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Volume 147, Issue 1

resistance of complex isolates to reactive oxygen species in relation to catalase and superoxide dismutase production Free

Abstract

The complex comprises groups of genomovars (genotypically distinct strains with very similar phenotypes) that have emerged as important opportunistic pathogens in cystic fibrosis (CF) patients. The inflammatory response against bacteria in the airways of CF individuals is dominated by polymorphonuclear cells and involves the generation of oxidative stress, which leads to further inflammation and tissue damage. Bacterial catalase, catalase-peroxidase and superoxide dismutase activities may contribute to the survival of following exposure to reactive oxygen metabolites generated by host cells in response to infection. In the present study the authors investigated the production of catalase, peroxidase and SOD by isolates belonging to various genomovars of the complex. Production of both catalase and SOD was maximal during late stationary phase in almost all isolates examined. Native PAGE identified 13 catalase electrophoretotypes and two SOD electrophoretotypes (corresponding to an Fe-SOD class) in strains belonging to the six genomovars of the complex. Seven out of 11 strains displaying high-level survival after HO treatment had a bifunctional catalase/peroxidase, and included all the genomovar III strains examined. These isolates represent most of the epidemic isolates that are often associated with the cepacia syndrome. The majority of the isolates from all the genomovars were resistant to extracellular \(O_{2}^{{-}}\) , while resistance to intracellularly generated \(O_{2}^{{-}}\) was highly variable and could not be correlated with the detected levels of SOD activity. Altogether the results suggest that resistance to toxic oxygen metabolites from extracellular sources may be a factor involved in the persistence of in the airways of CF individuals.

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Keyword(s): CF, cystic fibrosis , CGD, chronic granulomatous disease , chronic granulomatous disease , cystic fibrosis , hydrogen peroxide , oxidative stress , SOD, superoxide dismutase and superoxide anion
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2001-01-01
2025-11-08

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References

  1. Bals, R., Weiner, D. J. & Wilson, J. M.(1999). The innate immune system in cystic fibrosis lung disease. J Clin Invest 103, 303-307.[CrossRef] [Google Scholar]
  2. Bandyopadhyay, P. & Steinman, H. M.(1998).Legionella pneumophila catalase-peroxidases: cloning of the katB gene and studies of KatB function. J Bacteriol 180, 5369-5374. [Google Scholar]
  3. Bannister, J. V. & Calabrese, L.(1987). Assays for superoxide dismutase. Methods Biochem Anal 32, 279-312. [Google Scholar]
  4. Barnes, A. C., Horne, M. T. & Ellis, A. E.(1996). Effect of iron on expression of superoxide dismutase by Aeromonas salmonicida and associated resistance to superoxide anion. FEMS Microbiol Lett 142, 19-26.[CrossRef] [Google Scholar]
  5. Barnes, A. C., Balebona, M. C., Horne, M. T. & Ellis, A. E.(1999). Superoxide dismutase and catalase in Photobacterium damselae subsp. piscidia and their roles in resistance to reactive oxygen species. Microbiology 145, 483-494.[CrossRef] [Google Scholar]
  6. Beauchamp, C. & Fridovich, I.(1971). Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44, 276-287.[CrossRef] [Google Scholar]
  7. Brown, S. M., Howell, M. L., Vasil, M. L., Anderson, A. J. & Hassett, D. J.(1995). Cloning and characterization of the katB gene of Pseudomonas aeruginosa encoding a hydrogen peroxide-inducible catalase: purification of KatB, cellular localization, and demonstration that it is essential for optimal resistance to hydrogen peroxide. J Bacteriol 177, 6536-6544. [Google Scholar]
  8. Burkholder, W. H.(1950). Sour skin, a bacterial rot of onion bulbs. Phytopathology 40, 115-117. [Google Scholar]
  9. Burns, J. L., Jonas, M., Chi, E. Y., Clark, D. K., Berger, A. & Griffith, A.(1996). Invasion of respiratory epithelial cells by Burkholderia (Pseudomonas) cepacia. Infect Immun 64, 4054-4059. [Google Scholar]
  10. Carlioz, A. & Touati, D.(1986). Isolation of superoxide dismutase mutants in Escherichia coli: is superoxide dismutase necessary for aerobic life? EMBO J 5, 623-630. [Google Scholar]
  11. Cline, M. J.(1975). Chemotaxis, phagocytosis and microbial killing. In The White Cell , pp. 71-82. Edited by M. J. Cline. Cambridge, MA:Harvard University Press.
