Subinhibitory concentrations of the cationic antimicrobial peptide colistin induce the pseudomonas quinolone signal in Pseudomonas aeruginosa

Microbiology

Volumn 155, Issue 9, 2009, Pages 2826-2837

  Cummins, Joanne ^a   Reen, F Jerry ^a   Baysse, Christine ^a,b   Mooij, Marlies J ^a   O'Gara, Fergal ^a  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITÉ DE RENNES 1   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; BACTERIAL PROTEIN; CARBENICILLIN; COLISTIN; GENTAMICIN; KANAMYCIN; LIPOPOLYSACCHARIDE; PHENAZINE; PROTEIN PQSB; PROTEIN PQSE; PROTEIN PQSH; PSEUDOMONAS QUINOLONE SIGNAL BIOSYNTHESIS PROTEIN; QUINOLONE; TETRACYCLINE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL VIRULENCE; CONCENTRATION PROCESS; FUNCTIONAL GENOMICS; GENE EXPRESSION; GENE INDUCTION; MINIMUM INHIBITORY CONCENTRATION; NUCLEOTIDE SEQUENCE; OSMOTIC STRESS; PRIORITY JOURNAL; PROTEIN MODIFICATION; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; TRANSCRIPTOMICS; UPREGULATION;

ANTI-BACTERIAL AGENTS; COLISTIN; DNA, BACTERIAL; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; HUMANS; HYDROXYQUINOLINES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; PYOCYANINE; QUINOLONES; QUORUM SENSING; TRANSCRIPTIONAL ACTIVATION;

BACTERIA (MICROORGANISMS); PSEUDOMONAS; PSEUDOMONAS AERUGINOSA;

EID: 69949115529     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.025643-0     Document Type: Article

References (68)

