Phenylpiperidine selective serotonin reuptake inhibitors interfere with multidrug efflux pump activity in Staphylococcus aureus

International Journal of Antimicrobial Agents

Volumn 22, Issue 3, 2003, Pages 254-261

  Kaatz, Glenn W ^a   Moudgal, Varsha V ^a   Seo, Susan M ^a   Hansen, John Bondo ^b   Kristiansen, Jette E ^c  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NOVO NORDISK A S   (Denmark)

^c Klinisk Mikrobiologisk Afdeling   (Denmark)

Author keywords

Efflux; Ethidium; Fluoroquinolone; Paroxetine; Staphylococcus aureus

Indexed keywords

3 (3,4 METHYLENEDIOXYPHENOXYMETHYL) 4 (4 FLUOROPHENYL)PIPERIDINE; 3 (3,4 METHYLENEDIOXYPHENOXYMETHYL) 4 (4 FLUOROPHENYL)PIPERIDINE MALEATE; 3 (4 METHOXYPHENOXYMETHYL) 1 METHYL 4 PHENYLPIPERIDINE; ACRIFLAVINE; ETHIDIUM; FEMOXETINE; NNC 20 4962; NNC 20 4963; NNC 20 7051; NNC 20 7052; NORFLOXACIN; PAROXETINE; PIPERIDINE DERIVATIVE; PYRONINE; SEROTONIN UPTAKE INHIBITOR; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DRUG INHIBITION; DRUG SELECTIVITY; EFFUSION; IC 50; MINIMUM INHIBITORY CONCENTRATION; MULTIDRUG RESISTANCE; NONHUMAN; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; PUMP; STAPHYLOCOCCUS AUREUS;

EID: 0042835371     PISSN: 09248579     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0924-8579(03)00220-6     Document Type: Article

References (38)

