Regulation of traJ transcription in the Salmonella virulence plasmid by strand-specific DNA adenine hemimethylation

Molecular Microbiology

Volumn 57, Issue 6, 2005, Pages 1700-1718

  Camacho, Eva M ^a   Casadesús, Josep ^a  

^a UNIVERSITY OF SEVILLE   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

DNA ADENINE METHYLTRANSFERASE; DNA FRAGMENT;

ARTICLE; BACTERIAL VIRULENCE; BINDING AFFINITY; BINDING SITE; EPIGENETICS; METHYLATION; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; SALMONELLA ENTERICA; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

ADENINE; BACTERIAL OUTER MEMBRANE PROTEINS; BASE SEQUENCE; DNA METHYLATION; DNA, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; OPERON; PLASMIDS; SALMONELLA TYPHIMURIUM; SITE-SPECIFIC DNA-METHYLTRANSFERASE (ADENINE-SPECIFIC); TRANSCRIPTION, GENETIC; VIRULENCE;

SALMONELLA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM;

EID: 25144451821     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2005.04788.x     Document Type: Article

References (83)

1. Ahmer, B.M.M., Tran, M., and Heffron, F. (1999) The virulence plasmid of Salmonella typhimurium is self-transmissible. J Bacteriol 181: 1364-1368.
2. van Biesen, T., and Frost, L.S. (1992) Differential levels of fertility inhibition among F-like plasmids are related to the celluar concentration of finO mRNA. Mol Microbiol 6: 771-780.
3. van Biesen, T., Soderborn, F., Wagner, E.G., and Frost, L.S. (1993) Structural and functional analyses of the FinP anti-sense RNA regulatory system of the F conjugative plasmid. Mol Microbiol 10: 35-43.
4. Blyn, L.B., Braaten, B.A., White-Ziegler, C.A., Rolfson, D.A., and Low, D.A. (1989) Phase variation of pyelonephritis-associated pili in Escherichia coli: evidence for transcriptional regulation. EMBO J 8: 613-620.
5. Bolker, M., and Kahmann, R. (1989) The Escherichia coli protein OxyR discriminates between methylated and unmethylated states of the phage Mu promoter. EMBO J 8: 2403-2410.
6. Braaten, B.A., Platko, J.V., van der Woude, M., Simons, B.H., de Graaf, F.K., Calvo, J.M., and Low, D.A. (1992) Leucine-responsive regulatory protein controls the expression of both the pap and fan pili operons in Escherichia coli. Proc Natl Acad Sci USA 89: 4250-4254.
7. Calvo, J.M., and Matthews, R.G. (1994) The leucine-responsive regulatory protein, a global regulator of metabolism in Escherichia coli. Microbiol Rev 58: 466-490.
8. Camacho, E.M., and Casadesús, J. (2002) Conjugal transfer of the virulence plasmid of Salmonella enterica is regulated by the leucine-responsive regulatory protein and DNA adenine methylation. Mol Microbiol 44: 1589-1598.
9. Camacho, E.M., Serna, A., Madrid, C., Marqués, S., Fernández, R., de la Cruz, F., et al. (2005) Regulation of finP transcription by DNA adenine methylation in the virulence plasmid of Salmonella enterica. J Bacteriol 187.
10. Casadesús, J., and D'Ari, R. (2002) Memory in bacteria and phage. Bioessays 24: 512-518.
11. Cheng, X. (1995) Structure and function of DNA methyltransferases. Annu Rev Biophys Biomol Struct 24: 293-318.
12. Cullum, J., Collins, J.F., and Broda, P. (1978) The spread of plasmids in model populations of Escherichia coli K12. Plasmid 1: 545-556.
13. Curtiss, R., III, and Stallions, D.R. (1967) Energy requirements for specific pair formation during conjugation in Escherichia coli K-12. J Bacteriol 94: 490-497.
14. Datsenko, K.A., and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 90: 6640-6645.
15. Dempsey, W.B. (1993) Key regulatory aspects of transfer of F-related factors. In Bacterial Conjugation. Clewell, D.B. (eds). New York: Plenum Press, pp. 53-73.
16. Dempsey, W.B. (1994) Regulation of R100 conjugation requires traM in cis to traJ. Mol Microbiol 13: 313-316.
17. Diekmann, S. (1987) DNA methylation can enhance or induce DNA curvature. EMBO J 6: 4213-4217.
18. Ellermeier, C.D., Janakiraman, A., and Slauch, J.M. (2002) Construction of targeted single copy lac fusions using lambda Red and FLP-mediated site-specific recombination in bacteria. Gene 290: 153-161.
