Quorum-sensing antagonistic activities of azithromycin in Pseudomonas aeruginosa PAO1: A global approach

Antimicrobial Agents and Chemotherapy

Volumn 50, Issue 5, 2006, Pages 1680-1688

  Nalca, Yusuf ^a   Jänsch, Lothar ^a   Bredenbruch, Florian ^a   Geffers, Robert ^a   Buer, Jan ^a   Häussler, Susanne ^a  

^a HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AZITHROMYCIN; MACROLIDE; VIRULENCE FACTOR;

ANTIBACTERIAL ACTIVITY; ANTIBIOTIC THERAPY; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BACTERIAL INFECTION; BACTERIAL VIRULENCE; BACTERIUM CULTURE; BIOFILM; CELL MOTILITY; CELL SECRETION; CONTROLLED STUDY; CYSTIC FIBROSIS; DRUG EFFECT; DRUG MECHANISM; GENETIC TRANSCRIPTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS AERUGINOSA PAO1; QUORUM SENSING; QUORUM SENSING ANTAGONISTIC ACTIVITY; TYPE III SECRETION SYSTEM;

ANTI-BACTERIAL AGENTS; AZITHROMYCIN; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; HYDROGEN PEROXIDE; MASS SPECTROMETRY; OXIDANTS; PEPTIDE MAPPING; PROTEIN ARRAY ANALYSIS; PROTEOME; PSEUDOMONAS AERUGINOSA; TRANSCRIPTION, GENETIC; VIRULENCE;

EID: 33646452555     PISSN: 00664804     EISSN: None     Source Type: Journal    
DOI: 10.1128/AAC.50.5.1680-1688.2006     Document Type: Article

References (56)

