Danger signals released during cold ischemia storage activate NLRP3 inflammasome in myeloid cells and influence early allograft function in liver transplantation.


Journal

EBioMedicine
ISSN: 2352-3964
Titre abrégé: EBioMedicine
Pays: Netherlands
ID NLM: 101647039

Informations de publication

Date de publication:
Jan 2023
Historique:
received: 14 07 2022
revised: 04 11 2022
accepted: 01 12 2022
pubmed: 22 12 2022
medline: 21 1 2023
entrez: 21 12 2022
Statut: ppublish

Résumé

Innate immunity plays a fundamental role in solid organ transplantation. Myeloid cells can sense danger signals or DAMPs released after tissue or cell damage, such as during ischemia processes. This study aimed to identify DAMPs released during cold ischemia storage of human liver and analyze their ability to activate the inflammasome in myeloid cells and the possible implications in terms of short-term outcomes of liver transplantation. 79 samples of organ preservation solution (OPS) from 79 deceased donors were collected after cold static storage. We used different analytical methods to measure DAMPs in these end-ischemic OPS (eiOPS) samples. We also used eiOPS in the human macrophage THP-1 cell line and primary monocyte cultures to study inflammasome activation. Different DAMPs were identified in eiOPS, several of which induced both priming and activation of the NLRP3 inflammasome in human myeloid cells. Cold ischemia time and donation after circulatory death negatively influenced the DAMP signature. Moreover, the presence of oligomeric inflammasomes and interleukin-18 in eiOPS correlated with early allograft dysfunction in liver transplant patients. DAMPs released during cold ischemia storage prime and activate the NLRP3 inflammasome in liver macrophages after transplantation, inducing a pro-inflammatory environment that will complicate the outcome of the graft. The use of pharmacological blockers targeting DAMPs or the NLRP3 inflammasome in liver ischemia during static cold storage or through extracorporeal organ support could be a suitable strategy to increase the success of liver transplantation. Fundación Mutua Madrileña and Instituto de Salud Carlos III, Madrid, Spain.

Sections du résumé

BACKGROUND BACKGROUND
Innate immunity plays a fundamental role in solid organ transplantation. Myeloid cells can sense danger signals or DAMPs released after tissue or cell damage, such as during ischemia processes. This study aimed to identify DAMPs released during cold ischemia storage of human liver and analyze their ability to activate the inflammasome in myeloid cells and the possible implications in terms of short-term outcomes of liver transplantation.
METHODS METHODS
79 samples of organ preservation solution (OPS) from 79 deceased donors were collected after cold static storage. We used different analytical methods to measure DAMPs in these end-ischemic OPS (eiOPS) samples. We also used eiOPS in the human macrophage THP-1 cell line and primary monocyte cultures to study inflammasome activation.
FINDINGS RESULTS
Different DAMPs were identified in eiOPS, several of which induced both priming and activation of the NLRP3 inflammasome in human myeloid cells. Cold ischemia time and donation after circulatory death negatively influenced the DAMP signature. Moreover, the presence of oligomeric inflammasomes and interleukin-18 in eiOPS correlated with early allograft dysfunction in liver transplant patients.
INTERPRETATION CONCLUSIONS
DAMPs released during cold ischemia storage prime and activate the NLRP3 inflammasome in liver macrophages after transplantation, inducing a pro-inflammatory environment that will complicate the outcome of the graft. The use of pharmacological blockers targeting DAMPs or the NLRP3 inflammasome in liver ischemia during static cold storage or through extracorporeal organ support could be a suitable strategy to increase the success of liver transplantation.
FUNDING BACKGROUND
Fundación Mutua Madrileña and Instituto de Salud Carlos III, Madrid, Spain.

Identifiants

pubmed: 36543018
pii: S2352-3964(22)00601-6
doi: 10.1016/j.ebiom.2022.104419
pmc: PMC9794897
pii:
doi:

Substances chimiques

Inflammasomes 0
NLR Family, Pyrin Domain-Containing 3 Protein 0
NLRP3 protein, human 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

104419

Informations de copyright

Copyright © 2022 The Author(s). Published by Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests P.P. is scientific consultant of Glenmak Ltd, FirstThought, Donation and Transplantation Institute and Viva in vitro diagnostics. P.P. is co-inventor on patent application to use NLRP3 inflammasome as biomarker of disease, which have been licensed to Viva in vitro diagnostics S.L, a company co-funded by P.P., A.B.-M. and L.M-A. A.B-M. is co-inventor on provisional patent application of an in vitro method for predicting organ transplant rejection, but declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The rest of authors declare no competing interests.

