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Volume 146, Issue 10

Detection of -acylhomoserine lactones in lung tissues of mice infected with Free

Abstract

The pathogenesis of is associated with expression of virulence factors, many of which are controlled by two -acylhomoserine lactone (AHL)-based quorum-sensing systems. strains equipped with a -based monitor system expressing green fluorescent protein (GFP) in the presence of exogenous AHL molecules were used to detect the production of AHLs from . Mice were challenged intratracheally with alginate beads containing and and killed on different days after the challenge. By means of confocal scanning laser microscopy, GFP-expressing bacteria could be detected in the lung tissues, indicating production and excretion of AHL molecules by the infecting . AHL signals were detected mainly in lung tissues exhibiting severe pathological changes. These findings support the view that expression of AHL molecules by during infection coincides with its pathogenesis.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): AHL, N-acylhomoserine lactone (BHL, N-butanoyl-, HHL, N-hexanoyl-, OdDHL, N-(3-oxododecanoyl)-, ODHL, N-(3-oxodecanoyl)-, OHHL, N-(3-oxohexanoyl)-, OHL, N-octanoylhomoserine lactone); CF, cystic fibrosis , AHL, quorum sensing , CSLM, confocal scanning laser microscopy; GFP, green fluorescent protein , green fluorescent protein (GFP) , lung infection , mouse model and PMN, polymorphonuclear leukocyte
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2000-10-01
2024-04-16
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References

  1. Andersen J. B., Sternberg C., Poulsen L., Bjorn S., Givskov M., Molin S. 1998; New unstable variants of green fluorescent protein for studies of transient gene expression in bacteria. Appl Environ Microbiol 64:2240–2246
     [Google Scholar]
  2. Baltimore R. S., Christie C. D., Smith G. J. 1989; Immunohistopathologic localization of Pseudomonas aeruginosa in lungs from patients with cystic fibrosis. Implications for the pathogenesis of progressive lung deterioration. Am Rev Respir Dis 140:1650–1661 [CrossRef]
     [Google Scholar]
  3. Bergen G., Shelhamer J. 1996; Pulmonary infiltrates in the cancer patient. New approaches to an old problem. Infect Dis Clin N Am 10:297–325 [CrossRef]
     [Google Scholar]
  4. Bowton D. 1999; Nosocomial pneumonia in the ICU – year 2000 and beyond. Chest 115:28S–33S [CrossRef]
     [Google Scholar]
  5. Brint J. M., Ohman D. E. 1995; 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]
  6. Chapon-Herve V., Akrim M., Latifi A., Williams P., Lazdunski A., Bally M. 1997; Regulation of the xcp secretion pathway by multiple quorum-sensing modulons in Pseudomonas aeruginosa. Mol Microbiol 24:1169–1178 [CrossRef]
     [Google Scholar]
  7. Cormack B. P., Valdivia R. H., Falkow S. 1996; FACS-optimized mutants of the green fluorescent protein (GFP). Gene 173:33–38 [CrossRef]
     [Google Scholar]
  8. 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]
  9. 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]
  10. Finch R., Pritchard D., Bycroft B., Williams P., Stewart G. 1998; Quorum sensing: a novel target for anti-infective therapy. J Antimicrob Chemother 42:569–571 [CrossRef]
     [Google Scholar]
  11. Fuqua C., Greenberg E. 1998; Self perception in bacteria: quorum sensing with acylated homoserine lactones. Curr Opin Microbiol 1:183–189 [CrossRef]
     [Google Scholar]
  12. Fuqua C., Winans S., Greenberg E. 1996; Census and consensus in bacterial ecosystems: the LuxR-LuxI family of quorum-sensing transcriptional regulators. Annu Rev Microbiol 50:727–751 [CrossRef]
     [Google Scholar]
  13. 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]
  14. Gambello M. J., Kaye S., Iglewski B. H. 1993; LasR of Pseudomonas aeruginosa is a transcriptional activator of the alkaline protease gene (apr) and an enhancer of exotoxin A expression. Infect Immun 61:1180–1184
     [Google Scholar]
