The control of transcriptional memory by stable mitotic bookmarking

Maëlle Bellec, Jérémy Dufourt, George Hunt, Hélène Lenden-Hasse, Antonio Trullo, Amal Zine El Aabidine, Marie Lamarque, Marissa M. Gaskill, Heloïse Faure-Gautron, Mattias Mannervik, Melissa M. Harrison, Jean-Christophe Andrau, Cyril Favard, Ovidiu Radulescu and Mounia Lagha ()
Additional contact information
Maëlle Bellec: University of Montpellier, CNRS-UMR 5535
Jérémy Dufourt: University of Montpellier, CNRS-UMR 5535
George Hunt: Stockholm University
Hélène Lenden-Hasse: University of Montpellier, CNRS-UMR 5535
Antonio Trullo: University of Montpellier, CNRS-UMR 5535
Amal Zine El Aabidine: University of Montpellier, CNRS-UMR 5535
Marie Lamarque: University of Montpellier, CNRS-UMR 5535
Marissa M. Gaskill: University of Wisconsin-Madison
Heloïse Faure-Gautron: University of Montpellier, CNRS-UMR 5535
Mattias Mannervik: Stockholm University
Melissa M. Harrison: University of Wisconsin-Madison
Jean-Christophe Andrau: University of Montpellier, CNRS-UMR 5535
Cyril Favard: University of Montpellier
Ovidiu Radulescu: LPHI, UMR CNRS 5235, University of Montpellier, Place E. Bataillon – Bât. 24 cc 107
Mounia Lagha: University of Montpellier, CNRS-UMR 5535

Nature Communications, 2022, vol. 13, issue 1, 1-14

Abstract: Abstract To maintain cellular identities during development, gene expression profiles must be faithfully propagated through cell generations. The reestablishment of gene expression patterns upon mitotic exit is mediated, in part, by transcription factors (TF) mitotic bookmarking. However, the mechanisms and functions of TF mitotic bookmarking during early embryogenesis remain poorly understood. In this study, taking advantage of the naturally synchronized mitoses of Drosophila early embryos, we provide evidence that GAGA pioneer factor (GAF) acts as a stable mitotic bookmarker during zygotic genome activation. We show that, during mitosis, GAF remains associated to a large fraction of its interphase targets, including at cis-regulatory sequences of key developmental genes with both active and repressive chromatin signatures. GAF mitotic targets are globally accessible during mitosis and are bookmarked via histone acetylation (H4K8ac). By monitoring the kinetics of transcriptional activation in living embryos, we report that GAF binding establishes competence for rapid activation upon mitotic exit.

Date: 2022
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DOI: 10.1038/s41467-022-28855-y

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