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Adaptative response to changes in pyruvate metabolism on the epigenetic landscapes and transcriptomics of bovine embryos

The epigenetic reprogramming that occurs during the earliest stages of embryonic development has been described as crucial for the initial events of cell specification and differentiation. Recently, the metabolic status of the embryo has gained attention as one of the main factors coordinating epige...

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Autores principales: da Fonseca Junior, Aldcejam Martins, Ispada, Jessica, dos Santos, Erika Cristina, de Lima, Camila Bruna, da Silva, João Vitor Alcantara, Paulson, Erika, Goszczynski, Daniel Estanislao, Goissis, Marcelo Demarchi, Ross, Pablo Juan, Milazzotto, Marcella Pecora
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10352246/
https://www.ncbi.nlm.nih.gov/pubmed/37460590
http://dx.doi.org/10.1038/s41598-023-38686-6
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author da Fonseca Junior, Aldcejam Martins
Ispada, Jessica
dos Santos, Erika Cristina
de Lima, Camila Bruna
da Silva, João Vitor Alcantara
Paulson, Erika
Goszczynski, Daniel Estanislao
Goissis, Marcelo Demarchi
Ross, Pablo Juan
Milazzotto, Marcella Pecora
author_facet da Fonseca Junior, Aldcejam Martins
Ispada, Jessica
dos Santos, Erika Cristina
de Lima, Camila Bruna
da Silva, João Vitor Alcantara
Paulson, Erika
Goszczynski, Daniel Estanislao
Goissis, Marcelo Demarchi
Ross, Pablo Juan
Milazzotto, Marcella Pecora
author_sort da Fonseca Junior, Aldcejam Martins
collection PubMed
description The epigenetic reprogramming that occurs during the earliest stages of embryonic development has been described as crucial for the initial events of cell specification and differentiation. Recently, the metabolic status of the embryo has gained attention as one of the main factors coordinating epigenetic events. In this work, we investigate the link between pyruvate metabolism and epigenetic regulation by culturing bovine embryos from day 5 in the presence of dichloroacetate (DCA), a pyruvate analog that increases the pyruvate to acetyl-CoA conversion, and iodoacetate (IA), which inhibits the glyceraldehyde-3-phosphate dehydrogenase (GAPDH), leading to glycolysis inhibition. After 8 h of incubation, both DCA and IA-derived embryos presented higher mitochondrial membrane potential. Nevertheless, in both cases, lower levels of acetyl-CoA, ATP-citrate lyase and mitochondrial membrane potential were found in blastocysts, suggesting an adaptative metabolic response, especially in the DCA group. The metabolic alteration found in blastocysts led to changes in the global pattern of H3K9 and H3K27 acetylation and H3K27 trimethylation. Transcriptome analysis revealed that such alterations resulted in molecular differences mainly associated to metabolic processes, establishment of epigenetic marks, control of gene expression and cell cycle. The latter was further confirmed by the alteration of total cell number and cell differentiation in both groups when compared to the control. These results corroborate previous evidence of the relationship between the energy metabolism and the epigenetic reprogramming in preimplantation bovine embryos, reinforcing that the culture system is decisive for precise epigenetic reprogramming, with consequences for the molecular control and differentiation of cells.
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spelling pubmed-103522462023-07-19 Adaptative response to changes in pyruvate metabolism on the epigenetic landscapes and transcriptomics of bovine embryos da Fonseca Junior, Aldcejam Martins Ispada, Jessica dos Santos, Erika Cristina de Lima, Camila Bruna da Silva, João Vitor Alcantara Paulson, Erika Goszczynski, Daniel Estanislao Goissis, Marcelo Demarchi Ross, Pablo Juan Milazzotto, Marcella Pecora Sci Rep Article The epigenetic reprogramming that occurs during the earliest stages of embryonic development has been described as crucial for the initial events of cell specification and differentiation. Recently, the metabolic status of the embryo has gained attention as one of the main factors coordinating epigenetic events. In this work, we investigate the link between pyruvate metabolism and epigenetic regulation by culturing bovine embryos from day 5 in the presence of dichloroacetate (DCA), a pyruvate analog that increases the pyruvate to acetyl-CoA conversion, and iodoacetate (IA), which inhibits the glyceraldehyde-3-phosphate dehydrogenase (GAPDH), leading to glycolysis inhibition. After 8 h of incubation, both DCA and IA-derived embryos presented higher mitochondrial membrane potential. Nevertheless, in both cases, lower levels of acetyl-CoA, ATP-citrate lyase and mitochondrial membrane potential were found in blastocysts, suggesting an adaptative metabolic response, especially in the DCA group. The metabolic alteration found in blastocysts led to changes in the global pattern of H3K9 and H3K27 acetylation and H3K27 trimethylation. Transcriptome analysis revealed that such alterations resulted in molecular differences mainly associated to metabolic processes, establishment of epigenetic marks, control of gene expression and cell cycle. The latter was further confirmed by the alteration of total cell number and cell differentiation in both groups when compared to the control. These results corroborate previous evidence of the relationship between the energy metabolism and the epigenetic reprogramming in preimplantation bovine embryos, reinforcing that the culture system is decisive for precise epigenetic reprogramming, with consequences for the molecular control and differentiation of cells. Nature Publishing Group UK 2023-07-17 /pmc/articles/PMC10352246/ /pubmed/37460590 http://dx.doi.org/10.1038/s41598-023-38686-6 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
da Fonseca Junior, Aldcejam Martins
Ispada, Jessica
dos Santos, Erika Cristina
de Lima, Camila Bruna
da Silva, João Vitor Alcantara
Paulson, Erika
Goszczynski, Daniel Estanislao
Goissis, Marcelo Demarchi
Ross, Pablo Juan
Milazzotto, Marcella Pecora
Adaptative response to changes in pyruvate metabolism on the epigenetic landscapes and transcriptomics of bovine embryos
title Adaptative response to changes in pyruvate metabolism on the epigenetic landscapes and transcriptomics of bovine embryos
title_full Adaptative response to changes in pyruvate metabolism on the epigenetic landscapes and transcriptomics of bovine embryos
title_fullStr Adaptative response to changes in pyruvate metabolism on the epigenetic landscapes and transcriptomics of bovine embryos
title_full_unstemmed Adaptative response to changes in pyruvate metabolism on the epigenetic landscapes and transcriptomics of bovine embryos
title_short Adaptative response to changes in pyruvate metabolism on the epigenetic landscapes and transcriptomics of bovine embryos
title_sort adaptative response to changes in pyruvate metabolism on the epigenetic landscapes and transcriptomics of bovine embryos
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10352246/
https://www.ncbi.nlm.nih.gov/pubmed/37460590
http://dx.doi.org/10.1038/s41598-023-38686-6
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