Structural mechanics of DNA wrapping in the nucleosome

Journal of Molecular Biology

Volumn 396, Issue 2, 2010, Pages 264-279

  Battistini, Federica ^a   Hunter, Christopher A ^a   Gardiner, Eleanor J ^a   Packer, Martin J ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Base step parameter; DNA bending; DNA protein recognition; Nucleosome; Sequence dependent DNA structure

Indexed keywords

NAKED DNA; OLIGOMER; DNA;

ARTICLE; BASE PAIRING; BINDING AFFINITY; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA CONFORMATION; DNA HELIX; DNA SEQUENCE; DNA STRUCTURE; DNA SUPERCOILING; ENERGY TRANSFER; MOLECULAR MECHANICS; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN DNA BINDING; BIOLOGICAL MODEL; BIOMECHANICS; CHEMICAL STRUCTURE; CHEMISTRY; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONFORMATION; METABOLISM; MOLECULAR DYNAMICS; PHYSIOLOGY; PROTEIN QUATERNARY STRUCTURE; THEORETICAL MODEL; X RAY CRYSTALLOGRAPHY;

BIOMECHANICS; CHROMATIN ASSEMBLY AND DISASSEMBLY; CRYSTALLOGRAPHY, X-RAY; DNA; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MODELS, THEORETICAL; MOLECULAR DYNAMICS SIMULATION; NUCLEIC ACID CONFORMATION; NUCLEOSOMES; PROTEIN STRUCTURE, QUATERNARY;

EID: 77449136648     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.11.040     Document Type: Article

References (75)

