1887

Abstract

Polymorphonuclear neutrophilic leukocytes (PMNs) play a central role in innate immunity, where they dominate the response to infections, in particular in the cystic fibrosis lung. PMNs are phagocytic cells that produce a wide range of antimicrobial agents aimed at killing invading bacteria. However, the opportunistic pathogen can evade destruction by PMNs and thus cause persistent infections. In this study, we show that biofilm cells of recognize the presence of attracted PMNs and direct this information to their fellow bacteria through the quorum sensing (QS) signalling system. The bacteria respond to the presence of PMNs by upregulating synthesis of a number of QS-controlled virulence determinants including rhamnolipids, all of which are able to cripple and eliminate cells of the host defence. Our and analyses support a ‘launch a shield’ model by which rhamnolipids surround the biofilm bacteria and on contact eliminate incoming PMNs. Our data strengthen the view that cross-kingdom communication plays a key role in recognition and evasion of the host defence.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.031443-0
2009-11-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/11/3500.html?itemId=/content/journal/micro/10.1099/mic.0.031443-0&mimeType=html&fmt=ahah

References

  1. Aaron S. D., Ferris W., Ramotar K., Vandemheen K., Chan F., Saginur R. 2002; Single and combination antibiotic susceptibilities of planktonic, adherent, and biofilm-grown Pseudomonas aeruginosa isolates cultured from sputa of adults with cystic fibrosis. J Clin Microbiol 40:4172–4179
    [Google Scholar]
  2. Aendekerk S., Diggle S. P., Song Z., Høiby N., Cornelis P., Williams P., Camara M. 2005; The MexGHI-OpmD multidrug efflux pump controls growth, antibiotic susceptibility and virulence in Pseudomonas aeruginosa via 4-quinolone-dependent cell-to-cell communication. Microbiology 151:1113–1125
    [Google Scholar]
  3. Allen L., Dockrell D. H., Pattery T., Lee D. G., Cornelis P., Hellewell P. G., Whyte M. K. 2005; Pyocyanin production by Pseudomonas aeruginosa induces neutrophil apoptosis and impairs neutrophil-mediated host defenses in vivo. J Immunol 174:3643–3649
    [Google Scholar]
  4. Bjarnsholt T., Jensen P. Ø., Burmolle M., Hentzer M., Haagensen J. A., Hougen H. P., Calum H., Madsen K. G., Moser C. other authors 2005; Pseudomonas aeruginosa tolerance to tobramycin, hydrogen peroxide and polymorphonuclear leukocytes is quorum-sensing dependent. Microbiology 151:373–383
    [Google Scholar]
  5. Bjarnsholt T., Kirketerp-Moller K., Jensen P. Ø., Madsen K. G., Phipps R., Krogfelt K., Høiby N., Givskov M. 2008; Why chronic wounds will not heal: a novel hypothesis. Wound Repair Regen 16:2–10
    [Google Scholar]
  6. Bortolussi R., Vandenbroucke-Grauls C. M., van Asbeck B. S., Verhoef J. 1987; Relationship of bacterial growth phase to killing of Listeria monocytogenes by oxidative agents generated by neutrophils and enzyme systems. Infect Immun 55:3197–3203
    [Google Scholar]
  7. 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]
  8. Cabot P. J., Carter L., Schafer M., Stein C. 2001; Methionine-enkephalin-and Dynorphin A-release from immune cells and control of inflammatory pain. Pain 93:207–212
    [Google Scholar]
  9. Chadzinska M., Starowicz K., Scislowska-Czarnecka A., Bilecki W., Pierzchala-Koziec K., Przewlocki R., Przewlocka B., Plytycz B. 2005; Morphine-induced changes in the activity of proopiomelanocortin and prodynorphin systems in zymosan-induced peritonitis in mice. Immunol Lett 101:185–192
