The DNA methylation landscape of human early embryos
Base-resolution maps of DNA methylation in human gametes and early embryos offer novel insights into human methylation dynamics and the functional relationship between DNA methylation and gene expression. DNA methylation in the early embryo Global patterns of DNA methylation are drastically reprogra...
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| Published in | Nature (London) Vol. 511; no. 7511; pp. 606 - 610 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
31.07.2014
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Base-resolution maps of DNA methylation in human gametes and early embryos offer novel insights into human methylation dynamics and the functional relationship between DNA methylation and gene expression.
DNA methylation in the early embryo
Global patterns of DNA methylation are drastically reprogrammed in primordial germ cells and early embryonic development in mammals. This reprogramming has been well characterized in mouse embryos, but a detailed understanding of DNA methylation dynamics in human embryos is lacking. Two papers published this week [in this issue of
Nature
] reveal there is a massive loss of DNA methylation from most of the human genome immediately after fertilization, confirming that this epigenetic reprogramming is an evolutionarily conserved feature of development. Hongshan Guo
et al
. produced base-resolution maps of DNA methylation for human gametes and at several developmental stages of embryogenesis. Zachary Smith
et al
. obtained similar maps of DNA methylation at several developmental stages of early human embryogenesis and during derivation of human embryonic stem cell lines. The studies provide insights into differences between mouse and human methylation dynamics and the functional relationship between DNA methylation and the expression of genes and transposable elements.
DNA methylation is a crucial element in the epigenetic regulation of mammalian embryonic development
1
,
2
,
3
,
4
,
5
. However, its dynamic patterns have not been analysed at the genome scale in human pre-implantation embryos due to technical difficulties and the scarcity of required materials. Here we systematically profile the methylome of human early embryos from the zygotic stage through to post-implantation by reduced representation bisulphite sequencing and whole-genome bisulphite sequencing. We show that the major wave of genome-wide demethylation is complete at the 2-cell stage, contrary to previous observations in mice. Moreover, the demethylation of the paternal genome is much faster than that of the maternal genome, and by the end of the zygotic stage the genome-wide methylation level in male pronuclei is already lower than that in female pronuclei. The inverse correlation between promoter methylation and gene expression gradually strengthens during early embryonic development, reaching its peak at the post-implantation stage. Furthermore, we show that active genes, with the trimethylation of histone H3 at lysine 4 (H3K4me3) mark at the promoter regions in pluripotent human embryonic stem cells, are essentially devoid of DNA methylation in both mature gametes and throughout pre-implantation development. Finally, we also show that long interspersed nuclear elements or short interspersed nuclear elements that are evolutionarily young are demethylated to a milder extent compared to older elements in the same family and have higher abundance of transcripts, indicating that early embryos tend to retain higher residual methylation at the evolutionarily younger and more active transposable elements. Our work provides insights into the critical features of the methylome of human early embryos, as well as its functional relation to the regulation of gene expression and the repression of transposable elements. |
|---|---|
| AbstractList | DNA methylation is a crucial element in the epigenetic regulation of mammalian embryonic development. However, its dynamic patterns have not been analysed at the genome scale in human pre-implantation embryos due to technical difficulties and the scarcity of required materials. Here we systematically profile the methylome of human early embryos from the zygotic stage through to post-implantation by reduced representation bisulphite sequencing and whole-genome bisulphite sequencing. We show that the major wave of genome-wide demethylation is complete at the 2-cell stage, contrary to previous observations in mice. Moreover, the demethylation of the paternal genome is much faster than