Resistance and virulence of Pseudomonas aeruginosa clinical strains overproducing the MexCD-OprJ efflux pump

Antimicrobial Agents and Chemotherapy

Volumn 52, Issue 7, 2008, Pages 2455-2462

  Jeannot, Katy ^a   Elsen, Sylvie ^b   Köhler, Thilo ^c   Attree, Ina ^b   Van Delden, Christian ^c   Plésiat, Patrick ^a,d  

^a UNIVERSITÉ DE FRANCHE COMTÉ   (France)

^b CEA GRENOBLE   (France)

^c UNIVERSITY OF GENEVA   (Switzerland)

^d UNIVERSITY HOSPITAL JEAN MINJOZ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMIKACIN; AMINOGLYCOSIDE ANTIBIOTIC AGENT; AZTREONAM; CARRIER PROTEIN; CEFEPIME; CEFPODOXIME; CEFTAZIDIME; CEFTRIAXONE; CHLORAMPHENICOL; CIPROFLOXACIN; IMIPENEM; LACTATE DEHYDROGENASE; OFLOXACIN; PHOSPHOLIPASE C; PROTEIN MEXCD OPRJ; PYOCYANINE; RHAMNOLIPID; TICARCILLIN;

ADULT; AGED; ANIMAL CELL; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; CASE REPORT; GENE OVEREXPRESSION; GRAM NEGATIVE INFECTION; HUMAN; MINIMUM INHIBITORY CONCENTRATION; MOUSE; NFXB GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSEUDOMONAS AERUGINOSA;

EID: 46249116233     PISSN: 00664804     EISSN: None     Source Type: Journal    
DOI: 10.1128/AAC.01107-07     Document Type: Article

References (62)

