In vivo analysis reveals that ATP-hydrolysis couples remodeling to SWI/SNF release from chromatin
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 Br...
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2021-07-01
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| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/69424 |
| _version_ | 1811236823647649792 |
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| author | Ben C Tilly Gillian E Chalkley Jan A van der Knaap Yuri M Moshkin Tsung Wai Kan Dick HW Dekkers Jeroen AA Demmers C Peter Verrijzer |
| author_facet | Ben C Tilly Gillian E Chalkley Jan A van der Knaap Yuri M Moshkin Tsung Wai Kan Dick HW Dekkers Jeroen AA Demmers C Peter Verrijzer |
| author_sort | Ben C Tilly |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-12T12:14:46Z |
| format | Article |
| id | doaj.art-9127d0482a2844bc94f9f9006ff6118e |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T12:14:46Z |
| publishDate | 2021-07-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-9127d0482a2844bc94f9f9006ff6118e2022-12-22T03:33:27ZengeLife Sciences Publications LtdeLife2050-084X2021-07-011010.7554/eLife.69424In vivo analysis reveals that ATP-hydrolysis couples remodeling to SWI/SNF release from chromatinBen C Tilly0Gillian E Chalkley1Jan A van der Knaap2Yuri M Moshkin3Tsung Wai Kan4Dick HW Dekkers5Jeroen AA Demmers6C Peter Verrijzer7https://orcid.org/0000-0002-6476-3264Department of Biochemistry, Rotterdam, NetherlandsDepartment of Biochemistry, Rotterdam, NetherlandsDepartment of Biochemistry, Rotterdam, NetherlandsDepartment of Biochemistry, Rotterdam, NetherlandsDepartment of Biochemistry, Rotterdam, NetherlandsDepartment of Biochemistry, Rotterdam, Netherlands; Proteomics Center, Erasmus University Medical Center, Rotterdam, NetherlandsDepartment of Biochemistry, Rotterdam, Netherlands; Proteomics Center, Erasmus University Medical Center, Rotterdam, NetherlandsDepartment of Biochemistry, Rotterdam, NetherlandsATP-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.https://elifesciences.org/articles/69424ATP-dependent chromatin remodelingSWI/SNFbrahmalive-cell imagingpolytene chromosomesRNA polymerase II |
| spellingShingle | Ben C Tilly Gillian E Chalkley Jan A van der Knaap Yuri M Moshkin Tsung Wai Kan Dick HW Dekkers Jeroen AA Demmers C Peter Verrijzer In vivo analysis reveals that ATP-hydrolysis couples remodeling to SWI/SNF release from chromatin eLife ATP-dependent chromatin remodeling SWI/SNF brahma live-cell imaging polytene chromosomes RNA polymerase II |
| title | In vivo analysis reveals that ATP-hydrolysis couples remodeling to SWI/SNF release from chromatin |
| title_full | In vivo analysis reveals that ATP-hydrolysis couples remodeling to SWI/SNF release from chromatin |
| title_fullStr | In vivo analysis reveals that ATP-hydrolysis couples remodeling to SWI/SNF release from chromatin |
| title_full_unstemmed | In vivo analysis reveals that ATP-hydrolysis couples remodeling to SWI/SNF release from chromatin |
| title_short | In vivo analysis reveals that ATP-hydrolysis couples remodeling to SWI/SNF release from chromatin |
| title_sort | in vivo analysis reveals that atp hydrolysis couples remodeling to swi snf release from chromatin |
| topic | ATP-dependent chromatin remodeling SWI/SNF brahma live-cell imaging polytene chromosomes RNA polymerase II |
| url | https://elifesciences.org/articles/69424 |
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