Effect of maternal methionine supplementation on the transcriptome of bovine preimplantation embryos.

Maternal nutrition exclusively during the periconceptional period can induce remarkable effects on both oocyte maturation and early embryo development, which in turn can have lifelong consequences. The objective of this study was to evaluate the effect of maternal methionine supplementation on the t...

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Main Authors: Francisco Peñagaricano, Alex H Souza, Paulo D Carvalho, Ashley M Driver, Rocio Gambra, Jenna Kropp, Katherine S Hackbart, Daniel Luchini, Randy D Shaver, Milo C Wiltbank, Hasan Khatib
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2013-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC3749122?pdf=render
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spelling doaj-976c8a25b92045e791aa2f22510a787e2020-11-24T21:51:07ZengPublic Library of Science (PLoS)PLoS ONE1932-62032013-01-0188e7230210.1371/journal.pone.0072302Effect of maternal methionine supplementation on the transcriptome of bovine preimplantation embryos.Francisco PeñagaricanoAlex H SouzaPaulo D CarvalhoAshley M DriverRocio GambraJenna KroppKatherine S HackbartDaniel LuchiniRandy D ShaverMilo C WiltbankHasan KhatibMaternal nutrition exclusively during the periconceptional period can induce remarkable effects on both oocyte maturation and early embryo development, which in turn can have lifelong consequences. The objective of this study was to evaluate the effect of maternal methionine supplementation on the transcriptome of bovine preimplantation embryos. Holstein cows were randomly assigned to one of two treatments differing in level of dietary methionine (1.89 Met vs. 2.43 Met % of metabolizable protein) from calving until embryo flushing. High quality preimplantation embryos from individual cows were pooled and then analyzed by RNA sequencing. Remarkably, a subtle difference in methionine supplementation in maternal diet was sufficient to cause significant changes in the transcriptome of the embryos. A total of 276 genes out of 10,662 showed differential expression between treatments (FDR <0.10). Interestingly, several of the most significant genes are related to embryonic development (e.g., VIM, IFI6, BCL2A1, and TBX15) and immune response (e.g., NKG7, TYROBP, SLAMF7, LCP1, and BLA-DQB). Likewise, gene set enrichment analysis revealed that several Gene Ontology terms, InterPro entries, and KEGG pathways were enriched (FDR <0.05) with differentially expressed genes involved in embryo development and immune system. The expression of most genes was decreased by maternal methionine supplementation, consistent with reduced transcription of genes with increased methylation of specific genes by increased methionine. Overall, our findings provide evidence that supplementing methionine to dams prior to conception and during the preimplantation period can modulate gene expression in bovine blastocysts. The ramifications of the observed gene expression changes for subsequent development of the pregnancy and physiology of the offspring warrant further investigation in future studies.http://europepmc.org/articles/PMC3749122?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Francisco Peñagaricano
Alex H Souza
Paulo D Carvalho
Ashley M Driver
Rocio Gambra
Jenna Kropp
Katherine S Hackbart
Daniel Luchini
Randy D Shaver
Milo C Wiltbank
Hasan Khatib
spellingShingle Francisco Peñagaricano
Alex H Souza
Paulo D Carvalho
Ashley M Driver
Rocio Gambra
Jenna Kropp
Katherine S Hackbart
Daniel Luchini
Randy D Shaver
Milo C Wiltbank
Hasan Khatib
Effect of maternal methionine supplementation on the transcriptome of bovine preimplantation embryos.
PLoS ONE
author_facet Francisco Peñagaricano
Alex H Souza
Paulo D Carvalho
Ashley M Driver
Rocio Gambra
Jenna Kropp
Katherine S Hackbart
Daniel Luchini
Randy D Shaver
Milo C Wiltbank
Hasan Khatib
author_sort Francisco Peñagaricano
title Effect of maternal methionine supplementation on the transcriptome of bovine preimplantation embryos.
title_short Effect of maternal methionine supplementation on the transcriptome of bovine preimplantation embryos.
title_full Effect of maternal methionine supplementation on the transcriptome of bovine preimplantation embryos.
title_fullStr Effect of maternal methionine supplementation on the transcriptome of bovine preimplantation embryos.
title_full_unstemmed Effect of maternal methionine supplementation on the transcriptome of bovine preimplantation embryos.
title_sort effect of maternal methionine supplementation on the transcriptome of bovine preimplantation embryos.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2013-01-01
description Maternal nutrition exclusively during the periconceptional period can induce remarkable effects on both oocyte maturation and early embryo development, which in turn can have lifelong consequences. The objective of this study was to evaluate the effect of maternal methionine supplementation on the transcriptome of bovine preimplantation embryos. Holstein cows were randomly assigned to one of two treatments differing in level of dietary methionine (1.89 Met vs. 2.43 Met % of metabolizable protein) from calving until embryo flushing. High quality preimplantation embryos from individual cows were pooled and then analyzed by RNA sequencing. Remarkably, a subtle difference in methionine supplementation in maternal diet was sufficient to cause significant changes in the transcriptome of the embryos. A total of 276 genes out of 10,662 showed differential expression between treatments (FDR <0.10). Interestingly, several of the most significant genes are related to embryonic development (e.g., VIM, IFI6, BCL2A1, and TBX15) and immune response (e.g., NKG7, TYROBP, SLAMF7, LCP1, and BLA-DQB). Likewise, gene set enrichment analysis revealed that several Gene Ontology terms, InterPro entries, and KEGG pathways were enriched (FDR <0.05) with differentially expressed genes involved in embryo development and immune system. The expression of most genes was decreased by maternal methionine supplementation, consistent with reduced transcription of genes with increased methylation of specific genes by increased methionine. Overall, our findings provide evidence that supplementing methionine to dams prior to conception and during the preimplantation period can modulate gene expression in bovine blastocysts. The ramifications of the observed gene expression changes for subsequent development of the pregnancy and physiology of the offspring warrant further investigation in future studies.
url http://europepmc.org/articles/PMC3749122?pdf=render
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