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Mechanisms of Action: Physiological Effects

Ciprofloxacin Induction of a Susceptibility Determinant in Pseudomonas aeruginosa

Michelle D. Brazas, Robert E. W. Hancock
Michelle D. Brazas
Department of Microbiology and Immunology, University of British Columbia, Vancouver, British Columbia, Canada
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Robert E. W. Hancock
Department of Microbiology and Immunology, University of British Columbia, Vancouver, British Columbia, Canada
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  • For correspondence: bob@cmdr.ubc.ca
DOI: 10.1128/AAC.49.8.3222-3227.2005
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  • FIG. 1.
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    FIG. 1.

    Growth curve for P. aeruginosa strain H103 in the presence or absence of ciprofloxacin. ⧫, untreated PAO1-H103; □, PAO1-H103 plus 0.01 μg/ml ciprofloxacin; ▵, PAO1-H103 plus 0.03 μg/ml ciprofloxacin; and ×, PAO1-H103 plus 0.1 μg/ml ciprofloxacin.

  • FIG. 2.
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    FIG. 2.

    Electron micrographs of supernatants from P. aeruginosa cells that were untreated or treated with 1× MIC of ciprofloxacin. (A) Untreated strain H103 cells. (B) 1× MIC of ciprofloxacin-treated strain H103 cells. Arrows point to the presence of pyocin/phage tail structures. (C) Untreated strain PA0620::luxCDABE cells. (D) 1× MIC of ciprofloxacin-treated PA0620::luxCDABE cells showing absence of R-type pyocin tail structures.

  • FIG. 3.
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    FIG. 3.

    Induction of PA0620::luxCDABE fusions in LB media alone (black bars), with 0.1× MIC of ciprofloxacin (0.01 μg/ml; grey bars), with 0.3× MIC of ciprofloxacin (0.03 μg/ml; white bars), or with 1× MIC of ciprofloxacin (0.1 μg/ml; patterned bars).

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  • TABLE 1.

    Pseudomonas aeruginosa strains used in this study

    StrainGenotypeAbbreviationReference or source
    H103Wild-type P. aeruginosa PAO1H103
    57PA0611::ISlacZ/hah derivative of PAO1 prtR::lacZ 15
    6322PA0613::ISlacZ/hah derivative of PAO1PA0613::lacZ 15
    PAO1_lux_22_E4PA0620::luxCDABE derivative of H103; TcrPA0620::luxThis study
    3501PA0621::ISlacZ/hah derivative of PAO1PA0621::lacZ 15
    PAO1_lux_26_H2PA0641::luxCDABE derivative of H103; TcrPA0641::luxThis study
    43080PA3617::ISphoA/hah derivative of PAO1 recA::phoA 15
    PAO1_lux_24_A3PA3866::luxCDABE derivative of H103; TcrPA3866::luxThis study
  • TABLE 2.

    Primer sequences used in this study

    PrimerSequence
    PA0610_sense5′-TAGCACTCCGATTCCACGC-3′
    PA0610_antisense5′-CCGAAGATGCGGTAGACCA-3′
    PA0611_sense5′-AGCTTCAACCGCGAGGAATA-3′
    PA0611_antisense5′-CATGTCCTCCGGCGAGTACT-3′
    PA0621_sense5′-TTTCCCGTCAGCAACGTAGC-3′
    PA0621_antisense5′-GCTGACTATCCCGCCATCTC-3′
    PA0623_sense5′-CCGAGAAGCGCTGAATTTCT-3′
    PA0623_antisense5′-CCATTGAAAGCGCTCTGGTC-3′
    PA3617_sense5′-GTGAAGAACAAGGTTTCCCCG-3′
    PA3617_antisense5′-GAGGATCTGGAACTCGGCCT-3′
    PA3866_sense5′-CCACTTGTCGTGACCAGAGGA-3′
    PA3866_antisense5′-CATCGACCCAGGCTCGTAA-3′
    rplF_sense5′-AGGTTGCTGCCGAAATTCG-3′
    rplF_antisense5′-CTTGCCTTTGTAAGGCTCCG-3′
  • TABLE 3.

    MICs of different antimicrobials for various strains of P. aeruginosa grown in LB medium

    StrainMIC (μg/ml)a
    CIPENONORNALAMKFEPGAT
    H1030.060.30.1515.60.40.61.75
    prtR::lacZ0.060.30.1531.250.40.60.875
    PA0613::lacZ0.51.6>2.52500.40.60.875
    PA0620::lux0.51.6>2.52500.41.250.875
    PA0621::lacZ0.5>5>2.52500.20.30.875
    PA0641::lux0.51.61.251250.41.251.75
    recA::phoA0.53.2>2.52500.40.60.875
    PA3866::lux0.060.30.1531.250.40.3ND
    • ↵ a Results shown are the mode of four independent experiments. CIP, ciprofloxacin; ENO, enofloxacin; NOR, norfloxacin; NAL, naldixic acid; AMK, amikacin; FEP, cefepime; GAENT, gentamicin; ND, not determined.

  • TABLE 4.

