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Genome-wide DNA methylation patterns of bovine blastocysts derived from in vivo embryos subjected to in vitro culture before, during or after embryonic genome activation

BACKGROUND: Aberrant DNA methylation patterns of genes required for development are common in in vitro produced embryos. In this regard, we previously identified altered DNA methylation patterns of in vivo developed blastocysts from embryos which spent different stages of development in vitro, indic...

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Autores principales: Salilew-Wondim, Dessie, Saeed-Zidane, Mohammed, Hoelker, Michael, Gebremedhn, Samuel, Poirier, Mikhaël, Pandey, Hari Om, Tholen, Ernst, Neuhoff, Christiane, Held, Eva, Besenfelder, Urban, Havlicek, Vita, Rings, Franca, Fournier, Eric, Gagné, Dominic, Sirard, Marc-André, Robert, Claude, Gad, Ahmed, Schellander, Karl, Tesfaye, Dawit
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5984773/
https://www.ncbi.nlm.nih.gov/pubmed/29859035
http://dx.doi.org/10.1186/s12864-018-4826-3
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author Salilew-Wondim, Dessie
Saeed-Zidane, Mohammed
Hoelker, Michael
Gebremedhn, Samuel
Poirier, Mikhaël
Pandey, Hari Om
Tholen, Ernst
Neuhoff, Christiane
Held, Eva
Besenfelder, Urban
Havlicek, Vita
Rings, Franca
Fournier, Eric
Gagné, Dominic
Sirard, Marc-André
Robert, Claude
Gad, Ahmed
Schellander, Karl
Tesfaye, Dawit
author_facet Salilew-Wondim, Dessie
Saeed-Zidane, Mohammed
Hoelker, Michael
Gebremedhn, Samuel
Poirier, Mikhaël
Pandey, Hari Om
Tholen, Ernst
Neuhoff, Christiane
Held, Eva
Besenfelder, Urban
Havlicek, Vita
Rings, Franca
Fournier, Eric
Gagné, Dominic
Sirard, Marc-André
Robert, Claude
Gad, Ahmed
Schellander, Karl
Tesfaye, Dawit
author_sort Salilew-Wondim, Dessie
collection PubMed
description BACKGROUND: Aberrant DNA methylation patterns of genes required for development are common in in vitro produced embryos. In this regard, we previously identified altered DNA methylation patterns of in vivo developed blastocysts from embryos which spent different stages of development in vitro, indicating carryover effects of suboptimal culture conditions on epigenetic signatures of preimplantation embryos. However, epigenetic responses of in vivo originated embryos to suboptimal culture conditions are not fully understood. Therefore, here we investigated DNA methylation patterns of in vivo derived bovine embryos subjected to in vitro culture condition before, during or after major embryonic genome activation (EGA). For this, in vivo produced 2-, 8- and 16-cell stage embryos were cultured in vitro until the blastocyst stage and blastocysts were used for genome-wide DNA methylation analysis. RESULTS: The 2- and 8-cell flushed embryo groups showed lower blastocyst rates compared to the 16-cell flush group. This was further accompanied by increased numbers of differentially methylated genomic regions (DMRs) in blastocysts of the 2- and 8-cell flush groups compared to the complete in vivo control ones. Moreover, 1623 genomic loci including imprinted genes were hypermethylated in blastocyst of 2-, 8- and 16-cell flushed groups, indicating the presence of genomic regions which are sensitive to the in vitro culture at any stage of embryonic development. Furthermore, hypermethylated genomic loci outnumbered hypomethylated ones in blastocysts of 2- and 16-cell flushed embryo groups, but the opposite occurred in the 8-cell group. Moreover, DMRs which were unique to blastocysts of the 2-cell flushed group and inversely correlated with corresponding mRNA expression levels were involved in plasma membrane lactate transport, amino acid transport and phosphorus metabolic processes, whereas DMRs which were specific to the 8-cell group and inversely correlated with corresponding mRNA expression levels were involved in several biological processes including regulation of fatty acids and steroid biosynthesis processes. CONCLUSION: In vivo embryos subjected to in vitro culture before and during major embryonic genome activation (EGA) are prone to changes in DNA methylation marks and exposure of in vivo embryos to in vitro culture during the time of EGA increased hypomethylated genomic loci in blastocysts. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-4826-3) contains supplementary material, which is available to authorized users.
