Genomics of DNA cytosine methylation in Escherichia coli reveals its role in stationary phase transcription

Nature Communications

Volumn 3, Issue , 2012, Pages

  Kahramanoglou, Christina ^a,b   Prieto, Ana I ^a,c,d   Khedkar, Supriya ^e   Haase, Bettina ^f   Gupta, Ankur ^e   Benes, Vladimir ^f   Fraser, Gillian M ^a   Luscombe, Nicholas M ^d,g,h,i   Seshasayee, Aswin S N ^e  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^c WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^d WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^e TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

^f EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^g OKINAWA INSTITUTE OF SCIENCE AND TECHNOLOGY GRADUATE UNIVERSITY   (Japan)

^h UNIVERSITY COLLEGE LONDON   (United Kingdom)

ⁱ IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BISULFITE; CYTOSINE; DNA BASE; GENOMIC DNA; SIGMA FACTOR RPOS; THYMINE;

ARTICLE; BACTERIAL CELL; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL GROWTH; CONTROLLED STUDY; DNA METHYLATION; ESCHERICHIA COLI K 12; GENOMICS; HIGH THROUGHPUT SEQUENCING; LAMB GENE; MALK GENE; MICROARRAY ANALYSIS; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION; OSMB GENE; RISK FACTOR; RPOS GENE; SLP GENE; TRANSCRIPTION REGULATION; WILD TYPE; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PHYSIOLOGY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; MAMMALIA;

CYTOSINE; DNA METHYLATION; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; TRANSCRIPTION, GENETIC;

EID: 84863314385     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms1878     Document Type: Article

References (59)

