Inhibition of ATG3 ameliorates liver steatosis by increasing mitochondrial function.


Journal

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

Informations de publication

Date de publication:
01 2022
Historique:
received: 18 03 2021
revised: 03 08 2021
accepted: 13 09 2021
pubmed: 24 9 2021
medline: 16 2 2022
entrez: 23 9 2021
Statut: ppublish

Résumé

Autophagy-related gene 3 (ATG3) is an enzyme mainly known for its actions in the LC3 lipidation process, which is essential for autophagy. Whether ATG3 plays a role in lipid metabolism or contributes to non-alcoholic fatty liver disease (NAFLD) remains unknown. By performing proteomic analysis on livers from mice with genetic manipulation of hepatic p63, a regulator of fatty acid metabolism, we identified ATG3 as a new target downstream of p63. ATG3 was evaluated in liver samples from patients with NAFLD. Further, genetic manipulation of ATG3 was performed in human hepatocyte cell lines, primary hepatocytes and in the livers of mice. ATG3 expression is induced in the liver of animal models and patients with NAFLD (both steatosis and non-alcoholic steatohepatitis) compared with those without liver disease. Moreover, genetic knockdown of ATG3 in mice and human hepatocytes ameliorates p63- and diet-induced steatosis, while its overexpression increases the lipid load in hepatocytes. The inhibition of hepatic ATG3 improves fatty acid metabolism by reducing c-Jun N-terminal protein kinase 1 (JNK1), which increases sirtuin 1 (SIRT1), carnitine palmitoyltransferase 1a (CPT1a), and mitochondrial function. Hepatic knockdown of SIRT1 and CPT1a blunts the effects of ATG3 on mitochondrial activity. Unexpectedly, these effects are independent of an autophagic action. Collectively, these findings indicate that ATG3 is a novel protein implicated in the development of steatosis. We show that autophagy-related gene 3 (ATG3) contributes to the progression of non-alcoholic fatty liver disease in humans and mice. Hepatic knockdown of ATG3 ameliorates the development of NAFLD by stimulating mitochondrial function. Thus, ATG3 is an important factor implicated in steatosis.

Sections du résumé

BACKGROUND & AIMS
Autophagy-related gene 3 (ATG3) is an enzyme mainly known for its actions in the LC3 lipidation process, which is essential for autophagy. Whether ATG3 plays a role in lipid metabolism or contributes to non-alcoholic fatty liver disease (NAFLD) remains unknown.
METHODS
By performing proteomic analysis on livers from mice with genetic manipulation of hepatic p63, a regulator of fatty acid metabolism, we identified ATG3 as a new target downstream of p63. ATG3 was evaluated in liver samples from patients with NAFLD. Further, genetic manipulation of ATG3 was performed in human hepatocyte cell lines, primary hepatocytes and in the livers of mice.
RESULTS
ATG3 expression is induced in the liver of animal models and patients with NAFLD (both steatosis and non-alcoholic steatohepatitis) compared with those without liver disease. Moreover, genetic knockdown of ATG3 in mice and human hepatocytes ameliorates p63- and diet-induced steatosis, while its overexpression increases the lipid load in hepatocytes. The inhibition of hepatic ATG3 improves fatty acid metabolism by reducing c-Jun N-terminal protein kinase 1 (JNK1), which increases sirtuin 1 (SIRT1), carnitine palmitoyltransferase 1a (CPT1a), and mitochondrial function. Hepatic knockdown of SIRT1 and CPT1a blunts the effects of ATG3 on mitochondrial activity. Unexpectedly, these effects are independent of an autophagic action.
CONCLUSIONS
Collectively, these findings indicate that ATG3 is a novel protein implicated in the development of steatosis.
LAY SUMMARY
We show that autophagy-related gene 3 (ATG3) contributes to the progression of non-alcoholic fatty liver disease in humans and mice. Hepatic knockdown of ATG3 ameliorates the development of NAFLD by stimulating mitochondrial function. Thus, ATG3 is an important factor implicated in steatosis.

Identifiants

pubmed: 34555423
pii: S0168-8278(21)02038-9
doi: 10.1016/j.jhep.2021.09.008
pii:
doi:

Substances chimiques

Autophagy-Related Proteins 0
Ubiquitin-Conjugating Enzymes EC 2.3.2.23
ATG3 protein, human EC 6.3.2.-

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

11-24

Informations de copyright

Copyright © 2021 The Author(s). Published by Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Conflict of interest The authors declare that they have no conflicts of interest related to the study. Please refer to the accompanying ICMJE disclosure forms for further details.

Auteurs

Natália da Silva Lima (N)

Department of Physiology, CIMUS, University of Santiago de Compostela-Instituto de Investigación Sanitaria, Santiago de Compostela, Spain.

