Tension-dependent free energies of nucleosome unwrapping

Lequieu, Joshua; Cordoba, Andres; Schwartz, David C.; de Pablo, Juan J.

doi:10.1021/acscentsci.6b00201

Title: Tension-dependent free energies of nucleosome unwrapping

Abstract

Here, nucleosomes form the basic unit of compaction within eukaryotic genomes, and their locations represent an important, yet poorly understood, mechanism of genetic regulation. Quantifying the strength of interactions within the nucleosome is a central problem in biophysics and is critical to understanding how nucleosome positions influence gene expression. By comparing to single-molecule experiments, we demonstrate that a coarse-grained molecular model of the nucleosome can reproduce key aspects of nucleosome unwrapping. Using detailed simulations of DNA and histone proteins, we calculate the tension-dependent free energy surface corresponding to the unwrapping process. The model reproduces quantitatively the forces required to unwrap the nucleosome and reveals the role played by electrostatic interactions during this process. We then demonstrate that histone modifications and DNA sequence can have significant effects on the energies of nucleosome formation. Most notably, we show that histone tails contribute asymmetrically to the stability of the outer and inner turn of nucleosomal DNA and that depending on which histone tails are modified, the tension-dependent response is modulated differently.

Authors:

Lequieu, Joshua ^[1]; Cordoba, Andres ^[1]; Schwartz, David C. ^[2]; de Pablo, Juan J. ^[3]

Univ. of Chicago, Chicago, IL (United States)
Univ. of Wisconsin-Madison, Madison, WI (United States)
Univ. of Chicago, Chicago, IL (United States); Argonne National Lab. (ANL), Argonne, IL (United States)

Publication Date:: Tue Aug 23 00:00:00 EDT 2016

Research Org.:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Materials Sciences and Engineering Division; US Department of Commerce; National Institute of Standards and Technology (NIST); National Institutes of Health (NIH) - National Human Genome Research Institute (NHGRI)

OSTI Identifier:: 1332925

Grant/Contract Number:: AC02-06CH11357

Resource Type:: Accepted Manuscript

Journal Name:: ACS Central Science

Additional Journal Information:: Journal Volume: 2; Journal Issue: 9; 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; 59 BASIC BIOLOGICAL SCIENCES

Citation Formats


                    Lequieu, Joshua, Cordoba, Andres, Schwartz, David C., and de Pablo, Juan J. Tension-dependent free energies of nucleosome unwrapping.  United States: N. p., 2016. 
Web.  doi:10.1021/acscentsci.6b00201.

Copy to clipboard


                    Lequieu, Joshua, Cordoba, Andres, Schwartz, David C., & de Pablo, Juan J. Tension-dependent free energies of nucleosome unwrapping.  United States.  https://doi.org/10.1021/acscentsci.6b00201

Copy to clipboard


                    Lequieu, Joshua, Cordoba, Andres, Schwartz, David C., and de Pablo, Juan J. Tue .  
"Tension-dependent free energies of nucleosome unwrapping".  United States.  https://doi.org/10.1021/acscentsci.6b00201.  https://www.osti.gov/servlets/purl/1332925.

Copy to clipboard


                    
@article{osti_1332925,

  title        = {Tension-dependent free energies of nucleosome unwrapping},

  author       = {Lequieu, Joshua and Cordoba, Andres and Schwartz, David C. and de Pablo, Juan J.},

  abstractNote = {Here, nucleosomes form the basic unit of compaction within eukaryotic genomes, and their locations represent an important, yet poorly understood, mechanism of genetic regulation. Quantifying the strength of interactions within the nucleosome is a central problem in biophysics and is critical to understanding how nucleosome positions influence gene expression. By comparing to single-molecule experiments, we demonstrate that a coarse-grained molecular model of the nucleosome can reproduce key aspects of nucleosome unwrapping. Using detailed simulations of DNA and histone proteins, we calculate the tension-dependent free energy surface corresponding to the unwrapping process. The model reproduces quantitatively the forces required to unwrap the nucleosome and reveals the role played by electrostatic interactions during this process. We then demonstrate that histone modifications and DNA sequence can have significant effects on the energies of nucleosome formation. Most notably, we show that histone tails contribute asymmetrically to the stability of the outer and inner turn of nucleosomal DNA and that depending on which histone tails are modified, the tension-dependent response is modulated differently.},

  doi          = {10.1021/acscentsci.6b00201},

  journal      = {ACS Central Science},

  number       = 9,

  volume       = 2,

  place        = {United States},

  year         = {Tue Aug 23 00:00:00 EDT 2016},

  month        = {Tue Aug 23 00:00:00 EDT 2016}

}

Copy to clipboard

Journal Article:

Free Publicly Available Full Text

Accepted Manuscript (DOE)

Publisher's Version of Record

https://doi.org/10.1021/acscentsci.6b00201

Other availability

Search WorldCat to find libraries that may hold this journal

Citation Metrics:

Cited by: 46 works

Citation information provided by
Web of Science

Save / Share:

Export Metadata

Save to My Library

Works referenced in this record:

Crystal structure of the nucleosome core particle at 2.8 Å resolution
journal, September 1997

Luger, Karolin; Mäder, Armin W.; Richmond, Robin K.
Nature, Vol. 389, Issue 6648
DOI: 10.1038/38444

Solvent Mediated Interactions in the Structure of the Nucleosome Core Particle at 1.9Å Resolution
journal, June 2002

Davey, Curt A.; Sargent, David F.; Luger, Karolin
Journal of Molecular Biology, Vol. 319, Issue 5
DOI: 10.1016/S0022-2836(02)00386-8

