1887

Abstract

The pathogenesis of is at least partially attributable to its ability to synthesize and secrete the siderophore pyoverdin and the two zinc metalloproteases elastase and LasA, and its ability to form biofilms in which bacterial cells are embedded in an alginate matrix. In the present study, a lysophospholipid, 1-palmitoyl-2-hydroxy--glycero-3-phosphate [also called monopalmitoylphosphatidic acid (MPPA)], which accumulates in inflammatory exudates, was shown to inhibit the extracellular accumulation of PAO1 alginate, elastase, LasA protease and the siderophore pyoverdin. MPPA also inhibited biofilm formation. The inhibitory effects of MPPA occur independently of expression and without affecting the accumulation of the autoinducers -(3-oxododecanoyl) homoserine lactone and -butyryl-L-homoserine lactone, and may be due, at least in part, to the ability of MPPA to bind divalent cations.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-148-6-1709
2002-06-01
2019-10-16
Loading full text...

Full text loading...

/deliver/fulltext/micro/148/6/1481709a.html?itemId=/content/journal/micro/10.1099/00221287-148-6-1709&mimeType=html&fmt=ahah

References

  1. Abraham, E., Bursten, S., Shenkar, R. & 7 other authors ( 1995; ). Phosphatidic acid signaling mediates lung cytokine expression and lung inflammatory injury after hemorrhage in mice. J Exp Med 18, 569–575.
    [Google Scholar]
  2. Baltimore, R. S. (1993). Mucoid colony variants: the exopolysaccharide of Pseudomonas aeruginosa and microcolony formation. In Pseudomonas aeruginosa the Opportunist: Pathogenesis and Disease, pp. 26–40. Edited by R. B. Fick, Jr. Boca Raton, FL: CRC Press.
  3. Bodey, G. P., Bolivar, R., Fainstein, V. & Jadeja, L. ( 1983; ). Infections caused by Pseudomonas aeruginosa. Rev Infect Dis 5, 279-313.[CrossRef]
    [Google Scholar]
  4. Brint, J. M. & Ohman, D. E. ( 1996; ). Synthesis of multiple exoproducts in Pseudomonas aeruginosa is under the control of RhlR–RhlI, another set of regulators in strain PAO1 with homology to the autoinducer-responsive LuxR–LuxI family. J Bacteriol 177, 7155-7163.
    [Google Scholar]
  5. Brumlik, M. J. & Storey, D. G. ( 1992; ). Zinc and iron regulate translation of the gene encoding Pseudomonas aeruginosa elastase. Mol Microbiol 6, 337-344.[CrossRef]
    [Google Scholar]
  6. Brumlik, M. J. & Storey, D. G. ( 1998; ). Post-transcriptional control of Pseudomonas aeruginosa lasB expression involves the 5′ untranslated region of the mRNA. FEMS Microbiol Lett 159, 233-239.
    [Google Scholar]
  7. Charlton, T. S., de Nys, R., Netting, A., Kumar, N., Hentzer, M., Givskov, M. & Kjelleberg, S. ( 2000; ). A novel and sensitive method for the quantification of N-3-oxoacyl homoserine lactones using gas chromatography-mass spectrometry: application to a model bacterial biofilm. Environ Microbiol 2, 530-541.[CrossRef]
    [Google Scholar]
  8. Chettibi, S., Sawrence, A. J., Stevenson, R. D. & Young, J. D. ( 1994; ). Effect of lysophosphatidic acid on motility, polarisation, and metabolic burst of human neutrophils. FEMS Immunol Med Microbiol 8, 271-281.[CrossRef]
    [Google Scholar]
  9. Christiansen, K. & Carlsen, J. ( 1983; ). Reconstitution of a protein into lipid vesicles using natural detergents. Biochim Biophys Acta 735, 225-233.[CrossRef]
    [Google Scholar]
  10. Clark, D. J. & Maaløe, O. ( 1967; ). DNA replication and the division cycle in Escherichia coli. J Mol Biol 23, 99-112.[CrossRef]
    [Google Scholar]
  11. Costerton, J. W., Cheng, K. J., Geesey, G. G., Ladd, T. I., Nickel, J. C., Dasgupta, M. & Marrie, T. J. ( 1987; ). Bacterial biofilms in nature and disease. Annu Rev Microbiol 41, 435-464.[CrossRef]
    [Google Scholar]
  12. Cox, C. D. (1993). Iron and the virulence of Pseudomonas aeruginosa. In Pseudomonas aeruginosa the Opportunist: Pathogenesis and Disease, pp. 41–58. Edited by R. B. Fick, Jr. Boca Raton, FL: CRC Press.
