Hepatic levels of S-adenosylmethionine regulate the adaptive response to fasting.

S-adenosylmethionine adipose tissue caloric restriction endoplasmic reticulum stress fasting liver methionine adenosyltransferase a1 mitochondria-associated-membranes phosphatidylethanolamine methyltransferase β-oxidation

Journal

Cell metabolism
ISSN: 1932-7420
Titre abrégé: Cell Metab
Pays: United States
ID NLM: 101233170

Informations de publication

Date de publication:
08 08 2023
Historique:
received: 27 08 2020
revised: 30 03 2023
accepted: 06 07 2023
medline: 11 8 2023
pubmed: 2 8 2023
entrez: 1 8 2023
Statut: ppublish

Résumé

There has been an intense focus to uncover the molecular mechanisms by which fasting triggers the adaptive cellular responses in the major organs of the body. Here, we show that in mice, hepatic S-adenosylmethionine (SAMe)-the principal methyl donor-acts as a metabolic sensor of nutrition to fine-tune the catabolic-fasting response by modulating phosphatidylethanolamine N-methyltransferase (PEMT) activity, endoplasmic reticulum-mitochondria contacts, β-oxidation, and ATP production in the liver, together with FGF21-mediated lipolysis and thermogenesis in adipose tissues. Notably, we show that glucagon induces the expression of the hepatic SAMe-synthesizing enzyme methionine adenosyltransferase α1 (MAT1A), which translocates to mitochondria-associated membranes. This leads to the production of this metabolite at these sites, which acts as a brake to prevent excessive β-oxidation and mitochondrial ATP synthesis and thereby endoplasmic reticulum stress and liver injury. This work provides important insights into the previously undescribed function of SAMe as a new arm of the metabolic adaptation to fasting.

Identifiants

pubmed: 37527658
pii: S1550-4131(23)00261-9
doi: 10.1016/j.cmet.2023.07.002
pmc: PMC10432853
pii:
doi:

Substances chimiques

S-Adenosylmethionine 7LP2MPO46S
Adenosine Triphosphate 8L70Q75FXE
Methionine Adenosyltransferase EC 2.5.1.6
PEMT protein, mouse EC 2.1.1.17
Phosphatidylethanolamine N-Methyltransferase EC 2.1.1.17

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

1373-1389.e8

Informations de copyright

Copyright © 2023 The Authors. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests M.L.M.-C. advises for Mitotherapeutix.

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Auteurs

Alba Capelo-Diz (A)

Gene Regulatory Control in Disease Laboratory, Center for Research in Molecular Medicine and Chronic Diseases (CIMUS), Instituto de Investigación Sanitaria de Santiago de Compostela (IDIS), University of Santiago de Compostela, Santiago de Compostela, A Coruña 15706, Spain.

Sofía Lachiondo-Ortega (S)

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

David Fernández-Ramos (D)

Precision Medicine and Metabolism Laboratory, Center for Cooperative Research in Biosciences (CIC bioGUNE), Basque Research and Technology Alliance (BRTA), Bizkaia Technology Park, 48160 Derio, Spain; Centro de investigación Biomedica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd), Instituto de salud Carlos III, 28029 Madrid, Spain.

Jorge Cañas-Martín (J)

Gene Regulatory Control in Disease Laboratory, Center for Research in Molecular Medicine and Chronic Diseases (CIMUS), Instituto de Investigación Sanitaria de Santiago de Compostela (IDIS), University of Santiago de Compostela, Santiago de Compostela, A Coruña 15706, Spain.

Naroa Goikoetxea-Usandizaga (N)

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

Marina Serrano-Maciá (M)

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

Maria J González-Rellan (MJ)

Department of Physiology, CIMUS, University of Santiago de Compostela, Instituto de Investigación Sanitaria de Santiago de Compostela (IDIS), Santiago de Compostela, A Coruña 15706, Spain.

Laura Mosca (L)

Department of Precision Medicine, University of Campania "Luigi Vanvitelli", Via Luigi De Crecchio 7, 80138 Naples, Italy.

Joan Blazquez-Vicens (J)

Gene Regulatory Control in Disease Laboratory, Center for Research in Molecular Medicine and Chronic Diseases (CIMUS), Instituto de Investigación Sanitaria de Santiago de Compostela (IDIS), University of Santiago de Compostela, Santiago de Compostela, A Coruña 15706, Spain.

Alberto Tinahones-Ruano (A)

Gene Regulatory Control in Disease Laboratory, Center for Research in Molecular Medicine and Chronic Diseases (CIMUS), Instituto de Investigación Sanitaria de Santiago de Compostela (IDIS), University of Santiago de Compostela, Santiago de Compostela, A Coruña 15706, Spain.

