DNA structure, nucleosome placement and chromatin remodelling: A perspective

Biochemical Society Transactions

Volumn 40, Issue 2, 2012, Pages 335-340

  Travers, Andrew A ^a,b   Vaillant, Cédric ^c   Arneodo, Alain ^c   Muskhelishvili, Georgi ^d  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b Department of Biochemistry ^*  (United Kingdom)

^c Laboratoire Joliot Curie   (France)

^d JACOBS UNIVERSITY BREMEN   (Germany)

Author keywords

Chromatin; DNA structure; Histone; Nucleosome; Octamer

Indexed keywords

DNA;

CHROMATIN; DNA SEQUENCE; DNA STRUCTURE; EUKARYOTE; GENE; GENOME; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; REVIEW; THERMODYNAMICS; YEAST;

CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOME POSITIONING; DNA; GENES; NUCLEOSOMES;

EUKARYOTA; SACCHAROMYCETALES;

EID: 84859329057     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20110757     Document Type: Review

References (51)

1. Travers, A.A, Muskhelishvili, G. and Thompson, J.M.T. (2012) DNA information: from digital code to analogue structure. Philos. Trans. R. Soc. London Ser. A, in the press
2. Buttinelli, M., Minnock, A., Panetta, G., Waring, M. and Travers, A. (1998) The exocyclic groups of DNA modulate the affinity and positioning of the histone octamer. Proc. Natl. Acad. Sci. U.S.A. 95, 8544-8549
3. Satchwell, S.C., Drew, H.R. and Travers, A.A. (1986) Sequence periodicities in chicken nucleosome core DNA. J. Mol. Biol. 191, 659-675
4. Segal, E., Fondufe-Mittendorf, Y., Chen, L., Thåström, A., Field, Y., Moore, I.K., Wang, J.P. and Widom, J. (2006) A genomic code for nucleosome positioning. Nature 442, 772-778 (Pubitemid 44258903)
5. Luger, K., Mäder, A.W., Richmond, R.K., Sargent, D.F. and Richmond, T.J. (1997) Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389, 301-311
6. Rohs, R., West, S.M., Sosinsky, A., Liu, P., Mann, R.S. and Honig, B. (2009) The role of DNA shape in protein-DNA recognition. Nature 461, 1248-1253
7. Thåström, A., Lowary, P.T., Widlund, H.R., Cao, H., Kubista, M. and Widom, J. (1999) Sequence motifs and free energies of selected natural and non-natural nucleosome positioning DNA sequences. J. Mol. Biol. 288, 213-229
8. Caserta, M., Agricola, E., Churcher, M., Hiriart, E., Verdone, L., Di Mauro, E. and Travers, A. (2009) A translational signal for nucleosome positioning in vivo. Nucleic Acids Res. 37, 5309-5321
9. Lowary, P.T. and 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
10. Wu, C. and Travers, A. (2005) Relative affinities of DNA sequences for the histone octamer depend strongly upon both the temperature and octamer concentration. Biochemistry 44, 14329-14334 (Pubitemid 41533057)
11. Kaplan, N., Moore, I.K., Fondufe-Mittendorf, Y., Gossett, A.J., Tillo, D., Field, Y., Leproust, E.M., Hughes, T.R., Lieb, J.D., Widom, J. et al. (2008) The DNA-encoded nucleosome organization of a eukaryotic genome. Nature 458, 362-366
12. Virstedt, J., Berge, T., Henderson, R.M., Waring, M.J. and Travers, A.A. (2004) The influence of DNA stiffness upon nucleosome formation. J. Struct. Biol. 148, 66-85
13. Nelson, H.C., Finch, J.T., Luisi, B.F. and Klug, A. (1987) The structure of an oligo(dA)?oligo(dT) tract and its biological implications. Nature 330, 221-226 (Pubitemid 18006417)
14. Protozanova, E., Yakovchuk, P. and Frank-Kamenetskii, M.D. (2004) Stacked-unstacked equilibrium at the nick site of DNA. J. Mol. Biol. 342, 775-785
