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Mechanical and structural properties of archaeal hypernucleosomes

Many archaea express histones, which organize the genome and play a key role in gene regulation. The structure and function of archaeal histone–DNA complexes remain however largely unclear. Recent studies show formation of hypernucleosomes consisting of DNA wrapped around an ‘endless’ histone-protei...

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Autores principales: Henneman, Bram, Brouwer, Thomas B, Erkelens, Amanda M, Kuijntjes, Gert-Jan, van Emmerik, Clara, van der Valk, Ramon A, Timmer, Monika, Kirolos, Nancy C S, van Ingen, Hugo, van Noort, John, Dame, Remus T
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8096283/
https://www.ncbi.nlm.nih.gov/pubmed/33341892
http://dx.doi.org/10.1093/nar/gkaa1196
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author Henneman, Bram
Brouwer, Thomas B
Erkelens, Amanda M
Kuijntjes, Gert-Jan
van Emmerik, Clara
van der Valk, Ramon A
Timmer, Monika
Kirolos, Nancy C S
van Ingen, Hugo
van Noort, John
Dame, Remus T
author_facet Henneman, Bram
Brouwer, Thomas B
Erkelens, Amanda M
Kuijntjes, Gert-Jan
van Emmerik, Clara
van der Valk, Ramon A
Timmer, Monika
Kirolos, Nancy C S
van Ingen, Hugo
van Noort, John
Dame, Remus T
author_sort Henneman, Bram
collection PubMed
description Many archaea express histones, which organize the genome and play a key role in gene regulation. The structure and function of archaeal histone–DNA complexes remain however largely unclear. Recent studies show formation of hypernucleosomes consisting of DNA wrapped around an ‘endless’ histone-protein core. However, if and how such a hypernucleosome structure assembles on a long DNA substrate and which interactions provide for its stability, remains unclear. Here, we describe micromanipulation studies of complexes of the histones HMfA and HMfB with DNA. Our experiments show hypernucleosome assembly which results from cooperative binding of histones to DNA, facilitated by weak stacking interactions between neighboring histone dimers. Furthermore, rotational force spectroscopy demonstrates that the HMfB–DNA complex has a left-handed chirality, but that torque can drive it in a right-handed conformation. The structure of the hypernucleosome thus depends on stacking interactions, torque, and force. In vivo, such modulation of the archaeal hypernucleosome structure may play an important role in transcription regulation in response to environmental changes.
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spelling pubmed-80962832021-05-10 Mechanical and structural properties of archaeal hypernucleosomes Henneman, Bram Brouwer, Thomas B Erkelens, Amanda M Kuijntjes, Gert-Jan van Emmerik, Clara van der Valk, Ramon A Timmer, Monika Kirolos, Nancy C S van Ingen, Hugo van Noort, John Dame, Remus T Nucleic Acids Res Gene regulation, Chromatin and Epigenetics Many archaea express histones, which organize the genome and play a key role in gene regulation. The structure and function of archaeal histone–DNA complexes remain however largely unclear. Recent studies show formation of hypernucleosomes consisting of DNA wrapped around an ‘endless’ histone-protein core. However, if and how such a hypernucleosome structure assembles on a long DNA substrate and which interactions provide for its stability, remains unclear. Here, we describe micromanipulation studies of complexes of the histones HMfA and HMfB with DNA. Our experiments show hypernucleosome assembly which results from cooperative binding of histones to DNA, facilitated by weak stacking interactions between neighboring histone dimers. Furthermore, rotational force spectroscopy demonstrates that the HMfB–DNA complex has a left-handed chirality, but that torque can drive it in a right-handed conformation. The structure of the hypernucleosome thus depends on stacking interactions, torque, and force. In vivo, such modulation of the archaeal hypernucleosome structure may play an important role in transcription regulation in response to environmental changes. Oxford University Press 2020-12-21 /pmc/articles/PMC8096283/ /pubmed/33341892 http://dx.doi.org/10.1093/nar/gkaa1196 Text en © The Author(s) 2020. Published by Oxford University Press on behalf of Nucleic Acids Research. https://creativecommons.org/licenses/by-nc/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (http://creativecommons.org/licenses/by-nc/4.0/ (https://creativecommons.org/licenses/by-nc/4.0/) ), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Gene regulation, Chromatin and Epigenetics
Henneman, Bram
Brouwer, Thomas B
Erkelens, Amanda M
Kuijntjes, Gert-Jan
van Emmerik, Clara
van der Valk, Ramon A
Timmer, Monika
Kirolos, Nancy C S
van Ingen, Hugo
van Noort, John
Dame, Remus T
Mechanical and structural properties of archaeal hypernucleosomes
title Mechanical and structural properties of archaeal hypernucleosomes
title_full Mechanical and structural properties of archaeal hypernucleosomes
title_fullStr Mechanical and structural properties of archaeal hypernucleosomes
title_full_unstemmed Mechanical and structural properties of archaeal hypernucleosomes
title_short Mechanical and structural properties of archaeal hypernucleosomes
title_sort mechanical and structural properties of archaeal hypernucleosomes
topic Gene regulation, Chromatin and Epigenetics
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8096283/
https://www.ncbi.nlm.nih.gov/pubmed/33341892
http://dx.doi.org/10.1093/nar/gkaa1196
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