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


Por: Moreau, R, Claria, J, Aguilar, F, Fenaille, F, Lozano, JJ, Junot, C, Colsch, B, Caraceni, P, Trebicka, J, Pavesi, M, Alessandria, C, Nevens, F, Saliba, F, Welzel, TM, Albillos, A, Gustot, T, Fernandez, J, Moreno, C, Baldassarre, M, Zaccherini, G, Piano, S, Montagnese, S, Vargas, V, Genesca, J, Sola, E, Bernal, W, Butin, N, Hautbergue, T, Cholet, S, Castelli, F, Jansen, C, Steib, C, Campion, D, Mookerjee, R, Rodriguez-Gandia, M, Soriano, G, Durand, F, Benten, D, Banares, R, Stauber, RE, Gronbaek, H, Coenraad, MJ, Gines, P, Gerbes, A, Jalan, R, Bernardi, M, Arroyo, V, Angeli, P

Publicada: 1 abr 2020
Resumen:
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 alpha, soluble CD206, and soluble CD163. ACLF was characterizedbyintense proteolysis andlipolysis; aminoacid catabolism; extra-mitochondrial glucose metabolism through glycolysis, pentose phosphate, and D-glucuronate pathways; depressed mitochondrial ATP-producing fatty acid beta-oxidation; and extramitochondrial 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. (C) 2019 European Association for the Study of the Liver. Published by Elsevier B.V. All rights reserved.

Filiaciones:
Moreau, R:
 EASL CLIF Consortium & Grifols Chair, EF Clif, Barcelona, Spain

 Univ Paris, CRI, INSERM, U1149,UMRS1149, Clichy, France

Claria, J:
 EASL CLIF Consortium & Grifols Chair, EF Clif, Barcelona, Spain

 Univ Barcelona, Hosp Clin IDIBAPS, Barcelona, Spain

 CIBEREHD, Barcelona, Spain

Aguilar, F:
 EASL CLIF Consortium & Grifols Chair, EF Clif, Barcelona, Spain

Fenaille, F:
 Univ Paris Saclay, Lab Etud Metabol Medicaments, SPI, CEA,INRA,MetaboHUB, F-91191 Gif Sur Yvette, France

Lozano, JJ:
 CIBEREHD, Barcelona, Spain

Junot, C:
 Univ Paris Saclay, Lab Etud Metabol Medicaments, SPI, CEA,INRA,MetaboHUB, F-91191 Gif Sur Yvette, France

Colsch, B:
 Univ Paris Saclay, Lab Etud Metabol Medicaments, SPI, CEA,INRA,MetaboHUB, F-91191 Gif Sur Yvette, France

Caraceni, P:
 Univ Bologna, Dept Med & Surg Sci, Bologna, Italy

Trebicka, J:
 EASL CLIF Consortium & Grifols Chair, EF Clif, Barcelona, Spain

 JW Goethe Univ Hosp, Frankfurt, Germany

Pavesi, M:
 EASL CLIF Consortium & Grifols Chair, EF Clif, Barcelona, Spain

Alessandria, C:
 San Giovanni Battista Hosp, Div Gastroenterol & Hepatol, Turin, Italy

Nevens, F:
 Katholieke Univ Leuven, Univ Hosp Gasthuisberg, Leuven, Belgium

Saliba, F:
 Univ Paris Sud, Hop Paul Brousse, Villejuif, France

Welzel, TM:
 JW Goethe Univ Hosp, Frankfurt, Germany

Albillos, A:
 Hosp Ramon & Cajal, Madrid, Spain

 Univ Bonn, Dept Internal Med 1, Bonn, Germany

Gustot, T:
 Univ Libre Bruxelles, CUB Hop Erasme, Brussels, Belgium

Fernandez, J:
 EASL CLIF Consortium & Grifols Chair, EF Clif, Barcelona, Spain

 Univ Barcelona, Hosp Clin IDIBAPS, Barcelona, Spain

 CIBEREHD, Barcelona, Spain

Moreno, C:
 Univ Libre Bruxelles, CUB Hop Erasme, Brussels, Belgium

Baldassarre, M:
 Univ Bologna, Dept Med & Surg Sci, Bologna, Italy

Zaccherini, G:
 Univ Bologna, Dept Med & Surg Sci, Bologna, Italy

Piano, S:
 Univ Padua, Dept Med, Unit Internal Med & Hepatol, DIMED, Padua, Italy