  15. Geisenberger O., Givskov M., Riedel K., Høiby N., Tümmler B., Eberl L. 2000; Production of N-acyl-l-homoserine lactones by Pseudomonas aeruginosa isolates from chronic lung infections associated with cystic fibrosis. . FEMS Microbiol Lett 184:273–277
     [Google Scholar]
  16. Givskov M., de-Nys R., Manefield M., Gram L., Maximilien R., Eberl L., Molin S., Steinberg P. D., Kjelleberg S. 1996; Eukaryotic interference with homoserine lactone mediated procaryotic signalling. J Bacteriol 178:6618–6622
     [Google Scholar]
  17. Glessner A., Smith R., Iglewski B., Robinson J. 1999; Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of twitching motility. J Bacteriol 181:1623–1629
     [Google Scholar]
  18. Govan J. R., Deretic V. 1996; Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol Rev 60:539–574
     [Google Scholar]
  19. Hardman A., Stewart G., Williams P. 1998; Quorum sensing and the cell-cell communication dependent regulation of gene expression in pathogenic and non-pathogenic bacteria. Antonie Leeuwenhoek 74:199–210 [CrossRef]
     [Google Scholar]
  20. Hardman A., Rodgers H. C., Middleton B., Camara M., Knox A. J., Williams P. 1999; Detection of N-acylhomoserine lactones in CF sputum – a new marker of inflammation in cystic fibrosis. Pediat Pulmonol(suppl.) 19:274
     [Google Scholar]
  21. Hartman G., Wise R. 1998; Quorum sensing: potential means of treating gram-negative infection?. Lancet 351:848–849 [CrossRef]
     [Google Scholar]
  22. Hastings J., Greenberg E. 1999; Quorum sensing: the explanation of a curious phenomenon reveals a common characteristic of bacteria. . J Bacteriol 181:2667–2668
     [Google Scholar]
  23. Hoiby N. 1995; Microbiology of cystic fibrosis. In Cystic Fibrosis pp. 75–98Edited by Hodson M. E., Geddes D. M. London: Chapman & Hall;
     [Google Scholar]
  24. Hoiby N., Giwercman B., Jensen T., Johansen H. K., Kronborg G., Pressler T., Kharazmi A. 1993; Immune response in cystic fibrosis – helpful or harmful?. In Clinical Ecology of Cystic Fibrosis pp. 133–141Edited by Scobar H.others Amsterdam: Excerpta Medica;
     [Google Scholar]
  25. Holloway B. W., Morgan A. F. 1986; Genome organization in Pseudomonas. Annu Rev Microbiol 40:79–105 [CrossRef]
     [Google Scholar]
  26. Jensen E. T., Kharazmi A., Garred P., Kronborg G., Fomsgaard A., Mollnes T. E., Hoiby N. 1993; Complement activation by Pseudomonas aeruginosa biofilms. Microb Pathog 15:377–388 [CrossRef]
     [Google Scholar]
  27. Johansen H. K., Espersen F., Pedersen S. S., Hougen H. P., Rygaard J., Hoiby N. 1993; Chronic Pseudomonas aeruginosa lung infection in normal and athymic rats. APMIS 101:207–225 [CrossRef]
     [Google Scholar]
  28. Jones S., Yu B., Bainton N. J.11 other authors 1993; The lux autoinducer regulates the production of exoenzyme virulence determinants in Erwinia carotovora and Pseudomonas aeruginosa. EMBO J 12:2477–2482
     [Google Scholar]
  29. Kharazmi A., Schitz P. O., Hoiby N., Baek L., Doring G. 1986; Demonstration of neutrophil chemotactic activity in the sputum of cystic fibrosis patients with Pseudomonas aeruginosa infection. Eur J Clin Invest 16:143–148 [CrossRef]
     [Google Scholar]
  30. Koch C., Hoiby N. 1993; Pathogenesis of cystic fibrosis. Lancet 341:1065–1069 [CrossRef]
     [Google Scholar]
  31. Latifi A., Foglino M., Tanaka K., Williams P., Lazdunski A. 1996; A hierarchical quorum-sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhIR (VsmR) to expression of the stationary-phase sigma factor RpoS. Mol Microbiol 21:1137–1146 [CrossRef]
     [Google Scholar]
  32. Manefield M., De Nys R., Kumar N., Read R., Givskov M., Steinberg P., Kjellebjerg S. 1999; Evidence that halogenated furanones from Delisea pulchra inhibit acylated homoserine lactone (AHL)-mediated gene expression by displacing the AHL signal from its receptor protein. Microbiology 145:283–291 [CrossRef]
     [Google Scholar]
  33. Moser C., Johansen H. K., Song Z. J., Hougen H. P., Rygaard J., Hoiby N. 1997; Chronic Pseudomonas aeruginosa lung infection is more severe in Th2 responding BALB/c mice compared to Th1 responding C3H/HeN mice. APMIS 105:838–842 [CrossRef]
