Skip to main content
NCBI home page
Infection and Immunity logoLink to Infection and Immunity
. 1993 Apr;61(4):1442–1446. doi: 10.1128/iai.61.4.1442-1446.1993

Superoxide dismutase and the resistance of Escherichia coli to phagocytic killing by human neutrophils.

E Papp-Szabò 1, C L Sutherland 1, P D Josephy 1
PMCID: PMC281383  PMID: 8454348

Abstract

Transformation of Escherichia coli K-12-derived strains with a plasmid carrying the genetic determinants for synthesis of lipopolysaccharide O antigen by Shigella dysenteriae allows the construction of phenotypically smooth derivatives. We show that such E. coli K-12 derivatives are highly resistant to killing by human serum. Isogenic wild-type and sodB mutant (Fe superoxide dismutase-deficient) strains were constructed. The results of experiments on phagocytic killing of these strains by human neutrophils are reported. We observed no difference between the sensitivities of wild-type and sodB mutant strains to phagocytic killing, in contrast to the results reported by other researchers who used species other than E. coli or strains other than K-12.

Full text

PDF
1442

Images in this article

1444Image
on p.1444

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Beaman L., Beaman B. L. Monoclonal antibodies demonstrate that superoxide dismutase contributes to protection of Nocardia asteroides within the intact host. Infect Immun. 1990 Sep;58(9):3122–3128. doi: 10.1128/iai.58.9.3122-3128.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Beauchamp C., Fridovich I. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem. 1971 Nov;44(1):276–287. doi: 10.1016/0003-2697(71)90370-8. [DOI] [PubMed] [Google Scholar]
  3. Buchmeier N. A., Heffron F. Induction of Salmonella stress proteins upon infection of macrophages. Science. 1990 May 11;248(4956):730–732. doi: 10.1126/science.1970672. [DOI] [PubMed] [Google Scholar]
  4. Carlioz A., Touati D. Isolation of superoxide dismutase mutants in Escherichia coli: is superoxide dismutase necessary for aerobic life? EMBO J. 1986 Mar;5(3):623–630. doi: 10.1002/j.1460-2075.1986.tb04256.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chan E., Weiss B. Endonuclease IV of Escherichia coli is induced by paraquat. Proc Natl Acad Sci U S A. 1987 May;84(10):3189–3193. doi: 10.1073/pnas.84.10.3189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. DeBruin L. S., Josephy P. D. Dichlorobenzidine-DNA binding catalyzed by peroxidative activation in Salmonella typhimurium. Arch Biochem Biophys. 1989 Feb 15;269(1):25–31. doi: 10.1016/0003-9861(89)90083-0. [DOI] [PubMed] [Google Scholar]
  7. Demple B. Regulation of bacterial oxidative stress genes. Annu Rev Genet. 1991;25:315–337. doi: 10.1146/annurev.ge.25.120191.001531. [DOI] [PubMed] [Google Scholar]
  8. Diedrich D. L., Stein M. A., Schnaitman C. A. Associations of Escherichia coli K-12 OmpF trimers with rough and smooth lipopolysaccharides. J Bacteriol. 1990 Sep;172(9):5307–5311. doi: 10.1128/jb.172.9.5307-5311.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fang F. C., Libby S. J., Buchmeier N. A., Loewen P. C., Switala J., Harwood J., Guiney D. G. The alternative sigma factor katF (rpoS) regulates Salmonella virulence. Proc Natl Acad Sci U S A. 1992 Dec 15;89(24):11978–11982. doi: 10.1073/pnas.89.24.11978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Farr S. B., D'Ari R., Touati D. Oxygen-dependent mutagenesis in Escherichia coli lacking superoxide dismutase. Proc Natl Acad Sci U S A. 1986 Nov;83(21):8268–8272. doi: 10.1073/pnas.83.21.8268. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Farr S. B., Touati D., Kogoma T. Effects of oxygen stress on membrane functions in Escherichia coli: role of HPI catalase. J Bacteriol. 1988 Apr;170(4):1837–1842. doi: 10.1128/jb.170.4.1837-1842.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fields P. I., Swanson R. V., Haidaris C. G., Heffron F. Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc Natl Acad Sci U S A. 1986 Jul;83(14):5189–5193. doi: 10.1073/pnas.83.14.5189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Franzon V. L., Arondel J., Sansonetti P. J. Contribution of superoxide dismutase and catalase activities to Shigella flexneri pathogenesis. Infect Immun. 1990 Feb;58(2):529–535. doi: 10.1128/iai.58.2.529-535.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gargan R. A., Brumfitt W., Hamilton-Miller J. M. Pre-opsonisation of Escherichia coli induces resistance to neutrophil killing in serum and urine: relationship to growth phase. J Med Microbiol. 1991 Jul;35(1):12–17. doi: 10.1099/00222615-35-1-12. [DOI] [PubMed] [Google Scholar]
  15. Greenberg J. T., Demple B. A global response induced in Escherichia coli by redox-cycling agents overlaps with that induced by peroxide stress. J Bacteriol. 1989 Jul;171(7):3933–3939. doi: 10.1128/jb.171.7.3933-3939.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Greenberg J. T., Monach P., Chou J. H., Josephy P. D., Demple B. Positive control of a global antioxidant defense regulon activated by superoxide-generating agents in Escherichia coli. Proc Natl Acad Sci U S A. 1990 Aug;87(16):6181–6185. doi: 10.1073/pnas.87.16.6181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hassett D. J., Cohen M. S. Bacterial adaptation to oxidative stress: implications for pathogenesis and interaction with phagocytic cells. FASEB J. 1989 Dec;3(14):2574–2582. doi: 10.1096/fasebj.3.14.2556311. [DOI] [PubMed] [Google Scholar]
