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Title: The Free Energy Landscape of Internucleosome Interactions and Its Relation to Chromatin Fiber Structure

Abstract

The supramolecular chromatin fiber is governed by molecular scale energetics and interactions. Such energetics originate from the fiber's building block, the nucleosome core particle (NCP). In recent years, the chromatin fiber has been examined through perturbative methods in attempts to extract the energetics of nucleosome association in the fiber. This body of work has led to different results from experiments and simulations concerning the nucleosome-nucleosome energetics. Here, we expand on previous experiments and use coarse-grained simulations to evaluate the energetics inherent to nucleosomes across a variety of parameters in configurational and environmental space. Through this effort, we are able to uncover molecular processes that are critical to understanding the 30 nm chromatin fiber structure. In particular, we describe the NCP-NCP interactions by relying on an anisotropic energetic landscape, rather than a single potential energy value. The attractions in that landscape arise predominantly from the highly anisotropic interactions provided by the NCP histone N-terminal domain (NTD) tails. Our results are found to be in good agreement with recent nucleosome interaction experiments that suggest a maximum interaction energy of 2.69kBT. Furthermore, we examine the influence of crucial epigenetic modifications, such as acetylation of the H4 tail, and how they modify the underlyingmore » landscape. Our results for acetylated NCP interactions are also in agreement with experiment. We additionally find an induced chirality in NCP-NCP interactions upon acetylation that reduces interactions which would correspond to a left-handed superhelical chromatin fiber.« less

Authors:
 [1];  [2]; ORCiD logo [3]
+ Show Author Affiliations
  1. Univ. of Chicago, Chicago, IL (United States)
  2. Univ. of Chicago, Chicago, IL (United States); Univ. of California, Santa Barbara, CA (United States)
  3. Univ. of Chicago, Chicago, IL (United States); Argonne National Lab. (ANL), Argonne, IL (United States)
Publication Date:
Research Org.:
Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Org.:
National Science Foundation (NSF); USDOE
OSTI Identifier:
1557994
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
ACS Central Science
Additional Journal Information:
Journal Volume: 5; Journal Issue: 2; Journal ID: ISSN 2374-7943
Publisher:
American Chemical Society (ACS)
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Citation Formats

Moller, Joshua, Lequieu, Joshua, and de Pablo, Juan J. The Free Energy Landscape of Internucleosome Interactions and Its Relation to Chromatin Fiber Structure. United States: N. p., 2019. Web. doi:10.1021/acscentsci.8b00836.
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Moller, Joshua, Lequieu, Joshua, & de Pablo, Juan J. The Free Energy Landscape of Internucleosome Interactions and Its Relation to Chromatin Fiber Structure. United States. https://doi.org/10.1021/acscentsci.8b00836
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Moller, Joshua, Lequieu, Joshua, and de Pablo, Juan J. Thu . "The Free Energy Landscape of Internucleosome Interactions and Its Relation to Chromatin Fiber Structure". United States. https://doi.org/10.1021/acscentsci.8b00836. https://www.osti.gov/servlets/purl/1557994.
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@article{osti_1557994,
title = {The Free Energy Landscape of Internucleosome Interactions and Its Relation to Chromatin Fiber Structure},
author = {Moller, Joshua and Lequieu, Joshua and de Pablo, Juan J.},
abstractNote = {The supramolecular chromatin fiber is governed by molecular scale energetics and interactions. Such energetics originate from the fiber's building block, the nucleosome core particle (NCP). In recent years, the chromatin fiber has been examined through perturbative methods in attempts to extract the energetics of nucleosome association in the fiber. This body of work has led to different results from experiments and simulations concerning the nucleosome-nucleosome energetics. Here, we expand on previous experiments and use coarse-grained simulations to evaluate the energetics inherent to nucleosomes across a variety of parameters in configurational and environmental space. Through this effort, we are able to uncover molecular processes that are critical to understanding the 30 nm chromatin fiber structure. In particular, we describe the NCP-NCP interactions by relying on an anisotropic energetic landscape, rather than a single potential energy value. The attractions in that landscape arise predominantly from the highly anisotropic interactions provided by the NCP histone N-terminal domain (NTD) tails. Our results are found to be in good agreement with recent nucleosome interaction experiments that suggest a maximum interaction energy of 2.69kBT. Furthermore, we examine the influence of crucial epigenetic modifications, such as acetylation of the H4 tail, and how they modify the underlying landscape. Our results for acetylated NCP interactions are also in agreement with experiment. We additionally find an induced chirality in NCP-NCP interactions upon acetylation that reduces interactions which would correspond to a left-handed superhelical chromatin fiber.},
doi = {10.1021/acscentsci.8b00836},
journal = {ACS Central Science},
number = 2,
volume = 5,
place = {United States},
year = {Thu Jan 24 00:00:00 EST 2019},
month = {Thu Jan 24 00:00:00 EST 2019}
}
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https://doi.org/10.1021/acscentsci.8b00836
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Histone H3 and H4 N-Terminal Tails in Nucleosome Arrays at Cellular Concentrations Probed by Magic Angle Spinning NMR Spectroscopy
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Chromatin Unfolding by Epigenetic Modifications Explained by Dramatic Impairment of Internucleosome Interactions: A Multiscale Computational Study
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journal, January 2003