    Pyocin/phage operon and related genes induced by 0.3× and 1× MIC of ciprofloxacina

    ORFGene namebChange (n-fold) with 0.3× MICChange (n-fold) with 1× MICDescription
    PA0610 prtN 2.06.8Transcriptional activator
    PA0611 prtR 1.33.0Transcriptional repressor
    PA0612—c8.5Homolog of Zn2+ finger protein
    PA06134.019.3Conserved hypothetical
    PA0614 Hol 3.315.3Holin
    PA06151.77.2Conserved hypothetical
    PA0616 VR2 2.913.0Homologous to baseplate assembly protein V
    PA0617 WR2 3.013.9Homologous to baseplate assembly protein W
    PA0618 JR2 2.110.0Homologous to baseplate assembly protein J
    PA0619 IR2 3.214.7Homologous to tail protein I
    PA0620 HR2 2.712.1Homologous to tail fiber protein H
    PA06214.316.7Homologous to tail fiber assembly protein
    PA0622 FIR2 2.410.3Homologous to contractile sheath protein FI
    PA0623 FIIR2 2.912.8Homologous to tail tube protein FII
    PA06242.712.8Conserved hypothetical
    PA06252.514.1Homologous to tail length determination protein
    PA0626 UR2 1.89.8Homologous to tail formation protein U
    PA0627 XR2 2.310.8Homologous to tail protein X
    PA0628 DR2 1.810.0Homologous to tail formation protein D
    PA0629 Lys 2.28.7Lytic protein; homology to predicted chitinase
    PA06301.610.6Hypothetical protein
    PA06312.416.2Unique hypothetical protein
    PA06323.421.2Unique hypothetical protein
    PA0633 VF2 4.316.4Homologous to major tail protein V
    PA06343.215.8Unique hypothetical protein
    PA06352.015.9Conserved hypothetical protein
    PA0636 HF2 2.110.0Homologous to tail length determination protein H
    PA0637 MF2 2.711.0Homologous to tail fiber protein M
    PA0638 LF2 —8.5Homologous to tail fiber protein L
    PA0639 KF2 3.015.9Homologous to tail assembly protein K
    PA0640 IF2 3.116.4Homologous to tail assembly protein I
    PA0641 JF2 2.49.8Homologous to tail fiber protein J
    PA06422.712.9Hypothetical protein
    PA06431.98.9Homologous to tail fiber domain protein
    PA06444.018.0Hypothetical protein
    PA06451.815.8Hypothetical protein
    PA06463.113.4Homologous to putative tail fiber protein
    PA06473.823.0Conserved hypothetical protein
    PA0648—8.2Conserved hypothetical protein
    PA0985 pys5 4.518.1Pyocin S5
    PA1150 pys2 —5.4Pyocin S2
    PA3617 recA 2.84.6Recombinase for DNA recombination and repair
    PA3866 pys4 13.951.3Pyocin S4
    • ↵ a Only genes identified as being affected by subinhibitory (0.3 μg/ml) or inhibitory (1 μg/ml) ciprofloxacin relative to untreated strain H103 and that were of interest in this study are included. A list of all genes identified as being affected by this concentration of ciprofloxacin and exhibiting a statistically significant change (P ≤ 0.05) is available in the supplemental material. Genes are identified by ORF designation, gene name or alternative gene name, and homology description based on the Pseudomonas genome project (www.pseudomonas.com ).

    • ↵ b Genes were named as per Table 1 of Nakayama et al. (21) and reflect the homology observed by these authors to phages P2 and λ.

    • ↵ c —, no significant change in expression.

  • TABLE 5.

    Comparison of expression changes for various pyocin/phage-related open reading frames as analyzed by relative real-time PCR and custom P. aeruginosa microarray

    ORFGene NameChange (n-fold) in PAO1 strain H103 at 0.3× MIC of ciprofloxacin
    Custom microarrayReal-time PCR
    PA0610 prtN 2.010.0
    PA0611 prtR 1.311.4
    PA06214.33.0
    PA0623 FIIR2 2.93.7
    PA3617 recA 2.83.9
    PA3866 pys3 13.922.5

Additional Files

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  • HTML Page - index.htslp

    Files in this Data Supplement:

    • Supplemental file 1 - List of up- and down-regulated genes induced by ciprofloxacin in Pseudomonas aeruginosa
      Excel document, 186K.
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Ciprofloxacin Induction of a Susceptibility Determinant in Pseudomonas aeruginosa
Michelle D. Brazas, Robert E. W. Hancock
Antimicrobial Agents and Chemotherapy Jul 2005, 49 (8) 3222-3227; DOI: 10.1128/AAC.49.8.3222-3227.2005

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Ciprofloxacin Induction of a Susceptibility Determinant in Pseudomonas aeruginosa
Michelle D. Brazas, Robert E. W. Hancock
Antimicrobial Agents and Chemotherapy Jul 2005, 49 (8) 3222-3227; DOI: 10.1128/AAC.49.8.3222-3227.2005
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KEYWORDS

anti-infective agents
ciprofloxacin
Gene Expression Regulation, Bacterial
Pseudomonas aeruginosa

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