The docking domain of histone H2A is required for H1 binding and RSC-mediated nucleosome remodeling

Manu Shubhdarshan Shukla, Sajad Hussain Syed, Damien Goutte-Gattat, John Lalith Charles Richard, Fabien Montel, Ali Hamiche, Andrew Travers, Cendrine Faivre-Moskalenko, Jan Bednar, Jeffrey J. Hayes, Dimitar Angelov, Stefan Dimitrov

Research output: Contribution to journalArticle

29 Citations (Scopus)

Abstract

Histone variants within the H2A family show high divergences in their C-terminal regions. In this work, we have studied how these divergences and in particular, how a part of the H2A COOH-terminus, the docking domain, is implicated in both structural and functional properties of the nucleosome. Using biochemical methods in combination with Atomic Force Microscopy and Electron Cryo-Microscopy, we show that the H2A-docking domain is a key structural feature within the nucleosome. Deletion of this domain or replacement with the incomplete docking domain from the variant H2A.Bbd results in significant structural alterations in the nucleosome, including an increase in overall accessibility to nucleases, un-wrapping of ∼10bp of DNA from each end of the nucleosome and associated changes in the entry/exit angle of DNA ends. These structural alterations are associated with a reduced ability of the chromatin remodeler RSC to both remodel and mobilize the nucleosomes. Linker histone H1 binding is also abrogated in nucleosomes containing the incomplete docking domain of H2A.Bbd. Our data illustrate the unique role of the H2A-docking domain in coordinating the structural-functional aspects of the nucleosome properties. Moreover, our data suggest that incorporation of a 'defective' docking domain may be a primary structural role of H2A.Bbd in chromatin.

Original languageEnglish
Pages (from-to)2559-2570
Number of pages12
JournalNucleic Acids Research
Volume39
Issue number7
DOIs
Publication statusPublished - Apr 2011
Externally publishedYes

Fingerprint

Nucleosomes
Histones
Chromatin
Cryoelectron Microscopy
Atomic Force Microscopy
DNA

ASJC Scopus subject areas

  • Genetics

Cite this

The docking domain of histone H2A is required for H1 binding and RSC-mediated nucleosome remodeling. / Shukla, Manu Shubhdarshan; Syed, Sajad Hussain; Goutte-Gattat, Damien; Richard, John Lalith Charles; Montel, Fabien; Hamiche, Ali; Travers, Andrew; Faivre-Moskalenko, Cendrine; Bednar, Jan; Hayes, Jeffrey J.; Angelov, Dimitar; Dimitrov, Stefan.

In: Nucleic Acids Research, Vol. 39, No. 7, 04.2011, p. 2559-2570.

Research output: Contribution to journalArticle

Shukla, MS, Syed, SH, Goutte-Gattat, D, Richard, JLC, Montel, F, Hamiche, A, Travers, A, Faivre-Moskalenko, C, Bednar, J, Hayes, JJ, Angelov, D & Dimitrov, S 2011, 'The docking domain of histone H2A is required for H1 binding and RSC-mediated nucleosome remodeling', Nucleic Acids Research, vol. 39, no. 7, pp. 2559-2570. https://doi.org/10.1093/nar/gkq1174
Shukla, Manu Shubhdarshan ; Syed, Sajad Hussain ; Goutte-Gattat, Damien ; Richard, John Lalith Charles ; Montel, Fabien ; Hamiche, Ali ; Travers, Andrew ; Faivre-Moskalenko, Cendrine ; Bednar, Jan ; Hayes, Jeffrey J. ; Angelov, Dimitar ; Dimitrov, Stefan. / The docking domain of histone H2A is required for H1 binding and RSC-mediated nucleosome remodeling. In: Nucleic Acids Research. 2011 ; Vol. 39, No. 7. pp. 2559-2570.
@article{e64f3d2bd2b44588b1b9ade768231dab,
title = "The docking domain of histone H2A is required for H1 binding and RSC-mediated nucleosome remodeling",
abstract = "Histone variants within the H2A family show high divergences in their C-terminal regions. In this work, we have studied how these divergences and in particular, how a part of the H2A COOH-terminus, the docking domain, is implicated in both structural and functional properties of the nucleosome. Using biochemical methods in combination with Atomic Force Microscopy and Electron Cryo-Microscopy, we show that the H2A-docking domain is a key structural feature within the nucleosome. Deletion of this domain or replacement with the incomplete docking domain from the variant H2A.Bbd results in significant structural alterations in the nucleosome, including an increase in overall accessibility to nucleases, un-wrapping of ∼10bp of DNA from each end of the nucleosome and associated changes in the entry/exit angle of DNA ends. These structural alterations are associated with a reduced ability of the chromatin remodeler RSC to both remodel and mobilize the nucleosomes. Linker histone H1 binding is also abrogated in nucleosomes containing the incomplete docking domain of H2A.Bbd. Our data illustrate the unique role of the H2A-docking domain in coordinating the structural-functional aspects of the nucleosome properties. Moreover, our data suggest that incorporation of a 'defective' docking domain may be a primary structural role of H2A.Bbd in chromatin.",
author = "Shukla, {Manu Shubhdarshan} and Syed, {Sajad Hussain} and Damien Goutte-Gattat and Richard, {John Lalith Charles} and Fabien Montel and Ali Hamiche and Andrew Travers and Cendrine Faivre-Moskalenko and Jan Bednar and Hayes, {Jeffrey J.} and Dimitar Angelov and Stefan Dimitrov",
year = "2011",
month = "4",
doi = "10.1093/nar/gkq1174",
language = "English",
volume = "39",
pages = "2559--2570",
journal = "Nucleic Acids Research",
issn = "0305-1048",
publisher = "Oxford University Press",
number = "7",

