A novel knock-in mouse model of cryopyrin-associated periodic syndromes with development of amyloidosis: Therapeutic efficacy of proton pump inhibitors.


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:
01 2020
Historique:
received: 20 07 2018
revised: 18 04 2019
accepted: 07 05 2019
pubmed: 14 6 2019
medline: 28 7 2020
entrez: 14 6 2019
Statut: ppublish

Résumé

Cryopyrin-associated periodic syndromes (CAPS) are a group of autoinflammatory diseases linked to gain-of-function mutations in the NOD-like receptor family, pyrin domain containing 3 (NLRP3) gene, which cause uncontrolled IL-1β secretion. Proton pump inhibitors (PPIs), which are commonly used as inhibitors of gastric acid production, also have anti-inflammatory properties, protect mice from sepsis, and prevent IL-1β secretion by monocytes from patients with CAPS. We sought to develop a novel Nlrp3 knock-in (KI) mouse model of CAPS to study amyloidosis, a severe CAPS complication, and test novel therapeutic approaches. We generated KI mice by engineering the N475K mutation, which is associated with the CAPS phenotype, into the mouse Nlrp3 gene. KI and wild-type mice received PPIs or PBS intraperitoneally and were analyzed for survival, inflammation, cytokine secretion, and amyloidosis development. Mutant Nlrp3 KI mice displayed features that recapitulate the immunologic and clinical phenotype of CAPS. They showed systemic inflammation with high levels of serum proinflammatory cytokines, inflammatory infiltrates in various organs, and amyloid deposits in the spleen, liver, and kidneys. Toll-like receptor stimulated macrophages from KI mice secreted high levels of IL-1β, IL-18, and IL-1α but low amounts of IL-1 receptor antagonist. Treatment of KI mice with PPIs had a clear clinical effect, showing a reduction in inflammatory manifestations, regression of amyloid deposits, and normalization of proinflammatory and anti-inflammatory cytokine production by macrophages. Nlrp3 KI mice displayed a CAPS phenotype with many characteristics of autoinflammation, including amyloidosis. The therapeutic effectiveness of PPIs associated with a lack of toxicity indicates that these drugs could represent relevant adjuvants to the anti-IL-1 drugs in patients with CAPS and other IL-1-driven diseases.

Sections du résumé

BACKGROUND
Cryopyrin-associated periodic syndromes (CAPS) are a group of autoinflammatory diseases linked to gain-of-function mutations in the NOD-like receptor family, pyrin domain containing 3 (NLRP3) gene, which cause uncontrolled IL-1β secretion. Proton pump inhibitors (PPIs), which are commonly used as inhibitors of gastric acid production, also have anti-inflammatory properties, protect mice from sepsis, and prevent IL-1β secretion by monocytes from patients with CAPS.
OBJECTIVE
We sought to develop a novel Nlrp3 knock-in (KI) mouse model of CAPS to study amyloidosis, a severe CAPS complication, and test novel therapeutic approaches.
METHODS
We generated KI mice by engineering the N475K mutation, which is associated with the CAPS phenotype, into the mouse Nlrp3 gene. KI and wild-type mice received PPIs or PBS intraperitoneally and were analyzed for survival, inflammation, cytokine secretion, and amyloidosis development.
RESULTS
Mutant Nlrp3 KI mice displayed features that recapitulate the immunologic and clinical phenotype of CAPS. They showed systemic inflammation with high levels of serum proinflammatory cytokines, inflammatory infiltrates in various organs, and amyloid deposits in the spleen, liver, and kidneys. Toll-like receptor stimulated macrophages from KI mice secreted high levels of IL-1β, IL-18, and IL-1α but low amounts of IL-1 receptor antagonist. Treatment of KI mice with PPIs had a clear clinical effect, showing a reduction in inflammatory manifestations, regression of amyloid deposits, and normalization of proinflammatory and anti-inflammatory cytokine production by macrophages.
CONCLUSION
Nlrp3 KI mice displayed a CAPS phenotype with many characteristics of autoinflammation, including amyloidosis. The therapeutic effectiveness of PPIs associated with a lack of toxicity indicates that these drugs could represent relevant adjuvants to the anti-IL-1 drugs in patients with CAPS and other IL-1-driven diseases.