     [Google Scholar]
  34. Ochsner U. A., Reiser J. 1995; Autoinducer-mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. . Proc Natl Acad Sci U S A 92:6424–6428 [CrossRef]
     [Google Scholar]
  35. 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]
  36. 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 the expression of Pseudomonas aeruginosa virulence genes. Proc Natl Acad Sci U S A 91:197–201 [CrossRef]
     [Google Scholar]
  37. 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 U S A 92:1490–1494 [CrossRef]
     [Google Scholar]
  38. Pearson J., Pesci E., Iglewski B. 1997; Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of elastase and rhamnolipid biosynthesis genes. J Bacteriol 179:5756–5767
     [Google Scholar]
  39. Pearson J., Van Delden C., Iglewski B. 1999; Active efflux and diffusion are involved in transport of Pseudomonas aeruginosa cell-to-cell signals. J Bacteriol 181:1203–1210
     [Google Scholar]
  40. Pedersen S. S., Shand G. H., Hansen B. L., Hansen G. N. 1990; Induction of experimental chronic Pseudomonas aeruginosa lung infection with P. aeruginosa entrapped in alginate microspheres. APMIS 98:203–211 [CrossRef]
     [Google Scholar]
  41. Pesci E., Pearson J., Seed P., Iglewski B. 1997; Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. J Bacteriol 179:3127–3132
     [Google Scholar]
  42. Pirhonen M., Flego D., Heikinheimo R., Palva E. T. 1993; A small diffusible signal molecule is responsible for the global control of virulence and exoenzyme production in the plant pathogen Erwinia carotovora. . EMBO J 12:2467–2476
     [Google Scholar]
  43. Richard P., Le Floch R., Chamoux C., Pannier M., Espaze E., Richet H. 1994; Pseudomonas aeruginosa outbreak in a burn unit: role of antimicrobials in the emergence of multiply resistant strains. J Infect Dis 170:377–383 [CrossRef]
     [Google Scholar]
  44. Salmond G. P., Bycroft B. W., Stewart G. S., Williams P. 1995; The bacterial ‘enigma’: cracking the code of cell–cell communication. Mol Microbiol 16:615–624 [CrossRef]
     [Google Scholar]
  45. Seed P. C., Passador L., Iglewski B. H. 1995; Activation of the Pseudomonas aeruginosa lasI gene by LasR and the Pseudomonas autoinducer PAI: an autoinduction regulatory hierarchy. J Bacteriol 177:654–659
     [Google Scholar]
  46. Shaw P., Ping G., Daly S., Cha C., Cronan J. J., Rinehart K., Farrand S. 1997; Detecting and characterizing N-acyl-homoserine lactone signal molecules by thin-layer chromatography. Proc Natl Acad Sci USA 94:6036–6041 [CrossRef]
     [Google Scholar]
  47. Song Z., Kharazmi A., Wu H., Faber V., Moser C., Johansen H. K., Rygaard J., Hoiby N. 1998; Effects of ginseng treatment on neutrophil chemiluminescence and immunoglobulin G subclasses in a rat model of chronic Pseudomonas aeruginosa pneumonia. . Clin Diagn Lab Immunol 5:882–887
     [Google Scholar]
  48. Swift S., Karlyshev A., Fish L., Durant E., Winson M., Chhabra S., Williams P., Macintyre S., Stewart G. 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]
  49. 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]
  50. 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]
  51. Van Delden C., Iglewski B. 1998; Cell-to-cell signaling and Pseudomonas aeruginosa infections. Emerg Infect Dis 4:551–560 [CrossRef]
     [Google Scholar]
  52. 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 U S A 92:9427–9431 [CrossRef]
     [Google Scholar]
  53. Yanisch-Perron C., Vieira J., Messing J. 1985; Improved M13 cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. . Gene 33:103–119 [CrossRef]
     [Google Scholar]
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Detection of N-acylhomoserine lactones in lung tissues of mice infected with Pseudomonas aeruginosa
Microbiology 146, 2481 (2000); https://doi.org/10.1099/00221287-146-10-2481
/content/journal/micro/10.1099/00221287-146-10-2481
/content/journal/micro/10.1099/00221287-146-10-2481
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