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An acetylation-mediated chromatin switch governs H3K4 methylation read-write capability

In nucleosomes, histone N-terminal tails exist in dynamic equilibrium between free/accessible and collapsed/DNA-bound states. The latter state is expected to impact histone N-termini availability to the epigenetic machinery. Notably, H3 tail acetylation (e.g. K9ac, K14ac, K18ac) is linked to increas...

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Autores principales: Jain, Kanishk, Marunde, Matthew R, Burg, Jonathan M, Gloor, Susan L, Joseph, Faith M, Poncha, Karl F, Gillespie, Zachary B, Rodriguez, Keli L, Popova, Irina K, Hall, Nathan W, Vaidya, Anup, Howard, Sarah A, Taylor, Hailey F, Mukhsinova, Laylo, Onuoha, Ugochi C, Patteson, Emily F, Cooke, Spencer W, Taylor, Bethany C, Weinzapfel, Ellen N, Cheek, Marcus A, Meiners, Matthew J, Fox, Geoffrey C, Namitz, Kevin EW, Cowles, Martis W, Krajewski, Krzysztof, Sun, Zu-Wen, Cosgrove, Michael S, Young, Nicolas L, Keogh, Michael-Christopher, Strahl, Brian D
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10229121/
https://www.ncbi.nlm.nih.gov/pubmed/37204295
http://dx.doi.org/10.7554/eLife.82596
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author Jain, Kanishk
Marunde, Matthew R
Burg, Jonathan M
Gloor, Susan L
Joseph, Faith M
Poncha, Karl F
Gillespie, Zachary B
Rodriguez, Keli L
Popova, Irina K
Hall, Nathan W
Vaidya, Anup
Howard, Sarah A
Taylor, Hailey F
Mukhsinova, Laylo
Onuoha, Ugochi C
Patteson, Emily F
Cooke, Spencer W
Taylor, Bethany C
Weinzapfel, Ellen N
Cheek, Marcus A
Meiners, Matthew J
Fox, Geoffrey C
Namitz, Kevin EW
Cowles, Martis W
Krajewski, Krzysztof
Sun, Zu-Wen
Cosgrove, Michael S
Young, Nicolas L
Keogh, Michael-Christopher
Strahl, Brian D
author_facet Jain, Kanishk
Marunde, Matthew R
Burg, Jonathan M
Gloor, Susan L
Joseph, Faith M
Poncha, Karl F
Gillespie, Zachary B
Rodriguez, Keli L
Popova, Irina K
Hall, Nathan W
Vaidya, Anup
Howard, Sarah A
Taylor, Hailey F
Mukhsinova, Laylo
Onuoha, Ugochi C
Patteson, Emily F
Cooke, Spencer W
Taylor, Bethany C
Weinzapfel, Ellen N
Cheek, Marcus A
Meiners, Matthew J
Fox, Geoffrey C
Namitz, Kevin EW
Cowles, Martis W
Krajewski, Krzysztof
Sun, Zu-Wen
Cosgrove, Michael S
Young, Nicolas L
Keogh, Michael-Christopher
Strahl, Brian D
author_sort Jain, Kanishk
collection PubMed
description In nucleosomes, histone N-terminal tails exist in dynamic equilibrium between free/accessible and collapsed/DNA-bound states. The latter state is expected to impact histone N-termini availability to the epigenetic machinery. Notably, H3 tail acetylation (e.g. K9ac, K14ac, K18ac) is linked to increased H3K4me3 engagement by the BPTF PHD finger, but it is unknown if this mechanism has a broader extension. Here, we show that H3 tail acetylation promotes nucleosomal accessibility to other H3K4 methyl readers, and importantly, extends to H3K4 writers, notably methyltransferase MLL1. This regulation is not observed on peptide substrates yet occurs on the cis H3 tail, as determined with fully-defined heterotypic nucleosomes. In vivo, H3 tail acetylation is directly and dynamically coupled with cis H3K4 methylation levels. Together, these observations reveal an acetylation ‘chromatin switch’ on the H3 tail that modulates read-write accessibility in nucleosomes and resolves the long-standing question of why H3K4me3 levels are coupled with H3 acetylation.