  13. Coyne, M. J.Jr, Russell, K. S., Coyle, C. L. & Goldberg, J. B. ( 1994; ). The Pseudomonas aeruginosa algC gene encodes phosphoglucomutase, required for the synthesis of a complete lipopolysaccharide core. J Bacteriol 176, 3500-3507.
    [Google Scholar]
  14. Cryz, S. J.Jr, Pitt, T. L., Furer, E. & Germanier, R. ( 1984; ). Role of lipopolysaccharide in virulence of Pseudomonas aeruginosa. Infect Immun 44, 508-513.
    [Google Scholar]
  15. Davies, D., Parsek, M., Pearson, J., Iglewski, B., Costerton, J. & Greenberg, E. ( 1998; ). The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280, 295-298.[CrossRef]
    [Google Scholar]
  16. Ediger, T. L. & Towes, M. L. ( 2001; ). Dual effects of lysophosphatidic acid on human airway smooth muscle cell proliferation and survival. Biochim Biophys Acta 1531, 59-67.[CrossRef]
    [Google Scholar]
  17. Fourcade, O., Le Balle, F., Fauvel, J., Simon, M. F. & Chap, H. ( 1998; ). Regulation of secretory type-II phospholipase A2 and of lysophosphatidic acid synthesis. Adv Enzyme Regul 38, 99-107.[CrossRef]
    [Google Scholar]
  18. Gallagher, S. R. (1999). One-dimensional SDS gel electrophoresis of proteins. In Current Protocols in Molecular Biology, pp. 10.2A.1–10.2A.34. New York: Wiley.
  19. Gallagher, S., Winston, S. E., Fuller, S. A. & Hurrell, J. G. R. (1997). Immunoblotting and immunodetection. In Current Protocols in Molecular Biology, pp. 10.8.1–10.8.21. New York: Wiley.
  20. Gambello, M. J. & Iglewski, B. H. ( 1991; ). Cloning and characterization of the Pseudomonas aeruginosa lasR gene: a transcriptional activator of elastase expression. J Bacteriol 173, 3000-3009.
    [Google Scholar]
  21. Haas, B., Kraut, J., Marks, J., Zanker, S. C. & Castignetti, D. ( 1991; ). Siderophore presence in sputa of cystic fibrosis patents. Infect Immun 59, 3997-4000.
    [Google Scholar]
  22. Halmerbauer, G., Arri, S., Schierl, M., Strauch, E. & Koller, D. Y. ( 2000; ). The relationship of eosinophil granule proteins to ions in the sputum of patients with cystic fibrosis. Clin Exp Allergy 30, 1771-1776.[CrossRef]
    [Google Scholar]
  23. Hancock, R. E. W., Mutharia, L. M., Chan, L., Darveau, R. P., Speert, D. P. & Pier, G. B. ( 1983; ). Pseudomonas aeruginosa isolates from patients with cystic fibrosis: a class of serum-sensitive, nontypable strains deficient in lipopolysaccharide O side chains. Infect Immun 42, 170-177.
    [Google Scholar]
  24. Hodgins, G. R. ( 1961; ). Chelating agents. In Handbook of Chemistry and Physics , pp. 1476-1491. Edited by C. D. Hodgman, R. C. Weast & S. M. Selby. Cleveland, OH:The Chemical Rubber Publishing Company.
  25. Höfte, M., Buysens, A., Koedam, N. & Cornelis, P. ( 1993; ). Zinc affects siderophore-mediated high affinity iron uptake systems in the rhizosphere Pseudomonas aeruginosa 7NSK2. Biometals 6, 85-91.
    [Google Scholar]
  26. Howe, T. R. & Iglewski, B. H. ( 1984; ). Isolation and characterization of alkaline protease-deficient mutants of Pseudomonas aeruginosa in vitro and in a mouse eye model. Infect Immun 43, 1058-1063.
