In silico evidence for sequence-dependent nucleosome sliding

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

doi:10.1073/pnas.1705685114

Title: In silico evidence for sequence-dependent nucleosome sliding

Journal Article · Wed Oct 18 00:00:00 EDT 2017 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1705685114· OSTI ID:1400015

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

Institute for Molecular Engineering, University of Chicago, Chicago, IL 60637,
Laboratory for Molecular and Computational Genomics, Department of Chemistry, University of Wisconsin–Madison, Madison, WI 53706,, Laboratory of Genetics, University of Wisconsin–Madison, Madison, WI 53706,, UW-Biotechnology Center, University of Wisconsin–Madison, Madison, WI 53706,
Institute for Molecular Engineering, University of Chicago, Chicago, IL 60637,, Materials Science Division, Argonne National Laboratory, Argonne, IL 60439

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 surfaces and the corresponding dynamics of nudeosome repositioning. The mechanism of nudeosome repositioning is shown to be strongly linked to DNA sequence and directly related to the binding energy of a given DNA sequence to the histone core. It is also demonstrated that chromatin remodelers can override DNA-sequence preferences by exerting torque, and the histone H4 tail is then identified as a key component by which DNA-sequence, histone modifications, and chromatin remodelers could in fact be coupled.

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

Sponsoring Organization:: USDOE; US Department of Commerce; USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22). Materials Sciences & Engineering Division; Midwest Integrated Center for Computational Materials (MICCoM); National Institutes of Health (NIH), National Human Genome Research Institute (NHGRI); National Institute of Standards and Technology (NIST), Center for Hierarchical Materials Design (CHiMaD)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1400015

Alternate ID(s):: OSTI ID: 1419955

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Vol. 114 Journal Issue: 44; ISSN 0027-8424

Publisher:: Proceedings of the National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 46 works

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References (76)