1. Aires, J. R., T. Köhler, H. Nikaido, and P. Plésiat. 1999. Involvement of an efflux system in the natural resistance of Pseudomonas aeruginosa to aminoglycosides. Antimicrob. Agents Chemother. 43:2624-2628.
2. Berka, R. M., G. L. Gray, and M. L. Vasil. 1981. Studies of phospholipase C (heat-labile hemolysin) in Pseudomonas aeruginosa. Infect. Immun. 34:1071-1074.
3. Berthelot, P., I. Attrée, P. Plésiat, J. Chabert, S. de Bentzmann, B. Pozzetto, and F. Grattard. 2003. Genotypic and phenotypic analysis of type III secretion system in a cohort of Pseudomonas aeruginosa bacteremia isolates: evidence for a possible association between O serotypes and exo genes. J. Infect. Dis. 188:512-518.
4. Choi, K.-H., A. Kumar, and H. P. Schweizer. 2006. A 10-min method for preparation of highly electrocompetent Pseudomonas aeruginosa cells: application for DNA fragment transfer between chromosomes and plasmid transformation. J. Microbiol. Methods 64:391-397.
5. Chuanchuen, R., K. Beinlich, T. T. Hoang, A. Becher, R. R. Karkhoff-Schweizer, and H. P. Schweizer. 2001. Cross-resistance between triclosan and antihiotics in Pseudomonas aeruginosa is mediated by multidrug efflux pumps: exposure of a susceptible mutant strain to triclosan selects nfxB mutants overexpressing MexCD-OprJ. Antimicrob. Agents Chemother. 45:428-432.
6. Clinical and Laboratory Standards Institute/NCCLS. 2008. Performance standards for antimicrobial susceptibility testing; 18th informational supplement. CLSI M100-S18. Clinical and Laboratory Standards Institute, Wayne, PA.
7. Dacheux, D., I. Attrée, C. Schneider, and B. Toussaint. 1999. Cell death of human polymorphonuclear neutrophils induced by a Pseudomonas aeruginosa cystic fibrosis isolate requires a functional type III secretion system. Infect. Immun. 67:6164-6167.
8. Dean, C. R., M. A. Visalli, S. J. Projan, P. E. Sum, and P. A. Bradford. 2003. Efflux-mediated resistance to tigecycline (GAR-936) in Pseudomonas aeruginosa PAO1. Antimicrob. Agents Chemother. 47:972-978.
9. Dumas, J.-L., C. van Delden, K. Perron, and T. Köhler. 2006. Analysis of antibiotic resistance gene expression in Pseudomonas aeruginosa by quantitative real-time-PCR. FEMS Microbiol. Lett. 254:217-225.
10. El'Garch, F., K. Jeannot, D. Hocquet, C. Llanes-Barakat, and P. Plésiat. 2007. Cumulative effects of several nonenzymatic mechanisms on the resistance of Pseudomonas aeruginosa to aminoglycosides. Antimicrob. Agents Chemother. 51:1016-1021.
11. Essar, D. W., L. Eberly, A. Hadero, and I. P. Crawford. 1990. Identification and characterization of genes for a second anthranilate synthase in Pseudomonas aeruginosa: interchangeability of the two anthranilate synthases and evolutionary implications. J. Bacteriol. 172:884-900.
12. Evans, K., L. Passador, R. Srikumar, E. Tsang, J. Nezezon, and K. Poole. 1998. Influence of the MexAB-OprM multidrug efflux system on quorum sensing in Pseudomonas aeruginosa. J. Bacteriol. 180:5443-5447.
13. Gotoh, N., H. Tsujimoto, M. Tsuda, K. Okamoto, A. Nomura, T. Wada, M. Nakahashi, and T. Nishino. 1998. Characterization of the MexC-MexD-OprJ multidrug efflux system in ΔmexA-mexB-oprM mutants of Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 42:1938-1943.
14. Hamzehpour, M. M., J. C. Pechère, P. Plésiat, and T. Köhler. 1995. OprK and OprM define two genetically distinct multidrug efflux systems in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 39:2392-2396.
15. Hirai, K., S. Suzue, T. Irikura, S. Iyobe, and S. Mitsuhashi. 1987. Mutations producing resistance to norfloxacin in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 31:582-586.
