Abstract
We investigated the role of various hemolysin-producing strains (Escherichia coli, Serratia marcescens, Aeromonas hydrophila, and Listeria monocytogenes) in induction of inflammatory mediators, e.g., histamine release from rat mast cells as well as the chemiluminescence response and the release of lipoxygenase transformation products from human polymorphonuclear neutrophils. Our data show that the hemolysin-positive bacteria as well as the hemolysin-positive culture supernatants were active in inducing the chemiluminescence response, leukotriene (LTB4 and LTC4) release from human granulocytes, and histamine release from rat mast cells. The degree of leukotriene release was dependent on the hemolysin type and on the expression of hemolysin activity. The E. coli alpha-hemolysin and the aerolysin-producing A. hydrophila were the most potent stimuli whether washed bacteria or bacterial supernatant was used. Bacteria expressing the S. marcescens hemolysin and the listeriolysin were only poor inducers of leukotriene generation. In contrast to leukotriene generation, all hemolysin-positive strains induced nearly the same histamine release in a dose-dependent manner. Our data suggest a potent role for various hemolysins as virulence factors in inducing the release of inflammatory mediators.
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- 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]
- Asao T., Kinoshita Y., Kozaki S., Uemura T., Sakaguchi G. Purification and some properties of Aeromonas hydrophila hemolysin. Infect Immun. 1984 Oct;46(1):122–127. doi: 10.1128/iai.46.1.122-127.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Berger H., Hacker J., Juarez A., Hughes C., Goebel W. Cloning of the chromosomal determinants encoding hemolysin production and mannose-resistant hemagglutination in Escherichia coli. J Bacteriol. 1982 Dec;152(3):1241–1247. doi: 10.1128/jb.152.3.1241-1247.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Braun V., Günther H., Neuss B., Tautz C. Hemolytic activity of Serratia marcescens. Arch Microbiol. 1985 May;141(4):371–376. doi: 10.1007/BF00428852. [DOI] [PubMed] [Google Scholar]
- Braun V., Neuss B., Ruan Y., Schiebel E., Schöffler H., Jander G. Identification of the Serratia marcescens hemolysin determinant by cloning into Escherichia coli. J Bacteriol. 1987 May;169(5):2113–2120. doi: 10.1128/jb.169.5.2113-2120.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bremm K. D., Brom H. J., Alouf J. E., König W., Spur B., Crea A., Peters W. Generation of leukotrienes from human granulocytes by alveolysin from Bacillus alvei. Infect Immun. 1984 Apr;44(1):188–193. doi: 10.1128/iai.44.1.188-193.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bremm K. D., Brom J., König W., Spur B., Crea A., Bhakdi S., Lutz F., Fehrenbach F. J. Generation of leukotrienes and lipoxygenase factors from human polymorphonuclear granulocytes during bacterial phagocytosis and interaction with bacterial exotoxins. Zentralbl Bakteriol Mikrobiol Hyg A. 1983 Jul;254(4):500–514. [PubMed] [Google Scholar]
- 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]
- Bremm K. D., König W., Spur B., Crea A., Galanos C. Generation of slow-reacting substance (leukotrienes) by endotoxin and lipid A from human polymorphonuclear granulocytes. Immunology. 1984 Oct;53(2):299–305. [PMC free article] [PubMed] [Google Scholar]
- 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]