Mobile nucleosomes--a general behavior. Meersseman, G.; Pennings, S.; Bradbury, E. M. The EMBO Journal, Vol. 11, Issue 8 https://doi.org/10.1002/j.1460-2075.1992.tb05365.x	journal	August 1992
Solvent Mediated Interactions in the Structure of the Nucleosome Core Particle at 1.9Å Resolution Davey, Curt A.; Sargent, David F.; Luger, Karolin Journal of Molecular Biology, Vol. 319, Issue 5 https://doi.org/10.1016/S0022-2836(02)00386-8	journal	June 2002
Revisiting the finite temperature string method for the calculation of reaction tubes and free energies Vanden-Eijnden, Eric; Venturoli, Maddalena The Journal of Chemical Physics, Vol. 130, Issue 19 https://doi.org/10.1063/1.3130083	journal	May 2009
Human diseases with underlying defects in chromatin structure and modification Hendrich, B. Human Molecular Genetics, Vol. 10, Issue 20 https://doi.org/10.1093/hmg/10.20.2233	journal	October 2001
Dynamics of Nucleosome Invasion by DNA Binding Proteins Tims, Hannah S.; Gurunathan, Kaushik; Levitus, Marcia Journal of Molecular Biology, Vol. 411, Issue 2 https://doi.org/10.1016/j.jmb.2011.05.044	journal	August 2011
A genomic code for nucleosome positioning Segal, Eran; Fondufe-Mittendorf, Yvonne; Chen, Lingyi Nature, Vol. 442, Issue 7104 https://doi.org/10.1038/nature04979	journal	July 2006
Effect of force on mononucleosomal dynamics Mihardja, S.; Spakowitz, A. J.; Zhang, Y. Proceedings of the National Academy of Sciences, Vol. 103, Issue 43 https://doi.org/10.1073/pnas.0607526103	journal	October 2006
Chromatin remodeling by ISW2 and SWI/SNF requires DNA translocation inside the nucleosome Zofall, Martin; Persinger, Jim; Kassabov, Stefan R. Nature Structural & Molecular Biology, Vol. 13, Issue 4 https://doi.org/10.1038/nsmb1071	journal	March 2006
Telomeric Nucleosomes Are Intrinsically Mobile Pisano, Sabrina; Marchioni, Enrico; Galati, Alessandra Journal of Molecular Biology, Vol. 369, Issue 5 https://doi.org/10.1016/j.jmb.2007.04.027	journal	June 2007
Using DNA mechanics to predict in vitro nucleosome positions and formation energies Morozov, Alexandre V.; Fortney, Karissa; Gaykalova, Daria A. Nucleic Acids Research, Vol. 37, Issue 14 https://doi.org/10.1093/nar/gkp475	journal	June 2009
Multidimensional free-energy calculations using the weighted histogram analysis method Kumar, Shankar; Rosenberg, John M.; Bouzida, Djamal Journal of Computational Chemistry, Vol. 16, Issue 11 https://doi.org/10.1002/jcc.540161104	journal	November 1995
Mapping nucleosome position at single base-pair resolution by using site-directed hydroxyl radicals. Flaus, A.; Luger, K.; Tan, S. Proceedings of the National Academy of Sciences, Vol. 93, Issue 4 https://doi.org/10.1073/pnas.93.4.1370	journal	February 1996
Intrinsic histone-DNA interactions are not the major determinant of nucleosome positions in vivo Zhang, Yong; Moqtaderi, Zarmik; Rattner, Barbara P. Nature Structural & Molecular Biology, Vol. 16, Issue 8 https://doi.org/10.1038/nsmb.1636	journal	July 2009
Rigid-body molecular dynamics of DNA inside a nucleosome Fathizadeh, Arman; Berdy Besya, Azim; Reza Ejtehadi, Mohammad The European Physical Journal E, Vol. 36, Issue 3 https://doi.org/10.1140/epje/i2013-13021-4	journal	March 2013
The main role of the sequence-dependent DNA elasticity in determining the free energy of nucleosome formation on telomeric DNAs Filesi, Ilaria; Cacchione, Stefano; De Santis, Pasquale Biophysical Chemistry, Vol. 83, Issue 3 https://doi.org/10.1016/S0301-4622(99)00143-X	journal	January 2000
Mobility of positioned nucleosomes on 5 S rDNA Pennings, Sari; Meersseman, Geert; Bradbury, E. Morton Journal of Molecular Biology, Vol. 220, Issue 1 https://doi.org/10.1016/0022-2836(91)90384-I	journal	July 1991
Nucleosome sliding mechanisms: new twists in a looped history Mueller-Planitz, Felix; Klinker, Henrike; Becker, Peter B. Nature Structural & Molecular Biology, Vol. 20, Issue 9 https://doi.org/10.1038/nsmb.2648	journal	September 2013
An experimentally-informed coarse-grained 3-site-per-nucleotide model of DNA: Structure, thermodynamics, and dynamics of hybridization Hinckley, Daniel M.; Freeman, Gordon S.; Whitmer, Jonathan K. The Journal of Chemical Physics, Vol. 139, Issue 14 https://doi.org/10.1063/1.4822042	journal	October 2013
