NOD1 sensing of house dust mite-derived microbiota promotes allergic experimental asthma.


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:
08 2021
Historique:
received: 01 07 2020
revised: 27 10 2020
accepted: 28 12 2020
pubmed: 29 1 2021
medline: 21 10 2021
entrez: 28 1 2021
Statut: ppublish

Résumé

Asthma severity has been linked to exposure to gram-negative bacteria from the environment that are recognized by NOD1 receptor and are present in house dust mite (HDM) extracts. NOD1 polymorphism has been associated with asthma. We sought to evaluate whether either host or HDM-derived microbiota may contribute to NOD1-dependent disease severity. A model of HDM-induced experimental asthma was used and the effect of NOD1 deficiency was evaluated. Contribution of host microbiota was evaluated by fecal transplantation. Contribution of HDM-derived microbiota was assessed by 16S ribosomal RNA sequencing, mass spectrometry analysis, and peptidoglycan depletion of the extracts. In this model, loss of the bacterial sensor NOD1 and its adaptor RIPK2 improved asthma features. Such inhibitory effect was not related to dysbiosis caused by NOD1 deficiency, as shown by fecal transplantation of Nod1-deficient microbiota to wild-type germ-free mice. The 16S ribosomal RNA gene sequencing and mass spectrometry analysis of HDM allergen, revealed the presence of some muropeptides from gram-negative bacteria that belong to the Bartonellaceae family. While such HDM-associated muropeptides were found to activate NOD1 signaling in epithelial cells, peptidoglycan-depleted HDM had a decreased ability to instigate asthma in vivo. These data show that NOD1-dependent sensing of HDM-associated gram-negative bacteria aggravates the severity of experimental asthma, suggesting that inhibiting the NOD1 signaling pathway may be a therapeutic approach to treating asthma.

Sections du résumé

BACKGROUND
Asthma severity has been linked to exposure to gram-negative bacteria from the environment that are recognized by NOD1 receptor and are present in house dust mite (HDM) extracts. NOD1 polymorphism has been associated with asthma.
OBJECTIVE
We sought to evaluate whether either host or HDM-derived microbiota may contribute to NOD1-dependent disease severity.
METHODS
A model of HDM-induced experimental asthma was used and the effect of NOD1 deficiency was evaluated. Contribution of host microbiota was evaluated by fecal transplantation. Contribution of HDM-derived microbiota was assessed by 16S ribosomal RNA sequencing, mass spectrometry analysis, and peptidoglycan depletion of the extracts.
RESULTS
In this model, loss of the bacterial sensor NOD1 and its adaptor RIPK2 improved asthma features. Such inhibitory effect was not related to dysbiosis caused by NOD1 deficiency, as shown by fecal transplantation of Nod1-deficient microbiota to wild-type germ-free mice. The 16S ribosomal RNA gene sequencing and mass spectrometry analysis of HDM allergen, revealed the presence of some muropeptides from gram-negative bacteria that belong to the Bartonellaceae family. While such HDM-associated muropeptides were found to activate NOD1 signaling in epithelial cells, peptidoglycan-depleted HDM had a decreased ability to instigate asthma in vivo.
CONCLUSIONS
These data show that NOD1-dependent sensing of HDM-associated gram-negative bacteria aggravates the severity of experimental asthma, suggesting that inhibiting the NOD1 signaling pathway may be a therapeutic approach to treating asthma.

Identifiants

pubmed: 33508265
pii: S0091-6749(21)00093-2
doi: 10.1016/j.jaci.2020.12.649
pii:
doi:

Substances chimiques

Nod1 Signaling Adaptor Protein 0
Nod1 protein, mouse 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

394-406

Informations de copyright

Copyright © 2021 American Academy of Allergy, Asthma & Immunology. Published by Elsevier Inc. All rights reserved.

Auteurs

Saliha Ait Yahia (S)

University of Lille, Centre National de la Recherche Scientifique (CNRS), Institut National de la Santé et de la Recherche Médicale, Centre Hospitalier Universitaire Lille, Institut Pasteur de Lille, U1019-Unite Mixte de Recherche (UMR) 9017-Centre d'Infection et d'Immunité de Lille, Lille, France.

Camille Audousset (C)

University of Lille, Centre National de la Recherche Scientifique (CNRS), Institut National de la Santé et de la Recherche Médicale, Centre Hospitalier Universitaire Lille, Institut Pasteur de Lille, U1019-Unite Mixte de Recherche (UMR) 9017-Centre d'Infection et d'Immunité de Lille, Lille, France.

Daniel Alvarez-Simon (D)

University of Lille, Centre National de la Recherche Scientifique (CNRS), Institut National de la Santé et de la Recherche Médicale, Centre Hospitalier Universitaire Lille, Institut Pasteur de Lille, U1019-Unite Mixte de Recherche (UMR) 9017-Centre d'Infection et d'Immunité de Lille, Lille, France.

Han Vorng (H)

University of Lille, Centre National de la Recherche Scientifique (CNRS), Institut National de la Santé et de la Recherche Médicale, Centre Hospitalier Universitaire Lille, Institut Pasteur de Lille, U1019-Unite Mixte de Recherche (UMR) 9017-Centre d'Infection et d'Immunité de Lille, Lille, France.

Dieudonnée Togbe (D)

Laboratory of Experimental and Molecular Immunology and Neurogenetics, UMR 7355 CNRS-Universitaire of Orléans, Orléans, France.

Philippe Marquillies (P)

University of Lille, Centre National de la Recherche Scientifique (CNRS), Institut National de la Santé et de la Recherche Médicale, Centre Hospitalier Universitaire Lille, Institut Pasteur de Lille, U1019-Unite Mixte de Recherche (UMR) 9017-Centre d'Infection et d'Immunité de Lille, Lille, France.

Myriam Delacre (M)

University of Lille, Centre National de la Recherche Scientifique (CNRS), Institut National de la Santé et de la Recherche Médicale, Centre Hospitalier Universitaire Lille, Institut Pasteur de Lille, U1019-Unite Mixte de Recherche (UMR) 9017-Centre d'Infection et d'Immunité de Lille, Lille, France.

Stéphanie Rose (S)

Laboratory of Experimental and Molecular Immunology and Neurogenetics, UMR 7355 CNRS-Universitaire of Orléans, Orléans, France.

Hélène Bouscayrol (H)

Laboratory of Experimental and Molecular Immunology and Neurogenetics, UMR 7355 CNRS-Universitaire of Orléans, Orléans, France.

Aline Rifflet (A)

Institut Pasteur, Unité Biologie et Génétique de la Paroi Bactérienne, Paris, France; CNRS, UMR 2001, Paris, France; Institut National de la Santé et de la Recherche Médicale, Équipe Avenir, Paris, France.

Valérie Quesniaux (V)

Laboratory of Experimental and Molecular Immunology and Neurogenetics, UMR 7355 CNRS-Universitaire of Orléans, Orléans, France.

Ivo Gomperts Boneca (IG)

Institut Pasteur, Unité Biologie et Génétique de la Paroi Bactérienne, Paris, France; CNRS, UMR 2001, Paris, France; Institut National de la Santé et de la Recherche Médicale, Équipe Avenir, Paris, France.

Mathias Chamaillard (M)

University of Lille, Centre National de la Recherche Scientifique (CNRS), Institut National de la Santé et de la Recherche Médicale, Centre Hospitalier Universitaire Lille, Institut Pasteur de Lille, U1019-Unite Mixte de Recherche (UMR) 9017-Centre d'Infection et d'Immunité de Lille, Lille, France.

Anne Tsicopoulos (A)

University of Lille, Centre National de la Recherche Scientifique (CNRS), Institut National de la Santé et de la Recherche Médicale, Centre Hospitalier Universitaire Lille, Institut Pasteur de Lille, U1019-Unite Mixte de Recherche (UMR) 9017-Centre d'Infection et d'Immunité de Lille, Lille, France. Electronic address: anne.tsicopoulos@pasteur-lille.fr.

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