Marcos F Fondevila (MF)

Department of Physiology, CIMUS, University of Santiago de Compostela-Instituto de Investigación Sanitaria, Santiago de Compostela, Spain; CIBER Fisiopatologia de la Obesidad y Nutrición (CIBERobn), Spain.

Eva Nóvoa (E)

Department of Physiology, CIMUS, University of Santiago de Compostela-Instituto de Investigación Sanitaria, Santiago de Compostela, Spain.

Xabier Buqué (X)

Department of Physiology, University of the Basque Country UPV/EHU, Spain; Biocruces Bizkaia Health Research Institute, Spain.

Maria Mercado-Gómez (M)

Liver Disease Lab, Center for Cooperative Research in Biosciences (CIC bioGUNE), Basque Research and Technology Alliance (BRTA), 48160 Derio, Bizkaia, Spain.

Sarah Gallet (S)

Univ. Lille, Inserm, CHU Lille, Laboratory of Development and Plasticity of the Neuroendocrine Brain, Lille Neuroscience & Cognition, UMR-S 1172, European Genomic Institute for Diabetes (EGID), F-59000 Lille, France.

Maria J González-Rellan (MJ)

Department of Physiology, CIMUS, University of Santiago de Compostela-Instituto de Investigación Sanitaria, Santiago de Compostela, Spain.

Uxia Fernandez (U)

Department of Physiology, CIMUS, University of Santiago de Compostela-Instituto de Investigación Sanitaria, Santiago de Compostela, Spain.

Anne Loyens (A)

Univ. Lille, Inserm, CHU Lille, Laboratory of Development and Plasticity of the Neuroendocrine Brain, Lille Neuroscience & Cognition, UMR-S 1172, European Genomic Institute for Diabetes (EGID), F-59000 Lille, France.

Maria Garcia-Vence (M)

Proteomic Unit, Health Research Institute of Santiago de Compostela (IDIS), Santiago de Compostela, 15705 A Coruña, Spain.

Maria Del Pilar Chantada-Vazquez (MDP)

Proteomic Unit, Health Research Institute of Santiago de Compostela (IDIS), Santiago de Compostela, 15705 A Coruña, Spain.

Susana B Bravo (SB)

Proteomic Unit, Health Research Institute of Santiago de Compostela (IDIS), Santiago de Compostela, 15705 A Coruña, Spain.

Patricia Marañon (P)

LiverResearchUnit, Santa Cristina University Hospital, Instituto de Investigación Sanitaria Princesa, Madrid, Spain.

Ana Senra (A)

Department of Physiology, CIMUS, University of Santiago de Compostela-Instituto de Investigación Sanitaria, Santiago de Compostela, Spain.

Adriana Escudero (A)

Department of Physiology, CIMUS, University of Santiago de Compostela-Instituto de Investigación Sanitaria, Santiago de Compostela, Spain.

Magdalena Leiva (M)

Centro Nacional de Investigaciones Cardiovasculares (CNIC), Madrid, Spain.

Diana Guallar (D)

Department of Biochemistry, CIMUS, University of Santiago de Compostela-Instituto de Investigación Sanitaria, Santiago de Compostela, Spain.

Miguel Fidalgo (M)

Department of Physiology, CIMUS, University of Santiago de Compostela-Instituto de Investigación Sanitaria, Santiago de Compostela, Spain.

Pedro Gomes (P)

Department of Biomedicine, Unit of Pharmacology and Therapeutics, Faculty of Medicine, University of Porto, Porto, Portugal; Coimbra Institute for Clinical and Biomedical Research (iCBR), Faculty of Medicine, University of Coimbra, Coimbra, Portugal; Institute of Pharmacology and Experimental Therapeutics, Coimbra Institute for Clinical and Biomedical Research(iCBR), Faculty of Medicine, University of Coimbra, Coimbra, Portugal.

Marc Claret (M)

Neuronal Control of Metabolism (NeuCoMe) Laboratory, Institut d'Investigacions Biomèdiques August Pi iSunyer (IDIBAPS), 08036, Barcelona, Spain; CIBER de Diabetes y Enfermedades Metabólicas Asociadas (CIBERDEM), 08036, Barcelona, Spain.

Guadalupe Sabio (G)

Centro Nacional de Investigaciones Cardiovasculares (CNIC), Madrid, Spain.

Marta Varela-Rey (M)

Liver Disease Lab, Center for Cooperative Research in Biosciences (CIC bioGUNE), Basque Research and Technology Alliance (BRTA), 48160 Derio, Bizkaia, Spain; Gene Regulatory Control in Disease, CIMUS, University of Santiago de Compostela, Santiago de Compostela, Spain.

