A combined phenotypic and genotypic method for the detection of Mex efflux pumps in Pseudomonas aeruginosa

Journal of Antimicrobial Chemotherapy

Volumn 59, Issue 3, 2007, Pages 378-386

  Mesaros, Narcisa ^a   Glupczynski, Youri ^b   Avrain, Laëtitia ^a   Caceres, Nancy E ^a   Tulkens, Paul M ^a   Van Bambeke, Françoise ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b UNIVERSITY HOSPITAL OF MONT GODINNE   (Belgium)

Author keywords

Diagnostic; Efflux pump; Multidrug resistance; Phe Arg naphthylamide; Pseudomonas aeruginosa

Indexed keywords

2 NAPHTHYLAMINE; CARBENICILLIN; CARRIER PROTEIN; ERYTHROMYCIN; GENTAMICIN; IMIPENEM; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN MEXAB OPRM; MULTIDRUG RESISTANCE PROTEIN MEXCD OPRJ; MULTIDRUG RESISTANCE PROTEIN MEXEF OPRN; MULTIDRUG RESISTANCE PROTEIN MEXXY OPRM; NORFLOXACIN; PHENYLARGININE 2 NAPHTHYLAMINE; PRIMER DNA; PROTEIN MEXA; PROTEIN MEXC; PROTEIN MEXE; PROTEIN MEXX; UNCLASSIFIED DRUG; MEMBRANE PROTEIN; MEXA PROTEIN, PSEUDOMONAS AERUGINOSA; MEXB PROTEIN, PSEUDOMONAS AERUGINOSA; MEXC PROTEIN, PSEUDOMONAS AERUGINOSA; MEXD PROTEIN, PSEUDOMONAS AERUGINOSA; OPRJ PROTEIN, PSEUDOMONAS AERUGINOSA; OPRM PROTEIN, PSEUDOMONAS AERUGINOSA; OPRN PROTEIN, PSEUDOMONAS AERUGINOSA; OUTER MEMBRANE PROTEIN;

ARTICLE; BACTERIAL STRAIN; BACTERIUM ISOLATE; CONTROLLED STUDY; CONVERGENT EVOLUTION; CORRELATION ANALYSIS; DIFFERENTIAL DIAGNOSIS; GENE OVEREXPRESSION; GENOTYPE; MINIMUM INHIBITORY CONCENTRATION; MULTIDRUG RESISTANCE; NONHUMAN; PHENOTYPE; PSEUDOMONAS AERUGINOSA; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VALIDATION PROCESS; ANTIBIOTIC RESISTANCE; DRUG EFFECT; GENETICS; METABOLISM; PHYSIOLOGY;

BACTERIAL OUTER MEMBRANE PROTEINS; DRUG RESISTANCE, BACTERIAL; GENOTYPE; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; PHENOTYPE; PSEUDOMONAS AERUGINOSA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 34248197053     PISSN: 03057453     EISSN: 14602091     Source Type: Journal    
DOI: 10.1093/jac/dkl504     Document Type: Article

References (51)

1. Rossolini GM, Mantengoli E. Treatment and control of severe infections caused by multiresistant Pseudomonas aeruginosa. Clin Microbiol Infect 2005; 11 Suppl 4: 17-32.
2. Hocquet D, Patry I, Dupont P et al. Low-level resistance to fluoroquinolones conferred by efflux overproduction in Pseudomonas aeruginosa: Clinical significance and routine detection, Pathol Biol (Paris) 2005; 53: 495-9.
3. Aeschlimann JR. The role of multidrug efflux pumps in the antibiotic resistance of Pseudomonas aeruginosa and other gram-negative bacteria. Insights from the Society of Infectious Diseases Pharmacists. Pharmacotherapy 2003; 23: 916-24.
4. Poole K. Multidrug efflux pumps and antimicrobial resistance in Pseudomonas aeruginosa and related organisms. J Mol Microbiol Biolechnol 2001; 3: 255-64.
5. Stover CK, Pham XQ, Erwin AL et al. Complete genome sequence of Pseudomonas aeruginosa PA01, an opportunistic pathogen. Nature 2000; 406: 959-64.
6. Li XZ, Nikaido H. Efflux-mediated drug resistance in bacteria. Drugs 2004; 64:159-204.
7. Vedel G. Simple method to determine β-lactam resistance phenotypes in Pseudomonas aeruginosa using the disc agar diffusion test. J Antimicrob Chemother 2005; 56: 657-64.
8. Llanes C, Hocquet D, Vogne C et al. Clinical strains of Pseudomonas aeruginosa overproducing MexAB-OprM and MexXY efflux pumps simultaneously. Antimicrob Agents Chemother 2004; 48 1797-802.
9. Masuda N, Sakagawa E, Ohya S et al. Contribution of the MexX-MexY-oprM efflux system to intrinsic resistance in Pseudomonas aeniginosa. Antimicrob Agents Chemother 2000; 44: 2242-6.
10. Kohler T, Michea-Hamzehpour M, Henze U et al. Characterization of MexE-MexF-OprN, a positively regulated multidrug efflux system of Pseudomonas aeruginosa. Mol Microbiol 1997; 23: 345-54.
11. Niga T, Ito H, Oyamada Y et al Cooperation between alteration of DNA gyrase genes and over-expression of MexB and MexX confers high-level fluoroquinolone resistance in Pseudomonas aeruginosa strains isolated from a patient who received a liver transplant followed by treatment with fluoroquinolones. Microbiol Immunol 2005; 49: 443-6.
12. De Kievit TR, Parkins MD, Gillis RJ et al. Multidrug efflux pumps: expression patterns and contribution to antibiotic resistance in Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 2001; 45: 1761-70.
13. Jannes G, De Vos D. A review of current and future molecular diagnostic tests for use in the microbiology laboratory. Methods Mol Biol 2006; 345: 1-21.
14. Wolter DJ, Smith-Moland E, Goering RV et al. Multidrug resistance associated with mexXY expression in clinical isolates of Pseudomonas aeruginosa from a Texas hospital. Diagn Microbiol Infect Dis 2004; 50: 43-50.
15. Poumaras S, Maniati M, Spanakis N et al. Spread of efflux pump-overexpressing, non-metallo-β-lactamase-producing, meropenem-resistant but ceftazidime-susceptible Pseudomonas aeruginosa in a region with blaVIM endemicity. J Antimicrob Chemother 2005; 56: 761-4.
16. Morita Y, Murata T, Mima T et al. Induction of mexCD-oprJ operon for a multidrug efflux pump by disinfectants in wild-type Pseudomonas aeruginosa PAO1. J Antimicrob Chemother 2003; 51: 991-4.
17. Li XZ, Barre N, Poole K. Influence of the MexA-MexB-oprM multidrug efflux system on expression of the MexC-MexD-oprJ and MexE-MexF-oprN multidrug efflux systems in Pseudomonas aeruginosa. J Antimicrob Chemother 2000; 46: 885-93.
18. Dumas JL, Van Delden C, Perron K et al. Analysis of antibiotic resistance gene expression in Pseudomonas aeruginosa by quantitative real-time-PCR. FEMS Microbiol Lett 2006; 254: 217-25.
19. Yoneda K, Chikumi H, Murata T et al. Measurement of Pseudomonas aeruginosa multidrug efflux pumps by quantitative real-time polymerase chain reaction.FEMS Microbiol Lett 2005; 243: 125-31.
20. Quale J, Bratu S, Gupta J et al. Interplay of efflux system, ampC, and oprD expression in carbapenem resistance of Pseudomonas aeruginosa clinical isolates. Antimicrob Agents Chemother 2006; 50: 1633-41.
21. Hocquet D, Nordmann P, El Garch F et al. Involvement of the MexXY-OprM efflux system in emergence of cefepime resistance in clinical strains of Pseudomonas aeruginosa. Antimicrob Agents Chemother 2006; 50: 1347-51.
22. Hamzehpour MM, Pechere JC, Plesiat P et al. OprK and OprM define two genetically distinct multidrug efflux systems in Pseudomonas aeruginosa. Antimicrob Agents Chemother 1995; 39: 2392-6.
23. Hocquet D, Vogne C, El Garch F et al. MexXY-OprM efflux pump is necessary for adaptive resistance of Pseudomonas aeruginosa to aminoglycosides. Antimicrob Agents Chemother 2003; 47, 1371-5.
24. Kohler T, Michea-Hamzehpour M, Plesiat P et al. Differential selection of multidrug efflux systems by quinolones in Pseudomonas aeruginosa. Antimicrob Agents Chemother 1997; 41: 2540-3.
25. Maseda H, Saito K, Nakajima A et al. Variation of the mexT gene, a regulator of the MexEF-oprN efflux pump expression in wild-type strains of Pseudomonas aeruginosa. FEMS Microbiol Lett 2000; 192: 107-12.