1. Arevalo-Ferro, C., M. Hentzer, G. Reil, A. Gorg, S. Kjelleberg, M. Givskov, K. Riedel, and L. Eberl. 2003. Identification of quorum-sensing regulated proteins in the opportunistic pathogen Pseudomonas aeruginosa by proteomics. Environ. Microbiol. 5:1350-1369.
2. Carr, R. R., and M. C. Nahata. 2004. Azithromycin for improving pulmonary function in cystic fibrosis. Ann. Pharmacother. 38:1520-1524.
3. Davies, D. G., M. R. Parsek, J. P. Pearson, B. H. Iglewski, J. W. Costerton, and E. P. Greenberg. 1998. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280:295-298.
4. Davies, J. C. 2002. Pseudomonas aeruginosa in cystic fibrosis: pathogenesis and persistence. Paediatr. Respir. Rev. 3:128-134.
5. Gibson, R. L., J. L. Burns, and B. W. Ramsey. 2003. Pathophysiology and management of pulmonary infections in cystic fibrosis. Am. J. Respir. Crit. Care Med. 168:918-951.
6. Gillis, R. J., and B. H. Iglewski. 2004. Azithromycin retards Pseudomonas aeruginosa biofilm formation. J. Clin. Microbiol. 42:5842-5845.
7. Hassett, D. J., J. F. Ma, J. G. Elkins, T. R. McDermott, U. A. Ochsner, S. E. West, C. T. Huang, J. Fredericks, S. Burnett, P. S. Stewart, G. McFeters, L. Passador, and B. H. Iglewski. 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.
8. Hentzer, M., H. Wu, J. B. Andersen, K. Riedel, T. B. Rasmussen, N. Bagge, N. Kumar, M. A. Schembri, Z. Song, P. Kristoffersen, M. Manefield, J. W. Costerton, S. Molin, L. Eberl, P. Steinberg, S. Kjelleberg, N. Hoiby, and M. Givskov. 2003. Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J. 22:3803-3815.
9. Hirakata, Y., M. Kaku, R. Mizukane, K. Ishida, N. Furuya, T. Matsumoto, K. Tateda, and K. Yamaguchi. 1992. Potential effects of erythromycin on host defense systems and virulence of Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 36:1922-1927.
10. Hogardt, M., M. Roeder, A. M. Schreff, L. Eberl, and J. Heesemann. 2004. Expression at Pseudomonas aeruginosa exoS is controlled by quorum sensing and RpoS. Microbiology 150:843-851.
11. Hoiby, N. 2002. New antimicrobials in the management of cystic fibrosis. J. Antimicrob. Chemother. 49:235-238.
12. Ichimiya, T., K. Takeoka, K. Hiramatsu, K. Hirai, T. Yamasaki, and M. Nasu. 1996. The influence of azithromycin on the biofilm formation of Pseudomonas aeruginosa in vitro. Chemotherapy 42:186-191.
13. Kadota, J., H. Mukae, H. Ishii, T. Nagata, H. Kaida, K. Tomono, and S. Kohno. 2003. Long-term efficacy and safety of clarithromycin treatment in patients with diffuse panbronchiolitis. Respir. Med. 97:844-850.
14. Kawamura-Sato, K., Y. Iinuma, T. Hasegawa, T. Horii, T. Yamashino, and M. Ohta. 2000. Effect of subinhibitory concentrations of macrolides on expression of flagellin in Pseudomonas aeruginosa and Proteus mirabilis. Antimicrob. Agents Chemother. 44:2869-2872.
15. Keicho, N., and S. Kudoh. 2002. Diffuse panbronchiolitis: role of macrolides in therapy. Am. J. Respir. Med. 1:119-131.
16. Kita, E., M. Sawaki, F. Nishikawa, K. Mikasa, Y. Yagyu, S. Takeuchi, K. Yasui, N. Narita, and S. Kashiba. 1990. Enhanced interleukin production after long-term administration of erythromycin stearate. Pharmacology 41:177-183.
17. Kita, E., M. Sawaki, D. Oku, A. Hamuro, K. Mikasa, M. Konishi, M. Emoto, S. Takeuchi, N. Narita, and S. Kashiba. 1991. Suppression of virulence factors of Pseudomonus aeruginosa by erythromycin. J. Antimicrob. Chemother. 27:273-284.
18. Kobayashi, K., and S. Tagawa. 2004. Activation of SoxR-dependent transcription in Pseudomonas aeruginosa. J. Biochem. (Tokyo) 136:607-615.
19. Kobayashi, T., K. Tateda, T. Matsumoto, S. Miyazaki, A. Watanabe, T. Nukiwa, and K. Yamaguchi. 2002. Macrolide-treated Pseudomonas aeruginosa induces paradoxical host responses in the lungs of mice and a high mortality rate. J. Antimicrob. Chemother. 50:59-66.
20. Koch, C., and N. Hoiby. 2000. Diagnosis and treatment of cystic fibrosis. Respiration 67:239-247.
21. Kudoh, S., A. Azuma, M. Yamamoto, T. Izumi, and M. Ando. 1998. Improvement of survival in patients with diffuse panbronchiolitis treated with low-dose erythromycin. Am. J. Respir. Crit. Care Med. 157:1829-1832.
22. Lamanda, A., A. Zahn, D. Roder, and H. Langen. 2004. Improved Ruthenium II tris (bathophenantroline disulfonate) staining and destaining protocol for a better signal-to-background ratio and improved baseline resolution. Proteomics 4:599-608.
23. Leichert, L. I., and U. Jakob. 2004. Protein thiol modifications visualized in vivo. PLoS Biol. 2:c333.
24. Lyczak, J. B., C. L. Cannon, and G. B. Pier. 2002. Lung infections associated with cystic fibrosis. Clin. Microbiol. Rev. 15:194-222.
25. Molinari, G., C. A. Guzman, A. Pesce, and G. C. Schito. 1993. Inhibition of Pseudomonas aeruginosa virulence factors by subinhibitory concentrations of azithromycin and other macrolide antibiotics. J. Antimicrob. Chemother. 31:681-688.
26. Molinari, G., P. Paglia, and G. C. Schito. 1992. Inhibition of motility of Pseudomonas aeruginosa and Proteus mirabilis by subinhibitory concentrations of azithromycin. Eur. J. Clin. Microbiol. Infect. Dis. 11:469-471.
27. Nagino, K., and H. Kobayashi. 1997. Influence of macrolides on mucoid alginate biosynthetic enzyme from Pseudomonas aeruginosa. Clin. Microbiol. Infect. 3:432-439.
28. Nicolau, D. P., M. A. Banevicius, C. H. Nightingale, and R. Quintiliani. 1999. Beneficial effect of adjunctive azithromycin in treatment of mucoid Pseudomonas aeruginosa pneumonia in the murine model. Antimicrob. Agents Chemother. 43:3033-3035.