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spelling pubmed-102291212023-05-31 An acetylation-mediated chromatin switch governs H3K4 methylation read-write capability Jain, Kanishk Marunde, Matthew R Burg, Jonathan M Gloor, Susan L Joseph, Faith M Poncha, Karl F Gillespie, Zachary B Rodriguez, Keli L Popova, Irina K Hall, Nathan W Vaidya, Anup Howard, Sarah A Taylor, Hailey F Mukhsinova, Laylo Onuoha, Ugochi C Patteson, Emily F Cooke, Spencer W Taylor, Bethany C Weinzapfel, Ellen N Cheek, Marcus A Meiners, Matthew J Fox, Geoffrey C Namitz, Kevin EW Cowles, Martis W Krajewski, Krzysztof Sun, Zu-Wen Cosgrove, Michael S Young, Nicolas L Keogh, Michael-Christopher Strahl, Brian D eLife Biochemistry and Chemical Biology In nucleosomes, histone N-terminal tails exist in dynamic equilibrium between free/accessible and collapsed/DNA-bound states. The latter state is expected to impact histone N-termini availability to the epigenetic machinery. Notably, H3 tail acetylation (e.g. K9ac, K14ac, K18ac) is linked to increased H3K4me3 engagement by the BPTF PHD finger, but it is unknown if this mechanism has a broader extension. Here, we show that H3 tail acetylation promotes nucleosomal accessibility to other H3K4 methyl readers, and importantly, extends to H3K4 writers, notably methyltransferase MLL1. This regulation is not observed on peptide substrates yet occurs on the cis H3 tail, as determined with fully-defined heterotypic nucleosomes. In vivo, H3 tail acetylation is directly and dynamically coupled with cis H3K4 methylation levels. Together, these observations reveal an acetylation ‘chromatin switch’ on the H3 tail that modulates read-write accessibility in nucleosomes and resolves the long-standing question of why H3K4me3 levels are coupled with H3 acetylation. eLife Sciences Publications, Ltd 2023-05-19 /pmc/articles/PMC10229121/ /pubmed/37204295 http://dx.doi.org/10.7554/eLife.82596 Text en © 2023, Jain 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 Biochemistry and Chemical Biology
Jain, Kanishk
Marunde, Matthew R
Burg, Jonathan M
Gloor, Susan L
Joseph, Faith M
Poncha, Karl F
Gillespie, Zachary B
Rodriguez, Keli L
Popova, Irina K
Hall, Nathan W
Vaidya, Anup
Howard, Sarah A
Taylor, Hailey F
Mukhsinova, Laylo
Onuoha, Ugochi C
Patteson, Emily F
Cooke, Spencer W
Taylor, Bethany C
Weinzapfel, Ellen N
Cheek, Marcus A
Meiners, Matthew J
Fox, Geoffrey C
Namitz, Kevin EW
Cowles, Martis W
Krajewski, Krzysztof
Sun, Zu-Wen
Cosgrove, Michael S
Young, Nicolas L
Keogh, Michael-Christopher
Strahl, Brian D
An acetylation-mediated chromatin switch governs H3K4 methylation read-write capability
title An acetylation-mediated chromatin switch governs H3K4 methylation read-write capability
title_full An acetylation-mediated chromatin switch governs H3K4 methylation read-write capability
title_fullStr An acetylation-mediated chromatin switch governs H3K4 methylation read-write capability
title_full_unstemmed An acetylation-mediated chromatin switch governs H3K4 methylation read-write capability
title_short An acetylation-mediated chromatin switch governs H3K4 methylation read-write capability
title_sort acetylation-mediated chromatin switch governs h3k4 methylation read-write capability
topic Biochemistry and Chemical Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10229121/
https://www.ncbi.nlm.nih.gov/pubmed/37204295
http://dx.doi.org/10.7554/eLife.82596
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