Substrate competition studies using whole-cell accumulation assays with the major tripartite multidrug efflux pumps of Escherichia coli

Antimicrobial Agents and Chemotherapy

Volumn 51, Issue 3, 2007, Pages 923-929

  Elkins, Christopher A ^a   Mullis, Lisa B ^a  

^a NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACRA PROTEIN; ACRB PROTEIN; AMPICILLIN; ANTIBIOTIC AGENT; BACTERIAL PROTEIN; CARBONYL CYANIDE CHLOROPHENYLHYDRAZONE; CHLORAMPHENICOL; CHOLIC ACID; CIPROFLOXACIN; CRYSTAL VIOLET; DIRITHROMYCIN; DODECYL SULFATE SODIUM; DYE; ERYTHROMYCIN; ETHIDIUM BROMIDE; FUSIDIC ACID; JOSAMYCIN; KANAMYCIN; MACROLIDE; MEMBRANE FUSION PROTEIN; NOVOBIOCIN; OLEANDOMYCIN; PROTEIN EMRA; PROTEIN EMRB; STEROID; TAUROCHOLIC ACID; TETRACYCLINE; TOLC PROTEIN; TRITON X 100; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ARTICLE; BINDING SITE; COMPETITIVE INHIBITION; ESCHERICHIA COLI; GENE MUTATION; ION TRANSPORT; MINIMUM INHIBITORY CONCENTRATION; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; WHOLE CELL; WILD TYPE;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BINDING, COMPETITIVE; CARRIER PROTEINS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ESCHERICHIA COLI; INDICATORS AND REAGENTS; MICROBIAL SENSITIVITY TESTS; PROGESTERONE; STEROIDS;

EID: 33847616996     PISSN: 00664804     EISSN: None     Source Type: Journal    
DOI: 10.1128/AAC.01048-06     Document Type: Article

References (39)