1. Richmond T.J., Davey C.A. The structure of DNA in the nucleosome core. Nature 2003, 423:145-150.
2. Elgin S.C.R., Workman J.L. Chromatin Structure and Gene Expression 2000, Oxford University Press, Oxford, UK, 328 pp.
3. Widom J. Structure, dynamics, and function of chromatin in vitro. Annu. Rev. Biophys. Biomol. Struct. 1998, 27:285-327.
4. Wolffe A. Chromatin Structure and Function 1998, Academic Press, San Diego, CA. 3rd edit.
5. Polach K.J., Widom J. Mechanism of protein access to specific DNA sequences in chromatin: a dynamic equilibrium model for gene regulation. J. Mol. Biol. 1995, 254:130-149.
6. Polach K.J., Widom J. A model for the cooperative binding of ukaryotic regulatory proteins to nucleosomal target sites. J. Mol. Biol. 1996, 258:800-812.
7. Anderson J.D., Widom J. Sequence- and position-dependence of the equilibrium accessibility of nucleosomal DNA target sites. J. Mol. Biol. 2000, 296:979-987.
8. Anderson J.D., Widom J. Poly(dA-dT) promoter elements increase the equilibrium accessibility of nucleosomal DNA target sites. Mol. Cell. Biol. 2001, 21:3830-3839.
9. Lowary P.T., Widom J. Nucleosome packaging and nucleosome positioning of genomic DNA. Proc. Natl Acad. Sci. USA 1997, 94:1183-1188.
10. Thastrom A., Lowary P.T., Widlund H.R., Cao H., Kubista M., Widom J. Sequence motifs and free energies of selected natural and non-natural nucleosome positioning DNA sequences. J. Mol. Biol. 1999, 288:213-229.
11. Thastrom A., Lowary P.T., Widom J. Measurement of histone-DNA interaction free energy in nucleosomes. Methods (San Diego) 2004, 33:33-44.
12. Thastrom A., Bingham L.M., Widom J. Nucleosomal locations of dominant DNA sequence motifs for histone-DNA interactions and nucleosome positioning. J. Mol. Biol. 2004, 338:695-709.
13. Sekinger E.A., Moqtaderi Z., Struhl K. Intrinsic histone-DNA interactions and low nucleosome density are important for preferential accessibility of promoter regions in yeast. Mol. Cell 2005, 18:735-748.
14. Satchwell S.C., Drew H.R., Travers A.A. Sequence periodicities in chicken nucleosome core DNA. J. Mol. Biol. 1986, 191:659-675.
15. Travers A., Drew H. DNA recognition and nucleosome organization. Biopolymers 1998, 44:423-433.
16. Drew H.R., Travers A.A. DNA bending and its relation to nucleosome positioning. J. Mol. Biol. 1985, 186:773-790.
17. Shrader T.E., Crothers D.M. Artificial nucleosome positioning sequences. Proc. Natl Acad. Sci. USA 1989, 86:7418-7422.
18. Travers A.A., Klug A. The bending of DNA in nucleosomes and its wider implications. Philos. Trans. R. Soc. London, Ser. B 1987, 317:537-561.
19. Lowary P.T., Widom J. New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J. Mol. Biol. 1998, 276:19-42.
20. Widom J. Role of DNA sequence in nucleosome stability and dynamics. Q. Rev. Biophys. 2001, 34:269-324.
21. Stein A., Bina M. A signal encoded in vertebrate DNA that influences nucleosome positioning and alignment. Nucleic Acids Res. 1999, 27:848-853.
22. Yuan G., Liu Y., Dion M.F., Slack M.D., Wu L.F., Altschuler S.J., Rando O.J. Genome-scale identification of nucleosome positions in S. cerevisiae. Science 2005, 309:626-630.
23. Ozsolak F., Song J.S., Liu X.S., Fisher D.E. High-throughput mapping of the chromatin structure of human promoters. Nat. Biotechnol. 2007, 25:244-248.
24. Kornberg R.D., Stryer L. Statistical distributions of nucleosomes: non-random locations by a stochastic mechanism. Nucleic Acids Res. 1988, 16:6677-6690.
25. Albert I., Mavrich T.N., Tomsho L.P., Qi J., Zanton S.J., Schuster S.C., Pugh B.F. Translational and rotational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome. Nature 2007, 446:572-576.
26. Lee W., Tillo D., Bray N., Morse R.H., Davis R.W., Hughes T.R., Nislow C. A high-resolution atlas of nucleosome occupancy in yeast. Nat. Genet. 2007, 39:1235-1244.