Histone acetylation and deacetylation in yeast
journal, April 2003

  • Kurdistani, Siavash K.; Grunstein, Michael
  • Nature Reviews Molecular Cell Biology, Vol. 4, Issue 4
  • DOI: 10.1038/nrm1075

Single-molecule force spectroscopy reveals a highly compliant helical folding for the 30-nm chromatin fiber
journal, April 2009

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DNA mechanical flexibility controls DNA potential to activate cGAS-mediated immune surveillance
journal, November 2022

Intra- and inter-nucleosomal interactions of the histone H4 tail revealed with a human nucleosome core particle with genetically-incorporated H4 tetra-acetylation
journal, November 2015

  • Wakamori, Masatoshi; Fujii, Yoshifumi; Suka, Noriyuki
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Distinct Roles of Histone H3 and H2A Tails in Nucleosome Stability
journal, August 2016

  • Li, Zhenhai; Kono, Hidetoshi
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep31437

The Global Relationship between Chromatin Physical Topology, Fractal Structure, and Gene Expression
journal, January 2017

  • Almassalha, L. M.; Tiwari, A.; Ruhoff, P. T.
  • Scientific Reports, Vol. 7, Issue 1
  • DOI: 10.1038/srep41061

Salt causes ion disequilibrium-induced programmed cell death in yeast and plants
journal, March 2002

Superresolution intrinsic fluorescence imaging of chromatin utilizing native, unmodified nucleic acids for contrast
journal, August 2016

  • Dong, Biqin; Almassalha, Luay M.; Stypula-Cyrus, Yolanda
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 35
  • DOI: 10.1073/pnas.1602202113

In silico evidence for sequence-dependent nucleosome sliding
journal, October 2017

  • Lequieu, Joshua; Schwartz, David C.; de Pablo, Juan J.
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 44
  • DOI: 10.1073/pnas.1705685114

Acetylation and Methylation of Histones and Their Possible role in the Regulation of rna Synthesis
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A Distinct Switch in Interactions of the Histone H4 Tail Domain upon Salt-dependent Folding of Nucleosome Arrays
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The higher-order structure of chromatin: evidence for a helical ribbon arrangement
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The effects of histone H4 tail acetylations on cation-induced chromatin folding and self-association
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Uncovering the forces between nucleosomes using DNA origami
journal, November 2016

  • Funke, Jonas J.; Ketterer, Philip; Lieleg, Corinna
  • Science Advances, Vol. 2, Issue 11
  • DOI: 10.1126/sciadv.1600974

Translating the Histone Code
journal, August 2001

Nucleosome Arrays Reveal the Two-Start Organization of the Chromatin Fiber
journal, November 2004

Chromatin Structure: A Repeating Unit of Histones and DNA
journal, May 1974

Epigenetic balance of gene expression by Polycomb and COMPASS families
journal, June 2016

The H4 Tail Domain Participates in Intra- and Internucleosome Interactions with Protein and DNA during Folding and Oligomerization of Nucleosome Arrays
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Tension-dependent Free Energies of Nucleosome Unwrapping
text, January 2016

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