Identifiants

pubmed: 31194989
pii: S0091-6749(19)30757-2
doi: 10.1016/j.jaci.2019.05.034
pii:
doi:

Substances chimiques

IL1B protein, mouse 0
Interleukin-1beta 0
NLR Family, Pyrin Domain-Containing 3 Protein 0
Nlrp3 protein, mouse 0
Proton Pump Inhibitors 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

368-378.e13

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2019 American Academy of Allergy, Asthma & Immunology. Published by Elsevier Inc. All rights reserved.

Auteurs

Arinna Bertoni (A)

UOSD Centro Malattie Autoinfiammatorie ed Immunodeficienze, IRCCS Istituto G. Gaslini, Genova, Italy.

Sonia Carta (S)

Unità di Biologia Cellulare, IRCCS Ospedale Policlinico San Martino, Genova, Italy.

Chiara Baldovini (C)

Anatomia Patologica, IRCCS Istituto G. Gaslini, Genova, Italy.

Federica Penco (F)

UOSD Centro Malattie Autoinfiammatorie ed Immunodeficienze, IRCCS Istituto G. Gaslini, Genova, Italy.

Enrica Balza (E)

Unità di Biologia Cellulare, IRCCS Ospedale Policlinico San Martino, Genova, Italy.

Silvia Borghini (S)

Genetica Medica, IRCCS Istituto G. Gaslini, Genova, Italy.

Marco Di Duca (M)

Laboratorio di Fisiopatologia dell' Uremia, IRCCS Istituto G. Gaslini, Genova, Italy.

Emanuela Ognio (E)

S.S Animal Facility, IRCCS Ospedale Policlinico San Martino, Genova, Italy.

Alessio Signori (A)

Dipartimento di Scienze della Salute, Sezione di Biostatistica, DISSAL, Università degli studi di Genova, Genova, Italy.

Paolo Nozza (P)

Anatomia Patologica, IRCCS Istituto G. Gaslini, Genova, Italy.

Francesca Schena (F)

UOSD Centro Malattie Autoinfiammatorie ed Immunodeficienze, IRCCS Istituto G. Gaslini, Genova, Italy.

Patrizia Castellani (P)

Unità di Biologia Cellulare, IRCCS Ospedale Policlinico San Martino, Genova, Italy.

Claudia Pastorino (C)

UOSD Centro Malattie Autoinfiammatorie ed Immunodeficienze, IRCCS Istituto G. Gaslini, Genova, Italy.

Carola Perrone (C)

UOSD Centro Malattie Autoinfiammatorie ed Immunodeficienze, IRCCS Istituto G. Gaslini, Genova, Italy.

Laura Obici (L)

Centro per lo Studio e la Cura delle Amiloidosi Sistemiche, Fondazione IRCCS Policlinico San Matteo, Pavia, Italy.

Alberto Martini (A)

Direzione Scientifica, IRCCS Istituto G. Gaslini, Genova, Italy.

Isabella Ceccherini (I)

Genetica Medica, IRCCS Istituto G. Gaslini, Genova, Italy.

Marco Gattorno (M)

UOSD Centro Malattie Autoinfiammatorie ed Immunodeficienze, IRCCS Istituto G. Gaslini, Genova, Italy; UOC Clinica Pediatrica e Reumatologica, IRCCS Istituto G. Gaslini, Genova, Italy. Electronic address: marcogattorno@gaslini.org.

Anna Rubartelli (A)

Unità di Biologia Cellulare, IRCCS Ospedale Policlinico San Martino, Genova, Italy.

Sabrina Chiesa (S)

UOSD Centro Malattie Autoinfiammatorie ed Immunodeficienze, IRCCS Istituto G. Gaslini, Genova, Italy. Electronic address: sabrinachiesa@gaslini.org.

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Classifications MeSH