    [Google Scholar]
  27. Iglewski, B. H., Rust, L. & Bever, R. ( 1990; ). Molecular analysis of elastase. In Pseudomonas: Biotransformations, Pathogenesis, and Evolving Biotechnology , pp. 36-43. Edited by S. Silver, A. M. Chakrabarty, B. Iglewski & S. Kaplan. Washington, DC:American Society for Microbiology.
  28. Kadurugamuwa, J. L. & Beveridge, T. J. ( 1997; ). Natural release of virulence factors in membrane vesicles by Pseudomonas aeruginosa and the effect of aminoglycoside antibiotics on their release. J Antimicrob Chemother 40, 615-621.[CrossRef]
    [Google Scholar]
  29. Kessler, E. & Safrin, M. ( 1988; ). Synthesis, processing, and transport of Pseudomonas aeruginosa elastase. J Bacteriol 170, 5241-5247.
    [Google Scholar]
  30. Kessler, E., Safrin, M., Abrams, W. R., Rosenbloom, J. & Ohman, D. E. ( 1997; ). Inhibitors and specificity of Pseudomonas aeruginosa LasA. J Biol Chem 272, 9884-9889.[CrossRef]
    [Google Scholar]
  31. Kessler, E., Safrin, M., Gustin, J. K. & Ohman, D. E. ( 1998; ). Elastase and the LasA protease of Pseudomonas aeruginosa are secreted with their propeptides. J Biol Chem 273, 30225-30231.[CrossRef]
    [Google Scholar]
  32. Krogfelt, K. A., Utley, M., Krivan, H. C., Laux, D. C. & Cohen, P. S. ( 2000; ). Specific phospholipids enhance the activity of β-lactam antibiotics against Pseudomonas aeruginosa. J Antimicrob Chemother 46, 377-384.[CrossRef]
    [Google Scholar]
  33. Kronborg, G. ( 1995; ). Lipopolysaccharide (LPS), LPS immune complexes and cytokines as inducers of inflammation in patients with cystic fibrosis and chronic Pseudomonas aeruginosa lung infection. APMIS 103, 1-30.[CrossRef]
    [Google Scholar]
  34. Kronborg, G., Fomsgaard, A., Galanos, C., Freudenberg, M. A. & Hoiby, N. ( 1992; ). Antibody response to lipid A, core, and O sugars of the Pseudomonas aeruginosa lipopolysaccharide in chronically infected cystic fibrosis patients. J Clin Microbiol 30, 1848-1855.
    [Google Scholar]
  35. Liu, P. V., Matsumoto, H., Kusama, H. & Bergan, T. ( 1983; ). Survey of heat-stable, major somatic antigens of Pseudomonas aeruginosa. Int J Syst Bacteriol 33, 256-264.[CrossRef]
    [Google Scholar]
  36. Luzar, M. A. & Montie, T. C. ( 1985; ). Avirulence and altered physiological properties of cystic fibrosis strains of Pseudomonas aeruginosa. Infect Immun 50, 572-576.
    [Google Scholar]
  37. Martinez, A., Ostrovsky, P. & Nunn, D. N. ( 1998; ). Identification of an additional member of the secretin superfamily of proteins in Pseudomonas aeruginosa that is able to function in type II protein secretion. Mol Microbiol 28, 1235-1246.[CrossRef]
    [Google Scholar]
  38. May, T. B. & Chakrabarty, A. M. ( 1994; ). Isolation and assay of Pseudomonas aeruginosa alginate. Methods Enzymol 235, 295-298.
    [Google Scholar]
  39. Nicas, T. I., Frank, D. W., Stenzel, P., Bradley, J. & Iglewski, B. H. ( 1985; ). Role of exoenzyme S in chronic Pseudomonas aeruginosa lung infections. Eur J Clin Microbiol Infect Dis 4, 175-179.
    [Google Scholar]
  40. Ochsner, U. A. & Reiser, J. ( 1995; ). Autoinducer mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 92, 6424-6428.[CrossRef]
    [Google Scholar]
  41. Ojeniji, B. ( 1994; ). Polyagglutinable Pseudomonas aeruginosa from cystic fibrosis patients: a survey. APMIS 102 (Suppl. 46), 1–44.