Auteurs

Fernando Lucas-Ruiz (F)

Molecular Inflammation Group, University Clinical Hospital Virgen de la Arrixaca, Biomedical Research Institute of Murcia (IMIB-Pascual Parrilla), 30120, Murcia, Spain.

Sandra V Mateo (SV)

Molecular Inflammation Group, University Clinical Hospital Virgen de la Arrixaca, Biomedical Research Institute of Murcia (IMIB-Pascual Parrilla), 30120, Murcia, Spain.

Marta Jover-Aguilar (M)

Transplant Unit, Surgery Service, University Clinical Hospital Virgen de la Arrixaca, Murcia, Spain; Biomedical Research Institute of Murcia IMIB-Pascual Parrilla, Murcia, Spain.

Felipe Alconchel (F)

Transplant Unit, Surgery Service, University Clinical Hospital Virgen de la Arrixaca, Murcia, Spain; Biomedical Research Institute of Murcia IMIB-Pascual Parrilla, Murcia, Spain.

Laura Martínez-Alarcón (L)

Transplant Unit, Surgery Service, University Clinical Hospital Virgen de la Arrixaca, Murcia, Spain; Biomedical Research Institute of Murcia IMIB-Pascual Parrilla, Murcia, Spain.

Carlos de Torre-Minguela (C)

Molecular Inflammation Group, University Clinical Hospital Virgen de la Arrixaca, Biomedical Research Institute of Murcia (IMIB-Pascual Parrilla), 30120, Murcia, Spain.

Daniel Vidal-Correoso (D)

Molecular Inflammation Group, University Clinical Hospital Virgen de la Arrixaca, Biomedical Research Institute of Murcia (IMIB-Pascual Parrilla), 30120, Murcia, Spain.

Francisco Villalba-López (F)

Molecular Inflammation Group, University Clinical Hospital Virgen de la Arrixaca, Biomedical Research Institute of Murcia (IMIB-Pascual Parrilla), 30120, Murcia, Spain.

Víctor López-López (V)

Transplant Unit, Surgery Service, University Clinical Hospital Virgen de la Arrixaca, Murcia, Spain; Biomedical Research Institute of Murcia IMIB-Pascual Parrilla, Murcia, Spain.

Antonio Ríos-Zambudio (A)

Transplant Unit, Surgery Service, University Clinical Hospital Virgen de la Arrixaca, Murcia, Spain; Biomedical Research Institute of Murcia IMIB-Pascual Parrilla, Murcia, Spain.

José A Pons (JA)

Liver Transplantation Unit, Gastroenterology and Hepatology Service, University Clinical Hospital Virgen de la Arrixaca, Biomedical Research Institute of Murcia (IMIB-Pascual Parrilla), 30120, Murcia, Spain.

Pablo Ramírez (P)

Transplant Unit, Surgery Service, University Clinical Hospital Virgen de la Arrixaca, Murcia, Spain; Biomedical Research Institute of Murcia IMIB-Pascual Parrilla, Murcia, Spain.

Pablo Pelegrín (P)

Molecular Inflammation Group, University Clinical Hospital Virgen de la Arrixaca, Biomedical Research Institute of Murcia (IMIB-Pascual Parrilla), 30120, Murcia, Spain; Department of Biochemistry and Molecular Biology B and Immunology, Faculty of Medicine, University of Murcia, 30120, Murcia, Spain. Electronic address: pablo.pelegrin@imib.es.

Alberto Baroja-Mazo (A)

Molecular Inflammation Group, University Clinical Hospital Virgen de la Arrixaca, Biomedical Research Institute of Murcia (IMIB-Pascual Parrilla), 30120, Murcia, Spain. Electronic address: alberto.baroja@ffis.es.

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