Human diseases with underlying defects in chromatin structure and modification
journal, October 2001

Hendrich, B.
Human Molecular Genetics, Vol. 10, Issue 20
DOI: 10.1093/hmg/10.20.2233

Covalent modifications of histones during development and disease pathogenesis
journal, November 2007

Bhaumik, Sukesh R.; Smith, Edwin; Shilatifard, Ali
Nature Structural & Molecular Biology, Vol. 14, Issue 11
DOI: 10.1038/nsmb1337

Histones associated with downregulated genes are hypo-acetylated in Huntington's disease models
journal, April 2007

Sadri-Vakili, Ghazaleh; Bouzou, Bérengère; Benn, Caroline L.
Human Molecular Genetics, Vol. 16, Issue 11
DOI: 10.1093/hmg/ddm078

Mechanical disruption of individual nucleosomes reveals a reversible multistage release of DNA
journal, February 2002

Brower-Toland, B. D.; Smith, C. L.; Yeh, R. C.
Proceedings of the National Academy of Sciences, Vol. 99, Issue 4
DOI: 10.1073/pnas.022638399

Pulling a single chromatin fiber reveals the forces that maintain its higher-order structure
journal, January 2000

Cui, Y.; Bustamante, C.
Proceedings of the National Academy of Sciences, Vol. 97, Issue 1
DOI: 10.1073/pnas.97.1.127

Forced Unraveling of Nucleosomes Assembled on Heterogeneous DNA Using Core Histones, NAP-1, and ACF
journal, August 2005

Gemmen, Gregory J.; Sim, Ronald; Haushalter, Karl A.
Journal of Molecular Biology, Vol. 351, Issue 1
DOI: 10.1016/j.jmb.2005.05.058

Specific Contributions of Histone Tails and their Acetylation to the Mechanical Stability of Nucleosomes
journal, February 2005

Brower-Toland, Brent; Wacker, David A.; Fulbright, Robert M.
Journal of Molecular Biology, Vol. 346, Issue 1
DOI: 10.1016/j.jmb.2004.11.056

Effect of force on mononucleosomal dynamics
journal, October 2006

Mihardja, S.; Spakowitz, A. J.; Zhang, Y.
Proceedings of the National Academy of Sciences, Vol. 103, Issue 43
DOI: 10.1073/pnas.0607526103

Hidden Markov Analysis of Nucleosome Unwrapping Under Force
journal, May 2009

Kruithof, M.; van Noort, J.
Biophysical Journal, Vol. 96, Issue 9
DOI: 10.1016/j.bpj.2009.01.048

High-resolution dynamic mapping of histone-DNA interactions in a nucleosome
journal, January 2009

Hall, Michael A.; Shundrovsky, Alla; Bai, Lu
Nature Structural & Molecular Biology, Vol. 16, Issue 2
DOI: 10.1038/nsmb.1526

Torque modulates nucleosome stability and facilitates H2A/H2B dimer loss
journal, October 2013

Sheinin, Maxim Y.; Li, Ming; Soltani, Mohammad
Nature Communications, Vol. 4, Issue 1
DOI: 10.1038/ncomms3579

Kinetics and Thermodynamics of Phenotype: Unwinding and Rewinding the Nucleosome
journal, November 2012

Mack, Andrew H.; Schlingman, Daniel J.; Ilagan, Robielyn P.
Journal of Molecular Biology, Vol. 423, Issue 5
DOI: 10.1016/j.jmb.2012.08.021

Asymmetric Unwrapping of Nucleosomes under Tension Directed by DNA Local Flexibility
journal, March 2015

Ngo, Thuy T. M.; Zhang, Qiucen; Zhou, Ruobo
Cell, Vol. 160, Issue 6
DOI: 10.1016/j.cell.2015.02.001

Tension-dependent structural deformation alters single-molecule transition kinetics
journal, January 2011

Sudhanshu, B.; Mihardja, S.; Koslover, E. F.
Proceedings of the National Academy of Sciences, Vol. 108, Issue 5
DOI: 10.1073/pnas.1010047108

Nucleosome Dynamics between Tension-Induced States
journal, May 2012

Mollazadeh-Beidokhti, Laleh; Mohammad-Rafiee, Farshid; Schiessel, Helmut
Biophysical Journal, Vol. 102, Issue 10
DOI: 10.1016/j.bpj.2012.04.012

Brownian Dynamics Simulation of DNA Unrolling from the Nucleosome
journal, December 2008

Wocjan, T.; Klenin, K.; Langowski, J.
The Journal of Physical Chemistry B, Vol. 113, Issue 9
DOI: 10.1021/jp806137e

Translating the Histone Code
journal, August 2001

Jenuwein, T.
Science, Vol. 293, Issue 5532
DOI: 10.1126/science.1063127

Mapping Global Histone Acetylation Patterns to Gene Expression
journal, June 2004

Kurdistani, Siavash K.; Tavazoie, Saeed; Grunstein, Michael
Cell, Vol. 117, Issue 6
DOI: 10.1016/j.cell.2004.05.023

High-Resolution Profiling of Histone Methylations in the Human Genome
journal, May 2007

Barski, Artem; Cuddapah, Suresh; Cui, Kairong
Cell, Vol. 129, Issue 4
DOI: 10.1016/j.cell.2007.05.009

Charting histone modifications and the functional organization of mammalian genomes
journal, November 2010

Zhou, Vicky W.; Goren, Alon; Bernstein, Bradley E.
Nature Reviews Genetics, Vol. 12, Issue 1
DOI: 10.1038/nrg2905