    [Google Scholar]
  42. Olson, J. C. & Ohman, D. E. ( 1992; ). Efficient production and processing of elastase and LasA by Pseudomonas aeruginosa require zinc and calcium ions. J Bacteriol 174, 4140-4147.
    [Google Scholar]
  43. O’Toole, G. A., Pratt, L. A., Watnick, P. I., Newman, D. K., Weaver, V. B. & Kolter, R. ( 1999; ). Genetic approaches to study of biofilms. Methods Enzymol 130, 91-109.
    [Google Scholar]
  44. Passador, L., Cook, J. M., Gambello, M. J., Rust, L. & Iglewski, B. H. ( 1993; ). Expression of Pseudomonas aeruginosa virulence genes requires cell-to-cell communication. Science 260, 1127-1130.[CrossRef]
    [Google Scholar]
  45. Paya, M., Terencio, M. C., Ferrandiz, M. L. & Alcaraz, M. J. ( 1996; ). Involvement of secretory phospholipase A2 activity in the zymosan rat air pouch model of inflammation. Br J Pharmacol 117, 1773-1779.[CrossRef]
    [Google Scholar]
  46. Pearson, J. P., Gray, K. M., Passador, L., Tucker, K. D., Eberhard, A., Iglewski, B. H. & Greenberg, E. P. ( 1994; ). Structure of the autoinducer required for expression of Pseudomonas aeruginosa virulence genes. Proc Natl Acad Sci USA 91, 197-201.[CrossRef]
    [Google Scholar]
  47. Pearson, J. P., Passador, L., Iglewski, B. H. & Greenberg, E. P. ( 1995; ). A second N-acylhomoserine lactone signal produced by Pseudomonas aeruginosa. Proc Natl Acad Sci USA 92, 1490-1494.[CrossRef]
    [Google Scholar]
  48. Pearson, J. P., Pesci, E. C. & Iglewski, B. H. ( 1997; ). Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in the control of elastase and rhamnolipid biosynthesis genes. J Bacteriol 179, 5756-5767.
    [Google Scholar]
  49. Preston, M. J., Seed, P. C., Toder, D. S., Iglewski, B. H., Ohman, D. E., Gustin, J. K., Goldberg, J. B. & Pier, G. B. ( 1997; ). Contribution of proteases and LasR to the virulence of Pseudomonas aeruginosa during corneal infections. Infect Immun 65, 3086-3090.
    [Google Scholar]
  50. Rossbach, S., Wilson, T. L., Kukuk, M. L. & Carty, H. A. ( 2000; ). Elevated zinc induces siderophore biosynthesis genes and a zntA-like gene in Pseudomonas fluorescens. FEMS Microbiol Lett 191, 61-70.[CrossRef]
    [Google Scholar]
  51. Rust, L., Pesci, E. C. & Iglewski, B. H. ( 1996; ). Analysis of the Pseudomonas aeruginosa elastase (lasB) regulatory region. J Bacteriol 178, 1134-1140.
    [Google Scholar]
  52. Shortridge, V. D., Lazdunski, A. & Vasil, M. L. ( 1992; ). Osmoprotectants and phosphate regulate expression of phospholipase C in Pseudomonas aeruginosa. Mol Microbiol 6, 863-871.[CrossRef]
    [Google Scholar]
  53. Speert, D. P., Dimmick, J. E., Pier, G. B., Saunders, J. M., Hancock, R. E. W. & Kelly, N. ( 1987; ). An immunohistological evaluation of Pseudomonas aeruginosa pulmonary infection in two patients with cystic fibrosis. J Clin Microbiol 22, 743-747.
    [Google Scholar]
  54. Suh, S., Silo-Suh, L., Woods, D., Hassett, D. J., West, S. & Ohman, D. E. ( 1999; ). Effect of rpoS mutation on the stress response and expression of virulence factors in Pseudomonas aeruginosa. J Bacteriol 181, 3890-3897.
