Metabolism-driven post-translational modifications of H3K9 in early bovine embryos

in Reproduction
Authors:
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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https://orcid.org/0000-0002-3972-3754
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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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Correspondence should be addressed to M P Milazzotto; Email: marcella.milazzotto@ufabc.edu.br

*(J Ispada and A M da Fonseca Junior contributed equally to this work)

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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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