Teresa C Delgado (TC)

Liver Disease Lab, Center for Cooperative Research in Biosciences (CIC bioGUNE), Basque Research and Technology Alliance (BRTA), 48160 Derio, Bizkaia, Spain.

Rocio Montero-Vallejo (R)

UGC Aparato Digestivo, Instituto de Biomedicina de Sevilla. Hospital Universitario Virgen del Rocío, Universidad de Sevilla, Sevilla, Spain.

Javier Ampuero (J)

UGC Aparato Digestivo, Instituto de Biomedicina de Sevilla. Hospital Universitario Virgen del Rocío, Universidad de Sevilla, Sevilla, Spain.

Miguel López (M)

Department of Physiology, CIMUS, University of Santiago de Compostela-Instituto de Investigación Sanitaria, Santiago de Compostela, Spain; CIBER Fisiopatologia de la Obesidad y Nutrición (CIBERobn), Spain.

Carlos Diéguez (C)

Department of Physiology, CIMUS, University of Santiago de Compostela-Instituto de Investigación Sanitaria, Santiago de Compostela, Spain; CIBER Fisiopatologia de la Obesidad y Nutrición (CIBERobn), Spain.

Laura Herrero (L)

CIBER Fisiopatologia de la Obesidad y Nutrición (CIBERobn), Spain; Department of Biochemistry and Physiology, School of Pharmacy and Food Sciences, Institut de Biomedicina de la Universitat de Barcelona (IBUB), Barcelona, Spain.

Dolors Serra (D)

CIBER Fisiopatologia de la Obesidad y Nutrición (CIBERobn), Spain; Department of Biochemistry and Physiology, School of Pharmacy and Food Sciences, Institut de Biomedicina de la Universitat de Barcelona (IBUB), Barcelona, Spain.

Markus Schwaninger (M)

University of Lübeck, Institute for Experimental and Clinical Pharmacology and Toxicology, Lübeck, Germany.

Vincent Prevot (V)

Univ. Lille, Inserm, CHU Lille, Laboratory of Development and Plasticity of the Neuroendocrine Brain, Lille Neuroscience & Cognition, UMR-S 1172, European Genomic Institute for Diabetes (EGID), F-59000 Lille, France.

Rocio Gallego-Duran (R)

Neuronal Control of Metabolism (NeuCoMe) Laboratory, Institut d'Investigacions Biomèdiques August Pi iSunyer (IDIBAPS), 08036, Barcelona, Spain; CIBER Enfermedades Hepáticas y Digestivas (CIBERehd), Spain.

Manuel Romero-Gomez (M)

UGC Aparato Digestivo, Instituto de Biomedicina de Sevilla. Hospital Universitario Virgen del Rocío, Universidad de Sevilla, Sevilla, Spain; CIBER Enfermedades Hepáticas y Digestivas (CIBERehd), Spain.

Paula Iruzubieta (P)

Gastroenterology and Hepatology Department, Marqués de Valdecilla University Hospital. Clinical and Translational Digestive Research Group, IDIVAL, Santander, Spain.

Javier Crespo (J)

Gastroenterology and Hepatology Department, Marqués de Valdecilla University Hospital. Clinical and Translational Digestive Research Group, IDIVAL, Santander, Spain.

Maria L Martinez-Chantar (ML)

Liver Disease Lab, Center for Cooperative Research in Biosciences (CIC bioGUNE), Basque Research and Technology Alliance (BRTA), 48160 Derio, Bizkaia, Spain; CIBER Enfermedades Hepáticas y Digestivas (CIBERehd), Spain.

Carmelo Garcia-Monzon (C)

LiverResearchUnit, Santa Cristina University Hospital, Instituto de Investigación Sanitaria Princesa, Madrid, Spain; CIBER Enfermedades Hepáticas y Digestivas (CIBERehd), Spain.

Agueda Gonzalez-Rodriguez (A)

LiverResearchUnit, Santa Cristina University Hospital, Instituto de Investigación Sanitaria Princesa, Madrid, Spain; CIBER de Diabetes y Enfermedades Metabólicas Asociadas (CIBERdem), Spain.

Patricia Aspichueta (P)

Department of Physiology, University of the Basque Country UPV/EHU, Spain; Biocruces Bizkaia Health Research Institute, Spain; CIBER Enfermedades Hepáticas y Digestivas (CIBERehd), Spain.

Ruben Nogueiras (R)

Department of Physiology, CIMUS, University of Santiago de Compostela-Instituto de Investigación Sanitaria, Santiago de Compostela, Spain; CIBER Fisiopatologia de la Obesidad y Nutrición (CIBERobn), Spain. Electronic address: ruben.nogueiras@usc.es.

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