Skip to main content
NCBI home page
Infection and Immunity logoLink to Infection and Immunity
. 1989 Jul;57(7):2187–2195. doi: 10.1128/iai.57.7.2187-2195.1989

Induction of inflammatory mediators (histamine and leukotrienes) from rat peritoneal mast cells and human granulocytes by Pseudomonas aeruginosa strains from burn patients.

U Bergmann 1, J Scheffer 1, M Köller 1, W Schönfeld 1, G Erbs 1, F E Müller 1, W König 1
PMCID: PMC313859  PMID: 2471693

Abstract

Clinical isolates of Pseudomonas aeruginosa from severely burned patients were analyzed with regard to their capacity to induce inflammatory-mediator release from rat mast cells or human granulocytes. The bacterial strains were characterized according to their cell-associated hemolysin activity as well as their secreted hemolysin and phospholipase C activities. P. aeruginosa expressing heat-labile hemolysin and phospholipase C induced histamine release from rat mast cells and leukotriene formation from human granulocytes, while bacterial strains expressing heat-stable hemolysin were potent releasers of histamine but did not lead to leukotriene formation. The mediator-inducing capacity was dependent on the growth characteristics of the bacterial strains. The purified glycolipid (heat-stable hemolysin) of P. aeruginosa was a potent inducer of histamine release but did not initiate leukotriene formation. Exotoxin A did not affect inflammatory-mediator release. P. aeruginosa with leukotriene-inducing capacity also enhanced omega oxidation of endogenous leukotriene B4, suggesting an additional inactivation of the chemotactic potential. Our data suggest that both hemolysins of P. aeruginosa contribute to the pathogenicity of P. aeruginosa by inducing and modulating inflammatory-mediator release from various cells.

