Role of DNA methyltransferases in epigenetic regulation in bacteria

Sub-Cellular Biochemistry

Volumn 61, Issue , 2013, Pages 81-102

  Kumar, Ritesh ^a   Rao, Desirazu N ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); PROKARYOTA;

BACTERIAL DNA; BACTERIAL PROTEIN; DNA METHYLTRANSFERASE;

BACTERIAL GENOME; BACTERIUM; DNA METHYLATION; DNA REPAIR; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; GENOTYPE; HOST PATHOGEN INTERACTION; METABOLISM; PATHOGENICITY; PHENOTYPE; REVIEW; VIRULENCE;

BACTERIA; BACTERIAL PROTEINS; DNA METHYLATION; DNA MODIFICATION METHYLASES; DNA REPAIR; DNA, BACTERIAL; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; GENOTYPE; HOST-PATHOGEN INTERACTIONS; PHENOTYPE; VIRULENCE;

EID: 84890366686     PISSN: 03060225     EISSN: None     Source Type: Journal    
DOI: 10.1007/978-94-007-4525-4_4     Document Type: Article

References (141)

1. Adamczyk-Poplawska M, Lower M, Piekarowicz A (2009) Characterization of the NgoAXP: phase-variable type III restriction-modification system in Neisseria gonorrhoeae. FEMS Microbiol Lett 300: 25-35.
2. Alm RA, Ling LSL, Moir DT, King BL, Brown ED, Doig PC, Smith DR, Noonan B, Guild BC, deJonge BL, Carmel G, Tummino PJ, Caruso A, Uria-Nickelsen M, Mills DM, Ives C, Gibson R, Merberg D, Mills SD, Jiang Q, Taylor DE, Vovis GF, Trost TJ (1999) Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 397: 176-180.
3. Ando T, Ishiguro K, Watanabe O, Miyake N, Kato T, Hibi S, Mimura S, Nakamura M, Miyahara R, Ohmiya N, Niwa Y, Goto H (2010) Restriction-modification systems may be associated with Helicobacter pylori virulence. J Gastroenterol Hepatol 1: S95-S98.
4. Arber W (2000) Genetic variation: molecular mechanisms and impact on microbial evolution. FEMS Microbiol Rev 24: 1-7.
5. Arber W (2002) Evolution of prokaryotic genomes. Curr Top Microbiol Immunol 264: 1-14.
6. Arber W, Dussoix D (1962) Host specificity of DNA produced by Escherichia coli. I. Host controlled modification of bacteriophage lambda. J Mol Biol 5: 18-36.
7. Au KG, Welsh K, Modrich P (1992) Initiation of methyl-directed mismatch repair. J Biol Chem 267: 12142-12148.
8. Barbeyron T, Kean K, Forterre P (1984) DNA adenine methylation of GATC sequences appeared recently in the Escherichia coli lineage. J Bacteriol 160: 586-590.
9. Bell DC, Cupples CG (2001) Very-short-patch repair in Escherichia coli requires the dam adenine methylase. J Bacteriol 183: 3631-3635.
10. Bergerat A, Kriebardis A, Guschlbauer W (1989) Preferential site-specific hemimethylation of GATC sites in pBR322 DNA by Dam methyltransferase from Escherichia coli. J Biol Chem 264: 4064-4070.
11. Bertani G, Weigle JJ (1953) Host controlled variation in bacterial viruses. J Bacteriol 65: 113-121.
12. Bestor TH (2000) The DNA methyltransferases of mammals. Hum Mol Genet 9: 2395-2402.
13. Bheemanaik S, Reddy YV, Rao DN (2006) Structure, function and mechanism of exocyclic DNA methyltransferases. Biochem J 399: 177-190.
14. Bickle TA, Kruger DH (1993) Biology of DNA restriction. Microbiol Rev 57: 434-450.
15. Blaisdell BE, Campbell AM, Karlin S (1996) Similarities and dissimilarities of phage genomes. Proc Natl Acad Sci USA 93: 5854-5859.
16. Bogan JA, Helmstetter CE (1997) DNA sequestration and transcription in the oriC region of Escherichia coli. Mol Microbiol 26: 889-896.
