The genome-wide distribution of non-B DNA motifs is shaped by operon structure and suggests the transcriptional importance of non-B DNA structures in Escherichia coli

Nucleic Acids Research

Volumn 41, Issue 12, 2013, Pages 5965-5977

  Du, Xiangjun ^a   Wojtowicz, Damian ^a   Bowers, Albert A ^b   Levens, David ^c   Benham, Craig J ^d   Przytycka, Teresa M ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA;

ARTICLE; BACTERIAL GENOME; BINDING SITE; DNA BASE COMPOSITION; DNA DETERMINATION; DNA STRUCTURE; ESCHERICHIA COLI; GENETIC ANALYSIS; NON B DNA MOTIF; NONHUMAN; OPERON; PRIORITY JOURNAL; TRANSCRIPTION REGULATION; TRANSCRIPTION TERMINATION;

BINDING SITES; DNA, BACTERIAL; DNA, CRUCIFORM; DNA, INTERGENIC; ESCHERICHIA COLI; GENOME, BACTERIAL; NUCLEOTIDE MOTIFS; OPERON; PROMOTER REGIONS, GENETIC; REGULATORY ELEMENTS, TRANSCRIPTIONAL; TRANSCRIPTION FACTORS; TRANSCRIPTION TERMINATION, GENETIC; TRANSCRIPTION, GENETIC;

EID: 84880207699     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt308     Document Type: Article

References (82)

