Efflux-mediated response of Staphylococcus aureus exposed to ethidium bromide

Journal of Antimicrobial Chemotherapy

Volumn 62, Issue 3, 2008, Pages 504-513

  Couto, Isabel ^a,b   Costa, Sofia Santos ^a   Viveiros, Miguel ^a   Martins, Marta ^a   Amaral, Leonard ^a  

^a INSTITUTO DE HIGIENE E MEDICINA TROPICAL   (Portugal)

^b UNIVERSIDADE NOVA DE LISBOA   (Portugal)

Author keywords

Efflux pumps; NorA; Overexpression; Staphylococci

Indexed keywords

BACTERIAL DNA; BIOCIDE; CARRIER PROTEIN; CEFOTAXIME; CHLORAMPHENICOL; CHLORPROMAZINE; CIPROFLOXACIN; DNA TOPOISOMERASE (ATP HYDROLYSING) A; ERYTHROMYCIN; ETHIDIUM BROMIDE; FUSIDIC ACID; GENTAMICIN; NALIDIXIC ACID; NORFLOXACIN; OXACILLIN; PENICILLIN G; PROTEIN NORA; PROTEIN PARC; QUINOLINE DERIVED ANTIINFECTIVE AGENT; RESERPINE; RIFAMPICIN; TETRACYCLINE; THIORIDAZINE;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL MUTATION; BACTERIAL STRAIN; BACTERIAL TRANSLOCATION; CONTROLLED STUDY; DNA SEQUENCE; FLUOROMETRY; GENE DELETION; GENE EXPRESSION; GENE OVEREXPRESSION; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PROGENY; PROMOTER REGION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STAPHYLOCOCCUS AUREUS; STRAIN DIFFERENCE;

ADAPTATION, PHYSIOLOGICAL; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BASE SEQUENCE; CARRIER PROTEINS; CHLORPROMAZINE; DNA GYRASE; DNA, BACTERIAL; DRUG RESISTANCE, BACTERIAL; ENZYME INHIBITORS; ETHIDIUM; FLUORESCENT DYES; GENE EXPRESSION PROFILING; MICROBIAL SENSITIVITY TESTS; MOLECULAR SEQUENCE DATA; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; POLYMERASE CHAIN REACTION; PROMOTER REGIONS (GENETICS); RESERPINE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SEQUENCE DELETION; STAPHYLOCOCCUS AUREUS; THIORIDAZINE;

EID: 49649085104     PISSN: 03057453     EISSN: 14602091     Source Type: Journal    
DOI: 10.1093/jac/dkn217     Document Type: Article

References (48)

