Phenothiazines and thioxanthenes inhibit multidrug efflux pump activity in Staphylococcus aureus

Antimicrobial Agents and Chemotherapy

Volumn 47, Issue 2, 2003, Pages 719-726

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

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

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

^c Klinisk Mikrobiologisk Afdeling   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ACRIFLAVINE; CHLORPROMAZINE; ETHIDIUM; FLUPENTIXOL; FLUPHENAZINE; PHENOTHIAZINE; PROCHLORPERAZINE; PYRONINE; THIORIDAZINE; THIOXANTHENE;

ANTIBIOTIC RESISTANCE; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL GENOME; BACTERIAL MEMBRANE; DRUG STRUCTURE; GENE SEQUENCE; IC 50; ION TRANSPORT; MEMBRANE POTENTIAL; MINIMUM INHIBITORY CONCENTRATION; MULTIDRUG RESISTANCE; PHENOTYPE; PRIORITY JOURNAL; PROTON MOTIVE FORCE; STAPHYLOCOCCUS AUREUS; STEREOISOMERISM;

DRUG RESISTANCE, MULTIPLE, BACTERIAL; GENOME, BACTERIAL; MICROBIAL SENSITIVITY TESTS; PHENOTHIAZINES; STAPHYLOCOCCUS AUREUS; THIOXANTHENES;

EID: 0037308580     PISSN: 00664804     EISSN: None     Source Type: Journal    
DOI: 10.1128/AAC.47.2.719-726.2003     Document Type: Article

References (42)

