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PMID: 12193619 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

The MexJK efflux pump of Pseudomonas aeruginosa requires OprM for antibiotic efflux but not for efflux of triclosan.

Journal of bacteriology ·Vol. 184 ·No. 18 ·2002-09-00 ·Pages 5036-44

Chuanchuen R, Narasaki CT, Schweizer HP

Abstract

Using the biocide triclosan as a selective agent, several triclosan-resistant mutants of a susceptible Pseudomonas aeruginosa strain were isolated. Cloning and characterization of a DNA fragment conferring triclosan resistance from one of these mutants revealed a hitherto uncharacterized efflux system of the resistance nodulation cell division (RND) family, which was named MexJK and which is encoded by the mexJK operon. Expression of this operon is negatively regulated by the product of mexL, a gene located upstream of and transcribed divergently from mexJK. The triclosan-resistant mutant contained a single nucleotide change in mexL, which caused an amino acid change in the putative helix-turn-helix domain of MexL. The MexL protein belongs to the TetR family of repressor proteins. The MexJK system effluxed tetracycline and erythromycin but only in the presence of the outer membrane protein channel OprM; OprJ and OprN did not function with MexJK. Triclosan efflux required neither of the outer membrane protein channels tested but necessitated the MexJ membrane fusion protein and the MexK inner membrane RND transporter. The results presented in this study suggest that MexJK may function as a two-component RND pump for triclosan efflux but must associate with OprM to form a tripartite antibiotic efflux system. Furthermore, the results confirm that triclosan is an excellent tool for the study of RND multidrug efflux systems and that this popular biocide therefore readily selects mutants which are cross-resistant with antibiotics.

MeSH Terms
Amino Acid Sequence Anti-Bacterial Agents/metabolism,pharmacology Anti-Infective Agents, Local/metabolism,pharmacology Bacterial Outer Membrane Proteins/genetics,metabolism Bacterial Proteins/chemistry,genetics,metabolism Base Sequence Biological Transport Carrier Proteins/genetics,metabolism Cloning, Molecular Drug Resistance, Bacterial/genetics Gene Expression Regulation, Bacterial Membrane Transport Proteins/chemistry,genetics,metabolism Microbial Sensitivity Tests Molecular Sequence Data Pseudomonas aeruginosa/drug effects,genetics Sequence Analysis, DNA Triclosan/metabolism,pharmacology
Chemicals
Anti-Bacterial Agents Anti-Infective Agents, Local Bacterial Outer Membrane Proteins Bacterial Proteins Carrier Proteins Membrane Transport Proteins OprM protein, Pseudomonas aeruginosa Triclosan
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Chuanchuen Rungtip
Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado 80523-1682, USA.
Narasaki Craig T
Schweizer Herbert P
References (54)
54 references, click to expand
  1. Involvement of an active efflux system in the natural resistance of Pseudomonas aeruginosa to aminoglycosides.
    Antimicrob Agents Chemother. 1999 Nov;43(11):2624-8 PMID: 10543738
  2. Analysis of Pseudomonas gene products using lacIq/Ptrp-lac plasmids and transposons that confer conditional phenotypes.
    Gene. 1993 Jan 15;123(1):17-24 PMID: 8380783
  3. Identification of genes controlled by quorum sensing in Pseudomonas aeruginosa.
    Proc Natl Acad Sci U S A. 1999 Nov 23;96(24):13904-9 PMID: 10570171
  4. Functional replacement of OprJ by OprM in the MexCD-OprJ multidrug efflux system of Pseudomonas aeruginosa.
    FEMS Microbiol Lett. 1998 Aug 1;165(1):21-7 PMID: 9711836
  5. Broad spectrum antimicrobial biocides target the FabI component of fatty acid synthesis.
    J Biol Chem. 1998 Nov 13;273(46):30316-20 PMID: 9804793
  6. In vivo emergence of multidrug-resistant mutants of Pseudomonas aeruginosa overexpressing the active efflux system MexA-MexB-OprM.
    Antimicrob Agents Chemother. 1999 Feb;43(2):287-91 PMID: 9925520
  7. Expression in Escherichia coli of a new multidrug efflux pump, MexXY, from Pseudomonas aeruginosa.
    Antimicrob Agents Chemother. 1999 Feb;43(2):415-7 PMID: 9925549
  8. Mechanism of triclosan inhibition of bacterial fatty acid synthesis.
    J Biol Chem. 1999 Apr 16;274(16):11110-4 PMID: 10196195
  9. Use of a genetic approach to evaluate the consequences of inhibition of efflux pumps in Pseudomonas aeruginosa.
    Antimicrob Agents Chemother. 1999 Jun;43(6):1340-6 PMID: 10348749
  10. Characterization of Pseudomonas aeruginosa enoyl-acyl carrier protein reductase (FabI): a target for the antimicrobial triclosan and its role in acylated homoserine lactone synthesis.
    J Bacteriol. 1999 Sep;181(17):5489-97 PMID: 10464225
  11. nalB-type mutations causing the overexpression of the MexAB-OprM efflux pump are located in the mexR gene of the Pseudomonas aeruginosa chromosome.
    FEMS Microbiol Lett. 1999 Oct 1;179(1):67-72 PMID: 10481088
  12. AcrA is a highly asymmetric protein capable of spanning the periplasm.
    J Mol Biol. 1999 Jan 8;285(1):409-20 PMID: 9878415
  13. Characterization of a Pseudomonas aeruginosa efflux pump contributing to aminoglycoside impermeability.
    Antimicrob Agents Chemother. 1999 Dec;43(12):2975-83 PMID: 10582892
  14. Influence of mutations in the mexR repressor gene on expression of the MexA-MexB-oprM multidrug efflux system of Pseudomonas aeruginosa.
    J Bacteriol. 2000 Mar;182(5):1410-4 PMID: 10671465
  15. Function of the membrane fusion protein, MexA, of the MexA, B-OprM efflux pump in Pseudomonas aeruginosa without an anchoring membrane.
    J Biol Chem. 2000 Feb 18;275(7):4628-34 PMID: 10671490
  16. Inhibition of the Staphylococcus aureus NADPH-dependent enoyl-acyl carrier protein reductase by triclosan and hexachlorophene.
    J Biol Chem. 2000 Feb 18;275(7):4654-9 PMID: 10671494
  17. Assignment of the substrate-selective subunits of the MexEF-OprN multidrug efflux pump of Pseudomonas aeruginosa.
    Antimicrob Agents Chemother. 2000 Mar;44(3):658-64 PMID: 10681335
  18. AcrD of Escherichia coli is an aminoglycoside efflux pump.
    J Bacteriol. 2000 Mar;182(6):1754-6 PMID: 10692383
  19. Multidrug resistance mechanisms: drug efflux across two membranes.
    Mol Microbiol. 2000 Jul;37(2):219-25 PMID: 10931319
  20. Contribution of the MexX-MexY-oprM efflux system to intrinsic resistance in Pseudomonas aeruginosa.
    Antimicrob Agents Chemother. 2000 Sep;44(9):2242-6 PMID: 10952562
  21. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen.
    Nature. 2000 Aug 31;406(6799):959-64 PMID: 10984043
  22. Two efflux systems expressed simultaneously in multidrug-resistant Pseudomonas aeruginosa.
    Antimicrob Agents Chemother. 2000 Oct;44(10):2861-4 PMID: 10991874
  23. 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 Nov 1;192(1):107-12 PMID: 11040437
  24. High-frequency flp recombinase-mediated inversions of the oriC-containing region of the Pseudomonas aeruginosa genome.
    J Bacteriol. 2000 Dec;182(24):7070-4 PMID: 11092871
  25. Cross-resistance between triclosan and antibiotics 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. 2001 Feb;45(2):428-32 PMID: 11158736
  26. Differential selection of multidrug efflux mutants by trovafloxacin and ciprofloxacin in an experimental model of Pseudomonas aeruginosa acute pneumonia in rats.
    Antimicrob Agents Chemother. 2001 Feb;45(2):571-6 PMID: 11158756
  27. Multidrug efflux pumps and antimicrobial resistance in Pseudomonas aeruginosa and related organisms.
    J Mol Microbiol Biotechnol. 2001 Apr;3(2):255-64 PMID: 11321581
  28. Contribution of multidrug efflux pumps to multiple antibiotic resistance in veterinary clinical isolates of Pseudomonas aeruginosa.
    FEMS Microbiol Lett. 2001 May 1;198(2):129-34 PMID: 11430403
  29. Triclosan: a widely used biocide and its link to antibiotics.
    FEMS Microbiol Lett. 2001 Aug 7;202(1):1-7 PMID: 11506900
  30. Vector design and development of host systems for Pseudomonas.
    Genet Eng (N Y). 2001;23:69-81 PMID: 11570107
  31. Small broad-host-range lacZ operon fusion vector with low background activity.
    Biotechniques. 2001 Dec;31(6):1258, 1260, 1262 PMID: 11768652
  32. Soap bacteriostats.
    J Am Oil Chem Soc. 1968 May;45(5):345-50 PMID: 4871909
  33. Antimicrobial actions of hexachlorophene: cytological manifestations.
    J Bacteriol. 1971 Oct;108(1):482-91 PMID: 4107813
  34. Multiple antibiotic resistance in Pseudomonas aeruginosa: evidence for involvement of an efflux operon.
    J Bacteriol. 1993 Nov;175(22):7363-72 PMID: 8226684
  35. Electrotransformation of Pseudomonas.
    Methods Mol Biol. 1995;47:125-33 PMID: 7550726
  36. Triclosan: applications and safety.
    Am J Infect Control. 1996 Jun;24(3):209-18 PMID: 8807001
  37. Overexpression of the mexC-mexD-oprJ efflux operon in nfxB-type multidrug-resistant strains of Pseudomonas aeruginosa.
    Mol Microbiol. 1996 Aug;21(4):713-24 PMID: 8878035
  38. Expression of the multidrug resistance operon mexA-mexB-oprM in Pseudomonas aeruginosa: mexR encodes a regulator of operon expression.
    Antimicrob Agents Chemother. 1996 Sep;40(9):2021-8 PMID: 8878574
  39. The bacterial outer membrane as a drug barrier.
    Trends Microbiol. 1997 Jan;5(1):37-42 PMID: 9025234
  40. Characterization of MexE-MexF-OprN, a positively regulated multidrug efflux system of Pseudomonas aeruginosa.
    Mol Microbiol. 1997 Jan;23(2):345-54 PMID: 9044268
  41. Use of fluorescence probes to monitor function of the subunit proteins of the MexA-MexB-oprM drug extrusion machinery in Pseudomonas aeruginosa.
    J Biol Chem. 1997 Aug 29;272(35):21964-9 PMID: 9268332
  42. Inner membrane efflux components are responsible for beta-lactam specificity of multidrug efflux pumps in Pseudomonas aeruginosa.
    J Bacteriol. 1997 Dec;179(24):7875-81 PMID: 9401051
  43. Intrinsic resistance to inhibitors of fatty acid biosynthesis in Pseudomonas aeruginosa is due to efflux: application of a novel technique for generation of unmarked chromosomal mutations for the study of efflux systems.
    Antimicrob Agents Chemother. 1998 Feb;42(2):394-8 PMID: 9527792
  44. Contribution of outer membrane efflux protein OprM to antibiotic resistance in Pseudomonas aeruginosa independent of MexAB.
    Antimicrob Agents Chemother. 1998 Jul;42(7):1682-8 PMID: 9661004
  45. A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants.
    Gene. 1998 May 28;212(1):77-86 PMID: 9661666
  46. Triclosan targets lipid synthesis.
    Nature. 1998 Aug 6;394(6693):531-2 PMID: 9707111
  47. Chromosome mapping in Pseudomonas aeruginosa PAT.
    J Bacteriol. 1978 Mar;133(3):1113-25 PMID: 417059
  48. Active efflux of tetracycline encoded by four genetically different tetracycline resistance determinants in Escherichia coli.
    Proc Natl Acad Sci U S A. 1980 Jul;77(7):3974-7 PMID: 7001450
  49. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors.
    Gene. 1985;33(1):103-19 PMID: 2985470
  50. In vivo cloning of Pseudomonas aeruginosa genes with mini-D3112 transposable bacteriophage.
    J Bacteriol. 1989 Jul;171(7):3917-25 PMID: 2544563
  51. Transformation of Pseudomonas aeruginosa by electroporation.
    Anal Biochem. 1990 Aug 15;189(1):75-9 PMID: 2126169
  52. The agmR gene, an environmentally responsive gene, complements defective glpR, which encodes the putative activator for glycerol metabolism in Pseudomonas aeruginosa.
    J Bacteriol. 1991 Nov;173(21):6798-806 PMID: 1938886
  53. Allelic exchange in Pseudomonas aeruginosa using novel ColE1-type vectors and a family of cassettes containing a portable oriT and the counter-selectable Bacillus subtilis sacB marker.
    Mol Microbiol. 1992 May;6(9):1195-204 PMID: 1588818
  54. Identification of a gene cluster, czr, involved in cadmium and zinc resistance in Pseudomonas aeruginosa.
    Gene. 1999 Oct 1;238(2):417-25 PMID: 10570969
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
2002-09-00
Pages
5036-44
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC135324
Subset
IM
Grants
NIGMS NIH HHS · GM56685 · United States
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