1. Ainsworth, G. C., Brown, A. M. & Brownlee, G. (1947). Aerosporin. An antibiotic produced by Bacillus aerosporus. Nature 160, 263.
2. Beringer, P. (2001). The clinical use of colistin in patients with cystic fibrosis. Curr Opin Pulm Med 7, 434-440.
3. Bodey, G. P., Bolivar, R., Fainstein, V. & Jadeja, L. (1983). Infections caused by Pseudomonas aeruginosa. Rev Infect Dis 5, 279-313.
4. Bonomo, R. A. & Szabo, D. (2006). Mechanisms of multidrug resistance in Acinetobacter species and Pseudomonas aeruginosa. Clin Infect Dis 43 (suppl 2), S49-S56.
5. Brazas, M. D. & Hancock, R. E. (2005). Ciprofloxacin induction of a susceptibility determinant in Pseudomonas aeruginosa. Antimicrob Agents Chemother 49, 3222-3227.
6. Bredenbruch, F., Geffers, R., Nimtz, M., Buer, J. & Häussler, S. (2006). The Pseudomonas aeruginosa quinolone signal (PQS) has an iron-chelating activity. Environ Microbiol 8, 1318-1329.
7. Brown, J. M., Dorman, D. C. & Roy, L. P. (1970). Acute renal failure due to overdosage of colistin. Med J Aust 2, 923-924.
8. Cao, H., Krishnan, G., Goumnerov, B., Tsongalis, J., Tompkins, R. & Rahme, L. G. (2001). A quorum sensing-associated virulence gene of Pseudomonas aeruginosa encodes a LysR-like transcription regulator with a unique self-regulatory mechanism. Proc Natl Acad Sci U S A 98, 14613-14618.
9. Davies, J., Spiegelman, G. B. & Yim, G. (2006). The world of subinhibitory antibiotic concentrations. Curr Opin Microbiol 9, 445-453.
10. Denton, M., Kerr, K., Mooney, L., Keer, V., Rajgopal, A., Brownlee, K., Arundel, P. & Conway, S. (2002). Transmission of colistin-resistant Pseudomonas aeruginosa between patients attending a pediatric cystic fibrosis center. Pediatr Pulmonol 34, 257-261.
11. Déziel, E., Lépine, F., Milot, S., He, J., Mindrinos, M. N., Tompkins, R. G. & Rahme, L. G. (2004). Analysis of Pseudomonas aeruginosa 4-hydroxy-2-alkylquinolines (HAQs) reveals a role for 4-hydroxy-2-heptylquinoline in cell-to-cell communication. Proc Natl Acad Sci U S A 101, 1339-1344.
12. 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.
13. Diggle, S. P., Matthijs, S., Wright, V. J., Fletcher, M. P., Chhabra, S. R., Lamont, I. L., Kong, X., Hider, R. C., Cornelis, P. & other authors (2007). The Pseudomonas aeruginosa 4-quinolone signal molecules HHQ and PQS play multifunctional roles in quorum sensing and iron entrapment. Chem Biol 14, 87-96.
14. Dubern, J. F. & Diggle, S. P. (2008). Quorum sensing by 2-alkyl-4-quinolones in Pseudomonas aeruginosa and other bacterial species. Mol Biosyst 4, 882-888.
15. Evans, M. E., Feola, D. J. & Rapp, R. P. (1999). Polymyxin B sulfate and colistin: old antibiotics for emerging multiresistant Gram-negative bacteria. Ann Pharmacother 33, 960-967.
16. Fletcher, M. P., Diggle, S. P., Camara, M. & Williams, P. (2007). Biosensor-based assays for PQS, HHQ and related 2-alkyl-4-quinolone quorum sensing signal molecules. Nat Protoc 2, 1254-1262.
17. Frederiksen, B., Koch, C. & Høiby, N. (1999). Changing epidemiology of Pseudomonas aeruginosa infection in Danish cystic fibrosis patients (1974-1995). Pediatr Pulmonol 28, 159-166.
18. Gallagher, L. A. & Manoil, C. (2001). Pseudomonas aeruginosa PAO1 kills Caenorhabditis elegans by cyanide poisoning. J Bacteriol 183, 6207-6214.
19. Garnacho-Montero, J., Ortiz-Leyba, C., Jiménez-Jiménez, F. J., Barrero-Almodóvar, A. E., García-Garmendia, J. L., Bernabeu-Wittel, I. M., Gallego-Lara, S. L. & Madrazo-Osuna, J. (2003). Treatment of multidrug-resistant Acinetobacter baumannii ventilator-associated pneumonia (VAP) with intravenous colistin: a comparison with imipenem-susceptible VAP. Clin Infect Dis 36, 1111-1118.
20. Gerber, M., Walch, C., Löffler, B., Tischendorf, K., Reischl, U. & Ackermann, G. (2008). Effect of sub-MIC concentrations of metronidazole, vancomycin, clindamycin and linezolid on toxin gene transcription and production in Clostridium difficile. J Med Microbiol 57, 776-783.
21. Goh, E. B., Yim, G., Tsui, W., McClure, J., Surette, M. G. & Davies, J. (2002). Transcriptional modulation of bacterial gene expression by subinhibitory concentrations of antibiotics. Proc Natl Acad Sci U S A 99, 17025-17030.
22. Govan, J. R. & Deretic, V. (1996). Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol Rev 60, 539-574.
23. Guina, T., Purvine, S. O., Yi, E. C., Eng, J., Goodlett, D. R., Aebersold, R. & Miller, S. I. (2003). Quantitative proteomic analysis indicates increased synthesis of a quinolone by Pseudomonas aeruginosa isolates from cystic fibrosis airways. Proc Natl Acad Sci U S A 100, 2771-2776.
