The structural basis of DNA flexibility

Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences

Volumn 362, Issue 1820, 2004, Pages 1423-1438

  Travers, A A ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

Anisotropic bending; Bending flexibility; Genomic distribution of 'flexible' sequences; Nucleosome; Torsional flexibility; TpA base step

Indexed keywords

EID: 3042581815     PISSN: 1364503X     EISSN: None     Source Type: Journal    
DOI: 10.1098/rsta.2004.1390     Document Type: Article

References (61)

1. Anselmi, C., Bocchinfuso, G., De Santis, P., Savino, M. & Scipioni, A. 1999 Dual role of DNA intrinsic curvature and flexibility in determining nucleosome stability. J. Mol. Biol. 286, 1293-1301.
2. Baldi, P., Brunak, S., Chauvin, Y. & Krogh, A. 1996 Naturally occuring nucleosome positioning signals in human exons and introns. J. Mol. Biol. 263, 503-510.
3. Bednar, J., Furrer, P., Katritch, V., Stasiak, A. Z., Dubochet, J. & Stasiak, A. 1995 Determination of DNA persistence length by cryo-electron microscopy. Separation of the static and dynamic contributions to the apparent persistence length of DNA. J. Mol. Biol. 254, 579-594.
4. Berge, T., Jenkins, N. S., Hopkirk, R. B., Waring, M. J., Edwardson, J. M. & Henderson, R. M. 2002 Structural perturbations in DNA caused by bis-intercalation of ditercalinium visualised by atomic force microscopy. Nucleic Acids Res. 30, 2980-2986.
5. Bloomfield, V. A., Crothers, D. M. & Tinoco, I. 1974 Physical chemistry of nucleic acids. New York: Harper and Row.
6. Brukner, I., Diakic, M., Savic, A., Susic, S., Pongor, S. & Suck, D. 1993 Evidence for opposite groove-directed curvature of GGGCCC and AAAAAA tracts. Nucleic Acids Res. 21, 1025-1029.
7. Brukner, I., Sanchez, R., Suck, D. & Pongor, S. 1995 Sequence-dependent bending propensity of DNA are revealed by DNase I: parameters for trinucleotides. EMBO J. 14, 1812-1818.
8. Buttinelli, M., Minnock, A., Panetta, G., Waring, M. & Travers, A. 1998 The exocyclic groups of DNA modulate the affinity and positioning of the histone octamer. Proc. Natl. Acad. Sci. USA 95, 8544-8549.
9. Calladine, C. R. 1982 Mechanics of sequence-dependent stacking of bases in B-DNA. J. Mol. Biol. 161, 343-352.
10. Calladine, C. R. & Drew, H. R. 1986 The principles of sequence-dependent flexure of DNA. J. Mol. Biol. 192, 907-918.
11. Charney, E., Chen, H.-H. & Rau, D. C. 1991 The flexibility of A-form DNA. J. Biomol. Struct. Dynam. 9, 353-362.
12. Chastain, P. D. & Sinden, R. R. 1998 CTG repeats associated with human genetic disease are inherently flexible. J. Mol. Biol. 275, 405-411.
13. de Chadarevian, S. & Kammioga, H. 2002 Representations of the double helix. Cambridge: Whipple Museum of the History of Science.
14. Dickerson, R. E. (and 12 others) 1989 Definitions and nomenclature of nucleic acid structure components. EMBO J. 8, 1-4.
15. Diekmann, S. 1992 Analyzing DNA curvature in polyacrylamide gels. Meth. Enzymol. 212, 30-46.
16. Dornberger, U., Flemming, J. & Fritsche, H. 1998 Structure determination and analysis of helix parameters in the DNA decamer d(CATGGCCATG)2: comparision of results from NMR and crystallography. J. Mol. Biol. 284, 1453-1463.
17. Drew, H. R. & Travers, A. A. 1985 DNA bending and its relation to nucleosome positioning. J. Mol. Biol. 186, 773-790.
18. Drew, H. R., Weeks, J. R. & Travers, A. A. 1985 Negative supercoiling induces spontaneous unwinding of a bacterial promoter. EMBO J. 4, 1025-1032.