17. Braaten BA, Nou X, Kaltenbach LS, Low DA (1994) Methylation patterns in pap regulatory DNA control pyelonephritis-associated pili phase variation in E. coli. Cell 76: 577-588.
18. Braun RE, O'Day K, Wright A (1985) Autoregulation of the DNA replication gene dnaA in E. coli K-12. Cell 40: 159-169.
19. Broadbent SE, Davies MR, van der Woude MW (2010) Phase variation controls expression of Salmonella lipopolysaccharide modification genes by a DNA methylation-dependent mechanism. Microbiology 77: 337-353.
20. Bucci C, Lavitola A, Salvatore P, Del Giudice L, Massardo DR, Bruni CB, Alifano P (1999) Hypermutation in pathogenic bacteria: frequent phase variation in meningococci is a phenotypic trait of a specialized mutator biotype. Mol Cell 3: 435-445.
21. Bujnicki JM (2002) Sequence permutations in the molecular evolution of DNA methyltransferases. BMC Evol Biol 2: 3.
22. Bujnicki JM, Radlinska M (1999) Molecular evolution of DNA-(-cytosine N4) methyltransferases: evidence for their polyphyletic origin. Nucleic Acids Res 27: 4501-4509.
23. Calmann MA, Marinus MG (2003) Regulated expression of the Escherichia coli dam gene. J Bacteriol 185: 5012-5014.
24. Camacho EM, Casadesus 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.
25. Campbell JL, Kleckner N (1990) 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.
26. Carlson K, Kosturko LD (1998) Endonuclease II of coliphage T4: a recombinase disguised as a restriction endonuclease? Mol Microbiol 27: 671-676.
27. Casadesu's J, Low D (2006) Epigenetic gene regulation in the bacterial world. Microbiol Mol Biol Rev 70: 830-856.
28. Chen L, Paulsen DB, Scruggs DW, Banes MM, Reeks BY, Lawrence ML (2003) Alteration of DNA adenine methylase (Dam) activity in Pasteurella multocida causes increased spontaneous mutation frequency and attenuation in mice. Microbiology 149: 2283-2290.
29. Cheng X (1995) Structure and function of DNA methyltransferases. Annu Rev Biophys Biomol Struct 24: 293-318.
30. De Bolle X, Bayliss CD, Field D, van de Ven T, Saunders NJ, Hood DW, Moxon ER (2000) The length of a tetranucleotide repeat tract in Haemophilus influenzae determines the phase variation rate of a gene with homology to type III DNA methyltransferases. Mol Microbiol 35: 211-222.
31. de Vries N, Duinsbergen D, Kuipers EJ, Pot RG, Wiesenekker P, Penn CW, van Vliet AH, Vandenbroucke-Grauls CM, Kusters JG (2002) Transcriptional phase variation of a type III restriction-modification system in Helicobacter pylori. J Bacteriol 184: 6615-6623.
32. Dodson KW, Berg DE (1989) Factors affecting transposition activity of IS50 and Tn5 ends. Gene 76: 207-213.
33. Donahue JP, Israel DA, Torres VJ, Necheva AS, Miller GG (2002) Inactivation of a Helicobacter pylori DNA methyltransferase alters dnaK operon expression following host-cell adherence. FEMS Microbiol Lett 208: 295-301.
34. Dybvig K, Sitaraman R, French CT (1998) A family of phase-variable restriction enzymes with differing specificities generated by high-frequency gene rearrangements. Proc Natl Acad Sci USA 95: 13923-13928.
35. Fälker S, Schmidt MA, Heusipp G (2005) DNA methylation in Yersinia enterocolitica: role of the DNA adenine methyltransferase in mismatch repair and regulation of virulence factors. Microbiology 151: 2291-2299.
36. Fälker S, Schmidt MA, Heusipp G (2007) DNA adenine methylation and bacterial pathogenesis. Int J Med Microbiol 297: 1-7.
37. Fox KL, Srikhanta YN, Jennings MP (2007) Phase variable Type III restriction-modification systems of host-adapted bacterial pathogens. Mol Microbiol 65: 1375-1379.