Frustration, specific sequence dependence, and nonlinearity in large-amplitude fluctuations of allosteric proteins Li, Wenfei; Wolynes, Peter G.; Takada, Shoji Proceedings of the National Academy of Sciences, Vol. 108, Issue 9 https://doi.org/10.1073/pnas.1018983108	journal	February 2011
In vitro low propensity to form nucleosomes of four telomeric sequences Cacchione, Stefano; Cerone, Maria Antonietta; Savino, Maria FEBS Letters, Vol. 400, Issue 1 https://doi.org/10.1016/S0014-5793(96)01318-X	journal	January 1997
Nucleosomes in Solution Exist as a Mixture of Twist-defect States Edayathumangalam, Rajeswari S.; Weyermann, Philipp; Dervan, Peter B. Journal of Molecular Biology, Vol. 345, Issue 1 https://doi.org/10.1016/j.jmb.2004.10.012	journal	January 2005
Mechanisms of ATP-dependent nucleosome sliding Bowman, Gregory D. Current Opinion in Structural Biology, Vol. 20, Issue 1 https://doi.org/10.1016/j.sbi.2009.12.002	journal	February 2010
The chromatin remodeller ACF acts as a dimeric motor to space nucleosomes Racki, Lisa R.; Yang, Janet G.; Naber, Nariman Nature, Vol. 462, Issue 7276 https://doi.org/10.1038/nature08621	journal	December 2009
Dynamics of nucleosome remodelling by individual ACF complexes Blosser, Timothy R.; Yang, Janet G.; Stone, Michael D. Nature, Vol. 462, Issue 7276 https://doi.org/10.1038/nature08627	journal	December 2009
Positioning and stability of nucleosomes on MMTV 3′LTR sequences Flaus, Andrew; Richmond, Timothy J. Journal of Molecular Biology, Vol. 275, Issue 3 https://doi.org/10.1006/jmbi.1997.1464	journal	January 1998
ISWI Remodelers Slide Nucleosomes with Coordinated Multi-Base-Pair Entry Steps and Single-Base-Pair Exit Steps Deindl, Sebastian; Hwang, William L.; Hota, Swetansu K. Cell, Vol. 152, Issue 3 https://doi.org/10.1016/j.cell.2012.12.040	journal	January 2013
Nucleosome structural studies Tan, Song; Davey, Curt A. Current Opinion in Structural Biology, Vol. 21, Issue 1 https://doi.org/10.1016/j.sbi.2010.11.006	journal	February 2011
DNA Shape Dominates Sequence Affinity in Nucleosome Formation Freeman, Gordon S.; Lequieu, Joshua P.; Hinckley, Daniel M. Physical Review Letters, Vol. 113, Issue 16 https://doi.org/10.1103/PhysRevLett.113.168101	journal	October 2014
The ATPase domain of ISWI is an autonomous nucleosome remodeling machine Mueller-Planitz, Felix; Klinker, Henrike; Ludwigsen, Johanna Nature Structural & Molecular Biology, Vol. 20, Issue 1 https://doi.org/10.1038/nsmb.2457	journal	December 2012
Transcription factor access is mediated by accurately positioned nucleosomes on the mouse mammary tumor virus promoter Archer, T. K.; Cordingley, M. G.; Wolford, R. G. Molecular and Cellular Biology, Vol. 11, Issue 2 https://doi.org/10.1128/mcb.11.2.688-698.1991	journal	February 1991
Coarse-Grained Ions for Nucleic Acid Modeling Hinckley, Daniel M.; de Pablo, Juan J. Journal of Chemical Theory and Computation, Vol. 11, Issue 11 https://doi.org/10.1021/acs.jctc.5b00341	journal	October 2015
High-resolution dynamic mapping of histone-DNA interactions in a nucleosome Hall, Michael A.; Shundrovsky, Alla; Bai, Lu Nature Structural & Molecular Biology, Vol. 16, Issue 2 https://doi.org/10.1038/nsmb.1526	journal	January 2009
Rapid spontaneous accessibility of nucleosomal DNA Li, Gu; Levitus, Marcia; Bustamante, Carlos Nature Structural & Molecular Biology, Vol. 12, Issue 1 https://doi.org/10.1038/nsmb869	journal	December 2004
Crystal structure of the nucleosome core particle at 2.8 Å resolution Luger, Karolin; Mäder, Armin W.; Richmond, Robin K. Nature, Vol. 389, Issue 6648 https://doi.org/10.1038/38444	journal	September 1997
Single-base resolution mapping of H1-nucleosome interactions and 3D organization of the nucleosome Syed, S. H.; Goutte-Gattat, D.; Becker, N. Proceedings of the National Academy of Sciences, Vol. 107, Issue 21 https://doi.org/10.1073/pnas.1000309107	journal	May 2010
Histone H4 tail mediates allosteric regulation of nucleosome remodelling by linker DNA Hwang, William L.; Deindl, Sebastian; Harada, Bryan T. Nature, Vol. 512, Issue 7513 https://doi.org/10.1038/nature13380	journal	June 2014
Coarse-grained modeling of DNA curvature Freeman, Gordon S.; Hinckley, Daniel M.; Lequieu, Joshua P. The Journal of Chemical Physics, Vol. 141, Issue 16 https://doi.org/10.1063/1.4897649	journal	October 2014