19. Ernsting, B.R., Denninger, J.W., Blumenthal, R.M., and Matthews, R.G. (1993) Regulation of the gltDBF operon of Escherichia coli: how is a leucine-insensitive operon regulated by the leucine-responsive regulatory protein? J Bacteriol 175: 7160-7169.
20. Firth, N., Ippen-Ihler, K., and Skurray, R. (1996) Structure and function of the F factor and mechanism of conjugation. In Escherichia coli and Salmonella: Cellular and Molecular Biology. Neidhardt, F.C., Curtiss R., III, Ingraham, J.L., Lin, E.G.C., Low, K.B., Magasanik, B., et al. (eds). Washington, DC: American Society for Microbiology Press, pp. 2377-2401.
21. Frost, L.S., and Manchak, J. (1998) F-phenocopies: characterization of expression of the F transfer region in stationary phase. Microbiology 144: 2579-2587.
22. García-del Portillo, F., Pucciarelli, M.G., and Casadesús, J. (1999) DNA adenine methylase mutants of Salmonella typhimurium are deficient in protein secretion, cell invasion and M cell cytotoxicity. Proc Natl Acad Sci USA 96:11584-11588.
23. - mutants of Escherichia coli: a role for 6-methyladenine residues in mutation avoidance. Mol Gen Genet 167: 307-312.
24. Gubbins, M.J., Lau, I., Will, W.R., Manchak, J.M., Raivio, T.L., and Frost, L.S. (2002) The positive regulator, TraJ, of the Escherichia coli F plasmid is unstable in a cpxA* background. J Bacteriol 184: 5781-5788.
25. Haagmans, W., and van der Woude, M. (2000) Phase variation of Ag43 in Escherichia coli: dam-dependent methylation abrogates OxyR binding and OxyR-mediated repression of transcription. Mol Microbiol 35: 877-887.
26. Hayes, W. (1953) Observations on a transmissible agent determining sexual differentiation in Bacterium coli. J Gen Microbiol 8: 72-88.
27. Hayes, W. (1957) The kinetics of the mating process in Escherichia coli. J Gen Microbiol 16: 97-119.
28. Heithoff, D.M., Sinsheimer, R.L., Low, D.A., and Mahan, M.J. (1999) An essential role for DNA adenine methylation in bacterial virulence. Science 284: 967-970.
29. Henderson, I.R., and Owen, P. (1999) The major phase-variable outer membrane protein of Escherichia coli structurally resembles the immunoglobulin A1 protease class of exported protein and is regulated by a novel mechanism involving Dam and OxyR. J Bacteriol 181: 2132-2141.
30. Herman, G.E., and Modrich, P. (1982) Escherichia coli dam methylase. J Biol Chem 257: 2605-2612.
31. Hernday, A., Krabbe, M., Braaten, B., and Low, D.A. (2003) The mechanism by which DNA adenine methylase and PapI activate the pap epigenetic switch. Mol Cell 12: 954-957.
32. Ho, S.N., Hunt, H.D., Horton, R.M., Pullen, J.K., and Pease, L.R. (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51-59.
33. Jafri, S., Chen, S., and Calvo, J.M. (2002) ilvIH operon expression in Escherichia coli requires Lrp binding to two distinct regions in DNA. J Bacteriol 184: 5293-5300.
34. Jerome, L.J., and Frost, L.S. (1999) In vitro analysis of the interaction between the FinO protein and FinP antisense RNA of F-like conjugative plasmids. J Biol Chem 274: 10356-10362.
35. Jerome, L.J., van Biesen, T., and Frost, L.S. (1999) Degradation of FinP antisense RNA from F-like plasmids: the RNA-binding protein, FinO, protects FinP from ribonuclease E. J Mol Biol 285: 1457-1473.
36. Julio, S.M., Heithoff, D.M., Provenzano, D., Klose, K.E., Sinsheimer, R.L., Low, D.A., and Mahan, M.J. (2001) DNA adenine methylase is essential for viability and plays a role in the pathogenesis of Yersinia pseudotuberculosis and Vibrio cholerae. Infect Immun 69: 7610-7615.
37. Lederberg, J., Cavalli, L.L., and Lederberg, E.M. (1952) Sex compatibility in Escherichia coli. Genetics 37: 720-730.
38. Lee, S.H., Frost, L.S., and Paranchych, W. (1992) FinOP repression of the F plasmid involves extension of the half-life of FinP antisense RNA by FinO. Mol Gen Genet 235: 131-139.
