1887

Abstract

It has been shown that the loss of PilD, a prepilin peptidase necessary for type IV pilus biogenesis and establishment of the type II secretion apparatus is associated with loss of virulence in . is the species most frequently associated with Legionnaires’ disease, but virulence factors unique to this species are not known, so the secretion kinetics of several -dependent enzyme activities, including protease, acid phosphatase, phospholipase A (PLA) and lysophospholipase A (LPLA), of and non- species were compared during growth in BYE broth. Enzyme activity appeared during mid-exponential growth phase and reached maximal levels on entry into stationary growth phase. None of the enzyme activities were unique to and it did not exclusively secrete the highest amounts of the hydrolytic proteins. However, the timing of PLA and LPLA secretion in differed compared to other species. PLA activity was secreted prior to LPLA activity in , which may lead to an accumulation of the cytotoxic agent lysophosphatidylcholine (LPC). In addition to , several other species, including and , were able to enrich for LPC due to a very potent PLA activity accompanied by only moderate LPLA activity. These species, in contrast to , have not been shown to multiply within monocytic host cells. Thus none of the secreted enzymic activities investigated were unique to , nor were they secreted at high concentrations. However, the timing of PLA and LPLA secretion may contribute to pathogenicity.

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2001-11-01
2024-04-24
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References

