H2AK119ub1 guides maternal inheritance and zygotic deposition of H3K27me3 in mouse embryos

doi:10.1038/s41588-021-00820-3

. 2021 Apr;53(4):539-550.

doi: 10.1038/s41588-021-00820-3. Epub 2021 Apr 5.

H2AK119ub1 guides maternal inheritance and zygotic deposition of H3K27me3 in mouse embryos

Hailiang Mei^#¹, Chisayo Kozuka¹, Ryoya Hayashi^{1

2}, Mami Kumon¹, Haruhiko Koseki^{3

4

5}, Azusa Inoue^#^{6

7}

Affiliations

¹ YCI Laboratory for Metabolic Epigenetics, RIKEN Center for Integrative Medical Sciences, Yokohama, Japan.
² Tokyo Metropolitan University, Hachioji, Japan.
³ Laboratory for Developmental Genetics, RIKEN Center for Integrative Medical Sciences, Yokohama, Japan.
⁴ AMED-CREST, Yokohama, Japan.
⁵ Cellular and Molecular Medicine, Advanced Research Departments, Graduate School of Medicine, Chiba University, Chiba, Japan.
⁶ YCI Laboratory for Metabolic Epigenetics, RIKEN Center for Integrative Medical Sciences, Yokohama, Japan. azusa.inoue@riken.jp.
⁷ Tokyo Metropolitan University, Hachioji, Japan. azusa.inoue@riken.jp.

^# Contributed equally.

PMID: 33821003
DOI: 10.1038/s41588-021-00820-3

H2AK119ub1 guides maternal inheritance and zygotic deposition of H3K27me3 in mouse embryos

Hailiang Mei et al. Nat Genet. 2021 Apr.

. 2021 Apr;53(4):539-550.

doi: 10.1038/s41588-021-00820-3. Epub 2021 Apr 5.

Authors

Hailiang Mei^#¹, Chisayo Kozuka¹, Ryoya Hayashi^{1

2}, Mami Kumon¹, Haruhiko Koseki^{3

4

5}, Azusa Inoue^#^{6

7}

Affiliations

¹ YCI Laboratory for Metabolic Epigenetics, RIKEN Center for Integrative Medical Sciences, Yokohama, Japan.
² Tokyo Metropolitan University, Hachioji, Japan.
³ Laboratory for Developmental Genetics, RIKEN Center for Integrative Medical Sciences, Yokohama, Japan.
⁴ AMED-CREST, Yokohama, Japan.
⁵ Cellular and Molecular Medicine, Advanced Research Departments, Graduate School of Medicine, Chiba University, Chiba, Japan.
⁶ YCI Laboratory for Metabolic Epigenetics, RIKEN Center for Integrative Medical Sciences, Yokohama, Japan. azusa.inoue@riken.jp.
⁷ Tokyo Metropolitan University, Hachioji, Japan. azusa.inoue@riken.jp.

^# Contributed equally.

PMID: 33821003
DOI: 10.1038/s41588-021-00820-3

Abstract

Parental epigenomes are established during gametogenesis. While they are largely reset after fertilization, broad domains of Polycomb repressive complex 2 (PRC2)-mediated formation of lysine 27-trimethylated histone H3 (H3K27me3) are inherited from oocytes in mice. How maternal H3K27me3 is established and inherited by embryos remains elusive. Here, we show that PRC1-mediated formation of lysine 119-monoubiquititinated histone H2A (H2AK119ub1) confers maternally heritable H3K27me3. Temporal profiling of H2AK119ub1 dynamics revealed that atypically broad H2AK119ub1 domains are established, along with H3K27me3, during oocyte growth. From the two-cell stage, H2AK119ub1 is progressively deposited at typical Polycomb targets and precedes H3K27me3. Reduction of H2AK119ub1 by depletion of Polycomb group ring finger 1 (PCGF1) and PCGF6-essential components of variant PRC1 (vPRC1)-leads to H3K27me3 loss at a subset of genes in oocytes. The gene-selective H3K27me3 deficiency is irreversibly inherited by embryos, causing loss of maternal H3K27me3-dependent imprinting, embryonic sublethality and placental enlargement at term. Collectively, our study unveils preceding dynamics of H2AK119ub1 over H3K27me3 at the maternal-to-zygotic transition, and identifies PCGF1/6-vPRC1 as an essential player in maternal epigenetic inheritance.