26. Kolayli F, Karadenizli A, Savli H et al. Effect of carbapenems on the transcriptional expression of the QprD, oprM and oprN genes in Pseudomonas aeruginosa. J Med Microbiol 2004; 53: 915-20.
27. Kohler T, Epp SF, Curty LK et al. Characterization of MexT, the regulator of the MexE-MexF-OprN multidrug efflux system of Pseudomonas aeruginosa. J Bacteriol 1999; 181: 6300-5.
28. Anonymous, Performance Standards for Antimicrobial Susceptibility Testing (16th Informational Supplement) - document M100-S16. Clinical and Laboratory Standards Institute, Wayne, Pa, USA, 2006.
29. Lomovskaya O, Warren MS, Lee A et al. Identification and characterization of inhibitors of multidrug resistance efflux pumps in Pseudomonas aeruginosa: Novel agents for combination therapy. Antimicrob Agents Chemother 2001; 45: 105-16.
30. Coban AY, Ekinci B, Durupinar B. A multidrug efflux pump inhibitor reduces fluoroquinolone resistance in Pseudomonas aeruginosa isolates. Chemotherapy 2004; 50: 22-6.
31. Kem WV, Steinke P, Schumacher A et al. Effect of 1-(1-naphthylmethyl)-piperazine, a novel putative efflux pump inhibitor, on antimicrobial drug susceptibility in clinical isolates of Escherichia coli. J Antimicrob Chemother 2006; 57: 339-43.
32. Evans K, Poole K. The MexA-MexB-OprM multidrug efflux system of Pseudomonas aeruginosa is growth-phase regulated. FEMS Microbiol Lett 1999; 173: 35-9.
33. El Amin N, Giske CG, Jalal S et al. Carbapenem resistance mechanisms in Pseudomonas aeruginosa: Alterations of porin OprD and efflux proteins do not fully explain resistance patterns observed in clinical isolates. APMIS 2005; 113: 187-96.
34. Gilliland G, Perrin S, Blanchard K et al. Analysis of cytokine mRNA and DNA: Detection and quantitation by competitive polymerase chain reaction. Proc Natl Acad Sci USA 1990; 87: 2725-9.
35. Cell FS, Zenilman ME, Shuldiner AR. A rapid and versatile method to synthesize internal standards for competitive PCR. Nucleic Acids Res. 1993; 21: 1047.
36. Skarits C, Fischer S, Haas OA. Quantitation of the sterol regulatory element-binding protein mRNA in mononuclear blood cells by competitive RT-PCR. Clin Chim Acta 2003; 336: 27-37.
37. Poole K, Srikumar R. Multidrug efflux in Pseudomonas aeruginosa: components, mechanisms and clinical significance. Curr Top Med Chem 2001; 1: 59-71.
38. Li XZ, Nikaido H, Poole K. Role of mexA-mexB-oprM in antibiotic efflux in Pseudomonas aeruginosa. Antimicrob Agents Chemother 1995; 39 1948-53.
39. Poole K. Efflux-mediated multiresistance in Gram-negative bacteria. Clin Microbiol Infect 2004: 10: 12-26.
40. Jo JT, Brinkman FS, Hancock RE. Aminoglycoside efflux in Pseudomonas aeruginosa: Involvement of novel outer membrane proteins. Antimicrob Agents Chemother 2003; 47: 1101-11.
41. Poole K, Gotoh N, Tsujimoto H et al. Overexpression of the mexC-mexD-oprJ efflux operon in nfxB-type multidrug-resistant strains of Pseudumonas aeruginosa. Mol Microbiol 1996; 21, 713-24,
42. Poole K, Krebes K, McNally C et al. Multiple antibiotic resistance in Pseudomonas aeruginosa: Evidence for involvement of an efflux operon. J Bacteriol 1993; 175: 7363-72.
43. Kriengkauykiat J, Porter E, Lomovskaya O et al. Use of an efflux pump inhibitor to determine the prevalence of efflux pump-mediated fluoroquinolone resistance and multidrug resistance in Pseudomonas aeruginosa. Antimicrob Agents' Chemother 2005; 49: 565-70.
44. Yoshida K, Nakayama K, Kuru N et al. MexAB-OprM specific efflux pump inhibitors in Pseudomonas aeruginosa. Part 5: Carbon-substituted analogues at the C-2 position. Bioorg Med Chem 2006; 14: 1993-2004.
45. Achenbach JE, Topliff CL, Vassilev VB et al. Detection and quantitation of bovine respiratory syncytial virus using real-time quantitative RT-PCR and quantitative competitive RT-PCR assays. J Virol Methods 2004; 121: 1-6.
46. Kim Y, Gharaibeh SM, Stedman NL et al. Comparison and verification of quantitative competitive reverse transcription polymerase chain reaction (QC-RT-PCR) and real time RT-PCR for avian leukosis vinis subgroup J. J Virol Methods 2002; 102: 1-8.
47. Islam S, Jalal S, Wretlind B. Expression of the MexXY efflux pump in amikacin-resistant isolates of Pseudomonas aeruginosa. Clin Microbiol Infect 2004; 10: 877-83.
48. Espy MJ, Uhl JR, Sloan LM et al. Real-time PCR in clinical microbiology: Applications for routine laboratory testing. Clin Microbiol Rev 2006; 19:165-256.
49. Poole K, Tetro K, Zhao Q et al. Expression of the multidrug resistance operon mexA-mexB-oprM in Pseudomonas aeruginosa: MexR encodes a regulator of operon expression. Antimicrob Agents Chemother 1996; 40: 2021-8.
50. Linares JF, Lopez JA, Camafeita E et al. 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 2005; 187: 1384-91.
51. Sobel ML, McKay GA, Poole K. Contribution of the MexXY multidrug transporter to aminoglycoside resistance in Pseudomonas aeruginosa clinical isolates. Antimicrob Agents Chemother 2003; 47: 3202-7.