1887

Abstract

Inactivation of the gene encoding DNA adenine methylase () has been shown to attenuate some pathogens such as serovar Typhimurium and is a lethal mutation in others such as strain YPIII. In this study the methylase gene in strain IP32953 was inactivated. Unlike the wild-type, DNA isolated from the mutant could be digested with I, which is consistent with an altered pattern of DNA methylation. The mutant was sensitive to bile salts but not to 2-aminopurine. The effect of inactivation on gene expression was examined using a DNA microarray. In BALB/c mice inoculated orally or intravenously with the mutant, the median lethal dose (MLD) was at least 10-fold higher than the MLD of the wild-type. BALB/c mice inoculated with the mutant were protected against a subcutaneous challenge with 100 MLDs of strain GB and an intravenous challenge with 300 MLDs of IP32953.

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2005-06-01
2020-08-07
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References

  1. Achtman M., Zurth K., Morelli G., Torrea G., Guiyoule A., Carniel E. 1999; Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis. Proc Natl Acad Sci U S A96:14043–14048[CrossRef]
    [Google Scholar]
  2. Barras F., Marinus M. G. 1989; The great GATC: DNA methylation in E. coli. Trends Genet5:139–143[CrossRef]
    [Google Scholar]
  3. Boye E., Lobner-Olesen A. 1990; The role of dam methyltransferase in the control of DNA replication inE. coli. Cell62:981–989[CrossRef]
    [Google Scholar]
  4. Brubaker R. R. 1991; Factors promoting acute and chronic diseases caused by yersiniae. Clin Microbiol Rev4:309–324
    [Google Scholar]
  5. Bucci C., Lavitola A., Salvatore P., Del Giudice L., Massardo D. R., Bruni C. B., Alifano P. 1999; Hypermutation in pathogenic bacteria: frequent phase variation in meningococci is a phenotypic trait of a specialized mutator biotype. Mol Cell3:435–445[CrossRef]
    [Google Scholar]
  6. de Almeida A. M. P., Guiyoule A., Guilvout I., Iteman I., Baranton G., Carniel E. 1993; Chromosomal irp2 gene in Yersinia: distribution, expression, deletion and impact on virulence. Microb Pathog14:9–21[CrossRef]
    [Google Scholar]
  7. Donnenburg M. S., Kaper J. B. 1991; Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide mutant. Infect Immun59:4310–4317
    [Google Scholar]
  8. Dower W. J., Miller J. F., Ragsdale C. W. 1988; High efficiency transformation of Escherichia coli by high voltage electroporation. Nucleic Acids Res16:6127–6145[CrossRef]
    [Google Scholar]
  9. Fukushima H., Hao Q., Wu K.. 7 other authors 2001; Yersinia enterocolitica O9 as a possible barrier against Y. pestis in natural plague foci in Ningxia, China. Curr Microbiol42:1–7[CrossRef]
    [Google Scholar]
  10. Glickman B., van den Elsen P., Radman M. 1978; Induced mutagenesis in dam mutants of Escherichia coli: a role for 6-methyladenine residues in mutation avoidance. Mol Gen Genet163:307–312[CrossRef]
    [Google Scholar]
  11. Grinter N. J. 1983; A broad-host-range cloning vector transposable to various replicons. Gene21:133–143[CrossRef]
    [Google Scholar]
  12. Guo L., Lim K. B., Gunn J. S., Bainbridge B., Darveau R. P., Hackett M., Miller S. I. 1997; Regulation of lipid A modification by Salmonella typhimurium virulence genes phoP-phoQ. Science276:250–253[CrossRef]
    [Google Scholar]
  13. Heithoff D. M., Sinsheimer R. L., Low D. A., Mahan M. J. 1999; An essential role for DNA adenine methylation in bacterial virulence. Science284:967–970[CrossRef]
    [Google Scholar]
  14. 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 Immun69:6725–6730[CrossRef]
    [Google Scholar]
  15. Jonczyk P., Hines R., Smith D. W. 1989; The Escherichia coli dam gene is expressed as a distal gene of a new operon. Mol Gen Genet217:85–96[CrossRef]
    [Google Scholar]
  16. 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 Immun69:7610–7615[CrossRef]
    [Google Scholar]
  17. Li S. R., Dorrell N., Everest P. H., Dougan G., Wren B. W. 1996; Construction and characterization of a Yersinia enterocolitica O : 8 high-temperature requirement (htrA) isogenic mutant. Infect Immun64:2088–2094
    [Google Scholar]
  18. Ljungberg P., Valtonen M., Harjola V. P., Kaukoranta-Tolvanen S. S., Vaara M. 1995; Report of four cases of Yersinia pseudotuberculosis septicemia and a literature review. Eur J Clin Microbiol14:804–810[CrossRef]
    [Google Scholar]
  19. Metcalf W. W., Jiang W., Wanner B. L. 1994; Use of the rep technique for allele replacement to construct new Escherichia coli hosts for maintenance of R6K gamma origin plasmids at different copy numbers. Gene138:1–7[CrossRef]
    [Google Scholar]
  20. 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 Bacteriol170:2575–2583
    [Google Scholar]
  21. Nagano T., Kiyohara T., Suzuki K., Tsubokura M., Otsuki K. 1997; Identification of pathogenic strains within serogroups of Yersinia pseudotuberculosis and the presence of non-pathogenic strains isolated from animals and the environment. J Vet Med Sci59:153–158[CrossRef]
    [Google Scholar]
  22. Niskanen T., Fredriksson-Ahomaa M., Korkeala H. 2002; Yersinia pseudotuberculosis with limited genetic diversity is a common finding in tonsils of fattening pigs. J Food Prot65:540–545
    [Google Scholar]
  23. Noyer-Weidner M., Trautner T. A. 1993; Methylation of DNA in Prokaryotes. In DNA Methylation: Molecular Biology and Biological Significance pp39–108 Edited by Jost J. P., Saluz H. P.. Switzerland: Birkhauser Verlag;
    [Google Scholar]
  24. Oh T. J., Kim I. G. 1999; Identification of genetic factors altering the SOS induction of DNA damage-inducible yebG gene in Escherichia coli. FEMS Microbiol Lett177:271–277[CrossRef]
    [Google Scholar]
  25. 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 Microbiol45:673–695[CrossRef]
    [Google Scholar]
  26. Ostendorf T., Cherepanov P., De Vries J., Wackernagel W. 1999; Characterization of a dam mutant of Serratia marcescens and nucleotide sequence of the dam region. J Bacteriol181:3880–3885
    [Google Scholar]
  27. Oyston P. C., Russell P., Williamson E. D., Titball R. W. 1996; An aroA mutant of Yersinia pestis is attenuated in guinea-pigs, but virulent in mice. Microbiology142:1847–1853[CrossRef]
    [Google Scholar]
  28. Oyston P. C., Dorrell N., Williams K., Li S. R., Green M., Titball R. W., Wren B. W. 2000; The response regulator PhoP is important for survival under conditions of macrophage-induced stress and virulence in Yersinia pestis. Infect Immun68:3419–3425[CrossRef]
    [Google Scholar]
  29. Parkhill J., Wren B. W., Thompson N. R. & 33 other authors. 2001; Genome sequence of Yersinia pestis, causative agent of plague. Nature413:523–527[CrossRef]
    [Google Scholar]
  30. Peterson K. R., Wertman K. F., Mount D. W., Marinus M. G. 1985; Viability of Escherichia coli K-12 DNA adenine methylase (dam) mutants requires increased expression of specific genes in the SOS regulon. Mol Gen Genet201:14–19[CrossRef]
    [Google Scholar]
  31. Prior J., Hitchin P. G., Wiliamson E. D., Reason A. J., Morris H. R., Dell A., Wren B., Titball R. W. 2001; Characterisation of the lipopolysaccharide of Yersinia pestis. Microb Pathog30:49–57[CrossRef]
    [Google Scholar]
  32. Pucciarelli M. G., Prieto A. I., Casadesus J., Portillo F. G. 2002; Envelope instability in DNA adenine methylase mutants of Salmonella enterica. Microbiology148:1171–1182
    [Google Scholar]
  33. Putzker M., Sauer H., Sobe D. 2001; Plague and other human infections caused by Yersinia species. Clin Lab47:453–466
    [Google Scholar]
  34. Reed L. J., Muench H. 1938; A simple method for estimating fifty percent endpoints. Am J Hyg27:493–497
    [Google Scholar]
  35. Ritchie L. J., Hall R. M., Podger D. M. 1986; Mutant of Salmonella typhimurium LT2 deficient in DNA adenine methylation. J Bacteriol167:420–422
    [Google Scholar]
  36. Roggenkamp A., Geiger A. M., Leitritz L., Kessler A., Heesemann J. 1997; Passive immunity to infection with Yersinia spp. mediated by anti-recombinant V antigen is dependent on polymorphism of V antigen. Infect Immun65:446–451
    [Google Scholar]
  37. Sambrook J., Fritsch E. F., Maniatis T. 1989; Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  38. Sanford S. E. 1995; Outbreaks of yersiniosis caused by Yersinia pseudotuberculosis in farmed cervids. J Vet Diagn Invest7:78–81[CrossRef]
    [Google Scholar]
  39. Schmidt A., Schaffelhofer S., Muller K., Rollinghoff M., Beuscher H. U. 1999; Analysis of the Yersinia enterocolitica O : 8 V antigen for cross protectivity. Microb Pathog26:221–233[CrossRef]
    [Google Scholar]
  40. Simonet M., Berche P., Mazigh D., Veron M. 1985; Protection against Yersinia infection by non-virulence-plasmid-encoded antigens. J Med Microbiol20:225–231[CrossRef]
    [Google Scholar]
  41. Skurnik M., Peippo A., Ervela E. 2000; Characterization of the O-antigen gene clusters of Yersinia pseudotuberculosis and the cryptic O-antigen gene cluster of Yersinia pestis shows that the plague bacillus is most closely related to and has evolved fromY. pseudotuberculosis serotype O : 1b. Mol Microbiol37:316–330[CrossRef]
    [Google Scholar]
  42. Titball R. W., Williamson E. D. 2004; Yersinia pestis (plague) vaccines. Expert Opin Biol Ther4:965–973[CrossRef]
    [Google Scholar]
  43. Torreblanca J., Casadesus J. 1996; DNA adenine methylase mutants of Salmonella typhimurium and a novel dam-regulated locus. Genetics144:15–26
    [Google Scholar]
  44. Williams K., Oyston P. C., Dorrell N., Li S., Titball R. W., Wren B. W. 2000; Investigation into the role of the serine protease HtrA in Yersinia pestis pathogenesis. FEMS Microbiol Lett186:281–286[CrossRef]
    [Google Scholar]
  45. Yura T., Kanemori A., Morita M. T. 2000; The heat shock response: regulation and function. In Bacterial Stress Responses pp3–18 Edited by Stortz G., Hengge-Aronis R.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
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