  12. De Groote, M. A., Ochsner, U. A., Shiloh, M. U. & 7 other authors (1997). Periplasmic superoxide dismutase protects Salmonella from products of phagocyte NADPH-oxidase and nitric oxide synthase. Proc Natl Acad Sci USA 94, 13997–14001.[CrossRef] [Google Scholar]
  13. Fang, F. C., DeGroote, M. A., Foster, J. H. & 8 other authors (1999). Virulent Salmonella typhimurium has two periplasmic Cu,Zn-superoxide dismutases. Proc Natl Acad Sci USA 96, 7502–7507.[CrossRef] [Google Scholar]
  14. Forehand, J. R., Johnston, R. B. J. & Bomalaski, J. S.(1993). Phospholipase A2 activity in human neutrophils. Stimulation by lipopolysaccharide and possible involvement in priming for an enhanced respiratory burst. J Immunol 151, 4918-4925. [Google Scholar]
  15. Franzon, V. L., Arondel, I. & Sansonetti, P. I.(1990). Contribution of superoxide dismutase and catalase activities to Shigella flexneri pathogenesis. Infect Immun 58, 529-535. [Google Scholar]
  16. Fridovich, I.(1978). The biology of oxygen radicals. Science 201, 875-879.[CrossRef] [Google Scholar]
  17. Gillis, M., Van, T. V., Bardin, R. & 7 other authors (1995). Polyphasic taxonomy in the genus Burkholderia leading to an emended description of the genus and proposition of Burkholderia vietnamiensis sp. nov. for N2-fixing isolates from rice in Vietnam. Int J Syst Bacteriol 45, 274–289.[CrossRef] [Google Scholar]
  18. Govan, J. R. W. & Deretic, V.(1996). Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol Rev 60, 539-574. [Google Scholar]
  19. Govan, J. R. W. & Vandamme, P.(1998). Agricultural and medical microbiology: a time for bridging gaps. Microbiology 144, 2373-2375.[CrossRef] [Google Scholar]
  20. Govan, J. R., Hughes, J. E. & Vandamme, P.(1996).Burkholderia cepacia: medical, taxonomic and ecological issues. J Med Microbiol 45, 395-407.[CrossRef] [Google Scholar]
  21. Heikkila, R. E. & Cabbat, F.(1976). A sensitive assay for superoxide dismutase based on the autoxidation of 6-hydroxydopamine. Anal Biochem 75, 356-362.[CrossRef] [Google Scholar]
  22. Hughes, J. E., Stewart, J., Barclay, G. R. & Govan, J. R.(1997). Priming of neutrophil respiratory burst activity by lipopolysaccharide from Burkholderia cepacia. Infect Immun 65, 4281-4287. [Google Scholar]
  23. Imlay, J. A. & Linn, S.(1988). DNA damage and oxygen radical toxicity. Science 240, 1302-1309.[CrossRef] [Google Scholar]
  24. Katsuwon, J. & Anderson, A. J.(1989). Response of plant-colonizing pseudomonads to hydrogen peroxide. Appl Environ Microbiol 55, 2985-2989. [Google Scholar]
  25. Katsuwon, J. & Anderson, A. J.(1992). Characterization of catalase activities in a root-colonizing isolate of Pseudomonas putida. Can J Microbiol 38, 1026-1032.[CrossRef] [Google Scholar]
  26. Kelley, T. G. & Drumm, M. L.(1998). Inducible nitric oxide synthase expression is reduced in cystic fibrosis murine and human airway epithelial cells. J Clin Invest 102, 1200-1207.[CrossRef] [Google Scholar]
  27. Kitzler, J. W., Minakami, H. & Fridovich, I.(1990). Effects of Paraquat on Escherichia coli: differences between B and K-12 strains. J Bacteriol 172, 686-690. [Google Scholar]