}

TY - JOUR

T1 - The docking domain of histone H2A is required for H1 binding and RSC-mediated nucleosome remodeling

AU - Shukla, Manu Shubhdarshan

AU - Syed, Sajad Hussain

AU - Goutte-Gattat, Damien

AU - Richard, John Lalith Charles

AU - Montel, Fabien

AU - Hamiche, Ali

AU - Travers, Andrew

AU - Faivre-Moskalenko, Cendrine

AU - Bednar, Jan

AU - Hayes, Jeffrey J.

AU - Angelov, Dimitar

AU - Dimitrov, Stefan

PY - 2011/4

Y1 - 2011/4

N2 - Histone variants within the H2A family show high divergences in their C-terminal regions. In this work, we have studied how these divergences and in particular, how a part of the H2A COOH-terminus, the docking domain, is implicated in both structural and functional properties of the nucleosome. Using biochemical methods in combination with Atomic Force Microscopy and Electron Cryo-Microscopy, we show that the H2A-docking domain is a key structural feature within the nucleosome. Deletion of this domain or replacement with the incomplete docking domain from the variant H2A.Bbd results in significant structural alterations in the nucleosome, including an increase in overall accessibility to nucleases, un-wrapping of ∼10bp of DNA from each end of the nucleosome and associated changes in the entry/exit angle of DNA ends. These structural alterations are associated with a reduced ability of the chromatin remodeler RSC to both remodel and mobilize the nucleosomes. Linker histone H1 binding is also abrogated in nucleosomes containing the incomplete docking domain of H2A.Bbd. Our data illustrate the unique role of the H2A-docking domain in coordinating the structural-functional aspects of the nucleosome properties. Moreover, our data suggest that incorporation of a 'defective' docking domain may be a primary structural role of H2A.Bbd in chromatin.

AB - Histone variants within the H2A family show high divergences in their C-terminal regions. In this work, we have studied how these divergences and in particular, how a part of the H2A COOH-terminus, the docking domain, is implicated in both structural and functional properties of the nucleosome. Using biochemical methods in combination with Atomic Force Microscopy and Electron Cryo-Microscopy, we show that the H2A-docking domain is a key structural feature within the nucleosome. Deletion of this domain or replacement with the incomplete docking domain from the variant H2A.Bbd results in significant structural alterations in the nucleosome, including an increase in overall accessibility to nucleases, un-wrapping of ∼10bp of DNA from each end of the nucleosome and associated changes in the entry/exit angle of DNA ends. These structural alterations are associated with a reduced ability of the chromatin remodeler RSC to both remodel and mobilize the nucleosomes. Linker histone H1 binding is also abrogated in nucleosomes containing the incomplete docking domain of H2A.Bbd. Our data illustrate the unique role of the H2A-docking domain in coordinating the structural-functional aspects of the nucleosome properties. Moreover, our data suggest that incorporation of a 'defective' docking domain may be a primary structural role of H2A.Bbd in chromatin.

UR - http://www.scopus.com/inward/record.url?scp=79954582772&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=79954582772&partnerID=8YFLogxK

U2 - 10.1093/nar/gkq1174

DO - 10.1093/nar/gkq1174

M3 - Article

VL - 39

SP - 2559

EP - 2570

JO - Nucleic Acids Research

JF - Nucleic Acids Research

SN - 0305-1048

IS - 7

ER -