38. Garcia-Del Portillo F, Pucciarelli MG, Casadesus J (1999) DNA adenine methylase mutants of Salmonella typhimurium show defects in protein secretion, cell invasion, and M cell cytotoxicity. Proc Natl Acad Sci USA 96: 11578-11583.
39. Geier GE, Modrich P (1979) Recognition sequence of the dam methylase of Escherichia coli K12 and mode of cleavage of Dpn I endonuclease. J Biol Chem 254: 1408-1413.
40. Haagmans W, 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.
41. Hallet B (2001) Playing Dr Jekyll and Mr Hyde: combined mechanisms of phase variation in bacteria. Curr Opin Microbiol 4: 570-581.
42. Hattman S, Malygin EG (2004) Bacteriophage T2Dam and T4Dam DNA-[N6-adenine]-methyltransferases. Prog Nucleic Acid Res Mol Biol 77: 67-126.
43. Hattman S, Sun W (1997) Escherichia coli OxyR modulation of bacteriophage Mu mom expression in dam+ cells can be attributed to its ability to bind Pmom promoter DNA. Nucleic Acids Res 25: 4385-4388.
44. Heithoff D, Sinsheimer RL, Low DA, Mahan MJ (1999) An essential role for DNA adenine methylation in bacterial virulence. Science 284: 967-970.
45. Heithoff DM, Enioutina EI, Daynes RA, Sinsheimer RL, Low DA, Mahan MJ (2001) Salmonella DNA adenine methylase mutants confer cross-protective immunity. Infect Immun 69: 6725-6730.
46. Heitman J (1993) On the origins, structures and functions of restriction-modification enzymes. Genet Eng (NY) 15: 57-108.
47. Herman GE, Modrich P (1982) Escherichia coli dam methylase. Physical and catalytic properties of the homogeneous enzyme. J Biol Chem 257: 2605-2612.
48. Heusipp G, Falker S, Schmidt MA (2006) DNA adenine methylation and bacterial pathogenesis. Int J Med Microbiol 29: 1-7.
49. Jafri S, Chen S, Calvo JM (2002) ilvIH operon expression in Escherichia coli requires Lrp binding to two distinct regions of DNA. J Bacteriol 184: 5293-5300.
50. Jeltsch A (1999) Circular permutation in the molecular evolution of DNA methyltransferases. J Mol Evol 49: 161-164.
51. Jeltsch A (2002) Beyond Watson and Crick: DNA methylation and molecular enzymology of DNA methyltransferases. Chembiochem 3: 274-293.
52. Jeltsch A (2003) Maintenance of species identity and controlling speciation of bacteria: a new function for restriction/modification systems? Gene 317: 13-16.
53. Jennings MP, Hood DW, Peak IR, Virji M, Moxon ER (1995) Molecular analysis of a locus for the biosynthesis and phase-variable expression of the lacto-N-neotetraose terminal lipopolysaccharide structure in Neisseria meningitidis. Mol Microbiol 18: 729-740.
54. Jorgensen HF, Bird A (2002) MeCP2 and other methyl-CpG binding proteins. Ment Retard Dev Disabil Res Rev 8: 87-93.
55. Julio SM, Heithoff DM, Provenzano D, Klose KE, Sinsheimer RL, Low DA, Mahan MJ (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.
56. Julio SM, Heithoff DM, Sinsheimer RL, Low DA, Mahan MJ (2002) DNA adenine methylase overproduction in Yersinia pseudotuberculosis alters YopE expression and secretion and host immune responses to infection. Infect Immun 70: 1006-1009.
57. Kim JS, Li J, Barnes IH et al (2008) Role of the Campylobacter jejuni Cj1461 DNA methyltransferase in regulating virulence characteristics. J Bacteriol 190: 6524-6529.
58. Kita K, Kotani H, Sugisaki H, Takanami M (1989) The FokI restriction-modification system I. Organization and nucleotide sequences of the restriction and modification genes. J Biol Chem 264: 5751-5756.