1. Aeshlimann, J. R., L. D. Dresser, G. W. Kaatz, and M. J. Rybak. 1999. 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: 335-340.
2. Ahmed, M., C. M. Borsch, A. A. Neyfakh, and S. Schuldiner. 1993. Mutants of the Bacillus subtilis multidrug transporter Bmr with altered susceptibility to the antihypertensive alkaloid reserpine. J. Biol. Chem. 268:11086-11089.
3. Crowle, A. J., G. S. Douvas, and M. H. May. 1992. Chlorpromazine: a drug potentially useful for treating mycobacterial infections. Chemotherapy 38: 410-419.
4. Dey, S., P. Hafkemeyer, I. Pastan, and M. M. Gottesman. 1999. A single amino acid residue contributes to distinct mechanisms of inhibition of the human multidrug transporter by stereoisomers of the dopamine receptor antagonist flupentixol. Biochemistry 38:6630-6639.
5. Eisenberg, E. S., L. J. Mandell, H. R. Kaback, and M. H. Miller. 1984. Quantitative association between electrical potential across the cytoplasmic membrane and early gentamicin uptake and killing in Staphylococcus aureus. J. Bacteriol. 157:863-867.
6. Eliam, Y. 1983. Membrane effects of phenothiazines in yeasts. I. Stimulation of calcium and potassium fluxes. Biochim. Biophys. Acta 733:242-248.
7. Eliopoulos, G. M., and R. C. Moellering, Jr. 1991. Antimicrobial combinations, p. 432-492. In V. Lorian (ed.), Antibiotics in laboratory medicine. Williams and Wilkins, Baltimore, Md.
8. Ford, J. M., W. C. Prozialeck, and W. N. Halt. 1989. Structural features determining activity of phenothiazines and related drugs for inhibition of cell growth and reversal of multidrug resistance. Mol. Pharmacol. 35:105-115.
9. Ford, J. M., E. P. Bruggemann, I. Pastan, M. M. Gottesman, and W. N. Hait. 1990. Cellular and biochemical characterization of thioxanthenes for reversal of multidrug resistance in human and murine cell lines. Cancer Res. 50: 1748-1756.
10. + antiporter TetA(K) from Staphylococcus aureus. J. Bacteriol. 179:3786-3789.
11. Guz, N. R., F. R. Stermitz, J. B. Johnson, T. D. Beeson, S. Willen, J.-F. Hsiang, and K. Lewis. 2001. Flavonolignan and flavone inhibitors of a Staphylococcus aureus multidrug resistance pump: structure-activity relationships. J. Med. Chem. 44:261-268.
12. Kaatz, G. W., S. L. Barriere, D. R. Schaberg, and R. Fekety. 1987. The emergence of resistance to ciprofloxacin during therapy of experimental methicillin-susceptible Staphylococcus aureus endocarditis. J. Antimicrob. Chemother. 20:753-758.
13. Kaatz, G. W., S. M. Seo, and C. A. Ruble. 1993. Efflux-mediated fluoroquinolone resistance in Staphylococcus aureus. Antimicrob. Agents Chemother. 37:1086-1094.
14. Kaatz, G. W., S. M. Seo, L. O'Brien, M. Wahiduzzaman, and T. J. Foster. 2000. Evidence for the existence of a multidrug efflux transporter distinct from norA in Staphylococcus aureus. Antimicrob. Agents Chemother. 44: 1404-1406.
15. Kaatz, G. W., V. V. Moudgal, and S. M. Seo. 2002. Identification and characterization of a novel efflux-related multidrug resistance phenotype in Staphylococcus aureus. J. Antimicrob. Chemother. 50:833-838.
16. Kristiansen, J. E., and J. Blom. 1981. Effect of chlorpromazine on the ultrastructure of Staphylococcus aureus. Acta Pathol. Microbiol. Scand. B 89:399-405.
17. Kristiansen, J. E., and I. Mortensen. 1981. Stereo-isomeric dissociation of the antibacterial and the neuroleptic effect of clopenthixol. Acta Pathol. Microbiol. Scand. B 89:437-438.
18. Kristiansen, J. E. 1990. The antimicrobial activity of psychotherapeutic drugs and stereo-isomeric analogues. Dan. Med. Bull. 37:165-182.
19. Kristiansen, J. E. 1993. Chlorpromazine: non-antibiotics with antimicrobial activity - new insights in managing resistance? Curr. Opin. Investig. Drugs 2:587-591.
20. Kristiansen, J. E., and L. Amaral. 1997. The potential management of resistant infections with non-antibiotics. J. Antimicrob. Chemother. 40:319-327.
21. Kristiansen, J. E., I. Mortensen, and B. Nissen. 1982. Membrane stabilizers inhibit potassium efflux from Staphylococcus aureus strain U2275. Biochim. Biophys. Acta 685:379-382.