24. Hanberger, H., Diekema, D., Fluit, A., Jones, R., Struelens, M., Spencer, R. & Wolff, M. (2001). Surveillance of antibiotic resistance in European ICUs. J Hosp Infect 48, 161-176.
25. Hancock, R. E. (1997a). The bacterial outer membrane as a drug barrier. Trends Microbiol 5, 37-42.
26. Hancock, R. E. (1997b). Peptide antibiotics. Lancet 349, 418-422.
27. Häussler, S. & Becker, T. (2008). The pseudomonas quinolone signal (PQS) balances life and death in Pseudomonas aeruginosa populations. PLoS Pathog 4, e1000166.
28. Hawley, J. S., Murray, C. K. & Jorgensen, J. H. (2008). Colistin heteroresistance in Acinetobacter and its association with previous colistin therapy. Antimicrob Agents Chemother 52, 351-352.
29. Hays, E. E., Wells, I. C., Katzman, P. A., Cain, C. K., Jacobs, F. A., Thayer, S. A., Doisy, E. A., Gaby, W. L., Roberts, E. C. & other authors (1945). Antibiotic substances produced by Pseudomonas aeruginosa. J Biol Chem 159, 725-750.
30. Hermsen, E. D., Sullivan, C. J. & Rotschafer, J. C. (2003). Polymyxins: pharmacology, pharmacokinetics, pharmacodynamics, and clinical applications. Infect Dis Clin North Am 17, 545-562.
31. Hoffman, L. R., D'Argenio, D. A., MacCoss, M. J., Zhang, Z., Jones, R. A. & Miller, S. I. (2005). Aminoglycoside antibiotics induce bacterial biofilm formation. Nature 436, 1171-1175.
32. Hostacka, A. & Ciznar, I. (2008). Aminoglycosides and colistin inhibit biofilm formation in Klebsiella pneumoniae.)..Epidemiol Mikrobiol Imunol 57, 101-105.
33. Labro, M. T., el Benna, J. & Jemni, A. (1992). Alteration of bacteria induced by subinhibitory concentrations of cefixime: consequences on bactericidal activity of human polynuclear neutrophils. Pathol Biol (Paris) 40, 427-432.
34. Lépine, F., Déziel, E., Milot, S. & Rahme, L. G. (2003). A stable isotope dilution assay for the quantification of the Pseudomonas quinolone signal in Pseudomonas aeruginosa cultures. Biochim Biophys Acta 1622, 36-41.
35. Li, J., Rayner, C. R., Nation, R. L., Owen, R. J., Spelman, D., Tan, K. E. & Liolios, L. (2006). Heteroresistance to colistin in multidrug-resistant Acinetobacter baumannii. Antimicrob Agents Chemother 50, 2946-2950.
36. Liang, H., Li, L., Dong, Z., Surette, M. G. & Duan, K. (2008). The YebC family protein PA0964 negatively regulates the Pseudomonas aeruginosa quinolone signal system and pyocyanin production. J Bacteriol 190, 6217-6227.
37. Linares, J. F., Gustafsson, I., Baquero, F. & Martinez, J. L. (2006). Antibiotics as intermicrobial signaling agents instead of weapons. Proc Natl Acad Sci U S A 103, 19484-19489.
38. Mahajan-Miklos, S., Tan, M. W., Rahme, L. G. & Ausubel, F. M. (1999). Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model. Cell 96, 47-56.
39. Markou, N., Apostolakos, H., Koumoudiou, C., Athanasiou, M., Koutsoukou, A., Alamanos, I. & Gregorakos, L. (2003). Intravenous colistin in the treatment of sepsis from multi-resistant Gram-negative bacilli in critically ill patients. Crit Care 7, R78-R83.
40. Mashburn-Warren, L., Howe, J., Garidel, P., Richter, W., Steiniger, F., Roessle, M., Brandenburg, K. & Whiteley, M. (2008). Interaction of quorum signals with outer membrane lipids: insights into prokaryotic membrane vesicle formation. Mol Microbiol 69, 491-502.
41. Mavrodi, D. V., Bonsall, R. F., Delaney, S. M., Soule, M. J., Phillips, G. & Thomashow, L. S. (2001). Functional analysis of genes for biosynthesis of pyocyanin and phenazine-1-carboxamide from Pseudomonas aeruginosa PAO1. J Bacteriol 183, 6454-6465.
42. McGrath, S., Wade, D. S. & Pesci, E. C. (2004). Dueling quorum sensing systems in Pseudomonas aeruginosa control the production of the Pseudomonas quinolone signal (PQS). FEMS Microbiol Lett 230, 27-34.
43. McPhee, J. B., Lewenza, S. & Hancock, R. E. (2003). Cationic antimicrobial peptides activate a two-component regulatory system, PmrA-PmrB, that regulates resistance to polymyxin B and cationic antimicrobial peptides in Pseudomonas aeruginosa. Mol Microbiol 50, 205-217.
44. Miller, J. H. (1972). Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
45. Mitova, M. I., Lang, G., Wiese, J. & Imhoff, J. F. (2008). Subinhibitory concentrations of antibiotics induce phenazine production in a marine Streptomyces sp. J Nat Prod 71, 824-827.
