NOX2 deficiency enhances priming and activation of the NLRP3 inflammasome.

K(+) efflux NLRP3 NOX2 gasdermin D mitochondrial damage reactive oxygen species

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:
05 Oct 2023
Historique:
received: 22 06 2023
revised: 18 08 2023
accepted: 15 09 2023
pubmed: 8 10 2023
medline: 8 10 2023
entrez: 7 10 2023
Statut: aheadofprint

Résumé

Nicotinamide adenine dinucleotide phosphate oxidase complex 2 (NOX2) deficiency, or chronic granulomatous disease (CGD), is an inborn error of immunity associated with increased susceptibility to infection and inflammatory manifestations. The pathophysiologic mechanism leading to the increased inflammatory response in CGD remains elusive. We investigated the pathophysiologic mechanisms leading to NOD-like receptor family pyrin domain containing 3 (NLRP3) inflammasome activation in NOX2 deficiency. We used NOX2-deficient human primary and CRISPR-engineered macrophages to show that NOX2 deficiency enhances the inflammatory response mainly by modulating the 2 steps of NLRP3 inflammasome activation: its transcriptional priming and its posttranslational triggering. At the transcriptional level, NOX2-deficient phagocytes display increased priming of the NLRP3 inflammasome, as evidenced by increased transcription of NLRP3 and IL-1β through an IL-1β-dependent stimulation of the nuclear factor kappa-light-chain enhancer of activated B cells (aka NF-κB) pathway. At the posttranslational level, the absence of NOX2 triggers the NLRP3 inflammasome activation by increased K Our results unveil the role of NOX2 as a repressor of the inflammatory response at both transcriptional and posttranslational levels and pave the way for a more targeted approach to treating CGD patients with inflammatory manifestations.

Sections du résumé

BACKGROUND BACKGROUND
Nicotinamide adenine dinucleotide phosphate oxidase complex 2 (NOX2) deficiency, or chronic granulomatous disease (CGD), is an inborn error of immunity associated with increased susceptibility to infection and inflammatory manifestations. The pathophysiologic mechanism leading to the increased inflammatory response in CGD remains elusive.
OBJECTIVE OBJECTIVE
We investigated the pathophysiologic mechanisms leading to NOD-like receptor family pyrin domain containing 3 (NLRP3) inflammasome activation in NOX2 deficiency.
METHODS METHODS
We used NOX2-deficient human primary and CRISPR-engineered macrophages to show that NOX2 deficiency enhances the inflammatory response mainly by modulating the 2 steps of NLRP3 inflammasome activation: its transcriptional priming and its posttranslational triggering.
RESULTS RESULTS
At the transcriptional level, NOX2-deficient phagocytes display increased priming of the NLRP3 inflammasome, as evidenced by increased transcription of NLRP3 and IL-1β through an IL-1β-dependent stimulation of the nuclear factor kappa-light-chain enhancer of activated B cells (aka NF-κB) pathway. At the posttranslational level, the absence of NOX2 triggers the NLRP3 inflammasome activation by increased K
CONCLUSION CONCLUSIONS
Our results unveil the role of NOX2 as a repressor of the inflammatory response at both transcriptional and posttranslational levels and pave the way for a more targeted approach to treating CGD patients with inflammatory manifestations.

Identifiants

pubmed: 37805023
pii: S0091-6749(23)01242-3
doi: 10.1016/j.jaci.2023.09.030
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

Copyright © 2023 American Academy of Allergy, Asthma & Immunology. Published by Elsevier Inc. All rights reserved.

Auteurs

Blandine Monjarret (B)

CHU Sainte-Justine Research Center, Montreal, Quebec, Canada.

Sara Shour (S)

CHU Sainte-Justine Research Center, Montreal, Quebec, Canada.

Aissa Benyoucef (A)

CHU Sainte-Justine Research Center, Montreal, Quebec, Canada.

Emilie Heckel (E)

CHU Sainte-Justine Research Center, Montreal, Quebec, Canada.

Lorie Marchitto (L)

CHU Sainte-Justine Research Center, Montreal, Quebec, Canada.

Jennifer W Leiding (JW)

Pediatric Infectious Disease and Immunology Arnold Palmer Hospital for Children at Orlando Health, Orlando, Fla; Department of Pediatrics, Division of Allergy and Immunology, Johns Hopkins University, Baltimore, Md.

Guilhem Cros (G)

Centre Hospitalier de l'Université de Montréal, Université de Montréal, Montreal, Quebec, Canada.

Isabel Fernandez (I)

Department of Microbiology, Infectiology and Immunology, Université de Montréal, Montreal, Quebec, Canada.

Jean-Sebastien Joyal (JS)

CHU Sainte-Justine Research Center, Montreal, Quebec, Canada; Department of Pathology and Cellular Biology, Faculty of Medicine, Université de Montréal, Montreal, Quebec, Canada; Department of Pediatrics, Faculty of Medicine, Université de Montréal, Montreal, Quebec, Canada.

Fabien Touzot (F)

CHU Sainte-Justine Research Center, Montreal, Quebec, Canada; Department of Microbiology, Infectiology and Immunology, Université de Montréal, Montreal, Quebec, Canada; Department of Pediatrics, Faculty of Medicine, Université de Montréal, Montreal, Quebec, Canada. Electronic address: fabien.touzot@umontreal.ca.

Classifications MeSH