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Transient Changes of Metabolism at the Pronuclear Stage in Mice Influences Skeletal Muscle Phenotype in Adulthood

Skeletal muscle has a remarkable plasticity, and its phenotype is strongly influenced by hormones, transcription factors, and physical activity. However, whether skeletal phenotype can be oriented or not during early embryonic stages has never been investigated. Here, we report that pyruvate as the...

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Autores principales: Bertrand-Gaday, Christelle, Letheule, Martine, Blanchet, Emilie, Vernus, Barbara, Pessemesse, Laurence, Bonnet-Garnier, Amélie, Bonnieu, Anne, Casas, François
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7582979/
https://www.ncbi.nlm.nih.gov/pubmed/33003470
http://dx.doi.org/10.3390/ijms21197203
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author Bertrand-Gaday, Christelle
Letheule, Martine
Blanchet, Emilie
Vernus, Barbara
Pessemesse, Laurence
Bonnet-Garnier, Amélie
Bonnieu, Anne
Casas, François
author_facet Bertrand-Gaday, Christelle
Letheule, Martine
Blanchet, Emilie
Vernus, Barbara
Pessemesse, Laurence
Bonnet-Garnier, Amélie
Bonnieu, Anne
Casas, François
author_sort Bertrand-Gaday, Christelle
collection PubMed
description Skeletal muscle has a remarkable plasticity, and its phenotype is strongly influenced by hormones, transcription factors, and physical activity. However, whether skeletal phenotype can be oriented or not during early embryonic stages has never been investigated. Here, we report that pyruvate as the only source of carbohydrate in the culture medium of mouse one cell stage embryo influenced the establishment of the muscular phenotype in adulthood. We found that pyruvate alone induced changes in the contractile phenotype of the skeletal muscle in a sexually dependent manner. For male mice, a switch to a more glycolytic phenotype was recorded, whereas, in females, the pyruvate induced a switch to a more oxidative phenotype. In addition, the influence of pyruvate on the contractile phenotypes was confirmed in two mouse models of muscle hypertrophy: the well-known myostatin deficient mouse (Mstn−/−) and a mouse carrying a specific deletion of p43, a mitochondrial triiodothyronine receptor. Finally, to understand the link between these adult phenotypes and the early embryonic period, we assessed the levels of two histone H3 post-translational modifications in presence of pyruvate alone just after the wave of chromatin reprogramming specific of the first cell cycle. We showed that H3K4 acetylation level was decreased in Mstn−/− 2-cell embryos, whereas no difference was found for H3K27 trimethylation level, whatever the genotype. These findings demonstrate for the first time that changes in the access of energy substrate during the very first embryonic stage can induce a precocious orientation of skeletal muscle phenotype in adulthood.
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spelling pubmed-75829792020-10-28 Transient Changes of Metabolism at the Pronuclear Stage in Mice Influences Skeletal Muscle Phenotype in Adulthood Bertrand-Gaday, Christelle Letheule, Martine Blanchet, Emilie Vernus, Barbara Pessemesse, Laurence Bonnet-Garnier, Amélie Bonnieu, Anne Casas, François Int J Mol Sci Article Skeletal muscle has a remarkable plasticity, and its phenotype is strongly influenced by hormones, transcription factors, and physical activity. However, whether skeletal phenotype can be oriented or not during early embryonic stages has never been investigated. Here, we report that pyruvate as the only source of carbohydrate in the culture medium of mouse one cell stage embryo influenced the establishment of the muscular phenotype in adulthood. We found that pyruvate alone induced changes in the contractile phenotype of the skeletal muscle in a sexually dependent manner. For male mice, a switch to a more glycolytic phenotype was recorded, whereas, in females, the pyruvate induced a switch to a more oxidative phenotype. In addition, the influence of pyruvate on the contractile phenotypes was confirmed in two mouse models of muscle hypertrophy: the well-known myostatin deficient mouse (Mstn−/−) and a mouse carrying a specific deletion of p43, a mitochondrial triiodothyronine receptor. Finally, to understand the link between these adult phenotypes and the early embryonic period, we assessed the levels of two histone H3 post-translational modifications in presence of pyruvate alone just after the wave of chromatin reprogramming specific of the first cell cycle. We showed that H3K4 acetylation level was decreased in Mstn−/− 2-cell embryos, whereas no difference was found for H3K27 trimethylation level, whatever the genotype. These findings demonstrate for the first time that changes in the access of energy substrate during the very first embryonic stage can induce a precocious orientation of skeletal muscle phenotype in adulthood. MDPI 2020-09-29 /pmc/articles/PMC7582979/ /pubmed/33003470 http://dx.doi.org/10.3390/ijms21197203 Text en © 2020 by the authors. 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 (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Bertrand-Gaday, Christelle
Letheule, Martine
Blanchet, Emilie
Vernus, Barbara
Pessemesse, Laurence
Bonnet-Garnier, Amélie
Bonnieu, Anne
Casas, François
Transient Changes of Metabolism at the Pronuclear Stage in Mice Influences Skeletal Muscle Phenotype in Adulthood
title Transient Changes of Metabolism at the Pronuclear Stage in Mice Influences Skeletal Muscle Phenotype in Adulthood
title_full Transient Changes of Metabolism at the Pronuclear Stage in Mice Influences Skeletal Muscle Phenotype in Adulthood
title_fullStr Transient Changes of Metabolism at the Pronuclear Stage in Mice Influences Skeletal Muscle Phenotype in Adulthood
title_full_unstemmed Transient Changes of Metabolism at the Pronuclear Stage in Mice Influences Skeletal Muscle Phenotype in Adulthood
title_short Transient Changes of Metabolism at the Pronuclear Stage in Mice Influences Skeletal Muscle Phenotype in Adulthood
title_sort transient changes of metabolism at the pronuclear stage in mice influences skeletal muscle phenotype in adulthood
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7582979/
https://www.ncbi.nlm.nih.gov/pubmed/33003470
http://dx.doi.org/10.3390/ijms21197203
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