Coarse-grained modeling of DNA curvature
journal, October 2014

Freeman, Gordon S.; Hinckley, Daniel M.; Lequieu, Joshua P.
The Journal of Chemical Physics, Vol. 141, Issue 16
DOI: 10.1063/1.4897649

DNA Shape Dominates Sequence Affinity in Nucleosome Formation
journal, October 2014

Freeman, Gordon S.; Lequieu, Joshua P.; Hinckley, Daniel M.
Physical Review Letters, Vol. 113, Issue 16
DOI: 10.1103/PhysRevLett.113.168101

Frustration, specific sequence dependence, and nonlinearity in large-amplitude fluctuations of allosteric proteins
journal, February 2011

Li, Wenfei; Wolynes, Peter G.; Takada, Shoji
Proceedings of the National Academy of Sciences, Vol. 108, Issue 9
DOI: 10.1073/pnas.1018983108

VMD: Visual molecular dynamics
journal, February 1996

Humphrey, William; Dalke, Andrew; Schulten, Klaus
Journal of Molecular Graphics, Vol. 14, Issue 1
DOI: 10.1016/0263-7855(96)00018-5

Partial Unwrapping and Histone Tail Dynamics in Nucleosome Revealed by Coarse-Grained Molecular Simulations
journal, August 2015

Kenzaki, Hiroo; Takada, Shoji
PLOS Computational Biology, Vol. 11, Issue 8
DOI: 10.1371/journal.pcbi.1004443

New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning
journal, February 1998

Lowary, P. T.; Widom, J.
Journal of Molecular Biology, Vol. 276, Issue 1
DOI: 10.1006/jmbi.1997.1494

Structural Constraints in Collaborative Competition of Transcription Factors against the Nucleosome
journal, September 2011

Moyle-Heyrman, Georgette; Tims, Hannah S.; Widom, Jonathan
Journal of Molecular Biology, Vol. 412, Issue 4
DOI: 10.1016/j.jmb.2011.07.032

Measurement of histone–DNA interaction free energy in nucleosomes
journal, May 2004

Thåström, A.; Lowary, P. T.; Widom, J.
Methods, Vol. 33, Issue 1
DOI: 10.1016/j.ymeth.2003.10.018

A genomic code for nucleosome positioning
journal, July 2006

Segal, Eran; Fondufe-Mittendorf, Yvonne; Chen, Lingyi
Nature, Vol. 442, Issue 7104
DOI: 10.1038/nature04979

A coarse grain model for DNA
journal, February 2007

Knotts, Thomas A.; Rathore, Nitin; Schwartz, David C.
The Journal of Chemical Physics, Vol. 126, Issue 8
DOI: 10.1063/1.2431804

A Mesoscale Model of DNA and Its Renaturation
journal, March 2009

Sambriski, E. J.; Schwartz, D. C.; de Pablo, J. J.
Biophysical Journal, Vol. 96, Issue 5
DOI: 10.1016/j.bpj.2008.09.061

An experimentally-informed coarse-grained 3-site-per-nucleotide model of DNA: Structure, thermodynamics, and dynamics of hybridization
journal, October 2013

Hinckley, Daniel M.; Freeman, Gordon S.; Whitmer, Jonathan K.
The Journal of Chemical Physics, Vol. 139, Issue 14
DOI: 10.1063/1.4822042

Single-base resolution mapping of H1-nucleosome interactions and 3D organization of the nucleosome
journal, May 2010

Syed, S. H.; Goutte-Gattat, D.; Becker, N.
Proceedings of the National Academy of Sciences, Vol. 107, Issue 21
DOI: 10.1073/pnas.1000309107

From crystal and NMR structures, footprints and cryo-electron-micrographs to large and soft structures: nanoscale modeling of the nucleosomal stem
journal, August 2011

Meyer, Sam; Becker, Nils B.; Syed, Sajad Hussain
Nucleic Acids Research, Vol. 39, Issue 21
DOI: 10.1093/nar/gkr573

Multidimensional free-energy calculations using the weighted histogram analysis method
journal, November 1995

Kumar, Shankar; Rosenberg, John M.; Bouzida, Djamal
Journal of Computational Chemistry, Vol. 16, Issue 11
DOI: 10.1002/jcc.540161104

Umbrella sampling: Umbrella sampling
journal, May 2011

Kästner, Johannes
Wiley Interdisciplinary Reviews: Computational Molecular Science, Vol. 1, Issue 6
DOI: 10.1002/wcms.66

Nucleosome Dynamics between Tension-Induced States
journal, May 2012

Mollazadeh-Beidokhti, Laleh; Mohammad-Rafiee, Farshid; Schiessel, Helmut
Biophysical Journal, Vol. 102, Issue 10
DOI: 10.1016/j.bpj.2012.04.012

High-Resolution Profiling of Histone Methylations in the Human Genome
journal, May 2007

Barski, Artem; Cuddapah, Suresh; Cui, Kairong
Cell, Vol. 129, Issue 4
DOI: 10.1016/j.cell.2007.05.009

Specific Contributions of Histone Tails and their Acetylation to the Mechanical Stability of Nucleosomes
journal, February 2005

Brower-Toland, Brent; Wacker, David A.; Fulbright, Robert M.
Journal of Molecular Biology, Vol. 346, Issue 1
DOI: 10.1016/j.jmb.2004.11.056

Forced Unraveling of Nucleosomes Assembled on Heterogeneous DNA Using Core Histones, NAP-1, and ACF
journal, August 2005