that of the maternal genome, and by the end of the zygotic stage the genome-wide methylation level in male pronuclei is already lower than that in female pronuclei. The inverse correlation between promoter methylation and gene expression gradually strengthens during early embryonic development, reaching its peak at the post-implantation stage. Furthermore, we show that active genes, with the trimethylation of histone H3 at lysine 4 (H3K4me3) mark at the promoter regions in pluripotent human embryonic stem cells, are essentially devoid of DNA methylation in both mature gametes and throughout pre-implantation development. Finally, we also show that long interspersed nuclear elements or short interspersed nuclear elements that are evolutionarily young are demethylated to a milder extent compared to older elements in the same family and have higher abundance of transcripts, indicating that early embryos tend to retain higher residual methylation at the evolutionarily younger and more active transposable elements. Our work provides insights into the critical features of the methylome of human early embryos, as well as its functional relation to the regulation of gene expression and the repression of transposable elements.DNA methylation is a crucial element in the epigenetic regulation of mammalian embryonic development. However, its dynamic patterns have not been analysed at the genome scale in human pre-implantation embryos due to technical difficulties and the scarcity of required materials. Here we systematically profile the methylome of human early embryos from the zygotic stage through to post-implantation by reduced representation bisulphite sequencing and whole-genome bisulphite sequencing. We show that the major wave of genome-wide demethylation is complete at the 2-cell stage, contrary to previous observations in mice. Moreover, the demethylation of the paternal genome is much faster than that of the maternal genome, and by the end of the zygotic stage the genome-wide methylation level in male pronuclei is already lower than that in female pronuclei. The inverse correlation between promoter methylation and gene expression gradually strengthens during early embryonic development, reaching its peak at the post-implantation stage. Furthermore, we show that active genes, with the trimethylation of histone H3 at lysine 4 (H3K4me3) mark at the promoter regions in pluripotent human embryonic stem cells, are essentially devoid of DNA methylation in both mature gametes and throughout pre-implantation development. Finally, we also show that long interspersed nuclear elements or short interspersed nuclear elements that are evolutionarily young are demethylated to a milder extent compared to older elements in the same family and have higher abundance of transcripts, indicating that early embryos tend to retain higher residual methylation at the evolutionarily younger and more active transposable elements. Our work provides insights into the critical features of the methylome of human early embryos, as well as its functional relation to the regulation of gene expression and the repression of transposable elements. Base-resolution maps of DNA methylation in human gametes and early embryos offer novel insights into human methylation dynamics and the functional relationship between DNA methylation and gene expression. DNA methylation in the early embryo Global patterns of DNA methylation are drastically reprogrammed in primordial germ cells and early embryonic development in mammals. This reprogramming has been well characterized in mouse embryos, but a detailed understanding of DNA methylation dynamics in human embryos is lacking. Two papers published this week [in this issue of Nature ] reveal there is a massive loss of DNA methylation from most of the human genome immediately after fertilization, confirming that this epigenetic reprogramming is an evolutionarily conserved feature of development. Hongshan Guo et al . produced base-resolution maps of DNA methylation for human gametes and at several developmental stages of embryogenesis. Zachary Smith et al . obtained similar maps of DNA methylation at several developmental stages of early human embryogenesis and during derivation of human embryonic stem cell lines. The studies provide insights into differences between mouse and human methylation dynamics and the functional relationship between DNA methylation and the expression of genes and transposable elements. DNA methylation is a crucial element in the epigenetic regulation of mammalian embryonic development 