<i>Agaricus</i> Mushroom-Enriched Diets Modulate the Microbiota-Gut-Brain Axis and Reduce Brain Oxidative Stress in Mice

Neurodegenerative diseases pose a major problem for developed countries, and stress has been identified as one of the main risk factors in the development of these disorders. Here, we have examined the protective properties against brain oxidative stress of two diets supplemented with 5% (<i>w...

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Main Authors: Josune García-Sanmartín, Miriam Bobadilla, Eduardo Mirpuri, Vanessa Grifoll, Margarita Pérez-Clavijo, Alfredo Martínez
Format: Article
Language:English
Published: MDPI AG 2022-03-01
Series:Antioxidants
Subjects:
Online Access:https://www.mdpi.com/2076-3921/11/4/695
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author Josune García-Sanmartín
Miriam Bobadilla
Eduardo Mirpuri
Vanessa Grifoll
Margarita Pérez-Clavijo
Alfredo Martínez
author_facet Josune García-Sanmartín
Miriam Bobadilla
Eduardo Mirpuri
Vanessa Grifoll
Margarita Pérez-Clavijo
Alfredo Martínez
author_sort Josune García-Sanmartín
collection DOAJ
description Neurodegenerative diseases pose a major problem for developed countries, and stress has been identified as one of the main risk factors in the development of these disorders. Here, we have examined the protective properties against brain oxidative stress of two diets supplemented with 5% (<i>w</i>/<i>w</i>) of <i>Agaricus bisporus</i> (white button mushroom) or <i>Agaricus bisporus brunnescens</i> (Portobello mushroom) in mice. These diets did not modify the weight gain of the animals when compared to those fed with a regular diet, even after feeding on them for 15 weeks. The long-term modification of the microbiota after 12 weeks on the diets was investigated. At the phylum level, there was a large increase of <i>Verrucomicrobia</i> and a reduction of <i>Cyanobacteria</i> associated with the mushroom diets. No changes were observed in the <i>Firmicutes/Bacteroidetes</i> ratio, whose stability is a marker for a healthy diet. At the family level, three groups presented significant variations. These included <i>Akkermansiaceae</i> and <i>Tannerellaceae</i>, which significantly increased with both diets; and <i>Prevotellaceae</i>, which significantly decreased with both diets. These bacteria participate in the generation of microbiota-derived short-chain fatty acids (SCFAs) and provide a link between the microbiota and the brain. Mice subjected to restraint stress showed an upregulation of <i>Il-6</i>, <i>Nox-2</i>, and <i>Hmox-1</i> expression; a reduction in the enzymatic activities of catalase and superoxide dismutase; and an increase in lipid peroxidation in their brains. All these parameters were significantly prevented by feeding for 3 weeks on the <i>Agaricus</i>-supplemented diets. In summary, the supplementation of a healthy diet with <i>Agaricus</i> mushrooms may significantly contribute to prevent neurodegenerative diseases in the general population.