1. Suzuki, M. M. & Bird, A. DNA methylation landscapes: provocative insights from epigenomics. Nat. Rev. Genet. 9, 465-476 (2008). (Pubitemid 351693975)
2. Ehrlich, M. DNA methylation in cancer: too much, but also too little. Oncogene 21, 5400-5413 (2002). (Pubitemid 34983477)
3. Deaton, A. M. & Bird, A. CpG islands and the regulation of transcription. Genes Dev. 25, 1010-1022 (2011).
4. Rambach, A. & Tiollais, P. Bacteriophage lambda having EcoRI endonuclease sites only in the nonessential region of the genome. Proc. Natl Acad. Sci. USA 71, 3927-3930 (1974).
5. Handa, N. & Kobayashi, I. Post-segregational killing by restriction modification gene complexes: observations of individual cell deaths. Biochimie 81, 931-938 (1999). (Pubitemid 29520621)
6. Kobayashi, I., Nobusato, A., Kobayashi-Takahashi, N. & Uchiyama, I. Shaping the genome-restriction-modification systems as mobile genetic elements. Curr. Opin. Genet. Dev. 9, 649-656 (1999).
7. Kobayashi, I. Behavior of restriction-modification systems as selfish mobile elements and their impact on genome evolution. Nucleic Acids Res. 29, 3742-3756 (2001). (Pubitemid 32910516)
8. Naito, T., Kusano, K. & Kobayashi, I. Selfish behavior of restriction-modification systems. Science 267, 897-899 (1995).
9. Jeltsch, A. & Pingoud, A. Horizontal gene transfer contributes to the wide distribution and evolution of type II restriction-modification systems. J. Mol. Evol. 42, 91-96 (1996). (Pubitemid 26102474)
10. Kita, K. et al. Evidence of horizontal transfer of the EcoO109I restriction-modification gene to Escherichia coli chromosomal DNA. J. Bacteriol. 181, 6822-6827 (1999). (Pubitemid 29517999)
11. Lin, L. F., Posfai, J., Roberts, R. J. & Kong, H. Comparative genomics of the restriction-modification systems in Helicobacter pylori. Proc. Natl Acad. Sci. USA 98, 2740-2745 (2001). (Pubitemid 32209553)
12. Palmer, B. R. & Marinus, M. G. The dam and dcm strains of Escherichia coli-a review. Gene 143, 1-12 (1994).
13. Wion, D. & Casadesus, J. N6-methyl-adenine: an epigenetic signal for DNA-protein interactions. Nat. Rev. Microbiol. 4, 183-192 (2006).
14. Waldron, D. E., Owen, P. & Dorman, C. J. Competitive interaction of the OxyR DNA-binding protein and the Dam methylase at the antigen 43 gene regulatory region in Escherichia coli. Mol. Microbiol. 44, 509-520 (2002). (Pubitemid 34429752)
15. Peterson, S. N. & Reich, N. O. Competitive Lrp and Dam assembly at the pap regulatory region: implications for mechanisms of epigenetic regulation. J. Mol. Biol. 383, 92-105 (2008).
16. Campbell, J. L. & Kleckner, N. E. coli oriC and the dnaA gene promoter are sequestered from dam methyltransferase following the passage of the chromosomal replication fork. Cell 62, 967-979 (1990).
17. Boye, E. & Lobner-Olesen, A. The role of dam methyltransferase in the control of DNA replication in E. coli. Cell 62, 981-989 (1990).
18. Glickman, B., van den Elsen, P. & Radman, M. Induced mutagenesis in dam-mutants of Escherichia coli: a role for 6-methyladenine residues in mutation avoidance. Mol. Gen. Genet. 163, 307-312 (1978). (Pubitemid 8391950)
19. Glickman, B. W. Spontaneous mutagenesis in Escherichia coli strains lacking 6-methyladenine residues in their DNA: an altered mutational spectrum in dam-mutants. Mutat. Res. 61, 153-162 (1979). (Pubitemid 9215520)
20. Glickman, B. W. & Radman, M. Escherichia coli mutator mutants deficient in methylation-instructed DNA mismatch correction. Proc. Natl Acad. Sci. USA 77, 1063-1067 (1980). (Pubitemid 10105057)
21. Reisenauer, A., Kahng, L. S., McCollum, S. & Shapiro, L. Bacterial DNA methylation: a cell cycle regulator? J. Bacteriol. 181, 5135-5139 (1999). (Pubitemid 29416329)
22. Bigger, C. H., Murray, K. & Murray, N. E. Recognition sequence of a restriction enzyme. Nat. New Biol. 244, 7-10 (1973).
23. Boyer, H. W., Chow, L. T., Dugaiczyk, A., Hedgpeth, J. & Goodman, H. M. DNA substrate site for the EcoRII restriction endonuclease and modification methylase. Nat. New Biol. 244, 40-43 (1973).
24. Takahashi, N., Naito, Y., Handa, N. & Kobayashi, I. A DNA methyltransferase can protect the genome from postdisturbance attack by a restriction-modification gene complex. J. Bacteriol. 184, 6100-6108 (2002). (Pubitemid 35265889)
25. Yang, M. K., Ser, S. C. & Lee, C. H. Involvement of E. coli dcm methylase in Tn3 transposition. Proc. Natl Sci. Counc. Repub. China B 13, 276-283 (1989).
26. Korba, B. E. & Hays, J. B. Partially deficient methylation of cytosine in DNA at CCATGG sites stimulates genetic recombination of bacteriophage lambda. Cell 28, 531-541 (1982). (Pubitemid 12111926)
27. Militello, K. et al. Conservation of Dcm-mediated cytosine DNA methylation in Escherichia coli. FEMS Microbiol. Lett. 328, 78-85 (2011).
28. Marinus, M. G. & Morris, N. R. Isolation of deoxyribonucleic acid methylase mutants of Escherichia coli K-12. J. Bacteriol. 114, 1143-1150 (1973).
29. Bhagwat, A. S., Sohail, A. & Roberts, R. J. Cloning and characterization of the dcm locus of Escherichia coli K-12. J. Bacteriol. 166, 751-755 (1986). (Pubitemid 16098152)
