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Genome-Wide DNA Methylation Patterns of Bovine Blastocysts Developed In Vivo from Embryos Completed Different Stages of Development In Vitro.
PLoS One. 2015; 10(11):e0140467.Plos

Abstract

Early embryonic loss and altered gene expression in in vitro produced blastocysts are believed to be partly caused by aberrant DNA methylation. However, specific embryonic stage which is sensitive to in vitro culture conditions to alter the DNA methylation profile of the resulting blastocysts remained unclear. Therefore, the aim of this study was to investigate the stage specific effect of in vitro culture environment on the DNA methylation response of the resulting blastocysts. For this, embryos cultured in vitro until zygote (ZY), 4-cell (4C) or 16-cell (16C) were transferred to recipients and the blastocysts were recovery at day 7 of the estrous cycle. Another embryo group was cultured in vitro until blastocyst stage (IVP). Genome-wide DNA methylation profiles of ZY, 4C, 16C and IVP blastocyst groups were then determined with reference to blastocysts developed completely under in vivo condition (VO) using EmbryoGENE DNA Methylation Array. To assess the contribution of methylation changes on gene expression patterns, the DNA methylation data was superimposed to the transcriptome profile data. The degree of DNA methylation dysregulation in the promoter and/or gene body regions of the resulting blastocysts was correlated with successive stages of development the embryos advanced under in vitro culture before transfer to the in vivo condition. Genomic enrichment analysis revealed that in 4C and 16C blastocyst groups, hypermethylated loci were outpacing the hypomethylated ones in intronic, exonic, promoter and proximal promoter regions, whereas the reverse was observed in ZY blastocyst group. However, in the IVP group, as much hypermethylated as hypomethylated probes were detected in gene body and promoter regions. In addition, gene ontology analysis indicated that differentially methylated regions were found to affected several biological functions including ATP binding in the ZY group, programmed cell death in the 4C, glycolysis in 16C and genetic imprinting and chromosome segregation in IVP blastocyst groups. Furthermore, 1.6, 3.4, 3.9 and 9.4% of the differentially methylated regions that were overlapped to the transcriptome profile data were negatively correlated with the gene expression patterns in ZY, 4C, 16C and IVP blastocyst groups, respectively. Therefore, this finding indicated that suboptimal culture condition during preimplantation embryo development induced changes in the DNA methylation landscape of the resulting blastocysts in a stage dependent manner and the altered DNA methylation pattern was only partly explained the observed aberrant gene expression patterns of the blastocysts.

Authors+Show Affiliations

Institute of Animal Science, Animal Breeding and Husbandry Group, University of Bonn, 53115 Bonn, Germany.Centre de recherche en biologie de la reproduction, Faculté des sciences de l'agriculture et de l'alimentation, INAF, Pavillon des services, Université Laval (Québec), Canada G1V 0A6.Institute of Animal Science, Animal Breeding and Husbandry Group, University of Bonn, 53115 Bonn, Germany.Institute of Animal Science, Animal Breeding and Husbandry Group, University of Bonn, 53115 Bonn, Germany.Institute of Animal Science, Animal Breeding and Husbandry Group, University of Bonn, 53115 Bonn, Germany.Institute of Animal Science, Animal Breeding and Husbandry Group, University of Bonn, 53115 Bonn, Germany.Institute of Animal Science, Animal Breeding and Husbandry Group, University of Bonn, 53115 Bonn, Germany.Institute of Animal Breeding and Genetics, University of Veterinary Medicine Vienna, A-1210, Vienna, Austria.Institute of Animal Breeding and Genetics, University of Veterinary Medicine Vienna, A-1210, Vienna, Austria.Institute of Animal Science, Animal Breeding and Husbandry Group, University of Bonn, 53115 Bonn, Germany.Centre de recherche en biologie de la reproduction, Faculté des sciences de l'agriculture et de l'alimentation, INAF, Pavillon des services, Université Laval (Québec), Canada G1V 0A6.Centre de recherche en biologie de la reproduction, Faculté des sciences de l'agriculture et de l'alimentation, INAF, Pavillon des services, Université Laval (Québec), Canada G1V 0A6.Centre de recherche en biologie de la reproduction, Faculté des sciences de l'agriculture et de l'alimentation, INAF, Pavillon des services, Université Laval (Québec), Canada G1V 0A6.Centre de recherche en biologie de la reproduction, Faculté des sciences de l'agriculture et de l'alimentation, INAF, Pavillon des services, Université Laval (Québec), Canada G1V 0A6.Department of Animal Production, Faculty of Agriculture, Cairo University, 12613, Giza, Egypt.Institute of Animal Science, Animal Breeding and Husbandry Group, University of Bonn, 53115 Bonn, Germany.Institute of Animal Science, Animal Breeding and Husbandry Group, University of Bonn, 53115 Bonn, Germany.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