Defining the axis of a helix Kahn, Peter C. Computers & Chemistry, Vol. 13, Issue 3 https://doi.org/10.1016/0097-8485(89)85005-3	journal	January 1989
New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning Lowary, P. T.; Widom, J. Journal of Molecular Biology, Vol. 276, Issue 1 https://doi.org/10.1006/jmbi.1997.1494	journal	February 1998
Are nucleosome positions in vivo primarily determined by histone–DNA sequence preferences? Stein, Arnold; Takasuka, Taichi E.; Collings, Clayton K. Nucleic Acids Research, Vol. 38, Issue 3 https://doi.org/10.1093/nar/gkp1043	journal	November 2009
Blocking Transcription Through a Nucleosome with Synthetic DNA Ligands Gottesfeld, Joel M.; Belitsky, Jason M.; Melander, Christian Journal of Molecular Biology, Vol. 321, Issue 2 https://doi.org/10.1016/S0022-2836(02)00598-3	journal	August 2002
The DNA-encoded nucleosome organization of a eukaryotic genome Kaplan, Noam; Moore, Irene K.; Fondufe-Mittendorf, Yvonne Nature, Vol. 458, Issue 7236 https://doi.org/10.1038/nature07667	journal	December 2008
Structure and dynamics of DNA loops on nucleosomes studied with atomistic, microsecond-scale molecular dynamics Pasi, Marco; Lavery, Richard Nucleic Acids Research, Vol. 44, Issue 11 https://doi.org/10.1093/nar/gkw293	journal	April 2016
ACF, an ISWI-Containing and ATP-Utilizing Chromatin Assembly and Remodeling Factor Ito, Takashi; Bulger, Michael; Pazin, Michael J. Cell, Vol. 90, Issue 1 https://doi.org/10.1016/S0092-8674(00)80321-9	journal	July 1997
The chromatin-remodeling enzyme ACF is an ATP-dependent DNA length sensor that regulates nucleosome spacing Yang, Janet G.; Madrid, Tina Shahian; Sevastopoulos, Elena Nature Structural & Molecular Biology, Vol. 13, Issue 12 https://doi.org/10.1038/nsmb1170	journal	November 2006
Chromatin remodeling by DNA bending, not twisting Lorch, Y.; Davis, B.; Kornberg, R. D. Proceedings of the National Academy of Sciences, Vol. 102, Issue 5 https://doi.org/10.1073/pnas.0409413102	journal	January 2005
The presence of nucleosomes on a DNA template prevents initiation by RNA polymerase II in vitro Knezetic, Joseph A.; Luse, Donal S. Cell, Vol. 45, Issue 1 https://doi.org/10.1016/0092-8674(86)90541-6	journal	April 1986
Covalent modifications of histones during development and disease pathogenesis Bhaumik, Sukesh R.; Smith, Edwin; Shilatifard, Ali Nature Structural & Molecular Biology, Vol. 14, Issue 11 https://doi.org/10.1038/nsmb1337	journal	November 2007
Dynamic Regulation of Nucleosome Positioning in the Human Genome Schones, Dustin E.; Cui, Kairong; Cuddapah, Suresh Cell, Vol. 132, Issue 5 https://doi.org/10.1016/j.cell.2008.02.022	journal	March 2008
Disparity in the DNA translocase domains of SWI/SNF and ISW2 Dechassa, Mekonnen Lemma; Hota, Swetansu K.; Sen, Payel Nucleic Acids Research, Vol. 40, Issue 10 https://doi.org/10.1093/nar/gks007	journal	January 2012
Nucleosomes inhibit the initiation of transcription but allow chain elongation with the displacement of histones Lorch, Yahli; LaPointe, Janice W.; Kornberg, Roger D. Cell, Vol. 49, Issue 2 https://doi.org/10.1016/0092-8674(87)90561-7	journal	April 1987
Nucleosome dynamics: Sequence matters Eslami-Mossallam, Behrouz; Schiessel, Helmut; van Noort, John Advances in Colloid and Interface Science, Vol. 232 https://doi.org/10.1016/j.cis.2016.01.007	journal	June 2016
Determinants of nucleosome positioning Struhl, Kevin; Segal, Eran Nature Structural & Molecular Biology, Vol. 20, Issue 3 https://doi.org/10.1038/nsmb.2506	journal	March 2013
Chromatin Dynamics: Nucleosomes go Mobile through Twist Defects Kulić, I. M.; Schiessel, H. Physical Review Letters, Vol. 91, Issue 14 https://doi.org/10.1103/PhysRevLett.91.148103	journal	October 2003
Polymer Reptation and Nucleosome Repositioning Schiessel, H.; Widom, J.; Bruinsma, R. F. Physical Review Letters, Vol. 86, Issue 19 https://doi.org/10.1103/PhysRevLett.86.4414	journal	May 2001
Umbrella sampling: Umbrella sampling Kästner, Johannes Wiley Interdisciplinary Reviews: Computational Molecular Science, Vol. 1, Issue 6 https://doi.org/10.1002/wcms.66	journal	May 2011
Artificial nucleosome positioning sequences. Shrader, T. E.; Crothers, D. M. Proceedings of the National Academy of Sciences, Vol. 86, Issue 19 https://doi.org/10.1073/pnas.86.19.7418	journal	October 1989
The structure of DNA in the nucleosome core Richmond, Timothy J.; Davey, Curt A. Nature, Vol. 423, Issue 6936 https://doi.org/10.1038/nature01595	journal	May 2003
