CPT1C deficiency in SF1 neurons impairs early metabolic adaptation to dietary fats, leading to obesity

Objectives: SF1 neurons of the ventromedial hypothalamus (VMH) play a pivotal role in regulating body weight and adiposity, particularly in response to a high-fat diet (HFD), as well as in the recovery from insulin-induced hypoglycemia. While the brain-specific CPT1C isoform is well known for its ro...

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Main Authors: A. Fosch, D.S. Pizarro, S. Zagmutt, A.C. Reguera, G. Batallé, M. Rodríguez-García, J. García-Chica, O. Freire-Agulleiro, C. Miralpeix, P. Zizzari, D. Serra, L. Herrero, M. López, D. Cota, R. Rodríguez-Rodríguez, N. Casals
Format: Article
Language:English
Published: Elsevier 2025-06-01
Series:Molecular Metabolism
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Online Access:http://www.sciencedirect.com/science/article/pii/S2212877825000626
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author A. Fosch
D.S. Pizarro
S. Zagmutt
A.C. Reguera
G. Batallé
M. Rodríguez-García
J. García-Chica
O. Freire-Agulleiro
C. Miralpeix
P. Zizzari
D. Serra
L. Herrero
M. López
D. Cota
R. Rodríguez-Rodríguez
N. Casals
author_facet A. Fosch
D.S. Pizarro
S. Zagmutt
A.C. Reguera
G. Batallé
M. Rodríguez-García
J. García-Chica
O. Freire-Agulleiro
C. Miralpeix
P. Zizzari
D. Serra
L. Herrero
M. López
D. Cota
R. Rodríguez-Rodríguez
N. Casals
author_sort A. Fosch
collection DOAJ
description Objectives: SF1 neurons of the ventromedial hypothalamus (VMH) play a pivotal role in regulating body weight and adiposity, particularly in response to a high-fat diet (HFD), as well as in the recovery from insulin-induced hypoglycemia. While the brain-specific CPT1C isoform is well known for its role in controlling food intake and energy homeostasis, its function within specific hypothalamic neuronal populations remains largely unexplored. Here, we explore the role of CPT1C in SF1 neurons. Methods: Mice deficient in CPT1C within SF1 neurons were generated, and their response to a HFD was investigated. Results: SF1-Cpt1c-KO mice fail to adjust their caloric intake during initial HFD exposure, which is associated with impaired activation of the melanocortin system. Furthermore, these mice exhibit disrupted metabolic gene expression in the liver, muscle, and adipose tissue, leading to increased adiposity independently of food intake. In contrast, their response to glucose or insulin challenges remains intact. After long-term HFD exposure, SF1-Cpt1c-KO mice are more prone to developing obesity and glucose intolerance than control littermates, with males exhibiting a more severe phenotype. Interestingly, CPT1C deficiency in SF1 neurons also results in elevated hypothalamic endocannabinoid (eCB) levels under both chow and HFD conditions. We propose that this sustained eCB elevation reduces VMH activation by fatty acids and impairs the SF1-POMC drive upon fat intake. Conclusion: Our findings establish CPT1C in SF1 neurons as essential for VMH-driven dietary fat sensing, satiety, and lipid metabolic adaptation.
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spelling doaj-art-dce6ceb193734c2db833e638d3c5f2db2025-08-20T02:56:07ZengElsevierMolecular Metabolism2212-87782025-06-019610215510.1016/j.molmet.2025.102155CPT1C deficiency in SF1 neurons impairs early metabolic adaptation to dietary fats, leading to obesityA. Fosch0D.S. Pizarro1S. Zagmutt2A.C. Reguera3G. Batallé4M. Rodríguez-García5J. García-Chica6O. Freire-Agulleiro7C. Miralpeix8P. Zizzari9D. Serra10L. Herrero11M. López12D. Cota13R. Rodríguez-Rodríguez14N. Casals15Department of Biomedical Sciences, Faculty of Medicine and Health Sciences, Universitat Internacional de Catalunya, 08195 Sant Cugat del Vallès, SpainDepartment of Biomedical Sciences, Faculty of Medicine and Health Sciences, Universitat Internacional de Catalunya, 08195 Sant Cugat del Vallès, SpainDepartment of Biomedical Sciences, Faculty of Medicine and Health Sciences, Universitat Internacional de Catalunya, 08195 Sant Cugat del Vallès, SpainDepartment of Biomedical Sciences, Faculty of Medicine and Health Sciences, Universitat Internacional de Catalunya, 08195 Sant Cugat del Vallès, SpainDepartment of Biomedical Sciences, Faculty of Medicine and Health Sciences, Universitat Internacional de Catalunya, 08195 Sant Cugat del Vallès, SpainDepartment of Biomedical Sciences, Faculty of Medicine and Health Sciences, Universitat Internacional de Catalunya, 08195 Sant Cugat del Vallès, SpainDepartment of Biomedical Sciences, Faculty of Medicine and Health Sciences, Universitat Internacional de Catalunya, 08195 Sant Cugat del Vallès, SpainDepartment of Physiology, CIMUS, University of Santiago de Compostela-Instituto de Investigación Sanitaria, Santiago de Compostela, 15782, SpainDepartment of Biomedical Sciences, Faculty of Medicine and Health Sciences, Universitat Internacional de Catalunya, 08195 Sant Cugat del Vallès, Spain; INSERM, Neurocentre Magendie, U1215, University of Bordeaux, 3300 Bordeaux, FranceINSERM, Neurocentre Magendie, U1215, University of Bordeaux, 3300 