Genoprotective activity of the Pleurotus eryngii mushrooms following their in vitro and in vivo fermentation by fecal microbiota

Pleurotus eryngii mushrooms are commercially cultivated and widely consumed due to their organoleptic properties, and the low caloric and high nutritional value. In addition, they contain various biologically active and health-promoting compounds; very recently, their genoprotective effect in Caco-2...

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Main Authors: Athina Boulaka, Panagiota Mantellou, Gabriela-Monica Stanc, Efthymia Souka, Christoς Valavanis, Georgia Saxami, Evdokia Mitsou, Georgios Koutrotsios, Georgios I. Zervakis, Adamantini Kyriacou, Vasiliki Pletsa, Panagiotis Georgiadis
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-08-01
Series:Frontiers in Nutrition
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnut.2022.988517/full
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author Athina Boulaka
Panagiota Mantellou
Panagiota Mantellou
Gabriela-Monica Stanc
Efthymia Souka
Christoς Valavanis
Georgia Saxami
Evdokia Mitsou
Georgios Koutrotsios
Georgios I. Zervakis
Adamantini Kyriacou
Vasiliki Pletsa
Panagiotis Georgiadis
author_facet Athina Boulaka
Panagiota Mantellou
Panagiota Mantellou
Gabriela-Monica Stanc
Efthymia Souka
Christoς Valavanis
Georgia Saxami
Evdokia Mitsou
Georgios Koutrotsios
Georgios I. Zervakis
Adamantini Kyriacou
Vasiliki Pletsa
Panagiotis Georgiadis
author_sort Athina Boulaka
collection DOAJ
description Pleurotus eryngii mushrooms are commercially cultivated and widely consumed due to their organoleptic properties, and the low caloric and high nutritional value. In addition, they contain various biologically active and health-promoting compounds; very recently, their genoprotective effect in Caco-2 cells after their fermentation by the human fecal microbiota was also documented. In the current study, the effect of P. eryngii pre- and post-fermentation supernatants in micronuclei formation was evaluated in human lymphocytes. In addition, the genoprotective properties of increasing concentrations of aqueous extracts from P. eryngii mushrooms (150, 300, 600 mg/kg) against the cyclophosphamide-induced DNA damage were studied in young and elderly female and male mice in bone marrow and whole blood cells. The ability of the highest dose (600 mg/kg) to regulate the main cellular signaling pathways was also evaluated in gut and liver tissues of female animals by quantifying the mRNA expression of NrF2, Nfkβ, DNMT1, and IL-22 genes. P. eryngii post-fermentation, but not pre-fermentation, supernatants were able to protect human lymphocytes from the mitomycin C-induced DNA damage in a dose-dependent manner. Similarly, genoprotection was also observed in bone marrow cells of mice treated by gavage with P. eryngii extract. The effect was observed in all the experimental groups of mice (young and elderly, male and female) and was more potent in young female mice. Overexpression of all genes examined was observed in both tissues, mainly among the elderly animals. In conclusion, P. eryngii mushrooms were shown to maintain genome integrity through protecting cells from genotoxic insults. These beneficial effects can be attributed to their antioxidant and immunomodulatory properties, as well as their ability to regulate the cell’s epigenetic mechanisms and maintain cell homeostasis.