Gemmen, Gregory J.; Sim, Ronald; Haushalter, Karl A.
Journal of Molecular Biology, Vol. 351, Issue 1
DOI: 10.1016/j.jmb.2005.05.058

Kinetics and Thermodynamics of Phenotype: Unwinding and Rewinding the Nucleosome
journal, November 2012

Mack, Andrew H.; Schlingman, Daniel J.; Ilagan, Robielyn P.
Journal of Molecular Biology, Vol. 423, Issue 5
DOI: 10.1016/j.jmb.2012.08.021

Measurement of histone–DNA interaction free energy in nucleosomes
journal, May 2004

Thåström, A.; Lowary, P. T.; Widom, J.
Methods, Vol. 33, Issue 1
DOI: 10.1016/j.ymeth.2003.10.018

Brownian Dynamics Simulation of DNA Unrolling from the Nucleosome
journal, December 2008

Wocjan, T.; Klenin, K.; Langowski, J.
The Journal of Physical Chemistry B, Vol. 113, Issue 9
DOI: 10.1021/jp806137e

Crystal structure of the nucleosome core particle at 2.8 Å resolution
journal, September 1997

Luger, Karolin; Mäder, Armin W.; Richmond, Robin K.
Nature, Vol. 389, Issue 6648
DOI: 10.1038/38444

Torque modulates nucleosome stability and facilitates H2A/H2B dimer loss
journal, October 2013

Sheinin, Maxim Y.; Li, Ming; Soltani, Mohammad
Nature Communications, Vol. 4, Issue 1
DOI: 10.1038/ncomms3579

Charting histone modifications and the functional organization of mammalian genomes
journal, November 2010

Zhou, Vicky W.; Goren, Alon; Bernstein, Bradley E.
Nature Reviews Genetics, Vol. 12, Issue 1
DOI: 10.1038/nrg2905

High-resolution dynamic mapping of histone-DNA interactions in a nucleosome
journal, January 2009

Hall, Michael A.; Shundrovsky, Alla; Bai, Lu
Nature Structural & Molecular Biology, Vol. 16, Issue 2
DOI: 10.1038/nsmb.1526

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

Wang, Lina; Li, Siru; Wang, Kai
Nature Communications, Vol. 13, Issue 1
DOI: 10.1038/s41467-022-34858-6

Stepwise gating of the Sec61 protein-conducting channel by Sec63 and Sec62
journal, January 2021

Itskanov, Samuel; Kuo, Katie M.; Gumbart, James C.
Nature Structural & Molecular Biology, Vol. 28, Issue 2
DOI: 10.1038/s41594-020-00541-x

A coarse grain model for DNA
journal, February 2007

Knotts, Thomas A.; Rathore, Nitin; Schwartz, David C.
The Journal of Chemical Physics, Vol. 126, Issue 8
DOI: 10.1063/1.2431804

An experimentally-informed coarse-grained 3-site-per-nucleotide model of DNA: Structure, thermodynamics, and dynamics of hybridization
journal, October 2013

Hinckley, Daniel M.; Freeman, Gordon S.; Whitmer, Jonathan K.
The Journal of Chemical Physics, Vol. 139, Issue 14
DOI: 10.1063/1.4822042

Coarse-grained modeling of DNA curvature
journal, October 2014

Freeman, Gordon S.; Hinckley, Daniel M.; Lequieu, Joshua P.
The Journal of Chemical Physics, Vol. 141, Issue 16
DOI: 10.1063/1.4897649

Mechanical disruption of individual nucleosomes reveals a reversible multistage release of DNA
journal, February 2002

Brower-Toland, B. D.; Smith, C. L.; Yeh, R. C.
Proceedings of the National Academy of Sciences, Vol. 99, Issue 4
DOI: 10.1073/pnas.022638399

Effect of force on mononucleosomal dynamics
journal, October 2006

Mihardja, S.; Spakowitz, A. J.; Zhang, Y.
Proceedings of the National Academy of Sciences, Vol. 103, Issue 43
DOI: 10.1073/pnas.0607526103

Frustration, specific sequence dependence, and nonlinearity in large-amplitude fluctuations of allosteric proteins
journal, February 2011

Li, Wenfei; Wolynes, Peter G.; Takada, Shoji
Proceedings of the National Academy of Sciences, Vol. 108, Issue 9
DOI: 10.1073/pnas.1018983108

Human diseases with underlying defects in chromatin structure and modification
journal, October 2001

Hendrich, B.
Human Molecular Genetics, Vol. 10, Issue 20
DOI: 10.1093/hmg/10.20.2233

Histones associated with downregulated genes are hypo-acetylated in Huntington's disease models
journal, April 2007

Sadri-Vakili, Ghazaleh; Bouzou, Bérengère; Benn, Caroline L.
Human Molecular Genetics, Vol. 16, Issue 11
DOI: 10.1093/hmg/ddm078

From crystal and NMR structures, footprints and cryo-electron-micrographs to large and soft structures: nanoscale modeling of the nucleosomal stem
journal, August 2011

Meyer, Sam; Becker, Nils B.; Syed, Sajad Hussain
Nucleic Acids Research, Vol. 39, Issue 21
DOI: 10.1093/nar/gkr573

DNA Spools under Tension
journal, June 2004

Kulić, I. M.; Schiessel, H.
Physical Review Letters, Vol. 92, Issue 22
DOI: 10.1103/physrevlett.92.228101

Translating the Histone Code
journal, August 2001

Jenuwein, T.
Science, Vol. 293, Issue 5532
DOI: 10.1126/science.1063127

Partial Unwrapping and Histone Tail Dynamics in Nucleosome Revealed by Coarse-Grained Molecular Simulations
journal, August 2015

