Loss of mitochondrial adaptation associates with deterioration of mitochondrial turnover and structure in metabolic dysfunction-associated steatotic liver disease.

Fatty liver Insulin resistance MASH Mitochondrial function Mitophagy Obesity Ultrastructure

Journal

Metabolism: clinical and experimental
ISSN: 1532-8600
Titre abrégé: Metabolism
Pays: United States
ID NLM: 0375267

Informations de publication

Date de publication:
18 Dec 2023
Historique:
received: 16 08 2023
revised: 29 11 2023
accepted: 16 12 2023
medline: 21 12 2023
pubmed: 21 12 2023
entrez: 20 12 2023
Statut: aheadofprint

Résumé

Obesity and type 2 diabetes frequently have metabolic dysfunction-associated steatotic liver disease (MASLD) including steatohepatitis (MASH). In obesity, the liver may adapt its oxidative capacity, but the role of mitochondrial turnover in MASLD remains uncertain. This cross-sectional study compared individuals with class III obesity (n = 8/group) without (control, OBE CON; NAFLD activity score: 0.4 ± 0.1) or with steatosis (OBE MASL, 2.3 ± 0.4), or MASH (OBE MASH, 5.3 ± 0.3, p < 0.05 vs. other groups). Hepatic mitochondrial ultrastructure was assessed by transmission electron microscopy, mitochondrial respiration by high-resolution respirometry, biomarkers of mitochondrial quality control and endoplasmic reticulum (ER) stress by Western Blot. Mitochondrial oxidative capacity was 31 % higher in OBE MASL, but 25 % lower in OBE MASH (p < 0.05 vs. OBE CON). OBE MASH showed ~1.5fold lower mitochondrial number, but ~1.2-1.5fold higher diameter and area (p < 0.001 vs. other groups). Biomarkers of autophagy (p62), mitophagy (PINK1, PARKIN), fission (DRP-1, FIS1) and fusion (MFN1/2, OPA1) were reduced in OBE MASH (p < 0.05 vs. OBE CON). OBE MASL showed lower p62, p-PARKIN/PARKIN, and p-DRP-1 (p < 0.05 vs. OBE CON). OBE MASL and MASH showed higher ER stress markers (PERK, ATF4, p-eIF2α-S51/eIF2α; p < 0.05 vs. OBE CON). Mitochondrial diameter associated inversely with fusion/fission biomarkers and with oxidative capacity, but positively with H Humans with hepatic steatosis already exhibit impaired mitochondrial turnover, despite upregulated oxidative capacity, and evidence for ER stress. In MASH, oxidative stress likely mediates progressive decline of mitochondrial turnover, ultrastructure and respiration indicating that mitochondrial quality control is key for energy metabolism and may have potential for targeting MASH. ClinGovTrial:NCT01477957.

Sections du résumé

BACKGROUND BACKGROUND
Obesity and type 2 diabetes frequently have metabolic dysfunction-associated steatotic liver disease (MASLD) including steatohepatitis (MASH). In obesity, the liver may adapt its oxidative capacity, but the role of mitochondrial turnover in MASLD remains uncertain.
METHODS METHODS
This cross-sectional study compared individuals with class III obesity (n = 8/group) without (control, OBE CON; NAFLD activity score: 0.4 ± 0.1) or with steatosis (OBE MASL, 2.3 ± 0.4), or MASH (OBE MASH, 5.3 ± 0.3, p < 0.05 vs. other groups). Hepatic mitochondrial ultrastructure was assessed by transmission electron microscopy, mitochondrial respiration by high-resolution respirometry, biomarkers of mitochondrial quality control and endoplasmic reticulum (ER) stress by Western Blot.
RESULTS RESULTS
Mitochondrial oxidative capacity was 31 % higher in OBE MASL, but 25 % lower in OBE MASH (p < 0.05 vs. OBE CON). OBE MASH showed ~1.5fold lower mitochondrial number, but ~1.2-1.5fold higher diameter and area (p < 0.001 vs. other groups). Biomarkers of autophagy (p62), mitophagy (PINK1, PARKIN), fission (DRP-1, FIS1) and fusion (MFN1/2, OPA1) were reduced in OBE MASH (p < 0.05 vs. OBE CON). OBE MASL showed lower p62, p-PARKIN/PARKIN, and p-DRP-1 (p < 0.05 vs. OBE CON). OBE MASL and MASH showed higher ER stress markers (PERK, ATF4, p-eIF2α-S51/eIF2α; p < 0.05 vs. OBE CON). Mitochondrial diameter associated inversely with fusion/fission biomarkers and with oxidative capacity, but positively with H
CONCLUSION CONCLUSIONS
Humans with hepatic steatosis already exhibit impaired mitochondrial turnover, despite upregulated oxidative capacity, and evidence for ER stress. In MASH, oxidative stress likely mediates progressive decline of mitochondrial turnover, ultrastructure and respiration indicating that mitochondrial quality control is key for energy metabolism and may have potential for targeting MASH. ClinGovTrial:NCT01477957.