59. Klose RJ, Bird AP (2006) Genomic DNA methylation: the mark and its mediators. Trends Biochem Sci 31: 89-97.
60. Kobayashi I (2004) Restriction-modification systems as minimal forms of life. In: Pingoud A (ed) Restriction endonucleases. Springer, Berlin, pp 19-62.
61. Kossykh VG, Schlagman SL, Hattman S (1995) Phage T4 DNA [N6-adenine]methyltransferase. Overexpression, purification, and characterization. J Biol Chem 270: 14389-14393.
62. Kumar R, Rao DN (2011) A nucleotide insertion between two solitary MTases results in a bifunctional fusion MTase in H. pylor i. Biochem J 433: 487-495.
63. Kumar S, Cheng X, Klimasauskas S, Mi S, Posfai J, Roberts RJ, Wilson GG (1994) The DNA (cytosine-5) methyltransferases. Nucleic Acids Res 22: 1-10.
64. Kumar R, Mukhopadhyay AK, Rao DN (2010) Characterization of an N 6 adenine methyltransferase from H. pylori strain 26695 which methylates adjacent adenines on the same strand. FEBS J 277: 1666-1683.
65. Lewis JD, Meehan RR, Henzel WJ, Maurer-Fogy I, Jeppesen P, Klein F, Bird A (1992) Purification, sequence, and cellular localization of a novel chromosomal protein that binds to methylated DNA. Cell 69: 905-914.
66. Lin LF, Posfai J, Roberts RJ, Kong H (2001) Comparative genomics of the restriction-modification systems in Helicobacter pylori. Proc Natl Acad Sci USA 98: 2740-2745.
67. Løbner-Olesen A, Marinus MG, Hansen FG (2003) Role of SeqA and Dam in Escherichia coli gene expression: a global/microarray analysis. Proc Natl Acad Sci USA 100: 4672-4677.
68. Lobner-Olesen A, Skovgaard O, Marinus MG (2005) Dam methylation: coordinating cellular processes. Curr Opin Microbiol 8: 154-160.
69. López-Garrido J, Casadesús J (2010) Regulation of Salmonella enterica pathogenicity island 1 by DNA adenine methylation. Genetics 184: 637-649.
70. Low DA, Weyand NJ, Mahan MJ (2001) Roles of DNA adenine methylation in regulating bacterial gene expression and virulence. Infect Immun 69: 7197-7204.
71. Lu M, Campbell JL, Boye E, Kleckner N (1994) SeqA: a negative modulator of replication initiation in E. coli. Cell 77: 413-426.
72. Lupas AN, Pointing CP, Russell RB (2001) On the evolution of protein folds: are similar motifs in different protein folds the result of convergence, insertion, or relics of an ancient peptide world? J Struct Biol 134: 191-203.
73. Luria SE, Human ML (1952) A nonhereditary, host-induced variation of bacterial viruses. J Bacteriol 64: 557-569.
74. Malone T, Blumenthal RM, Cheng X (1995) Structure-guided analysis reveals nine sequence motifs conserved among DNA amino-methyltransferases, and suggests a catalytic mechanism for these enzymes. J Mol Biol 253: 618-632.
75. Marczynski GT, Shapiro L (2002) Control of chromosome replication in Caulobacter crescentus. Annu Rev Microbiol 56: 625-656.
76. Marinus MG (1996) Methylation of DNA. In: Neidhardt FC, Curtiss R, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE (eds) Escherichia coli and Salmonella: cellular and molecular biology. ASM Press, Washington DC, pp 782-791.
77. Marinus MG, Casadesus J (2009) Roles of DNA adenine methylation in host-pathogen interactions: mismatch repair, transcriptional regulation, and more. FEMS Microbiol Rev 33: 488-503.
78. Mashhoon N, Carroll M, Pruss C, Eberhard J, Ishikawa S, Estabrook RA, Reich N (2004) Functional characterization of Escherichia coli DNA adenine methyltransferase, a novel target for antibiotics. J Biol Chem 279: 52075-52081.
79. McClain MS, Shaffer CL, Israel DA, Peek RM Jr, Cover TL (2009) Genome sequence analysis of Helicobacter pylori strains associated with gastric ulceration and gastric cancer. BMC Genomics 10: 3.