22. Kuroda, M., T. Ohta, I. Uchiyama, T. Baba, H. Yuzawa, I. Kobayashi, L. Cui, A. Oguchi, K. Aoki, Y. Nagai, J. Lian, T. Ito, M. Kanamori, H. Matsumara, A., Maruyama, H. Murakami, A., Hosoyama, Y. Mizutani-Ui, N. K. Takahashi, T. Sawano, R. Inoue, C. Kaito, K. Sekimizu, H. Hirakawa, S. Kuhara, S. Goto, J. Yabuzaki, M. Kanehisa, A. Yamashita, K. Oshima, K. Furuya, C. Yoshino, T. Shiba, M. Hattori, N. Ogasawara, H. Hayashi, and K. Hiramatsu. 2001. Whole genome sequencing of methicillin-resistant Staphylococcus aureus. Lancet 357:1225-1240.
23. Li, X.-Z., H. Nikaido, and K. Poole. 1995. Role of MexA-MexB-OprM in antibiotic efflux in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 39:1948-1953.
24. Lomovskaya, O., M. S. Warren, A. Lee, J. Galazzo, R. Fronko, M. Lee, J. Blais, D. Cho, S. Chamberland, T. Renau, R. Leger, S. Hecker, W. Watkins, K. Hoshino, H. Ishida, and V. J. Lee. 2001. Identification and characterization of inhibitors of multidrug resistance efflux pumps in Pseudomonas aeruginosa: novel agents for combination therapy. Antimicrob. Agents Chemother. 45:105-116.
25. Markham, P. N., E. Westhaus, K. Klyachko, M. E. Johnson, and A. A. Neyfakh. 1999. Multiple novel inhibitors of the NorA multidrug transporter of Staphylococcus aureus. Antimicrob. Agents Chemother. 43:2404-2408.
26. Mates, S. M., E. S. Eisenberg, L. J. Mandel, L. Patel, H. R. Kaback, and M. H. Miller. 1982. Membrane potential and gentamicin uptake in Staphylococcus aureus. Proc. Natl. Acad. Sci. USA 79:6693-6697.
27. Munoz-Bellido, J. L., S. Munoz-Criado, and J. A. Garcia. 2000. Antimicrobial activity of psychotropic drugs: selective serotonin reuptake inhibitors. Int. J. Antimicrob. Agents 14:177-180.
28. National Committee for Clinical Laboratory Standards. 1999. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically, 5th ed. Approved standard M7-A5. National Committee for Clinical Laboratory Standards, Wayne, Pa.
29. 2C serotonin receptors by fluoxetine (Prozac). Proc. Natl. Acad. Sci. USA 94:2036-2040.
30. Noguchi, N., M. Hase, M. Kitta, M. Sasatsu, K. Deguchi, and M. Kono. 1999. Antiseptic susceptibility and distribution of antiseptic-resistance genes in methicillin-resistant Staphylococcus aureus. FEMS Microbiol. Lett. 172:247-253.
31. Novick, R. P. 1963. Properties of a cryptic high-frequency transducing phage in Staphylococcus aureus. Virology 33:155-166.
32. Paulsen, I. T., M. H. Brown, and R. A. Skurray. 1996. Proton-dependent multidrug efflux systems. Microbiol. Rev. 60:575-608.
33. Petersen, P. V. 1977. The thioxanthenes, p. 827-867. In E. Usdin and I. Forrest (ed.), Psychotherapeutic drugs. Marcel Dekker, New York, N.Y.
34. Poole, K., and R. Srikumar. 2001. Multidrug efflux in Pseudomonas aeruginosa: components, mechanisms and clinical significance. Curr. Top. Med. Chem. 1:59-71.
35. Rottenberg, H. 1979. The measurement of membrane potential and ΔpH in cells, organelles, and vesicles. Methods Enzymol. 55:547-569.
36. Silverman, J. A., N. Oliver, T. Andrew, and T. Li. 2001. Resistance studies with daptomycin. Antimicrob. Agents Chemother. 45:1799-1802.
37. Sridhar, K. S., A. Krishnan, T. S. Samy, A. Sauerteig, L. L. Wellam, G. V. McPhee, R. C. Duncan, S. Y. Anac, B. Ardalan, and P. W. Benedetto. 1993. Prochlorperazine as a doxorubicin-efflux blocker: phase I clinical and pharmacokinetic studies. Cancer Chemother. Pharmacol. 31:423-430.
38. , Sridhar, K. S., A. Krishnan, T. S. Samy, R. C. Duncan, A. Sauerteig, G. V. McPhee, M. E. Auguste, and P. W. Benedetto. 1994. Phase I and pharmacokinetics studies of prochlorperazine 2-h i.v. infusion as a doxorubicin-efflux blocker. Cancer Chemother. Pharmacol. 34:377-384.
39. Van Bambeke, F., E. Balzi, and P. M. Tulkens. 2000. Antibiotic efflux pumps. Biochem. Pharmacol. 60:457-470.
40. Viveiros, M., and L. Amaral. 2001. Enhancement of antibiotic activity against poly-drug resistant Mycobacterium tuberculosis by phenothiazines. Int. J. Antimicrob. Agents 17:225-228.
41. Zhang, Y., A. Scorpio, H. Nikaido, and Z. Sun. 1999. Role of acid pH and deficient efflux of pyrazinoic acid in unique susceptibility of Mycobacterium tuberculosis to pyrazinamide. J. Bacteriol. 181:2044-2049.
42. Zilberstein, D., V. Liveanu, and A. Gepstein. 1990. Tricyclic drugs reduce the proton motive force in Leishmania donovani promastigotes. Biochem. Pharmacol. 39:935-940.