19. El. Hassan, M. A. & Calladine, C. R. 1996 Propeller-twisting of base-pairs and the conformationational mobility of dinucleotide steps in DNA. J. Mol. Biol. 259, 95-103.
20. El. Hassan, M. A. & Calladine, C. R. 1997 Conformational characteristics of DNA: empirical classifications and a hypothesis for the conformational behaviour of dinucleotide steps. Phil. Trans. R. Soc. Lond. A 355, 43-100.
21. Fang, Y., Spisz, T. S. & Hoh, J. H. 1999 Ethanol-induced structural transitions in DNA. Nucleic Acids Res. 27, 1943-1949.
22. Fitzgerald, D. J. & Anderson, J. N. 1999 DNA distortion as a factor in nucleosome positioning. J. Mol. Biol. 203, 477-491.
23. Frontali, C., Dore, E., Ferrauto, A., Gratton, E., Bettini, A., Pozzan, M. R. & Valdevit, E. 1979 An absolute method for the determination of the persistence length of native DNA from electron micrographs. Biopolymers 18, 1353-1373.
24. Gale, J. M., Nissen, K. A. & Smerdon, M. J. 1987 UV-induced formation of pyrimidine dimers in nucleosome core DNA is strongly modulated with a period of 10.3 bases. Proc. Natl Acad. Sci. USA 84, 6644-6648.
25. Gallego, J., Pascual-Teresa, A. R., Pisabarro, M. T. & Gago, F. 1995 QSAR and molecular modeling; concepts, computational tools and applications (ed. F. Sanz, J. Giraldo, & F. Manaut), pp. 274-281. Barcelona: Prous Science.
26. Gartenberg, M. R. & Crothers, D. M. 1988 DNA sequence determinants of CAP-induced bending and protein binding affinity. Nature 333, 824-829.
27. Gorin, A., Zhurkin, V. B. & Olson, W. K. 1995 B-DNA twisting correlates with base-pair morphology. J. Mol. Biol. 247, 34-48.
28. Gotoh, O. & Tagashiia, Y. 1981 Stabilities of nearest-neighbour doublets in double-helical DNA determined by fitting calculated melting profiles to observed profiles. Biopolymers 20, 1033-1042.
29. Hagerman, P. J. 1988 Flexibility of DNA. A. Rev. Biophys. Biophys. Chem. 17, 265-286.
30. Hatfield, W. E. & Benham, C. J. 2002 DNA topology-mediated control of global gene expression in Escherichia coli. A. Rev. Genet. 36, 175-203.
31. Hayes, J. J., Tullius, T. D. & Wolffe, A. P. 1990 The structure of DNA in a nucleosome. Proc. Natl Acad. Sci. USA 87, 7405-7409.
32. Hogan, M. & Austin, R. H. 1987 Importance of DNA stiffness in protein-DNA binding specificity. Nature 329, 263-266.
33. Hogan, M., LeGrange, J. & Austin, R. H. 1983 Dependence of DNA helix flexibility on base composition. Nature 304, 752-754.
34. Hogan, M., Roberson, M. W. & Austin, R. H. 1989 DNA stiffness variation may dominate DNase I cleavage. Proc. Natl Acad. Sci. USA 86, 9273-9277.
35. Hunter, C. A. 1993 Sequence-dependent DNA structure. The role of base stacking interactions. J. Mol. Biol. 230, 1025-1054.
36. Hunter, C. A. 1996 Sequence-dependent DNA structure. Bioessays 18, 157-162.
37. Koo, H.-S., Wu, H.-M. & Crothers, D. M. 1986 DNA bending at adenine-thymine tracts. Nature 320, 501-506.
38. Lowary, P. T. & Widom, J. 1998 New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J. Mol. Biol. 276, 19-42.
39. Luger. K., Mäder, A. W., Richmond, R. K., Sargent, D. F. & Richmond, T. J. 1997 Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389, 251-260.
40. Neugebauerova, S. & Kypr, J. 2000 Invariant and variable base stacking geometries in B-DNA and A-DNA. J. Biomol. Struct. Dynam. 18, 73-81.