39. Løbner-Olesen, A., Marinus, M.G., and Hanssen, F.G. (2003) Role of SeqA and Dam in Escherichia coli gene expression: a global/microarray analysis. Proc Natl Acad Sci USA 100: 4672-4677.
40. Low, D.A., Weyand, N.J., and Mahan, M.J. (2001) Roles of DNA adenine methylation in regulating gene expression and virulence. Infect Immun 69: 7197-7204.
41. McClelland, M., Sanderson, K.E., Spieth, J., Clifton, S.W., Latreille, P., Courtney, L., et al. (2001) Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413: 852-856.
42. Macián, F., Pérez-Roger, I., and Armengod, M.E. (1994) An improved vector system for constructing transcriptional lacZ fusions: analysis of regulation of the dnaA, dnaN, recF and gyrB genes of Escherichia coli. Gene 145: 17-24.
43. + revertants and suppressor mutations that modify secondary phenotypes of dam-3 strains of Escherichia coli K-12. Mol Gen Genet 178: 309-315.
44. Maloy, S.R., Stewart, V.J., and Taylor, R.K. (1996) Genetic Analysis of Pathogenic Bacteria. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
45. Marinus, M.G. (1985) DNA methylation influences trpR promoter activity in Escherichia coli. Mol Gen Genet 200: 185-186.
46. Marinus, M.G. (1996) Methylation of DNA. In Escherichia coli and Salmonella: Cellular, Molecular Biology. Neidhardt, F.C., Curtiss, R., III, Ingraham, J.L., Lin, E.C.C., Low, K.B., Magasanik, B., et al. (eds). Washington, DC: American Society for Microbiology Press, pp. 782-791.
47. Marqués, S., Ramos, J.L., and Timmis, K. (1993) Analysis of the mRNA structure of the Pseudomonas putida TOL meta fission pathway operon around the transcription initiation point, the xylTE and the xylFJ regions. Biochim Biophys Acta 1216: 227-236.
48. Messer, W., Bellekes, U., and Lother, H. (1985) Effect of dam methylation on the activity of the E. coli replication origin, oriC. EMBO J 4: 1327-1332.
49. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
50. Modrich, P. (1989) Methyl-directed DNA mismatch correction. J Biol Chem 264: 6597-6600.
51. Nou, X., Skinner, B., Braaten, B., Blyn, L., Hirsh, D., and Low, D.A. (1993) Regulation of pyelonephritis-associated pili phase variation in Escherichia coli: binding of the PapI and Lrp regulatory proteins is controlled by DNA methylation. Mol Microbiol 7: 545-553.
52. Ogden, G.B., Pratt, M.J., and Schaechter, M. (1988) The replicative origin of the E. coli chromosome binds to cell membranes only when hemimethylated. Cell 54: 127-135.
53. Oshima, T., Wada, C., Kawagoe, Y., Ara, T., Maeda, M., Masuda, Y., et al. (2002) Genome-wide analysis of deoxy-adenosine methyltransferase-mediated control of gene expression in Escherichia coli. Mol Microbiol 45: 673-695.
54. Peterson, K.R., and Mount, D.W. (1978) Analysis of the genetic requirements for viability of Escherichia coli DNA adenine methylase (dam) mutants. J Bacteriol 175: 7505-7508.
55. 6-adenine methylation status: possible implications for DNA-protein recognition. Mol Gen Genet 258: 488-493.
56. Prieto, A.I., Ramos-Morales, F., and Casadesús, J. (2004) Bile-induced DNA damage in Salmonella enterica. Genetics 168: 1787-1794.
57. Pucciarelli, M.G., Prieto, A.I., Casadesús, J., and García del Portillo, F. (2002) Envelope instability in DNA adenine methylase mutants of Salmonella enterica. Microbiology 148: 1171-1182.
58. Razin, A., Urieli, S., Pollack, Y., Gruenbaum, Y., and Glaser, G. (1980) Studies on the biological role of DNA methylation. IV. Mode of methylation of DNA in E. coli cells. Nucleic Acids Res 8: 1783-1792.
59. Ringquist, S., and Smith, C.L. (1992) The Escherichia coli chromosome contains specific, unmethylated dam and dcm sites. Proc Natl Acad Sci USA 89: 4359-4343.
60. Roberts, D., Hoopes, B.C., McClure, W.R., and Kleckner, N. (1985) IS 10 transposition is regulated by DNA adenine methylation. Cell 43: 117-130.
61. Sambrook, J., and Russell, D.W. (2002) Molecular Cloning, 3rd edn, Vol. 1. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
