Polycomb function during oogenesis is required for mouse embryonic development

Eszter Posfai, Rico Kunzmann, Vincent Brochard, Juliette Salvaing, Erik Cabuy, Tim C. Roloff, Zichuan Liu, Mathieu Tardat, Maarten van Lohuizen, Miguel Vidal, Nathalie Beaujean, Antoine H.F.M. Peters

Research output: Contribution to journalArticle

68 Scopus citations

Abstract

In mammals, totipotent embryos are formed by fusion of highly differentiated gametes. Acquisition of totipotency concurs with chromatin remodeling of parental genomes, changes in the maternal transcriptome and proteome, and zygotic genome activation (ZGA). The inefficiency of reprogramming somatic nuclei in reproductive cloning suggests that intergenerational inheritance of germline chromatin contributes to developmental proficiency after natural conception. Here we show that Ring1 and Rnf2, components of Polycomb-repressive complex 1 (PRC1), serve redundant transcriptional functions during oogenesis that are essential for proper ZGA, replication and cell cycle progression in early embryos, and development beyond the two-cell stage. Exchange of chromosomes between control and Ring1/Rnf2-deficient metaphase II oocytes reveal cytoplasmic and chromosome-based contributions by PRC1 to embryonic development. Our results strongly support a model in which Polycomb acts in the female germline to establish developmental competence for the following generation by silencing differentiation-inducing genes and defining appropriate chromatin states.

Original languageEnglish (US)
Pages (from-to)920-932
Number of pages13
JournalGenes and Development
Volume26
Issue number9
DOIs
StatePublished - 2012

All Science Journal Classification (ASJC) codes

  • Genetics
  • Developmental Biology

Keywords

  • Epigenetic memory
  • Intergenerational inheritance
  • Intra-S-phase checkpoint
  • Maternal effect
  • Nuclear transfer
  • Polycomb-repressive complex 1

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  • Cite this

    Posfai, E., Kunzmann, R., Brochard, V., Salvaing, J., Cabuy, E., Roloff, T. C., Liu, Z., Tardat, M., van Lohuizen, M., Vidal, M., Beaujean, N., & Peters, A. H. F. M. (2012). Polycomb function during oogenesis is required for mouse embryonic development. Genes and Development, 26(9), 920-932. https://doi.org/10.1101/gad.188094.112