Skip to main content
PMC home page
Infection and Immunity logoLink to Infection and Immunity
. 1997 Jun;65(6):2483–2487. doi: 10.1128/iai.65.6.2483-2487.1997

Modulation of neutrophil superoxide response and intracellular diacylglyceride levels by the bacterial pigment pyocyanin.

M Muller 1, T C Sorrell 1
PMCID: PMC175349  PMID: 9169797

Abstract

Low concentrations of pyocyanin are reported to enhance superoxide production by human neutrophils exposed to various stimuli, yet the mechanism remains unknown. Using lucigenin-enhanced chemiluminescence, we examined the kinetics of the neutrophil superoxide response in the presence of pyocyanin. At all concentrations (12.5 to 200 microM), pyocyanin decreased the peak superoxide response while prolonging the duration of the response. The prolonged response may be associated with an observed increase in intracellular diacylglyceride levels due to pyocyanin exposure.

Full Text

The Full Text of this article is available as a PDF (150.2 KB).

Selected References

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

  1. BLIGH E. G., DYER W. J. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959 Aug;37(8):911–917. doi: 10.1139/o59-099. [DOI] [PubMed] [Google Scholar]
  2. Bauldry S. A., Elsey K. L., Bass D. A. Activation of NADPH oxidase and phospholipase D in permeabilized human neutrophils. Correlation between oxidase activation and phosphatidic acid production. J Biol Chem. 1992 Dec 15;267(35):25141–25152. [PubMed] [Google Scholar]
  3. Berridge M. J. Inositol trisphosphate and diacylglycerol: two interacting second messengers. Annu Rev Biochem. 1987;56:159–193. doi: 10.1146/annurev.bi.56.070187.001111. [DOI] [PubMed] [Google Scholar]
  4. Cantin A. M., North S. L., Fells G. A., Hubbard R. C., Crystal R. G. Oxidant-mediated epithelial cell injury in idiopathic pulmonary fibrosis. J Clin Invest. 1987 Jun;79(6):1665–1673. doi: 10.1172/JCI113005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chabot M. C., McPhail L. C., Wykle R. L., Kennerly D. A., McCall C. E. Comparison of diglyceride production from choline-containing phosphoglycerides in human neutrophils stimulated with N-formylmethionyl-leucylphenylalanine, ionophore A23187 or phorbol 12-myristate 13-acetate. Biochem J. 1992 Sep 15;286(Pt 3):693–699. doi: 10.1042/bj2860693. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dahlgren C., Aniansson H., Magnusson K. E. Pattern of formylmethionyl-leucyl-phenylalanine-induced luminol- and lucigenin-dependent chemiluminescence in human neutrophils. Infect Immun. 1985 Jan;47(1):326–328. doi: 10.1128/iai.47.1.326-328.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Davis G., Thornalley P. J. Free radical production from the aerobic oxidation of reduced pyridine nucleotides catalysed by phenazine derivatives. Biochim Biophys Acta. 1983 Sep 30;724(3):456–464. doi: 10.1016/0005-2728(83)90106-8. [DOI] [PubMed] [Google Scholar]
  8. Dusi S., Rossi F. Activation of NADPH oxidase of human neutrophils involves the phosphorylation and the translocation of cytosolic p67phox. Biochem J. 1993 Dec 1;296(Pt 2):367–371. doi: 10.1042/bj2960367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fujita I., Irita K., Takeshige K., Minakami S. Diacylglycerol, 1-oleoyl-2-acetyl-glycerol, stimulates superoxide-generation from human neutrophils. Biochem Biophys Res Commun. 1984 Apr 30;120(2):318–324. doi: 10.1016/0006-291x(84)91256-7. [DOI] [PubMed] [Google Scholar]
  10. Gyllenhammar H. Lucigenin chemiluminescence in the assessment of neutrophil superoxide production. J Immunol Methods. 1987 Mar 12;97(2):209–213. doi: 10.1016/0022-1759(87)90461-3. [DOI] [PubMed] [Google Scholar]
  11. Halliwell B., Gutteridge J. M. Oxygen toxicity, oxygen radicals, transition metals and disease. Biochem J. 1984 Apr 1;219(1):1–14. doi: 10.1042/bj2190001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Knight M., Hartman P. E., Hartman Z., Young V. M. A new method of preparation of pyocyanin and demonstration of an unusual bacterial sensitivity. Anal Biochem. 1979 May;95(1):19–23. doi: 10.1016/0003-2697(79)90179-9. [DOI] [PubMed] [Google Scholar]
  13. Miller K. M., Dearborn D. G., Sorensen R. U. In vitro effect of synthetic pyocyanine on neutrophil superoxide production. Infect Immun. 1987 Mar;55(3):559–563. doi: 10.1128/iai.55.3.559-563.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Muller M. Scavenging of neutrophil-derived superoxide anion by 1-hydroxyphenazine, a phenazine derivative associated with chronic Pseudomonas aeruginosa infection: relevance to cystic fibrosis. Biochim Biophys Acta. 1995 Dec 12;1272(3):185–189. doi: 10.1016/0925-4439(95)00086-0. [DOI] [PubMed] [Google Scholar]