80. McCommas SA, Syvanen M (1988) Temporal control of transposition in Tn 5. J Bacteriol 170: 889-894.
81. McKane M, Milkman R (1995) Transduction, restriction and recombination patterns in Escherichia coli. Genetics 139: 35-43.
82. Mehling JS, Lavender H, Clegg S (2006) A Dam methylation mutant of Klebsiella pneumoniae, is partially attenuated. FEMS Microbiol Lett 268: 187-193.
83. Messer W, Noyer-Weidner M (1988) Timing and targeting: the biological functions of Dam methylation in E. coli. Cell 54: 735-737.
84. Modrich P, Lahue R (1996) Mismatch repair in replicationfidelity, genetic recombination, and cancer biology. Annu Rev Biochem 65: 101-133.
85. Moxon ER, Thaler DS (1997) Microbial genetics. The tinkerer's evolving tool-box. Nature 387: 659-662.
86. Moxon R, Bayliss C, Hood D (2006) Bacterial contingency loci: the role of simple sequence DNA repeats in bacterial adaptation. Annu Rev Genet 40: 307-333.
87. Naito T, Kusano K, Kobayashi I (1995) Selfish behavior of restriction-modification systems. Science 267: 897-899.
88. Nan X, Cross S, Bird A (1998) Gene silencing by methyl-CpGbinding proteins. Novartis Found Symp 214: 6-16.
89. Ogden GB, Pratt MJ, Schaechter M (1988) The replicative origin of the E. coli chromosome binds to cell membranes only when hemimethylated. Cell 54: 121-135.
90. Oshima T, Wada C, Kawagoe Y, Ara T, Maeda M, Masuda Y, Hiraga S, Mori H (2002) Genomewide analysis of deoxyadenosine methyltransferase-mediated control of gene expression in Escherichia coli. Mol Microbiol 45: 673-695.
91. Oza JP, Yeh JB, Reich NO (2005) DNA methylation modulates Salmonella enterica serovar Typhimurium virulence in Caenorhabditis elegans. FEMS Microbiol Lett 245: 53-59.
92. Pingoud A, Fuxreiter M, Pingoud V, Wende W (2005) Type II restriction endonucleases: structure and mechanism. Cell Mol Life Sci 62: 685-707.
93. Polaczek P, Kwan K, Campbell L (1998) GATC motifs may alter the conformation of DNA depending on sequence context and N6-adenine methylation status: possible implications for DNA-protein recognition. Mol Gen Genet 258: 488-493.
94. Posfai J, Bhagwat AS, Posfai G, Roberts RJ (1989) Predictive motifs derived from cytosine methyltransferases. Nucleic Acids Res 17: 2421-2435.
95. Raleigh EA, Brooks JE (1998) Restriction modification systems: where they are and what they do. In: De Bruijn FJ, Lupski JR, Weinstock GM (eds) Bacterial genomes. Chapman and Hall, New York, pp 78-92.
96. Reisenauer A, Shapiro L (2002) DNA methylation affects the cell cycle transcription of the CtrA global regulator in Caulobacter. EMBO J 21: 4969-4977.
97. Reisenauer A, Kahng LS, McCollum S, Shapiro L (1999) Bacterial DNA methylation: a cell cycle regulator? J Bacteriol 181: 5135-5139.
98. Reznikoff WS (1993) The Tn5 transposon. Annu Rev Microbiol 47: 945-963.
99. Roberts D, Hoopes BC, McClure WR, Kleckner N (1985) IS10 transposition is regulated by DNA adenine methylation. Cell 43: 117-130.
100. Roberts RJ, Belfort M, Bestor T, Bhagwat AS, Bickle TA, Bitinaite J, Blumenthal RM, Degtyarev S, Dryden DT, Dybvig K et al (2003) A nomenclature for restriction enzymes, DNA methyltransferases, homing endonucleases and their genes. Nucleic Acids Res 31: 1805-1812.
101. Roberts RJ, Vincze T, Posfai J, Macelis D (2007) REBASE-enzymes and genes for DNA restriction and modification. Nucleic Acids Res 35: D269-D270.