26536655

Citation

Salilew-Wondim, Dessie, et al. "Genome-Wide DNA Methylation Patterns of Bovine Blastocysts Developed in Vivo From Embryos Completed Different Stages of Development in Vitro." PloS One, vol. 10, no. 11, 2015, pp. e0140467.
Salilew-Wondim D, Fournier E, Hoelker M, et al. Genome-Wide DNA Methylation Patterns of Bovine Blastocysts Developed In Vivo from Embryos Completed Different Stages of Development In Vitro. PLoS ONE. 2015;10(11):e0140467.
Salilew-Wondim, D., Fournier, E., Hoelker, M., Saeed-Zidane, M., Tholen, E., Looft, C., Neuhoff, C., Besenfelder, U., Havlicek, V., Rings, F., Gagné, D., Sirard, M. A., Robert, C., Shojaei Saadi, H. A., Gad, A., Schellander, K., & Tesfaye, D. (2015). Genome-Wide DNA Methylation Patterns of Bovine Blastocysts Developed In Vivo from Embryos Completed Different Stages of Development In Vitro. PloS One, 10(11), e0140467. https://doi.org/10.1371/journal.pone.0140467
Salilew-Wondim D, et al. Genome-Wide DNA Methylation Patterns of Bovine Blastocysts Developed in Vivo From Embryos Completed Different Stages of Development in Vitro. PLoS ONE. 2015;10(11):e0140467. PubMed PMID: 26536655.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Genome-Wide DNA Methylation Patterns of Bovine Blastocysts Developed In Vivo from Embryos Completed Different Stages of Development In Vitro. AU - Salilew-Wondim,Dessie, AU - Fournier,Eric, AU - Hoelker,Michael, AU - Saeed-Zidane,Mohammed, AU - Tholen,Ernst, AU - Looft,Christian, AU - Neuhoff,Christiane, AU - Besenfelder,Urban, AU - Havlicek,Vita, AU - Rings,Franca, AU - Gagné,Dominic, AU - Sirard,Marc-André, AU - Robert,Claude, AU - Shojaei Saadi,Habib A, AU - Gad,Ahmed, AU - Schellander,Karl, AU - Tesfaye,Dawit, Y1 - 2015/11/04/ PY - 2015/05/31/received PY - 2015/09/25/accepted PY - 2015/11/5/entrez PY - 2015/11/5/pubmed PY - 2016/7/1/medline SP - e0140467 EP - e0140467 JF - PloS one JO - PLoS ONE VL - 10 IS - 11 N2 - Early embryonic loss and altered gene expression in in vitro produced blastocysts are believed to be partly caused by aberrant DNA methylation. However, specific embryonic stage which is sensitive to in vitro culture conditions to alter the DNA methylation profile of the resulting blastocysts remained unclear. Therefore, the aim of this study was to investigate the stage specific effect of in vitro culture environment on the DNA methylation response of the resulting blastocysts. For this, embryos cultured in vitro until zygote (ZY), 4-cell (4C) or 16-cell (16C) were transferred to recipients and the blastocysts were recovery at day 7 of the estrous cycle. Another embryo group was cultured in vitro until blastocyst stage (IVP). Genome-wide DNA methylation profiles of ZY, 4C, 16C and IVP blastocyst groups were then determined with reference to blastocysts developed completely under in vivo condition (VO) using EmbryoGENE DNA Methylation Array. To assess the contribution of methylation changes on gene expression patterns, the DNA methylation data was superimposed to the transcriptome profile data. The degree of DNA methylation dysregulation in the promoter and/or gene body regions of the resulting blastocysts was correlated with successive stages of development the embryos advanced under in vitro culture before transfer to the in vivo condition. Genomic enrichment analysis revealed that in 4C and 16C blastocyst groups, hypermethylated loci were outpacing the hypomethylated ones in intronic, exonic, promoter and proximal promoter regions, whereas the reverse was observed in ZY blastocyst group. However, in the IVP group, as much hypermethylated as hypomethylated probes were detected in gene body and promoter regions. In addition, gene ontology analysis indicated that differentially methylated regions were found to affected several biological functions including ATP binding in the ZY group, programmed cell death in the 4C, glycolysis in 16C and genetic imprinting and chromosome segregation in IVP blastocyst groups. Furthermore, 1.6, 3.4, 3.9 and 9.4% of the differentially methylated regions that were overlapped to the transcriptome profile data were negatively correlated with the gene expression patterns in ZY, 4C, 16C and IVP blastocyst groups, respectively. Therefore, this finding indicated that suboptimal culture condition during preimplantation embryo development induced changes in the DNA methylation landscape of the resulting blastocysts in a stage dependent manner and the altered DNA methylation pattern was only partly explained the observed aberrant gene expression patterns of the blastocysts. SN - 1932-6203 UR - https://www.unboundmedicine.com/medline/citation/26536655/Genome_Wide_DNA_Methylation_Patterns_of_Bovine_Blastocysts_Developed_In_Vivo_from_Embryos_Completed_Different_Stages_of_Development_In_Vitro_ L2 - http://dx.plos.org/10.1371/journal.pone.0140467 DB - PRIME DP - Unbound Medicine ER -