Role of superoxide dismutase and catalase as determinants of pathogenicity of Nocardia asteroides: importance in resistance to microbicidal activities of human polymorphonuclear neutrophils (original) (raw)

Abstract

The roles of nocardial superoxide dismutase (SOD) and catalase in the resistance of Nocardia asteroides to the microbicidal properties of human polymorphonuclear leukocytes were determined in vitro. The neutrophils killed ca. 80% of the cells of the less virulent N. asteroides 10905 and ca. 50% of the log phase of the more virulent N. asteroides GUH-2 after 180 min of incubation. These phagocytes were not able to kill early-stationary-phase cells of strain GUH-2 that contained 10 times more intracytoplasmic catalase than log-phase cells of the same culture. However, the polymorphonuclear leukocytes were able to kill more than 50% of the cells of early-stationary-phase strain GUH-2 after treatment with purified antibody specific for surface-associated SOD. No killing was observed when the bacteria were treated with normal rabbit immunoglobulin G or with serum obtained from rabbits immunized against whole nocardial cells (containing little or no activity against SOD). These phagocytes killed more than 99% of Listeria monocytogenes used as a control. Chlorpromazine-treated polymorphonuclear leukocytes killed L. monocytogenes (70%) but they were not able to kill antibody-treated cells of N. asteroides GUH-2. Exogenously added SOD partially protected strain 10905, which lacked surface-associated enzyme, but it had no effect on the killing of strain GUH-2, which already possessed significant amounts of surface-bound SOD. In contrast, catalase added to the nocardiae provided almost complete protection to the log-phase cells of strain GUH-2, but strain 10905 was only partially protected. SOD combined with catalase had additive activity which completely protected the cells of strain 10905. A mutant of N. asteroides GUH-2 (SCII-C) is more virulent during the log phase than is the parental strain. This mutant contained at least 7 times more catalase at this stage of growth than did the parent. No other differences between these two strains were observed during the log phase. In sharp contrast to those of the parent, log-phase cells of this high-catalase mutant were not killed by polymorphonuclear phagocytes. These data indicate a role for both SOD and catalase in the resistance of Nocardia spp. to human neutrophils, and they represent at least two factors associated with virulence.

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Selected References

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  1. Beaman B. L., Bourgeois A. L., Moring S. E. Cell wall modification resulting from in vitro induction of L-phase variants of Nocardia asteroides. J Bacteriol. 1981 Nov;148(2):600–609. doi: 10.1128/jb.148.2.600-609.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Beaman B. L. Interaction of Nocardia asteroides at different phases of growth with in vitro-maintained macrophages obtained from the lungs of normal and immunized rabbits. Infect Immun. 1979 Oct;26(1):355–361. doi: 10.1128/iai.26.1.355-361.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Beaman B. L., Maslan S. Virulence of Nocardia asteroides during its growth cycle. Infect Immun. 1978 Apr;20(1):290–295. doi: 10.1128/iai.20.1.290-295.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Beaman B. L., Scates S. M., Moring S. E., Deem R., Misra H. P. Purification and properties of a unique superoxide dismutase from Nocardia asteroides. J Biol Chem. 1983 Jan 10;258(1):91–96. [PubMed] [Google Scholar]
  5. Beaman B. L. Structural and biochemical alterations of Nocardia asteroides cell walls during its growth cycle. J Bacteriol. 1975 Sep;123(3):1235–1253. doi: 10.1128/jb.123.3.1235-1253.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Beaman L., Beaman B. L. The role of oxygen and its derivatives in microbial pathogenesis and host defense. Annu Rev Microbiol. 1984;38:27–48. doi: 10.1146/annurev.mi.38.100184.000331. [DOI] [PubMed] [Google Scholar]
  7. Black C. M., Beaman B. L., Donovan R. M., Goldstein E. Effect of virulent and less virulent strains of Nocardia asteroides on acid-phosphatase activity in alveolar and peritoneal macrophages maintained in vitro. J Infect Dis. 1983 Jul;148(1):117–124. doi: 10.1093/infdis/148.1.117. [DOI] [PubMed] [Google Scholar]
  8. Davis-Scibienski C., Beaman B. L. Interaction of Nocardia asteroides with rabbit alveolar macrophages: association of virulence, viability, ultrastructural damage, and phagosome-lysosome fusion. Infect Immun. 1980 May;28(2):610–619. doi: 10.1128/iai.28.2.610-619.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Davis-Scibienski C., Beaman B. L. Interaction of Nocardia asteroides with rabbit alveolar macrophages: effect of growth phase and viability on phagosome-lysosome fusion. Infect Immun. 1980 Jul;29(1):24–29. doi: 10.1128/iai.29.1.24-29.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Deem R. L., Beaman B. L., Gershwin M. E. Adoptive transfer of immunity to Nocardia asteroides in nude mice. Infect Immun. 1982 Dec;38(3):914–920. doi: 10.1128/iai.38.3.914-920.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Filice G. A., Beaman B. L., Krick J. A., Remington J. S. Effects of human neutrophils and monocytes on Nocardia asteroides: failure of killing despite occurrence of the oxidative metabolic burst. J Infect Dis. 1980 Sep;142(3):432–438. doi: 10.1093/infdis/142.3.432. [DOI] [PubMed] [Google Scholar]
  12. Filice G. A. Resistance of Nocardia asteroides to oxygen-dependent killing by neutrophils. J Infect Dis. 1983 Nov;148(5):861–867. doi: 10.1093/infdis/148.5.861. [DOI] [PubMed] [Google Scholar]
  13. Jackett P. S., Aber V. R., Lowrie D. B. Virulence and resistance to superoxide, low pH and hydrogen peroxide among strains of Mycobacterium tuberculosis. J Gen Microbiol. 1978 Jan;104(1):37–45. doi: 10.1099/00221287-104-1-37. [DOI] [PubMed] [Google Scholar]
  14. Johnston R. B., Jr, Keele B. B., Jr, Misra H. P., Lehmeyer J. E., Webb L. S., Baehner R. L., RaJagopalan K. V. The role of superoxide anion generation in phagocytic bactericidal activity. Studies with normal and chronic granulomatous disease leukocytes. J Clin Invest. 1975 Jun;55(6):1357–1372. doi: 10.1172/JCI108055. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kusunose E., Ichihara K., Noda Y., Kusunose M. Superoxide dismutase from Mycobacterium tuberculosis. J Biochem. 1976 Dec;80(6):1343–1352. doi: 10.1093/oxfordjournals.jbchem.a131407. [DOI] [PubMed] [Google Scholar]
  16. Mandell G. L. Catalase, superoxide dismutase, and virulence of Staphylococcus aureus. In vitro and in vivo studies with emphasis on staphylococcal--leukocyte interaction. J Clin Invest. 1975 Mar;55(3):561–566. doi: 10.1172/JCI107963. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Vistica C. A., Beaman B. L. Pathogenic and virulence characterization of colonial mutants of Nocardia asteroides GUH-2. Can J Microbiol. 1983 Sep;29(9):1126–1135. doi: 10.1139/m83-173. [DOI] [PubMed] [Google Scholar]