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Maintenance of spatial gene expression by Polycomb-mediated repression after formation of a vertebrate body plan

Julien Rougeot, Naomi D. Chrispijn, Marco Aben, Dei M. Elurbe, Karolina M. Andralojc, Patrick J. Murphy, Pascal W.T.C. Jansen, Michiel Vermeulen, Bradley R. Cairns, View ORCID ProfileLeonie M. Kamminga
doi: https://doi.org/10.1101/468769
Julien Rougeot
1Radboud University, Faculty of Science, Department of Molecular Biology, Radboud Institute for Molecular Life Sciences, Nijmegen, the Netherlands
2Radboud University Medical Center, Department of Molecular Biology, Nijmegen, the Netherlands
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  • For correspondence: l.kamminga@science.ru.nl julien.rougeot@wur.nl
Naomi D. Chrispijn
1Radboud University, Faculty of Science, Department of Molecular Biology, Radboud Institute for Molecular Life Sciences, Nijmegen, the Netherlands
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Marco Aben
1Radboud University, Faculty of Science, Department of Molecular Biology, Radboud Institute for Molecular Life Sciences, Nijmegen, the Netherlands
2Radboud University Medical Center, Department of Molecular Biology, Nijmegen, the Netherlands
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Dei M. Elurbe
1Radboud University, Faculty of Science, Department of Molecular Biology, Radboud Institute for Molecular Life Sciences, Nijmegen, the Netherlands
2Radboud University Medical Center, Department of Molecular Biology, Nijmegen, the Netherlands
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Karolina M. Andralojc
1Radboud University, Faculty of Science, Department of Molecular Biology, Radboud Institute for Molecular Life Sciences, Nijmegen, the Netherlands
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Patrick J. Murphy
3Howard Hughes Medical Institute, Department of Oncological Sciences and Huntsman Cancer Institute, University of Utah School of Medicine, Salt Lake City, UT 84112, USA
4Wilmot Cancer Institute, Rochester Center for Biomedical Informatics, University of Rochester Medical Center, Rochester, NY
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Pascal W.T.C. Jansen
5Radboud University, Department of Molecular Biology, Faculty of Science, Radboud Institute for Molecular Life Sciences, Oncode Institute, Nijmegen, the Netherlands
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Michiel Vermeulen
5Radboud University, Department of Molecular Biology, Faculty of Science, Radboud Institute for Molecular Life Sciences, Oncode Institute, Nijmegen, the Netherlands
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Bradley R. Cairns
3Howard Hughes Medical Institute, Department of Oncological Sciences and Huntsman Cancer Institute, University of Utah School of Medicine, Salt Lake City, UT 84112, USA
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Leonie M. Kamminga
1Radboud University, Faculty of Science, Department of Molecular Biology, Radboud Institute for Molecular Life Sciences, Nijmegen, the Netherlands
2Radboud University Medical Center, Department of Molecular Biology, Nijmegen, the Netherlands
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  • ORCID record for Leonie M. Kamminga
  • For correspondence: l.kamminga@science.ru.nl julien.rougeot@wur.nl
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Abstract

Polycomb group (PcG) proteins are transcriptional repressors that are important regulators of cell fate during embryonic development. Among them, Ezh2 is responsible for catalyzing the epigenetic repressive mark H3K27me3 and is essential for animal development. The ability of zebrafish embryos lacking both maternal and zygotic ezh2 to form a normal body plan provides a unique model to comprehensively study Ezh2 function during early development in vertebrates. By using a multi-omics approach, we found that Ezh2 is required for the deposition of H3K27me3 and is essential for the recruitment of Polycomb group protein Rnf2. However, and despite the complete absence of PcG-associated epigenetic mark and proteins, only minor changes in H3K4me3 deposition and gene and protein expression occurred. These changes were mainly due to local deregulation of transcription factors outside their normal expression boundaries. Altogether, our results in zebrafish show that Polycomb-mediated gene repression is important right after the body plan is formed to maintain spatially restricted expression profiles of transcription factors and highlight the differences that exist in the timing of PcG protein action between vertebrate species.

Summary statement Our unique zebrafish model of maternal and zygotic mutant for the Polycomb group gene ezh2 reveals major conserved and divergent mechanisms in epigenetic gene repression during vertebrate development.

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Posted April 11, 2019.
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Maintenance of spatial gene expression by Polycomb-mediated repression after formation of a vertebrate body plan
Julien Rougeot, Naomi D. Chrispijn, Marco Aben, Dei M. Elurbe, Karolina M. Andralojc, Patrick J. Murphy, Pascal W.T.C. Jansen, Michiel Vermeulen, Bradley R. Cairns, Leonie M. Kamminga
bioRxiv 468769; doi: https://doi.org/10.1101/468769
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Maintenance of spatial gene expression by Polycomb-mediated repression after formation of a vertebrate body plan
Julien Rougeot, Naomi D. Chrispijn, Marco Aben, Dei M. Elurbe, Karolina M. Andralojc, Patrick J. Murphy, Pascal W.T.C. Jansen, Michiel Vermeulen, Bradley R. Cairns, Leonie M. Kamminga
bioRxiv 468769; doi: https://doi.org/10.1101/468769

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