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The effect of oxygen-dependent antimicrobial systems on strains of Legionella pneumophila of different virulence

Published online by Cambridge University Press:  19 October 2009

R. I. Jepras
Affiliation:
Experimental Pathology Laboratory, Public Health Laboratory Service, Centre for Applied Microbiology and Research, Porton Down, Salisbury, Wiltshire SP4 OJG
R. B. Fitzgeorge
Affiliation:
Experimental Pathology Laboratory, Public Health Laboratory Service, Centre for Applied Microbiology and Research, Porton Down, Salisbury, Wiltshire SP4 OJG
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Four strains of Legionella pneumophila of different virulence as identified by ability to produce pneumonia and death in guinea-pigs infected by a fine-particle aerosol were examined for factors which may intracellularly influence virulence. Possible bactericidal mechanisms possessed by alveolar phagocytes were examined. A relationship could be established between resistance to H2O2, catalase activity and virulence amongst the strains.

Virulent strains resisted the bactericidal activity generated by the xanthine oxidase system; avirulent strains did not. Incorporation of various specific inhibitors of the xanthine oxidase system indicated that the main bactericidal activities were associated with the production of H2O2 and hydroxyl radicals ('OH).

All strains of L. pneumophila were susceptible to the bactericidal activity generated by the myeloperoxidase-H202-halide system, confirming earlier observations that polymorphonuclear neutrophil leucocytes (PMNLS) are able to kill both virulent and avirulent strains of L. pneumophila.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1986