41. Pedersen, A. G., Jensen, L. J., Brunak, S., Staerfeldt, H. H. & Ussery, D. W. 2000 A DNA structural atlas for Escherichia coli. J. Mol. Biol. 290, 907-930.
42. Rhodes, D. 1979 Nucleosome cores reconstituted from poly (dA-dT) and the octamer of histones. Nucleic Acids Res. 6, 1805-1816.
43. Richmond, T. J. & Davey, C. A. 2003 The structure of DNA in the nucleosome core. Nature 423, 145-150.
44. Rochman, M., Aviv, M., Glaser, G. & Muskhelishvili, G. 2002 Promoter protection by a transcription factor acting as a local topological homeostat. EMBO Rep. 3, 335-360.
45. Roychoudhury, M., Sitlani, A., Lapham, J. & Crothers, D. M. 2000 Global structure and mechanical properties of a 10-bp nucleosome positioning motif. Proc. Natl Acad. Sci. USA 97, 13 608-13613.
46. SantaLucia Jr, J. 1998 A unified view of polymer, dumbbell and oligonucleotide nearest-neighbor thermodynamics. Proc. Natl Acad. Sci. USA 95, 1460-1465.
47. Satchwell, S. C., Drew, H. R. & Travers, A. A. 1986 Sequence periodicities in chicken nucleosome core DNA. J. Mol. Biol. 191, 659-575.
48. Shore, D. & Baldwin, R. L. 1983 Energetics of DNA twisting. J. Mol. Biol. 170, 957-1007.
49. Shrader, T. E. & Crothers, D. M. 1990 Effects of DNA sequence and histone-histone interactions on nucleosome placement. J. Mol. Biol. 216, 69-84.
50. Sivolob, A. V. & Khrapunov, S. N. 1995 Translational positioning of nucleosomes on DNA: the role of sequence-dependent Isotropic bending stiffness. J. Mol. Biol. 247, 918-931.
51. + on the persistence length and excluded volume of T7 bacteriophage DNA. Biopolymers 31, 1559-1564.
52. Taylor, W. H. & Hagerman, P. J. 1990 Application of the method of phage T4 DNA ligase-catalysed ring-closure to the study of DNA structure. II. NaCl-dependence of DNA flexibility. and helical repeat. J. Mol. Biol. 212, 363-376.
53. Thåström, A., Lowary, P. T., Widlund, H. R., Cao, H., Kubista, M. & Widom, J. 1999 Sequence motifs and free energies of selected natural and non-natural nucleosome positioning DNA sequences. J. Mol. Biol. 288, 213-229.
54. Travers, A. A. & Klug, A. 1987 The bending of DNA in nucleosomes and its wider implications. Phil. Trans. R. Soc. Lond. B 317, 537-561.
55. Virstedt, J., Berge, T., Henderson, R. M., Waring, M. J. & Travers, A. A. 2004 The exocyclic purine 2-amino group influences the stiffness of the DNA double helix. J. Struct. Biol. (In the press.)
56. Vologodskii, A. V., Amirikyan, B. R., Lyubchenko, Y. L. & Frank-Kamenetskii, M. D. 1984 Allowance for heterogeneous stacking in the DNA helix-coli transition theory. J. Biomol. Struct. Dynam. 2, 131-148.
57. Wang, Y. H. & Griffith, J. 1995 Expanded CTG triplet blocks from the myotonic dystrophy gene create the strongest known natural nucleosome positioning elements. Genomics 25, 570-573.
58. Widlund, H. R., Kuduvalli, P. N., Bengtsson, M., Cao, H., Tullius, T. D. & Kubista, M. 1999 Nucleosome structural features and intrinsic properties of the TATAAACGCC repeat sequence. J. Biol. Chem. 274, 31847-31852.
59. Widom, J. 1996 Short-range order in two eukaryotic genomes: relation to chromosome structure. J. Mol. Biol. 259, 579-588.
60. Yanagi, K., Privé, G. G. & Dickerson, R. E. 1991 Analysis of local helix geometry in three B-DNA decamers and eight dodecamers. J. Mol. Biol. 217, 201-214.
61. Young, M. A., Ravishanker, G., Beveridge, D. L. & Berman, H. M. 1995 Analysis of local helix bending in crystal structures of DNA oligonucleotides and DNA-protein complexes. Biophys. J. 68, 2454-2468.