Dietary Marine Oils Selectively Decrease Obesogenic Diet-Derived Carbonylation in Proteins Involved in ATP Homeostasis and Glutamate Metabolism in the Rat Cerebellum

The regular intake of diets high in saturated fat and sugars increases oxidative stress and has been linked to cognitive decline and premature brain aging. The cerebellum is highly vulnerable to oxidative stress and thus, obesogenic diets might be particularly detrimental to this tissue. However, th...

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Main Authors: Francisco Moreno, Lucía Méndez, Ana Raner, Bernat Miralles-Pérez, Marta Romeu, Sara Ramos-Romero, Josep Lluís Torres, Isabel Medina
Format: Article
Language:English
Published: MDPI AG 2024-01-01
Series:Antioxidants
Subjects:
Online Access:https://www.mdpi.com/2076-3921/13/1/103
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author Francisco Moreno
Lucía Méndez
Ana Raner
Bernat Miralles-Pérez
Marta Romeu
Sara Ramos-Romero
Josep Lluís Torres
Isabel Medina
author_facet Francisco Moreno
Lucía Méndez
Ana Raner
Bernat Miralles-Pérez
Marta Romeu
Sara Ramos-Romero
Josep Lluís Torres
Isabel Medina
author_sort Francisco Moreno
collection DOAJ
description The regular intake of diets high in saturated fat and sugars increases oxidative stress and has been linked to cognitive decline and premature brain aging. The cerebellum is highly vulnerable to oxidative stress and thus, obesogenic diets might be particularly detrimental to this tissue. However, the precise molecular mechanisms behind obesity-related brain damage are still not clear. Since protein carbonylation, a biomarker of oxidative stress, influences protein functions and is involved in metabolic control, the current investigation addressed the effect of long-term high-fat and high-sucrose diet intake on the cerebellum of Sprague-Dawley rats by deciphering the changes caused in the carbonylated proteome. The antioxidant effects of fish oil supplementation on cerebellar carbonylated proteins were also investigated. Lipid peroxidation products and carbonylated proteins were identified and quantified using immunoassays and 2D-LC-MS/MS in the cerebellum. After 21 weeks of nutritional intervention, the obesogenic diet selectively increased carbonylation of the proteins that participate in ATP homeostasis and glutamate metabolism in the cerebellum. Moreover, the data demonstrated that fish oil supplementation restrained carbonylation of the main protein targets oxidatively damaged by the obesogenic diet, and additionally protected against carbonylation of several other proteins involved in amino acid biosynthesis and neurotransmission. Therefore, dietary interventions with fish oils could help the cerebellum to be more resilient to oxidative damage. The results could shed some light on the effect of high-fat and high-sucrose diets on redox homeostasis in the cerebellum and boost the development of antioxidant-based nutritional interventions to improve cerebellum health.
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spelling doaj.art-e44527d75a50480eb30e4d0dc7944bb02024-01-26T14:41:51ZengMDPI AGAntioxidants2076-39212024-01-0113110310.3390/antiox13010103Dietary Marine Oils Selectively Decrease Obesogenic Diet-Derived Carbonylation in Proteins Involved in ATP Homeostasis and Glutamate Metabolism in the Rat CerebellumFrancisco Moreno0Lucía Méndez1Ana Raner2Bernat Miralles-Pérez3Marta Romeu4Sara Ramos-Romero5Josep Lluís Torres6Isabel Medina7Instituto de Investigaciones Marinas—Consejo Superior de Investigaciones Científicas (IIM-CSIC), Eduardo Cabello 6, E-36208 Vigo, SpainInstituto de Investigaciones Marinas—Consejo Superior de Investigaciones Científicas (IIM-CSIC), Eduardo Cabello 6, E-36208 Vigo, SpainInstituto de Investigaciones Marinas—Consejo Superior de Investigaciones Científicas (IIM-CSIC), Eduardo Cabello 6, E-36208 Vigo, SpainUnidad de Farmacología, Facultad de Medicina y Ciencias de la Salud, Universidad Rovira i Virgili, Sant Llorenç 21, E-43201 Reus, SpainUnidad de Farmacología, Facultad de Medicina y Ciencias de la Salud, Universidad Rovira