Kenzaki, Hiroo; Takada, Shoji
PLOS Computational Biology, Vol. 11, Issue 8
DOI: 10.1371/journal.pcbi.1004443

Works referencing / citing this record:

1CPN: A coarse-grained multi-scale model of chromatin
journal, June 2019

Lequieu, Joshua; Córdoba, Andrés; Moller, Joshua
The Journal of Chemical Physics, Vol. 150, Issue 21
DOI: 10.1063/1.5092976

Critical role of histone tail entropy in nucleosome unwinding
journal, May 2019

Parsons, Thomas; Zhang, Bin
The Journal of Chemical Physics, Vol. 150, Issue 18
DOI: 10.1063/1.5085663

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

Polymer physics across scales: Modeling the multiscale behavior of functional soft materials and biological systems
journal, December 2019

Spakowitz, Andrew J.
The Journal of Chemical Physics, Vol. 151, Issue 23
DOI: 10.1063/1.5126852

DNA sliding in nucleosomes via twist defect propagation revealed by molecular simulations
journal, February 2018

Brandani, Giovanni B.; Niina, Toru; Tan, Cheng
Nucleic Acids Research, Vol. 46, Issue 6
DOI: 10.1093/nar/gky158

Dynamic and Structural Modeling of the Specificity in Protein-DNA Interactions Guided by Binding Assay and Structure Data
posted_content, March 2018

Tan, Cheng; Takada, Shoji
bioRxiv
DOI: 10.1101/288795

Designing nucleosomal force sensors
journal, May 2017

Tompitak, M.; de Bruin, L.; Eslami-Mossallam, B.
Physical Review E, Vol. 95, Issue 5
DOI: 10.1103/physreve.95.052402

Free energy profiles for unwrapping the outer superhelical turn of nucleosomal DNA
journal, March 2018

Kono, Hidetoshi; Sakuraba, Shun; Ishida, Hisashi
PLOS Computational Biology, Vol. 14, Issue 3
DOI: 10.1371/journal.pcbi.1006024

Dynamic and Structural Modeling of the Specificity in Protein–DNA Interactions Guided by Binding Assay and Structure Data
journal, May 2018

Tan, Cheng; Takada, Shoji
Journal of Chemical Theory and Computation, Vol. 14, Issue 7
DOI: 10.1021/acs.jctc.8b00299

Dynamics of Chromatin Fibers: Comparison of Monte Carlo Simulations with Force Spectroscopy
journal, November 2018

Norouzi, Davood; Zhurkin, Victor B.
Biophysical Journal, Vol. 115, Issue 9
DOI: 10.1016/j.bpj.2018.06.032

Mechanism of Dynamic Binding of Replication Protein A to ssDNA
journal, September 2020

Mondal, Anupam; Bhattacherjee, Arnab
Journal of Chemical Information and Modeling, Vol. 60, Issue 10
DOI: 10.1021/acs.jcim.0c00564

Eliminating Fitting from the Modeling of Biological Processes
journal, September 2016

Spakowitz, Andrew J.
ACS Central Science, Vol. 2, Issue 9
DOI: 10.1021/acscentsci.6b00263

The Free Energy Landscape of Internucleosome Interactions and Its Relation to Chromatin Fiber Structure
journal, January 2019

Moller, Joshua; Lequieu, Joshua; de Pablo, Juan J.
ACS Central Science, Vol. 5, Issue 2
DOI: 10.1021/acscentsci.8b00836

DNA sliding in nucleosomes via twist defect propagation revealed by molecular simulations
journal, February 2018

Brandani, Giovanni B.; Niina, Toru; Tan, Cheng
Nucleic Acids Research, Vol. 46, Issue 6
DOI: 10.1093/nar/gky158

Free energy profiles for unwrapping the outer superhelical turn of nucleosomal DNA
journal, March 2018

Kono, Hidetoshi; Sakuraba, Shun; Ishida, Hisashi
PLOS Computational Biology, Vol. 14, Issue 3
DOI: 10.1371/journal.pcbi.1006024

Similar Records in DOE PAGES and OSTI.GOV collections:

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

Journal Article Chen, Yujie ; Tokuda, Joshua M. ; Topping, Traci ; ... - Proceedings of the National Academy of Sciences of the United States of America

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. Wemore »« less
Cited by 59
https://doi.org/10.1073/pnas.1611118114

Full Text Available
Real-Time Multistep Asymmetrical Disassembly of Nucleosomes and Chromatosomes Visualized by High-Speed Atomic Force Microscopy

Journal Article Onoa, Bibiana ; Díaz-Celis, César ; Cañari-Chumpitaz, Cristhian ; ... - ACS Central Science

During replication, expression, and repair of the eukaryotic genome, cellular machinery must access the DNA wrapped around histone proteins forming nucleosomes. These octameric protein·DNA complexes are modular, dynamic, and flexible and unwrap or disassemble either spontaneously or by the action of molecular motors. Thus, the mechanism of formation and regulation of subnucleosomal intermediates has gained attention genome-wide because it controls DNA accessibility. Here, we imaged nucleosomes and their more compacted structure with the linker histone H1 (chromatosomes) using high-speed atomic force microscopy to visualize simultaneously the changes in the DNA and the histone core during their disassembly when deposited onmore »« less
https://doi.org/10.1021/acscentsci.3c00735
DNA Shape Dominates Sequence Affinity in Nucleosome Formation

Journal Article Freeman, Gordon S. ; Lequieu, Joshua P. ; Hinckley, Daniel M. ; ... - Physical Review Letters

