Blood metabolomics uncovers inflammation-associated mitochondrial dysfunction as a potential mechanism underlying ACLF.


Journal

Journal of hepatology
ISSN: 1600-0641
Titre abrégé: J Hepatol
Pays: Netherlands
ID NLM: 8503886

Informations de publication

Date de publication:
04 2020
Historique:
received: 10 07 2019
revised: 29 10 2019
accepted: 11 11 2019
pubmed: 30 11 2019
medline: 7 10 2021
entrez: 29 11 2019
Statut: ppublish

Résumé

Acute-on-chronic liver failure (ACLF), which develops in patients with cirrhosis, is characterized by intense systemic inflammation and organ failure(s). Because systemic inflammation is energetically expensive, its metabolic costs may result in organ dysfunction/failure. Therefore, we aimed to analyze the blood metabolome in patients with cirrhosis, with and without ACLF. We performed untargeted metabolomics using liquid chromatography coupled to high-resolution mass spectrometry in serum from 650 patients with AD (acute decompensation of cirrhosis, without ACLF), 181 with ACLF, 43 with compensated cirrhosis, and 29 healthy individuals. Of the 137 annotated metabolites identified, 100 were increased in patients with ACLF of any grade, relative to those with AD, and 38 comprised a distinctive blood metabolite fingerprint for ACLF. Among patients with ACLF, the intensity of the fingerprint increased across ACLF grades, and was similar in patients with kidney failure and in those without, indicating that the fingerprint reflected not only decreased kidney excretion but also altered cell metabolism. The higher the ACLF-associated fingerprint intensity, the higher the plasma levels of inflammatory markers, tumor necrosis factor α, soluble CD206, and soluble CD163. ACLF was characterized by intense proteolysis and lipolysis; amino acid catabolism; extra-mitochondrial glucose metabolism through glycolysis, pentose phosphate, and D-glucuronate pathways; depressed mitochondrial ATP-producing fatty acid β-oxidation; and extra-mitochondrial amino acid metabolism giving rise to metabotoxins. In ACLF, intense systemic inflammation is associated with blood metabolite accumulation and profound alterations in major metabolic pathways, in particular inhibition of mitochondrial energy production, which may contribute to the development of organ failures. Acute-on-chronic liver failure (ACLF), which develops in patients with cirrhosis, is characterized by intense systemic inflammation and organ failure(s). Because systemic inflammation is energetically expensive, its metabolic costs may result in organ dysfunction/failure. We identified a 38-metabolite blood fingerprint specific for ACLF that revealed mitochondrial dysfunction in peripheral organs. This may contribute to organ failures.

Sections du résumé

BACKGROUND & AIMS
Acute-on-chronic liver failure (ACLF), which develops in patients with cirrhosis, is characterized by intense systemic inflammation and organ failure(s). Because systemic inflammation is energetically expensive, its metabolic costs may result in organ dysfunction/failure. Therefore, we aimed to analyze the blood metabolome in patients with cirrhosis, with and without ACLF.
METHODS
We performed untargeted metabolomics using liquid chromatography coupled to high-resolution mass spectrometry in serum from 650 patients with AD (acute decompensation of cirrhosis, without ACLF), 181 with ACLF, 43 with compensated cirrhosis, and 29 healthy individuals.
RESULTS
Of the 137 annotated metabolites identified, 100 were increased in patients with ACLF of any grade, relative to those with AD, and 38 comprised a distinctive blood metabolite fingerprint for ACLF. Among patients with ACLF, the intensity of the fingerprint increased across ACLF grades, and was similar in patients with kidney failure and in those without, indicating that the fingerprint reflected not only decreased kidney excretion but also altered cell metabolism. The higher the ACLF-associated fingerprint intensity, the higher the plasma levels of inflammatory markers, tumor necrosis factor α, soluble CD206, and soluble CD163. ACLF was characterized by intense proteolysis and lipolysis; amino acid catabolism; extra-mitochondrial glucose metabolism through glycolysis, pentose phosphate, and D-glucuronate pathways; depressed mitochondrial ATP-producing fatty acid β-oxidation; and extra-mitochondrial amino acid metabolism giving rise to metabotoxins.
CONCLUSIONS
In ACLF, intense systemic inflammation is associated with blood metabolite accumulation and profound alterations in major metabolic pathways, in particular inhibition of mitochondrial energy production, which may contribute to the development of organ failures.
LAY SUMMARY
Acute-on-chronic liver failure (ACLF), which develops in patients with cirrhosis, is characterized by intense systemic inflammation and organ failure(s). Because systemic inflammation is energetically expensive, its metabolic costs may result in organ dysfunction/failure. We identified a 38-metabolite blood fingerprint specific for ACLF that revealed mitochondrial dysfunction in peripheral organs. This may contribute to organ failures.

