Cargando…
Paternal Exercise Improves the Metabolic Health of Offspring via Epigenetic Modulation of the Germline
Background/Aims: Epigenetic regulation is considered the main molecular mechanism underlying the developmental origin of health and disease’s (DOHAD) hypothesis. Previous studies that have investigated the role of paternal exercise on the metabolic health of the offspring did not control for the amo...
Autores principales: | , , , , , , , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
MDPI
2021
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8744992/ https://www.ncbi.nlm.nih.gov/pubmed/35008427 http://dx.doi.org/10.3390/ijms23010001 |
_version_ | 1784630238327603200 |
---|---|
author | Costa-Júnior, José Maria Ferreira, Sandra Mara Kurauti, Mirian Ayumi Bernstein, Diana L. Ruano, Elena G. Kameswaran, Vasumathi Schug, Jonathan Freitas-Dias, Ricardo Zoppi, Claudio C. Boschero, Antonio C. de Oliveira, Camila A. M. Santos, Gustavo J. Carneiro, Everardo M. Kaestner, Klaus H. |
author_facet | Costa-Júnior, José Maria Ferreira, Sandra Mara Kurauti, Mirian Ayumi Bernstein, Diana L. Ruano, Elena G. Kameswaran, Vasumathi Schug, Jonathan Freitas-Dias, Ricardo Zoppi, Claudio C. Boschero, Antonio C. de Oliveira, Camila A. M. Santos, Gustavo J. Carneiro, Everardo M. Kaestner, Klaus H. |
author_sort | Costa-Júnior, José Maria |
collection | PubMed |
description | Background/Aims: Epigenetic regulation is considered the main molecular mechanism underlying the developmental origin of health and disease’s (DOHAD) hypothesis. Previous studies that have investigated the role of paternal exercise on the metabolic health of the offspring did not control for the amount and intensity of the training or possible effects of adaptation to exercise and produced conflicting results regarding the benefits of parental exercise to the next generation. We employed a precisely regulated exercise regimen to study the transgenerational inheritance of improved metabolic health. Methods: We subjected male mice to a well-controlled exercise -training program to investigate the effects of paternal exercise on glucose tolerance and insulin sensitivity in their adult progeny. To investigate the molecular mechanisms of epigenetic inheritance, we determined chromatin markers in the skeletal muscle of the offspring and the paternal sperm. Results: Offspring of trained male mice exhibited improved glucose homeostasis and insulin sensitivity. Paternal exercise modulated the DNA methylation profile of PI3Kca and the imprinted H19/Igf2 locus at specific differentially methylated regions (DMRs) in the skeletal muscle of the offspring, which affected their gene expression. Remarkably, a similar DNA methylation profile at the PI3Kca, H19, and Igf2 genes was present in the progenitor sperm indicating that exercise-induced epigenetic changes that occurred during germ cell development contributed to transgenerational transmission. Conclusion: Paternal exercise might be considered as a strategy that could promote metabolic health in the offspring as the benefits can be inherited transgenerationally. |
format | Online Article Text |
id | pubmed-8744992 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | MDPI |
record_format | MEDLINE/PubMed |
spelling | pubmed-87449922022-01-11 Paternal Exercise Improves the Metabolic Health of Offspring via Epigenetic Modulation of the Germline Costa-Júnior, José Maria Ferreira, Sandra Mara Kurauti, Mirian Ayumi Bernstein, Diana L. Ruano, Elena G. Kameswaran, Vasumathi Schug, Jonathan Freitas-Dias, Ricardo Zoppi, Claudio C. Boschero, Antonio C. de Oliveira, Camila A. M. Santos, Gustavo J. Carneiro, Everardo M. Kaestner, Klaus H. Int J Mol Sci Article Background/Aims: Epigenetic regulation is considered the main molecular mechanism underlying the developmental origin of health and disease’s (DOHAD) hypothesis. Previous studies that have investigated the role of paternal exercise on the metabolic health of the offspring did not control for the amount and intensity of the training or possible effects of adaptation to exercise and produced conflicting results regarding the benefits of parental exercise to the next generation. We employed a precisely regulated