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Comment in

The Polycomb landscape in mouse development.
Richard Albert J, Greenberg MVC. Richard Albert J, et al. Nat Genet. 2021 Apr;53(4):427-429. doi: 10.1038/s41588-021-00833-y. Nat Genet. 2021. PMID: 33821004 No abstract available.

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References

1. Eckersley-Maslin, M. A., Alda-Catalinas, C. & Reik, W.Dynamics of the epigenetic landscape during the maternal-to-zygotic transition. Nat. Rev. Mol. Cell Biol. 19, 436–450 (2018). - PubMed - DOI
1. Borsos, M. et al. Genome–lamina interactions are established de novo in the early mouse embryo. Nature 569, 729–733 (2019). - PubMed - PMC - DOI
1. Burton, A. & Torres-Padilla, M. Epigenetic reprogramming and development: a unique heterochromatin organization in the preimplantation mouse embryo. Brief. Funct. Genomics 9, 444–454 (2010). - PubMed - PMC - DOI
1. Burton, A. & Torres-Padilla, M. Chromatin dynamics in the regulation of cell fate allocation during early embryogenesis. Nat. Rev. Mol. Cell Biol. 15, 723–735 (2014). - PubMed - DOI
1. Xu, Q. & Xie, W. Epigenome in early mammalian development: inheritance, reprogramming and establishment. Trends Cell Biol. 28, 237–253 (2018). - PubMed - DOI

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[1] Eckersley-Maslin, M. A., Alda-Catalinas, C. & Reik, W.Dynamics of the epigenetic landscape during the maternal-to-zygotic transition. Nat. Rev. Mol. Cell Biol. 19, 436–450 (2018). - PubMed - DOI

[2] Eckersley-Maslin, M. A., Alda-Catalinas, C. & Reik, W.Dynamics of the epigenetic landscape during the maternal-to-zygotic transition. Nat. Rev. Mol. Cell Biol. 19, 436–450 (2018). - PubMed - DOI

[3] Borsos, M. et al. Genome–lamina interactions are established de novo in the early mouse embryo. Nature 569, 729–733 (2019). - PubMed - PMC - DOI

[4] Borsos, M. et al. Genome–lamina interactions are established de novo in the early mouse embryo. Nature 569, 729–733 (2019). - PubMed - PMC - DOI

[5] Burton, A. & Torres-Padilla, M. Epigenetic reprogramming and development: a unique heterochromatin organization in the preimplantation mouse embryo. Brief. Funct. Genomics 9, 444–454 (2010). - PubMed - PMC - DOI

[6] Burton, A. & Torres-Padilla, M. Epigenetic reprogramming and development: a unique heterochromatin organization in the preimplantation mouse embryo. Brief. Funct. Genomics 9, 444–454 (2010). - PubMed - PMC - DOI

[7] Burton, A. & Torres-Padilla, M. Chromatin dynamics in the regulation of cell fate allocation during early embryogenesis. Nat. Rev. Mol. Cell Biol. 15, 723–735 (2014). - PubMed - DOI

[8] Burton, A. & Torres-Padilla, M. Chromatin dynamics in the regulation of cell fate allocation during early embryogenesis. Nat. Rev. Mol. Cell Biol. 15, 723–735 (2014). - PubMed - DOI

[9] Xu, Q. & Xie, W. Epigenome in early mammalian development: inheritance, reprogramming and establishment. Trends Cell Biol. 28, 237–253 (2018). - PubMed - DOI

[10] Xu, Q. & Xie, W. Epigenome in early mammalian development: inheritance, reprogramming and establishment. Trends Cell Biol. 28, 237–253 (2018). - PubMed - DOI

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H2AK119ub1 guides maternal inheritance and zygotic deposition of H3K27me3 in mouse embryos

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H2AK119ub1 guides maternal inheritance and zygotic deposition of H3K27me3 in mouse embryos

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