Marcos F Fondevila (MF)

Department of Physiology, CIMUS, University of Santiago de Compostela, Instituto de Investigación Sanitaria de Santiago de Compostela (IDIS), Santiago de Compostela, A Coruña 15706, Spain; CIBER Fisiopatología de la Obesidad y Nutrición (CIBERobn), Santiago de Compostela, A Coruña 15706, Spain.

Mason Buyan (M)

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

Teresa C Delgado (TC)

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

Virginia Gutierrez de Juan (V)

Precision Medicine and Metabolism Laboratory, Center for Cooperative Research in Biosciences (CIC bioGUNE), Basque Research and Technology Alliance (BRTA), Bizkaia Technology Park, 48160 Derio, Spain.

Paula Ayuso-García (P)

Gene Regulatory Control in Disease Laboratory, Center for Research in Molecular Medicine and Chronic Diseases (CIMUS), Instituto de Investigación Sanitaria de Santiago de Compostela (IDIS), University of Santiago de Compostela, Santiago de Compostela, A Coruña 15706, Spain.

Alejandro Sánchez-Rueda (A)

Gene Regulatory Control in Disease Laboratory, Center for Research in Molecular Medicine and Chronic Diseases (CIMUS), Instituto de Investigación Sanitaria de Santiago de Compostela (IDIS), University of Santiago de Compostela, Santiago de Compostela, A Coruña 15706, Spain.

Sergio Velasco-Avilés (S)

Gene Regulatory Control in Disease Laboratory, Center for Research in Molecular Medicine and Chronic Diseases (CIMUS), Instituto de Investigación Sanitaria de Santiago de Compostela (IDIS), University of Santiago de Compostela, Santiago de Compostela, A Coruña 15706, Spain.

Héctor Fernández-Susavila (H)

Gene Regulatory Control in Disease Laboratory, Center for Research in Molecular Medicine and Chronic Diseases (CIMUS), Instituto de Investigación Sanitaria de Santiago de Compostela (IDIS), University of Santiago de Compostela, Santiago de Compostela, A Coruña 15706, Spain.

Cristina Riobello-Suárez (C)

Gene Regulatory Control in Disease Laboratory, Center for Research in Molecular Medicine and Chronic Diseases (CIMUS), Instituto de Investigación Sanitaria de Santiago de Compostela (IDIS), University of Santiago de Compostela, Santiago de Compostela, A Coruña 15706, Spain.

Bartlomiej Dziechciarz (B)

Gene Regulatory Control in Disease Laboratory, Center for Research in Molecular Medicine and Chronic Diseases (CIMUS), Instituto de Investigación Sanitaria de Santiago de Compostela (IDIS), University of Santiago de Compostela, Santiago de Compostela, A Coruña 15706, Spain.

Cristina Montiel-Duarte (C)

The John van Geest Cancer Research Centre, School of Science and Technology, Nottingham Trent University, Nottingham NG11 8NS, UK.

Fernando Lopitz-Otsoa (F)

Precision Medicine and Metabolism Laboratory, Center for Cooperative Research in Biosciences (CIC bioGUNE), Basque Research and Technology Alliance (BRTA), Bizkaia Technology Park, 48160 Derio, Spain.

Maider Bizkarguenaga (M)

Precision Medicine and Metabolism Laboratory, Center for Cooperative Research in Biosciences (CIC bioGUNE), Basque Research and Technology Alliance (BRTA), Bizkaia Technology Park, 48160 Derio, Spain.

Jon Bilbao-García (J)

Precision Medicine and Metabolism Laboratory, Center for Cooperative Research in Biosciences (CIC bioGUNE), Basque Research and Technology Alliance (BRTA), Bizkaia Technology Park, 48160 Derio, Spain.

Ganeko Bernardo-Seisdedos (G)

Precision Medicine and Metabolism Laboratory, Center for Cooperative Research in Biosciences (CIC bioGUNE), Basque Research and Technology Alliance (BRTA), Bizkaia Technology Park, 48160 Derio, Spain.

Ana Senra (A)

CIMUS, University of Santiago de Compostela, Instituto de Investigación Sanitaria de Santiago de Compostela (IDIS), Santiago de Compostela, A Coruña 15706, Spain.

Mario Soriano-Navarro (M)

Electron Microscopy Core Facility, Centro de Investigación Príncipe Felipe (CIPF), Valencia 46012, Spain.

Oscar Millet (O)

Precision Medicine and Metabolism Laboratory, Center for Cooperative Research in Biosciences (CIC bioGUNE), Basque Research and Technology Alliance (BRTA), Bizkaia Technology Park, 48160 Derio, Spain.

Ángel Díaz-Lagares (Á)

Epigenomics Unit, Cancer Epigenomics, Translational Medical Oncology Group (ONCOMET), Health Research Institute of Santiago de Compostela (IDIS), University Clinical Hospital of Santiago (CHUS/SERGAS), Santiago de Compostela, A Coruña 15706, Spain.