Nucleosomes provide the basic unit of compaction in eukaryotic genomes, and the mechanisms that dictate their position at specific locations along a DNA sequence are of central importance to genetics. In this Letter, we employ molecular models of DNA and proteins to elucidate various aspects of nucleosome positioning. In particular, we show how DNA’s histone affinity is encoded in its sequence-dependent shape, including subtle deviations from the ideal straight B-DNA form and local variations of minor groove width. By relying on high-precision simulations of the free energy of nucleosome complexes, we also demonstrate that, depending on DNA’s intrinsic curvature, histonemore »« less
https://doi.org/10.1103/PhysRevLett.113.168101
Assignment of structural transitions during mechanical unwrapping of nucleosomes and their disassembly products

Journal Article Díaz-Celis, César ; Cañari-Chumpitaz, Cristhian ; Sosa, Robert P. ; ... - Proceedings of the National Academy of Sciences of the United States of America

Nucleosome DNA unwrapping and its disassembly into hexasomes and tetrasomes is necessary for genomic access and plays an important role in transcription regulation. Previous single-molecule mechanical nucleosome unwrapping revealed a low- and a high-force transitions, and force-FRET pulling experiments showed that DNA unwrapping is asymmetric, occurring always first from one side before the other. However, the assignment of DNA segments involved in these transitions remains controversial. Here, using high-resolution optical tweezers with simultaneous single-molecule FRET detection, we show that the low-force transition corresponds to the undoing of the outer wrap of one side of the nucleosome (∼27 bp), a processmore »« less
https://doi.org/10.1073/pnas.2206513119
In silico evidence for sequence-dependent nucleosome sliding

Journal Article Lequieu, Joshua ; Schwartz, David C. ; de Pablo, Juan J. - Proceedings of the National Academy of Sciences of the United States of America

Nucleosomes represent the basic building block of chromatin and provide an important mechanism by which cellular processes are controlled. The locations of nucleosomes across the genome are not random but instead depend on both the underlying DNA sequence and the dynamic action of other proteins within the nucleus. Furthermore, these processes are central to cellular function, and the molecular details of the interplay between DNA sequence and nudeosome dynamics remain poorly understood. In this work, we investigate this interplay in detail by relying on a molecular model, which permits development of a comprehensive picture of the underlying free energy surfacesmore »« less
Cited by 46
https://doi.org/10.1073/pnas.1705685114

Similar Records

Title: Tension-dependent free energies of nucleosome unwrapping

Abstract

Citation Formats

Crystal structure of the nucleosome core particle at 2.8 Å resolution journal, September 1997

Solvent Mediated Interactions in the Structure of the Nucleosome Core Particle at 1.9Å Resolution journal, June 2002

Human diseases with underlying defects in chromatin structure and modification journal, October 2001

Covalent modifications of histones during development and disease pathogenesis journal, November 2007

Histones associated with downregulated genes are hypo-acetylated in Huntington's disease models journal, April 2007

Mechanical disruption of individual nucleosomes reveals a reversible multistage release of DNA journal, February 2002

Pulling a single chromatin fiber reveals the forces that maintain its higher-order structure journal, January 2000

Forced Unraveling of Nucleosomes Assembled on Heterogeneous DNA Using Core Histones, NAP-1, and ACF journal, August 2005

Specific Contributions of Histone Tails and their Acetylation to the Mechanical Stability of Nucleosomes journal, February 2005

Effect of force on mononucleosomal dynamics journal, October 2006

Hidden Markov Analysis of Nucleosome Unwrapping Under Force journal, May 2009

High-resolution dynamic mapping of histone-DNA interactions in a nucleosome journal, January 2009

Torque modulates nucleosome stability and facilitates H2A/H2B dimer loss journal, October 2013

Kinetics and Thermodynamics of Phenotype: Unwinding and Rewinding the Nucleosome journal, November 2012

Asymmetric Unwrapping of Nucleosomes under Tension Directed by DNA Local Flexibility journal, March 2015

Tension-dependent structural deformation alters single-molecule transition kinetics journal, January 2011

Nucleosome Dynamics between Tension-Induced States journal, May 2012

Brownian Dynamics Simulation of DNA Unrolling from the Nucleosome journal, December 2008

Translating the Histone Code journal, August 2001

Mapping Global Histone Acetylation Patterns to Gene Expression journal, June 2004

High-Resolution Profiling of Histone Methylations in the Human Genome journal, May 2007

Charting histone modifications and the functional organization of mammalian genomes journal, November 2010

Coarse-grained modeling of DNA curvature journal, October 2014

DNA Shape Dominates Sequence Affinity in Nucleosome Formation journal, October 2014

Frustration, specific sequence dependence, and nonlinearity in large-amplitude fluctuations of allosteric proteins journal, February 2011

VMD: Visual molecular dynamics journal, February 1996

Partial Unwrapping and Histone Tail Dynamics in Nucleosome Revealed by Coarse-Grained Molecular Simulations journal, August 2015

New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning journal, February 1998

Structural Constraints in Collaborative Competition of Transcription Factors against the Nucleosome journal, September 2011

Measurement of histone–DNA interaction free energy in nucleosomes journal, May 2004

A genomic code for nucleosome positioning journal, July 2006

A coarse grain model for DNA journal, February 2007

A Mesoscale Model of DNA and Its Renaturation journal, March 2009

An experimentally-informed coarse-grained 3-site-per-nucleotide model of DNA: Structure, thermodynamics, and dynamics of hybridization journal, October 2013

Single-base resolution mapping of H1-nucleosome interactions and 3D organization of the nucleosome journal, May 2010