- Cavalieri S. J., Bohach G. A., Snyder I. S. Escherichia coli alpha-hemolysin: characteristics and probable role in pathogenicity. Microbiol Rev. 1984 Dec;48(4):326–343. doi: 10.1128/mr.48.4.326-343.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chakraborty T., Huhle B., Bergbauer H., Goebel W. Cloning, expression, and mapping of the Aeromonas hydrophila aerolysin gene determinant in Escherichia coli K-12. J Bacteriol. 1986 Jul;167(1):368–374. doi: 10.1128/jb.167.1.368-374.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chakraborty T., Montenegro M. A., Sanyal S. C., Helmuth R., Bulling E., Timmis K. N. Cloning of enterotoxin gene from Aeromonas hydrophila provides conclusive evidence of production of a cytotonic enterotoxin. Infect Immun. 1984 Nov;46(2):435–441. doi: 10.1128/iai.46.2.435-441.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Donta S. T., Haddow A. D. Cytotoxic activity of Aeromonas hydrophila. Infect Immun. 1978 Sep;21(3):989–993. doi: 10.1128/iai.21.3.989-993.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Field M., Musch M. W., Miller R. L., Goetzl E. J. Regulation of epithelial electrolyte transport by metabolites of arachidonic acid. J Allergy Clin Immunol. 1984 Sep;74(3 Pt 2):382–385. doi: 10.1016/0091-6749(84)90135-0. [DOI] [PubMed] [Google Scholar]
- Ford-Hutchinson A. W., Bray M. A., Doig M. V., Shipley M. E., Smith M. J. Leukotriene B, a potent chemokinetic and aggregating substance released from polymorphonuclear leukocytes. Nature. 1980 Jul 17;286(5770):264–265. doi: 10.1038/286264a0. [DOI] [PubMed] [Google Scholar]
- Gaillard J. L., Berche P., Sansonetti P. Transposon mutagenesis as a tool to study the role of hemolysin in the virulence of Listeria monocytogenes. Infect Immun. 1986 Apr;52(1):50–55. doi: 10.1128/iai.52.1.50-55.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goebel W., Hedgpeth J. Cloning and functional characterization of the plasmid-encoded hemolysin determinant of Escherichia coli. J Bacteriol. 1982 Sep;151(3):1290–1298. doi: 10.1128/jb.151.3.1290-1298.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gracey M., Burke V., Robinson J. Aeromonas-associated gastroenteritis. Lancet. 1982 Dec 11;2(8311):1304–1306. doi: 10.1016/s0140-6736(82)91510-0. [DOI] [PubMed] [Google Scholar]
- Hacker J., Hughes C., Hof H., Goebel W. Cloned hemolysin genes from Escherichia coli that cause urinary tract infection determine different levels of toxicity in mice. Infect Immun. 1983 Oct;42(1):57–63. doi: 10.1128/iai.42.1.57-63.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hostacká A., Ciznár I., Korych B., Karolcek J. Toxic factors of Aeromonas hydrophila and Plesiomonas shigelloides. Zentralbl Bakteriol Mikrobiol Hyg A. 1982 Sep;252(4):525–534. [PubMed] [Google Scholar]
- Howard S. P., Buckley J. T. Membrane glycoprotein receptor and hole-forming properties of a cytolytic protein toxin. Biochemistry. 1982 Mar 30;21(7):1662–1667. doi: 10.1021/bi00536a029. [DOI] [PubMed] [Google Scholar]
- Kamata R., Yamamoto T., Matsumoto K., Maeda H. A serratial protease causes vascular permeability reaction by activation of the Hageman factor-dependent pathway in guinea pigs. Infect Immun. 1985 Jun;48(3):747–753. doi: 10.1128/iai.48.3.747-753.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Köller M., Schönfeld W., Knöller J., Bremm K. D., König W., Spur B., Crea A., Peters W. The metabolism of leukotrienes in blood plasma studied by high-performance liquid chromatography. Biochim Biophys Acta. 1985 Jan 9;833(1):128–134. doi: 10.1016/0005-2760(85)90260-7. [DOI] [PubMed] [Google Scholar]