Ana B Crujeiras (AB)

CIBER Fisiopatología de la Obesidad y Nutrición (CIBERobn), Santiago de Compostela, A Coruña 15706, Spain; Epigenomics in Endocrinology and Nutrition Group, Epigenomics Unit, Instituto de Investigacion Sanitaria de Santiago de Compostela (IDIS), Complejo Hospitalario Universitario de Santiago de Compostela (CHUS/SERGAS), 15706 Santiago de Compostela, Spain.

Aida Bao-Caamano (A)

Epigenomics in Endocrinology and Nutrition Group, Epigenomics Unit, Instituto de Investigacion Sanitaria de Santiago de Compostela (IDIS), Complejo Hospitalario Universitario de Santiago de Compostela (CHUS/SERGAS), 15706 Santiago de Compostela, Spain.

Diana Cabrera (D)

Metabolomics Platform, Center for Cooperative Research in Biosciences (CIC bioGUNE), Basque Research and Technology Alliance (BRTA), Bizkaia Technology Park, 48160 Derio, Spain.

Sebastiaan van Liempd (S)

Metabolomics Platform, Center for Cooperative Research in Biosciences (CIC bioGUNE), Basque Research and Technology Alliance (BRTA), Bizkaia Technology Park, 48160 Derio, Spain.

Miguel Tamayo-Carro (M)

Nerve Disorders Laboratory, Center for Cooperative Research in Biosciences (CIC bioGUNE), Basque Research and Technology Alliance (BRTA), Bizkaia Technology Park, 48160 Derio, Spain.

Luigi Borzacchiello (L)

Department of Precision Medicine, University of Campania "Luigi Vanvitelli", Via Luigi De Crecchio 7, 80138 Naples, Italy.

Beatriz Gomez-Santos (B)

Department of Physiology, Faculty of Medicine and Nursing, University of the Basque Country UPV/EHU, Leioa, Spain.

Xabier Buqué (X)

Department of Physiology, Faculty of Medicine and Nursing, University of the Basque Country UPV/EHU, Leioa, Spain.

Diego Sáenz de Urturi (D)

Department of Physiology, Faculty of Medicine and Nursing, University of the Basque Country UPV/EHU, Leioa, Spain.

Francisco González-Romero (F)

Department of Physiology, Faculty of Medicine and Nursing, University of the Basque Country UPV/EHU, Leioa, Spain.

Jorge Simon (J)

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

Rubén Rodríguez-Agudo (R)

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

Asier Ruiz (A)

Laboratory of Neurobiology, Achucarro Basque Center for Neuroscience, Department of Neurosciences, University of Basque Country (UPV/EHU), Centro de investigación Biomedica en Red de Enfermedades Neurodegenerativas (CIBERNED), 48940 Leioa, Spain.

Carlos Matute (C)

Laboratory of Neurobiology, Achucarro Basque Center for Neuroscience, Department of Neurosciences, University of Basque Country (UPV/EHU), Centro de investigación Biomedica en Red de Enfermedades Neurodegenerativas (CIBERNED), 48940 Leioa, Spain.

Daniel Beiroa (D)

Experimental Biomedicine Center (CEBEGA), University of Santiago de Compostela, A Coruña 15706, Spain.

Juan M Falcon-Perez (JM)

Centro de investigación Biomedica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd), Instituto de salud Carlos III, 28029 Madrid, Spain; Metabolomics Platform, Center for Cooperative Research in Biosciences (CIC bioGUNE), Basque Research and Technology Alliance (BRTA), Bizkaia Technology Park, 48160 Derio, Spain; IKERBASQUE, Basque Foundation for Science, Bilbao, Bizkaia 48009, Spain.

Patricia Aspichueta (P)

Centro de investigación Biomedica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd), Instituto de salud Carlos III, 28029 Madrid, Spain; Department of Physiology, Faculty of Medicine and Nursing, University of the Basque Country UPV/EHU, Leioa, Spain; Biocruces Bizkaia Health Research Institute, Barakaldo, Spain.

Juan Rodríguez-Cuesta (J)

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

Marina Porcelli (M)

Department of Precision Medicine, University of Campania "Luigi Vanvitelli", Via Luigi De Crecchio 7, 80138 Naples, Italy.

María A Pajares (MA)

Centro de Investigaciones Biológicas Margarita Salas (CSIC), Ramiro de Maeztu 9, 28040 Madrid, Spain.

Cristina Ameneiro (C)

Stem Cells and Human Diseases, CIMUS, University of Santiago de Compostela, Instituto de Investigación Sanitaria de Santiago de Compostela (IDIS), Santiago de Compostela, A Coruña 15706, Spain.