1. Ambudkar, S. V., I. W. Kim, and Z. E. Sauna. 2006. The power of the pump: mechanisms of action of P-glycoprotein (ABCB1). Eur. J. Pharm. Sci. 27:392-400.
2. Baranova, N., and H. Nikaido. 2002. The BaeSR two-component regulatory system activates transcription of the yegMNOB (mdtABCD) transporter gene cluster in Escherichia coli and increases its resistance to novobiocin and deoxycholate. J. Bacteriol. 184:4168-4176.
3. Baron, S. F., and P. B. Hylemon. 1997. Biotransformation of bile acids, cholesterol, and steroid hormones, p. 470-510. In R. I. Mackie and B. A. White (ed.), Gastrointestinal microbiology, vol. I. Gastrointestinal ecosystems and fermentations. International Thomson Publishing, New York, NY.
4. Bennett, A. D., and W. V. Shaw. 1983. Resistance to fusidic acid in Escherichia coli mediated by the type I variant of chloramphenicol acetyltransferase. A plasmid-encoded mechanism involving antibiotic binding. Biochem. J. 215:29-38.
5. Eda, S., H. Maseda, and T. Nakae. 2003. An elegant means of self-protection in gram-negative bacteria by recognizing and extruding xenobiotics from the periplasmic space. J. Biol. Chem. 278:2085-2088.
6. Eguchi, Y., T. Oshima, H. Mori, R. Aono, K. Yamamoto, A. Ishihama, and R. Utsumi. 2003. Transcriptional regulation of drug efflux genes by EvgAS, a two-component system in Escherichia coli. Microbiology 149:2819-2828.
7. Elkins, C. A., and K. E. Beenken. 2005. Modeling the tripartite drug efflux pump archetype: structural and functional studies of the macromolecular constituents reveal more than their names imply. J. Chemother. 17:581-592.
8. Elkins, C. A., and L. B. Mullis. 2004. Bile-mediated aminoglycoside sensitivity in Lactobacillus species likely results from increased membrane permeability attributable to cholic acid. Appl. Environ. Microbiol. 70:7200-7209.
9. Elkins, C. A., and L. B. Mullis. 2006. Mammalian steroid hormones are substrates for the major RND- and MFS-type tripartite multidrug efflux pumps of Escherichia coli. J. Bacteriol. 188:1191-1195.
10. Elkins, C. A., and H. Nikaido. 2002. Substrate specificity of the RND-type multidrug efflux pumps AcrB and AcrD of Escherichia coli is determined predominantly by two large periplasmic loops. J. Bacteriol. 184:6490-6498.
11. Elkins, C. A., and D. C. Savage. 1998. Identification of genes encoding conjugated bile salt hydrolase and transport in Lactobacillus johnsonii 100-100. J. Bacteriol. 180:4344-4349.
12. George, A. M., and S. B. Levy. 1983. Amplifiable resistance to tetracycline, chloramphenicol, and other antibiotics in Escherichia coli: involvement of a non-plasmid-determined efflux of tetracycline. J. Bacteriol. 155:531-540.
13. Graef, V., E. Furuya, and O. Nishikaze. 1977. Hydrolysis of steroid glucuronides with β-glucuronidase from bovine liver, Helix pomatia and Escherichia coli. Clin. Chem. 23:532-535.
14. Hall, J. G., A. H. Cory, and J. G. Cory. 1999. Lack of competition of substrates for P-glycoprotein in MCF-7 breast cancer cells overexpressing MDR1. Adv. Enzyme Regul. 39:113-128.
15. Hamilton, K. O., M. A. Yazdanian, and K. L. Audus. 2001. Modulation of P-glycoprotein activity in Calu-3 cells using steroids and β-ligands. Int. J. Pharm. 228:171-179.
16. Kobayashi, A., H. Hirakawa, T. Hirata, K. Nishino, and A. Yamaguchi. 2006. Growth phase-dependent expression of drug exporters in Escherichia coli and its contribution to drug tolerance. J. Bacteriol. 188:5693-5703.
17. Li, X. Z., and H. Nikaido. 2004. Efflux-mediated drug resistance in bacteria. Drugs 64:159-204.
18. Lomovskaya, O., and K. A. Bostian. 2006. Practical applications and feasibility of efflux pump inhibitors in the clinic-a vision for applied use. Biochem. Pharmacol. 71:910-918.
19. Lomovskaya, O., and K. Lewis. 1992. emr, an Escherichia coli locus for multidrug resistance. Proc. Natl. Acad. Sci. USA 89:8938-8942.
20. Lomovskaya, O., H. I. Zgurskaya, and H. Nikaido. 2002. It takes three to tango. Nat. Biotechnol. 20:1210-1212.
21. Mao, W., M. S. Warren, D. S. Black, T. Satou, T. Murata, T. Nishino, N. Gotoh, and O. Lomovskaya. 2002. On the mechanism of substrate specificity by resistance Modulation division (RND)-type multidrug resistance pumps: the large periplasmic loops of MexD from Pseudomonas aeruginosa are involved in substrate recognition. Mol. Microbiol. 46:889-901.
22. 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.
23. Murakami, S., R. Nakashima, E. Yamashita, and A. Yamaguchi. 2002. Crystal structure of bacterial multidrug efflux transporter AcrB. Nature 419:587-593.
24. Murakami, S., and A. Yamaguchi. 2003. Multidrug-exporting secondary transporters. Curr. Opin. Struct. Biol. 13:443-452.
25. Murata, T., M. Kuwagaki, T. Shin, N. Gotoh, and T. Nishino. 2002. The substrate specificity of tripartite efflux systems of Pseudomonas aeruginosa is determined by the RND component. Biochem. Biophys. Res. Commun. 299:247-251.
26. Nikaido, H. 1998. Antibiotic resistance caused by gram-negative multidrug efflux pumps. Clin. Infect. Dis. 27(Suppl. 1):S32-S41.
27. Nikaido, H. 2003. Molecular basis of bacterial outer membrane permeability revisited. Microbiol. Mol. Biol. Rev. 67:593-656.
28. Nikaido, H., M. Basina, V. Nguyen, and E. Y. Rosenberg. 1998. Multidrug efflux pump AcrAB of Salmonella typhimunum excretes only those β-lactam antibiotics containing lipophilic side chains. J. Bacteriol. 180:4686-4692.
29. Nikaido, H., and H. Zgurskaya. 1999. Antibiotic efflux mechanisms. Curr. Opin. Infect. Dis. 12:529-536.
30. 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.
31. 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.
32. Rosenberg, E. Y., D. Ma, and H. Nikaido. 2000. AcrD of Escherichia coli is an aminoglycoside efflux pump. J. Bacteriol. 182:1754-1756.
33. 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.
34. 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.
35. Tikhonova, E. B., Q. Wang, and H. I. Zgurskaya. 2002. Chimeric analysis of the multicomponent multidrug efflux transporters from gram-negative bacteria. J. Bacteriol. 184:6499-6507.
36. Yoshimoto, T., H. Higashi, A. Kanatani, X. S. Lin, H. Nagai, H. Oyama, K. Kurazono, and D. Tsuru. 1991. Cloning and sequencing of the 7α-hydroxysteroid dehydrogenase gene from Escherichia coli HB101 and characterization of the expressed enzyme. J. Bacteriol. 173:2173- 2179.
37. Yu, E. W., J. R. Aires, G. McDermott, and H. Nikaido. 2005. A periplasmic drug-binding site of the AcrB multidrug efflux pump: a crystallographic and site-directed mutagenesis study. J. Bacteriol. 187:6804-6815.
38. Yu, E. W., J. R. Aires, and H. Nikaido. 2003. AcrB multidrug efflux pump of Eschenchia coli: composite substrate-binding cavity of exceptional flexibility generates its extremely wide substrate specificity. J. Bacteriol. 185:5657-5664.
39. Yu, E. W., G. McDermott, H. I. Zgurskaya, H. Nikaido, and D. E. Koshland, Jr. 2003. Structural basis of multiple drug-binding capacity of the AcrB multidrug efflux pump. Science 300:976-980.