Genome scale patterns of supercoiling in a bacterial chromosome

Nature Communications

Volumn 7, Issue , 2016, Pages

  Lal, Avantika ^a   Dhar, Amlanjyoti ^b   Trostel, Andrei ^b   Kouzine, Fedor ^b   Seshasayee, Aswin S N ^a   Adhya, Sankar ^b  

^a TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA TOPOISOMERASE (ATP HYDROLYSING); HU PROTEIN; TRIMETHYLPSORALEN; BACTERIAL PROTEIN; DNA SUPERCOILING; HYDROXYUREA; PROTEIN BINDING; PSORALEN;

BACTERIUM; CELLS AND CELL COMPONENTS; CHROMOSOME; DNA; GENE EXPRESSION; GENOME; GROWTH RATE; PHENOLIC COMPOUND; PROTEIN;

ANIMAL CELL; ARTICLE; BACTERIAL CELL; BACTERIAL CHROMOSOME; BACTERIAL GENOME; CELL GROWTH; CONTROLLED STUDY; DNA CROSS LINKING; DNA MICROARRAY; DNA REPLICATION ORIGIN; DNA SUPERCOILING; ESCHERICHIA COLI; GENE DELETION; GROWTH CURVE; INTERCALATION COMPLEX; NONHUMAN; DRUG EFFECTS; GENETIC TRANSCRIPTION; GENETICS; METABOLISM;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

BACTERIAL PROTEINS; CHROMOSOMES, BACTERIAL; DNA GYRASE; DNA, SUPERHELICAL; ESCHERICHIA COLI; FICUSIN; GENOME, BACTERIAL; HYDROXYUREA; PROTEIN BINDING; TRANSCRIPTION, GENETIC;

EID: 84962473633     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms11055     Document Type: Article

References (54)