    [Google Scholar]
  10. Chang W., Small D. A., Toghrol F., Bentley W. E. 2005; Microarray analysis of Pseudomonas aeruginosa reveals induction of pyocin genes in response to hydrogen peroxide. BMC Genomics 6:115
    [Google Scholar]
  11. Christensen L. D., Moser C., Jensen P. Ø., Rasmussen T. B., Christophersen L., Kjelleberg S., Kumar N., Høiby N., Givskov M., Bjarnsholt T. 2007; Impact of Pseudomonas aeruginosa quorum sensing on biofilm persistence in an in vivo intraperitoneal foreign-body infection model. Microbiology 153:2312–2320
    [Google Scholar]
  12. Clark D. J., Maaløe O. 1967; DNA replication and division cycle in Escherichia coli . J Mol Biol 23:99–112
    [Google Scholar]
  13. Diggle S. P., Winzer K., Chhabra S. R., Worrall K. E., Camara M., Williams P. 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
    [Google Scholar]
  14. Donlan R. M., Costerton J. W. 2002; Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15:167–193
    [Google Scholar]
  15. 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]
  16. Hentzer M., Eberl L., Nielsen J., Givskov M. 2003; Quorum sensing: a novel target for the treatment of biofilm infections. BioDrugs 17:241–250
    [Google Scholar]
  17. Hentzer M., Eberl L., Givskov M. 2005; Transcriptome analysis of Pseudomonas aeruginosa biofilm development: anaerobic respiration and iron limitation. Biofilms 2:37–61
    [Google Scholar]
  18. 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]
  19. James G. A., Swogger E., Wolcott R., Pulcini E., Secor P., Sestrich J., Costerton J. W., Stewart P. S. 2008; Biofilms in chronic wounds. Wound Repair Regen 16:37–44
    [Google Scholar]
  20. Jensen P. Ø., Bjarnsholt T., Phipps R., Rasmussen T. B., Calum H., Christoffersen 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
    [Google Scholar]
  21. Jesaitis A. J., Franklin M. J., Berglund D., Sasaki M., Lord C. I., Bleazard J. B., Duffy J. E., Beyenal H., Lewandowski Z. 2003; Compromised host defense on Pseudomonas aeruginosa biofilms: characterization of neutrophil and biofilm interactions. J Immunol 171:4329–4339
    [Google Scholar]
  22. Kharazmi A. 1991; Mechanisms involved in the evasion of the host defence by Pseudomonas aeruginosa . Immunol Lett 30:201–205
    [Google Scholar]
  23. Kharazmi A., Doring G., Høiby N., Valerius N. H. 1984a; Interaction of Pseudomonas aeruginosa alkaline protease and elastase with human polymorphonuclear leukocytes in vitro . Infect Immun 43:161–165
    [Google Scholar]
  24. Kharazmi A., Høiby N., Doring G., Valerius N. H. 1984b; Pseudomonas aeruginosa exoproteases inhibit human neutrophil chemiluminescence. Infect Immun 44:587–591
    [Google Scholar]
  25. Kownatzki R., Tummler B., Doring G. 1987; Rhamnolipid of Pseudomonas aeruginosa in sputum of cystic fibrosis patients. Lancet 1:1026–1027
    [Google Scholar]
  26. Mah T. F., Pitts B., Pellock B., Walker G. C., Stewart P. S., O'Toole G. A. 2003; A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance. Nature 426:306–310
    [Google Scholar]
  27. Morici L. A., Carterson A. J., Wagner V. E., Frisk A., Schurr J. R., Höner zu Bentrup K., Hassett D. J., Iglewski B. H., Sauer K., Schurr M. J. 2007; Pseudomonas aeruginosa AlgR represses the Rhl quorum-sensing system in a biofilm-specific manner. J Bacteriol 189:7752–7764
    [Google Scholar]
  28. Pamp S. J., Tolker-Nielsen T. 2007; Multiple roles of biosurfactants in structural biofilm development by Pseudomonas aeruginosa . J Bacteriol 189:2531–2539
    [Google Scholar]
  29. 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
