1887

Abstract

is an opportunistic human pathogen that causes chronic biofilm-based infections in host organisms. employs quorum sensing (QS) to control expression of its virulence, and to establish and maintain chronic infections. Under such conditions, the biofilm mode of growth contributes significantly to tolerance to the action of the innate and adaptive defence system and numerous antibiotics. In the present study, an foreign-body infection model was established in the peritoneal cavity of mice. Experimental data showed that QS-deficient are cleared more rapidly from silicone implants as compared to their wild-type counterparts. Concurrently, treatment with the QS inhibitor furanone C-30 of mice harbouring implants colonized with the wild-type resulted in a significantly faster clearing of the implants as compared to the placebo-treated group. These results were obtained with both an inbred (BALB/c) and an outbred (NMRI) mouse strain. The present results support a model by which functional QS systems play a pivotal role in the ability of bacteria to resist clearing by the innate immune system and strongly suggest that the efficiency of the mouse innate defence against biofilm-forming is improved when the bacteria are treated with QS drugs that induce QS deficiency.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2007/006122-0
2007-07-01
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/7/2312.html?itemId=/content/journal/micro/10.1099/mic.0.2007/006122-0&mimeType=html&fmt=ahah

References

  1. Allesen-Holm M., Barken K. B., Yang L., Klausen M., Webb J. S., Kjelleberg S., Molin S., Givskov M., Tolker-Nielsen T. 2006; A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms. Mol Microbiol 59:1114–1128 [CrossRef]
    [Google Scholar]
  2. Bjarnsholt T., Jensen P. O., Burmolle M., Hentzer M., Haagensen J. A., Hougen H. P., Calum H., Madsen K. G., Moser C. other authors 2005a; Pseudomonas aeruginosa tolerance to tobramycin, hydrogen peroxide and polymorphonuclear leukocytes is quorum-sensing dependent. Microbiology 151:373–383 [CrossRef]
    [Google Scholar]
  3. Bjarnsholt T., Jensen P. O., Rasmussen T. B., Christophersen L., Calum H., Hentzer M., Hougen H. P., Rygaard J., Moser C. other authors 2005b; Garlic blocks quorum sensing and promotes rapid clearing of pulmonary Pseudomonas aeruginosa infections. Microbiology 151:3873–3880 [CrossRef]
    [Google Scholar]
  4. Braxton E. E. Jr, Ehrlich G. D., Hall-Stoodley L., Stoodley P., Veeh R., Fux C., Hu F. Z., Quigley M., Post J. C. 2005; Role of biofilms in neurosurgical device-related infections. Neurosurg Rev 28:249–255 [CrossRef]
    [Google Scholar]
  5. Buret A., Ward K. H., Olson M. E., Costerton J. W. 1991; An in vivo model to study the pathobiology of infectious biofilms on biomaterial surfaces. J Biomed Mater Res 25:865–874 [CrossRef]
    [Google Scholar]
  6. Cherney D. L., Amstutz H. C. 1983; Total hip replacement in the previously septic hip. J Bone Joint Surg Am 65:1256–1265
    [Google Scholar]
  7. Clegg C. D., Anderson J. M., Lappin-Scott H. M., van Elsas J. D. 1996; Survival of parental and genetically modified derivatives of a soil isolated Pseudomonas fluorescens under nutrient-limiting conditions. J Appl Bacteriol 81:19–26 [CrossRef]
    [Google Scholar]
  8. Costerton J. W., Stewart P. S., Greenberg E. P. 1999; Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1322 [CrossRef]
    [Google Scholar]
  9. Davies D. G., Parsek M. R., Pearson J. P., Iglewski B. H., Costerton J. W., Greenberg E. P. 1998; The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280:295–298 [CrossRef]
    [Google Scholar]
  10. Diggle S. P., Winzer K., Chhabra S. R., Worrall K. E., Williams P., Cámara M. 2003; The Pseudomonas aeruginosa quinolone signal molecule overcomes the cell density-dependency of the quorum sensing hierarchy, regulates rhl -dependent genes at the onset of stationary phase and can be produced in the absence of LasR. Mol Microbiol 50:29–43 [CrossRef]
