1887

Abstract

is an oral pathogen that is a causative agent for periodontal disease as well as other non-oral infections. The chronic inflammation associated with periodontal diseases suggests that the bacterium must be able to neutralize oxygen intermediates to survive in the host tissues. Methionine sulfoxide reductase (MsrA) is an enzyme that has been demonstrated to have a role in protection against oxidative damage and has also been identified to be required for the proper expression or maintenance of functional adhesins on the surface of several pathogenic bacteria. The homologue of has been isolated and a chromosomal insertion mutant constructed by allele replacement mutagenesis. Inactivation of the gene led to a complete loss of enzymic activity toward a synthetic substrate. However, the isogenic mutant was not more sensitive to oxidative stress or less adherent to epithelial cells as compared with the parent strain. These data suggest that this strain of has redundant systems that compensate for the MsrA activities ascribed for other organisms.

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2002-11-01
2020-04-04
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References

  1. Asikainen S., Alaluusua S. 1993; Bacteriology of dental infections. Eur Heart J14 Suppl K:43–50
    [Google Scholar]
  2. Berghammer H., Auer B. 1993; ’Easypreps’: fast and easy plasmid minipreparation for the analysis of recombinant clones in E. coli . Biotechniques14:527–528
    [Google Scholar]
  3. Brot N., Weissbach H. 1991; Biochemistry of methionine sulfoxide residues in proteins. Biofactors3:91–96
    [Google Scholar]
  4. Brot N, Weissbach L, Werth J., Weissbach H. 1981; Enzymatic reduction of protein-bound methionine sulfoxide. Proc Natl Acad Sci USA78:2155–2158
    [Google Scholar]
  5. Cao P, McClain M. S, Forsyth M. H., Cover T. L. 1998; Extracellular release of antigenic proteins by Helicobacter pylori . Infect Immun66:2984–2986
    [Google Scholar]
  6. Dhandayuthapani S, Blaylock M. W, Bebear C. M, Rasmussen W. G., Baseman J. B. 2001; Peptide methionine sulfoxide reductase (MsrA) is a virulence determinant in Mycoplasma genitalium . J Bacteriol183:5645–5650
    [Google Scholar]
  7. Feilmeier B. J, Iseminger G, Schroeder D, Webber H., Phillips G. J. 2000; Green fluorescent protein functions as a reporter for protein localization in Escherichia coli . J Bacteriol182:4068–4076
    [Google Scholar]
  8. Fives-Taylor P. M, Meyer D. H, Mintz K. P., Brissette C. 1999; Virulence factors of Actinobacillus actinomycetemcomitans . Periodontol 2000;20:136–167
    [Google Scholar]
  9. Fletcher J. M, Nair S. P, Ward J. M, Henderson B., Wilson M. 2001; Analysis of the effect of changing environmental conditions on the expression patterns of exported surface-associated proteins of the oral pathogen Actinobacillus actinomycetemcomitans . Microb Pathog30:359–368
    [Google Scholar]
  10. Guy R. L, Gonias L. A., Stein M. A. 2000; Aggregation of host endosomes by Salmonella requires SPI2 translocation of sseFG and involves spvR and the fms - aroE intragenic region. Mol Microbiol37:1417–1435
    [Google Scholar]
  11. Hassouni M. E, Chambost J. P, Expert D, Van Gijsegem F., Barras F. 1999; The minimal gene set member msr A, encoding peptide methionine sulfoxide reductase, is a virulence determinant of the plant pathogen Erwinia chrysanthemi . Proc Natl Acad Sci USA96:887–892
    [Google Scholar]
  12. Inouye T, Ohta H, Kokeguchi S, Fukui K., Kato K. 1990; Colonial variation and fimbriation of Actinobacillus actinomycetemcomitans . FEMS Microbiol Lett57:13–17
    [Google Scholar]
  13. Kaplan A. H, Weber D. J, Oddone E. Z., Perfect J. R. 1989; Infection due to Actinobacillus actinomycetemcomitans : 15 cases and review. Rev Infect Dis11:46–63
    [Google Scholar]
  14. Kuschel L, Hansel A, Schonherr R, Weissbach H, Brot N, Hoshi T., Heinemann S. H. 1999; Molecular cloning and functional expression of a human peptide methionine sulfoxide reductase (hMsrA). FEBS Lett456:17–21
    [Google Scholar]
  15. Lai C. H, Listgarten M. A., Hammond B. F. 1981; Comparative ultrastructure of leukotoxic and non-leukotoxic strains of Actinobacillus actinomycetemcomitans . J Periodontal Res16:379–389
    [Google Scholar]
  16. LeBlanc D. J, Lee L. N., Inamine J. M. 1991; Cloning and nucleotide base sequence analysis of a spectinomycin adenyltransferase AAD(9) determinant from Enterococcus faecalis . Antimicrob Agents Chemother35:1804–1810
