DNA thermodynamics shape chromosome organization and topology

Biochemical Society Transactions

Volumn 41, Issue 2, 2013, Pages 548-553

  Travers, Andrew A ^a,b   Muskhelishvili, Georgi ^c  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b Department of Biochemistry ^*  (United Kingdom)

^c JACOBS UNIVERSITY BREMEN   (Germany)

Author keywords

Chromatin; Chromosome organization; Chromosome topology; DNA thermodynamics; DNA translocase; Superhelicity

Indexed keywords

DNA;

ARTICLE; BACTERIAL GENOME; CHROMATIN; CHROMOSOME STRUCTURE; DNA REPLICATION; DNA SEQUENCE; FUNGAL GENOME; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; THERMODYNAMICS; YEAST;

CHROMOSOMES; DNA; GENOME, BACTERIAL; GENOME, FUNGAL; NUCLEIC ACID CONFORMATION; THERMODYNAMICS;

EID: 84875398745     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20120334     Document Type: Article

References (48)

1. Muskhelishvili, G., Sobetzko, P., Geertz, M. and Berger, M. (2010) General organisational principles of the transcriptional regulation system: a tree or a circleMol. Biosyst. 6, 662-676
2. Cozzarelli, N.R., Boles, T.C. and White, J.H. (1990) Primer on the topology and geometry of DNA supercoiling. In DNA topology and its biological effects (Cozzarelli, N.R. and Wang, J.C., eds), pp. 185-215, Cold Spring Harbor Laboratory Press, Cold Spring Harbor
3. Drew, H.R., Weeks, J.R. and Travers, A.A. (1985) Negative supercoiling induces spontaneous unwinding of a bacterial promoter. EMBO J. 4, 1025-1032
4. Travers, A. and Muskhelishvili, G. (2005) DNA supercoiling: a global transcriptional regulator of enterobacterial growth. Nat. Rev. Microbiol. 3, 157-169
5. Muskhelishvili, G. and Travers, A. (2013) DNA structure and bacterial nucleoid-Associated proteins. In Bacterial Gene Regulation and Transcriptional Networks (Babu, M.M., ed.), Caister Academic Press, Norwich, in the press
6. Rimsky, S. and Travers, A. (2011) Pervasive regulation of nucleoid structure and function by nucleoid-Associated proteins. Curr. Opin. Microbiol. 14, 136-141
7. Browning, D.F., Grainger, D.C. and Busby, S.J. (2010) Effects of nucleoid-Associated proteins on bacterial chromosome structure and gene expression. Curr. Opin. Microbiol. 13, 773-780
8. Liu, L.F. and Wang, J.C (1987) Supercoiling of the DNA template during transcription. Proc. Natl. Acad. Sci. U.S.A. 84, 7024-7027
9. Levens, D. and Benham, C.J (2011) DNA stress and strain, in silico, in vitro and in vivo. Phys. Biol. 8, 035011
10. Mace, H.A.F., Pelham, H.R.B. and Travers, A.A. (1983) Association of an S1 nuclease-sensitive structure with short direct repeats 5-of Drosophila heat shock genes. Nature 304, 555-557
11. Wong, H.M. and Huppert, J.L. (2009) Stable G-quadruplexes are found outside nucleosome-bound regions. Mol. Biosyst. 5, 1713-1719
12. Kouzine, F., Sanford, S., Elisha-Feil, Z. and Levens, D. (2008) The functional response of upstream DNA to dynamic supercoiling in vivo. Nat. Struct. Mol. Biol. 15, 146-54
13. Maurer, S., Fritz, J., Muskhelishvili, G. and Travers, A. (2006) RNA polymerase and an activator form discrete subcomplexes in a transcription initiation complex. EMBO J. 25, 3784-3790
14. Pemberton, I.K., Muskhelishvili, G., Travers, A.A. and Buckle, M. (2002) FIS modulates the kinetics of successive interactions of RNA polymerase with the core and upstream regions of the tyrT promoter. J. Mol. Biol. 318, 615-613