Identifiants

pubmed: 38122893
pii: S0026-0495(23)00366-9
doi: 10.1016/j.metabol.2023.155762
pii:
doi:

Banques de données

ClinicalTrials.gov
['NCT01477957']

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

155762

Informations de copyright

Copyright © 2023. Published by Elsevier Inc.

Auteurs

Theresia Sarabhai (T)

Department of Endocrinology and Diabetology, Medical Faculty and University Hospital Düsseldorf, Heinrich-Heine-University, Düsseldorf, Germany; Institute for Clinical Diabetology, German Diabetes Center, Leibniz Institute for Diabetes Research at Heinrich-Heine-University, Düsseldorf, Germany; German Center for Diabetes Research, Partner Düsseldorf, Neuherberg, Germany.

Sabine Kahl (S)

Department of Endocrinology and Diabetology, Medical Faculty and University Hospital Düsseldorf, Heinrich-Heine-University, Düsseldorf, Germany; Institute for Clinical Diabetology, German Diabetes Center, Leibniz Institute for Diabetes Research at Heinrich-Heine-University, Düsseldorf, Germany; German Center for Diabetes Research, Partner Düsseldorf, Neuherberg, Germany.

Sofiya Gancheva (S)

Department of Endocrinology and Diabetology, Medical Faculty and University Hospital Düsseldorf, Heinrich-Heine-University, Düsseldorf, Germany; Institute for Clinical Diabetology, German Diabetes Center, Leibniz Institute for Diabetes Research at Heinrich-Heine-University, Düsseldorf, Germany; German Center for Diabetes Research, Partner Düsseldorf, Neuherberg, Germany.

Lucia Mastrototaro (L)

Institute for Clinical Diabetology, German Diabetes Center, Leibniz Institute for Diabetes Research at Heinrich-Heine-University, Düsseldorf, Germany; German Center for Diabetes Research, Partner Düsseldorf, Neuherberg, Germany.

Bedair Dewidar (B)

Institute for Clinical Diabetology, German Diabetes Center, Leibniz Institute for Diabetes Research at Heinrich-Heine-University, Düsseldorf, Germany; German Center for Diabetes Research, Partner Düsseldorf, Neuherberg, Germany.

Dominik Pesta (D)

Institute of Aerospace Medicine, German Aerospace Center, Cologne, Germany; Centre for Endocrinology, Diabetes and Preventive Medicine, University Hospital Cologne, Cologne, Germany; Cologne Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases, Cologne, Germany.

Jacqueline M Ratter-Rieck (JM)

Institute for Clinical Diabetology, German Diabetes Center, Leibniz Institute for Diabetes Research at Heinrich-Heine-University, Düsseldorf, Germany; German Center for Diabetes Research, Partner Düsseldorf, Neuherberg, Germany.

Pavel Bobrov (P)

German Center for Diabetes Research, Partner Düsseldorf, Neuherberg, Germany; Institute for Biometrics and Epidemiology, German Diabetes Center, Leibniz Center for Diabetes Research at Heinrich-Heine-University, Düsseldorf, Germany.

Kay Jeruschke (K)

Institute for Clinical Diabetology, German Diabetes Center, Leibniz Institute for Diabetes Research at Heinrich-Heine-University, Düsseldorf, Germany; German Center for Diabetes Research, Partner Düsseldorf, Neuherberg, Germany.

Irene Esposito (I)

Institute of Pathology, University Hospital and Heinrich-Heine-University, Düsseldorf, Germany.

Matthias Schlensak (M)

Department of Obesity and Reflux Center, Neuwerk Hospital Mönchengladbach, Germany.

Michael Roden (M)

Department of Endocrinology and Diabetology, Medical Faculty and University Hospital Düsseldorf, Heinrich-Heine-University, Düsseldorf, Germany; Institute for Clinical Diabetology, German Diabetes Center, Leibniz Institute for Diabetes Research at Heinrich-Heine-University, Düsseldorf, Germany; German Center for Diabetes Research, Partner Düsseldorf, Neuherberg, Germany. Electronic address: michael.roden@ddz.de.

Classifications MeSH