Abstract
The effect of Legionella pneumophila sonic extract on human neutrophil and monocyte oxidative burst was studied by Superoxide anion release and luminol-enhanced chemiluminescence assays.Legionella pneumophila sonic extract by itself did not stimulate neutrophils and monocytes. The sonic extract at 8–2000μg/ml primed neutrophils for enhanced Superoxide release and, at 8–62.5 μg/ml, for enhanced chemiluminescence. Monocytes were only primed for enhanced chemiluminescence at very low extract concentrations (below 16μg/ml). Monocyte Superoxide release was suppressed by extract concentrations higher than 2000μg/ml and the chemiluminescence response of neutrophils and monocytes by concentrations higher than 250 and 125 μg/ml, respectively. The priming activity was heat stable and present in fractions below 5 kDa. On the basis of these findings it is suggested that enhanced production of oxygen metabolites by neutrophils in contact with legionella components at low concentrations could contribute to the lung tissue damage seen in Legionnaires' disease, whereas the suppression of phagocyte oxidative burst by higher extract concentrations may be one of the mechanisms by which Legionella pneumophila survives intracellularly.
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Baskerville, A., Dowsett, A. B., Fitzgeorge, R. B., Hambleton, P., Broster, M.: Ultrastructure of pulmonary alveoli and macrophages in experimental Legionnaires' disease. Journal of Pathology 1983, 140: 77–90.
Horwitz, M. A., Silverstein, S. C.: Legionnaires' disease bacterium (Legionella pneumophila) multiplies intracellularly in human monocytes. Journal of Clinical Investigation 1980, 66: 441–450.
Horwitz, M. A., Silvetstein, S. C.: Interaction of the Legionnaires' disease bacterium (Legionella pneumophila) with human phagocytes. I:Legionella pneumophila resists killing by polymorphonuclear leukocytes, antibody and complement. Journal of Experimental Medicine 1981, 153: 386–397.
Weinbaum, D. L., Bailey, J., Benner, R. R., Pasculle, W., Dowling, J. N.: The contribution of human neutrophils and serum to host defense againstLegionella micdadei. Journal of Infectious Diseases 1983, 148: 510–517.
Horwitz, M. A., Silverstein, S. C.: Activated monocytes inhibit the intracellular multiplication of Legionnaires' disease bacteria. Journal of Experimental Medicine 1981, 154: 1618–1635.
Horwitz, M. A.: The Legionnaires' disease bacterium (Legionella pneumophila) inhibits phagosome-lysosome fusion in human monocytes. Journal of Experimental Medicine 1983, 158: 2108–2126.
Horwitz, M. A., Maxfield, F. R.:Legionella pneumophila inhibits acidification of its phagosome in human monocytes. Journal of Cell Biology 1984, 99: 1936–1943.
Friedman, R. L., Lochner, J. E., Bigley, R. H., Iglewski, B. H.: The effects ofLegionella pneumophila toxin on oxidative processes and bacterial killing of human polymorphonuclear leukocytes. Journal of Infectious Diseases 1982, 146: 328–334.
Lochner, J. E., Bigley, R. H., Iglewski, B. H.: Defective triggering of polymorphonuclear leukocyte oxidative metabolism byLegionella pneumophila toxin. Journal of Infectious Diseases 1985, 151: 42–46.
Lochner, J. E., Friedman, R. L., Bigley, R. H., Iglewski, B. H.: Effect of oxygen-dependent antimicrobial systems onLegionella pneumophila. Infection and Immunity 1983, 39; 487–489.
Locksley, R. M., Jacobs, R. F., Wilson, C. B., Weaver, M., Klebanoff, S. J.: Susceptibility ofLegionella pneumophila to oxygen-dependent microbicidal systems. Journal of Immunology 1982, 129: 2192–2197.
Rechnitzer, C., Kharazmi, A., Nielsen, H.: Effects ofLegionella pneumophila sonicate on human neutrophil granulocyte and monocyte chemotaxis. European Journal of Clinical Investigation 1986, 16: 368–375.
Böyum, A.: Isolation of mononuclear cells and granulocytes from human blood. Scandinavian Journal of Clinical and Laboratory Investigation 1968, 21, Supplement 97: 77–89.
Nielsen, H., Larsen, S. O.: Human monocyte chemotaxis in vitro. Influence of in vitro variables in the filter assay. Acta Pathologica Microbiologica et Immunologica Scandinavica (C) 1983, 91: 109–115.
Edelstein, P. H.: Improved semiselective medium for isolation ofLegionella pneumophila from contaminated clinical and environmental specimens. Journal of Clinical Microbiology 1981, 14: 298–303.
Warren, W. J., Miller, R. D.: Growth of Legionnaires disease bacterium (Legionella pneumophila) in chemically defined medium. Journal of Clinical Microbiology 1979, 10: 50–55.
Lowry, O. H., Rosebrough, N. J., Farr, A. L., Randall, R. J.: Protein measurement with the folin phenol reagent. Journal of Biological Chemistry 1951, 193: 265–275.