  15. Muller M., Sorrell T. C. Leukotriene B4 omega-oxidation by human polymorphonuclear leukocytes is inhibited by pyocyanin, a phenazine derivative produced by Pseudomonas aeruginosa. Infect Immun. 1992 Jun;60(6):2536–2540. doi: 10.1128/iai.60.6.2536-2540.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Muller M., Sorrell T. C. Production of leukotriene B4 and 5-hydroxyeicosatetraenoic acid by human neutrophils is inhibited by Pseudomonas aeruginosa phenazine derivatives. Infect Immun. 1991 Sep;59(9):3316–3318. doi: 10.1128/iai.59.9.3316-3318.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Mullmann T. J., Siegel M. I., Egan R. W., Billah M. M. Phorbol-12-myristate-13-acetate activation of phospholipase D in human neutrophils leads to the production of phosphatides and diglycerides. Biochem Biophys Res Commun. 1990 Aug 16;170(3):1197–1202. doi: 10.1016/0006-291x(90)90520-w. [DOI] [PubMed] [Google Scholar]
  18. Müller P. K., Krohn K., Mühlradt P. F. Effects of pyocyanine, a phenazine dye from Pseudomonas aeruginosa, on oxidative burst and bacterial killing in human neutrophils. Infect Immun. 1989 Sep;57(9):2591–2596. doi: 10.1128/iai.57.9.2591-2596.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Nishizuka Y. The role of protein kinase C in cell surface signal transduction and tumour promotion. Nature. 1984 Apr 19;308(5961):693–698. doi: 10.1038/308693a0. [DOI] [PubMed] [Google Scholar]
  20. Park J. W., Babior B. M. Effects of diacylglycerol on the activation and kinetics of the respiratory burst oxidase in a cell-free system from human neutrophils: evidence that diacylglycerol may regulate nucleotide uptake by a GTP-binding protein. Arch Biochem Biophys. 1993 Oct;306(1):119–124. doi: 10.1006/abbi.1993.1488. [DOI] [PubMed] [Google Scholar]
  21. Ras G. J., Anderson R., Taylor G. W., Savage J. E., Van Niekerk E., Wilson R., Cole P. J. Proinflammatory interactions of pyocyanin and 1-hydroxyphenazine with human neutrophils in vitro. J Infect Dis. 1990 Jul;162(1):178–185. doi: 10.1093/infdis/162.1.178. [DOI] [PubMed] [Google Scholar]
  22. Samuni A., Krishna C. M., Cook J., Black C. D., Russo A. On radical production by PMA-stimulated neutrophils as monitored by luminol-amplified chemiluminescence. Free Radic Biol Med. 1991;10(5):305–313. doi: 10.1016/0891-5849(91)90037-4. [DOI] [PubMed] [Google Scholar]
  23. Smith R. J., Sam L. M., Justen J. M. Diacylglycerols modulate human polymorphonuclear neutrophil responsiveness: effects on intracellular calcium mobilization, granule exocytosis, and superoxide anion production. J Leukoc Biol. 1988 May;43(5):411–419. doi: 10.1002/jlb.43.5.411. [DOI] [PubMed] [Google Scholar]
  24. Sorensen R. U., Fredricks D. N., Waller R. L. Inhibition of normal and malignant cell proliferation by pyocyanine and 1-hydroxyphenazine. Antibiot Chemother (1971) 1991;44:85–93. doi: 10.1159/000420302. [DOI] [PubMed] [Google Scholar]
  25. Sparkman T. B., Johns T., Engerson T., Jones H. P. Activation-associated alterations in neutrophil pyridine nucleotide levels: a potential regulatory role for calcium and calmodulin. Biochim Biophys Acta. 1985 Jul 30;846(1):8–13. doi: 10.1016/0167-4889(85)90103-x. [DOI] [PubMed] [Google Scholar]
  26. Takahashi R., Edashige K., Sato E. F., Inoue M., Matsuno T., Utsumi K. Luminol chemiluminescence and active oxygen generation by activated neutrophils. Arch Biochem Biophys. 1991 Mar;285(2):325–330. doi: 10.1016/0003-9861(91)90367-r. [DOI] [PubMed] [Google Scholar]
  27. Umei T., Ohhara N., Okamura S., Harada M., Nakao M., Shirai T., Niho Y. Activation of neutrophils NADPH oxidase by PMA: cytosol activity is translocated in phorbol-primed neutrophils. Int J Biochem. 1993 May;25(5):631–633. doi: 10.1016/0020-711x(93)90346-g. [DOI] [PubMed] [Google Scholar]
  28. Watson D., MacDermot J., Wilson R., Cole P. J., Taylor G. W. Purification and structural analysis of pyocyanin and 1-hydroxyphenazine. Eur J Biochem. 1986 Sep 1;159(2):309–313. doi: 10.1111/j.1432-1033.1986.tb09869.x. [DOI] [PubMed] [Google Scholar]
  29. Weiss S. J. Tissue destruction by neutrophils. N Engl J Med. 1989 Feb 9;320(6):365–376. doi: 10.1056/NEJM198902093200606. [DOI] [PubMed] [Google Scholar]
  30. Wilson R., Sykes D. A., Watson D., Rutman A., Taylor G. W., Cole P. J. Measurement of Pseudomonas aeruginosa phenazine pigments in sputum and assessment of their contribution to sputum sol toxicity for respiratory epithelium. Infect Immun. 1988 Sep;56(9):2515–2517. doi: 10.1128/iai.56.9.2515-2517.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Winterbourn C. C. Cytochrome c reduction by semiquinone radicals can be indirectly inhibited by superoxide dismutase. Arch Biochem Biophys. 1981 Jun;209(1):159–167. doi: 10.1016/0003-9861(81)90268-x. [DOI] [PubMed] [Google Scholar]

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

RESOURCES