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Title: Asymmetric unwrapping of nucleosomal DNA propagates asymmetric opening and dissociation of the histone core

Abstract

The nucleosome core particle (NCP) is the basic structural unit for genome packaging in eukaryotic cells and consists of DNA wound around a core of eight histone proteins. DNA access is modulated through dynamic processes of NCP disassembly. Partly disassembled structures, such as the hexasome (containing six histones) and the tetrasome (four histones), are important for transcription regulation in vivo. However, the pathways for their formation have been difficult to characterize. We combine time-resolved (TR) small-angle X-ray scattering and TR-FRET to correlate changes in the DNA conformations with composition of the histone core during salt-induced disassembly of canonical NCPs. We find that H2A–H2B histone dimers are released sequentially, with the first dimer being released after the DNA has formed an asymmetrically unwrapped, teardrop-shape DNA structure. This finding suggests that the octasome-to-hexasome transition is guided by the asymmetric unwrapping of the DNA. Furthermore, the link between DNA structure and histone composition suggests a potential mechanism for the action of proteins that alter nucleosome configurations such as histone chaperones and chromatin remodeling complexes.

Authors:
 [1];  [1];  [2];  [3];  [1];  [2];  [1]
+ Show Author Affiliations
  1. Cornell Univ., Ithaca, NY (United States)
  2. Washington State Univ., Pullman, WA (United States)
  3. Cornell Univ., Ithaca, NY (United States); Princeton Univ., NJ (United States)
Publication Date:
Research Org.:
Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities Division; National Institutes of Health (NIH); National Institute of General Medical Sciences (NIGMS)
OSTI Identifier:
1340704
Grant/Contract Number:  
AC02-06CH11357; EUREKA R01-GM088645; R01-GM085062; GM073787; P41 GM103622
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 114; Journal Issue: 2; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences
Country of Publication:
United States
Language:
ENGLISH
Subject:
59 BASIC BIOLOGICAL SCIENCES; contrast variation SAXS; FRET; nucleosomes; hexasome; time resolved

Citation Formats

Chen, Yujie, Tokuda, Joshua M., Topping, Traci, Meisburger, Steve P., Pabit, Suzette A., Gloss, Lisa M., and Pollack, Lois. Asymmetric unwrapping of nucleosomal DNA propagates asymmetric opening and dissociation of the histone core. United States: N. p., 2016. Web. doi:10.1073/pnas.1611118114.
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Chen, Yujie, Tokuda, Joshua M., Topping, Traci, Meisburger, Steve P., Pabit, Suzette A., Gloss, Lisa M., & Pollack, Lois. Asymmetric unwrapping of nucleosomal DNA propagates asymmetric opening and dissociation of the histone core. United States. https://doi.org/10.1073/pnas.1611118114
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Chen, Yujie, Tokuda, Joshua M., Topping, Traci, Meisburger, Steve P., Pabit, Suzette A., Gloss, Lisa M., and Pollack, Lois. Tue . "Asymmetric unwrapping of nucleosomal DNA propagates asymmetric opening and dissociation of the histone core". United States. https://doi.org/10.1073/pnas.1611118114. https://www.osti.gov/servlets/purl/1340704.
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@article{osti_1340704,
title = {Asymmetric unwrapping of nucleosomal DNA propagates asymmetric opening and dissociation of the histone core},
author = {Chen, Yujie and Tokuda, Joshua M. and Topping, Traci and Meisburger, Steve P. and Pabit, Suzette A. and Gloss, Lisa M. and Pollack, Lois},
abstractNote = {The nucleosome core particle (NCP) is the basic structural unit for genome packaging in eukaryotic cells and consists of DNA wound around a core of eight histone proteins. DNA access is modulated through dynamic processes of NCP disassembly. Partly disassembled structures, such as the hexasome (containing six histones) and the tetrasome (four histones), are important for transcription regulation in vivo. However, the pathways for their formation have been difficult to characterize. We combine time-resolved (TR) small-angle X-ray scattering and TR-FRET to correlate changes in the DNA conformations with composition of the histone core during salt-induced disassembly of canonical NCPs. We find that H2A–H2B histone dimers are released sequentially, with the first dimer being released after the DNA has formed an asymmetrically unwrapped, teardrop-shape DNA structure. This finding suggests that the octasome-to-hexasome transition is guided by the asymmetric unwrapping of the DNA. Furthermore, the link between DNA structure and histone composition suggests a potential mechanism for the action of proteins that alter nucleosome configurations such as histone chaperones and chromatin remodeling complexes.},
doi = {10.1073/pnas.1611118114},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 2,
volume = 114,
place = {United States},
year = {Tue Dec 27 00:00:00 EST 2016},
month = {Tue Dec 27 00:00:00 EST 2016}
}
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https://doi.org/10.1073/pnas.1611118114
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