  18. Holmes D. S., Quigley M. A rapid boiling method for the preparation of bacterial plasmids. Anal Biochem. 1981 Jun;114(1):193–197. doi: 10.1016/0003-2697(81)90473-5. [DOI] [PubMed] [Google Scholar]
  19. Hopkin K. A., Papazian M. A., Steinman H. M. Functional differences between manganese and iron superoxide dismutases in Escherichia coli K-12. J Biol Chem. 1992 Dec 5;267(34):24253–24258. [PubMed] [Google Scholar]
  20. Ma M., Eaton J. W. Multicellular oxidant defense in unicellular organisms. Proc Natl Acad Sci U S A. 1992 Sep 1;89(17):7924–7928. doi: 10.1073/pnas.89.17.7924. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Minakami H., Fridovich I. Effects of paraquat on cultures of Escherichia coli: turbidity versus enumeration. Free Radic Biol Med. 1990;8(4):387–391. doi: 10.1016/0891-5849(90)90105-r. [DOI] [PubMed] [Google Scholar]
  23. Pluschke G., Mayden J., Achtman M., Levine R. P. Role of the capsule and the O antigen in resistance of O18:K1 Escherichia coli to complement-mediated killing. Infect Immun. 1983 Dec;42(3):907–913. doi: 10.1128/iai.42.3.907-913.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Privalle C. T., Fridovich I. Inductions of superoxide dismutases in Escherichia coli under anaerobic conditions. Accumulation of an inactive form of the manganese enzyme. J Biol Chem. 1988 Mar 25;263(9):4274–4279. [PubMed] [Google Scholar]
  25. Rotrosen D., Yeung C. L., Leto T. L., Malech H. L., Kwong C. H. Cytochrome b558: the flavin-binding component of the phagocyte NADPH oxidase. Science. 1992 Jun 5;256(5062):1459–1462. doi: 10.1126/science.1318579. [DOI] [PubMed] [Google Scholar]
  26. Royer-Pokora B., Kunkel L. M., Monaco A. P., Goff S. C., Newburger P. E., Baehner R. L., Cole F. S., Curnutte J. T., Orkin S. H. Cloning the gene for an inherited human disorder--chronic granulomatous disease--on the basis of its chromosomal location. Nature. 1986 Jul 3;322(6074):32–38. doi: 10.1038/322032a0. [DOI] [PubMed] [Google Scholar]
  27. Sawyer D. W., Donowitz G. R., Mandell G. L. Polymorphonuclear neutrophils: an effective antimicrobial force. Rev Infect Dis. 1989 Nov-Dec;11 (Suppl 7):S1532–S1544. doi: 10.1093/clinids/11.supplement_7.s1532. [DOI] [PubMed] [Google Scholar]
  28. Schellhorn H. E., Hassan H. M. Response of hydroperoxidase and superoxide dismutase deficient mutants of Escherichia coli K-12 to oxidative stress. Can J Microbiol. 1988 Oct;34(10):1171–1176. doi: 10.1139/m88-206. [DOI] [PubMed] [Google Scholar]
  29. Schellhorn H. E., Hassan H. M. Transcriptional regulation of katE in Escherichia coli K-12. J Bacteriol. 1988 Sep;170(9):4286–4292. doi: 10.1128/jb.170.9.4286-4292.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Schnaitman C. A., Austin E. A. Efficient incorporation of galactose into lipopolysaccharide by Escherichia coli K-12 strains with polar galE mutations. J Bacteriol. 1990 Sep;172(9):5511–5513. doi: 10.1128/jb.172.9.5511-5513.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Schwartz C. E., Krall J., Norton L., McKay K., Kay D., Lynch R. E. Catalase and superoxide dismutase in Escherichia coli. J Biol Chem. 1983 May 25;258(10):6277–6281. [PubMed] [Google Scholar]
  32. Storz G., Christman M. F., Sies H., Ames B. N. Spontaneous mutagenesis and oxidative damage to DNA in Salmonella typhimurium. Proc Natl Acad Sci U S A. 1987 Dec;84(24):8917–8921. doi: 10.1073/pnas.84.24.8917. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Storz G., Tartaglia L. A., Farr S. B., Ames B. N. Bacterial defenses against oxidative stress. Trends Genet. 1990 Nov;6(11):363–368. doi: 10.1016/0168-9525(90)90278-e. [DOI] [PubMed] [Google Scholar]
  34. Sturm S., Timmis K. N. Cloning of the rfb gene region of Shigella dysenteriae 1 and construction of an rfb-rfp gene cassette for the development of lipopolysaccharide-based live anti-dysentery vaccines. Microb Pathog. 1986 Jun;1(3):289–297. doi: 10.1016/0882-4010(86)90054-9. [DOI] [PubMed] [Google Scholar]
  35. Tatum F. M., Detilleux P. G., Sacks J. M., Halling S. M. Construction of Cu-Zn superoxide dismutase deletion mutants of Brucella abortus: analysis of survival in vitro in epithelial and phagocytic cells and in vivo in mice. Infect Immun. 1992 Jul;60(7):2863–2869. doi: 10.1128/iai.60.7.2863-2869.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Triggs-Raine B. L., Loewen P. C. Physical characterization of katG, encoding catalase HPI of Escherichia coli. Gene. 1987;52(2-3):121–128. doi: 10.1016/0378-1119(87)90038-2. [DOI] [PubMed] [Google Scholar]
  37. Yost F. J., Jr, Fridovich I. Superoxide radicals and phagocytosis. Arch Biochem Biophys. 1974 Apr 2;161(2):395–401. doi: 10.1016/0003-9861(74)90320-8. [DOI] [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES