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Volume 151, Issue 7

DNA methylation in : role of the DNA adenine methyltransferase in mismatch repair and regulation of virulence factors Free

Abstract

DNA adenine methyltransferase (Dam) plays an important role in physiological processes of Gram-negative bacteria such as mismatch repair and replication. In addition, Dam regulates the expression of virulence genes in various species. The authors cloned the gene of and showed that Dam is essential for viability. Dam overproduction in resulted in an increased frequency of spontaneous mutation and decreased resistance to 2-aminopurine; however, these effects were only marginal compared to the effect of overproduction of -derived Dam in , implying different roles or activities of Dam in mismatch repair of the two species. These differences in Dam function are not the cause for the essentiality of Dam in , as Dam of can complement a defect in . Instead, Dam seems to interfere with expression of essential genes. Furthermore, Dam mediates virulence of . Dam overproduction results in increased tissue culture invasion of , while the expression of specifically -expressed genes is not altered.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): 2-AP, 2-aminopurine and Dam, DNA adenine methyltransferase
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2005-07-01
2025-03-21
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References

  1. Altschul S. F., Madden T. L., Schaffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. 1997; Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402 [CrossRef]
     [Google Scholar]
  2. Bale A., d'Alarcao M., Marinus M. G. 1979; Characterization of DNA adenine methylation mutants of Escherichia coli K12. Mutat Res 59:157–165 [CrossRef]
     [Google Scholar]
  3. Bäumler A. J., Tsolis R. M., van der Velden A. W., Stojiljkovic I., Anic S., Heffron F. 1996; Identification of a new iron regulated locus of Salmonella typhi . Gene 183:207–213 [CrossRef]
     [Google Scholar]
  4. Bayliss C. D., Moxon E. R, van de Ven T. 2002; Mutations in polI but not mutSLH destabilize Haemophilus influenzae tetranucleotide repeats. EMBO J 21:1465–1476 [CrossRef]
     [Google Scholar]
  5. Bolker M., Kahmann R. 1989; The Escherichia coli regulatory protein OxyR discriminates between methylated and unmethylated states of the phage Mu mom promoter. EMBO J 8:2403–2410
     [Google Scholar]
  6. Braaten B. A., Nou X., Kaltenbach L. S., Low D. A. 1994; Methylation patterns in pap regulatory DNA control pyelonephritis-associated pili phase variation in E. coli . Cell 76:577–588 [CrossRef]
     [Google Scholar]
  7. Brooks J. E., Blumenthal R. M., Gingeras T. R. 1983; The isolation and characterization of the Escherichia coli DNA adenine methylase ( dam ) gene. Nucleic Acids Res 11:837–851 [CrossRef]
     [Google Scholar]
  8. Chen L., Paulsen D. B., Scruggs D. W., Banes M. M., Reeks B. Y., Lawrence M. L. 2003; Alteration of DNA adenine methylase (Dam) activity in Pasteurella multocida causes increased spontaneous mutation frequency and attenuation in mice. Microbiology 149:2283–2290 [CrossRef]
     [Google Scholar]
  9. De Lorenzo V., Eltis L., Kessler B., Timmis K. N. 1993; Analysis of Pseudomonas gene products using lacIq/Ptrp-lac plasmids and transposons that confer conditional phenotypes. Gene 123:17–24 [CrossRef]
     [Google Scholar]
  10. Dueger E. L., House J. K., Heithoff D. M., Mahan M. J. 2001; Salmonella DNA adenine methylase mutants elicit protective immune responses to homologous and heterologous serovars in chickens. Infect Immun 69:7950–7954 [CrossRef]
     [Google Scholar]
  11. Dueger E. L., House J. K., Heithoff D. M., Mahan M. J. 2003; Salmonella DNA adenine methylase mutants elicit early and late onset protective immune responses in calves. Vaccine 21:3249–3258 [CrossRef]
     [Google Scholar]
  12. Garcia-Del Portillo F., Pucciarelli M. G., 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 U S A 96:11578–11583 [CrossRef]
     [Google Scholar]
  13. Geier G. E., 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
     [Google Scholar]
  14. Glickman B. W. 1979; 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 [CrossRef]
     [Google Scholar]
  15. Glickman B., Radman M, van den Elsen P. 1978; Induced mutagenesis in dam − mutants of Escherichia coli : a role for 6-methyladenine residues in mutation avoidance. Mol Gen Genet 163:307–312 [CrossRef]
     [Google Scholar]
  16. Heithoff D. M., Sinsheimer R. L., Low D. A., Mahan M. J. 1999; An essential role for DNA adenine methylation in bacterial virulence. Science 284:967–970 [CrossRef]
     [Google Scholar]
  17. Heithoff D. M., Enioutina E. Y., Daynes R. A., Sinsheimer R. L., Low D. A., Mahan M. J. 2001; Salmonella DNA adenine methylase mutants confer cross-protective immunity. Infect Immun 69:6725–6730 [CrossRef]
     [Google Scholar]
  18. Herman G. E., Modrich P. 1981; Escherichia coli K-12 clones that overproduce Dam methylase are hypermutable. J Bacteriol 145:644–646
     [Google Scholar]
  19. Hernday A., Krabbe M., Braaten B., Low D. 2002; Self-perpetuating epigenetic pili switches in bacteria. Proc Natl Acad Sci U S A 99:16470–16476 [CrossRef]
     [Google Scholar]
  20. Heusipp G., Young G. M., Miller V. L. 2001; HreP, an in vivo-expressed protease of Yersinia enterocolitica , is a new member of the family of subtilisin/kexin-like proteases. J Bacteriol 183:3556–3563 [CrossRef]
     [Google Scholar]
  21. Heusipp G., Schmidt M. A., Miller V. L. 2003; Identification of rpoE and nadB as host responsive elements of Yersinia enterocolitica . FEMS Microbiol Lett 226:291–298 [CrossRef]
     [Google Scholar]
  22. Honma Y., Fernandez R. E., Maurelli A. T. 2004; A DNA adenine methylase mutant of Shigella flexneri shows no significant attenuation of virulence. Microbiology 150:1073–1078 [CrossRef]
     [Google Scholar]
  23. Julio S. M., Heithoff D. M., Provenzano D., Klose K. E., Sinsheimer R. L., Low D. A., 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 [CrossRef]
     [Google Scholar]
  24. Julio S. M., Heithoff D. M., Sinsheimer R. L., Low D. A., Mahan M. J. 2002; DNA adenine methylase overproduction in Yersinia pseudotuberculosis alters YopE expression and secretion and host immune responses to infection. Infect Immun 70:1006–1009 [CrossRef]
     [Google Scholar]
  25. Kinder S. A., Badger J. L., Bryant G. O., Pepe J. C., Miller V. L. 1993; Cloning of the Yen I restriction endonuclease and methyltransferase from Yersinia enterocolitica serotype O : 8 and construction of a transformable R−M+ mutant. Gene 136:271–275 [CrossRef]
     [Google Scholar]
  26. Low D. A., Weyand N. J., Mahan M. J. 2001; Roles of DNA adenine methylation in regulating bacterial gene expression and virulence. Infect Immun 69:7197–7204 [CrossRef]
     [Google Scholar]
  27. Lu M., Campbell J. L., Boye E., Kleckner N. 1994; SeqA: a negative modulator of replication initiation in E. coli . Cell 77:413–426 [CrossRef]
     [Google Scholar]
  28. Malone T., Blumenthal R. M., 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 [CrossRef]
     [Google Scholar]
  29. Marinus M. G. others 1996; Methylation of DNA. In Escherichia coli and Salmonella: Cellular and Molecular Biology pp 782–791 Edited by Neidhardt F. C. Washington, DC: American Society for Microbiology;
     [Google Scholar]
  30. Marinus M. G., Morris N. R. 1973; Isolation of deoxyribonucleic acid methylase mutants of Escherichia coli K-12. J Bacteriol 114:1143–1150
     [Google Scholar]
  31. Marinus M. G., Morris N. R. 1974; Biological function for 6-methyladenine residues in the DNA of Escherichia coli K12. J Mol Biol 85:309–322 [CrossRef]
     [Google Scholar]
  32. Marinus M. G., Carraway M., Frey A. Z., Brown L., Arraj J. A. 1983; Insertion mutations in the dam gene of Escherichia coli K-12. Mol Gen Genet 192:288–289 [CrossRef]
     [Google Scholar]
  33. Marinus M. G., Poteete A., Arraj J. A. 1984; Correlation of DNA adenine methylase activity with spontaneous mutability in Escherichia coli K-12. Gene 28:123–125 [CrossRef]
     [Google Scholar]
  34. Miller J. H. 1972 Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  35. Miller V. L., Falkow S. 1988; Evidence for two genetic loci in Yersinia enterocolitica that can promote invasion of epithelial cells. Infect Immun 56:1242–1248
     [Google Scholar]
  36. Miller V. L., Mekalanos J. J. 1988; A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR . J Bacteriol 170:2575–2583
     [Google Scholar]
  37. Modrich P. 1987; DNA mismatch correction. Annu Rev Biochem 56:435–466 [CrossRef]
     [Google Scholar]
  38. Nelson K. M., Young G. M., Miller V. L. 2001; Identification of a locus involved in systemic dissemination of Yersinia enterocolitica . Infect Immun 69:6201–6208 [CrossRef]
     [Google Scholar]
  39. Oshima T., Wada C., Kawagoe Y., Ara T., Maeda M., Masuda Y., Hiraga S., Mori H. 2002; Genome-wide analysis of deoxyadenosine methyltransferase-mediated control of gene expression in Escherichia coli . Mol Microbiol 45:673–695 [CrossRef]
     [Google Scholar]
  40. Ostendorf T., Cherepanov P., Wackernagel W, de Vries J. 1999; Characterization of a dam mutant of Serratia marcescens and nucleotide sequence of the dam region. J Bacteriol 181:3880–3885
     [Google Scholar]
  41. Sternberg N. 1985; Evidence that adenine methylation influences DNA–protein interactions in Escherichia coli . J Bacteriol 164:490–493
     [Google Scholar]
  42. Torreblanca J., Casadesus J. 1996; DNA adenine methylase mutants of Salmonella typhimurium and a novel dam-regulated locus. Genetics 144:15–26
     [Google Scholar]
  43. Watson M. E. Jr, Jarisch J., Smith A. L. 2004; Inactivation of deoxyadenosine methyltransferase ( dam ) attenuates Haemophilus influenzae virulence. Mol Microbiol 53:651–664 [CrossRef]
     [Google Scholar]
  44. Young G. M., Miller V. L. 1997; Identification of novel chromosomal loci affecting Yersinia enterocolitica pathogenesis. Mol Microbiol 25:319–328 [CrossRef]
     [Google Scholar]
/content/journal/micro/10.1099/mic.0.27946-0
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DNA methylation in Yersinia enterocolitica: role of the DNA adenine methyltransferase in mismatch repair and regulation of virulence factors
Microbiology 151, 2291 (2005); https://doi.org/10.1099/mic.0.27946-0
/content/journal/micro/10.1099/mic.0.27946-0
/content/journal/micro/10.1099/mic.0.27946-0
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