15. Olson, W.K., Clasanti, A.V., Czapla, L. and Zheng, G. (2008) Insights into the sequence-dependent macromolecular properties of DNA from base-pair level modeling. In Coarse-Graining of Condensed Phase and Biomolecular Systems (Voth, G.A., ed.), pp. 205-223, CRC Press, Boca Raton
16. Visnapuu, M.L. and Greene, E.C. (2009) Single-molecule imaging of DNA curtains reveals intrinsic energy landscapes for nucleosome deposition. Nat. Struct. Mol Biol. 16, 1056-1062
17. Chung, H.R. and Vingron, M. (2009) Sequence-dependent nucleosome positioning. J. Mol. Biol. 388, 1411-1422
18. Mavrich, T.N., Ioshikhes, I.P., Venters, B.J., Jiang, C., Tomsho, L.P., Qi, J., Schuster, S.C., Albert, I. and Pugh, B.F. (2008) A barrier nucleosome model for statistical positioning of nucleosomes throughout the yeast genome. Genome Res. 18, 1073-1083 (Pubitemid 351931158)
19. Lee, W., Tillo, D., Bray, N., Morse, R.H., Davis, R.W., Hughes, T.R. and Nislow, C. (2007) A high-resolution atlas of nucleosome occupancy in yeast. Nat. Genet. 39, 1235-1244
20. Milani, P., Chevereau, G., Vaillant, C., Audit, B., Haftek-Terreau, Z., Marilley, M., Bouvet, P., Argoul, F. and Arneodo, A. (2009) Nucleosome positioning by genomic excluding-energy barriers. Proc. Natl. Acad. Sci. U.S.A. 106, 22257-22262
21. Miele, V., Vaillant, C., d'Aubenton-Carafa, Y., Thermes, C. and Grange, T. (2008) DNA physical properties determine nucleosome occupancy from yeast to fly. Nucleic Acids Res. 36, 3746-3756
22. Olson, W.K. and Zhurkin, V.B. (2011) Working the kinks out of nucleosomal DNA. Curr. Opin. Struct. Biol. 21, 348-357
23. Richmond, T.J. and Davey, C.A. (2003) The structure of DNA in the nucleosome core. Nature 423, 145-150 (Pubitemid 36569532)
24. Ong, M.S., Richmond, T.J. and Davey, C.A. (2007) DNA stretching and extreme kinking in the nucleosome core. J. Mol. Biol. 368, 1067-1074
25. Makde, R.D., England, J.R., Yennawar, H.P. and Tan, S. (2010) Structure of the RCC1 chromatin factor bound to the nucleosome core particle. Nature 467, 562-566
26. Li, B., Carey, C. and Workman, J. (2007) The role of chromatin during transcription. Cell 128, 707-719 (Pubitemid 46273570)
27. Luco, R.F. and Misteli, T. (2011) More than a splicing code: integrating the role of RNA, chromatin and non-coding RNA in alternative splicing regulation. Curr. Opin. Genet. Dev. 21, 366-372
28. Almer, A., Rudolph, H., Hinnen, A. and Hörz, W. (1986) Removal of positioned nucleosomes from the yeast PHO5 promoter upon PHO5 induction releases additional upstream activating DNA elements. EMBO J. 5, 2689-2696
29. Verdone, L., Camilloni, G., Di Mauro, E. and Caserta, M. (1996) Chromatin remodeling during Saccharomyces cerevisiae ADH2 gene activation. Mol. Cell. Biol. 16, 1978-1988
30. Anderson, J.D. and Widom, J. (2000) Sequence and position-dependence of the equilibrium accessibility of nucleosomal DNA target sites. J. Mol. Biol. 296, 979-987
31. Li, G., Leviticus, M., Bustamante, C. and Widom, J. (2005) Rapid spontaneous accessibility of nucleosomal DNA. Nat. Struct. Mol. Biol. 12, 46-53
32. Tims, H.S., Gurunathan, K., Levitus, M. and Widom, J. (2011) Dynamics of nucleosome invasion by DNA binding proteins. J. Mol. Biol. 411, 430-448
33. Losa, R., Omari, S. and Thoma, F. (1990) Poly(dA)?poly(dT) rich sequences are not sufficient to exclude nucleosome formation in a constitutive yeast promoter. Nucleic Acids Res. 18, 3495-3502