15. Sobetzko, P., Travers, A. and Muskhelishvili, G. (2012) Gene order and chromosome dynamics coordinate spatiotemporal gene expression during the bacterial growth cycle. Proc. Natl. Acad. Sci. U.S.A. 109, E49-E50
16. Blot, N., Mavathur, R., Geertz, M., Travers, A. and Muskhelishvili, G. (2006) Homeostatic regulation of supercoiling sensitivity coordinates transcription of the bacterial genome. EMBO Rep. 7, 710-715
17. Kusano, S., Ding, Q., Fujita, N. and Ishihama, A. (1996) Promoter selectivity of Escherichia coli RNA polymerase Eσ70 and Eσ38 holoenzymes: effect of DNA supercoiling. J. Biol. Chem. 271, 1998-2004
18. van Workum, M., van Dooren, S.J., Oldenburg, N., Molenaar, D., Jensen, P.R., Snoep, J.L and Westerhoff, H.V (1996) DNA supercoiling depends on the phosphorylation potential in Escherichia coli. Mol. Microbiol. 20, 351-360
19. Zechiedrich, E.L., Khodursky, A.B., Bachellier, S., Schneider, R., Chen, D., Lilley, D.M.J. and Cozzarelli, N,R. (2000) Role of topoisomerases in maintaining steady-state DNA supercoiling in Escherichia coli. J. Biol. Chem. 275, 8103-8113
20. Bordes, P., Conter, A., Morales, V., Bouvier, J., Kolb, A. and Gutierrez, C. (2003) DNA supercoiling contributes to disconnect σS accumulation from σS-dependent transcription in Escherichia coli. Mol. Microbiol. 48, 561-571
21. Berger, M., Farcas, A., Geertz, M., Zhelyazkova, P., Brix, K., Travers, A. and Muskhelishvili, G. (2010) Coordination of genomic structure and function by the main bacterial nucleoid-Associated protein HU. EMBO Rep. 11, 59-64
22. Swinger, K.K. and Rice, P.A. (2004) IHF and HU: flexible architects of bent DNA. Curr. Opin. Struct. Biol. 14, 28-35
23. Guo, F. and Adhya, S. (2007) Spiral structure of Escherichia coli HUαβ provides foundation for DNA supercoiling. Proc. Natl. Acad. Sci. U.S.A. 104, 4309-4314
24. Travers, A.A, Muskhelishvili, G. and Thompson, J.M.T. (2012) DNA information: from digital code to analogue structure. Phil. Trans. R. Soc. London Ser. A 370, 2960-2986
25. Ball, C.A., Osuna, R., Ferguson, K.C. and Johnson, R.C. (1992) Dramatic changes in Fis levels upon nutrient upshift in Escherichia coli. J. Bacteriol. 174, 8043-8056
26. Schneider, R., Lurz, R., Tolksdorf, C., Luder, G., Travers, A. and Muskhelishvili, G. (2001) An architectural role of the Escherichia coli chromatin protein FIS in organising DNA. Nucleic Acids Res. 29, 5107-5114
27. Maurer, S., Fritz, J. and Muskhelishvili, G. (2009) A systematic in vitro study of nucleoprotein complexes formed by bacterial nucleoid associated proteins revealing novel types of DNA organization. J. Mol. Biol. 387, 1261-1276
28. Travers, A., Baillie, D.L. and Pedersen, S. (1973) The effect of DNA conformation on ribosomal RNA synthesis. Nat. New Biol. 243, 161-163
29. Auner, H., Buckle, M., Deufel, A., Kutateladze, T., Lazarus, L., Mavathur, R., Muskhelishvili, G., Pemberton, I., Schneider, R. and Travers, A. (2003) Mechanism of transcriptional activation by FIS: role of core promoter structure and DNA topology. J. Mol. Biol. 331, 331-344
30. Navarre, W.W., Porwollik, S., Wang, Y., McClelland, M., Rosen, H., Libby, S.J. and Fang, F.C (2006) Selective silencing of foreign DNA with low GC content by the H-NS protein in Salmonella. Science 313, 236-238