1. Watson, J.D. and Crick, F.H. (1953) Genetical implications of the structure of deoxyribonucleic acid. Nature, 171, 964-967.
2. Watson, J.D. and Crick, F.H. (1953) Molecular structure of nucleic acids; a structure for deoxyribose nucleic acid. Nature, 171, 737-738.
3. Mirkin, S.M. (2008) Discovery of alternative DNA structures: a heroic decade (1979-1989). Front. Biosci., 13, 1064-1071.
4. Wells, R.D. (1988) Unusual DNA structures. J. Biol. Chem., 263, 1095-1098.
5. Palecek, E. (1991) Local Supercoil-Stabilized DNA Structure. Crit. Rev. Biochem. Mol. Biol., 26, 151-226.
6. Travers, A. and Muskhelishvili, G. (2005) DNA supercoiling-a global transcriptional regulator for enterobacterial growth? Nat. Rev. Microbiol., 3, 157-169.
7. Kouzine, F. and Levens, D. (2007) Supercoil-driven DNA structures regulate genetic transactions. Front. Biosci., 12, 4409-4423.
8. Levens, D. and Benham, C.J. (2011) DNA stress and strain, in silico, in vitro and in vivo. Phys. Biol., 8, 035011.
9. Zhao, J., Bacolla, A., Wang, G. and Vasquez, K.M. (2010) Non-B DNA structure-induced genetic instability and evolution. Cell Mol. Life Sci., 67, 43-62.
10. Damas, J., Carneiro, J., Goncalves, J., Stewart, J.B., Samuels, D.C., Amorim, A. and Pereira, F. (2012) Mitochondrial DNA deletions are associated with non-B DNA conformations. Nucleic Acids Res., 40, 7606-7621.
11. Wells, R.D. (2007) Non-B DNA conformations, mutagenesis and disease. Trends Biochem. Sci., 32, 271-278.
12. Wells, R.D. (2009) Discovery of the role of Non-B DNA structures in mutagenesis and human genomic disorders. J. Biol. Chem., 284, 8997-9009.
13. Dai, X. and Rothman-Denes, L.B. (1999) DNA structure and transcription. Curr. Opin. Microbiol., 2, 126-130.
14. Rich, A., Nordheim, A. and Wang, A.H.J. (1984) The chemistry and biology of left-handed Z-DNA. Annu. Rev. Biochem., 53, 791-846.
15. Brooks, T.A. and Hurley, L.H. (2009) The role of supercoiling in transcriptional control of MYC and its importance in molecular therapeutics. Nat. Rev. Cancer, 9, 849-861.
16. Michelotti, G.A., Michelotti, E.F., Pullner, A., Duncan, R.C., Eick, D. and Levens, D. (1996) Multiple single-stranded cis elements are associated with activated chromatin of the human c-myc gene in vivo. Mol. Cell. Biol., 16, 2656-2669.
17. Kouzine, F., Liu, J., Sanford, S., Chung, H.J. and Levens, D. (2004) The dynamic response of upstream DNA to transcription-generated torsional stress. Nat. Struct. Mol. Biol., 11, 1092-1100.
18. 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, 146-154.
19. Sun, D. and Hurley, L.H. (2009) The Importance of Negative Superhelicity in Inducing the Formation of G-Quadruplex and i-Motif Structures in the c-Myc Promoter: Implications for Drug Targeting and Control of Gene Expression. J. Med. Chem., 52, 2863-2874.
20. Qin, Y. and Hurley, L.H. (2008) Structures, folding patterns, and functions of intramolecular DNA G-quadruplexes found in eukaryotic promoter regions. Biochimie, 90, 1149-1171.
21. Davis, T.L., Firulli, A.B. and Kinniburgh, A.J. (1989) Ribonucleoprotein and protein factors bind to an H-DNA-forming c-myc DNA element: possible regulators of the c-myc gene. Proc. Natl Acad. Sci. USA, 86, 9682-9686.
22. Kinniburgh, A.J. (1989) A cis-acting transcription element of the c-myc gene can assume an H-DNA conformation. Nucleic Acids Res., 17, 7771-7778.
23. Wittig, B., Wolfl, S., Dorbic, T., Vahrson, W. and Rich, A. (1992) Transcription of human c-myc in permeabilized nuclei is associated with formation of Z-DNA in three discrete regions of the gene. EMBO J., 11, 4653-4663.
24. Rich, A. and Zhang, S. (2003) Timeline: Z-DNA: the long road to biological function. Nat. Rev. Genet., 4, 566-572.
25. Mullen, M.A., Olson, K.J., Dallaire, P., Major, F., Assmann, S.M. and Bevilacqua, P.C. (2010) RNA G-Quadruplexes in the model plant species Arabidopsis thaliana: prevalence and possible functional roles. Nucleic Acids Res., 38, 8149-8163.
26. Capra, J.A., Paeschke, K., Singh, M. and Zakian, V.A. (2010) G-quadruplex DNA sequences are evolutionarily conserved and associated with distinct genomic features in Saccharomyces cerevisiae. PLoS Comput. Biol., 6, e1000861.
27. Du, Z., Zhao, Y. and Li, N. (2009) Genome-wide colonization of gene regulatory elements by G4 DNA motifs. Nucleic Acids Res., 37, 6784-6798.
28. Verma, A., Halder, K., Halder, R., Yadav, V.K., Rawal, P., Thakur, R.K., Mohd, F., Sharma, A. and Chowdhury, S. (2008) Genome-wide computational and expression analyses reveal G-quadruplex DNA motifs as conserved cis-regulatory elements in human and related species. J. Med. Chem., 51, 5641-5649.
29. Hershman, S.G., Chen, Q., Lee, J.Y., Kozak, M.L., Yue, P., Wang, L.S. and Johnson, F.B. (2008) Genomic distribution and functional analyses of potential G-quadruplex-forming sequences in Saccharomyces cerevisiae. Nucleic Acids Res., 36, 144-156.
