Caspase-1-driven neutrophil pyroptosis and its role in host susceptibility to Pseudomonas aeruginosa.


Journal

PLoS pathogens
ISSN: 1553-7374
Titre abrégé: PLoS Pathog
Pays: United States
ID NLM: 101238921

Informations de publication

Date de publication:
07 2022
Historique:
received: 27 01 2022
accepted: 01 06 2022
revised: 02 08 2022
pubmed: 19 7 2022
medline: 5 8 2022
entrez: 18 7 2022
Statut: epublish

Résumé

Multiple regulated neutrophil cell death programs contribute to host defense against infections. However, despite expressing all necessary inflammasome components, neutrophils are thought to be generally defective in Caspase-1-dependent pyroptosis. By screening different bacterial species, we found that several Pseudomonas aeruginosa (P. aeruginosa) strains trigger Caspase-1-dependent pyroptosis in human and murine neutrophils. Notably, deletion of Exotoxins U or S in P. aeruginosa enhanced neutrophil death to Caspase-1-dependent pyroptosis, suggesting that these exotoxins interfere with this pathway. Mechanistically, P. aeruginosa Flagellin activates the NLRC4 inflammasome, which supports Caspase-1-driven interleukin (IL)-1β secretion and Gasdermin D (GSDMD)-dependent neutrophil pyroptosis. Furthermore, P. aeruginosa-induced GSDMD activation triggers Calcium-dependent and Peptidyl Arginine Deaminase-4-driven histone citrullination and translocation of neutrophil DNA into the cell cytosol without inducing extracellular Neutrophil Extracellular Traps. Finally, we show that neutrophil Caspase-1 contributes to IL-1β production and susceptibility to pyroptosis-inducing P. aeruginosa strains in vivo. Overall, we demonstrate that neutrophils are not universally resistant for Caspase-1-dependent pyroptosis.

Identifiants

pubmed: 35849616
doi: 10.1371/journal.ppat.1010305
pii: PPATHOGENS-D-22-00169
pmc: PMC9345480
doi:

Substances chimiques

Apoptosis Regulatory Proteins 0
Exotoxins 0
Inflammasomes 0
Interleukin-1beta 0
Caspase 1 EC 3.4.22.36

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

e1010305

Subventions

Organisme : NIAMS NIH HHS
ID : P30 AR073752
Pays : United States

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

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Auteurs

Karin Santoni (K)

Institute of Pharmacology and Structural Biology (IPBS), University of Toulouse, CNRS, Toulouse, France.

David Pericat (D)

Institute of Pharmacology and Structural Biology (IPBS), University of Toulouse, CNRS, Toulouse, France.

Leana Gorse (L)

Institute of Pharmacology and Structural Biology (IPBS), University of Toulouse, CNRS, Toulouse, France.

Julien Buyck (J)

UFR Medicine and Pharmacy, INSERM U1070, University of Poitiers, Poitiers, France.

Miriam Pinilla (M)

Institute of Pharmacology and Structural Biology (IPBS), University of Toulouse, CNRS, Toulouse, France.

Laure Prouvensier (L)

UFR Medicine and Pharmacy, INSERM U1070, University of Poitiers, Poitiers, France.

Salimata Bagayoko (S)

Institute of Pharmacology and Structural Biology (IPBS), University of Toulouse, CNRS, Toulouse, France.

Audrey Hessel (A)

Institute of Pharmacology and Structural Biology (IPBS), University of Toulouse, CNRS, Toulouse, France.

Stephen Adonai Leon-Icaza (SA)

Institute of Pharmacology and Structural Biology (IPBS), University of Toulouse, CNRS, Toulouse, France.

Elisabeth Bellard (E)

Institute of Pharmacology and Structural Biology (IPBS), University of Toulouse, CNRS, Toulouse, France.

Serge Mazères (S)

Institute of Pharmacology and Structural Biology (IPBS), University of Toulouse, CNRS, Toulouse, France.

Emilie Doz-Deblauwe (E)

INRAE, Université de Tours, ISP, Nouzilly, France.

Nathalie Winter (N)

INRAE, Université de Tours, ISP, Nouzilly, France.

Christophe Paget (C)

Institut national de la santé et de la recherche médicale, Centre d'Etude des Pathologies Respiratoires, UMR 1100, Tours, France.

Jean-Philippe Girard (JP)

Institute of Pharmacology and Structural Biology (IPBS), University of Toulouse, CNRS, Toulouse, France.

Christine T N Pham (CTN)

Division of Rheumatology, Department of Internal Medicine, Washington University School of Medicine, Saint Louis, Missouri, United States of America.

Céline Cougoule (C)

Institute of Pharmacology and Structural Biology (IPBS), University of Toulouse, CNRS, Toulouse, France.

Renaud Poincloux (R)

Institute of Pharmacology and Structural Biology (IPBS), University of Toulouse, CNRS, Toulouse, France.

Mohamed Lamkanfi (M)

Department of Internal Medicine and Pediatrics, Ghent University, Ghent, Belgium.

Emma Lefrançais (E)

Institute of Pharmacology and Structural Biology (IPBS), University of Toulouse, CNRS, Toulouse, France.

Etienne Meunier (E)

Institute of Pharmacology and Structural Biology (IPBS), University of Toulouse, CNRS, Toulouse, France.

Rémi Planès (R)

Institute of Pharmacology and Structural Biology (IPBS), University of Toulouse, CNRS, Toulouse, France.

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