    [Google Scholar]
  17. LeBlanc D. J, Lee L. N, Abu-Al-Jaibat A. R, Sreenivasan P. K., Fives-Taylor P. M. 1993; Identification of plasmids in Actinobacillus actinomycetemcomitans and construction of intergeneric shuttle plasmids. Oral Microbiol Immunol8:94–99
    [Google Scholar]
  18. Lowther W. T, Brot N, Weissbach H, Honek J. F., Matthews B. W. 2000; Thiol-disulfide exchange is involved in the catalytic mechanism of peptide methionine sulfoxide reductase. Proc Natl Acad Sci USA97:6463–6468
    [Google Scholar]
  19. Meyer D. H., Fives-Taylor P. M. 1994; Characteristics of adherence of Actinobacillus actinomycetemcomitans to epithelial cells. Infect Immun62:928–935
    [Google Scholar]
  20. Mintz K. P., Fives-Taylor P. M. 1994; Adhesion of Actinobacillus actinomycetemcomitans to a human oral cell line. Infect Immun62:3672–3678
    [Google Scholar]
  21. Mintz K. P., Fives-Taylor P. M. 1999; Binding of the periodontopathogen Actinobacillus actinomycetemcomitans to extracellular matrix proteins. Oral Microbiol Immunol14:109–116
    [Google Scholar]
  22. Mintz K. P., Fives-Taylor P. M. 2000; impA , a gene coding for an inner membrane protein, influences colonial morphology of Actinobacillus actinomycetemcomitans . Infect Immun68:6580–6586
    [Google Scholar]
  23. Mintz K. P, Brissette C., Fives-Taylor P. M. 2002; A recombinase A-deficient strain of Actinobacillus actinomycetemcomitans constructed by insertional mutagenesis using a mobilizable plasmid. FEMS Microbiol Lett206:87–92
    [Google Scholar]
  24. Moskovitz J, Rahman M. A, Strassman J, Yancey S. O, Kushner S. R, Brot N., Weissbach H. 1995; Escherichia coli peptide methionine sulfoxide reductase gene: regulation of expression and role in protecting against oxidative damage. J Bacteriol177:502–507
    [Google Scholar]
  25. Moskovitz J, Jenkins N. A, Gilbert D. J, Copeland N. G, Jursky F, Weissbach H., Brot N. 1996a; Chromosomal localization of the mammalian peptide-methionine sulfoxide reductase gene and its differential expression in various tissues. Proc Natl Acad Sci USA93:3205–3208
    [Google Scholar]
  26. Moskovitz J, Weissbach H., Brot N. 1996b; Cloning and the expression of a mammalian gene involved in the reduction of methionine sulfoxide residues in proteins. Proc Natl Acad Sci USA93:2095–2099
    [Google Scholar]
  27. Moskovitz J, Flescher E, Berlett B. S, Azare J, Poston J. M., Stadtman E. R. 1998; Overexpression of peptide-methionine sulfoxide reductase in Saccharomyces cerevisiae and human T cells provides them with high resistance to oxidative stress. Proc Natl Acad Sci USA95:14071–14075
    [Google Scholar]
  28. Moskovitz J, Berlett B. S, Poston J. M., Stadtman E. R. 1999; Methionine sulfoxide reductase in antioxidant defence. Methods Enzymol300:239–244
    [Google Scholar]
  29. Moskovitz J, Poston J. M, Berlett B. S, Nosworthy N. J, Szczepanowski R., Stadtman E. R. 2000; Identification and characterization of a putative active site for peptide methionine sulfoxide reductase (MsrA) and its substrate stereospecificity. J Biol Chem275:14167–14172
    [Google Scholar]
  30. Moskovitz J, Bar-Noy S, Williams W. M, Requena J, Berlett B. S., Stadtman E. R. 2001; Methionine sulfoxide reductase (MsrA) is a regulator of antioxidant defense and lifespan in mammals. Proc Natl Acad Sci USA98:12920–12925
    [Google Scholar]
  31. Moskovitz J, Singh V. K, Requena J, Wilkinson B. J, Jayaswal R. K., Stadtman E. R. 2002; Purification and characterization of methionine sulfoxide reductase from mouse and Staphylococcus aureus and their substrate stereospecificity. Biochem Biophys Res Commun290:62–65
    [Google Scholar]
  32. Nowotny A, Behling U. H, Hammond B, Lai C. H, Listgarten M, Pham P. H., Sanavi F. 1982; Release of toxic microvesicles by Actinobacillus actinomycetemcomitans . Infect Immun37:151–154
    [Google Scholar]
  33. Ochman H, Ajoka J. W, Garaza D., Hartl D. L. 1989; Inverse polymerase chain reaction. In PCR Technology: Principles and Applications for DNA Amplification pp105–111 Edited by Erlich H. A.. New York: Stockton Press;
    [Google Scholar]
  34. Preus H. R, Namork E., Olsen I. 1988; Fimbriation of Actinobacillus actinomycetemcomitans . Oral Microbiol Immunol3:93–94
    [Google Scholar]