30. Eddy, J. and Maizels, N. (2008) Conserved elements with potential to form polymorphic G-quadruplex structures in the first intron of human genes. Nucleic Acids Res., 36, 1321-1333.
31. Huppert, J.L. and Balasubramanian, S. (2007) G-quadruplexes in promoters throughout the human genome. Nucleic Acids Res., 35, 406-413.
32. Du, Z., Kong, P., Gao, Y. and Li, N. (2007) Enrichment of G4 DNA motif in transcriptional regulatory region of chicken genome. Biochem. Biophys. Res. Commun., 354, 1067-1070.
33. Eddy, J., Vallur, A.C., Varma, S., Liu, H., Reinhold, W.C., Pommier, Y. and Maizels, N. (2011) G4 motifs correlate with promoter-proximal transcriptional pausing in human genes. Nucleic Acids Res., 39, 4975-4983.
34. Strawbridge, E.M., Benson, G., Gelfand, Y. and Benham, C.J. (2010) The distribution of inverted repeat sequences in the Saccharomyces cerevisiae genome. Curr. Genet., 56, 321-340.
35. Schroth, G.P., Chou, P.J. and Ho, P.S. (1992) Mapping Z-DNA in the human genome. Computer-aided mapping reveals a nonrandom distribution of potential Z-DNA-forming sequences in human genes. J. Biol. Chem., 267, 11846-11855.
36. Hamada, H., Petrino, M.G. and Kakunaga, T. (1982) A novel repeated element with Z-DNA-forming potential is widely found in evolutionarily diverse eukaryotic genomes. Proc. Natl Acad. Sci. USA, 79, 6465-6469.
37. Zhabinskaya, D. and Benham, C.J. (2012) Theoretical Analysis of Competing Conformational Transitions in Superhelical DNA. PLoS Comput. Biol., 8, e1002484.
38. He, L., Liu, J., Collins, I., Sanford, S., O'Connell, B., Benham, C.J. and Levens, D. (2000) Loss of FBP function arrests cellular proliferation and extinguishes c-myc expression. EMBO J., 19, 1034-1044.
39. Zhabinskaya, D. and Benham, C.J. (2011) Theoretical analysis of the stress induced B-Z transition in superhelical DNA. PLoS Comput. Biol., 7, e1001051.
40. Wang, H. and Benham, C.J. (2008) Superhelical destabilization in regulatory regions of stress response genes. PLoS Comput. Biol., 4, e17.
41. Gur-Arie, R., Cohen, C.J., Eitan, Y., Shelef, L., Hallerman, E.M. and Kashi, Y. (2000) Simple Sequence Repeats in Escherichia coli: Abundance, Distribution, Composition, and Polymorphism. Genome Res., 10, 62-71.
42. Hawley, D.K. and McClure, W.R. (1983) Compilation and analysis of Escherichia coli promoter DNA sequences. Nucleic Acids Res., 11, 2237-2255.
43. Horwitz, M. and Loeb, L. (1988) An E. coli promoter that regulates transcription by DNA superhelix-induced cruciform extrusion. Science, 241, 703-705.
44. Opel, M.L. and Hatfield, G.W. (2001) DNA supercoiling-dependent transcriptional coupling between the divergently transcribed promoters of the ilvYC operon of Escherichia coli is proportional to promoter strengths and transcript lengths. Mol. Microbiol., 39, 191-198.
45. Sheridan, S.D., Benham, C.J. and Hatfield, G.W. (1999) Inhibition of DNA supercoiling-dependent transcriptional activation by a distant B-DNA to Z-DNA transition. J. Biol. Chem., 274, 8169-8174.
46. Mela, I., Kranaster, R., Henderson, R.M., Balasubramanian, S. and Edwardson, J.M. (2012) Demonstration of ligand decoration, and ligand-induced perturbation, of G-quadruplexes in a plasmid using atomic force microscopy. Biochemistry, 51, 578-585.
47. Rawal, P., Kummarasetti, V.B.R., Ravindran, J., Kumar, N., Halder, K., Sharma, R., Mukerji, M., Das, S.K. and Chowdhury, S. (2006) Genome-wide prediction of G4 DNA as regulatory motifs: role in Escherichia coli global regulation. Genome Res., 16, 644-655.
48. Wang, H., Noordewier, M. and Benham, C.J. (2004) Stress-induced DNA duplex destabilization (SIDD) in the E. coli genome: SIDD sites are closely associated with promoters. Genome Res., 14, 1575-1584.
49. Champ, P.C., Maurice, S., Vargason, J.M., Camp, T. and Ho, P.S. (2004) Distributions of Z-DNA and nuclear factor I in human chromosome 22: a model for coupled transcriptional regulation. Nucleic Acids Res., 32, 6501-6510.
50. Wilson, K.S. and von Hippel, P.H. (1995) Transcription termination at intrinsic terminators: the role of the RNA hairpin. Proc. Natl Acad. Sci. USA, 92, 8793-8797.
51. Cardinale, C.J., Washburn, R.S., Tadigotla, V.R., Brown, L.M., Gottesman, M.E. and Nudler, E. (2008) Termination factor Rho and its cofactors NusA and NusG silence foreign DNA in E. coli. Science, 320, 935-938.
52. Pruitt, K.D., Tatusova, T. and Maglott, D.R. (2007) NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res., 35, D61-D65.
53. Sayers, E.W., Barrett, T., Benson, D.A., Bolton, E., Bryant, S.H., Canese, K., Chetvernin, V., Church, D.M., DiCuccio, M., Federhen, S. et al. (2011) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res., 39, D38-D51.
54. Gama-Castro, S., Salgado, H., Peralta-Gil, M., Santos-Zavaleta, A., Muniz-Rascado, L., Solano-Lira, H., Jimenez-Jacinto, V., Weiss, V., Garcia-Sotelo, J.S., Lopez-Fuentes, A. et al. (2011) RegulonDB version 7.0: transcriptional regulation of Escherichia coli K-12 integrated within genetic sensory response units (Gensor Units). Nucleic Acids Res., 39, D98-D105.
