The Role of Histone Tails in the Nucleosome: A Computational Study

Biophysical Journal

Volumn 107, Issue 12, 2014, Pages 2911-2922

  Erler, Jochen ^a   Zhang, Ruihan ^a   Petridis, Loukas ^b   Cheng, Xiaolin ^b   Smith, Jeremy C ^b   Langowski, Jörg ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b OAK RIDGE NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; HISTONE; NUCLEOSOME; PROTEIN BINDING;

AMINO ACID SEQUENCE; CHEMISTRY; METABOLISM; MOLECULAR DYNAMICS; MOLECULAR GENETICS; NUCLEOSOME; NUCLEOTIDE SEQUENCE;

AMINO ACID SEQUENCE; BASE SEQUENCE; DNA; HISTONES; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; NUCLEOSOMES; PROTEIN BINDING;

EID: 84930762917     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2014.10.065     Document Type: Article

References (66)

1. A.L. Olins, and D.E. Olins Spheroid chromatin units (ν bodies) Science 183 1974 330 332
2. C.L. Woodcock, and L.-L. Frado L. Ricciardiello Fine structure of active ribosomal genes Chromosoma 58 1976 33 39
3. K. Luger, and A.W. Mäder T.J. Richmond Crystal structure of the nucleosome core particle at 2.8 Å resolution Nature 389 1997 251 260
4. C.A. Davey, and T.J. Richmond DNA-dependent divalent cation binding in the nucleosome core particle Proc. Natl. Acad. Sci. USA 99 2002 11169 11174
5. L.L. Preez, and H.-G. Patterton Secondary structures of the core histone N-terminal tails: their role in regulating chromatin structure T.K. Kundu, Epigenetics: Development and Disease 2013 Springer New York 37 55
6. K. Luger, and T.J. Richmond The histone tails of the nucleosome Curr. Opin. Genet. Dev. 8 1998 140 146
7. B. Dorigo, and T. Schalch T.J. Richmond Chromatin fiber folding: requirement for the histone H4 N-terminal tail J. Mol. Biol. 327 2003 85 96
8. C. Zheng, and X. Lu J.J. Hayes Salt-dependent intra- and internucleosomal interactions of the H3 tail domain in a model oligonucleosomal array J. Biol. Chem. 280 2005 33552 33557
9. J.C. Hansen, and X. Lu R.W. Woody Intrinsic protein disorder, amino acid composition, and histone terminal domains J. Biol. Chem. 281 2006 1853 1856
10. D.A. Potoyan, and G.A. Papoian Energy landscape analyses of disordered histone tails reveal special organization of their conformational dynamics J. Am. Chem. Soc. 133 2011 7405 7415
11. X. Wang, and S.C. Moore J. Ausió Acetylation increases the α-helical content of the histone tails of the nucleosome J. Biol. Chem. 275 2000 35013 35020
12. H. Liu, and Y. Duan Effects of posttranslational modifications on the structure and dynamics of histone H3 N-terminal peptide Biophys. J. 94 2008 4579 4585
13. D. Yang, and G. Arya Structure and binding of the H4 histone tail and the effects of lysine 16 acetylation Phys. Chem. Chem. Phys. 13 2011 2911 2921
14. M. Shogren-Knaak, and H. Ishii C.L. Peterson Histone H4-K16 acetylation controls chromatin structure and protein interactions Science 311 2006 844 847
15. P.J. Robinson, and W. An D. Rhodes 30 nm Chromatin fibre decompaction requires both H4-K16 acetylation and linker histone eviction J. Mol. Biol. 381 2008 816 825
16. A. Allahverdi, and R. Yang L. Nordenskiöld The effects of histone H4 tail acetylations on cation-induced chromatin folding and self-association Nucleic Acids Res. 39 2011 1680 1691
17. J. Schwartzentruber, and A. Korshunov N. Jabado Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma Nature 482 2012 226 231
18. B.J. Wilkins, and N.A. Rall H. Neumann A cascade of histone modifications induces chromatin condensation in mitosis Science 343 2014 77 80
19. J.-L. Banères, A. Martin, and J. Parello The N tails of histones H3 and H4 adopt a highly structured conformation in the nucleosome J. Mol. Biol. 273 1997 503 508