    [Google Scholar]
  11. Emerson R. J., Camesano T. A. 2004; Nanoscale investigation of pathogenic microbial adhesion to a biomaterial. Appl Environ Microbiol 70:6012–6022 [CrossRef]
    [Google Scholar]
  12. Fuqua W. C., Winans S. C., Greenberg E. P. 1994; Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176:269–275
    [Google Scholar]
  13. Givskov M., Eberl L., Moller S., Poulsen L. K., Molin S. 1994; Responses to nutrient starvation in Pseudomonas putida KT2442: analysis of general cross-protection, cell shape, and macromolecular content. J Bacteriol 176:7–14
    [Google Scholar]
  14. Goldsby R. A., Osborne B. A., Kindt T. J., Kuby J. 2003 Immunology , 5th edn. New York: W.H. Freeman;
    [Google Scholar]
  15. Gristina A. G. 1987; Biomaterial-centered infection: microbial adhesion versus tissue integration. Science 237:1588–1595 [CrossRef]
    [Google Scholar]
  16. Hassett D. J., Ma J. F., Elkins J. G., McDermoot T. R., Ochsner U. A., West S. E., Huang C. T., Fredericks J., Burnett S. other authors 1999; Quorum sensing in Pseudomonas aeruginosa controls expression of catalase and superoxide dismutase genes and mediates biofilm susceptibility to hydrogen peroxide. Mol Microbiol 34:1082–1093 [CrossRef]
    [Google Scholar]
  17. Hentzer M., Riedel K., Rasmussen T. B., Heydorn A., Andersen J. B., Parsek M. R., Rice S. A., Eberl L., Molin S. other authors 2002; Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiology 148:87–102
    [Google Scholar]
  18. Hentzer M., Wu H., Andersen J. B., Riedel K., Rasmussen T. B., Bagge N., Kumar N., Schembri M. A., Song Z. other authors 2003; Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J 22:3803–3815 [CrossRef]
    [Google Scholar]
  19. Hentzer M., Eberl L., Givskov M. 2005; Transcriptome analysis of Pseudomonas aeruginosa biofilm development: anaerobic respiration and iron limitation. Biofilms 2:37–61 [CrossRef]
    [Google Scholar]
  20. Høiby N. 1974; Epidemiological investigations of the respiratory tract bacteriology in patients with cystic fibrosis. Acta Pathol Microbiol Scand [B] Microbiol Immunol 82:541–550
    [Google Scholar]
  21. Høiby N., Krogh Johansen H., Moser C., Song Z., Ciofu O., Kharazmi A. 2001; Pseudomonas aeruginosa and the in vitro and in vivo biofilm mode of growth. Microbes Infect 3:23–35 [CrossRef]
    [Google Scholar]
  22. Hooi D. S. W., Bycroft B. W., Chhabra S. R., Williams P., Pritchard D. I. 2004; Differential immune modulatory activity of Pseudomonas aeruginosa quorum-sensing signal molecules. Infect Immun 72:6463–6470 [CrossRef]
    [Google Scholar]
  23. Jensen P. Ø., Bjarnsholt T., Phipps R., Rasmussen T. B., Calum H., Christophersen L., Moser C., Williams P., Pressler T. other authors 2007; Rapid necrotic killing of polymorphonuclear leukocytes is caused by quorum-sensing-controlled production of rhamnolipid by Pseudomonas aeruginosa. Microbiology 153:1329–1338 [CrossRef]
    [Google Scholar]
  24. Klausen M., Heydorn A., Ragas P., Lambertsen L., Aaes-Jorgensen A., Molin S., Tolker-Nielsen T. 2003; Biofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants. Mol Microbiol 48:1511–1524 [CrossRef]
    [Google Scholar]
  25. Koch B., Jensen L. E., Nybroe O. 2001; A panel of Tn 7 -based vectors for insertion of the gfp marker gene or for delivery of cloned DNA into Gram-negative bacteria at a neutral chromosomal site. J Microbiol Methods 45:187–195 [CrossRef]
    [Google Scholar]
  26. Lappin-Scott H. M., Cusack F., MacLeod A., Costerton J. W. 1988; Starvation and nutrient resuscitation of Klebsiella pneumoniae isolated from oil well waters. J Appl Bacteriol 64:541–549 [CrossRef]
    [Google Scholar]
  27. 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]
