Biofilm formation by Pseudomonas aeruginosa: Role of the C4-HSL cell-to-cell signal and inhibition by azithromycin

Journal of Antimicrobial Chemotherapy

Volumn 52, Issue 4, 2003, Pages 598-604

  Favre Bonté, Sabine ^a,b   Köhler, Thilo ^a   Van Delden, Christian ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b UNIVERSITÉ LYON 1   (France)

Author keywords

3 oxo C12 HSL; Autoinducers; Homoserine lactones; Quorum sensing

Indexed keywords

AZITHROMYCIN; CRYSTAL VIOLET; GENTAMICIN; HOMOSERINE; LACTONE DERIVATIVE; MERCURY CHLORIDE; POLYSACCHARIDE; TETRACYCLINE;

ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIUM MUTANT; BIOFILM; CELL INTERACTION; CONTROLLED STUDY; NONHUMAN; PROTEIN FUNCTION; PROTEIN SECRETION; PSEUDOMONAS AERUGINOSA; SIGNAL TRANSDUCTION; WILD TYPE;

4-BUTYROLACTONE; AZITHROMYCIN; BIOFILMS; CELL COMMUNICATION; HUMANS; PSEUDOMONAS AERUGINOSA; SIGNAL TRANSDUCTION;

EID: 0141963088     PISSN: 03057453     EISSN: None     Source Type: Journal    
DOI: 10.1093/jac/dkg397     Document Type: Article

References (42)

