A High-Fat Diet Induces Oxidative Stress in OPA1<sup>+/−</sup> Mouse Cortices: A Critical Double Challenge

A high-fat diet (HFD) has significant effects on health, leading to cardiovascular, metabolic, neurodegenerative, and psychiatric conditions and contributing to obesity and type 2 diabetes. Mitochondria, essential for energy production and oxidative metabolism, are adversely affected by a HFD, causi...

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Main Authors: Camille Champigny, Marlène Botella, Djamaa Atamena, Sébastien Bullich, Corentin Coustham, Bruno Guiard, Pascale Belenguer, Noélie Davezac
Format: Article
Language:English
Published: MDPI AG 2025-07-01
Series:Antioxidants
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Online Access:https://www.mdpi.com/2076-3921/14/7/876
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author Camille Champigny
Marlène Botella
Djamaa Atamena
Sébastien Bullich
Corentin Coustham
Bruno Guiard
Pascale Belenguer
Noélie Davezac
author_facet Camille Champigny
Marlène Botella
Djamaa Atamena
Sébastien Bullich
Corentin Coustham
Bruno Guiard
Pascale Belenguer
Noélie Davezac
author_sort Camille Champigny
collection DOAJ
description A high-fat diet (HFD) has significant effects on health, leading to cardiovascular, metabolic, neurodegenerative, and psychiatric conditions and contributing to obesity and type 2 diabetes. Mitochondria, essential for energy production and oxidative metabolism, are adversely affected by a HFD, causing oxidative stress and impaired cellular function. Mutations in the <i>OPA1</i> (OPtic Atrophy 1) gene, crucial for mitochondrial dynamics and functions, are responsible for dominant optic atrophy (DOA), a mitochondrial neurodegenerative disease associated with increased reactive oxygen species (ROS). The expressivity of DOA is highly variable, even within the same family. This suggests that both modifying genetics and environmental factors could influence the penetrance of the disease. We previously demonstrated that genetic background modulates DOA expressivity and now ask if this is also the case for external cues. We thus explore how OPA1 deficiency interacts with HFD-induced metabolic disturbances, hypothesizing that long-term HFD consumption impairs brain mitochondrial function and disrupts oxidative metabolism. OPA1<sup>+/−</sup> mice were thus subjected to a HFD for a period of 12 weeks, and ROS levels and the expression of antioxidant genes were evaluated by Western blot and spectrophotometry. Cortices from high-fat diet-fed OPA1<sup>+/−</sup> mice showed lower aconitase activity than those of their wild-type (WT) litter mates, indicative of an unbalanced increase in mitochondrial ROS. Accordingly, OPA1<sup>+/−</sup> mice present lower levels of the antioxidant enzyme superoxide dismutase 2 compared to WT mice. Therefore, this study (i) reveals the onset of oxidative stress in brain cortices from OPA1<sup>+/−</sup> mice challenged with a HFD, (ii) shows that diet is a modifying factor for DOA, and (iii) suggests that food control could be used to moderate the severity of the disease.
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spelling doaj-art-bfc0203e9a0e46d4bb24074d6a542cf62025-08-20T03:13:39ZengMDPI AGAntioxidants2076-39212025-07-0114787610.3390/antiox14070876A High-Fat Diet Induces Oxidative Stress in OPA1<sup>+/−</sup> Mouse Cortices: A Critical Double ChallengeCamille Champigny0Marlène Botella1Djamaa Atamena2Sébastien Bullich3Corentin Coustham4Bruno Guiard5Pascale Belenguer6Noélie Davezac7Got-It Team, RESTORE—University of Toulouse, CNRS ERL5311, EFS, INP-ENVT, Inserm U1031, Bâtiment INCERE, 4bis avenue Hubert Curien, 31100 Toulouse, FranceMinding Team, Research Center on Animal Cognition (CRCA), Center of Integrative Biology (CBI)—University of Toulouse, CNRS, 31067 Toulouse, FranceMinding Team, Research Center on Animal Cognition (CRCA), Center of Integrative Biology (CBI)—University of Toulouse, CNRS, 31067 Toulouse, FranceRemember Team, Research Center on Animal Cognition (CRCA), Center of Integrative Biology (CBI)—University of Toulouse, CNRS, 31067 Toulouse, FranceGot-It Team, RESTORE—University of Toulouse, CNRS ERL5311, EFS, INP-ENVT, Inserm U1031, Bâtiment INCERE, 4bis avenue Hubert Curien, 31100 Toulouse, FranceRemember Team, Research Center on Animal Cognition (CRCA), Center of Integrative Biology (CBI)—University of Toulouse, CNRS, 31067 Toulouse, FranceMinding Team, Research Center on Animal Cognition (CRCA), Center of Integrative Biology (CBI)—University of Toulouse, CNRS, 31067 Toulouse, FranceGot-It Team, RESTORE—University of Toulouse, CNRS ERL5311, EFS, INP-ENVT, Inserm U1031, Bâtiment INCERE, 4bis avenue Hubert Curien, 31100 Toulouse, FranceA high-fat diet (HFD) has significant effects on health, leading to cardiovascular, metabolic, neurodegenerative, and psychiatric conditions and contributing to obesity and type 2 diabetes. Mitochondria, essential for energy production and oxidative metabolism, are adversely affected by a HFD, causing oxidative stress and impaired cellular function. Mutations in the <i>OPA1</i> (OPtic Atrophy 1) gene, crucial for mitochondrial dynamics and functions, are responsible for dominant optic atrophy (DOA), a mitochondrial neurodegenerative disease associated with increased reactive oxygen species (ROS). The expressivity of DOA is highly variable, even within the same family. This suggests that both modifying genetics and environmental factors could influence the penetrance of the disease. We previously demonstrated that genetic background modulates DOA expressivity and now ask if this is also the case for external cues. We thus explore how OPA1 deficiency interacts with HFD-induced metabolic disturbances, hypothesizing that long-term HFD consumption impairs brain mitochondrial function and disrupts oxidative metabolism. OPA1<sup>+/−</sup> mice were thus subjected to a HFD for a period of 12 weeks, and ROS levels and the expression of antioxidant genes were evaluated by Western blot and spectrophotometry. Cortices from high-fat diet-fed OPA1<sup>+/−</sup> mice showed lower aconitase activity than those of their wild-type (WT) litter mates, indicative of an unbalanced increase in mitochondrial ROS. Accordingly, OPA1<sup>+/−</sup> mice present lower levels of the antioxidant enzyme superoxide dismutase 2 compared to WT mice. Therefore, this study (i) reveals the onset of oxidative stress in brain cortices from OPA1<sup>+/−</sup> mice challenged with a HFD, (ii) shows that diet is a modifying factor for DOA, and (iii) suggests that food control could be used to moderate the severity of the disease.https://www.mdpi.com/2076-3921/14/7/876corticesantioxidant defensesmitochondriaOPA1neurodegenerative disease
spellingShingle Camille Champigny
Marlène Botella
Djamaa Atamena
Sébastien Bullich
Corentin Coustham
Bruno Guiard
Pascale Belenguer
Noélie Davezac
A High-Fat Diet Induces Oxidative Stress in OPA1<sup>+/−</sup> Mouse Cortices: A Critical Double Challenge
Antioxidants
cortices
antioxidant defenses
mitochondria
OPA1
neurodegenerative disease
title A High-Fat Diet Induces Oxidative Stress in OPA1<sup>+/−</sup> Mouse Cortices: A Critical Double Challenge
title_full A High-Fat Diet Induces Oxidative Stress in OPA1<sup>+/−</sup> Mouse Cortices: A Critical Double Challenge
title_fullStr A High-Fat Diet Induces Oxidative Stress in OPA1<sup>+/−</sup> Mouse Cortices: A Critical Double Challenge
title_full_unstemmed A High-Fat Diet Induces Oxidative Stress in OPA1<sup>+/−</sup> Mouse Cortices: A Critical Double Challenge
title_short A High-Fat Diet Induces Oxidative Stress in OPA1<sup>+/−</sup> Mouse Cortices: A Critical Double Challenge
title_sort high fat diet induces oxidative stress in opa1 sup sup mouse cortices a critical double challenge
topic cortices
antioxidant defenses
mitochondria
OPA1
neurodegenerative disease
url https://www.mdpi.com/2076-3921/14/7/876
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