Baek, L.: New, sensitive immunoelectrophoretic assay for measurement of the reaction between endotoxin and limulus amoebocyte lysate. Journal of Clinical Microbiology 1983, 17: 1013–1020.
Massey, V.: The microestimation of succinate and the extinction coefficient of cytochrome c. Biochimica et Biophysica Acta 1959, 34: 255–256.
Kharazmi, A., Döring, G., Høiby, N., Valerius, N. H.: Interaction ofPseudomonas aeruginosa alkaline protease and elastase with human polymorphonuclear leukocytes in vitro. Infection and Immunity 1984, 43: 161–165.
Kharazmi, A., Høiby, N., Döring, G., Valerius, N. H.:Pseudomonas aeruginosa exoproteases inhibit human neutrophil chemiluminescence. Infection and Immunity 1984, 44: 587–589.
Holzer, T. J., Nelson, K. E., Schauf, V., Crispen, R. G., Andersen, B. R.:Mycobacterium leprae fails to stimulate phagocytic cell superoxide anion generation. Infection and Immunity 1986, 51: 514–520.
Wilson, C. B., Tsai, V., Remington, J. S.: Failure to trigger the oxidative metabolic burstbynormal macrophages. Possible mechanism for survival of intracellular pathogens. Journal of Experimental Medicine 1980, 151: 328–346.
Guthrie, L. A., McPhail, L. C., Henson, P. M., Johnston, R. B.: Priming of neutrophils for enhanced release of oxygen metabolites by bacterial lipopolysaccharide. Evidence for increased activity of the superoxide-producing enzyme. Infection and Immunity 1984, 160: 1656–1671.
Sasada, M., Pabst, M. J., Johnston, R. B.: Activation of mouse peritoneal macrophages by lipopolysaccharide alters the kinetic parameters of the superoxide-producing NADPH oxidase. Journal of Biological Chemistry 1983, 258: 9631–9635.
Nelson, R. D., Herron, M. J., Schmidtke, J. R., Simmons, R. L.: Chemiluminescence response of human leukocytes: influence of medium components on light production. Infection and Immunity 1977, 17: 513–520.
Wildfeuer, A., Heymer, B., Schleifer, K. H., Haferkamp, O.: Investigations on the specificity of the limulus test for the detection of endotoxin. Applied Microbiology 1974, 28: 867–871.
Pabst, M. J., Johnston, R. B.: Increased production of superoxide anion by macrophages exposed in vitro to muramyl dipeptide and lipopolysaccharide. Journal of Experimental Medicine 1980, 151: 101–114.
Pabst, M. J., Hedegaard, H. B., Johnston, R. B.: Cultured human monocytes require exposure to bacterial products to maintain an optimal oxygen radical response. Journal of Immunology 1982, 128: 123–128.
Bender, J. G., McPhail, L. C., Van Epps, D. E.: Exposure of human neutrophils to chemotactic factors potentiates activation of the respiratory burst enzyme. Journal of Immunology 1983, 130: 2316–2323.
English, D., Roloff, J. S., Lukens, J. N.: Regulation of human polymorphonuclear leukocyte superoxide release by cellular responses to chemotactic peptides. Journal of Immunology 1981, 126: 165–171.
McPhail, L. C., Clayton, C. C., Snyderman, R.: The NADPH oxidase of human polymorphonuclear leukocytes. Evidence for regulation by multiple signals. Journal of Biological Chemistry 1984, 259: 5768–5775.
English, D., Roloff, J. S., Lukens, J. N.: Chemotactic factor enhancement of superoxide release from fluoride and phorbol myristate acetate stimulated neutrophils. Blood 1981, 58: 129–134.
Davis, G. S., Winn, W. C., Gump, D. W., Beaty, H. N.: The kinetics of early inflammatory events during experimental pneumonia due toLegionella pneumophila in guinea pigs. Journal of Infectious Diseases 1983, 148: 823–835.
Fantone, J. C., Ward, P. A.: Role of oxygen-derived free radicals and metabolites in leukocyte-dependent inflammatory reactions. American Journal of Pathology 1982, 107: 397–418.
Johnson, K. J., Fantone, J. C., Kaplan, J., Ward, P. A.: In vitro damage of rat lungs by oxygen metabolites. Journal of Clinical Investigation 1981, 67: 983–993.
Simon, R. H., DeHart, P. D., Todd, R. F.: Neutrophil induced injury of rat pulmonary alveolar epithelial cells. Journal of Clinical Investigation 1986, 78: 1375–1386.
Smedly, L. A., Tonnesen, M. G., Sandhaus, R. A., Haslett, C., Guthrie, L. A., Johnston, R. B., Henson, P. M., Worthen, G. S.: Neutrophil-mediated injury to endothelial cells. Enhancement by endotoxin and essential role of neutrophil elastase. Journal of Clinical Investigation 1986, 77: 1233–1243.
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Rechnitzer, C., Kharazmi, A., Nielsen, H. et al. Modulation of human neutrophil and monocyte oxidative burst byLegionella pneumophila sonic extract. Eur. J, Clin. Microbiol. 6, 646–652 (1987). https://doi.org/10.1007/BF02013061
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DOI: https://doi.org/10.1007/BF02013061