Identifiants

pubmed: 31778751
pii: S0168-8278(19)30696-8
doi: 10.1016/j.jhep.2019.11.009
pii:
doi:

Substances chimiques

Biomarkers 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

688-701

Commentaires et corrections

Type : ErratumIn
Type : CommentIn
Type : CommentIn
Type : CommentIn

Informations de copyright

Copyright © 2019 European Association for the Study of the Liver. Published by Elsevier B.V. All rights reserved.

Auteurs

Richard Moreau (R)

EF Clif, EASL-CLIF Consortium and Grifols Chair, Barcelona, Spain; Inserm, U1149, Centre de Recherche sur l'Inflammation (CRI) UMRS1149, Université de Paris, Service d'Hépatologie, Hôpital Beaujon, Assistance Publique-Hôpitaux de Paris, Clichy, France. Electronic address: richard.moreau@inserm.fr.

Joan Clària (J)

EF Clif, EASL-CLIF Consortium and Grifols Chair, Barcelona, Spain; Hospital Clínic-IDIBAPS, Universitat de Barcelona, Barcelona, Spain; CIBERehd, Barcelona, Spain.

Ferran Aguilar (F)

EF Clif, EASL-CLIF Consortium and Grifols Chair, Barcelona, Spain.

François Fenaille (F)

Service de Pharmacologie et Immuno-Analyse (SPI), Laboratoire d'Etude du Métabolisme des Médicaments, CEA, INRA, Université Paris Saclay, MetaboHUB, F-91191 Gif-sur-Yvette, France.

Juan José Lozano (JJ)

CIBERehd, Barcelona, Spain.

Christophe Junot (C)

Service de Pharmacologie et Immuno-Analyse (SPI), Laboratoire d'Etude du Métabolisme des Médicaments, CEA, INRA, Université Paris Saclay, MetaboHUB, F-91191 Gif-sur-Yvette, France.

Benoit Colsch (B)

Service de Pharmacologie et Immuno-Analyse (SPI), Laboratoire d'Etude du Métabolisme des Médicaments, CEA, INRA, Université Paris Saclay, MetaboHUB, F-91191 Gif-sur-Yvette, France.

Paolo Caraceni (P)

Department of Medical and Surgical Sciences, University of Bologna, Bologna, Italy.

Jonel Trebicka (J)

EF Clif, EASL-CLIF Consortium and Grifols Chair, Barcelona, Spain; J.W. Goethe University Hospital, Frankfurt, Germany.

Marco Pavesi (M)

EF Clif, EASL-CLIF Consortium and Grifols Chair, Barcelona, Spain.

Carlo Alessandria (C)

Division of Gastroenterology and Hepatology, San Giovanni Battista Hospital, Torino, Italy.

Frederik Nevens (F)

University Hospital Gasthuisberg, KU Leuven, Belgium.

Faouzi Saliba (F)

Hôpital Paul Brousse, Université Paris-Sud, Villejuif, France.

Tania M Welzel (TM)

J.W. Goethe University Hospital, Frankfurt, Germany.

Agustin Albillos (A)

Department of Gastroenterology, Hospital Universitario Ramón y Cajal, IRYCIS, University of Alcalá, CIBEREHD, Madrid, Spain.

Thierry Gustot (T)

CUB Hôpital Erasme, Université Libre de Bruxelles, Brussels, Belgium.

Javier Fernández (J)

EF Clif, EASL-CLIF Consortium and Grifols Chair, Barcelona, Spain; Hospital Clínic-IDIBAPS, Universitat de Barcelona, Barcelona, Spain; CIBERehd, Barcelona, Spain.

Christophe Moreno (C)

CUB Hôpital Erasme, Université Libre de Bruxelles, Brussels, Belgium.

Maurizio Baldassarre (M)

Department of Medical and Surgical Sciences, University of Bologna, Bologna, Italy.

Giacomo Zaccherini (G)

Department of Medical and Surgical Sciences, University of Bologna, Bologna, Italy.

Salvatore Piano (S)

Unit of Internal Medicine and Hepatology, Dept. of Medicine, DIMED, University of Padova, Italy.

Sara Montagnese (S)

Unit of Internal Medicine and Hepatology, Dept. of Medicine, DIMED, University of Padova, Italy.