A Mesoscale Model of DNA and Its Renaturation Sambriski, E. J.; Schwartz, D. C.; de Pablo, J. J. Biophysical Journal, Vol. 96, Issue 5 https://doi.org/10.1016/j.bpj.2008.09.061	journal	March 2009
ISWI Remodelling of Physiological Chromatin Fibres Acetylated at Lysine 16 of Histone H4 Klinker, Henrike; Mueller-Planitz, Felix; Yang, Renliang PLoS ONE, Vol. 9, Issue 2 https://doi.org/10.1371/journal.pone.0088411	journal	February 2014
Simplified and improved string method for computing the minimum energy paths in barrier-crossing events E., Weinan; Ren, Weiqing; Vanden-Eijnden, Eric The Journal of Chemical Physics, Vol. 126, Issue 16 https://doi.org/10.1063/1.2720838	journal	April 2007
Sequence motifs and free energies of selected natural and non-natural nucleosome positioning DNA sequences Thåström, A.; Lowary, P. T.; Widlund, H. R. Journal of Molecular Biology, Vol. 288, Issue 2 https://doi.org/10.1006/jmbi.1999.2686	journal	April 1999
Crystal Structures of Nucleosome Core Particles in Complex with Minor Groove DNA-binding Ligands Suto, Robert K.; Edayathumangalam, Rajeswari S.; White, Cindy L. Journal of Molecular Biology, Vol. 326, Issue 2 https://doi.org/10.1016/S0022-2836(02)01407-9	journal	February 2003
The human telomere terminal transferase enzyme is a ribonucleoprotein that synthesizes TTAGGG repeats Morin, Gregg B. Cell, Vol. 59, Issue 3 https://doi.org/10.1016/0092-8674(89)90035-4	journal	November 1989
Determinants of nucleosome organization in primary human cells Valouev, Anton; Johnson, Steven M.; Boyd, Scott D. Nature, Vol. 474, Issue 7352 https://doi.org/10.1038/nature10002	journal	May 2011
Nucleosome Repositioning via Loop Formation Kulić, I. M.; Schiessel, H. Biophysical Journal, Vol. 84, Issue 5 https://doi.org/10.1016/S0006-3495(03)70044-7	journal	May 2003
Chromatin remodelling at promoters suppresses antisense transcription Whitehouse, Iestyn; Rando, Oliver J.; Delrow, Jeff Nature, Vol. 450, Issue 7172 https://doi.org/10.1038/nature06391	journal	December 2007
A coarse grain model for DNA Knotts, Thomas A.; Rathore, Nitin; Schwartz, David C. The Journal of Chemical Physics, Vol. 126, Issue 8 https://doi.org/10.1063/1.2431804	journal	February 2007
The RSC chromatin remodelling enzyme has a unique role in directing the accurate positioning of nucleosomes: Unique role of RSC in nucleosome positioning Wippo, Christian J.; Israel, Lars; Watanabe, Shinya The EMBO Journal, Vol. 30, Issue 7 https://doi.org/10.1038/emboj.2011.43	journal	February 2011
Analysis of Nucleosome Repositioning by Yeast ISWI and Chd1 Chromatin Remodeling Complexes Stockdale, Chris; Flaus, Andrew; Ferreira, Helder Journal of Biological Chemistry, Vol. 281, Issue 24 https://doi.org/10.1074/jbc.M600682200	journal	April 2006
A Novel Roll-and-Slide Mechanism of DNA Folding in Chromatin: Implications for Nucleosome Positioning Tolstorukov, Michael Y.; Colasanti, Andrew V.; McCandlish, David M. Journal of Molecular Biology, Vol. 371, Issue 3 https://doi.org/10.1016/j.jmb.2007.05.048	journal	August 2007
Nucleosome hopping and sliding kinetics determined from dynamics of single chromatin fibers in Xenopus egg extracts Ranjith, P.; Yan, J.; Marko, J. F. Proceedings of the National Academy of Sciences, Vol. 104, Issue 34 https://doi.org/10.1073/pnas.0701459104	journal	August 2007
A highly conserved repetitive DNA sequence, (TTAGGG)n, present at the telomeres of human chromosomes. Moyzis, R. K.; Buckingham, J. M.; Cram, L. S. Proceedings of the National Academy of Sciences, Vol. 85, Issue 18 https://doi.org/10.1073/pnas.85.18.6622	journal	September 1988
Tension-Dependent Free Energies of Nucleosome Unwrapping Lequieu, Joshua; Córdoba, Andrés; Schwartz, David C. ACS Central Science, Vol. 2, Issue 9 https://doi.org/10.1021/acscentsci.6b00201	journal	August 2016
Chromatin Remodeling In Vivo Fazzio, Thomas G.; Tsukiyama, Toshio Molecular Cell, Vol. 12, Issue 5 https://doi.org/10.1016/S1097-2765(03)00436-2	journal	November 2003
A 'loop recapture' mechanism for ACF-dependent nucleosome remodeling Strohner, Ralf; Wachsmuth, Malte; Dachauer, Karoline Nature Structural & Molecular Biology, Vol. 12, Issue 8 https://doi.org/10.1038/nsmb966	journal	July 2005

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