102. Robertson BD, Meyer TF (1992) Genetic variation in pathogenic bacteria. Trends Genet 8: 422-427.
103. Robertson GT, Reisenauer A, Wright R, Jensen RB, Jensen A, Shapiro L, Roop RM II (2000) The Brucella abortus CcrM DNA methyltransferase is essential for viability, and its overexpression attenuates intracellular replication in murine macrophages. J Bacteriol 182: 3482-3489.
104. Robinson VL, Oyston PC, Titball RW (2005) Oral immunization with a dam mutant of Yersinia pseudotuberrculosis protects against plague. Microbiology 151: 1919-1926.
105. Ryan KA, Lo RY (1999) Characterization of a CACAG pentanucleotide repeat in Pasteurella haemolytica and its possible role in modulation of a novel type III restriction-modification system. Nucleic Acids Res 27: 1505-1511.
106. Salaun L, Bodo L, Suerbaum S, Saunders NJ (2004) The diversity within an expanded and redefined repertoire of phase-variable genes in Helicobacter pylori. Microbiology 150: 817-830.
107. Salaun L, Ayraud S, Saunders NJ (2005) Phase variation mediated niche adaptation during prolonged experimental murine infection with Helicobacter pylori. Microbiology 151: 917-923.
108. Saunders NJ, Peden JF, Hood DW, Moxon ER (1998) Simple sequence repeats in the Helicobacter pylori genome. Mol Microbiol 27: 1091-1098.
109. Saunders NJ, Jeffries AC, Peden JF, Hood DW, Tettelin H, Rappuoli R, Moxon ER (2000) Repeatassociated phase variable genes in the complete genome sequence of Neisseria meningitidis strain MC58. Mol Microbiol 37: 207-215.
110. Schlagman SL, Hattman S (1983) Molecular cloning of a functional dam+ gene coding for phage T4 DNA adenine methylase. Gene 22: 139-156.
111. Schlagman SL, Miner Z, Feher Z, Hattman S (1988) The DNA [adenine-N6]methyltransferase (Dam) of bacteriophage T4. Gene 73: 517-530.
112. Schluckebier G, O'Gara M, Saenger W, Cheng X (1995) Universal catalytic domain structure of AdoMet-dependent methyltransferases. J Mol Biol 247: 16-20.
113. Seib KL, Peak IR, Jennings MP (2002) Phase variable restriction-modification systems in Moraxella catarrhalis. FEMS Immunol Med Microbiol 32: 159-165.
114. Sistla S, Rao DN (2004) S-Adenosyl-L-methionine-dependent restriction enzymes. Crit Rev Biochem Mol Biol 39: 1-19.
115. Sohail A, Lieb M, Dar M, Bhagwat AS (1990) A gene required for very short patch repair in E. coli is adjacent to the DNA cytosine methylase gene. J Bacteriol 172: 4214-4221.
116. Srikhanta YN, Maguire TL, Stacey KJ, Grimmond SM, Jennings MP (2005) The phasevarion: a genetic system controlling coordinated, random switching of expression of multiple genes. Proc Natl Acad Sci USA 102: 5547-5551.
117. Srikhanta YN, Dowideit SJ, Edwards JL, Falsetta ML, Wu H-J, Harrison OB, Fox KL, Seib KL, Maguire TL, Wang AH-J, Maiden MC, Grimmond SM, Apicella MA, Jennings MP (2009) Phasevarions mediate random switching of gene expression in pathogenic Neisseria. PLoS Pathog 5: e1000400.
118. Srikhanta YN, Fox KL, Jennings MP (2010) The phasevarion: phase variation of Type III DNA methyltransferases controls coordinated switching in multiple genes. Nat Rev Microbiol 8: 196-206.
119. Sternberg N, Sauer B, Hoess R, Abremski K (1986) Bacteriophage P1 cre gene and its regulatory region. Evidence for multiple promoters and for regulation by Dam methylation. J Mol Biol 187: 197-212.
120. Sugisaki H, Kita K, Takanami M (1989) The FokI restriction-modification system II. Presence of two domains in FokI methylase responsible for modification of different strands. J Biol Chem 264: 5757-5761.