Bordeaux, FranceDepartment of Biochemistry and Physiology, School of Pharmacy and Food Sciences, Institut de Biomedicina de la Universitat de Barcelona (IBUB), Universitat de Barcelona, Barcelona, 08028 Spain; Centro de Investigación Biomédica en Red de Fisiopatología de la Obesidad y la Nutrición (CIBEROBN), Instituto de Salud Carlos III, 28029 Madrid, SpainDepartment of Biochemistry and Physiology, School of Pharmacy and Food Sciences, Institut de Biomedicina de la Universitat de Barcelona (IBUB), Universitat de Barcelona, Barcelona, 08028 Spain; Centro de Investigación Biomédica en Red de Fisiopatología de la Obesidad y la Nutrición (CIBEROBN), Instituto de Salud Carlos III, 28029 Madrid, SpainDepartment of Physiology, CIMUS, University of Santiago de Compostela-Instituto de Investigación Sanitaria, Santiago de Compostela, 15782, Spain; Centro de Investigación Biomédica en Red de Fisiopatología de la Obesidad y la Nutrición (CIBEROBN), Instituto de Salud Carlos III, 28029 Madrid, SpainINSERM, Neurocentre Magendie, U1215, University of Bordeaux, 3300 Bordeaux, FranceDepartment of Biomedical Sciences, Faculty of Medicine and Health Sciences, Universitat Internacional de Catalunya, 08195 Sant Cugat del Vallès, Spain; Centro de Investigación Biomédica en Red de Fisiopatología de la Obesidad y la Nutrición (CIBEROBN), Instituto de Salud Carlos III, 28029 Madrid, Spain; Corresponding author. Centro de Investigación Biomédica en Red de Fisiopatología de la Obesidad y la Nutrición (CIBEROBN), Instituto de Salud Carlos III, 28029 Madrid, Spain.Department of Biomedical Sciences, Faculty of Medicine and Health Sciences, Universitat Internacional de Catalunya, 08195 Sant Cugat del Vallès, Spain; Centro de Investigación Biomédica en Red de Fisiopatología de la Obesidad y la Nutrición (CIBEROBN), Instituto de Salud Carlos III, 28029 Madrid, Spain; Corresponding author. Centro de Investigación Biomédica en Red de Fisiopatología de la Obesidad y la Nutrición (CIBEROBN), Instituto de Salud Carlos III, 28029 Madrid, Spain.Objectives: SF1 neurons of the ventromedial hypothalamus (VMH) play a pivotal role in regulating body weight and adiposity, particularly in response to a high-fat diet (HFD), as well as in the recovery from insulin-induced hypoglycemia. While the brain-specific CPT1C isoform is well known for its role in controlling food intake and energy homeostasis, its function within specific hypothalamic neuronal populations remains largely unexplored. Here, we explore the role of CPT1C in SF1 neurons. Methods: Mice deficient in CPT1C within SF1 neurons were generated, and their response to a HFD was investigated. Results: SF1-Cpt1c-KO mice fail to adjust their caloric intake during initial HFD exposure, which is associated with impaired activation of the melanocortin system. Furthermore, these mice exhibit disrupted metabolic gene expression in the liver, muscle, and adipose tissue, leading to increased adiposity independently of food intake. In contrast, their response to glucose or insulin challenges remains intact. After long-term HFD exposure, SF1-Cpt1c-KO mice are more prone to developing obesity and glucose intolerance than control littermates, with males exhibiting a more severe phenotype. Interestingly, CPT1C deficiency in SF1 neurons also results in elevated hypothalamic endocannabinoid (eCB) levels under both chow and HFD conditions. We propose that this sustained eCB elevation reduces VMH activation by fatty acids and impairs the SF1-POMC drive upon fat intake. Conclusion: Our findings establish CPT1C in SF1 neurons as essential for VMH-driven dietary fat sensing, satiety, and lipid metabolic adaptation.http://www.sciencedirect.com/science/article/pii/S2212877825000626CPT1CSF1 neuronsHigh-fat dietEndocannabinoidsAdiposityFood intake
spellingShingle A. Fosch
D.S. Pizarro
S. Zagmutt
A.C. Reguera
G. Batallé
M. Rodríguez-García
J. García-Chica
O. Freire-Agulleiro
C. Miralpeix
P. Zizzari
D. Serra
L. Herrero
M. López
D. Cota
R. Rodríguez-Rodríguez
N. Casals
CPT1C deficiency in SF1 neurons impairs early metabolic adaptation to dietary fats, leading to obesity
Molecular Metabolism
CPT1C
SF1 neurons
High-fat diet
Endocannabinoids
Adiposity
Food intake
title CPT1C deficiency in SF1 neurons impairs early metabolic adaptation to dietary fats, leading to obesity
title_full CPT1C deficiency in SF1 neurons impairs early metabolic adaptation to dietary fats, leading to obesity
title_fullStr CPT1C deficiency in SF1 neurons impairs early metabolic adaptation to dietary fats, leading to obesity
title_full_unstemmed CPT1C deficiency in SF1 neurons impairs early metabolic adaptation to dietary fats, leading to obesity
title_short CPT1C deficiency in SF1 neurons impairs early metabolic adaptation to dietary fats, leading to obesity
title_sort cpt1c deficiency in sf1 neurons impairs early metabolic adaptation to dietary fats leading to obesity
topic CPT1C
SF1 neurons
High-fat diet
Endocannabinoids
Adiposity
Food intake
url http://www.sciencedirect.com/science/article/pii/S2212877825000626
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