1 , 2 , 3 , 4 , 5 . However, its dynamic patterns have not been analysed at the genome scale in human pre-implantation embryos due to technical difficulties and the scarcity of required materials. Here we systematically profile the methylome of human early embryos from the zygotic stage through to post-implantation by reduced representation bisulphite sequencing and whole-genome bisulphite sequencing. We show that the major wave of genome-wide demethylation is complete at the 2-cell stage, contrary to previous observations in mice. Moreover, the demethylation of the paternal genome is much faster than that of the maternal genome, and by the end of the zygotic stage the genome-wide methylation level in male pronuclei is already lower than that in female pronuclei. The inverse correlation between promoter methylation and gene expression gradually strengthens during early embryonic development, reaching its peak at the post-implantation stage. Furthermore, we show that active genes, with the trimethylation of histone H3 at lysine 4 (H3K4me3) mark at the promoter regions in pluripotent human embryonic stem cells, are essentially devoid of DNA methylation in both mature gametes and throughout pre-implantation development. Finally, we also show that long interspersed nuclear elements or short interspersed nuclear elements that are evolutionarily young are demethylated to a milder extent compared to older elements in the same family and have higher abundance of transcripts, indicating that early embryos tend to retain higher residual methylation at the evolutionarily younger and more active transposable elements. Our work provides insights into the critical features of the methylome of human early embryos, as well as its functional relation to the regulation of gene expression and the repression of transposable elements. DNA methylation is a crucial element in the epigenetic regulation of mammalian embryonic development (1-5). However, its dynamic patterns have not been analysed at the genome scale in human pre-implantation embryos due to technical difficulties and the scarcity of required materials. Here we systematically profile the methylome of human early embryos from the zygotic stage through to post-implantation by reduced representation bisulphite sequencing and whole-genome bisulphite sequencing. We show that the major wave of genome-wide demethylation is complete at the 2-cell stage, contrary to previous observations in mice. Moreover, the demethylation of the paternal genome is much faster than that of the maternal genome, and by the end of the zygotic stage the genome-wide methylation level in male pronuclei is already lower than that in female pronuclei. The inverse correlation between promoter methylation and gene expression gradually strengthens during early embryonic development, reaching its peak at the post-implantation stage. Furthermore, we show that active genes, with the trimethylation of histone H3 at lysine 4 (H3K4me3) mark at the promoter regions in pluripotent human embryonic stem cells, are essentially devoid of DNA methylation in both mature gametes and throughout pre-implantation development. Finally, we also show that long interspersed nuclear elements or short interspersed nuclear elements that are evolutionarily young are demethylated to a milder extent compared to older elements in the same family and have higher abundance of transcripts, indicating that early embryos tend to retain higher residual methylation at the evolutionarily younger and more active transposable elements. Our work provides insights into the critical features of the methylome of human early embryos, as well as its functional relation to the regulation of gene expression and the repression of transposable elements. DNA methylation is a crucial element in the epigenetic regulation of mammalian embryonic development. However, its dynamic patterns have not been analysed at the genome scale in human pre-implantation embryos due to technical difficulties and the scarcity of required materials. Here we systematically profile the methylome of human early embryos from the zygotic stage through to post-implantation by reduced representation bisulphite sequencing and whole-genome bisulphite sequencing. We show that the major wave of genome-wide demethylation is complete at the 2-cell stage, contrary to previous observations in mice. Moreover, the demethylation of the paternal genome is much faster than that of the maternal genome, and by the end of the zygotic stage the genome-wide methylation level in male