome is linked to systemic immune responses, using peripheral blood and nasopharyngeal swab samples from preschool-age children in the PreDicta cohort. Peripheral blood mononuclear cells from 51 children (32 asthmatics and 19 healthy controls) participating in the 2-year multinational PreDicta cohort were cultured with bacterial (Bacterial-DNA, LPS) or viral (R848, Poly:IC, RV) stimuli. Supernatants were analysed by Luminex for the presence of 22 relevant cytokines. Virome composition was obtained using untargeted high throughput sequencing of nasopharyngeal samples. The metagenomic data were used for the characterization of virome profiles and the presence of key viral families (Picornaviridae, Anelloviridae, Siphoviridae). These were correlated to cytokine secretion patterns, identified through hierarchical clustering and principal component analysis. High spontaneous cytokine release was associated with increased presence of Prokaryotic virome profiles and reduced presence of Eukaryotic and Anellovirus profiles. Antibacterial responses did not correlate with specific viral families or virome profile; however, low antiviral responders had more Prokaryotic and less Eukaryotic virome profiles. Anelloviruses and Anellovirus-dominated profiles were equally distributed among immune response clusters. The presence of Picornaviridae and Siphoviridae was associated with low interferon-λ responses. Asthma or allergy did not modify these correlations. Antiviral cytokine responses at a systemic level reflect the upper airway virome composition. Individuals with low innate interferon responses have higher abundance of Picornaviruses (mostly Rhinoviruses) and bacteriophages. Bacteriophages, particularly Siphoviridae, appear to be sensitive sensors of host antimicrobial capacity, while Anelloviruses are not correlated with TLR-induced immune responses.

Sections du résumé

BACKGROUND
From early life, respiratory viruses are implicated in the development, exacerbation and persistence of respiratory conditions such as asthma. Complex dynamics between microbial communities and host immune responses shape immune maturation and homeostasis, influencing health outcomes. We evaluated the hypothesis that the respiratory virome is linked to systemic immune responses, using peripheral blood and nasopharyngeal swab samples from preschool-age children in the PreDicta cohort.
METHODS
Peripheral blood mononuclear cells from 51 children (32 asthmatics and 19 healthy controls) participating in the 2-year multinational PreDicta cohort were cultured with bacterial (Bacterial-DNA, LPS) or viral (R848, Poly:IC, RV) stimuli. Supernatants were analysed by Luminex for the presence of 22 relevant cytokines. Virome composition was obtained using untargeted high throughput sequencing of nasopharyngeal samples. The metagenomic data were used for the characterization of virome profiles and the presence of key viral families (Picornaviridae, Anelloviridae, Siphoviridae). These were correlated to cytokine secretion patterns, identified through hierarchical clustering and principal component analysis.
RESULTS
High spontaneous cytokine release was associated with increased presence of Prokaryotic virome profiles and reduced presence of Eukaryotic and Anellovirus profiles. Antibacterial responses did not correlate with specific viral families or virome profile; however, low antiviral responders had more Prokaryotic and less Eukaryotic virome profiles. Anelloviruses and Anellovirus-dominated profiles were equally distributed among immune response clusters. The presence of Picornaviridae and Siphoviridae was associated with low interferon-λ responses. Asthma or allergy did not modify these correlations.
CONCLUSION
Antiviral cytokine responses at a systemic level reflect the upper airway virome composition. Individuals with low innate interferon responses have higher abundance of Picornaviruses (mostly Rhinoviruses) and bacteriophages. Bacteriophages, particularly Siphoviridae, appear to be sensitive sensors of host antimicrobial capacity, while Anelloviruses are not correlated with TLR-induced immune responses.

Identifiants

pubmed: 36595290
doi: 10.1111/all.15634
doi:

Substances chimiques

Antiviral Agents 0
Interferons 9008-11-1

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

1258-1268

Informations de copyright

© 2023 The Authors. Allergy published by European Academy of Allergy and Clinical Immunology and John Wiley & Sons Ltd.

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Auteurs

Judit Rovira Rubió (J)

Division of Infection, Immunity & Respiratory Medicine, University of Manchester, Manchester, UK.

Spyridon Megremis (S)

Division of Infection, Immunity & Respiratory Medicine, University of Manchester, Manchester, UK.

Maria Pasioti (M)

Allergy Department, 2nd Pediatric Clinic, National and Kapodistrian University of Athens, Athens, Greece.

John Lakoumentas (J)

Allergy Department, 2nd Pediatric Clinic, National and Kapodistrian University of Athens, Athens, Greece.

Bede Constantinides (B)

Nuffield Department of Medicine, John Radcliffe Hospital, University of Oxford, Oxford, UK.

Paraskevi Xepapadaki (P)

Allergy Department, 2nd Pediatric Clinic, National and Kapodistrian University of Athens, Athens, Greece.

Claus Bachert (C)

Upper Airway Research Laboratory, Ghent University Hospital, Ghent, Belgium.

Susetta Finotto (S)

Department of Molecular Pneumology, Friedrich-Alexander-Universität (FAU) Erlangen-Nürnberg, Universitätsklinikum Erlangen, Erlangen, Germany.

Tuomas Jartti (T)

PEDEGO Research Unit, University of Oulu, Oulu, Finland.
Department of Pediatrics and Adolescent Medicine, University of Oulu, Oulu, Finland.
Department of Pediatrics and Adolescent Medicine, Turku University Hospital and University of Turku, Turku, Finland.

Evangelos Andreakos (E)

Biomedical Research Foundation of the Academy of Athens, Athens, Greece.

Barbara Stanic (B)

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

Cezmi A Akdis (CA)

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

Mübeccel Akdis (M)

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

Nikolaos G Papadopoulos (NG)

Division of Infection, Immunity & Respiratory Medicine, University of Manchester, Manchester, UK.
Allergy Department, 2nd Pediatric Clinic, National and Kapodistrian University of Athens, Athens, Greece.

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