References

REFERENCES

Amin, V. M. & Olson, N. F. (1968). Influence of cntnlase activity on resistance of eoagulasepositive Staphylococei to hydrogen peroxide. Applied Microbiology 16. 207270.CrossRefGoogle ScholarPubMed
Badwey, J. A. & Karnovsky, M. L. (1980). Active oxygen species and the functions of phagocytic leukocytes. Annual Review of Biochemistry 49. 695726.CrossRefGoogle ScholarPubMed
Baggiolini, M., De Duve, C., Masson, P. L. & Heremans, J..E. (1970). Association of lactoferrin with specific granules in rabbit hetcrophil leukocytes. Journal of Experimental Medicine 131, 559570.CrossRefGoogle ScholarPubMed
Baggiolini, M., Hirsch, J. G. & De Duve, C. (1969). Resolution of granules from rabbit heterophil leukocytes into distinct populations by zonal sedimentation. Journal of Cell Biology 40, 529541.CrossRefGoogle ScholarPubMed
Baskerville, A., Fitzgeorge, R. B., Broster, M., Hambleton, P. & Dennis, P. J. (1981). Experimental transmission of Legionnaires’ disease by aerosol infection with Legionella pneumophila. Lancet ii, 1389.CrossRefGoogle Scholar
Beauchamp, C. & Fridovich, I. (1970). A mechanism for the production of ethylene from methional. The generation of hydroxyl radical by xanthine oxidase. Journal of Biological Chemistry 245, 46414840.CrossRefGoogle ScholarPubMed
Blackmon, J. A., Hicklin, M. D., Chandler, F. W. and the Special Expert Panel. (1978). Legionnaires’ disease. Pathological and historical aspects of a ‘new’ disease. Archives of Pathology and Laboratory Medicine 102, 337343.Google ScholarPubMed
Bornstein, N., Nowicki, M. & Fleurette, J. (1984). Loss of virulence of L. pneumophila serogroup 1 with conversion of cells to long filamentous rods. In Legionella: Proceedings of the 2nd International Symposium, pp. 7071. Washington, D.C.: American Society for Microbiology.Google Scholar
Bradford, M. M. (1976). A rapid and sensitive method for the quantification of microgram quantities of protein utilising the principle of protein-dye binding. Analytical Biochemistry 72, 248254.CrossRefGoogle Scholar
Cohn, Z. A. & Hirsch, J. G. (1960). The isolation and properties of the specific cytoplasmic granules of rabbit polymorphonuclear leukocytes. Journal of Experimental Medicine 112, 983987.CrossRefGoogle Scholar
Crapo, J. D., McCord, J. M. & Fridovich, I. (1978). Preparation and assay of superoxide dismutases. Methods in Enzymology 53, 382390.CrossRefGoogle ScholarPubMed
Davis, G. S., Winn, W. C., Gump, D. W. & Beaty, H. N. (1983). The kinetics of early inflammatory events during experimental pneumonia due to Legionella pneumophila in guinea pigs. The Journal of Infectious diseases 148, 823835.CrossRefGoogle ScholarPubMed
Del Rio, L. A., Ortega, M. G., Lopez, A. L. & Gorge, J. L. (1977). A more sensitive modification of the catalase assay with the Clark oxygen electrode. Application to the kinetic study of the pea leaf enzyme. Analytical Biochemistry 80, 409415.CrossRefGoogle Scholar
Edelstein, P. H. (1981). Improved semiselective medium for isolation of Legionella pneumophila from contaminated clinical and environmental specimens. Journal of Clinical Microbiology 14, 298303.CrossRefGoogle ScholarPubMed
Elsbach, P. (1980). Degradation of microorganisms by phagocytic cells. Reviews of Infectious Diseases 2, 106127.CrossRefGoogle ScholarPubMed
Fitzgeoroe, R. B., Baskerville, A., Broster, M., Hambleton, P. & Dennis, P. J. (1983). Aerosol infection of animals with strains of Legionella pneumophilaof different virulence: comparison with intraperitoneal and intranasal routes of infection. Journal of Hygience 90, 8189.CrossRefGoogle Scholar
Fitzgeorge, R. B., Keppie, J. & Smith, H. (1965). The relation between resistance to hydrogen peroxide and virulence in brucellae. Journal of Pathology and Bacteriology 89, 745747.CrossRefGoogle ScholarPubMed
Fridovich, I. (1970). Quantitative aspects of the production of superoxide anion radical by milk xanthine oxidase. Journal of Biological Chemistry 245, 40534057.CrossRefGoogle ScholarPubMed
Hanker, J. S., Yates, P. E., Metz, C. B. & Rustioni, A. (1977). A new specific sensitive and non-carcinogenic reagent for the demonstration of horseradish peroxidase. Histochemical Journal 9, 789790.CrossRefGoogle ScholarPubMed
Horwitz, M. A. & Silverstein, S. C. (1981 a). Interaction of the Legionnaires’ disease bacterium with human phagocytes. I. L. pneumophilaresists killing by polymorphonuclear leukocytes, antibody and complement. Journal of Experimental Medicine 153, 386397.CrossRefGoogle Scholar