29. Nouwens, A. S., S. A. Beatson, C. B. Whitchurch, B. J. Walsh, H. P. Schweizer, J. S. Mattick, and S. J. Cordwell. 2003. Proteome analysis of extracellular proteins regulated by the las and rhl quorum sensing systems in Pseudomonas aeruginosa PAO1. Microbiology 149:1311-1322.
30. Ordonez, C. L., M. Stulbarg, H. Grundland, J. T. Liu, and H. A. Boushey. 2001. Effect of clarithromycin on airway obstruction and inflammatory markers in induced sputum in cystic fibrosis: a pilot study. Pediatr. Pulmonol. 32:29-37.
31. O'Toole, G. A., and R. Kolter. 1998. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30:295-304.
32. Palma, M., D. DeLuca, S. Worgall, and L. E. Quadri. 2004. Transcriptome analysis of the response ot Pseudomonas aeruginosa to hydrogen peroxide. J. Bacteriol. 186:248-252.
33. Pechere, J. C. 2001. Azithromycin reduces the production of virulence factors in Pseudomonas aeruginosa by inhibiting quorum sensing. Jpn. J. Antibiot. 54(Suppl. C):87-89.
34. Pirzada, O. M., J. McGaw, C. J. Taylor, and M. L. Everard. 2003. Improved lung function and body mass index associated with long-term use of macrolide antibiotics. J. Cyst. Fibros. 2:69-71.
35. Poletti, V., M. Chilosi, G. Casoni, and T. V. Colby. 2004. Diffuse panbronchiolitis. Sarcoidosis Vasc. Diffuse Lung Dis. 21:94-104.
36. Rajan, S., and L. Saiman. 2002. Pulmonary infections in patients with cystic fibrosis. Semin. Respir. Infect. 17:47-56.
37. Ratjen, F. 2001. Changes in strategies for optimal antibacterial therapy in cystic fibrosis. Int. J. Antimicrob. Agents 17:93-96.
38. Saiman, L. 2004. The use of macrolide antibiotics in patients with cystic fibrosis. Curr. Opin. Pulmon. Med. 10:515-523.
39. Saiman, L., B. C. Marshall, N. Mayer-Hamblett, J. L. Burns, A. L. Quittner, D. A. Cibene, S. Coquillette, A. Y. Fieberg, F. J. Accurso, and P. W. Campbell III. 2003. Azithromycin in patients with cystic fibrosis chronically infected with Pseudomonas aeruginosa: a randomized controlled trial. JAMA 290:1749-1756.
40. Sawaki, M., R. Mikami, K. Mikasa, M. Kunimatsu, S. Ito, and N. Narita. 1986. The long term chemotherapy with erythromycin in chronic lower respiratory tract infections-first report: comparison with amoxicillin. Kansenshogaku Zasshi 60:37-44.
41. Sawaki, M., R. Mikami, K. Mikasa, M. Kunimatsu, S. Ito, and N. Narita. 1986. The long term chemotherapy with erythromycin in chronic lower respiratory tract infections-second report: including cases with Pseudomonas infections. Kansenshogaku Zasshi 60:45-50.
42. Schuster, M., C. P. Lostroh, T. Ogi, and E. P. Greenberg. 2003. Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J. Bacteriol. 185:2066-2079.
43. Shaver, C. M., and A. R. Hauser. 2004. Relative contributions of Pseudomonas aeruginosa ExoU, ExoS, and ExoT to virulence in the lung. Infect. Immun. 72:6969-6977.
44. Southern, K. W., P. M. Barker, and A. Solis. 2004. Macrolide antibiotics for cystic fibrosis. Cochrane Database Syst. Rev. CD002203. [Online.]
45. Tateda, K., R. Comte, J. C. Pechere, T. Kohler, K. Yamaguchi, and C. Van Delden. 2001. Azithromycin inhibits quorum sensing in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 45:1930-1933.
46. Tateda, K., Y. Ishii, T. Matsumoto, N, Furuya, M. Nagashima, T. Matsunaga, A. Ohno, S. Miyazaki, and K. Yamaguchi. 1996. Direct evidence for anti-pseudomonal activity of macrolides: exposure-dependent bactericidal activity and inhibition of protein synthesis by erythromycin, clarithromycin, and azithromycin. Antimicrob. Agents Chemother. 40:2271-2275.
47. Vasil, M. L., and U. A. Ochsner. 1999. The response of Pseudomonas aeruginosa to iron: genetics, biochemistry and virulence. Mol. Microbiol. 34:399-413.
48. Wagner, T., G. Soong, S. Sokol, L. Saiman, and A. Prince. 2005. Effects of azithromycin on clinical isolates of Pseudomonas aeruginosa from cystic fibrosis patients. Chest 128:912-919.
49. Wagner, V. E., D. Bushnell, L. Passador, A. I. Brooks, and B. H. Iglewski. 2003. Microarray analysis of Pseudomonas aeruginosa quorum-sensing regulons: effects of growth phase and environment. J. Bacteriol. 185:2080-2095.
50. Wagner, V. E., R. J. Gillis, and B. H. Iglewski, 2004. Transcriptome analysis of quorum-sensing regulation and virulence factor expression in Pseudomonas aeruginosa. Vaccine 22(Suppl. 1):S15-S20.
51. Wehmhoner, D., S. Haussler, B. Tummler, L. Jansch, F. Bredenbruch, J. Wehland, and I. Steinmetz. 2003. Inter- and intraclonal diversity of the Pseudomonas aeruginosa proteome manifests within the secretome. J. Bacteriol. 185:5807-5814.
52. Wolter, J., S. Seeney, S. Bell, S. Bowler, P. Masel, and J. McCormack. 2002. Effect of long term treatment with azithromycin on disease parameters in cystic fibrosis: a randomised trial. Thorax 57:212-216.
53. Welter, J. M., S. L. Seeney, and J. G. McCormack. 2002. Macrolides in cystic fibrosis: is there a role? Am. J. Respir. Med. 1:235-241.
54. Wozniak, D. J., and R. Keyser. 2004. Effects of subinhibitory concentrations of macrolide antibiotics on Pseudomonas aeruginosa. Chest 125:62S-69S.
55. Wu, H., Z. Song, M. Hentzer, J. B. Andersen, S. Molin, M. Givskov, and N. Hoiby. 2004. Synthetic furanones inhibit quorum-sensing and enhance bacterial clearance in Pseudomonas aeruginosa lung infection in mice. J. Antimicrob. Chemother. 53:1054-1061.
56. Yamagishi, M., H. Matsushima, A. Wada, M. Sakagami, N. Fujita, and A. Ishihama. 1993. Regulation of the Escherichia coli rmf gene encoding the ribosome modulation factor: growth phase- and growth rate-dependent control. EMBO J. 12:625-630.