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Opposing Epigenetic Signatures in Human Sperm by Intake of Fast Food Versus Healthy Food

Animal experiments have demonstrated that diets high in fats create a harmful environment for developing sperm cells, contributing to impaired reproductive health and induced risk for chronic diseases in the next generation. Changes at the level of the epigenome have been suggested to underlie these...

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Autores principales: Soubry, Adelheid, Murphy, Susan K., Vansant, Greet, He, Yang, Price, Thomas M., Hoyo, Cathrine
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8103543/
https://www.ncbi.nlm.nih.gov/pubmed/33967953
http://dx.doi.org/10.3389/fendo.2021.625204
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author Soubry, Adelheid
Murphy, Susan K.
Vansant, Greet
He, Yang
Price, Thomas M.
Hoyo, Cathrine
author_facet Soubry, Adelheid
Murphy, Susan K.
Vansant, Greet
He, Yang
Price, Thomas M.
Hoyo, Cathrine
author_sort Soubry, Adelheid
collection PubMed
description Animal experiments have demonstrated that diets high in fats create a harmful environment for developing sperm cells, contributing to impaired reproductive health and induced risk for chronic diseases in the next generation. Changes at the level of the epigenome have been suggested to underlie these observations. Human data are limited to verify this hypothesis. While we earlier demonstrated a link between male obesity and DNA methylation changes at imprinted genes in mature sperm cells and newborns, it is currently unknown if -or how- a paternal eating pattern (related to obesity) is related to indices for epigenetic inheritance. We here aim to examine a yet unexplored link between consumption of healthy (rich in vitamins and fibers) or unhealthy (“fast”) foods and methylation at imprint regulatory regions in DNA of sperm. We obtained semen and data from 67 men, as part of a North Carolina-based study: The Influence of the Environment on Gametic Epigenetic Reprogramming (TIEGER) study. Dietary data included intake of fruits/nuts, vegetables/soups, whole grain bread, meat, seafood/fish, and fatty or processed food items. Multiple regression models were used to explore the association between dietary habits and clinical sperm parameters as well as DNA methylation levels, quantified using bisulfite pyrosequencing at 12 differentially methylated regions (DMRs) of the following imprinted genes: GRB10, IGF2, H19, MEG3, NDN, NNAT, PEG1/MEST, PEG3, PLAGL1, SNRPN, and SGCE/PEG10. After adjusting for age, obesity status and recruitment method, we found that Total Motile Count (TMC) was significantly higher if men consumed fruits/nuts (β=+6.9, SE=1.9, p=0.0005) and vegetables (β=+5.4, SE=1.9, p=0.006), whereas consumption of fries was associated with lower TMC (β=-20.2, SE=8.7, p=0.024). Semen volume was also higher if vegetables or fruits/nuts were frequently consumed (β=+0.06, SE=0.03, p=0.03). Similarly, our sperm epigenetic analyses showed opposing associations for healthy versus fast food items. Frequent consumption of fries was related to a higher chance of sperm being methylated at the MEG3-IG CpG4 site (OR=1.073, 95%CI: 1.035-1.112), and high consumption of vegetables was associated with a lower risk of DNA methylation at the NNAT CpG3 site (OR=0.941, 95%CI: 0.914-0.968). These results remained significant after adjusting for multiple testing. We conclude that dietary habits are linked to sperm epigenetic outcomes. If carried into the next generation paternal unhealthy dietary patterns may result in adverse metabolic conditions and increased risk for chronic diseases in offspring.
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spelling pubmed-81035432021-05-08 Opposing Epigenetic Signatures in Human Sperm by Intake of Fast Food Versus Healthy Food Soubry, Adelheid Murphy, Susan K. Vansant, Greet He, Yang Price, Thomas M. Hoyo, Cathrine Front Endocrinol (Lausanne) Endocrinology Animal experiments have demonstrated that diets high in fats create a harmful environment for developing sperm cells, contributing to impaired reproductive health and induced risk for chronic diseases in the next generation. Changes at the level of the epigenome have been suggested to underlie these observations. Human data are limited to verify this hypothesis. While we earlier demonstrated a link between male obesity and DNA methylation changes at imprinted genes in mature sperm cells and newborns, it is currently unknown if -or how- a paternal eating pattern (related to obesity) is related to indices for epigenetic inheritance. We here aim to examine a yet unexplored link between consumption of healthy (rich in vitamins and fibers) or unhealthy (“fast”) foods and methylation at imprint regulatory regions in DNA of sperm. We obtained semen and data from 67 men, as part of a North Carolina-based study: The Influence of the Environment on Gametic Epigenetic Reprogramming (TIEGER) study. Dietary data included intake of fruits/nuts, vegetables/soups, whole grain bread, meat, seafood/fish, and fatty or processed food items. Multiple regression models were used to explore the association between dietary habits and clinical sperm parameters as well as DNA methylation levels, quantified using bisulfite pyrosequencing at 12 differentially methylated regions (DMRs) of the following imprinted genes: GRB10, IGF2, H19, MEG3, NDN, NNAT, PEG1/MEST, PEG3, PLAGL1, SNRPN, and SGCE/PEG10. After adjusting for age, obesity status and recruitment method, we found that Total Motile Count (TMC) was significantly higher if men consumed fruits/nuts (β=+6.9, SE=1.9, p=0.0005) and vegetables (β=+5.4, SE=1.9, p=0.006), whereas consumption of fries was associated with lower TMC (β=-20.2, SE=8.7, p=0.024). Semen volume was also higher if vegetables or fruits/nuts were frequently consumed (β=+0.06, SE=0.03, p=0.03). Similarly, our sperm epigenetic analyses showed opposing associations for healthy versus fast food items. Frequent consumption of fries was related to a higher chance of sperm being methylated at the MEG3-IG CpG4 site (OR=1.073, 95%CI: 1.035-1.112), and high consumption of vegetables was associated with a lower risk of DNA methylation at the NNAT CpG3 site (OR=0.941, 95%CI: 0.914-0.968). These results remained significant after adjusting for multiple testing. We conclude that dietary habits are linked to sperm epigenetic outcomes. If carried into the next generation paternal unhealthy dietary patterns may result in adverse metabolic conditions and increased risk for chronic diseases in offspring. Frontiers Media S.A. 2021-04-23 /pmc/articles/PMC8103543/ /pubmed/33967953 http://dx.doi.org/10.3389/fendo.2021.625204 Text en Copyright © 2021 Soubry, Murphy, Vansant, He, Price and Hoyo https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Endocrinology
Soubry, Adelheid
Murphy, Susan K.
Vansant, Greet
He, Yang
Price, Thomas M.
Hoyo, Cathrine
Opposing Epigenetic Signatures in Human Sperm by Intake of Fast Food Versus Healthy Food
title Opposing Epigenetic Signatures in Human Sperm by Intake of Fast Food Versus Healthy Food
title_full Opposing Epigenetic Signatures in Human Sperm by Intake of Fast Food Versus Healthy Food
title_fullStr Opposing Epigenetic Signatures in Human Sperm by Intake of Fast Food Versus Healthy Food
title_full_unstemmed Opposing Epigenetic Signatures in Human Sperm by Intake of Fast Food Versus Healthy Food
title_short Opposing Epigenetic Signatures in Human Sperm by Intake of Fast Food Versus Healthy Food
title_sort opposing epigenetic signatures in human sperm by intake of fast food versus healthy food
topic Endocrinology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8103543/
https://www.ncbi.nlm.nih.gov/pubmed/33967953
http://dx.doi.org/10.3389/fendo.2021.625204
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