From crystal and NMR structures, footprints and cryo-electron-micrographs to large and soft structures: nanoscale modeling of the nucleosomal stem journal, August 2011

Multidimensional free-energy calculations using the weighted histogram analysis method journal, November 1995

Umbrella sampling: Umbrella sampling journal, May 2011

Nucleosome Dynamics between Tension-Induced States journal, May 2012

High-Resolution Profiling of Histone Methylations in the Human Genome journal, May 2007

Specific Contributions of Histone Tails and their Acetylation to the Mechanical Stability of Nucleosomes journal, February 2005

Forced Unraveling of Nucleosomes Assembled on Heterogeneous DNA Using Core Histones, NAP-1, and ACF journal, August 2005

Kinetics and Thermodynamics of Phenotype: Unwinding and Rewinding the Nucleosome journal, November 2012

Measurement of histone–DNA interaction free energy in nucleosomes journal, May 2004

Brownian Dynamics Simulation of DNA Unrolling from the Nucleosome journal, December 2008

Crystal structure of the nucleosome core particle at 2.8 Å resolution journal, September 1997

Torque modulates nucleosome stability and facilitates H2A/H2B dimer loss journal, October 2013

Charting histone modifications and the functional organization of mammalian genomes journal, November 2010

High-resolution dynamic mapping of histone-DNA interactions in a nucleosome journal, January 2009

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

Stepwise gating of the Sec61 protein-conducting channel by Sec63 and Sec62 journal, January 2021

A coarse grain model for DNA journal, February 2007

An experimentally-informed coarse-grained 3-site-per-nucleotide model of DNA: Structure, thermodynamics, and dynamics of hybridization journal, October 2013

Coarse-grained modeling of DNA curvature journal, October 2014

Mechanical disruption of individual nucleosomes reveals a reversible multistage release of DNA journal, February 2002

Effect of force on mononucleosomal dynamics journal, October 2006

Frustration, specific sequence dependence, and nonlinearity in large-amplitude fluctuations of allosteric proteins journal, February 2011

Human diseases with underlying defects in chromatin structure and modification journal, October 2001

Histones associated with downregulated genes are hypo-acetylated in Huntington's disease models journal, April 2007

From crystal and NMR structures, footprints and cryo-electron-micrographs to large and soft structures: nanoscale modeling of the nucleosomal stem journal, August 2011

DNA Spools under Tension journal, June 2004

Translating the Histone Code journal, August 2001

Partial Unwrapping and Histone Tail Dynamics in Nucleosome Revealed by Coarse-Grained Molecular Simulations journal, August 2015

1CPN: A coarse-grained multi-scale model of chromatin journal, June 2019

Critical role of histone tail entropy in nucleosome unwinding journal, May 2019

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

Polymer physics across scales: Modeling the multiscale behavior of functional soft materials and biological systems journal, December 2019

DNA sliding in nucleosomes via twist defect propagation revealed by molecular simulations journal, February 2018

Dynamic and Structural Modeling of the Specificity in Protein-DNA Interactions Guided by Binding Assay and Structure Data posted_content, March 2018

Designing nucleosomal force sensors journal, May 2017

Free energy profiles for unwrapping the outer superhelical turn of nucleosomal DNA journal, March 2018

Dynamic and Structural Modeling of the Specificity in Protein–DNA Interactions Guided by Binding Assay and Structure Data journal, May 2018

Dynamics of Chromatin Fibers: Comparison of Monte Carlo Simulations with Force Spectroscopy journal, November 2018

Mechanism of Dynamic Binding of Replication Protein A to ssDNA journal, September 2020

Eliminating Fitting from the Modeling of Biological Processes journal, September 2016

The Free Energy Landscape of Internucleosome Interactions and Its Relation to Chromatin Fiber Structure journal, January 2019

DNA sliding in nucleosomes via twist defect propagation revealed by molecular simulations journal, February 2018

Crystal structure of the nucleosome core particle at 2.8 Å resolution
journal, September 1997

Solvent Mediated Interactions in the Structure of the Nucleosome Core Particle at 1.9Å Resolution
journal, June 2002

Human diseases with underlying defects in chromatin structure and modification
journal, October 2001

Covalent modifications of histones during development and disease pathogenesis
journal, November 2007

Histones associated with downregulated genes are hypo-acetylated in Huntington's disease models
journal, April 2007

Mechanical disruption of individual nucleosomes reveals a reversible multistage release of DNA
journal, February 2002

Pulling a single chromatin fiber reveals the forces that maintain its higher-order structure
journal, January 2000

Forced Unraveling of Nucleosomes Assembled on Heterogeneous DNA Using Core Histones, NAP-1, and ACF
journal, August 2005

Specific Contributions of Histone Tails and their Acetylation to the Mechanical Stability of Nucleosomes
journal, February 2005

Effect of force on mononucleosomal dynamics
journal, October 2006

Hidden Markov Analysis of Nucleosome Unwrapping Under Force
journal, May 2009

High-resolution dynamic mapping of histone-DNA interactions in a nucleosome
journal, January 2009

Torque modulates nucleosome stability and facilitates H2A/H2B dimer loss
journal, October 2013

Kinetics and Thermodynamics of Phenotype: Unwinding and Rewinding the Nucleosome
journal, November 2012

Asymmetric Unwrapping of Nucleosomes under Tension Directed by DNA Local Flexibility
journal, March 2015

Tension-dependent structural deformation alters single-molecule transition kinetics
journal, January 2011

Nucleosome Dynamics between Tension-Induced States
journal, May 2012

Brownian Dynamics Simulation of DNA Unrolling from the Nucleosome
journal, December 2008

