In vivo analysis reveals that ATP-hydrolysis couples remodeling to SWI/SNF release from chromatin

Ben C. Tilly*, Gillian E. Chalkley, Jan A. van der Knaap, Yuri M. Moshkin, Tsung Wai Kan, Dick H.W. Dekkers, Jeroen A.A. Demmers, C. Peter Verrijzer*

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

13 Citations (Scopus)
86 Downloads (Pure)

Abstract

ATP-dependent chromatin remodelers control the accessibility of genomic DNA through nucleosome mobilization. However, the dynamics of genome exploration by remodelers, and the role of ATP hydrolysis in this process remain unclear. We used live-cell imaging of Drosophila polytene nuclei to monitor Brahma (BRM) remodeler interactions with its chromosomal targets. In parallel, we measured local chromatin condensation and its effect on BRM association. Surprisingly, only a small portion of BRM is bound to chromatin at any given time. BRM binds decondensed chromatin but is excluded from condensed chromatin, limiting its genomic search space. BRM- chromatin interactions are highly dynamic, whereas histone-exchange is limited and much slower. Intriguingly, loss of ATP hydrolysis enhanced chromatin retention and clustering of BRM, which was associated with reduced histone turnover. Thus, ATP hydrolysis couples nucleosome remodeling to remodeler release, driving a continuous transient probing of the genome.

Original languageEnglish
Article numbere69424
JournaleLife
Volume10
DOIs
Publication statusPublished - 27 Jul 2021

Bibliographical note

Funding Information:
We thank Jean-Michel Gilbert, Francois Karch, and Renato Paro for the gift of fly stocks and the Erasmus Optical Imaging Centre (Gert van Cappellen, Adriaan Houtsmuller and Gert-Jan Kremers) for technical assistance and helpful discussions. We also acknowledge Olaf Voets, Adrie Verhoeven and Prasanth Kumar for their assistance in generating various constructs during the initial stages of this project. We thank Jesper Svejstrup and Aniek van der Vaart for valuable comments on the manuscript. Finally, we thank Carl Wu and Jee Min Kim for sharing their results prior to submission for publication. This work was supported in part by a network grant from FOM (?DNA in action: Physics of the genome?).

Funding Information:
We thank Jean-Michel Gilbert, Francois Karch, and Renato Paro for the gift of fly stocks and the Erasmus Optical Imaging Centre (Gert van Cappellen, Adriaan Houtsmuller and Gert-Jan Kremers) for technical assistance and helpful discussions. We also acknowledge Olaf Voets, Adrie Verhoeven and Prasanth Kumar for their assistance in generating various constructs during the initial stages of this project. We thank Jesper Svejstrup and Aniek van der Vaart for valuable comments on the manuscript. Finally, we thank Carl Wu and Jee Min Kim for sharing their results prior to submission for publication. This work was supported in part by a network grant from FOM ("DNA in action: Physics of the genome").

Publisher Copyright:
© 2021, eLife Sciences Publications Ltd. All rights reserved.

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