1. Bauer, W. R. Structure and reactions of closed duplex DNA. Annu. Rev. Biophys. Bioeng. 7, 287-313 (1978).
2. Botchan, P., Wang, J. C. & Echols, H. Effect of circularity and superhelicity on transcription from bacteriophagelambda DNA. Proc. Natl Acad. Sci. USA 70, 3077-3081 (1973).
3. Holloman, W. K. & Radding, C. M. Recombination promoted by superhelical DNA and the recA gene of Escherichia coli. Proc. Natl Acad. Sci. USA 73, 3910-3914 (1976).
4. Mizuuchi, K., O'Dea, M. H. & Gellert, M. DNA gyrase: subunit structure and ATPase activity of the purified enzyme. Proc. Natl Acad. Sci. USA 75, 5960-5963 (1978).
5. Smith, D. H. & Davis, B. D. Mode of action of novobiocin in Escherichia coli. J. Bacteriol. 93, 71-79 (1967).
6. Smith, C. L., Kubo, M. & Imamoto, F. Promoter-specific inhibition of transcription by antibiotics which act on DNA gyrase. Nature 275, 420-423 (1978).
7. Tsao, Y. P., Wu, H. Y. & Liu, L. F. Transcription-driven supercoiling of DNA: direct biochemical evidence from in vitro studies. Cell 56, 111-118 (1989).
8. Wu, H. Y., Shyy, S. H., Wang, J. C. & Liu, L. F. Transcription generates positively and negatively supercoiled domains in the template. Cell 53, 433-440 (1988).
9. Ali Azam, T., Iwata, A., Nishimura, A., Ueda, S. & Ishihama, A. Growth phasedependent variation in protein composition of the Escherichia coli nucleoid. J. Bacteriol. 181, 6361-6370 (1999).
10. Dixon, N. E. & Kornberg, A. Protein HU in the enzymatic replication of the chromosomal origin of Escherichia coli. Proc. Natl Acad. Sci. USA 81, 424-428 (1984).
11. Claret, L. & Rouviere-Yaniv, J. Variation in HU composition during growth of Escherichia coli: the heterodimer is required for long term survival. J. Mol. Biol. 273, 93-104 (1997).
12. Guo, F. & Adhya, S. Spiral structure of Escherichia coli HUalphabeta provides foundation for DNA supercoiling. Proc. Natl Acad. Sci. USA 104, 4309-4314 (2007).
13. Rouviere-Yaniv, J., Yaniv, M. & Germond, J. E. E. coli DNA binding protein HU forms nucleosomelike structure with circular double-stranded DNA. Cell 17, 265-274 (1979).
14. Hardy, C. D. & Cozzarelli, N. R. A genetic selection for supercoiling mutants of Escherichia coli reveals proteins implicated in chromosome structure. Mol. Microbiol. 57, 1636-1652 (2005).
15. Hsieh, L. S., Rouviere-Yaniv, J. & Drlica, K. Bacterial DNA supercoiling and [ATP]/[ADP] ratio: changes associated with salt shock. J. Bacteriol. 173, 3914-3917 (1991).
16. Malik, M., Bensaid, A., Rouviere-Yaniv, J. & Drlica, K. Histone-like protein HU and bacterial DNA topology: suppression of an HU deficiency by gyrase mutations. J. Mol. Biol. 256, 66-76 (1996).
17. Higgins, C. F. et al. A physiological role for DNA supercoiling in the osmotic regulation of gene expression in S. typhimurium and E. coli. Cell 52, 569-584 (1988).
18. Tupper, A. E. et al. The chromatin-associated protein H-NS alters DNA topology in vitro. EMBO J. 13, 258-268 (1994).
19. Schneider, R., Travers, A. & Muskhelishvili, G. FIS modulates growth phase-dependent topological transitions of DNA in Escherichia coli. Mol. Microbiol. 26, 519-530 (1997).
20. Schneider, R., Travers, A., Kutateladze, T. & Muskhelishvili, G. A DNA architectural protein couples cellular physiology and DNA topology in Escherichia coli. Mol. Microbiol. 34, 953-964 (1999).
21. Balke, V. L. & Gralla, J. D. Changes in the linking number of supercoiled DNA accompany growth transitions in Escherichia coli. J. Bacteriol. 169, 4499-4506 (1987).
22. Hsieh, L. S., Burger, R. M. & Drlica, K. Bacterial DNA supercoiling and [ATP]/ [ADP]. Changes associated with a transition to anaerobic growth. J. Mol. Biol. 219, 443-450 (1991).
23. Cheung, K. J., Badarinarayana, V., Selinger, D. W., Janse, D. & Church, G. M. A microarray-based antibiotic screen identifies a regulatory role for supercoiling in the osmotic stress response of Escherichia coli. Genome Res. 13, 206-215 (2003).
24. McClellan, J. A., Boublíková, P., Palecek, E. & Lilley, D. M. Superhelical torsion in cellular DNA responds directly to environmental and genetic factors. Proc. Natl Acad. Sci. USA 87, 8373-8377 (1990).
25. Goldstein, E. & Drlica, K. Regulation of bacterial DNA supercoiling: plasmid linking numbers vary with growth temperature. Proc. Natl Acad. Sci. USA 81, 4046-4050 (1984).
26. Blot, N., Mavathur, R., Geertz, M., Travers, A. & Muskhelishvili, G. Homeostatic regulation of supercoiling sensitivity coordinates transcription of the bacterial genome. EMBO Rep. 7, 710-715 (2006).