46. Nalca, Y., Jänsch, L., Bredenbruch, F., Geffers, R., Buer, J. & Häussler, S. (2006). Quorum-sensing antagonistic activities of azithromycin in Pseudomonas aeruginosa PAO1: a global approach. Antimicrob Agents Chemother 50, 1680-1688.
47. Nikaido, H. (1989). Outer membrane barrier as a mechanism of antimicrobial resistance. Antimicrob Agents Chemother 33, 1831-1836.
48. Oh, J. T., Cajal, Y., Skowronska, E. M., Belkin, S., Chen, J., Van Dyk, T. K., Sasser, M. & Jain, M. K. (2000). Cationic peptide antimicrobials induce selective transcription of micF and osmY in Escherichia coli. Biochim Biophys Acta 1463, 43-54.
49. Overhage, J., Campisano, A., Bains, M., Torfs, E. C., Rehm, B. H. & Hancock, R. E. (2008). The human host defence peptide LL-37 prevents bacterial biofilm formation. Infect Immun 76, 4176-4182.
50. Peschel, A. (2002). How do bacteria resist human antimicrobial peptides? Trends Microbiol 10, 179-186.
51. Pesci, E. C., Milbank, J. B., Pearson, J. P., McKnight, S., Kende, A. S., Greenberg, E. P. & Iglewski, B. H. (1999). Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 96, 11229-11234.
52. Rahal, J. J. (2006). Novel antibiotic combinations against infections with almost completely resistant Pseudomonas aeruginosa and Acinetobacter species. Clin Infect Dis 43 (suppl. 2), S95-S99.
53. Rahme, L. G., Ausubel, F. M., Cao, H., Drenkard, E., Goumnerov, B. C., Lau, G. W., Mahajan-Miklos, S., Plotnikova, J., Tan, M. W. & other authors (2000). Plants and animals share functionally common bacterial virulence factors. Proc Natl Acad Sci U S A 97, 8815-8821.
54. Ryan, R. P., Fouhy, Y., Garcia, B. F., Watt, S. A., Niehaus, K., Yang, L., Tolker-Nielsen, T. & Dow, J. M. (2008). Interspecies signalling via the Stenotrophomonas maltophilia diffusible signal factor influences biofilm formation and polymyxin tolerance in Pseudomonas aeruginosa. Mol Microbiol 68, 75-86.
55. 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.
56. Shen, L., Shi, Y., Zhang, D., Wei, J., Surette, M. G. & Duan, K. (2008). Modulation of secreted virulence factor genes by subinhibitory concentrations of antibiotics in Pseudomonas aeruginosa. J Microbiol 46, 441-447.
57. Skindersoe, M. E., Alhede, M., Phipps, R., Yang, L., Jensen, P. O., Rasmussen, T. B., Bjarnsholt, T., Tolker-Nielsen, T., Høiby, N. & Givskov, M. (2008). Effects of antibiotics on quorum sensing in Pseudomonas aeruginosa. Antimicrob Agents Chemother 52, 3648-3663.
58. Spaink, H. P., Okker, R. J. H., Wijffelman, C. A., Pees, E. & Lugtenberg, B. J. J. (1987). Promoters of nodulation region of the Rhizobium leguminosarum Sym plasmid pRL1J1. Plant Mol Biol 9, 27-39.
59. Tam, V. H., Schilling, A. N., Vo, G., Kabbara, S., Kwa, A. L., Wiederhold, N. P. & Lewis, R. E. (2005). Pharmacodynamics of polymyxin B against Pseudomonas aeruginosa. Antimicrob Agents Chemother 49, 3624-3630.
60. Tomasinsig, L., Scocchi, M., Mettulio, R. & Zanetti, M. (2004). Genome-wide transcriptional profiling of the Escherichia coli response to a proline-rich antimicrobial peptide. Antimicrob Agents Chemother 48, 3260-3267.
61. 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.
62. Waite, R. D., Papakonstantinopoulou, A., Littler, E. & Curtis, M. A. (2005). Transcriptome analysis of Pseudomonas aeruginosa growth: comparison of gene expression in planktonic cultures and developing and mature biofilms. J Bacteriol 187, 6571-6576.
63. Waite, R. D., Paccanaro, A., Papakonstantinopoulou, A., Hurst, J. M., Saqi, M., Littler, E. & Curtis, M. A. (2006). Clustering of Pseudomonas aeruginosa transcriptomes from planktonic cultures, developing and mature biofilms reveals distinct expression profiles. BMC Genomics 7, 162.
64. Wells, I. C., Elliott, W. H., Thayer, S. A. & Doisy, E. A. (1952). Ozonization of some antibiotic substances produced by Pseudomonas aeruginosa. J Biol Chem 196, 321-330.
65. Whiteley, M., Bangera, M. G., Bumgarner, R. E., Parsek, M. R., Teitzel, G. M., Lory, S. & Greenberg, E. P. (2001). Gene expression in Pseudomonas aeruginosa biofilms. Nature 413, 860-864.
66. Xiao, G., He, J. & Rahme, L. G. (2006). Mutation analysis of the Pseudomonas aeruginosa mvfR and pqsABCDE gene promoters demonstrates complex quorum-sensing circuitry. Microbiology 152, 1679-1686.
67. Yang, L., Barken, K. B., Skindersoe, M. E., Christensen, A. B., Givskov, M. & Tolker-Nielsen, T. (2007). Effects of iron on DNA release and biofilm development by Pseudomonas aeruginosa. Microbiology 153, 1318-1328.
68. Zaborina, O., Lépine, 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.