Cargando…
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...
Autores principales: | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
---|---|
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 |
_version_ | 1785051172363567104 |
---|---|
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. |
format | Online Article Text |
id | pubmed-10229121 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | eLife Sciences Publications, Ltd |
record_format | MEDLINE/PubMed |
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 |
work_keys_str_mv | AT jainkanishk anacetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT marundematthewr anacetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT burgjonathanm anacetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT gloorsusanl anacetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT josephfaithm anacetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT ponchakarlf anacetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT gillespiezacharyb anacetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT rodriguezkelil anacetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT popovairinak anacetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT hallnathanw anacetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT vaidyaanup anacetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT howardsaraha anacetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT taylorhaileyf anacetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT mukhsinovalaylo anacetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT onuohaugochic anacetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT pattesonemilyf anacetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT cookespencerw anacetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT taylorbethanyc anacetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT weinzapfelellenn anacetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT cheekmarcusa anacetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT meinersmatthewj anacetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT foxgeoffreyc anacetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT namitzkevinew anacetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT cowlesmartisw anacetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT krajewskikrzysztof anacetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT sunzuwen anacetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT cosgrovemichaels anacetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT youngnicolasl anacetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT keoghmichaelchristopher anacetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT strahlbriand anacetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT jainkanishk acetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT marundematthewr acetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT burgjonathanm acetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT gloorsusanl acetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT josephfaithm acetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT ponchakarlf acetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT gillespiezacharyb acetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT rodriguezkelil acetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT popovairinak acetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT hallnathanw acetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT vaidyaanup acetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT howardsaraha acetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT taylorhaileyf acetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT mukhsinovalaylo acetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT onuohaugochic acetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT pattesonemilyf acetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT cookespencerw acetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT taylorbethanyc acetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT weinzapfelellenn acetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT cheekmarcusa acetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT meinersmatthewj acetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT foxgeoffreyc acetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT namitzkevinew acetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT cowlesmartisw acetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT krajewskikrzysztof acetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT sunzuwen acetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT cosgrovemichaels acetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT youngnicolasl acetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT keoghmichaelchristopher acetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability AT strahlbriand acetylationmediatedchromatinswitchgovernsh3k4methylationreadwritecapability |