Translating the Histone Code
journal, August 2001

Mapping Global Histone Acetylation Patterns to Gene Expression
journal, June 2004

High-Resolution Profiling of Histone Methylations in the Human Genome
journal, May 2007

Charting histone modifications and the functional organization of mammalian genomes
journal, November 2010

Coarse-grained modeling of DNA curvature
journal, October 2014

DNA Shape Dominates Sequence Affinity in Nucleosome Formation
journal, October 2014

Frustration, specific sequence dependence, and nonlinearity in large-amplitude fluctuations of allosteric proteins
journal, February 2011

VMD: Visual molecular dynamics
journal, February 1996

Partial Unwrapping and Histone Tail Dynamics in Nucleosome Revealed by Coarse-Grained Molecular Simulations
journal, August 2015

New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning
journal, February 1998

Structural Constraints in Collaborative Competition of Transcription Factors against the Nucleosome
journal, September 2011

Measurement of histone–DNA interaction free energy in nucleosomes
journal, May 2004

A genomic code for nucleosome positioning
journal, July 2006

A coarse grain model for DNA
journal, February 2007

A Mesoscale Model of DNA and Its Renaturation
journal, March 2009

An experimentally-informed coarse-grained 3-site-per-nucleotide model of DNA: Structure, thermodynamics, and dynamics of hybridization
journal, October 2013

Single-base resolution mapping of H1-nucleosome interactions and 3D organization of the nucleosome
journal, May 2010

From crystal and NMR structures, footprints and cryo-electron-micrographs to large and soft structures: nanoscale modeling of the nucleosomal stem
journal, August 2011

Multidimensional free-energy calculations using the weighted histogram analysis method
journal, November 1995

Umbrella sampling: Umbrella sampling
journal, May 2011

Nucleosome Dynamics between Tension-Induced States
journal, May 2012

High-Resolution Profiling of Histone Methylations in the Human Genome
journal, May 2007

Specific Contributions of Histone Tails and their Acetylation to the Mechanical Stability of Nucleosomes
journal, February 2005

Forced Unraveling of Nucleosomes Assembled on Heterogeneous DNA Using Core Histones, NAP-1, and ACF
journal, August 2005

Kinetics and Thermodynamics of Phenotype: Unwinding and Rewinding the Nucleosome
journal, November 2012

Measurement of histone–DNA interaction free energy in nucleosomes
journal, May 2004

Brownian Dynamics Simulation of DNA Unrolling from the Nucleosome
journal, December 2008

Crystal structure of the nucleosome core particle at 2.8 Å resolution
journal, September 1997

Torque modulates nucleosome stability and facilitates H2A/H2B dimer loss
journal, October 2013

Charting histone modifications and the functional organization of mammalian genomes
journal, November 2010

High-resolution dynamic mapping of histone-DNA interactions in a nucleosome
journal, January 2009

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

Stepwise gating of the Sec61 protein-conducting channel by Sec63 and Sec62
journal, January 2021

A coarse grain model for DNA
journal, February 2007

An experimentally-informed coarse-grained 3-site-per-nucleotide model of DNA: Structure, thermodynamics, and dynamics of hybridization
journal, October 2013

Coarse-grained modeling of DNA curvature
journal, October 2014

Mechanical disruption of individual nucleosomes reveals a reversible multistage release of DNA
journal, February 2002

Effect of force on mononucleosomal dynamics
journal, October 2006

Frustration, specific sequence dependence, and nonlinearity in large-amplitude fluctuations of allosteric proteins
journal, February 2011

Human diseases with underlying defects in chromatin structure and modification
journal, October 2001

Histones associated with downregulated genes are hypo-acetylated in Huntington's disease models
journal, April 2007

From crystal and NMR structures, footprints and cryo-electron-micrographs to large and soft structures: nanoscale modeling of the nucleosomal stem
journal, August 2011

DNA Spools under Tension
journal, June 2004

Translating the Histone Code
journal, August 2001

Partial Unwrapping and Histone Tail Dynamics in Nucleosome Revealed by Coarse-Grained Molecular Simulations
journal, August 2015

1CPN: A coarse-grained multi-scale model of chromatin
journal, June 2019

Critical role of histone tail entropy in nucleosome unwinding
journal, May 2019

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

Polymer physics across scales: Modeling the multiscale behavior of functional soft materials and biological systems
journal, December 2019

DNA sliding in nucleosomes via twist defect propagation revealed by molecular simulations
journal, February 2018

Dynamic and Structural Modeling of the Specificity in Protein-DNA Interactions Guided by Binding Assay and Structure Data
posted_content, March 2018

Designing nucleosomal force sensors
journal, May 2017

Free energy profiles for unwrapping the outer superhelical turn of nucleosomal DNA
journal, March 2018

Dynamic and Structural Modeling of the Specificity in Protein–DNA Interactions Guided by Binding Assay and Structure Data
journal, May 2018

Dynamics of Chromatin Fibers: Comparison of Monte Carlo Simulations with Force Spectroscopy
journal, November 2018

Mechanism of Dynamic Binding of Replication Protein A to ssDNA
journal, September 2020

Eliminating Fitting from the Modeling of Biological Processes
journal, September 2016

The Free Energy Landscape of Internucleosome Interactions and Its Relation to Chromatin Fiber Structure
journal, January 2019

DNA sliding in nucleosomes via twist defect propagation revealed by molecular simulations
journal, February 2018

Free energy profiles for unwrapping the outer superhelical turn of nucleosomal DNA
journal, March 2018