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  • Author: Marcella Pecora Milazzotto x
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João Vitor Alcantara da Silva Laboratory of Embryonic Metabolism and Epigenetics, Center of Natural and Human Sciences, Federal University of ABC, Santo Andre, SP, Brazil

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Jessica Ispada Laboratory of Embryonic Metabolism and Epigenetics, Center of Natural and Human Sciences, Federal University of ABC, Santo Andre, SP, Brazil

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Ricardo Perecin Nociti Department of Veterinary Medicine, Faculty of Animal Sciences and Food Engineering, University of São Paulo, Pirassununga, SP, Brazil

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Aldcejam Martins da Fonseca Junior Laboratory of Embryonic Metabolism and Epigenetics, Center of Natural and Human Sciences, Federal University of ABC, Santo Andre, SP, Brazil

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Camila Bruna de Lima Département des Sciences Animales, Laval University, Canada

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Erika Cristina dos Santos Laboratory of Embryonic Metabolism and Epigenetics, Center of Natural and Human Sciences, Federal University of ABC, Santo Andre, SP, Brazil

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Marcos Roberto Chiaratti Department of Genetics and Evolution, Federal University of Sao Carlos, Sao Carlos, SP, Brazil

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Marcella Pecora Milazzotto Laboratory of Embryonic Metabolism and Epigenetics, Center of Natural and Human Sciences, Federal University of ABC, Santo Andre, SP, Brazil

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In brief

Pyruvate metabolism is one of the main metabolic pathways during oocyte maturation. This study demonstrates that pyruvate metabolism also regulates the epigenetic and molecular maturation in bovine oocytes.

Abstract

Pyruvate, the final product of glycolysis, undergoes conversion into acetyl-CoA within the mitochondria of oocytes, serving as a primary fuel source for the tricarboxylic acid (TCA) cycle. The citrate generated in the TCA cycle can be transported to the cytoplasm and converted back into acetyl-CoA. This acetyl-CoA can either fuel lipid synthesis or act as a substrate for histone acetylation. This study aimed to investigate how pyruvate metabolism influences lysine 9 histone 3 acetylation (H3K9ac) dynamics and RNA transcription in bovine oocytes during in vitro maturation (IVM). Bovine cumulus–oocyte complexes were cultured in vitro for 24 h, considering three experimental groups: Control (IVM medium only), DCA (IVM supplemented with sodium dichloroacetate, a stimulant of pyruvate oxidation into acetyl-CoA), or IA (IVM supplemented with sodium iodoacetate, a glycolysis inhibitor). The results revealed significant alterations in oocyte metabolism in both treatments, promoting the utilization of lipids as an energy source. These changes during IVM affected the dynamics of H3K9ac, subsequently influencing the oocyte's transcriptional activity. In the DCA and IA groups, a total of 148 and 356 differentially expressed genes were identified, respectively, compared to the control group. These findings suggest that modifications in pyruvate metabolism trigger the activation of metabolic pathways, particularly lipid metabolism, changing acetyl-CoA availability and H3K9ac levels, ultimately impacting the mRNA content of in vitro matured bovine oocytes.

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Jessica Ispada Laboratory of Embryonic Metabolism and Epigenetics, Center of Natural Sciences and Humanities, Universidade Federal do ABC, Santo André, São Paulo, Brazil
Institute of Biomedical Sciences, Universidade de São Paulo, São Paulo, Brazil

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Aldcejam Martins da Fonseca Junior Laboratory of Embryonic Metabolism and Epigenetics, Center of Natural Sciences and Humanities, Universidade Federal do ABC, Santo André, São Paulo, Brazil

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Otávio Luiz Ramos Santos Laboratory of Embryonic Metabolism and Epigenetics, Center of Natural Sciences and Humanities, Universidade Federal do ABC, Santo André, São Paulo, Brazil

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Camila Bruna de Lima Laboratory of Embryonic Metabolism and Epigenetics, Center of Natural Sciences and Humanities, Universidade Federal do ABC, Santo André, São Paulo, Brazil
Institute of Biomedical Sciences, Universidade de São Paulo, São Paulo, Brazil
Centre de Recherche en Reproduction, Développement et Santé Intergénérationnelle (CRDSI), Département des Sciences Animales, Faculté des Sciences de l’Agriculture et de l’Alimentation, Université Laval, Quebec, Canada

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Erika Cristina dos Santos Laboratory of Embryonic Metabolism and Epigenetics, Center of Natural Sciences and Humanities, Universidade Federal do ABC, Santo André, São Paulo, Brazil

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Vinicius Lourenço da Silva Bioinformatics and Health Informatics Group, Center for Engineering, Modeling and Applied Social Sciences, Universidade Federal do ABC, São Bernardo do Campo, São Paulo, Brazil

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Fernanda Nascimento Almeida Center for Mathematics Computation and Cognition, Universidade Federal do ABC, Santo André, São Paulo, Brazil

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Saul de Castro Leite Bioinformatics and Health Informatics Group, Center for Engineering, Modeling and Applied Social Sciences, Universidade Federal do ABC, São Bernardo do Campo, São Paulo, Brazil

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Pablo Juan Ross Department of Animal Science, University of California Davis, Davis, California, USA

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Marcella Pecora Milazzotto Laboratory of Embryonic Metabolism and Epigenetics, Center of Natural Sciences and Humanities, Universidade Federal do ABC, Santo André, São Paulo, Brazil
Institute of Biomedical Sciences, Universidade de São Paulo, São Paulo, Brazil

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Metabolic and molecular profiles were reported as different for bovine embryos with distinct kinetics during the first cleavages. In this study, we used this same developmental model (fast vs slow) to determine if the relationship between metabolism and developmental kinetics affects the levels of acetylation or tri-methylation at histone H3 lysine 9 (H3K9ac and H3K9me3, respectively). Fast and slow developing embryos presented different levels of H3K9ac and H3K9me3 from the earliest stages of development (40 and 96 hpi) and up to the blastocyst stage. For H3K9me3, both groups of embryos presented a wave of demethylation and de novo methylation, although it was more pronounced in fast than slow embryos, resulting in blastocysts with higher levels of this mark. The H3K9ac reprogramming profile was distinct between kinetics groups. While slow embryos presented a wave of deacetylation, followed by an increase in this mark at the blastocyst stage, fast embryos reduced this mark throughout all the developmental stages studied. H3K9me3 differences corresponded to writer and eraser transcript levels, while H3K9ac patterns were explained by metabolism-related gene expression. To verify if metabolic differences could alter levels of H3K9ac, embryos were cultured with sodium-iodoacetate (IA) or dichloroacetate (DCA) to disrupt the glycolytic pathway or increase acetyl-CoA production, respectively. IA reduced H3K9ac while DCA increased H3K9ac in blastocysts. Concluding, H3K9me3 and H3K9ac patterns differ between embryos with different kinetics, the second one explained by metabolic pathways involved in acetyl-CoA production. So far, this is the first study demonstrating a relationship between metabolic differences and histone post-translational modifications in bovine embryos.

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