exercise regimen to study the transgenerational inheritance of improved metabolic health. Methods: We subjected male mice to a well-controlled exercise -training program to investigate the effects of paternal exercise on glucose tolerance and insulin sensitivity in their adult progeny. To investigate the molecular mechanisms of epigenetic inheritance, we determined chromatin markers in the skeletal muscle of the offspring and the paternal sperm. Results: Offspring of trained male mice exhibited improved glucose homeostasis and insulin sensitivity. Paternal exercise modulated the DNA methylation profile of PI3Kca and the imprinted H19/Igf2 locus at specific differentially methylated regions (DMRs) in the skeletal muscle of the offspring, which affected their gene expression. Remarkably, a similar DNA methylation profile at the PI3Kca, H19, and Igf2 genes was present in the progenitor sperm indicating that exercise-induced epigenetic changes that occurred during germ cell development contributed to transgenerational transmission. Conclusion: Paternal exercise might be considered as a strategy that could promote metabolic health in the offspring as the benefits can be inherited transgenerationally. MDPI 2021-12-21 /pmc/articles/PMC8744992/ /pubmed/35008427 http://dx.doi.org/10.3390/ijms23010001 Text en © 2021 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). |
spellingShingle | Article Costa-Júnior, José Maria Ferreira, Sandra Mara Kurauti, Mirian Ayumi Bernstein, Diana L. Ruano, Elena G. Kameswaran, Vasumathi Schug, Jonathan Freitas-Dias, Ricardo Zoppi, Claudio C. Boschero, Antonio C. de Oliveira, Camila A. M. Santos, Gustavo J. Carneiro, Everardo M. Kaestner, Klaus H. Paternal Exercise Improves the Metabolic Health of Offspring via Epigenetic Modulation of the Germline |
title | Paternal Exercise Improves the Metabolic Health of Offspring via Epigenetic Modulation of the Germline |
title_full | Paternal Exercise Improves the Metabolic Health of Offspring via Epigenetic Modulation of the Germline |
title_fullStr | Paternal Exercise Improves the Metabolic Health of Offspring via Epigenetic Modulation of the Germline |
title_full_unstemmed | Paternal Exercise Improves the Metabolic Health of Offspring via Epigenetic Modulation of the Germline |
title_short | Paternal Exercise Improves the Metabolic Health of Offspring via Epigenetic Modulation of the Germline |
title_sort | paternal exercise improves the metabolic health of offspring via epigenetic modulation of the germline |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8744992/ https://www.ncbi.nlm.nih.gov/pubmed/35008427 http://dx.doi.org/10.3390/ijms23010001 |
work_keys_str_mv | AT costajuniorjosemaria paternalexerciseimprovesthemetabolichealthofoffspringviaepigeneticmodulationofthegermline AT ferreirasandramara paternalexerciseimprovesthemetabolichealthofoffspringviaepigeneticmodulationofthegermline AT kurautimirianayumi paternalexerciseimprovesthemetabolichealthofoffspringviaepigeneticmodulationofthegermline AT bernsteindianal paternalexerciseimprovesthemetabolichealthofoffspringviaepigeneticmodulationofthegermline AT ruanoelenag paternalexerciseimprovesthemetabolichealthofoffspringviaepigeneticmodulationofthegermline AT kameswaranvasumathi paternalexerciseimprovesthemetabolichealthofoffspringviaepigeneticmodulationofthegermline AT schugjonathan paternalexerciseimprovesthemetabolichealthofoffspringviaepigeneticmodulationofthegermline AT freitasdiasricardo paternalexerciseimprovesthemetabolichealthofoffspringviaepigeneticmodulationofthegermline AT zoppiclaudioc paternalexerciseimprovesthemetabolichealthofoffspringviaepigeneticmodulationofthegermline AT boscheroantonioc paternalexerciseimprovesthemetabolichealthofoffspringviaepigeneticmodulationofthegermline AT deoliveiracamilaam paternalexerciseimprovesthemetabolichealthofoffspringviaepigeneticmodulationofthegermline AT santosgustavoj paternalexerciseimprovesthemetabolichealthofoffspringviaepigeneticmodulationofthegermline AT carneiroeverardom paternalexerciseimprovesthemetabolichealthofoffspringviaepigeneticmodulationofthegermline AT kaestnerklaush paternalexerciseimprovesthemetabolichealthofoffspringviaepigeneticmodulationofthegermline |