Horwitz, M. A. & Silverstein, S. C. (1981 b). Interaction of the Legionnaires' disease bacterium with human phagocytes. II. Antibody promotes binding of L. pneumophila to monocytes but does not inhibit intracellular multiplication. Journal of Experimental Medicine 153, 398406.CrossRefGoogle Scholar
Jensen, M. S. & Bainton, D. F. (1973). Temporal changes in pH within the phagocytic vacuole of the polymorphonuclear neutrophilic leukocyte. Journal of Cell Biology 56, 379388.CrossRefGoogle ScholarPubMed
Jepras, R. I., Fitzgeorge, R. B. & Baskerville, A. (1985). A comparison of virulence of two strains of Legionella pneumophila based on experimental aerosol infection of guinea pigs. Journal of Hygiene 95, 2938.CrossRefGoogle ScholarPubMed
Johnson, R. J., Keel, B. B., Misra, H. P., Lehmeyer, L. S., Webb, R. L. & Rajacopalan, K. V. (1975). The role of superoxide anion generation in phagocytic bactericidal activity studies with normal and chronic granulomatous disease leukocytes. The Journal of Clinical Investigation 55, 13571372.CrossRefGoogle Scholar
Kellogg, E. W. III & Fridovich, I. (1975). Superoxide, hydrogen peroxide and singlet oxygen in lipid peroxidation by a xanthine oxidase system. Journal of Biological Chemistry 250, 88128817.CrossRefGoogle ScholarPubMed
Klebanoff, S. (1967). A peroxidase-mediated antimicrobial system in leukocytes. The Journal oj Clinical Investigation 46, 10781082.Google Scholar
Klebanoff, S. J. (1975). Antimicrobial mechanisms in neutrophilic polymorphonuclear leukocytes. Seminars In Hematology 12, 117192.Google ScholarPubMed
Klebanoff, S. J. (1980). Oxygen intermediates and the microcidal event. In Mononuclear Phagocytes. Functional Aspects, Part II (Ed. Furth, R. van), pp.11051137. The Hague, Boston & London: Martinus Nighoff Publishers.CrossRefGoogle Scholar
Klebanoff, S. J. & Hamon, C. B. (1972). Role of myeloperoxidase-mediated antimicrobial system in intact leukocytes. Journal of Reticuloendothelial Society 12, 170196.Google ScholarPubMed
Lattimer, G. L. & Ormsbee, R. A. (1981). Legionnaires’ Disease p. 176. New York and Basel: Marcel Dekker.Google Scholar
Leffell, M. S. & Spitznagel, J. K. (1982). Association of lactoferrin with lysozyme in granules of human polymorphonuclear leukocytes. Injection and Immunity 6, 761765.CrossRefGoogle Scholar
Lochner, J. E., Friedman, R. L., Bigley, R. H. & Iglewski, B. H. (1983). Effect of oxygen-dependent antimicrobial systems on Legionella pneumophila. Infection and Immunity 39, 487489.CrossRefGoogle ScholarPubMed
Locksley, R. M., Jacobs, R. F., Wilson, C. B., Weaver, W. M. & Klebanoff, S. J. (1982). Susceptibility of Legionella pneumophilato oxygen-dependent microbicidal systems. The Journal of Immunology 129, 21922197.CrossRefGoogle ScholarPubMed
Mandell, G. L. (1975). Catalase, superoxide dismutase and virulence of Staphylococus Aureus. In-vitro and in-vivo studies with emphasis on staphylococal-leukocyte interaction. The Journal of Clinical Investigation 55, 561566.CrossRefGoogle Scholar
Nelson, D. P. & Kiesow, L. A. (1972). Enthalpy of decomposition of hydrogen peroxide by catalase at 25 °C (with molar extinction coefficients of H2O2 solutions in the UV). Analytical Biochemistry 49, 474478.CrossRefGoogle ScholarPubMed
Ristroph, J. D., Hedlund, K. W. & Allen, R. G. (1980). Liquid medium for growth of Legionella pneumophila. Journal of Clinical Microbiology 11, 1921.CrossRefGoogle ScholarPubMed
Rosen, H. & Klebanoff, S. J. (1979). Bactericidal activity of a superoxide anion-generating system. A model for the polvmorphonuclear leukocyte. Journal of Experimental Medicine 149, 2739.CrossRefGoogle Scholar
Rossi, F., Bellaville, P. & Berton, G. (1982). The respiratory burst in phagocytic leukocytes. In Phagocytosis Past and Future (Ed. Karnovsky, M. L., and Bolis, L.), pp. 167191. New York: Academic Press.Google Scholar
Spitznagel, J. K. & Chi, M. Y. (1963). Cationic proteins and antibacterial properties of infected tissues and leukocytes. American Journal of Pathology 43, 697711.Google ScholarPubMed
Wilson, J. B. & Dasinger, B. L. (1960). Biochemical properties of virulent and avirulent strains of brucellae. Annals of the New York Academy of Science 88, 11551166.CrossRefGoogle ScholarPubMed
Winn, W. C. Jr, Glavin, F. L., Perl, D. P., Keller, J. K., Andres, T. L., Brown, T. M., Coffin, C. M., Sensecqua, J. E., Roman, L. N. & Craiohead, J. E. (1978). The pathology of Legionnaires' disease: fourteen fatal cases from the 1977 outbreak in Vermont. Archive of Pathology and Laboratory Medicine 102, 344350.Google ScholarPubMed
Winn, W. C. Jr & Myerowitz, R. L. (1981). The pathology of the Legionella pneumonias. Human Pathology 12, 401422.CrossRefGoogle ScholarPubMed