pronuclei is already lower than that in female pronuclei. The inverse correlation between promoter methylation and gene expression gradually strengthens during early embryonic development, reaching its peak at the post-implantation stage. Furthermore, we show that active genes, with the trimethylation of histone H3 at lysine 4 (H3K4me3) mark at the promoter regions in pluripotent human embryonic stem cells, are essentially devoid of DNA methylation in both mature gametes and throughout pre-implantation development. Finally, we also show that long interspersed nuclear elements or short interspersed nuclear elements that are evolutionarily young are demethylated to a milder extent compared to older elements in the same family and have higher abundance of transcripts, indicating that early embryos tend to retain higher residual methylation at the evolutionarily younger and more active transposable elements. Our work provides insights into the critical features of the methylome of human early embryos, as well as its functional relation to the regulation of gene expression and the repression of transposable elements. |
| Audience | Academic |
| Author | Wu, Xinglong Wang, Wei Lian, Ying Xie, Sunney X. Yan, Liying Hu, Boqiang Shi, Xiaodan Wei, Yuan Ren, Xiulian Jin, Xiaohu Yan, Jie Wang, Xiaoye Liu, Ping Li, Xianlong Lin, Shengli Li, Rong Tang, Fuchou Wen, Lu Qiao, Jie Fan, Xiaoying Guo, Hongshan Guo, Fan Zhu, Ping Li, Junsheng Yong, Jun |
| Author_xml | – sequence: 1 givenname: Hongshan surname: Guo fullname: Guo, Hongshan organization: Biodynamic Optical Imaging Center & Center for Reproductive Medicine, College of Life Sciences, Third Hospital, Peking University – sequence: 2 givenname: Ping surname: Zhu fullname: Zhu, Ping organization: Biodynamic Optical Imaging Center & Center for Reproductive Medicine, College of Life Sciences, Third Hospital, Peking University, Peking-Tsinghua Center for Life Sciences, Peking University – sequence: 3 givenname: Liying surname: Yan fullname: Yan, Liying organization: Biodynamic Optical Imaging Center & Center for Reproductive Medicine, College of Life Sciences, Third Hospital, Peking University, Key Laboratory of Assisted Reproduction, Ministry of Education – sequence: 4 givenname: Rong surname: Li fullname: Li, Rong organization: Biodynamic Optical Imaging Center & Center for Reproductive Medicine, College of Life Sciences, Third Hospital, Peking University, Key Laboratory of Assisted Reproduction, Ministry of Education – sequence: 5 givenname: Boqiang surname: Hu fullname: Hu, Boqiang organization: Biodynamic Optical Imaging Center & Center for Reproductive Medicine, College of Life Sciences, Third Hospital, Peking University – sequence: 6 givenname: Ying surname: Lian fullname: Lian, Ying organization: Biodynamic Optical Imaging Center & Center for Reproductive Medicine, College of Life Sciences, Third Hospital, Peking University, Key Laboratory of Assisted Reproduction, Ministry of Education – sequence: 7 givenname: Jie surname: Yan fullname: Yan, Jie organization: Biodynamic Optical Imaging Center & Center for Reproductive Medicine, College of Life Sciences, Third Hospital, Peking University, Key Laboratory of Assisted Reproduction, Ministry of Education – sequence: 8 givenname: Xiulian surname: Ren fullname: Ren, Xiulian organization: Biodynamic Optical Imaging Center & Center for Reproductive Medicine, College of Life Sciences, Third Hospital, Peking University, Key Laboratory of Assisted Reproduction, Ministry of Education – sequence: 9 givenname: Shengli surname: Lin fullname: Lin, Shengli organization: Biodynamic Optical Imaging Center & Center for Reproductive Medicine, College of Life Sciences, Third Hospital, Peking University, Key Laboratory of Assisted Reproduction, Ministry of Education – sequence: 10 givenname: Junsheng surname: Li fullname: Li, Junsheng organization: Biodynamic Optical Imaging Center & Center for Reproductive Medicine, College of Life Sciences, Third Hospital, Peking University, Key Laboratory of Assisted Reproduction, Ministry of Education – sequence: 11 givenname: Xiaohu surname: Jin fullname: Jin, Xiaohu organization: Biodynamic Optical Imaging Center & Center for Reproductive Medicine, College of Life Sciences, Third Hospital, Peking University, Key Laboratory of Assisted Reproduction, Ministry of Education – sequence: 12 givenname: Xiaodan surname: Shi fullname: Shi, Xiaodan organization: Biodynamic Optical Imaging Center & Center for Reproductive Medicine, College of Life Sciences, Third Hospital, Peking University, Key Laboratory of Assisted Reproduction, Ministry of Education – sequence: 13 givenname: Ping surname: Liu fullname: Liu, Ping organization: Biodynamic Optical Imaging Center & Center for Reproductive Medicine, College of Life Sciences, Third Hospital, Peking University, Key Laboratory of Assisted Reproduction, Ministry of Education – sequence: 14 givenname: Xiaoye surname: Wang fullname: Wang, Xiaoye organization: Department of Obstetrics and Gynecology, Peking University Third Hospital – sequence: 15 givenname: Wei surname: Wang fullname: Wang, Wei organization: Department of Obstetrics and Gynecology, Peking University Third Hospital – sequence: 16 givenname: Yuan surname: Wei fullname: Wei, Yuan organization: Department of Obstetrics and Gynecology, Peking University Third Hospital – sequence: 17 givenname: Xianlong surname: Li fullname: Li, Xianlong organization: Biodynamic Optical Imaging Center & Center for Reproductive Medicine, College of Life Sciences, Third Hospital, Peking University – sequence: 18 givenname: Fan surname: Guo fullname: Guo, Fan organization: Biodynamic Optical Imaging Center & Center for Reproductive Medicine, College of Life Sciences, Third Hospital, Peking University – sequence: 19 givenname: Xinglong surname: Wu fullname: Wu, Xinglong organization: Biodynamic Optical Imaging Center & Center for Reproductive Medicine, College of Life Sciences, Third Hospital, Peking University – sequence: 20 givenname: Xiaoying surname: Fan fullname: Fan, Xiaoying organization: Biodynamic Optical Imaging Center & Center for Reproductive Medicine, College of Life Sciences, Third Hospital, Peking University – sequence: 21 givenname: Jun surname: Yong fullname: Yong, Jun organization: Biodynamic Optical Imaging Center & Center for Reproductive Medicine, College of Life Sciences, Third Hospital, Peking University, Department of Chemistry and Chemical Biology, Harvard University – sequence: 22 givenname: Lu surname: Wen fullname: Wen, Lu organization: Biodynamic Optical Imaging Center & Center for Reproductive Medicine, College of Life Sciences, Third Hospital, Peking University – sequence: 23 givenname: Sunney X. surname: Xie fullname: Xie, Sunney X. organization: Biodynamic Optical Imaging Center & Center for Reproductive Medicine, College of Life Sciences, Third Hospital, Peking University, Department of Chemistry and Chemical Biology, Harvard University – sequence: 24 givenname: Fuchou surname: Tang fullname: Tang, Fuchou email: tangfuchou@pku.edu.cn organization: Biodynamic Optical Imaging Center & Center for Reproductive Medicine, College of Life Sciences, Third Hospital, Peking University, Ministry of Education Key Laboratory of Cell Proliferation and Differentiation, Beijing 100871, China – sequence: 25 givenname: Jie surname: Qiao fullname: Qiao, Jie email: jie.qiao@263.net organization: Biodynamic Optical Imaging Center & Center for Reproductive Medicine, College of Life Sciences, Third Hospital, Peking University, Key Laboratory of Assisted Reproduction, Ministry of Education |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25079557$$D View this record in MEDLINE/PubMed |
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| Snippet | Base-resolution maps of DNA methylation in human gametes and early embryos offer novel insights into human methylation dynamics and the functional relationship... DNA methylation is a crucial element in the epigenetic regulation of mammalian embryonic development. However, its dynamic patterns have not been analysed at... DNA methylation is a crucial element in the epigenetic regulation of mammalian embryonic development (1-5). However, its dynamic patterns have not been... |
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| SubjectTerms | 631/136/2086 631/136/2435 631/337/176/1988 Analysis Animals Deoxyribonucleic acid DNA DNA Methylation DNA Transposable Elements - genetics Embryo, Mammalian Embryonic development Embryonic growth stage Embryonic Stem Cells - physiology Embryos Epigenesis, Genetic Epigenetic inheritance Female Gene Expression Profiling Gene Expression Regulation, Developmental Genes Genome-wide association studies Genomes Genomics Germ Cells - metabolism Histones - metabolism Humanities and Social Sciences Humans letter Long Interspersed Nucleotide Elements - genetics Male Methylation Mice multidisciplinary Promoter Regions, Genetic - genetics Science Short Interspersed Nucleotide Elements - genetics Stem cells |
| Title | The DNA methylation landscape of human early embryos |
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