  28. Koch, C. & Hoiby, N.(1993). Pathogenesis of cystic fibrosis. Lancet 341, 1065-1069.[CrossRef] [Google Scholar]
  29. LiPuma, J. J., Dasen, S. E., Nielson, D. W., Stern, R. C. & Stull, T. L.(1990). Person-to-person transmission of Pseudomonas cepacia between patients with cystic fibrosis. Lancet 336, 1094-1096.[CrossRef] [Google Scholar]
  30. Loewen, P. C. & Triggs, B. L.(1984). Genetic mapping of katF, a locus that with katE affects the synthesis of a second catalase species in Escherichia coli. J Bacteriol 160, 668-675. [Google Scholar]
  31. Mahenthiralingam, E., Campbell, M. E., Henry, D. A. & Speert, D.(1996). Epidemiology of Burkholderia cepacia infection in patients with cystic fibrosis: analysis by randomly amplified polymorphic DNA fingerprinting. J Clin Microbiol 34, 2914-2930. [Google Scholar]
  32. Manca, C., Paul, S., Barry, C. L. I., Freedman, V. H. & Kaplan, G.(1999).Mycobacterium tuberculosis catalase and peroxidase activities and resistance to oxidative killing in human monocytes in vitro. Infect Immun 67, 74-79. [Google Scholar]
  33. Mandell, G. L.(1975). Catalase, superoxide dismutase, and virulence of Staphylococcus aureus. In vitro and in vivo studies with emphasis on staphylococcal–leukocyte interaction. J Clin Invest 55, 561-566.[CrossRef] [Google Scholar]
  34. Marcinkeviciene, J. A., Magliozzo, R. S. & Blanchard, J. S.(1995). Purification and characterization of the Mycobacterium smegmatis catalase-peroxidase involved in isoniazid activation. J Biol Chem 270, 22290-22295.[CrossRef] [Google Scholar]
  35. Marolda, C. L., Hauröder, B., John, M. A., Michel, R. & Valvano, M. A.(1999). Intracellular survival and saprophytic growth of isolates from the Burkholderia cepacia complex in free-living amoebae. Microbiology 145, 1509-1517.[CrossRef] [Google Scholar]
  36. Martin, D. W. & Mohr, C. D.(2000). Invasion and intracellular survival of Burkholderia cepacia. Infect Immun 68, 24-29.[CrossRef] [Google Scholar]
  37. Membrillo-Hernandez, J., Coopamah, M. D., Anjum, M. F., Stevanin, T. M., Kelly, A., Hughes, M. N. & Poole, R. K.(1999). The flavohemoglobin of Escherichia coli confers resistance to a nitrosating agent, a nitric oxide releaser, and paraquat and is essential for transcriptional responses to oxidative stress. J Biol Chem 274, 748-754.[CrossRef] [Google Scholar]
  38. Mongkolsuk, S., Loprasert, S., Vattanaviboon, P., Chanvanichayachai, C., Chamnongpol, S. & Supsamran, N.(1996). Heterologous growth phase- and temperature-dependent expression and H2O2 toxicity protection of a superoxide-inducible monofunctional catalase gene from Xanthomonas oryzae pv. oryzae. J Bacteriol 178, 3578-3584. [Google Scholar]
  39. Odell, E. W. & Segal, A. W.(1991). Killing of pathogens associated with chronic granulomatous disease by the non-oxidative microbicidal mechanisms of human neutrophils. J Med Microbiol 34, 129-135.[CrossRef] [Google Scholar]
  40. Palleroni, N. J.(1992). Human and animal pathogenic pseudomonads. In The Prokaryotes: a Handbook on the Biology of Bacteria; Ecophysiology, Isolation, Identification, Applications , pp. 3086-3103. Edited by A. Balows, H. G. Trüper, M. Dworkin, W. Harder & K. H. Schleifer. New York:Springer.
