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

doi:10.7554/eLife.69424

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

Biochemistry

Research output: Contribution to journal › Article › Academic › peer-review

5 Citations (Scopus)

29 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 language	English
Article number	e69424
Journal	eLife
Volume	10
DOIs	https://doi.org/10.7554/eLife.69424
Publication status	Published - 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.

Access to Document

10.7554/eLife.69424Licence: CC BY

n vivo analysis reveals that ATP-hydrolysis couples remodeling toFinal published version, 10 MBLicence: CC BY

Cite this

@article{bc8f989846d84f07bd3515737f9a383a,

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

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.",

author = "Tilly, {Ben C.} and Chalkley, {Gillian E.} and {van der Knaap}, {Jan A.} and Moshkin, {Yuri M.} and Kan, {Tsung Wai} and Dekkers, {Dick H.W.} and Demmers, {Jeroen A.A.} and {Peter Verrijzer}, C.",

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: {\textcopyright} 2021, eLife Sciences Publications Ltd. All rights reserved.",

year = "2021",

month = jul,

day = "27",

doi = "10.7554/eLife.69424",

language = "English",

volume = "10",

journal = "eLife",

issn = "2050-084X",

publisher = "eLife Sciences Publications",

}

TY - JOUR

T1 - In vivo analysis reveals that ATP-hydrolysis couples remodeling to SWI/SNF release from chromatin

AU - Tilly, Ben C.

AU - Chalkley, Gillian E.

AU - van der Knaap, Jan A.

AU - Moshkin, Yuri M.

AU - Kan, Tsung Wai

AU - Dekkers, Dick H.W.

AU - Demmers, Jeroen A.A.

AU - Peter Verrijzer, C.

N1 - 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.

PY - 2021/7/27

Y1 - 2021/7/27

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=85111868517&partnerID=8YFLogxK

U2 - 10.7554/eLife.69424

DO - 10.7554/eLife.69424

M3 - Article

C2 - 34313222

AN - SCOPUS:85111868517

SN - 2050-084X

VL - 10

JO - eLife

JF - eLife

M1 - e69424

ER -

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

Abstract

Bibliographical note

Access to Document

Other files and links

Fingerprint

Cite this