27. Peter, B. J. et al. Genomic transcriptional response to loss of chromosomal supercoiling in Escherichia coli. Genome Biol. 5, R87 (2004).
28. Lange, R. & Hengge-Aronis, R. Identification of a central regulator of stationary-phase gene expression in Escherichia coli. Mol. Microbiol. 5, 49-59 (1991).
29. Kusano, S., Ding, Q., Fujita, N. & Ishihama, A. Promoter selectivity of Escherichia coli RNA polymerase E sigma 70 and E sigma 38 holoenzymes. Effect of DNA supercoiling. J. Biol. Chem. 271, 1998-2004 (1996).
30. Ohlsen, K. L. & Gralla, J. D. Interrelated effects of DNA supercoiling, ppGpp, and low salt on melting within the Escherichia coli ribosomal RNA rrnB P1 promoter. Mol. Microbiol. 6, 2243-2251 (1992).
31. Sobetzko, P., Travers, A. & Muskhelishvili, G. Gene order and chromosome dynamics coordinate spatiotemporal gene expression during the bacterial growth cycle. Proc. Natl Acad. Sci. USA 109, E42-E50 (2012).
32. Cole, R. S. Psoralen monoadducts and interstrand cross-links in DNA. Biochim. Biophys. Acta 254, 30-39 (1971).
33. Musajo, L., Bordin, F., Caporale, G., Marciani, S. & Rigatti, G. Photoreactions at 3655 Angstrom between pyrimidine bases and skin-photosensitizing furocoumarins. Photochem. Photobiol. 6, 711-719 (1967).
34. Hyde, J. E. & Hearst, J. E. Binding of psoralen derivatives to DNA and chromatin: influence of the ionic environment on dark binding and photoreactivity. Biochemistry 17, 1251-1257 (1978).
35. Bermúdez, I., García-Martínez, J., Pérez-Ortín, J. E. & Roca, J. A method for genome-wide analysis of DNA helical tension by means of psoralen-DNA photobinding. Nucleic Acids Res. 38, e182 (2010).
36. Sinden, R. R., Carlson, J. O. & Pettijohn, D. E. Torsional tension in the DNA double helix measured with trimethylpsoralen in living E. coli cells: analogous measurements in insect and human cells. Cell 21, 773-783 (1980).
37. Ljungman, M. & Hanawalt, P. C. Localized torsional tension in the DNA of human cells. Proc. Natl Acad. Sci. USA 89, 6055-6059 (1992).
38. Kouzine, F. et al. Transcription-dependent dynamic supercoiling is a shortrange genomic force. Nat. Struct. Mol. Biol. 20, 396-403 (2013).
39. Naughton, C. et al. Transcription forms and remodels supercoiling domains unfolding large-scale chromatin structures. Nat. Struct. Mol. Biol. 20, 387-395 (2013).
40. Gellert, M., Mizuuchi, K., O'Dea, M. H. & Nash, H. A. DNA gyrase: an enzyme that introduces superhelical turns into DNA. Proc. Natl Acad. Sci. USA 73, 3872-3876 (1976).
41. Jeong, K. S., Ahn, J. & Khodursky, A. B. Spatial patterns of transcriptional activity in the chromosome of Escherichia coli. Genome Biol. 5, R86 (2004).
42. Yang, Y. & Ames, G. F. DNA gyrase binds to the family of prokaryotic repetitive extragenic palindromic sequences. Proc. Natl Acad. Sci. USA 85, 8850-8854 (1988).
43. Cook, D. N., Ma, D., Pon, N. G. & Hearst, J. E. Dynamics of DNA supercoiling by transcription in Escherichia coli. Proc. Natl Acad. Sci. USA 89, 10603-10607 (1992).
44. Lim, C. J., Kenney, L. J. & Yan, J. Single-molecule studies on the mechanical interplay between DNA supercoiling and H-NS DNA architectural properties. Nucleic Acids Res. 42, 8369-8378 (2014).
45. Berger, M. et al. Coordination of genomic structure and transcription by the main bacterial nucleoid-associated protein HU. EMBO Rep. 11, 59-64 (2010).
46. Swinger, K. K., Lemberg, K. M., Zhang, Y. & Rice, P. A. Flexible DNA bending in HU-DNA cocrystal structures. EMBO J. 22, 3749-3760 (2003).
47. Zacher, B., Kuan, P. F. & Tresch, A. Starr: simple tiling ARRay analysis of affymetrix ChIP-chip data. BMC Bioinformatics 11, 194 (2010).
48. Keseler, I. M. et al. EcoCyc: fusing model organism databases with systems biology. Nucleic Acids Res. 41, D605-D612 (2013).
49. Kahramanoglou, C. et al. Direct and indirect effects of H-NS and Fis on global gene expression control in Escherichia coli. Nucleic Acids Res. 39, 2073-2091 (2011).
50. Prieto, A. I. et al. Genomic analysis of DNA binding and gene regulation by homologous nucleoid-associated proteins IHF and HU in Escherichia coli K12. Nucleic Acids Res. 40, 3524-3537 (2012).
51. Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows- Wheeler transform. Bioinforma. Oxf. Engl. 25, 1754-1760 (2009).
52. Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinforma. Oxf. Engl. 25, 2078-2079 (2009).
53. Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinforma. Oxf. Engl. 26, 841-842 (2010).
54. Valens, M., Penaud, S., Rossignol, M., Cornet, F. & Boccard, F. Macrodomain organization of the Escherichai coli chromosome. EMBO J 23, 4330-4341 (2004).