62. Sanger, F.S., Nicklen, S., and Coulson, A.R. (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463-5467.
63. Silverman, P.M., Wickersham, E., and Harris, R. (1991) Regulation of the F plasmid tra/promoter in Escherichia coli by host and plasmid factors. J Mol Biol 218: 119-128.
64. + plasmid from strains of Salmonella typhimurium LT2. Mol Gen Genet 126: 143-151.
65. Starcic, M., Zgur-Bertok, D., Jordi, B.J., Wosten, M.M., Gaastra, W., and van Putten, J.P. (2003) The cyclic AMP-cyclic AMP receptor protein complex regulates activity of the traJ promoter of the Escherichia coli conjugative plasmid pRK100. J Bacteriol 185: 1616-1623.
66. Starcic-Erjavec, M., van Putten, J.P., Gaastra, W., Jordi, B.J., Grabnar, M., and Zgur-Bertok, D. (2003) H-NS and Lrp serve as positive modulators of traJ expression from the Escherichia coli plasmid pRK100. Mol Genet Genomics 270: 94-102.
67. Stephens, C., Reisenauer, A., Wright, R., and Shapiro, L. (1996) A cell cycle-regulated bacterial DNA methyltransferase is essential for viability. Proc Natl Acad Sci USA 93: 1210-1214.
68. Strohmaier, H., Noiges, R., Kotschan, S., Sawers, G., Högenauer, G., Zechner, E., and Koraimann, G. (1998) Signal transduction and bacterial conjugation: characterization of the role of ArcA in regulating conjugative transfer of the resistance plasmid R1. J Mol Biol 277: 309-316.
69. Szyf, M., Avraham-Haetzni, K., Reifman, A., Shlomai, J., Kaplan, F., Oppenheim, A., and Razin, A. (1984) DNA methylation pattern is determined by the intracellular level of the methylase. Proc Natl Acad Sci USA 81: 3278-3282.
70. Taki, K., Abo, T., and Othsubo, E. (1998) Regulatory mechanisms in expression of the traY-I operon of sex factor plasmid R100: involvement of traJ and traY gene products. Genes Cells 3: 331-345.
71. Torreblanca, J., and Casadesús, J. (1996) DNA adenine methylase mutants of Salmonella typhimurium and a novel Dam-regulated locus. Genetics 144: 15-26.
72. Torreblanca, J., Marqués, S., and Casadesús, J. (1999) Synthesis of FinP RNA by plasmids F and pSLT is regulated by DNA adenine methylation. Genetics 152: 31-45.
73. Vogel, H., and Bonner, D. (1956) Acetylornithase of Escherichia coli: partial purification and some properties. J Biol Chem 218: 97-106.
74. Wang, Q., and Calvo, J.M. (1993a) Lrp, a global regulatory protein of Escherichia coli, binds co-operatively to multiple sites and activates transcription of ilvIH. J Mol Biol 229: 306-318.
75. Wang, Q., and Calvo, J.M. (1993b) Lrp, a major regulatory protein in Escherichia coli, bends DNA and can organize the assembly of a higher-order nucleoprotein structure. EMBO J 12: 2495-2501.
76. Watanabe, T., and Fukasawa, T. (1961) Episome-mediated transfer of drug resistance in Enterobacteriaceae. I. Transfer of resistance factors by conjugation. J Bacteriol 81: 669-678.
77. Will, W.R., Lu, J., and Frost, L.S. (2004) The role of H-NS in silencing F transfer gene expression during entry into stationary phase. Mol Microbiol 54: 769-782.
78. van der Woude, M.W., Braaten, B., and Low, D.A. (1992) Evidence for global regulatory control of pilus expression in Escherichia coli by Lrp and DNA methylation: model building based on the analysis of Pap. Mol Microbiol 6: 2429-2435.
79. van der Woude, M., Braaten, B., and Low, D.A. (1996) Epigenetic phase variation of the pap operon in Escherichia coli. Trends Microbiol 4: 5-9.
80. van der Woude, M., Hale, W.B., and Low, D.A. (1998) Formation of DNA methylation patterns: nonmethylated GATC sequences in gut and pap operons. J Bacteriol 180: 5913-5920.
81. Yanisch-Perron, V., Vieira, J., and Messing, J. (1985) Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33: 103-119.
82. Zatyka, M., and Thomas, C.M. (1998) Control of genes for conjugative transfer of plasmids and other mobile elements. FEMS Microbiol Rev 21: 291-319.
83. Zweiger, G., Marczynski, G., and Shapiro, L. (1994) A Caulobacter DNA methyltransferase that functions only in the predivisional cell. J Mol Biol 235: 472-485.