20. H. Kato, and J. Gruschus Y. Bai Characterization of the N-terminal tail domain of histone H3 in condensed nucleosome arrays by hydrogen exchange and NMR J. Am. Chem. Soc. 131 2009 15104 15105
21. B.-R. Zhou, and H. Feng Y. Bai Histone H4 K16Q mutation, an acetylation mimic, causes structural disorder of its N-terminal basic patch in the nucleosome J. Mol. Biol. 421 2012 30 37
22. M. Gao, and P.S. Nadaud C.P. Jaroniec Histone H3 and H4 N-terminal tails in nucleosome arrays at cellular concentrations probed by magic angle spinning NMR spectroscopy J. Am. Chem. Soc. 135 2013 15278 15281
23. L. Zhong, and W.C. Johnson Jr. Environment affects amino acid preference for secondary structure Proc. Natl. Acad. Sci. USA 89 1992 4462 4465
24. Y. Yang, and A.P. Lyubartsev L. Nordenskiöld Computer modeling reveals that modifications of the histone tail charges define salt-dependent interaction of the nucleosome core particles Biophys. J. 96 2009 2082 2094
25. 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
26. J. Sun, Q. Zhang, and T. Schlick Electrostatic mechanism of nucleosomal array folding revealed by computer simulation Proc. Natl. Acad. Sci. USA 102 2005 8180 8185
27. G. Arya, Q. Zhang, and T. Schlick Flexible histone tails in a new mesoscopic oligonucleosome model Biophys. J. 91 2006 133 150
28. G. Arya, and T. Schlick Role of histone tails in chromatin folding revealed by a mesoscopic oligonucleosome model Proc. Natl. Acad. Sci. USA 103 2006 16236 16241
29. S. Sharma, F. Ding, and N.V. Dokholyan Multiscale modeling of nucleosome dynamics Biophys. J. 92 2007 1457 1470
30. K. Voltz, and J. Trylska J. Langowski Unwrapping of nucleosomal DNA ends: a multiscale molecular dynamics study Biophys. J. 102 2012 849 858
31. M. Biswas, J. Langowski, and T.C. Bishop Atomistic simulations of nucleosomes Wiley Interdiscip. Comput. Mol. Sci. 3 2013 378 392
32. J.Z. Ruscio, and A. Onufriev A computational study of nucleosomal DNA flexibility Biophys. J. 91 2006 4121 4132
33. D. Roccatano, A. Barthel, and M. Zacharias Structural flexibility of the nucleosome core particle at atomic resolution studied by molecular dynamics simulation Biopolymers 85 2007 407 421
34. M. Biswas, and K. Voltz J. Langowski Role of histone tails in structural stability of the nucleosome PLOS Comput. Biol. 7 2011 e1002279
35. 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
36. E.A. Cino, W.Y. Choy, and M. Karttunen Comparison of secondary structure formation using 10 different force fields in microsecond molecular dynamics simulations J. Chem. Theory Comput. 8 2012 2725 2740
37. K. Lindorff-Larsen, and P. Maragakis D.E. Shaw Systematic validation of protein force fields against experimental data PLoS ONE 7 2012 e32131
38. N. Korolev, and H. Yu L. Nordenskiöld Molecular dynamics simulations demonstrate the regulation of DNA-DNA attraction by H4 histone tail acetylations and mutations Biopolymers 101 2014 1051 1064
39. D.A. Potoyan, and G.A. Papoian Regulation of the H4 tail binding and folding landscapes via Lys-16 acetylation Proc. Natl. Acad. Sci. USA 109 2012 17857 17862
40. K. Hukushima, and K. Nemoto Exchange Monte Carlo method and application to spin glass simulations J. Phys. Soc. Jpn. 65 1996 1604 1608
41. T. Okabe, and M. Kawata M. Mikami Replica-exchange Monte Carlo method for the isobaric-isothermal ensemble Chem. Phys. Lett. 335 2001 435 439
42. Y. Okamoto Generalized-ensemble algorithms: enhanced sampling techniques for Monte Carlo and molecular dynamics simulations J. Mol. Graph. Model. 22 2004 425 439 (Conformational Sampling.)
43. A. Onufriev, D. Bashford, and D.A. Case Exploring protein native states and large-scale conformational changes with a modified generalized born model Proteins 55 2004 383 394
44. A. Bondi van der Waals volumes and radii J. Phys. Chem. 68 1964 441 451
45. V. Tsui, and D.A. Case Molecular dynamics simulations of nucleic acids with a generalized Born solvation model J. Am. Chem. Soc. 122 2000 2489 2498
46. B. Hess, and C. Kutzner E. Lindahl GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation J. Chem. Theory Comput. 4 2008 435 447
47. D. Van Der Spoel, and E. Lindahl H.J.C. Berendsen GROMACS: fast, flexible, and free J. Comput. Chem. 26 2005 1701 1718
48. E. Lindahl, B. Hess, and D. van der Spoel GROMACS 3.0: a package for molecular simulation and trajectory analysis J. Mol. Mod. 2001 306 317
49. H. Berendsen, D. van der Spoel, and R. van Drunen GROMACS: A message-passing parallel molecular dynamics implementation Comput. Phys. Commun. 91 1995 43 56
50. G. Bussi, D. Donadio, and M. Parrinello Canonical sampling through velocity rescaling J. Chem. Phys. 126 2007 014101
51. B. Hess, and H. Bekker J.G.E.M. Fraaije LINCS: A linear constraint solver for molecular simulations J. Comput. Chem. 18 1997 1463 1472
52. R. Anandakrishnan, M. Daga, and A.V. Onufriev An n log n generalized Born approximation J. Chem. Theory Comput. 7 2011 544 559
53. A.D. MacKerell Jr., N. Banavali, and N. Foloppe Development and current status of the CHARMM force field for nucleic acids Biopolymers 56 2000-2001 257 265
54. Y. Duan, and C. Wu P. Kollman A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations J. Comput. Chem. 24 2003 1999 2012
55. R.B. Best, N.V. Buchete, and G. Hummer Are current molecular dynamics force fields too helical? Biophys. J. 95 2008 L07 L09
56. A.T. Tzanov, M.A. Cuendet, and M.E. Tuckerman How accurately do current force fields predict experimental peptide conformations? An adiabatic free energy dynamics study J. Phys. Chem. B 118 2014 6539 6552
57. J. Huang, and A.D. MacKerell Jr. Induction of peptide bond dipoles drives cooperative helix formation in the (AAQAA)3 peptide Biophys. J. 107 2014 991 997
58. V. Hornak, and R. Abel C. Simmerling Comparison of multiple Amber force fields and development of improved protein backbone parameters Proteins. 65 2006 712 725
59. K. Lindorff-Larsen, and S. Piana D.E. Shaw Improved side-chain torsion potentials for the Amber ff99SB protein force field Proteins 78 2010 1950 1958
60. W. Kabsch, and C. Sander Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features Biopolymers 22 1983 2577 2637
61. M.M. Gromiha, C. Santhosh, and M. Suwa Influence of cation-π interactions in protein-DNA complexes Polymer 45 2004 633 639
62. M. Stewart, and T. Dunlap L. McFail-Isom Cations form sequence selective motifs within DNA grooves via a combination of cation-pi and ion-dipole/hydrogen bond interactions PLoS ONE 8 2013 e71420
63. Y. Hirano, and K. Hizume Y. Hiraoka Lamin B receptor recognizes specific modifications of histone H4 in heterochromatin formation J. Biol. Chem. 287 2012 42654 42663
64. S. Mangenot, and A. Leforestier F. Livolant Salt-induced conformation and interaction changes of nucleosome core particles Biophys. J. 82 2002 345 356
65. V. Mutskov, and D. Gerber S. Dimitrov Persistent interactions of core histone tails with nucleosomal DNA following acetylation and transcription factor binding Mol. Cell. Biol. 18 1998 6293 6304
66. P.-Y. Kan, and J.J. Hayes Detection of interactions between nucleosome arrays mediated by specific core histone tail domains Methods 41 2007 278 285 (Methods Related to the Structure and Function of Eukaryotic Chromatin.)