Full text

PDF
2187

Selected References

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

  1. Aehringhaus U., Wölbling R. H., König W., Patrono C., Peskar B. M., Peskar B. A. Release of leukotriene C4 from human polymorphonuclear leucocytes as determined by radioimmunoassay. FEBS Lett. 1982 Sep 6;146(1):111–114. doi: 10.1016/0014-5793(82)80715-1. [DOI] [PubMed] [Google Scholar]
  2. Berk R. S., Brown D., Coutinho I., Meyers D. In vivo studies with two phospholipase C fractions from Pseudomonas aeruginosa. Infect Immun. 1987 Jul;55(7):1728–1730. doi: 10.1128/iai.55.7.1728-1730.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Berka R. M., Gray G. L., Vasil M. L. Studies of phospholipase C (heat-labile hemolysin) in Pseudomonas aeruginosa. Infect Immun. 1981 Dec;34(3):1071–1074. doi: 10.1128/iai.34.3.1071-1074.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Berka R. M., Vasil M. L. Phospholipase C (heat-labile hemolysin) of Pseudomonas aeruginosa: purification and preliminary characterization. J Bacteriol. 1982 Oct;152(1):239–245. doi: 10.1128/jb.152.1.239-245.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bishop M. B., Baltch A. L., Hill L. A., Smith R. P., Lutz F., Pollack M. The effect of Pseudomonas aeruginosa cytotoxin and toxin A on human polymorphonuclear leukocytes. J Med Microbiol. 1987 Dec;24(4):315–324. doi: 10.1099/00222615-24-4-315. [DOI] [PubMed] [Google Scholar]
  6. Bremm K. D., König W., Pfeiffer P., Rauschen I., Theobald K., Thelestam M., Alouf J. E. Effect of thiol-activated toxins (streptolysin O, alveolysin, and theta toxin) on the generation of leukotrienes and leukotriene-inducing and -metabolizing enzymes from human polymorphonuclear granulocytes. Infect Immun. 1985 Dec;50(3):844–851. doi: 10.1128/iai.50.3.844-851.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bremm K. D., König W., Thelestam M., Alouf J. E. Modulation of granulocyte functions by bacterial exotoxin and endotoxins. Immunology. 1987 Nov;62(3):363–371. [PMC free article] [PubMed] [Google Scholar]
  8. Brom J., König W., Köller M., Gross-Weege W., Erbs G., Müller F. Metabolism of leukotriene B4 by polymorphonuclear granulocytes of severely burned patients. Prostaglandins Leukot Med. 1987 May;27(2-3):209–225. doi: 10.1016/0262-1746(87)90072-2. [DOI] [PubMed] [Google Scholar]
  9. Brom J., König W., Stüning M., Raulf M., Köller M. Characterization of leukotriene B4-omega-hydroxylase activity within human polymorphonuclear granulocytes. Scand J Immunol. 1987 Mar;25(3):283–294. doi: 10.1111/j.1365-3083.1987.tb01074.x. [DOI] [PubMed] [Google Scholar]
  10. Böyum A. A one-stage procedure for isolation of granulocytes and lymphocytes from human blood. General sedimentation properties of white blood cells in a 1g gravity field. Scand J Clin Lab Invest Suppl. 1968;97:51–76. [PubMed] [Google Scholar]
  11. Cicmanec J. F., Holder I. A. Growth of Pseudomonas aeruginosa in normal and burned skin extract: role of extracellular proteases. Infect Immun. 1979 Aug;25(2):477–483. doi: 10.1128/iai.25.2.477-483.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Coutinho I. R., Berk R. S., Mammen E. Platelet aggregation by a phospholipase C from Pseudomonas aeruginosa. Thromb Res. 1988 Sep 1;51(5):495–505. doi: 10.1016/0049-3848(88)90115-6. [DOI] [PubMed] [Google Scholar]
  13. Engels W., Endert J., Kamps M. A., van Boven C. P. Role of lipopolysaccharide in opsonization and phagocytosis of Pseudomonas aeruginosa. Infect Immun. 1985 Jul;49(1):182–189. doi: 10.1128/iai.49.1.182-189.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Franklin A. L., Todd T., Gurman G., Black D., Mankinen-Irvin P. M., Irvin R. T. Adherence of Pseudomonas aeruginosa to cilia of human tracheal epithelial cells. Infect Immun. 1987 Jun;55(6):1523–1525. doi: 10.1128/iai.55.6.1523-1525.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hingley S. T., Hastie A. T., Kueppers F., Higgins M. L., Weinbaum G., Shryock T. Effect of ciliostatic factors from Pseudomonas aeruginosa on rabbit respiratory cilia. Infect Immun. 1986 Jan;51(1):254–262. doi: 10.1128/iai.51.1.254-262.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Holt P. S., Misfeldt M. L. Alteration of murine immune response by Pseudomonas aeruginosa exotoxin A. Infect Immun. 1984 Jul;45(1):227–233. doi: 10.1128/iai.45.1.227-233.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Iglewski B. H., Kabat D. NAD-dependent inhibition of protein synthesis by Pseudomonas aeruginosa toxin,. Proc Natl Acad Sci U S A. 1975 Jun;72(6):2284–2288. doi: 10.1073/pnas.72.6.2284. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Johnson M. K., Boese-Marrazzo D. Production and properties of heat-stable extracellular hemolysin from Pseudomonas aeruginosa. Infect Immun. 1980 Sep;29(3):1028–1033. doi: 10.1128/iai.29.3.1028-1033.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kharazmi A., Høiby N., Döring G., Valerius N. H. Pseudomonas aeruginosa exoproteases inhibit human neutrophil chemiluminescence. Infect Immun. 1984 Jun;44(3):587–591. doi: 10.1128/iai.44.3.587-591.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kropinski A. M., Jewell B., Kuzio J., Milazzo F., Berry D. Structure and functions of Pseudomonas aeruginosa lipopolysaccharide. Antibiot Chemother (1971) 1985;36:58–73. doi: 10.1159/000410472. [DOI] [PubMed] [Google Scholar]