  35. Rahman M. A, Nelson H, Weissbach H., Brot N. 1992; Cloning, sequencing, and expression of the Escherichia coli peptide methionine sulfoxide reductase gene. J Biol Chem267:15549–15551
    [Google Scholar]
  36. Rosan B, Slots J, Lamont R. J, Listgarten M. A., Nelson G. M. 1988; Actinobacillus actinomycetemcomitans fimbriae. Oral Microbiol Immunol3:58–63
    [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. Scannapieco F. A, Millar S. J, Reynolds H. S, Zambon J. J., Levine M. J. 1987; Effect of anaerobiosis on the surface ultrastructure and surface proteins of Actinobacillus actinomycetemcomitans (Haemophilus actinomycetemcomitans) . Infect Immun55:2320–2323
    [Google Scholar]
  39. Singh V. K, Moskovitz J, Wilkinson B. J., Jayaswal R. K. 2001; Molecular characterization of a chromosomal locus in Staphylococcus aureus that contributes to oxidative defence and is highly induced by the cell-wall-active antibiotic oxacillin. Microbiology147:3037–3045
    [Google Scholar]
  40. Skaar E. P, Tobiason D. M, Quick J, Judd R. C, Weissbach H, Etienne F, Brot N., Seifert H. S. 2002; The outer membrane localization of the Neisseria gonorrhoeae MsrA/B is involved in survival against reactive oxygen species. Proc Natl Acad Sci USA99:10108–10113
    [Google Scholar]
  41. Slots J, Bragd L, Wikstrom M., Dahlen G. 1986; The occurrence of Actinobacillus actinomycetemcomitans, Bacteroides gingivalis and Bacteroides intermedius in destructive periodontal disease in adults. J Clin Periodontol13:570–577
    [Google Scholar]
  42. Sreenivasan P. K, LeBlanc D. J, Lee L. N., Fives-Taylor P. M. 1991; Transformation of Actinobacillus actinomycetemcomitans by electroporation, utilizing constructed shuttle plasmids. Infect Immun59:4621–4627
    [Google Scholar]
  43. Sreenivasan P. K, Meyer D. H., Fives-Taylor P. M. 1993; Factors influencing the growth and viability of Actinobacillus actinomycetemcomitans . Oral Microbiol Immunol8:361–369
    [Google Scholar]
  44. Storz G., Imlay J. A. 1999; Oxidative stress. Curr Opin Microbiol2:188–194
    [Google Scholar]
  45. Taha M. K, So M, Seifert H. S, Billyard E., Marchal C. 1988; Pilin expression in Neisseria gonorrhoeae is under both positive and negative transcriptional control. EMBO J7:4367–4378
    [Google Scholar]
  46. Taha M. K, Larribe M, Dupuy B, Giorgini D., Marchal C. 1992; Role of pilA , an essential regulatory gene of Neisseria gonorrhoeae , in the stress response. J Bacteriol174:5978–5981
    [Google Scholar]
  47. Thomson V. J, Bhattacharjee M. K, Fine D. H, Derbyshire K. M., Figurski D. H. 1999; Direct selection of IS 903 transposon insertions by use of a broad-host-range vector: isolation of catalase-deficient mutants of Actinobacillus actinomycetemcomitans . J Bacteriol181:7298–7307
    [Google Scholar]
  48. Tomb J. F, White O, Kerlavage A. R.. 39 other authors 1997; The complete genome sequence of the gastric pathogen Helicobacter pylori . Nature388:539–547
    [Google Scholar]
  49. von Heijne G. 1986; A new method for predicting signal sequence cleavage sites. Nucleic Acids Res14:4683–4690
    [Google Scholar]
  50. Vriesema A. J, Dankert J., Zaat S. A. 2000; A shift from oral to blood pH is a stimulus for adaptive gene expression of Streptococcus gordonii CH1 and induces protection against oxidative stress and enhanced bacterial growth by expression of msrA . Infect Immun68:1061–1068
    [Google Scholar]
  51. Ward J, Fletcher J, Nair S. P, Wilson M, Williams R. J, Poole S., Henderson B. 2001; Identification of the exported proteins of the oral opportunistic pathogen Actinobacillus actinomycetemcomitans by using alkaline phosphatase fusions. Infect Immun69:2748–2752
    [Google Scholar]
  52. Wizemann T. M, Moskovitz J, Pearce B. J, Cundell D, Arvidson C. G, So M, Weissbach H, Brot N., Masure H. R. 1996; Peptide methionine sulfoxide reductase contributes to the maintenance of adhesins in three major pathogens. Proc Natl Acad Sci USA93:7985–7990
    [Google Scholar]
  53. Zadeh H. H, Nichols F. C., Miyasaki K. T. 1999; The role of the cell-mediated immune response to Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis in periodontitis. Periodontol 2000;20:239–288
    [Google Scholar]
  54. Zambon J. J. 1985; Actinobacillus actinomycetemcomitans in human periodontal disease. J Clin Periodontol12:1–20
    [Google Scholar]
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