- König B., König W., Scheffer J., Hacker J., Goebel W. Role of Escherichia coli alpha-hemolysin and bacterial adherence in infection: requirement for release of inflammatory mediators from granulocytes and mast cells. Infect Immun. 1986 Dec;54(3):886–892. doi: 10.1128/iai.54.3.886-892.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- König W., Ishizaka K. Binding of rat IgE with the subcellular components of normal rat mast cells. Immunochemistry. 1976 Apr;13(4):345–353. doi: 10.1016/0019-2791(76)90346-3. [DOI] [PubMed] [Google Scholar]
- Linggood M. A., Ingram P. L. The role of alpha haemolysin in the virulence of Escherichia coli for mice. J Med Microbiol. 1982 Feb;15(1):23–30. doi: 10.1099/00222615-15-1-23. [DOI] [PubMed] [Google Scholar]
- Ljungh A., Wretlind B., Möllby R. Separation and characterization of enterotoxin and two haemolysins from Aeromonas hydrophila. Acta Pathol Microbiol Scand B. 1981 Dec;89(6):387–397. doi: 10.1111/j.1699-0463.1981.tb00205_89b.x. [DOI] [PubMed] [Google Scholar]
- Lyerly D. M., Kreger A. S. Importance of serratia protease in the pathogenesis of experimental Serratia marcescens pneumonia. Infect Immun. 1983 Apr;40(1):113–119. doi: 10.1128/iai.40.1.113-119.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maki D. G., Hennekens C. G., Phillips C. W., Shaw W. V., Bennett J. V. Nosocomial urinary tract infection with Serratia marcescens: an epidemiologic study. J Infect Dis. 1973 Nov;128(5):579–587. doi: 10.1093/infdis/128.5.579. [DOI] [PubMed] [Google Scholar]
- Matsumoto K., Yamamoto T., Kamata R., Maeda H. Pathogenesis of serratial infection: activation of the Hageman factor-prekallikrein cascade by serratial protease. J Biochem. 1984 Sep;96(3):739–749. doi: 10.1093/oxfordjournals.jbchem.a134892. [DOI] [PubMed] [Google Scholar]
- Minshew B. H., Jorgensen J., Counts G. W., Falkow S. Association of hemolysin production, hemagglutination of human erythrocytes, and virulence for chicken embryos of extraintestinal Escherichia coli isolates. Infect Immun. 1978 Apr;20(1):50–54. doi: 10.1128/iai.20.1.50-54.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Musch M. W., Miller R. J., Field M., Siegel M. I. Stimulation of colonic secretion by lipoxygenase metabolites of arachidonic acid. Science. 1982 Sep 24;217(4566):1255–1256. doi: 10.1126/science.6810465. [DOI] [PubMed] [Google Scholar]
- Palmer R. M., Salmon J. A. Release of leukotriene B4 from human neutrophils and its relationship to degranulation induced by N-formyl-methionyl-leucyl-phenylalanine, serum-treated zymosan and the ionophore A23187. Immunology. 1983 Sep;50(1):65–73. [PMC free article] [PubMed] [Google Scholar]
- Parrisius J., Bhakdi S., Roth M., Tranum-Jensen J., Goebel W., Seeliger H. P. Production of listeriolysin by beta-hemolytic strains of Listeria monocytogenes. Infect Immun. 1986 Jan;51(1):314–319. doi: 10.1128/iai.51.1.314-319.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Powell W. S. Properties of leukotriene B4 20-hydroxylase from polymorphonuclear leukocytes. J Biol Chem. 1984 Mar 10;259(5):3082–3089. [PubMed] [Google Scholar]
- 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]
- 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]
- Stüning M., Raulf M., König W. Localization of 5-lipoxygenase within human polymorphonuclear leukocytes. Biochem Pharmacol. 1985 Nov 15;34(22):3943–3950. doi: 10.1016/0006-2952(85)90370-3. [DOI] [PubMed] [Google Scholar]
- Welch D. F., Sword C. P., Brehm S., Dusanic D. Relationship between superoxide dismutase and pathogenic mechanisms of Listeria monocytogenes. Infect Immun. 1979 Mar;23(3):863–872. doi: 10.1128/iai.23.3.863-872.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]