27. MacIsaac K.D., Wang T., Gordon D.B., Gifford D.K., Stormo G.D., Fraenkel E. An improved map of conserved regulatory sites for Saccharomyces cerevisiae. BMC Bioinformatics 2006, 7:113.
28. Pokholok D.K., Harbison C.T., Levine S., Cole M., Hannett N.M., Lee T.I., et al. Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 2005, 122:517-527.
29. Raisner R.M., Hartley P.D., Meneghini M.D., Bao M.Z., Liu C.L., Schreiber S.L., et al. Histone variant H2A.Z marks the 5′ ends of both active and inactive genes in euchromatin. Cell 2005, 123:233-248.
30. Schones D., Cui K., Cuddapah S., Roh T.-Y., Barski A., Wang Z., et al. Dynamic regulation of nucleosome positioning in the human genome. Cell 2008, 132:887-898.
31. Shivaswamy S., Bhinge A., Zhao Y., Jones S., Hirst M., Iyer V.R. Dynamic remodeling of individual nucleosomes across a eukaryotic genome in response to transcriptional perturbation. PLoS Biol. 2008, 6:65.
32. Segal E., Fondufe-Mittendorf Y., Chen L., Thastrom A., Field Y., Moore I.K., et al. A genomic code for nucleosome positioning. Nature 2006, 442:772-778.
33. Ioshikhes I., Bolshoy A., Derenshteyn K., Borodovsky M., Trifonov E.N. Nucleosome DNA sequence pattern revealed by multiple alignment of experimentally mapped sequences. J. Mol. Biol. 1996, 262:129-139.
34. Peckham H.E., Thurman R.E., Fu Y., Stamatoyannopoulos J.A., Noble W.S., Struhl K., Weng Z. Nucleosome positioning signals in genomic DNA. Genome Res. 2007, 17:1170-1177.
35. Ioshikhes I.P., Albert I., Zanton S.J., Pugh B.F. Nucleosome positions predicted through comparative genomics. Nat. Genet. 2006, 38:1210-1215.
36. Yuan G.C., Liu J.S. Genomic sequence is highly predictive of local nucleosome depletion. PLoS Comput. Biol. 2008, 4:164-174.
37. Simpson R.T., Stafford D.W. Structural features of a phased nucleosome core particle. Proc. Natl Acad. Sci. USA 1983, 80:51-55.
38. Morozov A.V., Havranek J.J., Baker D., Siggia E.D. Protein-DNA binding specificity predictions with structural models. Nucleic Acids Res. 2005, 33:5781-5798.
39. Tolstorukov M.Y., Colasanti A.V., McCandlish D.M., Olson W.K., Zhurkin V.B. A novel roll-and-slide mechanism of DNA folding in chromatin: implications for nucleosome positioning. J. Mol. Biol. 2007, 371:725-738.
40. Anselmi C., Bocchinfuso G., De Santis P., Savino M., Scipioni A. A theoretical model for the prediction of sequence-dependent nucleosome thermodynamic stability. Biophys. J. 2000, 79:601-613.
41. Olson W.K., Gorin A.A., Lu X., Hock L.M., Zhurkin V.B. DNA sequence-dependent deformability deduced from protein-DNA crystal complexes. Proc. Natl Acad. Sci. USA 1998, 95:11163-11168.
42. Trifonov E.N., Kogan S., Cohanim A.B. Latest on the nucleosome positioning sequence patterns. DNA Structure, Chromatin and Gene Expression 2006, Transworld Research Network, Trivandrum, India. R. Kiyama, M. Shimizu (Eds.).
43. Hunter C.A. Sequence-dependent DNA structure. The role of base stacking interactions. J. Mol. Biol. 1993, 230:1025-1054.
44. Hunter C.A. Sequence-dependent DNA structure. BioEssays 1996, 18:157-162.
45. Hunter C.A., Lu X.-J. Construction of double-helical DNA structures based on dinucleotide building blocks. J. Biomol. Struct. Dyn. 1997, 14:747-756.
46. Hunter C.A., Lu X.-J. DNA base-stacking interactions: a comparison of theoretical calculations with oligonucleotide X-ray crystal structures. J. Mol. Biol. 1997, 265:603-619.
47. Packer M.J., Hunter C.A. Sequence-dependent DNA structure: the role of the sugar-phosphate backbone. J. Mol. Biol. 1998, 280:407-420.
48. Packer M.J., Dauncey M.P., Hunter C.A. Sequence-dependent DNA structure: dinucleotide conformational maps. J. Mol. Biol. 2000, 295:71-83.
49. Packer M.J., Dauncey M.P., Hunter C.A. Sequence-dependent DNA structure: tetranucleotide conformational maps. J. Mol. Biol. 2000, 295:85-103.
50. Packer M.J., Hunter C.A. Sequence-structure relationships in DNA oligomers: a computational approach. J. Am. Chem. Soc. 2001, 123:7399-7406.
51. Hunter C.A., Packer M.J. Computational approaches to predicting sequence-structure relationships in DNA. Solid Mech. Its Appl. 2002, 104:447-456.
52. Gardiner E.J., Hunter C.A., Packer M.J., Palmer D.S., Willett P. Sequence-dependent DNA structure: a database of octamer structural parameters. J. Mol. Biol. 2003, 332:1025-1035.
53. Farwer J., Packer M.J., Hunter C.A. PREDICTOR: a web-based tool for the prediction of atomic structure from sequence for double helical DNA with up to 150 base pairs. In Silico Biol. 2007, 7:595-600.
54. Farwer J., Packer Martin J., Hunter C.A. Prediction of atomic structure from sequence for double helical DNA oligomers. Biopolymers 2006, 81:51-61.
55. Davey C.A., Sargent D.F., Luger K., Maeder A.W., Richmond T.J. Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 Å resolution. J. Mol. Biol. 2002, 319:1097-1113.
56. Luger K., Mader A.W., Richmond R.K., Sargent D.F., Richmond T.J. Crystal structure of the nucleosome core particle at 2.8 Å of resolution. Nature 1997, 89:251-260.
57. Luger K., Rechsteiner T.J., Flaus A.J., Waye M.M.Y., Richmond T.J. Characterization of nucleosome core particles containing histone proteins made in bacteria. J. Mol. Biol. 1997, 272:301-311.
58. Ong M.S., Richmond T.J., Davey C.A. DNA stretching and extreme kinking in the nucleosome core. J. Mol. Biol. 2007, 368:1067-1074.
59. Luger K., Richmond T.J. DNA binding within the nucleosome core. Curr. Opin. Struct. Biol. 1998, 8:33-40.
60. Luger K., Richmond T.J. The histone tails of the nucleosome. Curr. Opin. Genet. Dev. 1998, 8:140-146.
61. Calladine C.R., Drew H.R. Understanding DNA: The Molecule and How it Works 1997, Academic Press, San Diego, CA. 2nd edit.
62. Kim J.L., Nikolov D.B., Burley S.K. Co-crystal structure of T BP recognizing the minor groove of a TATA element. Nature 1993, 365:520-527.
63. Kim Y., Geiger J.H., Hahn S., Sigler P.B. Crystal structure of a yeast T BP-TATA-box complex. Nature 1993, 365:512-520.
64. Lavery R., Sklenar H. The definition of generalised helicoidal parameters and of axis curvature for irregular nucleic acids. J. Biomol. Struct. Dyn. 1988, 6:63-91.
65. Zhurkin V.B., Lysov Y.P., Ivanov V.I. Anisotropic flexibility of DNA and the nucleosomal structure. Nucleic Acids Res. 1979, 6:1081-1096.
66. Lu X.-J., El Hassan M.A., Hunter C.A. Structure and conformation of helical nucleic acids: rebuilding program (SCHNArP). J. Mol. Biol. 1997, 273:681-691.
67. Lu X.-J., El Hassan M.A., Hunter C.A. Structure and conformation of helical nucleic acids: analysis program (SCHNAaP). J. Mol. Biol. 1997, 273:668-680.
68. Lu X., Olson W.K. 3DNA: a software package for the analysis, rebuilding and visualization of three-dimensional nucleic acid structure. Nucleic Acids Res. 2003, 31:5108-5121.
69. El Hassan M.A., Calladine C.R. The assessment of the geometry of dinucleotide steps in double-helical DNA; a new local calculation scheme. J. Mol. Biol. 1995, 251:648-664.
70. Calladine C.R., Drew H.R. Principles of sequence-dependent flexure of DNA. J. Mol. Biol. 1986, 192:907-918.
71. Calladine C.R., Drew H.R. Curvature and flexibility of DNA: sequence-directed effects seen from a structural mechanics viewpoint. Mol. Struct. Life 1992, 43:43-55.
72. El Hassan M.A., Calladine C.R. Structural mechanics of bent DNA. Endeavour 1996, 20:61-67.
73. El Hassan M.A., Calladine C.R. Propeller-twisting of base-pairs and the conformational mobility of dinucleotide steps in DNA. J. Mol. Biol. 1996, 259:95-103.
74. El Hassan M.A., Calladine C.R. Two distinct modes of protein-induced bending in DNA. J. Mol. Biol. 1998, 282:331-343.
75. Gorin A.A., Zhurkin V.B., Wilma K. B-DNA twisting correlates with base-pair morphology. J. Mol. Biol. 1995, 247:34-48.