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Single-molecule imaging of chromatin remodelers reveals role of ATPase in promoting fast kinetics of target search and dissociation from chromatin

Conserved ATP-dependent chromatin remodelers establish and maintain genome-wide chromatin architectures of regulatory DNA during cellular lifespan, but the temporal interactions between remodelers and chromatin targets have been obscure. We performed live-cell single-molecule tracking for RSC, SWI/S...

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Autores principales: Kim, Jee Min, Visanpattanasin, Pat, Jou, Vivian, Liu, Sheng, Tang, Xiaona, Zheng, Qinsi, Li, Kai Yu, Snedeker, Jonathan, Lavis, Luke D, Lionnet, Timothee, Wu, Carl
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8352589/
https://www.ncbi.nlm.nih.gov/pubmed/34313223
http://dx.doi.org/10.7554/eLife.69387
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author Kim, Jee Min
Visanpattanasin, Pat
Jou, Vivian
Liu, Sheng
Tang, Xiaona
Zheng, Qinsi
Li, Kai Yu
Snedeker, Jonathan
Lavis, Luke D
Lionnet, Timothee
Wu, Carl
author_facet Kim, Jee Min
Visanpattanasin, Pat
Jou, Vivian
Liu, Sheng
Tang, Xiaona
Zheng, Qinsi
Li, Kai Yu
Snedeker, Jonathan
Lavis, Luke D
Lionnet, Timothee
Wu, Carl
author_sort Kim, Jee Min
collection PubMed
description Conserved ATP-dependent chromatin remodelers establish and maintain genome-wide chromatin architectures of regulatory DNA during cellular lifespan, but the temporal interactions between remodelers and chromatin targets have been obscure. We performed live-cell single-molecule tracking for RSC, SWI/SNF, CHD1, ISW1, ISW2, and INO80 remodeling complexes in budding yeast and detected hyperkinetic behaviors for chromatin-bound molecules that frequently transition to the free state for all complexes. Chromatin-bound remodelers display notably higher diffusion than nucleosomal histones, and strikingly fast dissociation kinetics with 4–7 s mean residence times. These enhanced dynamics require ATP binding or hydrolysis by the catalytic ATPase, uncovering an additional function to its established role in nucleosome remodeling. Kinetic simulations show that multiple remodelers can repeatedly occupy the same promoter region on a timescale of minutes, implicating an unending ‘tug-of-war’ that controls a temporally shifting window of accessibility for the transcription initiation machinery.
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spelling pubmed-83525892021-08-11 Single-molecule imaging of chromatin remodelers reveals role of ATPase in promoting fast kinetics of target search and dissociation from chromatin Kim, Jee Min Visanpattanasin, Pat Jou, Vivian Liu, Sheng Tang, Xiaona Zheng, Qinsi Li, Kai Yu Snedeker, Jonathan Lavis, Luke D Lionnet, Timothee Wu, Carl eLife Chromosomes and Gene Expression Conserved ATP-dependent chromatin remodelers establish and maintain genome-wide chromatin architectures of regulatory DNA during cellular lifespan, but the temporal interactions between remodelers and chromatin targets have been obscure. We performed live-cell single-molecule tracking for RSC, SWI/SNF, CHD1, ISW1, ISW2, and INO80 remodeling complexes in budding yeast and detected hyperkinetic behaviors for chromatin-bound molecules that frequently transition to the free state for all complexes. Chromatin-bound remodelers display notably higher diffusion than nucleosomal histones, and strikingly fast dissociation kinetics with 4–7 s mean residence times. These enhanced dynamics require ATP binding or hydrolysis by the catalytic ATPase, uncovering an additional function to its established role in nucleosome remodeling. Kinetic simulations show that multiple remodelers can repeatedly occupy the same promoter region on a timescale of minutes, implicating an unending ‘tug-of-war’ that controls a temporally shifting window of accessibility for the transcription initiation machinery. eLife Sciences Publications, Ltd 2021-07-27 /pmc/articles/PMC8352589/ /pubmed/34313223 http://dx.doi.org/10.7554/eLife.69387 Text en © 2021, Kim et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Chromosomes and Gene Expression
Kim, Jee Min
Visanpattanasin, Pat
Jou, Vivian
Liu, Sheng
Tang, Xiaona
Zheng, Qinsi
Li, Kai Yu
Snedeker, Jonathan
Lavis, Luke D
Lionnet, Timothee
Wu, Carl
Single-molecule imaging of chromatin remodelers reveals role of ATPase in promoting fast kinetics of target search and dissociation from chromatin
title Single-molecule imaging of chromatin remodelers reveals role of ATPase in promoting fast kinetics of target search and dissociation from chromatin
title_full Single-molecule imaging of chromatin remodelers reveals role of ATPase in promoting fast kinetics of target search and dissociation from chromatin
title_fullStr Single-molecule imaging of chromatin remodelers reveals role of ATPase in promoting fast kinetics of target search and dissociation from chromatin
title_full_unstemmed Single-molecule imaging of chromatin remodelers reveals role of ATPase in promoting fast kinetics of target search and dissociation from chromatin
title_short Single-molecule imaging of chromatin remodelers reveals role of ATPase in promoting fast kinetics of target search and dissociation from chromatin
title_sort single-molecule imaging of chromatin remodelers reveals role of atpase in promoting fast kinetics of target search and dissociation from chromatin
topic Chromosomes and Gene Expression
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8352589/
https://www.ncbi.nlm.nih.gov/pubmed/34313223
http://dx.doi.org/10.7554/eLife.69387
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