1. Costerton, J. W., Stewart, P. S. & Greenberg, E. P. (1999). Bacterial biofilms: a common cause of persistent infections. Science 284, 1318-22.
2. Van Delden, C. & Iglewski, B. H. (1998). Cell-to-cell signaling and Pseudomonas aeruginosa infections. Emerging Infectious Diseases 4, 551-60.
3. Geisenberger, O., Givskov, M., Riedel, K. et al. (2000). Production of N-acyl-L-homoserine lactones by P. aeruginosa isolates from chronic lung infections associated with cystic fibrosis. FEMS Microbiology Letters 184, 273-8.
4. Singh, P. K., Schaefer, A. L., Parsek, M. R. et al. (2000). Quorumsensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 407, 762-4.
5. Wu, H., Song, Z., Hentzer, M. at al. (2000). Detection of N-acylhomoserine lactones in lung tissues of mice infected with Pseudomonas aeruginosa. Microbiology 146, 2481-93.
6. Stickler, D. J., Morris, N. S., McLean, R. J. et al. (1998). Biofilms on indwelling urethral catheters produce quorum-sensing signal molecules in situ and in vitro. Applied and Environmental Microbiology 64, 3486-90.
7. Middleton, B., Rodgers, H. C., Camara, M. et al. (2002). Direct detection of N-acylhomoserine lactones in cystic fibrosis sputum. FEMS Microbiology Letters 207, 1-7.
8. Erickson, D. L., Endersby, R., Kirkham, A. et al. (2002). Pseudomonas aeruginosa quorum-sensing systems may control virulence factor expression in the lungs of patients with cystic fibrosis. Infection and Immunity 70, 1783-90.
9. Davies, D. G., Parsek, M. R., Pearson, J. P. et al. (1998). The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280, 295-8.
10. De Kievit, T. R., Gillis, R., Marx, S. et al. (2001). Quorum-sensing genes in Pseudomonas aeruginosa biofilms: their role and expression patterns. Applied and Environmental Microbiology 67, 1865-73.
11. Favre-Bonte, S., Pache, J. C., Robert, J. et al. (2002). Detection of Pseudomonas aeruginosa cell-to-cell signals in lung tissue of cystic fibrosis patients. Microbial Pathogenesis 32, 143-7.
12. Yoon, S. S., Hennigan, R. F., Hilliard, G. M. et al. (2002). Pseudomonas aeruginosa anaerobic respiration in biofilms: relationships to cystic fibrosis pathogenesis. Developmental Cell 3, 593-603.
13. Davey, M. E., Caiazza, N. C. & O'Toole, G. A. (2003). Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PAO1. Journal of Bacteriology 185, 1027-36.
14. Kohler, T., Van Delden, C., Curly, L. K. et al. (2001). Overexpression of the MexEF-OprN multidrug efflux system affects cell-to-cell signaling in Pseudomonas aeruginosa. Journal of Bacteriology 183, 5213-22.
15. Tateda, K., Comte, R., Pechere, J. C. et al. (2001). Azithromycin inhibits quorum sensing in Pseudomonas aeruginosa. Antimicrobial Agents and Chemotherapy 45, 1930-3.
16. Terry, J. M., Pina, S. E. & Mattingly, S. J. (1992). Role of energy metabolism in conversion of nonmucoid Pseudomonas aeruginosa to the mucoid phenotype. Infection and Immunity 60, 1329-35.
17. Kohler, T., Michea-Hamzehpour, M., Henze, U. et al. (1997). Characterization of MexE-MexF-OprN, a positively regulated multidrug efflux system of Pseudomonas aeruginosa. Molecular Microbiology 23, 345-54.
18. Kohler, T., Curty, L. K., Barja, F. et al. (2000). Swarming of Pseudomonas aeruginosa is dependent on cell-to-cell signaling and requires flagella and pili. Journal of Bacteriology 182, 5990-6.
19. Van Delden, C., Comte, R. & Bally, A. M. (2001). Stringent response activates quorum sensing and modulates cell density-dependent gene expression in Pseudomonas aeruginosa. Journal of Bacteriology 183, 5376-84.
20. Miller, J. H. (1972). Experiments in Molecular Genetics, pp. 352-355. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, USA.
21. Takeoka, K., Ichimiya, T., Yamasaki, T. et al. (1998). The in vitro effect of macrolides on the interaction of human polymorphonuclear leukocytes with Pseudomonas aeruginosa in biofilm. Chemotherapy 44, 190-7.
22. O'Toole, G. A. & Koller, R. (1998). Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Molecular Microbiology 30, 295-304.
23. Kintner, P. K. & Van Buren, J. P. (1982). Carbohydrate interference and its correction in pectin analysis using the m-hydroxydiphenyl method. Journal of Food Science 47, 756-64.
24. Shih, P. C. & Huang, C. T. (2002). Effects of quorum-sensing deficiency on Pseudomonas aeruginosa biofilm formation and antibiotic resistance. Journal of Antimicrobial Chemotherapy 49, 309-14.
25. Heydorn, A., Ersboll, B., Kato, J. et al. (2002). Statistical analysis of Pseudomonas aeruginosa biofilm development: impact of mutations in genes involved in twitching motility, cell-to-cell signaling, and stationary-phase sigma factor expression. Applied and Environmental Microbiology 68, 2008-17.
26. Latifi, A., Foglino, M., Tanaka, K. et al. (1996). A hierarchical quorum-sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhlR (VsmR) to expression of the stationary-phase sigma factor RpoS. Molecular Microbiology 21, 1137-46.
27. Beatson, S. A., Whitchurch, C. B., Semmler, A. B. T. et al. (2002). Quorum sensing is not required for twitching motility in Pseudomonas aeruginosa. Journal of Bacteriology 184, 3598-604.
28. Beatson, S. A., Whitchurch, C. B., Sargent, J. L. et al. (2002). Differential regulation of twitching motility and elastase production by Vfr in Pseudomonas aeruginosa. Journal of Bacteriology 184, 3605-13.
29. Sauer, K., Camper, A. K., Ehrlich, G. D. et al. (2002). Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. Journal of Bacteriology 184, 1140-54.
30. Join-Lambert, O. F., Michea-Hamzehpour, M., Kohler, T. et al. (2001). Differential selection of multidrug efflux mutants by trovafloxacin and ciprofloxacin in an experimental model of Pseudomonas aeruginosa acute pneumonia in rats. Antimicrobial Agents and Chemotherapy 45, 571-6.
31. Cosson, P., Zulianello, L., Join-Lambert, O. et al. (2002). Pseudomonas aeruginosa virulence analyzed in a Dictyostelium discoideum host system. Journal of Bacteriology 184, 3027-33.
32. Hassett, D. J., Cuppoletti, J., Trapnell, B. et al. (2002). Anaerobic metabolism and quorum sensing by Pseudomonas aeruginosa biofilms in chronically infected cystic fibrosis airways: rethinking antibiotic treatment strategies and drug targets. Advanced Drug Delivery Reviews 54, 1425-43.
33. Retsema, J., Girard, A., Schelkly, W. et al. (1987). Spectrum and mode of action of azithromycin (CP-62,993), a new 15-membered-ring macrolide with improved potency against gram-negative organisms. Antimicrobial Agents and Chemotherapy 31, 1939-47.
34. Kucers, A., Crowe, S. M., Grayson, M. L. et al. (1997). Azithromycin. In The Use of Antibiotics, pp. 653-663. Butterworth-Heinemann, Oxford, UK.
35. Vranes, J. (2000). Effect of subminimal inhibitory concentrations of azithromycin on adherence of Pseudomonas aeruginosa to polystyrene. Journal of Chemotherapy 12, 280-5.
36. Ichimiya, T., Takeoka, K., Hiramatsu, K. et al. (1996). The influence of azithromycin on the biofilm formation of Pseudomonas aeruginosa in vitro. Chemotherapy 42, 186-91.
37. Jaffe, A., Francis, J., Rosenthal, M. et al. (1998). Long-term azithromycin may improve lung function in children with cystic fibrosis. Lancet 351, 420.
38. Wolter, J., Seeney, S., Bell, S. et al. (2002). Effect of long term treatment with azithromycin on disease parameters in cystic fibrosis: a randomised trial. Thorax 57, 212-6.
39. Equi, A., Balfour-Lynn, I. M., Bush, A. et al. (2002). Long term azithromycin in children with cystic fibrosis: a randomised, placebo-controlled crossover trial. Lancet 360, 978-84.
40. Seed, P. C., Passador, L. & Iglewski, B. H. (1995). Activation of the Pseudomonas aeruginosa lasl gene by LasR and the Pseudomonas autoinducer PAI: an autoinduction regulatory hierarchy. Journal of Bacteriology 177, 654-9.
41. Pearson, J. P., Pesci, E. C. & Iglewski, B. H. (1997). Role of Pseudomonas aeruginosa las and rhl quorum-sensing systems in the control of elastase and rhamnolipid biosynthesis genes. Journal of Bacteriology 179, 5756-67.
42. 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. Journal of Bacteriology 177, 7155-63.