  1. Aragon, V., Kurtz, S., Flieger, A., Neumeister, B. & Cianciotto, N. P. (2000). Secreted enzymatic activities of wild-type and pilD-deficient Legionella pneumophila. Infect Immun 68, 1855-1863.[CrossRef] [Google Scholar]
  2. Aragon, V., Kurtz, S. & Cianciotto, N. P. (2001).Legionella pneumophila major acid phosphatase and its role in intracellular infection. Infect Immun 69, 177-185.[CrossRef] [Google Scholar]
  3. Aronson, J. F. & Johns, L. W. (1977). Injury of lung alveolar cells by lysolecithin. Exp Mol Pathol 27, 35-42.[CrossRef] [Google Scholar]
  4. Bainbridge, T. & Fick, R. B.Jr (1989). Functional importance of cystic fibrosis immunoglobulin G fragments generated by Pseudomonas aeruginosa elastase. J Lab Clin Med 114, 728-733. [Google Scholar]
  5. Baine, W. B. (1988). A phospholipase C from the Dallas 1E strain of Legionella pneumophila serogroup 5: purification and characterization of conditions for optimal activity with an artificial substrate. J Gen Microbiol 134, 489-498. [Google Scholar]
  6. Berdal, B. P. (1983). Extracellular proteases from Legionella. Zentbl Bakteriol Mikrobiol Hyg Ser A 255, 127-131. [Google Scholar]
  7. Bligh, E. G. & Dyer, W. J. (1959). A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37, 911-917.[CrossRef] [Google Scholar]
  8. Bliska, J. B., Clemens, J. C., Dixon, J. E. & Falkow, S. (1992). The Yersinia tyrosine phosphatase: specificity of a bacterial virulence determinant for phosphoproteins in the J774A.1 macrophage. J Exp Med 176, 1625-1630.[CrossRef] [Google Scholar]
  9. Byrne, B. & Swanson, M. S. (1998). Expression of Legionella pneumophila virulence traits in response to growth conditions. Infect Immun 66, 3029-3034. [Google Scholar]
  10. Camilli, A., Tilney, L. G. & Portnoy, D. A. (1993). Dual roles of plcA in Listeria monocytogenes pathogenesis. Mol Microbiol 8, 143-157.[CrossRef] [Google Scholar]
  11. Conlan, J. W., Baskerville, A. & Ashworth, L. A. (1986). Separation of Legionella pneumophila proteases and purification of a protease which produces lesions like those of Legionnaires’ disease in guinea pig lung. J Gen Microbiol 132, 1565-1574. [Google Scholar]
  12. Dennis, E. A. (1997). The growing phospholipase A2 superfamily of signal transduction enzymes. Trends Biochem Sci 22, 1-2.[CrossRef] [Google Scholar]
  13. Flieger, A., Gong, S., Faigle, M., Deeg, M., Bartmann, P. & Neumeister, B. (2000a). Novel phospholipase A activity secreted by Legionella species. J Bacteriol 182, 1321-1327.[CrossRef] [Google Scholar]
  14. Flieger, A., Gong, S., Faigle, M., Mayer, H. A., Kehrer, U., Mußotter, J., Bartmann, P. & Neumeister, B. (2000b). Phospholipase A secreted by Legionella pneumophila destroys alveolar surfactant phospholipids. FEMS Microbiol Lett 188, 129-133.[CrossRef] [Google Scholar]
  15. Flieger, A., Gong, S., Faigle, M., Stefanovic, S., Cianciotto, N. P. & Neumeister, B. (2001). Novel lysophospholipase A secreted by L. pneumophila. J Bacteriol 183, 2121-2124.[CrossRef] [Google Scholar]
  16. Hales, L. M. & Shuman, H. A. (1999).Legionella pneumophila contains a type II general secretion pathway required for growth in amoebae as well as for secretion of the Msp protease. Infect Immun 67, 3662-3666. [Google Scholar]
  17. Hell, W., Essig, A., Bohnet, S., Gatermann, S. & Marre, R. (1993). Cleavage of tumour necrosis factor-alpha by Legionella exoprotease. APMIS 101, 120-126.[CrossRef] [Google Scholar]
  18. Holm, B. A., Keicher, L., Liu, M. Y., Sokolowski, J. & Enhorning, G. (1991). Inhibition of pulmonary surfactant function by phospholipases. J Appl Physiol 71, 317-321. [Google Scholar]
  19. Kume, N., Cybulsky, M. I. & Gimbrone, M. A.Jr (1992). Lysophosphatidylcholine, a component of atherogenic lipoproteins, induces mononuclear leukocyte adhesion molecules in cultured human and rabbit arterial endothelial cells. J Clin Invest 90, 1138-1144.[CrossRef] [Google Scholar]
  20. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.[CrossRef] [Google Scholar]
  21. Liles, M. R., Edelstein, P. H. & Cianciotto, N. P. (1999). The prepilin peptidase is required for protein secretion by and the virulence of the intracellular pathogen Legionella pneumophila. Mol Microbiol 31, 959-970.[CrossRef] [Google Scholar]
  22. Lindahl, M., Hede, A. R. & Tagesson, C. (1986). Lysophosphatidylcholine increases airway and capillary permeability in the isolated perfused rat lung. Exp Lung Res 11, 1-12.[CrossRef] [Google Scholar]
  23. McIntyre, M., Quinn, F. D., Fields, P. I. & Berdal, B. P. (1991). Rapid identification of Legionella pneumophila zinc metalloprotease using chromogenic detection. APMIS 99, 316-320.[CrossRef] [Google Scholar]
  24. Mintz, C. S., Miller, R. D., Gutgsell, N. S. & Malek, T. (1993).Legionella pneumophila protease inactivates interleukin-2 and cleaves CD4 on human T cells. Infect Immun 61, 3416-3421. [Google Scholar]
  25. Moffat, J. F., Edelstein, P. H., Regula, D. P., Cirillo, J. D. & Tompkins, L. S. (1994). Effects of an isogenic Zn-metalloprotease-deficient mutant of Legionella pneumophila in a guinea-pig pneumonia model. Mol Microbiol 12, 693-705.[CrossRef] [Google Scholar]
  26. Nagl, M., Starlinger, R. & Tiefenbrunner, F. (2000). Influence of sequential cultivation on virulence of Legionella pneumophila and Staphylococcus aureus. Int J Hyg Environ Health 203, 165-167.[CrossRef] [Google Scholar]
  27. Neumeister, B., Schoniger, S., Faigle, M., Eichner, M. & Dietz, K. (1997). Multiplication of different Legionella species in Mono Mac 6 cells and in Acanthamoeba castellanii. Appl Environ Microbiol 63, 1219-1224. [Google Scholar]
  28. Niewoehner, D. E., Rice, K., Sinha, A. A. & Wangensteen, D. (1987). Injurious effects of lysophosphatidylcholine on barrier properties of alveolar epithelium. J Appl Physiol 63, 1979-1986. [Google Scholar]
  29. Pasculle, A. W., Feeley, J. C., Gibson, R. J. & 7 other authors (1980). Pittsburgh pneumonia agent: direct isolation from human lung tissue. J Infect Dis 141, 727–732.[CrossRef] [Google Scholar]
  30. Prestidge, L., Gage, V. & Spizizen, J. (1971). Protease activities during the course of sporulation on Bacillus subtilis. J Bacteriol 107, 815-823. [Google Scholar]
  31. Prokazova, N. V., Zvezdina, N. D. & Korotaeva, A. A. (1998). Effect of lysophosphatidylcholine on transmembrane signal transduction. Biochemistry (Mosc) 63, 31-37. [Google Scholar]
  32. Rechnitzer, C., Williams, A., Wright, J. B., Dowsett, A. B., Milman, N. & Fitzgeorge, R. B. (1992). Demonstration of the intracellular production of tissue-destructive protease by Legionella pneumophila multiplying within guinea-pig and human alveolar macrophages. J Gen Microbiol 138, 1671-1677.[CrossRef] [Google Scholar]
  33. Rossier, O. & Cianciotto, N. P. (2001). Type II protein secretion is a subset of the PilD-dependent processes that facilitate intracellular infection by Legionella pneumophila. Infect Immun 69, 2092-2098.[CrossRef] [Google Scholar]
  34. Szeto, L. & Shuman, H. A. (1990). The Legionella pneumophila major secretory protein, a protease, is not required for intracellular growth or cell killing. Infect Immun 58, 2585-2592. [Google Scholar]
  35. Terada, L. S., Johansen, K. A., Nowbar, S., Vasil, A. I. & Vasil, M. L. (1999).Pseudomonas aeruginosa hemolytic phospholipase C suppresses neutrophil respiratory burst activity. Infect Immun 67, 2371-2376. [Google Scholar]
  36. Touchstone, J. C., Levin, S. S., Dobbins, M. F., Matthews, L., Beers, P. C. & Gabbe, S. G. (1983). (3-sn-Phosphatidyl)cholines (lecithins) in amniotic fluid. Clin Chem 29, 1951-1954. [Google Scholar]
  37. Weltzien, H. U. (1979). Cytolytic and membrane-perturbing properties of lysophosphatidylcholine. Biochim Biophys Acta 559, 259-287.[CrossRef] [Google Scholar]
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