Optimized Nile red efflux assay of AcrAB-TolC multidrug efflux system shows competition between substrates

Antimicrobial Agents and Chemotherapy

Volumn 54, Issue 9, 2010, Pages 3770-3775

  Bohnert, Jürgen A ^a,b   Karamian, Brian ^a   Nikaido, Hiroshi ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

1 NAPHTHYLMETHYLPIPERAZINE; ANTIINFECTIVE AGENT; AZITHROMYCIN; CARBONYL CYANIDE CHLOROPHENYLHYDRAZONE; CHLORTETRACYCLINE; DOXORUBICIN; DOXYCYCLINE; DYE; GLUCOSE; HYBRID PROTEIN; LINEZOLID; MINOCYCLINE; NAPHTHALENE DERIVATIVE; NILE RED DYE; PHENYLALANYLARGININE BETA NAPHTHYLAMIDE; PIPERAZINE DERIVATIVE; PROTEIN ACRAB TOLC; PROTON; PROTON PUMP INHIBITOR; TETRACYCLINE; TETRAPHENYLPHOSPHONIUM; TOLC PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BIOASSAY; CANDIDA ALBICANS; CONDUCTOR; DRUG COMPETITION; DRUG INHIBITION; DRUG TRANSPORT; ENERGY; LIPOPHILICITY; MULTIDRUG RESISTANCE; NONHUMAN; PHARMACODYNAMICS; PRIORITY JOURNAL; PUMP DESIGN;

ANTI-BACTERIAL AGENTS; CARBONYL CYANIDE M-CHLOROPHENYL HYDRAZONE; CHLORTETRACYCLINE; DIPEPTIDES; DOXORUBICIN; DOXYCYCLINE; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MINOCYCLINE; ONIUM COMPOUNDS; ORGANOPHOSPHORUS COMPOUNDS; TETRACYCLINE;

EID: 77956099483     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00620-10     Document Type: Article

References (33)