  21. Kurioka S., Liu P. V. Effect of the hemolysin of Pseudomonas aeruginosa on phosphatides and on phospholipase c activity. J Bacteriol. 1967 Feb;93(2):670–674. doi: 10.1128/jb.93.2.670-674.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. König W., Frickhofen N., Tesch H. Generation and secretion of eosinophilotactic activity from human polymorphonuclear neutrophils by various mechanisms of cell activation. Immunology. 1979 Apr;36(4):733–742. [PMC free article] [PubMed] [Google Scholar]
  23. Lee C. C., Sugerman H. J., Tatum J. L., Wright T. P., Hirsh P. D., Hirsch J. I. Effects of ibuprofen on a pig Pseudomonas ARDS model. J Surg Res. 1986 May;40(5):438–444. doi: 10.1016/0022-4804(86)90212-x. [DOI] [PubMed] [Google Scholar]
  24. Liu P. V. The roles of various fractions of Pseudomonas aeruginosa in its pathogenesis. II. Effects of lecithinase and protease. J Infect Dis. 1966 Feb;116(1):112–116. doi: 10.1093/infdis/116.1.112. [DOI] [PubMed] [Google Scholar]
  25. Lutz F. Purification of a cytotoxic protein from Pseudomonas aeruginosa. Toxicon. 1979;17(5):467–475. doi: 10.1016/0041-0101(79)90280-0. [DOI] [PubMed] [Google Scholar]
  26. Nicas T. I., Bradley J., Lochner J. E., Iglewski B. H. The role of exoenzyme S in infections with Pseudomonas aeruginosa. J Infect Dis. 1985 Oct;152(4):716–721. doi: 10.1093/infdis/152.4.716. [DOI] [PubMed] [Google Scholar]
  27. O'Driscoll B. R., Cromwell O., Kay A. B. Sputum leukotrienes in obstructive airways diseases. Clin Exp Immunol. 1984 Feb;55(2):397–404. [PMC free article] [PubMed] [Google Scholar]
  28. Ohman D. E., Burns R. P., Iglewski B. H. Corneal infections in mice with toxin A and elastase mutants of Pseudomonas aeruginosa. J Infect Dis. 1980 Oct;142(4):547–555. doi: 10.1093/infdis/142.4.547. [DOI] [PubMed] [Google Scholar]
  29. Pier G. B. Pulmonary disease associated with Pseudomonas aeruginosa in cystic fibrosis: current status of the host-bacterium interaction. J Infect Dis. 1985 Apr;151(4):575–580. doi: 10.1093/infdis/151.4.575. [DOI] [PubMed] [Google Scholar]
  30. Pollack M., Anderson S. E., Jr Toxicity of Pseudomonas aeruginosa exotoxin A for human macrophages. Infect Immun. 1978 Mar;19(3):1092–1096. doi: 10.1128/iai.19.3.1092-1096.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Pollack M. The virulence of Pseudomonas aeruginosa. Rev Infect Dis. 1984 Sep-Oct;6 (Suppl 3):S617–S626. doi: 10.1093/clinids/6.supplement_3.s617. [DOI] [PubMed] [Google Scholar]
  32. Scheffer J., König W., Hacker J., Goebel W. Bacterial adherence and hemolysin production from Escherichia coli induces histamine and leukotriene release from various cells. Infect Immun. 1985 Oct;50(1):271–278. doi: 10.1128/iai.50.1.271-278.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Scheffer J., Vosbeck K., König W. Induction of inflammatory mediators from human polymorphonuclear granulocytes and rat mast cells by haemolysin-positive and -negative E. coli strains with different adhesins. Immunology. 1986 Dec;59(4):541–548. [PMC free article] [PubMed] [Google Scholar]
  34. Sordelli D. O., Cerquetti M. C., Morris Hooke A., Bellanti J. A. Effect of chemotactins released by Staphylococcus aureus and Pseudomonas aeruginosa on the murine respiratory tract. Infect Immun. 1985 Aug;49(2):265–269. doi: 10.1128/iai.49.2.265-269.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Stinson M. W., Hayden C. Secretion of phospholipase C by Pseudomonas aeruginosa. Infect Immun. 1979 Aug;25(2):558–564. doi: 10.1128/iai.25.2.558-564.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Vasil M. L., Berka R. M., Gray G. L., Nakai H. Cloning of a phosphate-regulated hemolysin gene (phospholipase C) from Pseudomonas aeruginosa. J Bacteriol. 1982 Oct;152(1):431–440. doi: 10.1128/jb.152.1.431-440.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Vasil M. L., Berka R. M., Gray G. L., Pavlovskis O. R. Biochemical and genetic studies of iron-regulated (exotoxin A) and phosphate-regulated (hemolysin phospholipase C) virulence factors of Pseudomonas aeruginosa. Antibiot Chemother (1971) 1985;36:23–39. doi: 10.1159/000410469. [DOI] [PubMed] [Google Scholar]
  38. Woods D. E., Schaffer M. S., Rabin H. R., Campbell G. D., Sokol P. A. Phenotypic comparison of Pseudomonas aeruginosa strains isolated from a variety of clinical sites. J Clin Microbiol. 1986 Aug;24(2):260–264. doi: 10.1128/jcm.24.2.260-264.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Zehavi-Willner T. Induction of murine cytolytic T lymphocytes by Pseudomonas aeruginosa exotoxin A. Infect Immun. 1988 Jan;56(1):213–218. doi: 10.1128/iai.56.1.213-218.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES