Simultaneous overexpression of multidrug efflux pumps in Pseudomonas aeruginosa non-cystic fibrosis clinical isolates

Canadian Journal of Microbiology

Volumn 60, Issue 7, 2014, Pages 437-443

  Poonsuk, Kanchana ^a   Tribuddharat, Chanwit ^b   Chuanchuen, Rungtip ^a  

^a CHULALONGKORN UNIVERSITY   (Thailand)

^b MAHIDOL UNIVERSITY   (Thailand)

Author keywords

Multidrug efflux system; Multidrug resistance; Pseudomonas aeruginosa

Indexed keywords

AMIKACIN; AZTREONAM; CARBENICILLIN; CHLORAMPHENICOL; CIPROFLOXACIN; ERYTHROMYCIN; GENTAMICIN; IMIPENEM; KANAMYCIN; NEOMYCIN; PIPERACILLIN; SPECTINOMYCIN; STREPTOMYCIN; TETRACYCLINE; TOBRAMYCIN; TRIMETHOPRIM;

ANTIBIOTICS; BACTERIUM; DNA FINGERPRINTING; GENE EXPRESSION; PHENOTYPE; POLYMERASE CHAIN REACTION;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM ISOLATE; CYSTIC FIBROSIS; DNA SEQUENCE; GENE OVEREXPRESSION; MEXAB OPRM GENE; MEXCD OPRJ GENE; MEXEF OPRN GENE; MEXJK GENE; MEXVW GENE; MULTIDRUG RESISTANCE; NEXXY GENE; NON CYSTIC FIBROSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REGULATOR GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

MULTIDRUG EFFLUX SYSTEM; MULTIDRUG RESISTANCE; MULTIRÉSISTANCE AUX MÉDICAMENTS; PSEUDOMONAS AERUGINOSA; SYSTÈME D'EFFLUX POLYCHIMIOTHÉRAPEUTIQUE;

ANTI-BACTERIAL AGENTS; BACTERIAL OUTER MEMBRANE PROTEINS; DRUG RESISTANCE, MULTIPLE; GENE EXPRESSION REGULATION, BACTERIAL; GENES, REGULATOR; MEMBRANE TRANSPORT PROTEINS; MUTATION; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; REAL-TIME POLYMERASE CHAIN REACTION; RNA, BACTERIAL; SEQUENCE ANALYSIS, DNA;

EID: 84904248550     PISSN: 00084166     EISSN: 14803275     Source Type: Journal    
DOI: 10.1139/cjm-2014-0239     Document Type: Article

References (34)

1. Aendekerk, S., Ghysels, B., Cornelis, P., and Baysse, C. 2002. Characterization of a new efflux pump, MexGHI-OpmD, from Pseudomonas aeruginosa that confers resistance to vanadium. Microbiology, 148: 2371-2381. PMID:12177331.
2. Berlanga, M., Montero, M.T., Hernandez-Borrell, J., and Vinas, M. 2004. Influence of the cell wall on ciprofloxacin susceptibility in selected wild-type Gramnegative and Gram-positive bacteria. Int. J. Antimicrob. Agents, 23: 627-630. doi:10.1016/j.ijantimicag.2003.12.015. PMID:15194135.
3. Bunny, K.L., Hall, R.M., and Stokes, H.W. 1995. New mobile gene cassettes containing an aminoglycoside resistance gene, aacA7, and a chloramphenicol resistance gene, catB3, in an integron in pBWH301. Antimicrob. Agents Chemother. 39: 686-693. doi:10.1128/AAC.39.3.686. PMID:7793874.
4. Cao, L., Srikumar, R., and Poole, K. 2004. MexAB-OprM hyperexpression in NalC-type multidrug-resistant Pseudomonas aeruginosa: identification and characterization of the nalC gene encoding a repressor of PA3720-PA3719. Mol. Microbiol. 53: 1423-1436. doi:10.1111/j.1365-2958.2004.04210.x. PMID: 15387820.
5. Chuanchuen, R., and Padungtod, P. 2009. Antimicrobial resistance genes in Salmonella enterica isolates from poultry and swine in Thailand. J. Vet. Med. Sci. 71: 1349-1355. doi:10.1292/jvms.001349. PMID:19887742.
6. Chuanchuen, R., Beinlich, K., Hoang, T.T., Becher, A., Karkhoff-Schweizer, R.R., and Schweizer, H.P. 2001. Cross-resistance between triclosan and antibiotics in Pseudomonas aeruginosa is mediated by multidrug efflux pumps: exposure of a susceptible strain to triclosan selects nfxB mutants overexpressing MexCD-OprJ. Antimicrob. Agents Chemother. 45: 428-432. doi:10.1128/AAC. 45.2.428-432.2001. PMID:11158736.
7. Chuanchuen, R., Narasaki, C.T., and Schweizer, H.P. 2002. The MexJK efflux pump of Pseudomonas aeruginosa requires OprM for antibiotic efflux but not for efflux of triclosan. J. Bacteriol. 184: 5036-5044. doi:10.1128/JB.184.18.5036-5044.2002. PMID:12193619.
8. Chuanchuen, R., Wannaprasat, W., Ajariyakhajorn, K., and Schweizer, H.P. 2008. Role of the MexXY multidrug efflux pump in moderate aminoglycoside resistance in Pseudomonas aeruginosa isolates from Pseudomonas mastitis. Microbiol. Immunol. 52: 392-398. doi:10.1111/j.1348-0421.2008.00051.x. PMID: 18667038.
9. CLSI. 2008. Performance standards for antimicrobial susceptibility testing: eighteenth informational supplement. CLSI document M100-S18. Clinical Laboratory Standards Institute, Wayne, Penn., USA.
10. Evans, K., Adewoye, L., and Poole, K. 2001. MexR repressor of the mexAB-oprM multidrug efflux operon of Pseudomonas aeruginosa: identification of MexR binding sites in the mexA-mexR intergenic region. J. Bacteriol. 183: 807-812. doi:10.1128/JB.183.3.807-812.2001. PMID:11208776.
11. Gilleland, L.B., Gilleland, H.E., Gibson, J.A., and Champlin, F.R. 1989. Adaptive resistance to aminoglycoside antibiotics in Pseudomonas aeruginosa. J. Med. Microbiol. 29: 41-50. doi:10.1099/00222615-29-1-41. PMID:2498520.
12. Hachler, H., Santanam, P., and Kayser, F.H. 1996. Sequence and characterization of a novel chromosomal aminoglycoside phosphotransferase gene, aph(3=)-IIb, in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 40: 1254-1256. PMID:8723476.
13. Hocquet, D., Nordmann, P., El Garch, F., Cabanne, L., and Plesiat, P. 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. doi:10.1128/AAC.50.4.1347-1351.2006. PMID:16569851.
14. Islam, S., Jalal, S., and Wretlind, B. 2004. Expression of the MexXY efflux pump in amikacin-resistant isolates of Pseudomonas aeruginosa. Clin. Microbiol. Infect. 10: 877-883. doi:10.1111/j.1469-0691.2004.00991.x. PMID:15373880.
15. Kohler, T., Michea-Hamzehpour, M., Henze, U., Gotoh, N., Curty, L.K., and Pechere, J.C. 1997. Characterization of MexE-MexF-OprN, a positively regulated multidrug efflux system of Pseudomonas aeruginosa. Mol. Microbiol. 23: 345-354. doi:10.1046/j.1365-2958.1997.2281594.x. PMID:9044268.
16. Li, Y., Mima, T., Komori, Y., Morita, Y., Kuroda, T., Mizushima, T., et al. 2003. A new member of the tripartite multidrug efflux pumps, MexVW-OprM, in Pseudomonas aeruginosa. J. Antimicrob. Chemother. 52: 572-575. doi:10.1093/ jac/dkg390. PMID:12951344.
17. Lister, P.D., Wolter, D.J., and Hanson, N.D. 2009. Antibacterial-resistant Pseudomonas aeruginosa: clinical impact and complex regulation of chromosomally encoded resistance mechanisms. Clin. Microbiol. Rev. 22: 582-610. doi:10.1128/CMR.00040-09. PMID:19822890.
18. Llanes, C., Hocquet, D., Vogne, C., Benali-Baitich, D., Neuwirth, C., and Plesiat, P. 2004. Clinical strains of Pseudomonas aeruginosa overproducing MexAB-OprM and MexXY efflux pumps simultaneously. Antimicrob. Agents Chemother. 48: 1797-1802. doi:10.1128/AAC.48.5.1797-1802.2004. PMID:15105137.
19. Llanes, C., Kohler, T., Patry, I., Dehecq, B., van Delden, C., and Plesiat, P. 2011. Role of the MexEF-OprN efflux system in low-level resistance of Pseudomonas aeruginosa to ciprofloxacin. Antimicrob. Agents Chemother. 55: 5676-5684. doi:10.1128/AAC.00101-11. PMID:21911574.
20. Maseda, H., Saito, K., Nakajima, A., and Nakae, T. 2000. Variation of the mexT gene, a regulator of the MexEF-OprN efflux pump expression in wild-type strains of Pseudomonas aeruginosa. FEMS Microbiol. Lett. 192: 107-112. doi:10. 1111/j.1574-6968.2000.tb09367.x. PMID:11040437.
21. Masuda, N., Gotoh, N., Ishi, C., Sakagawa, E., Ohya, S., and Nishino, T. 1999. Interplay between chromosomal β-lactamase and the MexAB-OprM efflux system in intrinsic resistance to β-lactams in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 43: 400-402. PMID:9925544.
22. Masuda, N., Sagagawa, E., Ohya, S., Gotoh, N., Tsujimoto, H., and Nishino, T. 2000. Contribution of the MexX-MexY-OprM efflux system to intrinsic resistance in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 44: 2242-2246. doi:10.1128/AAC.44.9.2242-2246.2000. PMID:10952562.
23. Morita, Y., Komori, Y., Mima, T., Kuroda, T., Mizushima, T., and Tsuchiya, T. 2001. Construction of a series of mutants lacking all of the four major mex operons for multidrug efflux pumps or possessing each one of the operons from Pseudomonas aeruginosa PAO1: MexCD-OprJ is an inducible pump. FEMS Microbiol. Lett. 202: 139-143. doi:10.1111/j.1574-6968.2001.tb10794.x. PMID:11506922.
24. Ochs, M.M., McCusker, M.P., Bains, M., and Hancock, R.E. 1999. Negative regulation of the Pseudomonas aeruginosa outer membrane porin OprD selective for imipenem and basic amino acids. Antimicrob. Agents Chemother. 43: 1085-1090. PMID:10223918.
25. Poonsuk, K., Tribuddharat, C., and Chuanchuen, R. 2013. Aminoglycoside resistance mechanisms in Pseudomonas aeruginosa isolates from non-cystic fibrosis patients in Thailand. Can. J. Microbiol. 59(1): 51-56. doi:10.1139/cjm-2012-0465. PMID:23391230.
26. Pumbwe, L., and Piddock, L.J. 2000. Two efflux systems expressed simultaneously in multidrug-resistant Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 44: 2861-2864. doi:10.1128/AAC.44.10.2861-2864.2000. PMID:10991874.
27. Sobel, M.L., Hocquet, D., Cao, L., Plesiat, P., and Poole, K. 2005a. Mutations in PA3574 (nalD) lead to increased MexAB-OprM expression and multidrug resistance in laboratory and clinical isolates of Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 49: 1782-1786. doi:10.1128/AAC.49.5.1782-1786.2005. PMID:15855496.
28. Sobel, M.L., Neshat, S., and Poole, K. 2005b. Mutations in PA2491 (mexS) promote MexT-dependent mexEF-oprN expression and multidrug resistance in a clinical strain of Pseudomonas aeruginosa. J. Bacteriol. 187: 1246-1253. doi:10.1128/ JB.187.4.1246-1253.2005. PMID:15687188.
29. Srikumar, R., Paul, C.J., and Poole, K. 2000. Influence of mutations in the mexR repressor gene on expression of the MexA-MexB-OprM multidrug efflux system of Pseudomonas aeruginosa. J. Bacteriol. 182: 1410-1414. doi:10.1128/JB.182. 5.1410-1414.2000. PMID:10671465.
30. Watson, J.M., and Holloway, B.W. 1978. Chromosome mapping in Pseudomonas aeruginosa. J. Bacteriol. 133: 1113-1125. PMID:417059.
31. Westfall, L.W., Carty, N.L., Layland, N., Kuan, P., Colmer-Hamood, J.A., and Hamood, A.N. 2006. mvaT mutation modifies the expression of the Pseudomonas aeruginosa multidrug efflux operon mexEF-oprN. FEMS Microbiol. Lett. 255: 247-254. doi:10.1111/j.1574-6968.2005.00075.x. PMID:16448502.
32. Winsor, G.L., Lam, D.K., Fleming, L., Lo, R., Whiteside, M.D., Yu, N.Y., et al. 2011. Pseudomonas Genome Database: improved comparative analysis and population genomics capability for Pseudomonas genomes. Nucleic Acids Res. 39: D596-D600. doi:10.1093/nar/gkq869. PMID:20929876.
33. Wolter, D.J., Hanson, N.D., and Lister, P.D. 2008. Novel mechanism of mexEF-oprN efflux pump overexpression in Pseudomonas aeruginosa without co-regulation of oprD Expression. Abstr. 48th Intersci. Conf. Antimicrob. Agents Chemother. Washington, D.C., USA.
34. Woods, C.R., Versalovic, J., Koeuth, T., and Lupski, J.R. 1993. Whole-cell repetitive element sequence-based polymerase chain reaction allows rapid assessment of clonal relationships of bacterial isolates. J. Clin. Microbiol. 31: 1927-1931. PMID:8349778.