    [Google Scholar]
  30. Pfaffl M. W. 2001; A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45
    [Google Scholar]
  31. Przewlocki R., Hassan A. H., Lason W., Epplen C., Herz A., Stein C. 1992; Gene expression and localization of opioid peptides in immune cells of inflamed tissue: functional role in antinociception. Neuroscience 48:491–500
    [Google Scholar]
  32. Rasmussen T. B., Skindersø M. E., Bjarnsholt T., Phipps R. K., Christensen K. B., Jensen P. O., Andersen J. B., Koch B., Larsen T. O. other authors 2005; Identity and effects of quorum-sensing inhibitors produced by Penicillium species. Microbiology 151:1325–1340
    [Google Scholar]
  33. Savli H., Karadenizli A., Kolayli F., Gundes S., Ozbek U., Vahaboglu H. 2003; Expression stability of six housekeeping genes: a proposal for resistance gene quantification studies of Pseudomonas aeruginosa by real-time quantitative RT-PCR. J Med Microbiol 52:403–408
    [Google Scholar]
  34. Saye D. E. 2007; Recurring and antimicrobial-resistant infections: considering the potential role of biofilms in clinical practice. Ostomy Wound Manage 53:46–48 50:52
    [Google Scholar]
  35. Skindersoe M. E., Zeuthen L. H., Brix S., Fink L. N., Lazenby J., Whittall C., Williams P., Diggle S. P., Froekiaer H. other authors 2009; Pseudomonas aeruginosa quorum-sensing signal molecules interfere with dendritic cell-induced T-cell proliferation. FEMS Immunol Med Microbiol 55:335–345
    [Google Scholar]
  36. Small D. A., Chang W., Toghrol F., Bentley W. E. 2007; Comparative global transcription analysis of sodium hypochlorite, peracetic acid, and hydrogen peroxide on Pseudomonas aeruginosa . Appl Microbiol Biotechnol 76:1093–1105
    [Google Scholar]
  37. Sonawane A., Jyot J., Ramphal R. 2006; Pseudomonas aeruginosa LecB is involved in pilus biogenesis and protease IV activity but not in adhesion to respiratory mucins. Infect Immun 74:7035–7039
    [Google Scholar]
  38. Stender H. 2003; PNA FISH: an intelligent stain for rapid diagnosis of infectious diseases. Expert Rev Mol Diagn 3:649–655
    [Google Scholar]
  39. Stewart P. S., Costerton J. W. 2001; Antibiotic resistance of bacteria in biofilms. Lancet 358:135–138
    [Google Scholar]
  40. Wade D. S., Calfee M. W., Rocha E. R., Ling E. A., Engstrom E., Coleman J. P., Pesci E. C. 2005; Regulation of Pseudomonas quinolone signal synthesis in Pseudomonas aeruginosa . J Bacteriol 187:4372–4380
    [Google Scholar]
  41. Weyermann J., Lochmann D., Zimmer A. 2005; A practical note on the use of cytotoxicity assays. Int J Pharm 288:369–376
    [Google Scholar]
  42. Wu H., Song Z., Hentzer M., Andersen J. B., Heydorn A., Mathee K., Moser C., Eberl L., Molin S. other authors 2000; Detection of N-acylhomoserine lactones in lung tissues of mice infected with Pseudomonas aeruginosa . Microbiology 146:2481–2493
    [Google Scholar]
  43. Yang L., Haagensen J. A., Jelsbak L., Johansen H. K., Sternberg C., Høiby N., Molin S. 2008; In situ growth rates and biofilm development of Pseudomonas aeruginosa populations in chronic lung infections. J Bacteriol 190:2767–2776
    [Google Scholar]
  44. Zaborina O., Lepine F., Xiao G., Valuckaite V., Chen Y., Li T., Ciancio M., Zaborin A., Petrof E. O. other authors 2007; Dynorphin activates quorum sensing quinolone signaling in Pseudomonas aeruginosa . PLoS Pathog 3:e35
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.031443-0
Loading
/content/journal/micro/10.1099/mic.0.031443-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
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