1. Lowy FD. Antimicrobial resistance: The example of Staphylococcus aureus. J Clin Invest 2003; 111: 1265-73.
2. Poole K. Efflux pumps as antimicrobial resistance mechanisms. Ann Med 2007; 39: 162-76.
3. Yoshida H, Bogaki M, Nakamura S et al. Nucleotide sequence and characterization of the Staphylococcus aureus norA gene, which confers resistance to quinolones. J Bacteriol 1990; 172: 6942-9.
4. Truong-Bolduc QC, Dunman PM, Strahilevitz J et al. MgrA is a multiple regulator of two new efflux pumps in Staphylococcus aureus. J Bacteriol 2005; 187: 2395-405.
5. Truong-Bolduc QC, Strahilevitz J, Hooper DC. NorC a new efflux pump regulated by MgrA of Staphylococcus aureus. Antimicrob Agents Chemother 2006; 50: 1104-7.
6. Huang J, O'Toole P, Shen W et al. Novel chromosomally encoded multidrug efflux transporter MdeA in Staphylococcus aureus. Antimicrob Agents Chemother 2004; 48: 909-17.
7. Yamada Y, Hideka K, Shiota S et al. Gene cloning and characterization of SdrM, a chromosomally-encoded multidrug efflux pump, from Staphylococcus aureus. Biol Pharm Bull 2006; 29: 554-6.
8. Tennent JM, Lyon BR, Gillespie MT et al. Cloning and expression of Staphylococcus aureus plasmid-mediated quaternary ammonium resistance in Escherichia coli. Antimicrob Agents Chemother 1985; 27: 79-83.
9. Kaatz GW, McAleese F, Seo SM. Multidrug resistance in Staphylococcus aureus due to overexpression of a novel multidrug and toxin extrusion (MATE) transport protein. Antimicrob Agents Chemother 2005; 49 1857-64.
10. Narui K, Noguchi N, Wakasugi K et al. Cloning and characterization of a novel chromosomal drug efflux gone in Staphylococcus aureus. Biol Pharm Bull 2002; 25: 1533-6.
11. Paulsen IT, Brown MH, Dunstan SJ et al. Molecular characterization of the staphylococcal multidrug resistance export protein QacC. J Bacteriol 1995; 177: 2827-33.
12. Kaatz GW, Sao SM, Ruble CA. Efflux-mediated fluoroquinolones resistance in Staphylococcus aureus. Antimicrob Agents Chemother 1993; 37 1086-94.
13. Neyfakh AA, Borsch CM, Kaatz GW. Fluoroquinolone resistance protein NorA of Staphylococcus aureus is a multdrug efflux transporter. Antimicrob Agents Chemother 1993; 37: 128-9.
14. Kristiansen MM, Leandro C, Ordway D et al. Phenothiazines alter resistance of methicillin-resistant strains of Staphylococcus aureus (MRSA) to oxacillin in vitro. Int J Antimicrob Agents 2003; 22: 250-3.
15. Kristiansen MM, Leandro C, Ordway D et al. Thioridazine reduces resistance of methicillin-resistant Staphylococcus aureus by inhibiting a reserpine-sensitive efflux pump. In Vivo 2006; 20 361-6.
16. Kaatz GW, Mougdal VV, Seo SM et al. Phenothiazines and thioxanthenes inhibit multidrug efflux pump activity in Staphylococcus aureus. Antimicrob Agents Chemother 2003; 47: 719-26.
17. Viveiros M, Portugal I, Bettencourt R et al. Isoniazid-induced transient high-level resistance in Mycobacterium tuberculosis. Antimicrob Agents Chemother 2002; 46: 2804-10.
18. Viveiros M, Jesus A, Brito M et al. Inducement and reversal of tetracycline resistance in Escherichia coli K-12 and expression of proton gradient-dependent multidrug efflux pump genes. Antimicrob Agents Chemother 2005; 49: 3578-82.
19. Martins A, Couto I, Aagaard L et al. Prolonged exposure of methicillin-resistant Staphylococcus aureus (MRSA) COL strain to increasing concentrations of oxacillin results in a multidrug-resistant phenotype. Int J Antimicrob Agents 2007; 29: 302-5.
20. Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing: Sixteenth Informational Supplement M100-S16. CLSI, Wayne, PA, USA, 2006.
21. Andrews JM for the BSAC Working Party on Susceptibility Testing. BSAC standardized disc testing method (version 4). J Antimicrob Chemother 2005; 56: 60-76.
22. Marquez B. Bacterial efflux systems and efflux pumps inhibitors. Biochimie 2005; 87: 1137-47.
23. Chung M, Lencastre H, Matthews P et al. Molecular typing of methicillin-resistant Staphylocoocus aureus by pulsed-field gel electrophoresis: Comparison of results obtained in a multilaboratory effort using identical protocols and MRSA strains. Microb Drug Resist 2000; 6: 189-98.
24. Bjorland J, Sunde M, Waage S. Plasmid-bome smr gene causes resistance to quaternary ammonium compounds in bovine Staphylococcus aureus. J Clin Microbiol 2001; 39: 3999-4004.
25. Langmann T, Mauerer R, Zahn A et al. Real-time reverse transcription-PCR expression profiling of the complete human ATP-binding cassette transporter superfamily in various tissues. Clin Chem 2003; 49: 230-8.