1. Aires, J. R., and H. Nikaido. 2005. Aminoglycosides are captured from both periplasm and cytoplasm by the AcrD multidrug efflux transporter of Escherichia coli. J. Bacteriol. 187:1923-1929.
2. Bohnert, J. A., and W. V. Kern. 2005. Selected arylpiperazines are capable of reversing multidrug resistance in Escherichia coli overexpressing RND efflux pumps. Antimicrob. Agents Chemother. 49:849-852.
3. Bohnert, J. A., S. Schuster, M. A. Seeger, E. Fahnrich, K. M. Pos, and W. V. Kern. 2008. Site-directed mutagenesis reveals putative substrate binding residues in the Escherichia coli RND efflux pump AcrB. J. Bacteriol. 190: 8225-8229.
4. Elkins, C. A., and L. B. Mullis. 2007. Substrate competition studies using whole-cell accumulation assays with the major tripartite multidrug efflux pumps of Escherichia coli. Antimicrob. Agents Chemother. 51:923-929.
5. Greenspan, P., and S. D. Fowler. 1985. Spectrofluorometric studies of the lipid probe, Nile Red. J. Lipid Res. 26:781-789.
6. Ivnitski-Steele, I., A. R. Holmes, E. Lamping, B. C. Monk, R. D. Cannon, and L. A. Sklar. 2009. Identification of Nile Red as a fluorescent substrate of the Candida albicans ATP-binding cassette transporters Cdr1p and Cdr2p and the major facilitator superfamily transporter Mdr1p. Anal. Biochem. 394: 87-91.
7. Jellen-Ritter, A. S., and W. V. Kern. 2001. Enhanced expression of the multidrug efflux pumps AcrAB and AcrEF associated with insertion element transposition in Escherichia coli mutants selected with a fluoroquinolone. Antimicrob. Agents Chemother. 45:1467-1472.
8. Kashket, E. R. 1985. The proton motive force in bacteria: a critical assessment of methods. Annu. Rev. Microbiol. 39:219-242.
9. Kern, W. V., M. Oethinger, A. S. Jellen-Ritter, and S. B. Levy. 2000. Nontarget gene mutations in the development of fluoroquinolone resistance in Escherichia coli. Antimicrob. Agents Chemother. 44:814-820.
10. Klyachko, K. A., S. Schuldiner, and A. A. Neyfakh. 1997. Mutations affecting substrate specificity of the Bacillus subtilis multidrug transporter Bmr. J. Bacteriol. 179:2189-2193.
11. Koronakis, V., A. Sharff, E. Koronakis, B. Luisi, and C. Hughes. 2000. Crystal structure of the bacterial membrane protein TolC central to multidrug efflux and protein export. Nature 405:914-919. (Pubitemid 30435040)
12. Lim, S. P., and H. Nikaido. 2010. Kinetic parameters of efflux of penicillins by the multidrug efflux transporter acrab-tolc of Escherichia coli. Antimicrob. Agents Chemother. 54:1800-1806.
13. 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.
14. Mikolosko, J., K. Bobyk, H. I. Zgurskaya, and P. Ghosh. 2006. Conformational flexibility in the multidrug efflux system protein AcrA. Structure 14: 577-587. (Pubitemid 43363490)
15. Murakami, S., R. Nakashima, E. Yamashita, T. Matsumoto, and A. Yamaguchi. 2006. Crystal structures of a multidrug transporter reveal a functionally rotating mechanism. Nature 443:173-179. (Pubitemid 44387601)
16. Murakami, S., R. Nakashima, E. Yamashita, and A. Yamaguchi. 2002. Crystal structure of bacterial multidrug efflux transporter AcrB. Nature 419:587-593.
17. Murakami, S., N. Tamura, A. Saito, T. Hirata, and A. Yamaguchi. 2004. Extramembrane central pore of multidrug exporter AcrB in Escherichia coli plays an important role in drug transport. J. Biol. Chem. 279:3743-3748.
18. Nagano, K., and H. Nikaido. 2009. Kinetic behavior of the major multidrug efflux pump acrb of Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 106: 5854-5858.
19. Nikaido, H. 1998. Multiple antibiotic resistance and efflux. Curr. Opin. Microbiol. 1:516-523.
20. Nishino, K., and A. Yamaguchi. 2001. Analysis of a complete library of putative drug transporter genes in Escherichia coli. J. Bacteriol. 183:5803-5812. (Pubitemid 32917397)
21. Nishino, K., and A. Yamaguchi. 2002. EvgA of the two-component signal transduction system modulates production of the yhiUV multidrug transporter in Escherichia coli. J. Bacteriol. 184:2319-2323.
22. Ocaktan, A., H. Yoneyama, and T. Nakae. 1997. 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. 272:21964-21969.
23. Okusu, H., D. Ma, and H. Nikaido. 1996. AcrAB efflux pump plays a major role in the antibiotic resistance phenotype of Escherichia coli multiple-antibiotic-resistance (mar) mutants. J. Bacteriol. 178:306-308.
24. Purdy, D. R., and A. L. Koch. 1976. Energy cost of galactoside transport to Escherichia coli. J. Bacteriol. 127:1188-1196.
25. Renau, T. E., R. Leger, E. M. Flamme, J. Sangalang, M. W. She, R. Yen, C. L. Gannon, D. Griffith, S. Chamberland, O. Lomovskaya, S. J. Hecker, V. J. Lee, T. Ohta, and K. Nakayama. 1999. Inhibitors of efflux pumps in Pseudomonas aeruginosa potentiate the activity of the fluoroquinolone antibacterial levofloxacin. J. Med. Chem. 42:4928-4931.
26. Rotman, B. 1977. On the rate limiting step in downhill transport via the LacY permease of Escherichia coli. J. Supramol. Struct. 7:29-35.
27. Seeger, M. A., A. Schiefner, T. Eicher, F. Verrey, K. Diederichs, and K. M. Pos. 2006. Structural asymmetry of AcrB trimer suggests a peristaltic pump mechanism. Science 313:1295-1298.
28. Sennhauser, G., P. Amstutz, C. Briand, O. Storchenegger, and M. G. Grutter. 2007. Drug export pathway of multidrug exporter AcrB revealed by DARPin inhibitors. PLoS. Biol. 5:e7.
29. Sulavik, M. C., C. Houseweart, C. Cramer, N. Jiwani, N. Murgolo, J. Greene, B. DiDomenico, K. J. Shaw, G. H. Miller, R. Hare, and G. Shimer. 2001. Antibiotic susceptibility profiles of Escherichia coli strains lacking multidrug efflux pump genes. Antimicrob. Agents Chemother. 45:1126-1136.
30. Symmons, M. F., E. Bokma, E. Koronakis, C. Hughes, and V. Koronakis. 2009. The assembled structure of a complete tripartite bacterial multidrug efflux pump. Proc. Natl. Acad. Sci. U. S. A. 106:7173-7178.
31. Tal, N., and S. Schuldiner. 2009. A coordinated network of transporters with overlapping specificities provides a robust survival strategy. Proc. Natl. Acad. Sci. U. S. A. 106:9051-9056.
32. Takatsuka, Y., C. Chen, and H. Nikaido. 2010. Mechanism of recognition of compounds of diverse structures by the multidrug efflux pump AcrB of Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 107:6559-6565.
33. Zgurskaya, H. I., and H. Nikaido. 1999. Bypassing the periplasm: reconstitution of the AcrAB multidrug efflux pump of Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 96:7190-7195.