1. Poole K., Srikumar R. Multidrug efflux in Pseudomonas aeruginosa: components, mechanisms and clinical significance. Curr. Top. Med. Chem. 1:2001;59-71.
2. Li X.-Z., Nikaido H., Poole K. Role of MexA-MexB-OprM in antibiotic efflux in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 39:1995;1948-1953.
3. Van Bambeke F., Balzi E., Tulkens P.M. Antibiotic efflux pumps. Biochem. Pharmacol. 60:2000;457-470.
4. Paulsen I.T., Brown M.H., Skurray R.A. Proton-dependent multidrug efflux systems. Microbiol. Rev. 60:1996;575-608.
5. Noguchi N., Hase M., Kitta M., Sasatsu M., Deguchi K., Kono M. Antiseptic susceptibility and distribution of antiseptic-resistance genes in methicillin-resistant Staphylococcus aureus. FEMS Microbiol. Lett. 172:1999;247-253.
6. Kuroda M., Ohta T., Uchiyama I., et al. Whole genome sequencing of methicillin-resistant Staphylococcus aureus. Lancet. 357:2001;1225-1240.
7. Kaatz G.W., Seo S.M., O'Brien L., Wahiduzzaman M., Foster T.J. Evidence for the existence of a multidrug efflux transporter distinct from norA in Staphylococcus aureus. Antimicrob. Agents Chemother. 44:2000;1404-1406.
8. Kaatz G.W., Moudgal V.V., Seo S.M. Identification and characterization of a novel efflux-related multidrug resistance phenotype in Staphylococcus aureus. J. Antimicrob. Chemother. 50:2002;833-838.
9. Lomovskaya O., Warren M.S., 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. 45:2001;105-116.
10. Griffith D, Lomovskaya O, Lee V, Dudley M. Potentiation of levofloxacin by a broad-spectrum efflux pump inhibitor in mouse models of infection caused by Pseudomonas aeruginosa. In: Proceedings of the 39th Interscience Conference on Antimicrobial Agents and Chemotherapy; 1999 September 26-29; San Francisco, California, USA. Washington DC: American Society for Microbiology.
11. Ng E.Y.W., Trucksis M., Hooper D.C. Quinolone resistance mediated by norA: physiologic characterization and relationship to flqB, a quinolone resistance locus on the Staphylococcus aureus chromosome. Antimicrob. Agents Chemother. 38:1994;1345-1355.
12. Aeshlimann J.R., Dresser L.D., Kaatz G.W., Rybak M.J. Effects of NorA inhibitors on in vitro antibacterial activities and postantibiotic effects of levofloxacin, ciprofloxacin, and norfloxacin in genetically related strains of Staphylococcus aureus. Antimicrob. Agents Chemother. 43:1999;335-340.
13. Aeshlimann J.R., Kaatz G.W., Rybak M.J. The effects of NorA inhibition on the activities of levofloxacin, ciprofloxacin, and norfloxacin against two genetically related strains of Staphylococcus aureus in an in-vitro infection model. J. Antimicrob. Chemother. 44:1999;343-349.
14. Markham P.N., Westhaus E., Klyachko K., Johnson M.E., Neyfakh A.A. Multiple novel inhibitors of the NorA multidrug transporter of Staphylococcus aureus. Antimicrob. Agents Chemother. 43:1999;2404-2408.
15. Guz N.R., Stermitz F.R., Johnson J.B., et al. Flavonolignan and flavone inhibitors of a Staphylococcus aureus multidrug resistance pump: structure-activity relationships. J. Med. Chem. 44:2001;261-268.
16. Kristiansen J.E., Mortensen I., Gaarslev K. The antibiotic effect of the anti-depressive drug femoxetine and its stereo-isomeric analogs on diarrhoea-producing enterobacteriaceae. Acta Pathol. Microbiol. Immunol. Scand. 94:1986;103-106.
17. Kristiansen J.E. The antimicrobial activity of psychotherapeutic drugs and stereo-isomeric analogues. Dan. Med. Bull. 37:1990;165-182.
18. Kristiansen J.E., Bondo Hansen J. Inhibition of HIV replication by neuroleptic agents and their potential use in HIV infected patients with AIDS related dementia. Int. J. Antimicrob. Agents. 14:2000;209-213.
19. Munoz-Bellido J.L., Munoz-Criado S., Garcia-Rodriguez J.A. Antimicrobial activity of psychotropic drugs - selective serotonin reuptake inhibitors. Int. J. Antimicrob. Agents. 14:2000;177-180.
20. Lass-Flörl C., Dierich M.P., Fuchs D., Semenitz E., Jenewein I., Ledochowski M. Antifungal properties of selective serotonin reuptake inhibitors against Aspergillus species in vitro. J. Antimicrob. Chemother. 48:2001;775-779.
21. National Committee for Clinical Laboratory Standards. Approved standard M7-A5. In: Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically, 5th ed. Villanova, PA: National Committee for Clinical Laboratory Standards, 1999.
22. Eliopoulos G.M., Moellering R.C. Antimicrobial combinations. Lorian V. Antibiotics in laboratory medicine. 1991;432-492 Williams and Wilkins, Baltimore.
23. Kaatz G.W., Moudgal V.V., Seo S.M., Kristiansen J.E. Phenothiazines and thioxanthenes inhibit multidrug efflux pump activity in Staphylococcus aureus. Antimicrob. Agents Chemother. 47:2002;719-726.
24. Mates S.M., Eisenberg E.S., Mandel L.J., Patel L., Kaback H.R., Miller M.H. Membrane potential and gentamicin uptake in Staphylococcus aureus. Proc. Natl. Acad. Sci. USA. 79:1982;6693-6697.
25. Rottenberg H. The measurement of membrane potential and ΔpH in cells, organelles, and vesicles. Methods Enzymol. 55:1979;547-569.
26. Sridhar K.S., Krishnan A., Samy T.S., et al. Prochlorperazine as a doxorubicin-efflux blocker: phase I clinical and pharmacokinetic studies. Cancer Chemother. Pharmacol. 31:1993;423-430.
27. Sridhar K.S., Krishnan A., Samy T.S., et al. Phase I and pharmacokinetics studies of prochlorperazine 2-h i.v. infusion as a doxorubicin-efflux blocker. Cancer Chemother. Pharmacol. 34:1994;377-384.
28. Nikaido H. Preventing drug access to targets: cell surface permeability barriers and active efflux in bacteria. Semin. Cell Dev. Biol. 12:2001;215-223.
29. Ahmed M., Borsch C.M., Neyfakh A.A., Schuldiner S. Mutants of the Bacillus subtilis multidrug transporter Bmr with altered susceptibility to the antihypertensive alkaloid reserpine. J. Biol. Chem. 268:1993;11086-11089.
30. Smith D.F. The stereoselectivity of serotonin uptake in brain tissue and blood platelets: the topography of the serotonin uptake area. Neurosci. Biobehav. Rev. 10:1986;37-46.
31. Engelsoft M., Bondo Hansen J. Synthesis and 5HT modulating activity of stereoisomers of 3-phenoxymethyl-4-phenylpiperidines. Acta Chem. Scand. 50:1996;164-169.
32. Hiemke C., Härtter S. Pharmacokinetics of selective serotonin reuptake inhibitors. Pharmacol. Ther. 85:2000;11-28.
33. Kaatz G.W., Barriere S.L., Schaberg D.R., Fekety R. The emergence of resistance to ciprofloxacin during therapy of experimental methicillin-susceptible Staphylococcus aureus endocarditis. J. Antimicrob. Chemother. 20:1987;753-758.
34. Kaatz G.W., Seo S.M., Ruble C.A. Efflux-mediated fluoroquinolone resistance in Staphylococcus aureus. Antimicrob. Agents Chemother. 37:1993;1086-1094.
35. Novick R.P. Properties of a cryptic high-frequency transducing phage in Staphylococcus aureus. Virology. 33:1963;155-166.
36. Matsuda N., Ohya S. Cross-resistance to meropenem, cephems, and quinolones in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 36:1992;1847-1851.
37. De Kievit T.R., Parkins M.D., Gillis R.J., et al. Multidrug efflux pumps: expression patterns and contribution to antibiotic resistance in Pseudomonas aeruginosa biofilms. Antimicrob. Agents Chemother. 45:2001;1761-1770.
38. Okusu H., Ma D., Nikaido H. AcrAB efflux pump plays a major role in the antibiotic resistance phenotype of Escherichia coli multiple-antibiotic-resistance (Mar) mutants. J. Bacteriol. 178:1996;306-308.