  28. Matz C., Bergfeld T., Rice S. A., Kjelleberg S. 2004; Microcolonies, quorum sensing and cytotoxicity determine the survival of Pseudomonas aeruginosa biofilms exposed to protozoan grazing. Environ Microbiol 6:218–226 [CrossRef]
    [Google Scholar]
  29. Middleton B., Rodgers H. C., Camara M., Knox A. J., Williams P., Hardman A. 2002; Direct detection of N -acylhomoserine lactones in cystic fibrosis sputum. FEMS Microbiol Lett 207:1–7 [CrossRef]
    [Google Scholar]
  30. Neut D., Hendriks J. G., Busscher H. J., van Horn J. R., van der Mei H. C. 2005; Pseudomonas aeruginosa biofilm formation and slime excretion on antibiotic-loaded bone cement. Acta Orthop 76:109–114 [CrossRef]
    [Google Scholar]
  31. 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]
  32. 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]
  33. 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 U S A 91:197–201 [CrossRef]
    [Google Scholar]
  34. 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]
  35. 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]
  36. Pesci E. C., Pearson J. P., Seed P. C., Iglewski B. H. 1997; Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. J Bacteriol 179:3127–3132
    [Google Scholar]
  37. Rasmussen T. B., Bjarnsholt T., Skindersoe M. E., Hentzer M., Kristoffersen P., Kote M., Nielsen J., Eberl L., Givskov M. 2005a; Screening for quorum-sensing inhibitors (QSI) by use of a novel genetic system, the QSI selector. J Bacteriol 187:1799–1814 [CrossRef]
    [Google Scholar]
  38. Rasmussen T. B., Skindersoe M. E., Bjarnsholt T., Phipps R. K., Christensen K. B., Jensen P. O., Andersen J. B., Koch B., Larsen T. O. other authors 2005b; Identity and effects of quorum-sensing inhibitors produced by Penicillium species. Microbiology 151:1325–1340 [CrossRef]
    [Google Scholar]
  39. Saiman L. 2004; The use of macrolide antibiotics in patients with cystic fibrosis. Curr Opin Pulm Med 10:515–523 [CrossRef]
    [Google Scholar]
  40. Singh P. K., Parsek M. R., Greenberg E. P., Welsh M. J. 2002; A component of innate immunity prevents bacterial biofilm development. Nature 417:552–555 [CrossRef]
    [Google Scholar]
  41. Southern K. W., Barker P. M. 2004; Azithromycin for cystic fibrosis. Eur Respir J 24:834–838 [CrossRef]
    [Google Scholar]
  42. Tateda K., Comte R., Pechere J. C., Kohler T., Yamaguchi K., van Delden C. 2001; Azithromycin inhibits quorum sensing in Pseudomonas aeruginosa. Antimicrob Agents Chemother 45:1930–1933 [CrossRef]
    [Google Scholar]
  43. Tateda K., Ishii Y., Horikawa M., Matsumoto T., Miyairi S., Pechere J. C., Standiford T. J., Ishiguro M., Yamaguchi K. 2003; The Pseudomonas aeruginosa autoinducer N -3-oxododecanoyl homoserine lactone accelerates apoptosis in macrophages and neutrophils. Infect Immun 71:5785–5793 [CrossRef]
    [Google Scholar]
  44. Telford G., Wheeler D., Williams P., Tomkins P. T., Appleby P., Sewell H., Stewart G. S., 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]
  45. Van Delden C., Iglewski B. H. 1998; Cell-to-cell signaling and Pseudomonas aeruginosa infections. Emerg Infect Dis 4:551–560 [CrossRef]
    [Google Scholar]
  46. Verkerke G. J., Schraffordt Koops H., Veth R. P., Postma L., Grootenboer H. J., van Horn J. R. 1997; First clinical experience with a noninvasively extendable endoprosthesis: a limb-saving procedure in children suffering from a malignant bone tumor. Artif Organs 21:413–417
    [Google Scholar]
  47. Wu H., Song Z., Hentzer M., Andersen J. B., Molin S., Givskov M., Hoiby N. 2004; Synthetic furanones inhibit quorum-sensing and enhance bacterial clearance in Pseudomonas aeruginosa lung infection in mice. J Antimicrob Chemother 53:1054–1061 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2007/006122-0
Loading
/content/journal/micro/10.1099/mic.0.2007/006122-0
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