i Virgili, Sant Llorenç 21, E-43201 Reus, SpainDepartment of Cell Biology, Physiology and Immunology, Faculty of Biology, University of Barcelona, Av Diagonal 643, E-08028 Barcelona, SpainNutrition & Food Safety Research Institute (INSA-UB), Maria de Maeztu Unit of Excellence, E-08921 Santa Coloma de Gramenet, SpainInstituto de Investigaciones Marinas—Consejo Superior de Investigaciones Científicas (IIM-CSIC), Eduardo Cabello 6, E-36208 Vigo, SpainThe regular intake of diets high in saturated fat and sugars increases oxidative stress and has been linked to cognitive decline and premature brain aging. The cerebellum is highly vulnerable to oxidative stress and thus, obesogenic diets might be particularly detrimental to this tissue. However, the precise molecular mechanisms behind obesity-related brain damage are still not clear. Since protein carbonylation, a biomarker of oxidative stress, influences protein functions and is involved in metabolic control, the current investigation addressed the effect of long-term high-fat and high-sucrose diet intake on the cerebellum of Sprague-Dawley rats by deciphering the changes caused in the carbonylated proteome. The antioxidant effects of fish oil supplementation on cerebellar carbonylated proteins were also investigated. Lipid peroxidation products and carbonylated proteins were identified and quantified using immunoassays and 2D-LC-MS/MS in the cerebellum. After 21 weeks of nutritional intervention, the obesogenic diet selectively increased carbonylation of the proteins that participate in ATP homeostasis and glutamate metabolism in the cerebellum. Moreover, the data demonstrated that fish oil supplementation restrained carbonylation of the main protein targets oxidatively damaged by the obesogenic diet, and additionally protected against carbonylation of several other proteins involved in amino acid biosynthesis and neurotransmission. Therefore, dietary interventions with fish oils could help the cerebellum to be more resilient to oxidative damage. The results could shed some light on the effect of high-fat and high-sucrose diets on redox homeostasis in the cerebellum and boost the development of antioxidant-based nutritional interventions to improve cerebellum health.https://www.mdpi.com/2076-3921/13/1/103omega-3 fish oilhigh-fat and high-sucrose dietprediabetesprotein carbonylationcerebellumoxidative stress
spellingShingle Francisco Moreno
Lucía Méndez
Ana Raner
Bernat Miralles-Pérez
Marta Romeu
Sara Ramos-Romero
Josep Lluís Torres
Isabel Medina
Dietary Marine Oils Selectively Decrease Obesogenic Diet-Derived Carbonylation in Proteins Involved in ATP Homeostasis and Glutamate Metabolism in the Rat Cerebellum
Antioxidants
omega-3 fish oil
high-fat and high-sucrose diet
prediabetes
protein carbonylation
cerebellum
oxidative stress
title Dietary Marine Oils Selectively Decrease Obesogenic Diet-Derived Carbonylation in Proteins Involved in ATP Homeostasis and Glutamate Metabolism in the Rat Cerebellum
title_full Dietary Marine Oils Selectively Decrease Obesogenic Diet-Derived Carbonylation in Proteins Involved in ATP Homeostasis and Glutamate Metabolism in the Rat Cerebellum
title_fullStr Dietary Marine Oils Selectively Decrease Obesogenic Diet-Derived Carbonylation in Proteins Involved in ATP Homeostasis and Glutamate Metabolism in the Rat Cerebellum
title_full_unstemmed Dietary Marine Oils Selectively Decrease Obesogenic Diet-Derived Carbonylation in Proteins Involved in ATP Homeostasis and Glutamate Metabolism in the Rat Cerebellum
title_short Dietary Marine Oils Selectively Decrease Obesogenic Diet-Derived Carbonylation in Proteins Involved in ATP Homeostasis and Glutamate Metabolism in the Rat Cerebellum
title_sort dietary marine oils selectively decrease obesogenic diet derived carbonylation in proteins involved in atp homeostasis and glutamate metabolism in the rat cerebellum
topic omega-3 fish oil
high-fat and high-sucrose diet
prediabetes
protein carbonylation
cerebellum
oxidative stress
url https://www.mdpi.com/2076-3921/13/1/103
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