30. Ringquist, S. & Smith, C. L. The Escherichia coli chromosome contains specific, unmethylated dam and dcm sites. Proc. Natl Acad. Sci. USA 89, 4539-4543 (1992).
31. Bhagwat, A. S., Johnson, B., Weule, K. & Roberts, R. J. Primary sequence of the EcoRII endonuclease and properties of its fusions with beta-galactosidase. J. Biol. Chem. 265, 767-773 (1990).
32. Bibikova, M. & Fan, J. B. Genome-wide DNA methylation profiling. Wiley Interdiscip. Rev. Syst. Biol. Med. 2, 210-223 (2010).
33. Gomez-Eichelmann, M. C. & Ramirez-Santos, J. Methylated cytosine at Dcm (CCATGG) sites in Escherichia coli: possible function and evolutionary implications. J. Mol. Evol. 37, 11-24 (1993). (Pubitemid 23174571)
34. Seshasayee, A. S. An assessment of the role of DNA adenine methyltransferase on gene expression regulation in E coli. PLoS One 2, e273 (2007).
35. Henaut, A., Rouxel, T., Gleizes, A., Moszer, I. & Danchin, A. Uneven distribution of GATC motifs in the Escherichia coli chromosome, its plasmids and its phages. J. Mol. Biol. 257, 574-585 (1996). (Pubitemid 26107223)
36. Krueger, F. & Andrews, S. R. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics 27, 1571-1572 (2011).
37. Gama-Castro, S. et al. RegulonDB (version 6.0): gene regulation model of Escherichia coli K-12 beyond transcription, active (experimental) annotated promoters and Textpresso navigation. Nucleic Acids Res. 36, D120-D124 (2008). (Pubitemid 351149707)
38. Weber, H., Polen, T., Heuveling, J., Wendisch, V. F. & Hengge, R. Genome-wide analysis of the general stress response network in Escherichia coli: sigmaS-dependent genes, promoters, and sigma factor selectivity. J. Bacteriol. 187, 1591-1603 (2005). (Pubitemid 40289359)
39. Radonjic, M. et al. Genome-wide analyses reveal RNA polymerase II located upstream of genes poised for rapid response upon S. cerevisiae stationary phase exit. Mol. Cell. 18, 171-183 (2005).
40. 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).
41. Randall-Hazelbauer, L. & Schwartz, M. Isolation of the bacteriophage lambda receptor from Escherichia coli. J. Bacteriol. 116, 1436-1446 (1973).
42. Palmke, N., Santacruz, D. & Walter, J. Comprehensive analysis of DNA-methylation in mammalian tissues using MeDIP-chip. Methods 53, 175-184 (2011).
43. Bailey, T. L. et al. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 37, W202-W208 (2009).
44. Lutsenko, E. & Bhagwat, A. S. Principal causes of hot spots for cytosine to thymine mutations at sites of cytosine methylation in growing cells. A model, its experimental support and implications. Mutat. Res. 437, 11-20 (1999). (Pubitemid 29339074)
45. Lieb, M. Spontaneous mutation at a 5-methylcytosine hotspot is prevented by very short patch (VSP) mismatch repair. Genetics 128, 23-27 (1991).
46. Bhagwat, A. S. & Lieb, M. Cooperation and competition in mismatch repair: very short-patch repair and methyl-directed mismatch repair in Escherichia coli. Mol. Microbiol. 44, 1421-1428 (2002). (Pubitemid 34639422)
47. Macintyre, G., Pitsikas, P. & Cupples, C. G. Growth phase-dependent regulation of Vsr endonuclease may contribute to 5-methylcytosine mutational hot spots in Escherichia coli. J. Bacteriol. 181, 4435-4436 (1999). (Pubitemid 29331406)
48. Shen, J. C., Rideout, W. M. 3rd. & Jones, P. A. The rate of hydrolytic deamination of 5-methylcytosine in double-stranded DNA. Nucleic Acids Res. 22, 972-976 (1994). (Pubitemid 24162157)
49. Bhagwat, A. S. & McClelland, M. DNA mismatch correction by very short patch repair may have altered the abundance of oligonucleotides in the E. coli genome. Nucleic Acids Res. 20, 1663-1668 (1992).
50. Banerjee, S. & Chowdhury, R. An orphan DNA (cytosine-5-)- methyltransferase in Vibrio cholerae. Microbiology 152, 1055-1062 (2006).
51. Savageau, M. Escherichia coli habitats, cell types, and molecular mechanisms of gene control. Univ. Chicago Press Am. Soc. 122, 732-744 (1983). (Pubitemid 15272266)
52. Severin, P. M., Zou, X., Gaub, H. E. & Schulten, K. Cytosine methylation alters DNA mechanical properties. Nucleic Acids Res. 39, 8740-8751 (2011).
53. Datsenko, K. A. & Wanner, B. L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl Acad. Sci. USA 97, 6640-6645 (2000). (Pubitemid 30412767)
54. Lefrancois, P. et al. Efficient yeast ChIP-Seq using multiplex short-read DNA sequencing. BMC Genomics 10, 37 (2009).
55. Kanehisa, M., Goto, S., Furumichi, M., Tanabe, M. & Hirakawa, M. KEGG for representation and analysis of molecular networks involving diseases and drugs. Nucleic Acids Res. 38, D355-D360 (2010).
56. Mortazavi, A., Williams, B. A., McCue, K., Schaeffer, L. & Wold, B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5, 621-628 (2008). (Pubitemid 351911867)
57. Langmead, B., Trapnell, C., Pop, M. & Salzberg, S. L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).
58. Ritchie, M. E. et al. A comparison of background correction methods for two-colour microarrays. Bioinformatics 23, 2700-2707 (2007). (Pubitemid 350048334)
59. Huber, W., von Heydebreck, A., Sultmann, H., Poustka, A. & Vingron, M. Variance stabilization applied to microarray data calibration and to the quantification of differential expression. Bioinformatics 18(Suppl. 1), S96-S104 (2002). (Pubitemid 41185642)