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spelling doaj.art-2fc6f270832c491c9f73676589cc06532023-12-01T00:35:15ZengMDPI AGAntioxidants2076-39212022-03-0111469510.3390/antiox11040695<i>Agaricus</i> Mushroom-Enriched Diets Modulate the Microbiota-Gut-Brain Axis and Reduce Brain Oxidative Stress in MiceJosune García-Sanmartín0Miriam Bobadilla1Eduardo Mirpuri2Vanessa Grifoll3Margarita Pérez-Clavijo4Alfredo Martínez5Oncology Area, Center for Biomedical Research of La Rioja (CIBIR), 26006 Logroño, SpainOncology Area, Center for Biomedical Research of La Rioja (CIBIR), 26006 Logroño, SpainOncology Area, Center for Biomedical Research of La Rioja (CIBIR), 26006 Logroño, SpainCentro Tecnológico de Investigación del Champiñón de La Rioja (CTICH), 26560 Autol, SpainCentro Tecnológico de Investigación del Champiñón de La Rioja (CTICH), 26560 Autol, SpainOncology Area, Center for Biomedical Research of La Rioja (CIBIR), 26006 Logroño, SpainNeurodegenerative diseases pose a major problem for developed countries, and stress has been identified as one of the main risk factors in the development of these disorders. Here, we have examined the protective properties against brain oxidative stress of two diets supplemented with 5% (<i>w</i>/<i>w</i>) of <i>Agaricus bisporus</i> (white button mushroom) or <i>Agaricus bisporus brunnescens</i> (Portobello mushroom) in mice. These diets did not modify the weight gain of the animals when compared to those fed with a regular diet, even after feeding on them for 15 weeks. The long-term modification of the microbiota after 12 weeks on the diets was investigated. At the phylum level, there was a large increase of <i>Verrucomicrobia</i> and a reduction of <i>Cyanobacteria</i> associated with the mushroom diets. No changes were observed in the <i>Firmicutes/Bacteroidetes</i> ratio, whose stability is a marker for a healthy diet. At the family level, three groups presented significant variations. These included <i>Akkermansiaceae</i> and <i>Tannerellaceae</i>, which significantly increased with both diets; and <i>Prevotellaceae</i>, which significantly decreased with both diets. These bacteria participate in the generation of microbiota-derived short-chain fatty acids (SCFAs) and provide a link between the microbiota and the brain. Mice subjected to restraint stress showed an upregulation of <i>Il-6</i>, <i>Nox-2</i>, and <i>Hmox-1</i> expression; a reduction in the enzymatic activities of catalase and superoxide dismutase; and an increase in lipid peroxidation in their brains. All these parameters were significantly prevented by feeding for 3 weeks on the <i>Agaricus</i>-supplemented diets. In summary, the supplementation of a healthy diet with <i>Agaricus</i> mushrooms may significantly contribute to prevent neurodegenerative diseases in the general population.https://www.mdpi.com/2076-3921/11/4/695microbiota-gut-brain axisneurodegenerative diseasesbrain oxidative stress<i>Agaricus</i>-supplemented dietsantioxidant activitieslipid peroxidation
spellingShingle Josune García-Sanmartín
Miriam Bobadilla
Eduardo Mirpuri
Vanessa Grifoll
Margarita Pérez-Clavijo
Alfredo Martínez
<i>Agaricus</i> Mushroom-Enriched Diets Modulate the Microbiota-Gut-Brain Axis and Reduce Brain Oxidative Stress in Mice
Antioxidants
microbiota-gut-brain axis
neurodegenerative diseases
brain oxidative stress
<i>Agaricus</i>-supplemented diets
antioxidant activities
lipid peroxidation
title <i>Agaricus</i> Mushroom-Enriched Diets Modulate the Microbiota-Gut-Brain Axis and Reduce Brain Oxidative Stress in Mice
title_full <i>Agaricus</i> Mushroom-Enriched Diets Modulate the Microbiota-Gut-Brain Axis and Reduce Brain Oxidative Stress in Mice
title_fullStr <i>Agaricus</i> Mushroom-Enriched Diets Modulate the Microbiota-Gut-Brain Axis and Reduce Brain Oxidative Stress in Mice
title_full_unstemmed <i>Agaricus</i> Mushroom-Enriched Diets Modulate the Microbiota-Gut-Brain Axis and Reduce Brain Oxidative Stress in Mice
title_short <i>Agaricus</i> Mushroom-Enriched Diets Modulate the Microbiota-Gut-Brain Axis and Reduce Brain Oxidative Stress in Mice
title_sort i agaricus i mushroom enriched diets modulate the microbiota gut brain axis and reduce brain oxidative stress in mice
topic microbiota-gut-brain axis
neurodegenerative diseases
brain oxidative stress
<i>Agaricus</i>-supplemented diets
antioxidant activities
lipid peroxidation
url https://www.mdpi.com/2076-3921/11/4/695
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