Victor Vargas (V)

Liver Unit, Hospital Universitari Vall d'Hebron, Vall d'Hebron Institute of Research (VHIR), Universitat Autònoma de Barcelona, Barcelona, Spain.

Joan Genescà (J)

Liver Unit, Hospital Universitari Vall d'Hebron, Vall d'Hebron Institute of Research (VHIR), Universitat Autònoma de Barcelona, Barcelona, Spain.

Elsa Solà (E)

Hospital Clínic-IDIBAPS, Universitat de Barcelona, Barcelona, Spain; CIBERehd, Barcelona, Spain.

William Bernal (W)

Liver Intensive Therapy Unit, Institute of Liver Studies, Division of Inflammation Biology, King's College London, London, UK.

Noémie Butin (N)

Service de Pharmacologie et Immuno-Analyse (SPI), Laboratoire d'Etude du Métabolisme des Médicaments, CEA, INRA, Université Paris Saclay, MetaboHUB, F-91191 Gif-sur-Yvette, France.

Thaïs Hautbergue (T)

Service de Pharmacologie et Immuno-Analyse (SPI), Laboratoire d'Etude du Métabolisme des Médicaments, CEA, INRA, Université Paris Saclay, MetaboHUB, F-91191 Gif-sur-Yvette, France.

Sophie Cholet (S)

Service de Pharmacologie et Immuno-Analyse (SPI), Laboratoire d'Etude du Métabolisme des Médicaments, CEA, INRA, Université Paris Saclay, MetaboHUB, F-91191 Gif-sur-Yvette, France.

Florence Castelli (F)

Service de Pharmacologie et Immuno-Analyse (SPI), Laboratoire d'Etude du Métabolisme des Médicaments, CEA, INRA, Université Paris Saclay, MetaboHUB, F-91191 Gif-sur-Yvette, France.

Christian Jansen (C)

Department of Internal Medicine I, University of Bonn, Germany.

Christian Steib (C)

Department of Medicine II, Liver Center Munich, University Hospital LMU Munich, Munich, Germany.

Daniela Campion (D)

Division of Gastroenterology and Hepatology, San Giovanni Battista Hospital, Torino, Italy.

Raj Mookerjee (R)

Liver Failure Group, Institute for Liver Disease Health, University College London, Royal Free Hospital, London, UK.

Miguel Rodríguez-Gandía (M)

Department of Gastroenterology, Hospital Universitario Ramón y Cajal, IRYCIS, University of Alcalá, CIBEREHD, Madrid, Spain.

German Soriano (G)

Department of Gastroenterology, Hospital de la Santa Creu i Sant Pau, Universitat Autònoma de Barcelona, Barcelona, Spain.

François Durand (F)

Inserm, U1149, Centre de Recherche sur l'Inflammation (CRI) UMRS1149, Université de Paris, Service d'Hépatologie, Hôpital Beaujon, Assistance Publique-Hôpitaux de Paris, Clichy, France.

Daniel Benten (D)

University Hospital Hamburg-Eppendorf, Germany.

Rafael Bañares (R)

Digestive Diseases Department, Hospital General Universitario Gregorio Marañón; Instituto de Investigación Sanitaria Gregorio Marañón; Facultad de Medicina, Universidad Complutense, Madrid; and CIBERehd.

Rudolf E Stauber (RE)

Medical University of Graz, Graz, Austria.

Henning Gronbaek (H)

Department of Hepatology & Gastroenterology, Aarhus University Hospital, Aarhus, Denmark.

Minneke J Coenraad (MJ)

Department of Gastroenterology and Hepatology, Leiden University Medical Center, Leiden, the Netherlands.

Pere Ginès (P)

Hospital Clínic-IDIBAPS, Universitat de Barcelona, Barcelona, Spain; CIBERehd, Barcelona, Spain.

Alexander Gerbes (A)

Department of Medicine II, Liver Center Munich, University Hospital LMU Munich, Munich, Germany.

Rajiv Jalan (R)

EF Clif, EASL-CLIF Consortium and Grifols Chair, Barcelona, Spain; Liver Failure Group, Institute for Liver Disease Health, University College London, Royal Free Hospital, London, UK.

Mauro Bernardi (M)

Department of Medical and Surgical Sciences, University of Bologna, Bologna, Italy.

Vicente Arroyo (V)

EF Clif, EASL-CLIF Consortium and Grifols Chair, Barcelona, Spain.

Paolo Angeli (P)

EF Clif, EASL-CLIF Consortium and Grifols Chair, Barcelona, Spain; Unit of Internal Medicine and Hepatology, Dept. of Medicine, DIMED, University of Padova, Italy.

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