    [Google Scholar]
  55. Swift, S., Karlyshev, A. V., Fish, L., Durant, E. L., Winson, M. K., Chhabra, S. R., Williams, P., MacIntyre, S. & Stewart, G. S. ( 1997; ). Quorum sensing in Aeromonas hydrophila and Aeromonas salmonicida: identification of the LuxRI homologs AhyRI and AsaRI and their cognate N-acylhomoserine lactone signal molecules. J Bacteriol 179, 5271-5281.
    [Google Scholar]
  56. Tang, H., Kays, M. & Prince, A. ( 1995; ). Role of Pseudomonas aeruginosa pili in acute pulmonary infection. Infect Immun 63, 1278-1285.
    [Google Scholar]
  57. Tang, H. B., DiMango, D., Bryan, R., Gambello, M., Iglewski, B. H., Goldberg, J. B. & Prince, A. ( 1996; ). Contribution of specific Pseudomonas aeruginosa virulence factors to pathogenesis of pneumonia in a neonatal mouse model of infection. Infect Immun 64, 37-43.
    [Google Scholar]
  58. Telford, G., Wheeler, D., Williams, P., Tomkins, P. T., Appleby, P., Sewell, H., Stewart, G. S. A. B., Bycroft, B. W. & Pritchard, D. I. ( 1998; ). The Pseudomonas aeruginosa quorum-sensing signal molecule N-(3-oxododecanoyl)-l-homoserine lactone has immunomodulatory activity. Infect Immun 66, 36-42.
    [Google Scholar]
  59. Toder, D. S., Ferrell, S. J., Nezezon, J. L., Rust, L. & Iglewski, B. H. ( 1994; ). lasA and lasB genes of Pseudomonas aeruginosa: analysis of transcription and gene product activity. Infect Immun 62, 1320-1327.
    [Google Scholar]
  60. Tommassen, J., Fillous, A., Bally, M., Murgier, M. & Lazdunski, A. ( 1992; ). Protein secretion in Pseudomonas aeruginosa. FEMS Microbiol Rev 9, 73-90.
    [Google Scholar]
  61. Van Delden, C. & Iglewski, B. ( 1998; ). Cell-to-cell signaling and Pseudomonas aeruginosa infections. Emerg Infect Dis 4, 551-560.[CrossRef]
    [Google Scholar]
  62. Vasil, M. L. & Ochsner, U. A. ( 1999; ). The response of Pseudomonas aeruginosa to iron: genetics, biochemistry and virulence. Mol Microbiol 34, 399-413.[CrossRef]
    [Google Scholar]
  63. Vasil, M. L., Prince, R. W. & Shortridge, V. D. (1993). Exoproducts: Pseudomonas exotoxin A and phospholipase C. In Pseudomonas aeruginosa the Opportunist: Pathogenesis and Disease, pp. 59–77. Edited by R. B. Fick, Jr. Boca Raton, FL: CRC Press.
  64. Whiteley, M., Lee, K. M. & Greenberg, E. P. ( 1999; ). Identification of genes controlled by quorum sensing in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 96, 13904-13909.[CrossRef]
    [Google Scholar]
  65. Whiteley, M., Parsek, M. R. & Greenberg, E. P. ( 2000; ). Regulation of quorum sensing by RpoS in Pseudomonas aeruginosa. J Bacteriol 182, 4356-4360.[CrossRef]
    [Google Scholar]
  66. Winson, M., Camara, M., Latifi, A. & 10 other authors ( 1995; ). Multiple N-acyl-l-homoserine lactone signal molecules regulate production of virulence determinants and secondary metabolites in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 92, 9427–9431.[CrossRef]
    [Google Scholar]
  67. Woods, D. E., Cryz, S. J., Friedman, R. L. & Iglewski, B. H. ( 1982; ). Contribution of extoxin A and elastase to virulence of Pseudomonas aeruginosa in chronic lung infections of rats. Infect Immun 36, 1223-1228.
    [Google Scholar]
  68. Zhou, X., George, S. E., Frank, D. W., Utley, M., Gilmour, I., Krogfelt, K. A., Claxton, L. D., Laux, D. C. & Cohen, P. S. ( 1997; ). Isolation and characterization of an attenuated strain of Pseudomonas aeruginosa, a 3,5-dichlorobenzoate degrader. Appl Environ Microbiol 63, 1389-1395.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-148-6-1709
Loading
/content/journal/micro/10.1099/00221287-148-6-1709
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error