26. Martins M, Santos B, Martins A et al. An instrument-free method for the demonstration of efflux pump activity of bacteria. In Vivo 2006; 20: 657-64.
27. Viveiros M, Martins A, Paixão L et al. Demonstration of intrinsic efflux activity of E. coli K-12 AG100 by an automated ethidium bromide method. Int J Antimicrob Agents 2008; 31: 458-62.
28. EUCAST Clinical MIC breakpoint - fluoroquinolones. EUCAST Website (v2.4). http://www.srga.org/eucastwt/MICTAB/MICquinolones.htm (25 March 2008, date last accessed).
29. Ferrero L, Cameron B, Crouzet J. Analysis of gyrA and grlA mutations in stepwise-selected ciprofloxacin-resistant mutants of Staphylococcus aureus. Antimicrob Agents Chemother 1995; 39: 1554-8.
30. Horii T, Suzuki Y, Monji A et al. Detection of mutations in quinolone resistance-determining regions in levofloxacin- and methicillin-resistant Staphylococcus aureus: Effects of the mutations on fluoroquinolone MICs. Diagn Microbiol Infect Dis 2003; 46: 139-45.
31. Hooper DC. Mechanisms of fluoroquinolone resistance. Drug Resist Updat 1999; 2: 38-55.
32. Ng EYW, Trucksis M, Hooper DC. Quinolone resistance mediated by norA physiologic characterization and relationship to flqB, a quinolone resistance locus on the Staphylococcus aureus chromossome. Antimicrob Agents Chemother 1994; 38: 1345-55.
33. Fournier B, Truong-Bolduc Q, Zhang X et al. A mutation in the 5′ untranslated region increases stability of norA mRNA, encoding a multidrug resistance transporter of Staphylococcus aureus. J Bacteriol 2001; 183: 2367-71.
34. Viveiros M, Dupont M, Rodrigues L et al. Antibiotic stress, genetic response and altered permeability of E. coli. PLoS ONE 2007; 2: E365.
35. Brown MH, Skurray RA. Staphylococcal multidrug efflux protein QacA. J Mol Microbiol Biotechnol 2001; 3: 163-70.
36. Heir E, Sundheim G, Holck AL. The qacG gene on plasmid pST94 confers resistance to quaternary ammonium compounds in staphylococci isolated from the food industry. J Appl Microbiol 1999; 86: 378-88.
37. Kazama H, Harnashima H, Sasatsu M et al. Distribution of the antiseptic-resistance gone qacEΔ1 in Gram-positive bacteria. FEMS Microbiol Lett 1998; 165: 295-9.
38. Heir E, Sundheim G, Holck AL. The Staphylococcus qacH gene product: A new member of the SMR family encoding multidrug resistance. FEMS Microbiol Lett 1998; 163: 49-56.
39. DeMarco CE, Cushing LA, Frempong-Manso E et al. Efflux-related resistance to norfloxacin, dyes, and biocides in bloodstream isolates of Staphylococcus aureus. Antimicrob Agents Chemother 2007; 51: 3235-9.
40. Schmitz F-J, Hertel B, Hofmann B et al. Relationship between mutations in the coding and promoter regions of the norA genes in 42 unrelated clinical isolates of Staphylococcus aureus and the MICs of norfloxacin for these strains. J Antimicrob Chemother 1998; 42: 561-3.
41. Tanaka M, Wang T, Onodera Y et al. Mechanism of quinolone resistance in Staphylococcus aureus. J Infect Chemother 2000; 6 131-9.
42. DeMarco CE, Frempong-Manso E, Sao SM et al. Multidrug efflux-pump (MDEP) gene expression in geographically diverse Staphylococcus aureus (SA) strains. In: Proceedings of the 47th Interscience Conference on Antimicrobial Agents and Chemotherapy (ICAAC), Chicago, IL, 2007. Abstract C2-192, p. 113. American Society for Microbiology, Washington, DC, USA.
43. Kaatz GW, Seo SM. Inducible NorA-mediated multidrug resistance in Staphyloooccus aureus. Antimicrob Agents Chemother 1995; 39: 2650-5.
44. Garvey MI, Piddock LJV. The efflux pump inhibitor reserpine selects multidrug resistant Streptococcus pneumoniae that over-express the ABC transporters PatA and PatB. Antimicrob Agents Chemother 2008; 52: 1677-85.
45. Anthonisen I-L, Sunde M, Steinum TM et al. Organization of the antiseptic resistance gene qacA and Tn552-related β-lactamase genes in multidrug-resistant Staphylococcus haemolyticus strains of animal and human origins. Antimicrob Agents Chemother 2002; 46: 3606-12.
46. Sierra JM, Ruiz J, Anta MTJ et al. Prevalence of two different genes encoding NorA in 23 clinical strains of Staphylococcus aureus. J Antimicrob Chemother 2000; 46: 145-6.
47. Lane DJ. 16S/23S rRNA sequencing. In: Stackebrant E, Goodfellow M, eds. Nucleic Acid Techniques in Bacterial Systematics. London: John Wiley & Sons Ltd, 1991; 115-75.
48. Pan X, Hamlyn P, Talens-Visconti R et al. Small-oolony mutants of Staphylococcus aureus allow selection of gyrase-mediated resistance to dual-target fluoroquinolones. Antimicrob Agents Chemother 2002; 46: 2498-506.