Dynamics of forced nucleosome unraveling and role of nonuniform histone-DNA interactions

Biophysical Journal

Volumn 103, Issue 5, 2012, Pages 989-998

  Dobrovolskaia, Irina V ^a   Arya, Gaurav ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; HISTONE;

ARTICLE; BIOMECHANICS; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; MECHANICS; METABOLISM; NUCLEOSOME; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN QUATERNARY STRUCTURE;

BIOMECHANICS; DNA; HISTONES; MECHANICAL PROCESSES; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; NUCLEOSOMES; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY;

EID: 84865737311     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2012.07.043     Document Type: Article

References (36)

1. C.A. Davey, and D.F. Sargent T.J. Richmond Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 a resolution J. Mol. Biol. 319 2002 1097 1113
2. K. Luger, and A.W. Mäder T.J. Richmond Crystal structure of the nucleosome core particle at 2.8 A resolution Nature 389 1997 251 260
3. G. Felsenfeld, and M. Groudine Controlling the double helix Nature 421 2003 448 453
4. G. Arya, A. Maitra, and S.A. Grigoryev A structural perspective on the where, how, why, and what of nucleosome positioning J. Biomol. Struct. Dyn. 27 2010 803 820
5. K.J. Polach, and J. Widom A model for the cooperative binding of eukaryotic regulatory proteins to nucleosomal target sites J. Mol. Biol. 258 1996 800 812
6. G. Felsenfeld Chromatin unfolds Cell 86 1996 13 19
7. B.R. Cairns Chromatin remodeling: insights and intrigue from single-molecule studies Nat. Struct. Mol. Biol. 14 2007 989 996
8. G.D. Bowman Mechanisms of ATP-dependent nucleosome sliding Curr. Opin. Struct. Biol. 20 2010 73 81
9. K. Luger, and T.J. Richmond DNA binding within the nucleosome core Curr. Opin. Struct. Biol. 8 1998 33 40
10. B.D. Brower-Toland, and C.L. Smith M.D. Wang Mechanical disruption of individual nucleosomes reveals a reversible multistage release of DNA Proc. Natl. Acad. Sci. USA 99 2002 1960 1965
11. M.A. Hall, and A. Shundrovsky M.D. Wang High-resolution dynamic mapping of histone-DNA interactions in a nucleosome Nat. Struct. Mol. Biol. 16 2009 124 129
12. V.M. Studitsky, D.J. Clark, and G. Felsenfeld Overcoming a nucleosomal barrier to transcription Cell 83 1995 19 27
13. J. Jin, and L. Bai M.D. Wang Synergistic action of RNA polymerases in overcoming the nucleosomal barrier Nat. Struct. Mol. Biol. 17 2010 745 753
14. M.L. Bennink, and S.H. Leuba J. Greve Unfolding individual nucleosomes by stretching single chromatin fibers with optical tweezers Nat. Struct. Biol. 8 2001 606 610
15. G.J. Gemmen, and R. Sim D.E. Smith Forced unraveling of nucleosomes assembled on heterogeneous DNA using core histones, NAP-1, and ACF J. Mol. Biol. 351 2005 89 99
16. S. Mihardja, and A.J. Spakowitz C. Bustamante Effect of force on mononucleosomal dynamics Proc. Natl. Acad. Sci. USA 103 2006 15871 15876
17. L.H. Pope, and M.L. Bennink J.F. Marko Single chromatin fiber stretching reveals physically distinct populations of disassembly events Biophys. J. 88 2005 3572 3583
18. I.M. Kulić, and H. Schiessel DNA spools under tension Phys. Rev. Lett. 92 2004 228101
19. B. Sudhanshu, and S. Mihardja A.J. Spakowitz Tension-dependent structural deformation alters single-molecule transition kinetics Proc. Natl. Acad. Sci. USA 108 2011 1885 1890
20. T. Wocjan, K. Klenin, and J. Langowski Brownian dynamics simulation of DNA unrolling from the nucleosome J. Phys. Chem. B 113 2009 2639 2646
21. R. Ettig, and N. Kepper K. Rippe Dissecting DNA-histone interactions in the nucleosome by molecular dynamics simulations of DNA unwrapping Biophys. J. 101 2011 1999 2008
22. I.V. Dobrovolskaia, M. Kenward, and G. Arya Twist propagation in dinucleosome arrays Biophys. J. 99 2010 3355 3364
23. G. Arya, Q. Zhang, and T. Schlick Flexible histone tails in a new mesoscopic oligonucleosome model Biophys. J. 91 2006 133 150
24. B. Rupp, and S. Parkin PDBSUP: A Fortran Program that Determines the Rotation Matrix and Translation Vector for Best Fit Superposition of Two PDB Files by Solving the Quaternion Eigenvalue Problem 1996 Lawrence Livermore National Laboratory Livermore, CA
25. R.A. Forties, and J.A. North R. Bundschuh A quantitative model of nucleosome dynamics Nucleic Acids Res. 39 2011 8306 8313
26. O.K. Dudko, G. Hummer, and A. Szabo Intrinsic rates and activation free energies from single-molecule pulling experiments Phys. Rev. Lett. 96 2006 108101
27. A. Maitra, and G. Arya Model accounting for the effects of pulling-device stiffness in the analyses of single-molecule force measurements Phys. Rev. Lett. 104 2010 108301
28. M. Tomschik, and H. Zheng S.H. Leuba Fast, long-range, reversible conformational fluctuations in nucleosomes revealed by single-pair fluorescence resonance energy transfer Proc. Natl. Acad. Sci. USA 102 2005 3278 3283
29. A. Gansen, and A. Valeri C.A. Seidel Nucleosome disassembly intermediates characterized by single-molecule FRET Proc. Natl. Acad. Sci. USA 106 2009 15308 15313
30. S.A. Grigoryev, and G. Arya T. Schlick Evidence for heteromorphic chromatin fibers from analysis of nucleosome interactions Proc. Natl. Acad. Sci. USA 106 2009 13317 13322
31. G.H. Koenderink, and A.P. Philipse Rotational and translational self-diffusion in colloidal sphere suspensions and the applicability of generalized Stokes-Einstein relations Langmuir 16 2000 5631 5638
32. M. Simon, and J.A. North M.G. Poirier Histone fold modifications control nucleosome unwrapping and disassembly Proc. Natl. Acad. Sci. USA. 108 2011 12711 12716
33. D. Stigter Interactions of highly charged colloidal cylinders with applications to double-stranded Biopolymers 16 1977 1435 1448
34. A. Iniesta, and J.G. de la Torre A 2nd-order algorithm for the simulation of the Brownian dynamics of macromolecular models J. Chem. Phys. 92 1990 2015 2018
35. G. Arya, and T. Schlick A tale of tails: how histone tails mediate chromatin compaction in different salt and linker histone environments J. Phys. Chem. A 113 2009 4045 4059
36. A. Maitra, and G. Arya Influence of pulling handles and device stiffness in single-molecule force spectroscopy Phys. Chem. Chem. Phys. 13 2011 1836 1842