31. Dillon, S.C. and Dorman, C.J. (2010) Bacterial nucleoid-Associated proteins, nucleoid structure and gene expression. Nat. Rev. Microbiol. 8, 185-195
32. Bouffartigues, E., Buckle, M., Baudaut, C., Travers, A. and Rimsky, S. (2007) High affinity sites direct the cooperative binding of H-NS to a regulatory element required for transcriptional silencing. Nat. Struct. Mol. Biol. 14, 441-448
33. Lang, B., Blot, N., Bouffartigues, E., Buckle, M., Geertz, M., Gualerzi, C.O., Mavathur, R., Muskhelishvili, G., Pon, C., Rimsky, S. et al. (2007) High affinity DNA binding sites for H-NS provide a molecular basis for selective silencing within proteobacterial genomes. Nucleic Acids Res. 34, 6330-6337
34. Travers, A.A., Vaillant, C., Arneodo, A. and Muskhelishvili, G. (2012) DNA structure, nucleosome placement and chromatin remodelling: a perspective. Biochem. Soc. Trans. 40, 335-340
35. Burden, D.A. and Osheroff, N. (1999) In vitro evolution of preferred topoisomerase II DNA cleavage sites. J. Biol. Chem. 274, 5227-5223
36. Gasser, S.M., Laroche, T., Falquet, J., Boy de la Tour, E. and Laemmli, U.K. (1986) Metaphase chromosome structure. Involvement of topoisomerase II. J. Mol. Biol. 188, 613-629
37. Umbarger, M.A., Toro, E., Wright, M.A., Porreca, G.J., Baú, D., Hong, S.H., Fero, M.J., Zhu, L.J., Marti-Renom, M.A., McAdams, H.H. et al. (2011) The three-dimensional architecture of a bacterial genome and its alteration by genetic perturbation. Mol. Cell 44, 252-264
38. Segal, E. and Widom, J (2009) Poly(dA:dT) tracts: major determinants of nucleosome organization. Curr. Opin. Struct. Biol. 19, 65-71
39. Whitehouse, I. and Tsukiyama, T. (2006) Antagonistic forces that position nucleosome in vivo. Nat. Struct. Mol. Biol. 13, 633-640
40. Moshkin, Y.M., Chalkley, G.E., Kan, T.W., Reddy, B.A., Ozgur, Z., van Ijcken, W.F.J., Dekkers, D.H.W., Demmers, J.A., Travers, A.A. and Verrijzer, C.P. (2012) Remodelers organize cellular chromatin by counteracting intrinsic histone-DNA sequence preferences in a class-specific manner. Mol. Cell. Biol. 32, 675-688
41. Hughes, A.L., Jin, Y., Rando, O.J. and Struhl, K (2012) A functional evolutionary approach to identify determinants of nucleosome positioning: a unifying model for establishing the genome-wide pattern. Mol. Cell 48, 5-15
42. Arneodo, A., Vaillant, C., Audit, B., Argoul, F., d'Aubenton-Carafa, Y. and Thermes, C. (2011) Multi-scale coding of genetic information: from DNA sequence to genome structure and function. Phys. Rep. 498, 45-188
43. van der Heijden, T., van Vugt, J.J., Logie, C. and van Noort, J (2012) Sequence-based prediction of single nucleosome positioning and genome-wide nucleosome occupancy. Proc. Natl. Acad. Sci. U.S.A. 109, E2514-E2522
44. Chereji, R.V. and Morozov, A.V (2011) Statistical mechanics of nucleosomes constrained by higher-order chromatin structure. J. Stat. Phys. 144, 379-404
45. 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
46. 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
47. Brogaard, K., Xi, L., Wang, J.-P. and Widom, J. (2012) A map of nucleosome positions in yeast at base-pair resolution. Nature 486, 496-501
48. Studitsky, V.M., Clark, D.J. and Felsenfeld, G. (1994) A histone octamer can step around a transcribing polymerase without leaving the template. Cell 76, 371-382