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spelling doaj.art-0ecc11d0f6104542acd952dc1816443c2022-12-22T02:35:09ZengFrontiers Media S.A.Frontiers in Nutrition2296-861X2022-08-01910.3389/fnut.2022.988517988517Genoprotective activity of the Pleurotus eryngii mushrooms following their in vitro and in vivo fermentation by fecal microbiotaAthina Boulaka0Panagiota Mantellou1Panagiota Mantellou2Gabriela-Monica Stanc3Efthymia Souka4Christoς Valavanis5Georgia Saxami6Evdokia Mitsou7Georgios Koutrotsios8Georgios I. Zervakis9Adamantini Kyriacou10Vasiliki Pletsa11Panagiotis Georgiadis12Laboratory of Environment and Health, Institute of Chemical Biology, National Hellenic Research Foundation, Athens, GreeceLaboratory of Environment and Health, Institute of Chemical Biology, National Hellenic Research Foundation, Athens, GreeceDepartment of Biological Applications and Technology, University of Ioannina, Ioannina, GreeceDepartment of Pathology, Molecular Pathology Unit, Metaxa Cancer Hospital, Piraeus, GreeceDepartment of Pathology, Molecular Pathology Unit, Metaxa Cancer Hospital, Piraeus, GreeceDepartment of Pathology, Molecular Pathology Unit, Metaxa Cancer Hospital, Piraeus, GreeceDepartment of Nutrition and Dietetics, Harokopio University, Athens, GreeceDepartment of Nutrition and Dietetics, Harokopio University, Athens, GreeceLaboratory of General and Agricultural Microbiology, Agricultural University of Athens, Athens, GreeceLaboratory of General and Agricultural Microbiology, Agricultural University of Athens, Athens, GreeceDepartment of Nutrition and Dietetics, Harokopio University, Athens, GreeceLaboratory of Environment and Health, Institute of Chemical Biology, National Hellenic Research Foundation, Athens, GreeceLaboratory of Environment and Health, Institute of Chemical Biology, National Hellenic Research Foundation, Athens, GreecePleurotus eryngii mushrooms are commercially cultivated and widely consumed due to their organoleptic properties, and the low caloric and high nutritional value. In addition, they contain various biologically active and health-promoting compounds; very recently, their genoprotective effect in Caco-2 cells after their fermentation by the human fecal microbiota was also documented. In the current study, the effect of P. eryngii pre- and post-fermentation supernatants in micronuclei formation was evaluated in human lymphocytes. In addition, the genoprotective properties of increasing concentrations of aqueous extracts from P. eryngii mushrooms (150, 300, 600 mg/kg) against the cyclophosphamide-induced DNA damage were studied in young and elderly female and male mice in bone marrow and whole blood cells. The ability of the highest dose (600 mg/kg) to regulate the main cellular signaling pathways was also evaluated in gut and liver tissues of female animals by quantifying the mRNA expression of NrF2, Nfkβ, DNMT1, and IL-22 genes. P. eryngii post-fermentation, but not pre-fermentation, supernatants were able to protect human lymphocytes from the mitomycin C-induced DNA damage in a dose-dependent manner. Similarly, genoprotection was also observed in bone marrow cells of mice treated by gavage with P. eryngii extract. The effect was observed in all the experimental groups of mice (young and elderly, male and female) and was more potent in young female mice. Overexpression of all genes examined was observed in both tissues, mainly among the elderly animals. In conclusion, P. eryngii mushrooms were shown to maintain genome integrity through protecting cells from genotoxic insults. These beneficial effects can be attributed to their antioxidant and immunomodulatory properties, as well as their ability to regulate the cell’s epigenetic mechanisms and maintain cell homeostasis.https://www.frontiersin.org/articles/10.3389/fnut.2022.988517/fullmushroomgenoprotectionanticancerCpG methylationimmunomodulationantioxidative mechanisms
spellingShingle Athina Boulaka
Panagiota Mantellou
Panagiota Mantellou
Gabriela-Monica Stanc
Efthymia Souka
Christoς Valavanis
Georgia Saxami
Evdokia Mitsou
Georgios Koutrotsios
Georgios I. Zervakis
Adamantini Kyriacou
Vasiliki Pletsa
Panagiotis Georgiadis
Genoprotective activity of the Pleurotus eryngii mushrooms following their in vitro and in vivo fermentation by fecal microbiota
Frontiers in Nutrition
mushroom
genoprotection
anticancer
CpG methylation
immunomodulation
antioxidative mechanisms
title Genoprotective activity of the Pleurotus eryngii mushrooms following their in vitro and in vivo fermentation by fecal microbiota
title_full Genoprotective activity of the Pleurotus eryngii mushrooms following their in vitro and in vivo fermentation by fecal microbiota
title_fullStr Genoprotective activity of the Pleurotus eryngii mushrooms following their in vitro and in vivo fermentation by fecal microbiota
title_full_unstemmed Genoprotective activity of the Pleurotus eryngii mushrooms following their in vitro and in vivo fermentation by fecal microbiota
title_short Genoprotective activity of the Pleurotus eryngii mushrooms following their in vitro and in vivo fermentation by fecal microbiota
title_sort genoprotective activity of the pleurotus eryngii mushrooms following their in vitro and in vivo fermentation by fecal microbiota
topic mushroom
genoprotection
anticancer
CpG methylation
immunomodulation
antioxidative mechanisms
url https://www.frontiersin.org/articles/10.3389/fnut.2022.988517/full
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