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
2019-10-16
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References

  1. Asikainen, S. & Alaluusua, S. ( 1993; ). Bacteriology of dental infections. Eur Heart J 14 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. Biotechniques 14, 527-528.
    [Google Scholar]
  3. Brot, N. & Weissbach, H. ( 1991; ). Biochemistry of methionine sulfoxide residues in proteins. Biofactors 3, 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 USA 78, 2155-2158.[CrossRef]
    [Google Scholar]
  5. Cao, P., McClain, M. S., Forsyth, M. H. & Cover, T. L. ( 1998; ). Extracellular release of antigenic proteins by Helicobacter pylori. Infect Immun 66, 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 Bacteriol 183, 5645-5650.[CrossRef]
    [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 Bacteriol 182, 4068-4076.[CrossRef]
    [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.[CrossRef]
    [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 Pathog 30, 359-368.[CrossRef]
    [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 Microbiol 37, 1417-1435.[CrossRef]
    [Google Scholar]
  11. Hassouni, M. E., Chambost, J. P., Expert, D., Van Gijsegem, F. & Barras, F. ( 1999; ). The minimal gene set member msrA, encoding peptide methionine sulfoxide reductase, is a virulence determinant of the plant pathogen Erwinia chrysanthemi. Proc Natl Acad Sci USA 96, 887-892.[CrossRef]
    [Google Scholar]
  12. Inouye, T., Ohta, H., Kokeguchi, S., Fukui, K. & Kato, K. ( 1990; ). Colonial variation and fimbriation of Actinobacillus actinomycetemcomitans. FEMS Microbiol Lett 57, 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 Dis 11, 46-63.[CrossRef]
    [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 Lett 456, 17-21.[CrossRef]
    [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 Res 16, 379-389.[CrossRef]
    [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 Chemother 35, 1804-1810.[CrossRef]
    [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 Immunol 8, 94-99.[CrossRef]
    [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 USA 97, 6463-6468.[CrossRef]
    [Google Scholar]
  19. Meyer, D. H. & Fives-Taylor, P. M. ( 1994; ). Characteristics of adherence of Actinobacillus actinomycetemcomitans to epithelial cells. Infect Immun 62, 928-935.
    [Google Scholar]
  20. Mintz, K. P. & Fives-Taylor, P. M. ( 1994; ). Adhesion of Actinobacillus actinomycetemcomitans to a human oral cell line. Infect Immun 62, 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 Immunol 14, 109-116.[CrossRef]
    [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 Immun 68, 6580-6586.[CrossRef]
    [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 Lett 206, 87-92.[CrossRef]
    [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 Bacteriol 177, 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 USA 93, 3205-3208.[CrossRef]
    [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 USA 93, 2095-2099.[CrossRef]
    [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 USA 95, 14071-14075.[CrossRef]
    [Google Scholar]
  28. Moskovitz, J., Berlett, B. S., Poston, J. M. & Stadtman, E. R. ( 1999; ). Methionine sulfoxide reductase in antioxidant defence. Methods Enzymol 300, 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 Chem 275, 14167-14172.[CrossRef]
    [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 USA 98, 12920-12925.[CrossRef]
    [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 Commun 290, 62-65.[CrossRef]
    [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 Immun 37, 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 , pp. 105-111. Edited by H. A. Erlich. New York:Stockton Press.
  34. Preus, H. R., Namork, E. & Olsen, I. ( 1988; ). Fimbriation of Actinobacillus actinomycetemcomitans. Oral Microbiol Immunol 3, 93-94.[CrossRef]
    [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 Chem 267, 15549-15551.
    [Google Scholar]
  36. Rosan, B., Slots, J., Lamont, R. J., Listgarten, M. A. & Nelson, G. M. ( 1988; ). Actinobacillus actinomycetemcomitans fimbriae. Oral Microbiol Immunol 3, 58-63.[CrossRef]
    [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.
  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 Immun 55, 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. Microbiology 147, 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 USA 99, 10108-10113.[CrossRef]
    [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 Periodontol 13, 570-577.[CrossRef]
    [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 Immun 59, 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 Immunol 8, 361-369.[CrossRef]
    [Google Scholar]
  44. Storz, G. & Imlay, J. A. ( 1999; ). Oxidative stress. Curr Opin Microbiol 2, 188-194.[CrossRef]
    [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 J 7, 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 Bacteriol 174, 5978-5981.
    [Google Scholar]
  47. Thomson, V. J., Bhattacharjee, M. K., Fine, D. H., Derbyshire, K. M. & Figurski, D. H. ( 1999; ). Direct selection of IS903 transposon insertions by use of a broad-host-range vector: isolation of catalase-deficient mutants of Actinobacillus actinomycetemcomitans. J Bacteriol 181, 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. Nature 388, 539–547.[CrossRef]
    [Google Scholar]
  49. von Heijne, G. ( 1986; ). A new method for predicting signal sequence cleavage sites. Nucleic Acids Res 14, 4683-4690.[CrossRef]
    [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 Immun 68, 1061-1068.[CrossRef]
    [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 Immun 69, 2748-2752.[CrossRef]
    [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 USA 93, 7985-7990.[CrossRef]
    [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.[CrossRef]
    [Google Scholar]
  54. Zambon, J. J. ( 1985; ). Actinobacillus actinomycetemcomitans in human periodontal disease. J Clin Periodontol 12, 1-20.[CrossRef]
    [Google Scholar]
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