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spelling pubmed-59847732018-06-07 Genome-wide DNA methylation patterns of bovine blastocysts derived from in vivo embryos subjected to in vitro culture before, during or after embryonic genome activation Salilew-Wondim, Dessie Saeed-Zidane, Mohammed Hoelker, Michael Gebremedhn, Samuel Poirier, Mikhaël Pandey, Hari Om Tholen, Ernst Neuhoff, Christiane Held, Eva Besenfelder, Urban Havlicek, Vita Rings, Franca Fournier, Eric Gagné, Dominic Sirard, Marc-André Robert, Claude Gad, Ahmed Schellander, Karl Tesfaye, Dawit BMC Genomics Research Article BACKGROUND: Aberrant DNA methylation patterns of genes required for development are common in in vitro produced embryos. In this regard, we previously identified altered DNA methylation patterns of in vivo developed blastocysts from embryos which spent different stages of development in vitro, indicating carryover effects of suboptimal culture conditions on epigenetic signatures of preimplantation embryos. However, epigenetic responses of in vivo originated embryos to suboptimal culture conditions are not fully understood. Therefore, here we investigated DNA methylation patterns of in vivo derived bovine embryos subjected to in vitro culture condition before, during or after major embryonic genome activation (EGA). For this, in vivo produced 2-, 8- and 16-cell stage embryos were cultured in vitro until the blastocyst stage and blastocysts were used for genome-wide DNA methylation analysis. RESULTS: The 2- and 8-cell flushed embryo groups showed lower blastocyst rates compared to the 16-cell flush group. This was further accompanied by increased numbers of differentially methylated genomic regions (DMRs) in blastocysts of the 2- and 8-cell flush groups compared to the complete in vivo control ones. Moreover, 1623 genomic loci including imprinted genes were hypermethylated in blastocyst of 2-, 8- and 16-cell flushed groups, indicating the presence of genomic regions which are sensitive to the in vitro culture at any stage of embryonic development. Furthermore, hypermethylated genomic loci outnumbered hypomethylated ones in blastocysts of 2- and 16-cell flushed embryo groups, but the opposite occurred in the 8-cell group. Moreover, DMRs which were unique to blastocysts of the 2-cell flushed group and inversely correlated with corresponding mRNA expression levels were involved in plasma membrane lactate transport, amino acid transport and phosphorus metabolic processes, whereas DMRs which were specific to the 8-cell group and inversely correlated with corresponding mRNA expression levels were involved in several biological processes including regulation of fatty acids and steroid biosynthesis processes. CONCLUSION: In vivo embryos subjected to in vitro culture before and during major embryonic genome activation (EGA) are prone to changes in DNA methylation marks and exposure of in vivo embryos to in vitro culture during the time of EGA increased hypomethylated genomic loci in blastocysts. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-4826-3) contains supplementary material, which is available to authorized users. BioMed Central 2018-06-01 /pmc/articles/PMC5984773/ /pubmed/29859035 http://dx.doi.org/10.1186/s12864-018-4826-3 Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Salilew-Wondim, Dessie
Saeed-Zidane, Mohammed
Hoelker, Michael
Gebremedhn, Samuel
Poirier, Mikhaël
Pandey, Hari Om
Tholen, Ernst
Neuhoff, Christiane
Held, Eva
Besenfelder, Urban
Havlicek, Vita
Rings, Franca
Fournier, Eric
Gagné, Dominic
Sirard, Marc-André
Robert, Claude
Gad, Ahmed
Schellander, Karl
Tesfaye, Dawit
Genome-wide DNA methylation patterns of bovine blastocysts derived from in vivo embryos subjected to in vitro culture before, during or after embryonic genome activation
title Genome-wide DNA methylation patterns of bovine blastocysts derived from in vivo embryos subjected to in vitro culture before, during or after embryonic genome activation
title_full Genome-wide DNA methylation patterns of bovine blastocysts derived from in vivo embryos subjected to in vitro culture before, during or after embryonic genome activation
title_fullStr Genome-wide DNA methylation patterns of bovine blastocysts derived from in vivo embryos subjected to in vitro culture before, during or after embryonic genome activation
title_full_unstemmed Genome-wide DNA methylation patterns of bovine blastocysts derived from in vivo embryos subjected to in vitro culture before, during or after embryonic genome activation
title_short Genome-wide DNA methylation patterns of bovine blastocysts derived from in vivo embryos subjected to in vitro culture before, during or after embryonic genome activation
title_sort genome-wide dna methylation patterns of bovine blastocysts derived from in vivo embryos subjected to in vitro culture before, during or after embryonic genome activation
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5984773/
https://www.ncbi.nlm.nih.gov/pubmed/29859035
http://dx.doi.org/10.1186/s12864-018-4826-3
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