16. Hirakata, Y., R. Srikumar, K. Poole, N. Gotoh, T. Suematsu, S. Kohno, S. Kamihira, R. E. Hancock, and D. P. Speert. 2002. Multidrug efflux systems play an important role in the invasiveness of Pseudomonas aeruginosa. J. Exp. Med. 196:109-118.
17. Hocquet, D., P. Berthelot, M. Roussel-Delvallez, R. Favre, K. Jeannot, O. Bajolet, N. Marty, F. Grattard, P. Mariani-Kurkdjian, E. Bingen, M.-O. Husson, G. Couedic, and P. Plésiat. 2007. Pseudomonas aeruginosa may accumulate drug resistance mechanisms without losing its ability to cause bloodstream infections. Antimicrob. Agents Chemother. 51:3531-3536.
18. Hocquet, D., X. Bertrand, T. Köhler, D. Talon, and P. Plésiat. 2003. Genetic and phenotypic variations of a resistant Pseudomonas aeruginosa epidemic clone. Antimicrob. Agents Chemother. 47:1887-1894.
19. Hocquet, D., A. Muller, K. Blanc, P. Plésiat, D. Talon, D. L. Monnet, and X. Bertrand. 2008. Relationship between antibiotic use and incidence of MexXY-OprM overproducers among clinical isolates of Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 52:1173-1175.
20. Hocquet, D., P. Nordmann, F. El'Garch, L. Cabanne, and P. Plésiat. 2006. Involvement of the MexXY-OprM efflux system in emergence of cefepime resistance in clinical strains of Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 50:1347-1351.
21. Hocquet, D., M. Roussel-Delvallez, J.-D. Cavallo, and P. Plésiat. 2007. MexAB-OprM- and MexXY-overproducing mutants are very prevalent among clinical strains of Pseudomonas aeruginosa with reduced susceptibility to ticarcillin. Antimicrob. Agents Chemother. 51:1582-1583.
22. Hocquet, D., C. Vogne, F. El'Garch, A. Vejux, N. Gotoh, A. Lee, O. Lomovskaya, and P. Plésiat. 2003. MexXY-OprM efflux pump is necessary for adaptive resistance of Pseudomonas aeruginosa to aminoglycosides. Antimicrob. Agents Chemother. 47:1371-1375.
23. Holloway, B. W. 1955. Genetic recombination in Pseudomonas aeruginosa. J. Gen. Microbiol. 13:572-581.
24. Hosaka, M., N. Gotoh, and T. Nishino. 1995. Purification of a 54-kilodalton protein (OprJ) produced in nfxB mutants of Pseudomonas aeruginosa and production of a monoclonal antibody specific to OprJ. Antimicrob. Agents Chemother. 39:1731-1735.
25. Jakics, E. B., S. Iyobe, K. Hirai, H. Fukuda, and H. Hashimoto. 1992. Occurrence of the nfxB type mutation in clinical isolates of Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 36:2562-2565.
26. Jalal, S., O. Ciofu, N. Høiby, N. Gotoh, and B. Wretlind. 2000. Molecular mechanisms of fluoroquinolone resistance in Pseudomonas aeruginosa isolates from cystic fibrosis patients. Antimicrob. Agents Chemother. 44:710-712.
27. Jeannot, K., M. L. Sobel, F. El Garch, K. Poole, and P. Plésiat. 2005. Induction of the MexXY efflux pump in Pseudomonas aeruginosa is dependent on drug-ribosome interaction. J. Bacteriol. 187:5341-5346.
28. Jo, J. T., F. S. Brinkman, and R. E. Hancock. 2003. Aminoglycoside efflux in Pseudomonas aeruginosa: involvement of novel outer membrane proteins. Antimicrob. Agents Chemother. 47:1101-1111.
29. Join-Lambert, O. F., M. Michéa-Hamzehpour, T. Köhler, F. Chau, F. Faurisson, S. Dautrey, C. Vissuzaine, C. Carbon, and J.-C. Pechère. 2001. Differential selection of multidrug efflux mutants by trovafloxacin and ciprofloxacin in an experimental model of Pseudomonas aeruginosa acute pneumonia in rats. Antimicrob. Agents Chemother. 45:571-576.
30. Jorgensen, J. H., and J. D. Turnidge. 2003. Susceptibility test methods: dilution and disk diffusion methods, p. 1108-1127. In P. R. Murray, E. J. Baron, J. H. Jorgensen, M. A. Pfaller, and R. H. Yolken (ed.), Manual of clinical microbiology, 8th ed. ASM Press, Washington, DC.
31. Jumbe, N., A. Louie, R. Leary, W. Liu, M. R. Deziel, V. H. Tam, R. Bachhawat, C. Freeman, J. B. Kahn, K. Bush, M. N. Dudley, M. H. Miller, and G. L. Drusano. 2003. Applications of a mathematical model to prevent in vivo amplification of antibiotic-resistant bacterial populations during therapy. J. Clin. Investig. 112:275-285.
32. Köhler, T., M. Michéa-Hamzehpour, P. Plésiat, A. L. Kahr, and J. C. Pechère. 1997. Differential selection of multidrug efflux systems by quinolones in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 41:2540-2543.
33. Köhler, T., C. Van Delden, L. K. Curty, M. Michéa- Hamzehpour, and J.-C. Pechère. 2001. Overexpression of the MexEF-OprN multidrug efflux system affects cell-to-cell signaling in Pseudomonas aeruginosa. J. Bacteriol. 183:5213-5222.
34. Kugelberg, E., S. Löfmark, B. Wretlind, and D. I. Andersson. 2005. Reduction of the fitness burden of quinolone resistance in Pseudomonas aeruginosa. J. Antimicrob. Chemother. 55:22-30.
35. Lee, A., W. Mao, M. S. Warren, A. Mistry, K. Hoshino, R. Okumura, H. Ishida, and O. Lomovskaya. 2000. Interplay between efflux pumps may provide either additive or multiplicative effects on drug resistance. J. Bacteriol. 182:3142-3150.
36. Lee, D. G., J. M. Urbach, G. Wu, N. T. Liberati, R. L. Feinbaum, S. Miyata, L. T. Diggins, J. He, M. Saucier, E. Déziel, L. Friedman, L. Li, G. Grills, K. Montgomery, R. Kucherlapati, L. G. Rahme, and F. M. Ausubel. 2006. Genomic analysis reveals that Pseudomonas aeruginosa virulence is combinatorial. Genome Biol. 7:R90.
37. Li, Y., T. Mima, Y. Komori, Y. Morita, T. Kuroda, T. Mizushima, and T. Tsuchiya. 2003. A new member of the tripartite multidrug efflux pumps, MexVW-OprM, in Pseudomonas aeruginosa. J. Antimicrob. Chemother. 52:572-575.
38. Linares, J. F., J. A. López, E. Camafeita, J. P. Albar, F. Rojo, and J. L. Martinez. 2005. Overexpression of the multidrug efflux pumps MexCD-OprJ and MexEF-OprN is associated with a reduction of type III secretion in Pseudomonas aeruginosa. J. Bacteriol. 187:1384-1391.
39. Llanes, C., D. Hocquet, C. Vogne, D. Benali-Baitich, C. Neuwirth, and P. Plésiat. 2004. Clinical strains of Pseudomonas aeruginosa overproducing MexAB-OprM and MexXY efflux pumps simultaneously. Antimicrob. Agents Chemother. 48:1797-1802.
40. Llanes, C., C. Neuwirth, F. El'Garch, D. Hocquet, and P. Plésiat. 2006. Genetic analysis of a multiresistant strain of Pseudomonas aeruginosa producing PER-1 β-lactamase. Clin. Microbiol. Infect. 12:270-278.
41. Lomovskaya, O., A. Lee, K. Hoshino, H. Ishida, A. Mistry, M. S. Warren, E. Boyer, S. Chamberland, and V. J. Lee. 1999. Use of a genetic approach to evaluate the consequences of inhibition of efflux pumps in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 43:1340-1346.
42. Lomovskaya, O., and W. Watkins. 2001. Inhibition of efflux pumps as a novel approach to combat drug resistance in bacteria. J. Mol. Microbiol. Biotechnol. 3:225-236.
43. Macià, M. D., N. Borrell, M. Segura, C. Gómez, J. L. Pérez, and A. Oliver. 2006. Efficacy and potential for resistance selection of antipseudomonal treatments in a mouse model of lung infection by hypermutable Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 50:975-983.
44. Mahenthiralingam, E., M. E. Campbell, J. Foster, J. S. Lam, and D. P. Speert. 1996. Random amplified polymorphic DNA typing of Pseudomonas aeruginosa isolates recovered from patients with cystic fibrosis. J. Clin. Microbiol. 34:1129-1135.
45. Masuda, N., N. Gotoh, S. Ohya, and T. Nishino. 1996. Quantitative correlation between susceptibility and OprJ production in NfxB mutants of Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 40:909-913.
46. Masuda, N., E. Sakagawa, and S. Ohya. 1995. Outer membrane proteins responsible for multiple drug resistance in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 39:645-649.
47. Masuda, N., E. Sakagawa, S. Ohya, N. Gotoh, and T. Nishino. 2001. Hypersusceptibility of the Pseudomonas aeruginosa nfxB mutant to β-lactams due to reduced expression of the AmpC β-lactamase. Antimicrob. Agents Chemother. 45:1284-1286.
48. Masuda, N., E. Sakagawa, S. Ohya, N. Gotoh, H. Tsujimoto, and T. Nishino. 2000. Contribution of the MexX-MexY-OprM efflux system to intrinsic resistance in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 44:2242-2246.
49. Masuda, N., E. Sakagawa, S. Ohya, N. Gotoh, H. Tsujimoto, and T. Nishino. 2000. Substrate specificities of MexAB-OprM, MexCD-OprJ, and MexXY-OprM efflux pumps in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 44:3322-3327.
50. Morita, Y., M. L. Sobel, and K. Poole. 2006. Antibiotic inducibility of the MexXY multidrug efflux system of Pseudomonas aeruginosa: involvement of the antibiotic-inducible PA5471 gene product. J. Bacteriol. 188:1847-1855.
51. Okazaki, T., and K. Hirai. 1992. Cloning and nucleotide sequence of the Pseudomonas aeruginosa nfxB gene, conferring resistance to new quinolones. FEMS Microbiol. Lett. 97:197-202.
52. Okazaki, T., S. Iyobe, H. Hashimoto, and K. Hirai. 1991. Cloning and characterization of a DNA fragment that complements the nfxB mutation in Pseudomonas aeruginosa PAO. FEMS Microbiol. Lett. 63:31-35.
53. Poole, K. 2005. Efflux-mediated antimicrobial resistance. J. Antimicrob. Chemother. 56:20-51.
54. Poole, K., N. Gotoh, H. Tsujimoto, Q. X. Zhao, A. Wada, T. Yamasaki, S. Neshat, J. I. Yamagishi, X. Z. Li, and T. Nishino. 1996. Overexpression of the mexC-mexD-oprJ efflux operon in nflxB-type multidrug-resistant strains of Pseudomonas aeruginosa. Mol. Microbiol. 21:713-724.
55. Rahme, L. G., E. J. Stevens, S. F. Wolfort, J. Shao, R. G. Tomkins, and F. M. Ausubel. 1995. Common virulence factors for bacterial pathogenicity in plants and animals. Science 268:1899-1902.
56. Reinhardt, A., T. Köhler, P. Wood, P. Rohner, J.-L. Dumas, B. Ricou, and C. van Delden. 2007. Development and persistence of antimicrobial resistance in Pseudomonas aeruginosa: a longitudinal observation in mechanically ventilated patients. Antimicrob. Agents Chemother. 51:1341-1350.
57. Sanchez, P., J. F. Linares, B. Ruiz-Diez, E. Campanario, A. Navas, F. Baquero, and J. L. Martinez. 2002. Fitness of in vitro selected Pseudomonas aeruginosa nalB and nfxB multidrug resistant mutants. J. Antimicrob. Chemother. 50:657-664.
58. Schweizer, H. P. 2003. Efflux as a mechanism to antimicrobials in Pseudomonas aeruginosa and related bacteria: unanswered questions. Genet. Mol. Res. 2:48-62.
59. Siegmund, I., and F. Wagner. 1991. New technique for detecting rhamnolipids excreted by Pseudomonas species during growth in mineral agar. Biotechnol. Tech. 5:265-268.
60. Sobel, M. L., G. A. McKay, and K. Poole. 2003. Contribution of the MexXY multidrug transporter to aminoglycoside resistance in Pseudomonas aeruginosa clinical isolates. Antimicrob. Agents Chemother. 47:3202-3207.
61. van Delden, C., E. C. Pesci, J. P. Pearson, and B. H. Iglewski. 1998. Starvation selection restores elastase and rhamnolipid production in a Pseudomonas aeruginosa quorum-sensing mutant. Infect. Immun. 66:4499-4502.
62. Yoshida, T., T. Muratani, S. Iyobe, and S. Mitsuhashi. 1994. Mechanisms of high-level resistance to quinolones in urinary tract isolates of Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 38:1466-1469.