Miguel Fidalgo (M)

Stem Cells and Human Diseases, CIMUS, University of Santiago de Compostela, Instituto de Investigación Sanitaria de Santiago de Compostela (IDIS), Santiago de Compostela, A Coruña 15706, Spain.

Ana M Aransay (AM)

Genome Analysis Plataform, Center for Cooperative Research in Biosciences (CIC bioGUNE), Basque Research and Technology Alliance (BRTA), Bizkaia Technology Park, 48160 Derio, Spain.

Tomas Lama-Díaz (T)

DNA Repair and Genome Integrity Laboratory, CIMUS, University of Santiago de Compostela, Instituto de Investigación Sanitaria de Santiago de Compostela (IDIS), Santiago de Compostela, A Coruña 15706, Spain.

Miguel G Blanco (MG)

DNA Repair and Genome Integrity Laboratory, CIMUS, University of Santiago de Compostela, Instituto de Investigación Sanitaria de Santiago de Compostela (IDIS), Santiago de Compostela, A Coruña 15706, Spain; Department of Biochemistry and Molecular Biology, University of Santiago de Compostela, Plaza do Obradoiro s/n, Santiago de Compostela, Spain.

Miguel López (M)

Department of Physiology, CIMUS, University of Santiago de Compostela, Instituto de Investigación Sanitaria de Santiago de Compostela (IDIS), Santiago de Compostela, A Coruña 15706, Spain; CIBER Fisiopatología de la Obesidad y Nutrición (CIBERobn), Santiago de Compostela, A Coruña 15706, Spain.

Ricardo Villa-Bellosta (R)

Department of Biochemistry and Molecular Biology, University of Santiago de Compostela, Plaza do Obradoiro s/n, Santiago de Compostela, Spain; Metabolic Homeostasis and Vascular Calcification Laboratory, Center for Research in Molecular Medicine and Chronic Diseases (CiMUS), Universidade de Santiago de Compostela, Santiago de Compostela, A Coruña 15706, Spain.

Timo D Müller (TD)

Institute for Diabetes and Obesity, Helmholtz Zentrum Munich, and German Center for Diabetes Research (DZD), 85764 Neuherberg, Germany.

Rubén Nogueiras (R)

Department of Physiology, CIMUS, University of Santiago de Compostela, Instituto de Investigación Sanitaria de Santiago de Compostela (IDIS), Santiago de Compostela, A Coruña 15706, Spain; CIBER Fisiopatología de la Obesidad y Nutrición (CIBERobn), Santiago de Compostela, A Coruña 15706, Spain; Oportunius Program, Galician Agency of Innovation (GAIN), Xunta de Galicia, Santiago de Compostela, A Coruña, Spain.

Ashwin Woodhoo (A)

Gene Regulatory Control in Disease Laboratory, Center for Research in Molecular Medicine and Chronic Diseases (CIMUS), Instituto de Investigación Sanitaria de Santiago de Compostela (IDIS), University of Santiago de Compostela, Santiago de Compostela, A Coruña 15706, Spain; Nerve Disorders Laboratory, Center for Cooperative Research in Biosciences (CIC bioGUNE), Basque Research and Technology Alliance (BRTA), Bizkaia Technology Park, 48160 Derio, Spain; IKERBASQUE, Basque Foundation for Science, Bilbao, Bizkaia 48009, Spain; Oportunius Program, Galician Agency of Innovation (GAIN), Xunta de Galicia, Santiago de Compostela, A Coruña, Spain; Department of Functional Biology, University of Santiago de Compostela, Plaza do Obradoiro s/n, Santiago de Compostela, Spain.

María Luz Martínez-Chantar (ML)

Liver Disease Laboratory, Center for Cooperative Research in Biosciences (CIC bioGUNE), Basque Research and Technology Alliance (BRTA), Bizkaia Technology Park, 48160 Derio, Spain; Centro de investigación Biomedica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd), Instituto de salud Carlos III, 28029 Madrid, Spain. Electronic address: mlmartinez@cicbiogune.es.

Marta Varela-Rey (M)

Gene Regulatory Control in Disease Laboratory, Center for Research in Molecular Medicine and Chronic Diseases (CIMUS), Instituto de Investigación Sanitaria de Santiago de Compostela (IDIS), University of Santiago de Compostela, Santiago de Compostela, A Coruña 15706, Spain; Liver Disease Laboratory, Center for Cooperative Research in Biosciences (CIC bioGUNE), Basque Research and Technology Alliance (BRTA), Bizkaia Technology Park, 48160 Derio, Spain; Centro de investigación Biomedica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd), Instituto de salud Carlos III, 28029 Madrid, Spain; Department of Biochemistry and Molecular Biology, University of Santiago de Compostela, Plaza do Obradoiro s/n, Santiago de Compostela, Spain. Electronic address: martavarela.rey@usc.es.

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