121. Sun K, Jiao XD, Zhang M, Sun L (2010) DNA adenine methylase is involved in the pathogenesis of Edwardsiella tarda. Vet Microbiol 141: 149-154.
122. Taylor VL, Titball RW, Oyston PCF (2005) Oral immunization with a dam mutant of Yersinia pseudotuberculosis protects against plague. Microbiology 151: 1919-1926.
123. Tomb JF, White O, Kerlavage AR, Clayton RA, Sutton GG, Fleischmann RD et al (1997) The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388: 539-547.
124. Torreblanca J, Marqués S, Casadesús J (1999) Synthesis of FinP RNA by plasmids F and pSLT is regulated by DNA adenine methylation. Genetics 152: 31-45.
125. Urig S, Gowher H, Hermann A, Beck C, Fatemi M, Humeny A, Jeltsch A (2002) The Escherichia coli dam DNA methyltransferase modifies DNA in a highly processive reaction. J Mol Biol 319: 1085-1096.
126. van der Ende A, Hopman CT, Zaat S, Essink BB, Berkhout B, Dankert J (1995) Variable expression of class 1 outer membrane protein in Neisseria meningitides is caused by variation in the spacing between the-10 and-35 regions of the promoter. J Bacteriol 177: 2475-2480.
127. van der Woude MW (2006) Re-examining the role and random nature of phase variation. FEMS Microbiol Lett 254: 190-197.
128. van der Woude MW, Baumler AJ (2004) Phase and antigenic variation in bacteria. Clin Microbiol Rev 17: 581-611.
129. Van Etten JL (2003) Unusual life style of giant chlorella viruses. Annu Rev Genet 37: 153-195.
130. van Ham SM, van Alphen L, Mooi FR, van Putten JP (1993) Phase variation of Haemophilus influenzaefimbriae: transcriptional control of two divergent genes through a variable combined promoter region. Cell 73: 1187-1196.
131. Vitkute J, Stankevicius K, Tamulaitiene G, Maneliene Z, Timinskas A, Berg DE, Janulaitis A (2001) Specificities of eleven different DNA methyltransferases of Helicobacter pylori strain 26695. J Bacteriol 183: 443-450.
132. Waldron DE, Owen P, Dorman CJ (2002) 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.
133. Watson ME, Jarisch J, Smith AL (2004) Inactivation of deoxyadenosine methyltransferase (dam) attenuates Haemophilus influenzae virulence. Mol Microbiol 55: 651-654.
134. Weiser JN, Williams A, Moxon ER (1990) Phasevariable lipopolysaccharide structures enhance the invasive capacity of Haemophilus influenzae. Infect Immun 58: 3455-3457.
135. Wilson GG, Murray NE (1991) Restriction and modification systems. Annu Rev Genet 25: 585-627.
136. Wion D, Casadesus J (2006) N6-methyl-adenine: an epigenetic signal for DNA-protein interactions. Nat Rev Microbiol 4: 183-192.
137. Wright R, Stephens C, Zweiger G, Shapiro L, Alley MR (1996) Caulobacter Lon protease has a critical role in cell-cycle control of DNA methylation. Genes Dev 10: 1532-1542.
138. Xu Q, Stickel S, Roberts RJ, Blaser MJ, Morgan RD (2000) Purification of the novel endonuclease, Hpy188I, and cloning of its restriction-modification genes reveal evidence of its horizontal transfer to the Helicobacter pylori genome. J Biol Chem 275: 17086-17093.
139. Yamaki H, Ohtsubo E, Nagai K, Maeda Y (1988) The oriC unwinding by dam methylation in Escherichia coli. Nucleic Acids Res 16: 5067-5073.
140. Yarmolinski MB, Sternberg N (1988) Bacteriophage P1. In: Calendar R (ed) The bacteriophages, vol 1. Plenum Press, New York, pp 782-791.
141. Zweiger G, Marczynski G, Shapiro L (1994) A Caulobacter DNA methyltransferase that functions only in the predivisional cell. J Mol Biol 235: 472-485.