  41. Saini, L., Galsworthy, S., John, M. & Valvano, M. A.(1999). Intracellular survival of isolates from the Burkholderia cepacia complex in a murine macrophage cell line. Microbiology 145, 3465-3475. [Google Scholar]
  42. Schnell, S. & Steinman, H. M.(1995). Function and stationary-phase induction of periplasmic copper-zinc superoxide dismutase and catalase/peroxidase in Caulobacter crescentus. J Bacteriol 177, 5924-5929. [Google Scholar]
  43. Smith, A. W., Green, J., Eden, C. E. & Watson, M. L.(1999). Nitric oxide-induced potentiation of the killing of Burkholderia cepacia by reactive oxygen species: implications for cystic fibrosis. J Med Microbiol 48, 419-423.[CrossRef] [Google Scholar]
  44. Speert, D. P., Bond, M., Woodman, R. C. & Curnutte, J. T.(1994). Infection with Pseudomonas cepacia in chronic granulomatous disease: role of non-oxidative killing by neutrophils in host defense. J Infect Dis 170, 1524-1531.[CrossRef] [Google Scholar]
  45. Steinman, H. M.(1993). Function of periplasmic copper-zinc superoxide dismutase in Caulobacter crescentus. J Bacteriol 175, 1198-1202. [Google Scholar]
  46. Suttorp, N. & Simon, L. M.(1982). Lung cell oxidant injury. Enhancement of polymorphonuclear leukocyte-mediated cytotoxicity in lung cells exposed to sustained in vitro hyperoxia. J Clin Invest 70, 342-350.[CrossRef] [Google Scholar]
  47. Tablan, O. C., Chroba, T. L., Schidlow, D. V. & 7 other authors (1985).Pseudomonas cepacia colonization in patients with cystic fibrosis: risk factors and clinical outcome. J Pediatr 107, 382–387.[CrossRef] [Google Scholar]
  48. Tager, A. M., Wu, J. & Vermeulen, M. W.(1998). The effect of chloride concentration on human neutrophil functions: potential relevance to cystic fibrosis. Am J Respir Cell Mol Biol 19, 642-652. [Google Scholar]
  49. Tsolis, R. M., Baumler, A. J. & Heffron, F.(1995). Role of Salmonella typhimurium Mn-superoxide dismutase (SodA) in protection against early killing by J774 macrophages. Infect Immun 63, 1739-1744. [Google Scholar]
  50. Vandamme, P., Holmes, B., Vancanneyt, M. & 8 other authors (1997). Occurrence of multiple genomovars of Burkholderia cepacia in cystic fibrosis patients and proposal of Burkholderia multivorans sp. nov. Int J Syst Bacteriol 47, 1188–1200.[CrossRef] [Google Scholar]
  51. Vandamme, P., Mahenthiralingam, E., Holmes, B., Coyene, T., Hoste, B., De Vos, P., Henry, D. & Speert, D. P.(2000). Identification and population structure of Burkholderia stabilis sp. nov. (formerly Burkholderia cepacia Genomovar IV). J Clin Microbiol 38, 1042-1047. [Google Scholar]
  52. Wayne, L. G. & Diaz, G. A.(1986). A double staining method for differentiating between two classes of mycobacterial catalase in polyacrylamide electrophoresis gels. Anal Biochem 157, 89-92.[CrossRef] [Google Scholar]
  53. Weisiger, R. A. & Fridovich, I.(1973). Superoxide dismutase: organelle specificity. J Biol Chem 248, 3582-3592. [Google Scholar]
  54. Welch, D. F., Sword, C. P., Brehm, S. & Dusanic, D.(1979). Relationship between superoxide dismutase and pathogenic mechanisms of Listeria monocytogenes. Infect Immun 23, 863-872. [Google Scholar]
  55. Wilks, K. E., Dunn, K. L. R., Farrant, J. L., Reddin, K. M., Gorringe, A. R., Langford, P. R. & Kroll, J. S.(1998). Periplasmic superoxide dismutase in meningococcal pathogenicity. Infect Immun 66, 213-217. [Google Scholar]
  56. Worthen, G. S., Seccombe, J. F., Clay, K. L., Guthrie, L. A. & Johnston, R. B. J.(1988). The priming of neutrophils by lipopolysaccharide for production of intracellular platelet-activating factor. Potential role in mediation of enhanced superoxide secretion. J Immunol 140, 3553-3559. [Google Scholar]
  57. Xiu, Q. & Pan, S. Q.(2000). An Agrobacterium catalase is a virulence factor involved in tumourigenesis. Mol Microbiol 35, 407-414.[CrossRef] [Google Scholar]
  58. Zughaier, S. M., Ryley, H. C. & Jackson, S. K.(1999). Lipopolysaccharide (LPS) from Burkholderia cepacia is more active than LPS from Pseudomonas aeruginosa and Stenotrophomonas maltophilia in stimulating tumour necrosis factor alpha from human monocytes. Infect Immun 67, 1505-1507. [Google Scholar]
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In vitro resistance of Burkholderia cepacia complex isolates to reactive oxygen species in relation to catalase and superoxide dismutase production
Microbiology 147, 97 (2001); https://doi.org/10.1099/00221287-147-1-97
/content/journal/micro/10.1099/00221287-147-1-97
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