34. Travers, A.A. and Klug, A. (1987) The bending of DNA in nucleosomes and its wider implications. Philos. Trans. R. Soc. London Ser. B 317, 537-561
35. Thomas, J.O. and Travers, A.A. (2001) HMG1 and 2 and related 'architectural' DNA-binding proteins. Trends Biochem. Sci. 27, 168-175
36. Ragab, A. and Travers, A. (2003) HMG-D and histone H1 alter the local accessibility of nucleosomal DNA. Nucleic Acids Res. 21, 7083-7089 (Pubitemid 38008441)
37. Cato, L., Stott, K., Watson, M. and Thomas, J.O. (2008) The interaction of HMGB1 and linker histones occurs through their acidic and basic tails. J. Mol. Biol. 384, 1262-1272
38. Kawase, T., Sato, K., Ueda, T. and Yoshida, M. (2008) Distinct domains in HMGB1 are involved in specific intramolecular and nucleosomal interactions. Biochemistry 47, 13991-13996
39. Bonaldi, T., La?ngst, G., Strohner, R., Becker, P.B. and Bianchi, M.E. (2002) The DNA chaperone HMGB1 facilitates ACF/CHRAC-dependent nucleosome sliding. EMBO J. 21, 6865-6873
40. Ragab, A., Thompson, E. and Travers, A. (2006) HmgD and HmgZ interact genetically with the Brahma chromatin remodeling complex in Drosophila. Genetics 172, 1069-1078 (Pubitemid 43345439)
41. Lantermann, A.B., Straub, T., Str?fors, A., Yuan, G.C., Ekwall, K. and Korber, P. (2010) Schizosaccharomyces pombe genome-wide nucleosome mapping reveals positioning mechanisms distinct from those of Saccharomyces cerevisiae. Nat. Struct. Mol. Biol. 17, 251-257
42. Cole, H.A., Howard, B.H. and Clark, D.J. (2011) The centromeric nucleosome of budding yeast is perfectly positioned and covers the entire centromere. Proc. Natl. Acad. Sci. U.S.A. 108, 12687-12692
43. Zhang, Z., Wippo, C.J., Wal, M., Ward, E., Korber, P. and Pugh, B.F. (2011) A packing mechanism for nucleosome organization reconstituted across a eukaryotic genome. Science 332, 977-980
44. Wippo, C.J., Israel, L., Watanabe, S., Hochheimer, A., Peterson, C.L. and Korber, P. (2011) The RSC chromatin remodelling enzyme has a unique role in directing the accurate positioning of nucleosomes. EMBO J. 30, 1277-1288
45. Zhang, Y., Moqtaderi, Z., Rattner, B.P., Euskirchen, G., Snyder, M. and Struhl, K. (2009) Intrinsic histone-DNA interactions are not the major determinant of nucleosome positions in vivo. Nat. Struct. Mol. Biol. 16, 847-852
46. Xella, B., Goding, C., Agricola, E., Di Mauro, E. and Caserta, M. (2006) The ISWI and CHD1 chromatin remodelling activities influence ADH2 expression and chromatin organization. Mol. Microbiol. 59, 1531-1541
47. Teif, V.B. and Rippe, K. (2009) Predicting nucleosome positions on the DNA: combining intrinsic sequence preferences and remodeler activities. Nucleic Acids Res. 37, 5641-5655
48. Kornberg, R.D. and Stryer, L. (1988) Statistical distributions of nucleosomes: nonrandom locations by a stochastic mechanism. Nucleic Acids Res. 16, 6677-6690
49. Lange, S.S., Mitchell, D.L. and Vasquez, K.M. (2008) High mobility group protein B1 enhances DNA repair and chromatin modification after DNA damage. Proc. Natl. Acad. Sci. U.S.A. 105, 10320-10325
50. Travers, A.A and Muskhelishvili, G. (2005) DNA supercoiling: a global transcriptional regulator for enterobacterial growth. Nat. Rev. Microbiol. 3, 157-169
51. Schrödinger, E. (1944) What is Life? Cambridge University Press, Cambridge