55. Lipps, H.J. and Rhodes, D. (2009) G-quadruplex structures: in vivo evidence and function. Trends Cell Biol., 19, 414-422.
56. Huppert, J.L. and Balasubramanian, S. (2005) Prevalence of quadruplexes in the human genome. Nucleic Acids Res., 33, 2908-2916.
57. Todd, A.K., Johnston, M. and Neidle, S. (2005) Highly prevalent putative quadruplex sequence motifs in human DNA. Nucleic Acids Res., 33, 2901-2907.
58. Brazda, V., Laister, R.C., Jagelska, E.B. and Arrowsmith, C. (2011) Cruciform structures are a common DNA feature important for regulating biological processes. BMC Mol. Biol., 12, 33.
59. Warburton, P.E., Giordano, J., Cheung, F., Gelfand, Y. and Benson, G. (2004) Inverted repeat structure of the human genome: the X-chromosome contains a preponderance of large, highly homologous inverted repeats that contain testes genes. Genome Res., 14, 1861-1869.
60. Benham, C.J. (1993) Sites of predicted stress-induced DNA duplex destabilization occur preferentially at regulatory loci. Proc. Natl Acad. Sci. USA, 90, 2999-3003.
61. Jain, A., Wang, G. and Vasquez, K.M. (2008) DNA triple helices: biological consequences and therapeutic potential. Biochimie, 90, 1117-1130.
62. Lexa, M., Martinek, T., Burgetova, I., Kopecek, D. and Brazdova, M. (2011) A dynamic programming algorithm for identification of triplex-forming sequences. Bioinformatics, 27, 2510-2517.
63. Sinden, R.R., Pytlos-Sinden, M.J. and Potaman, V.N. (2007) Slipped strand DNA structures. Front. Biosci., 12, 4788-4799.
64. Benson, G. (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res., 27, 573-580.
65. Peters, J.M., Mooney, R.A., Kuan, P.F., Rowland, J.L., Keles, S. and Landick, R. (2009) Rho directs widespread termination of intragenic and stable RNA transcription. Proc. Natl Acad. Sci. USA, 106, 15406-15411.
66. Kingsford, C.L., Ayanbule, K. and Salzberg, S.L. (2007) Rapid, accurate, computational discovery of Rho-independent transcription terminators illuminates their relationship to DNA uptake. Genome Biol., 8, R22.
67. Parzen, E. (1962) On estimation of a probability density function and mode. Ann. Math. Stat., 33, 1065-1076.
68. Ho, P.S., Ellison, M.J., Quigley, G.J. and Rich, A. (1986) A computer aided thermodynamic approach for predicting the formation of Z-DNA in naturally occurring sequences. EMBO J., 5, 2737-2744.
69. Wang, H., Kaloper, M. and Benham, C.J. (2006) SIDDBASE: a database containing the stress-induced DNA duplex destabilization (SIDD) profiles of complete microbial genomes. Nucleic Acids Res., 34, D373-D378.
70. Johnson, J.E., Cao, K., Ryvkin, P., Wang, L.S. and Johnson, F.B. (2010) Altered gene expression in the Werner and Bloom syndromes is associated with sequences having G-quadruplex forming potential. Nucleic Acids Res., 38, 1114-1122.
71. Verma, A., Yadav, V.K., Basundra, R., Kumar, A. and Chowdhury, S. (2009) Evidence of genome-wide G4 DNAmediated gene expression in human cancer cells. Nucleic Acids Res., 37, 4194-4204.
72. Fernando, H., Sewitz, S., Darot, J., Tavare, S., Huppert, J.L. and Balasubramanian, S. (2009) Genome-wide analysis of a G-quadruplex-specific single-chain antibody that regulates gene expression. Nucleic Acids Res., 37, 6716-6722.
73. Du, Z., Zhao, Y. and Li, N. (2008) Genome-wide analysis reveals regulatory role of G4 DNA in gene transcription. Genome Res., 18, 233-241.
74. Khuu, P., Sandor, M., DeYoung, J. and Ho, P.S. (2007) Phylogenomic analysis of the emergence of GC-rich transcription elements. Proc. Natl Acad. Sci. USA, 104, 16528-16533.
75. Schroth, G.P. and Ho, P.S. (1995) Occurrence of potential cruciform and H-DNA forming sequences in genomic DNA. Nucleic Acids Res., 23, 1977-1983.
76. Edwards, S.F., Sirito, M., Krahe, R. and Sinden, R.R. (2009) A Z-DNA sequence reduces slipped-strand structure formation in the myotonic dystrophy type 2 (CCTG) x (CAGG) repeat. Proc. Natl Acad. Sci. USA, 106, 3270-3275.
77. Leng, F. and McMacken, R. (2002) Potent stimulation of transcription-coupled DNA supercoiling by sequence-specific DNA-binding proteins. Proc. Natl Acad. Sci. USA, 99, 9139-9144.
78. Hatfield, G.W. and Benham, C.J. (2002) DNA topology-mediated control of global gene expression in Escherichia coli. Annu. Rev. Genet., 36, 175-203.
79. Oh, D.B., Kim, Y.G. and Rich, A. (2002) Z-DNA-binding proteins can act as potent effectors of gene expression in vivo. Proc. Natl Acad. Sci., 99, 16666-16671.
80. Schon, E., Evans, T., Welsh, J. and Efstratiadis, A. (1983) Conformation of promoter DNA: Fine mapping of S1-hypersensitive sites. Cell, 35, 837-848.
81. Wang, G. and Vasquez, K.M. (2007) Z-DNA, an active element in the genome. Front. Biosci., 12, 4424-4438.
82. Grabczyk, E. and Fishman, M.C. (1995) A long purine-pyrimidine homopolymer acts as a transcriptional diode. J. Biol. Chem., 270, 1791-1797.