Montagnese, S:
 Univ Padua, Dept Med, Unit Internal Med & Hepatol, DIMED, Padua, Italy

Vargas, V:
 Univ Autonoma Barcelona, VHIR, Hosp Univ Vall Hebron, Liver Unit, Barcelona, Spain

Genesca, J:
 Univ Autonoma Barcelona, VHIR, Hosp Univ Vall Hebron, Liver Unit, Barcelona, Spain

Sola, E:
 Univ Barcelona, Hosp Clin IDIBAPS, Barcelona, Spain

 CIBEREHD, Barcelona, Spain

Bernal, W:
 Kings Coll London, Div Inflammat Biol, Inst Liver Studies, Liver Intens Therapy Unit, London, England

Butin, N:
 Univ Paris Saclay, Lab Etud Metabol Medicaments, SPI, CEA,INRA,MetaboHUB, F-91191 Gif Sur Yvette, France

Hautbergue, T:
 Univ Paris Saclay, Lab Etud Metabol Medicaments, SPI, CEA,INRA,MetaboHUB, F-91191 Gif Sur Yvette, France

Cholet, S:
 Univ Paris Saclay, Lab Etud Metabol Medicaments, SPI, CEA,INRA,MetaboHUB, F-91191 Gif Sur Yvette, France

Castelli, F:
 Univ Paris Saclay, Lab Etud Metabol Medicaments, SPI, CEA,INRA,MetaboHUB, F-91191 Gif Sur Yvette, France

Jansen, C:
 Univ Bonn, Dept Internal Med 1, Bonn, Germany

Steib, C:
 Univ Hosp LMU Munich, Liver Ctr Munich, Dept Med 2, Munich, Germany

Campion, D:
 San Giovanni Battista Hosp, Div Gastroenterol & Hepatol, Turin, Italy

Mookerjee, R:
 UCL, Royal Free Hosp, Inst Liver Dis Hlth, Liver Failure Grp, London, England

Rodriguez-Gandia, M:
 Hosp Ramon & Cajal, Madrid, Spain

Soriano, G:
 Univ Autonoma Barcelona, Hosp Santa Creu & St Pau, Dept Gastroenterol, Barcelona, Spain

Durand, F:
 Univ Paris, CRI, INSERM, U1149,UMRS1149, Clichy, France

Benten, D:
 Univ Hosp Hamburg Eppendorf, Hamburg, Germany

Banares, R:
 Hosp Gen Univ Gregorio Maranon, Digest Dis Dept, Madrid, Spain

 Inst Invest Sanitaria Gregorio Maranon, Madrid, Spain

 Univ Complutense, Fac Med, Madrid, Spain

 CIBEREHD, Madrid, Spain

Stauber, RE:
 Med Univ Graz, Graz, Austria

Coenraad, MJ:
 Leiden Univ, Med Ctr, Dept Gastroenterol & Hepatol, Leiden, Netherlands

Gines, P:
 Univ Barcelona, Hosp Clin IDIBAPS, Barcelona, Spain

 CIBEREHD, Barcelona, Spain

Gerbes, A:
 Hosp Ramon & Cajal, Madrid, Spain

 Univ Hosp LMU Munich, Liver Ctr Munich, Dept Med 2, Munich, Germany

Jalan, R:
 EASL CLIF Consortium & Grifols Chair, EF Clif, Barcelona, Spain

 UCL, Royal Free Hosp, Inst Liver Dis Hlth, Liver Failure Grp, London, England

Bernardi, M:
 Univ Bologna, Dept Med & Surg Sci, Bologna, Italy

Arroyo, V:
 EASL CLIF Consortium & Grifols Chair, EF Clif, Barcelona, Spain

Angeli, P:
 EASL CLIF Consortium & Grifols Chair, EF Clif, Barcelona, Spain

 Univ Padua, Dept Med, Unit Internal Med & Hepatol, DIMED, Padua, Italy

Hop Beaujon, AP HP, Serv Hepatol, Clichy, France.
Aarhus Univ Hosp, Dept Gastroenterol & Hepatol, Aarhus, Denmark.
ISSN: 01688278
Editorial
ELSEVIER, RADARWEG 29, 1043 NX AMSTERDAM, NETHERLANDS, Países Bajos
Tipo de documento: Article
Volumen: 72 Número: 4
Páginas: 688-701
WOS Id: 000520050900013
ID de PubMed: 31778751
imagen Green Published

MÉTRICAS