Directed evolution of a bacterial efflux pump: Adaptation of the E. coli TolC exit duct to the Pseudomonas MexAB translocase

FEBS Letters

Volumn 580, Issue 22, 2006, Pages 5339-5343

  Bokma, Evert ^a   Koronakis, Eva ^a   Lobedanz, Sune ^a   Hughes, Colin ^a   Koronakis, Vassilis ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Efflux pump; Membrane protein; Multidrug resistance

Indexed keywords

BACTERIAL ENZYME; MEXAB TRANSLOCASE; NOVOBIOCIN; TOLC PROTEIN; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO ACID SUBSTITUTION; ARTICLE; ESCHERICHIA COLI; MOLECULAR EVOLUTION; MULTIDRUG RESISTANCE; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PSEUDOMONAS;

ANTI-BACTERIAL AGENTS; BACTERIAL OUTER MEMBRANE PROTEINS; DIRECTED MOLECULAR EVOLUTION; DRUG RESISTANCE, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MEMBRANE TRANSPORT PROTEINS; MUTANT CHIMERIC PROTEINS; NOVOBIOCIN; PERIPLASM; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PSEUDOMONAS AERUGINOSA;

BACTERIA (MICROORGANISMS); PSEUDOMONAS;

EID: 33748759588     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2006.09.005     Document Type: Article

References (26)

1. Sulavik M.C., Houseweart C., Cramer C., Jiwani N., Murgolo N., Greene J., DiDomenico B., Shaw K.J., Miller G.H., Hare R., and Shimer G. Antibiotic susceptibility profiles of Escherichia coli strains lacking multidrug efflux pump genes. Antimicrob. Agents Chemother. 45 (2001) 1126-1136
2. Lomovskaya O., Zgurskaya H.I., and Nikaido H. It takes three to tango. Nat. Biotechnol. 20 (2002) 1210-1212
3. Koronakis V. TolC - the bacterial exit duct for proteins and drugs. Febs Lett. 555 (2003) 66-71
4. Thanabalu T., Koronakis E., Hughes C., and Koronakis V. Substrate-induced assembly of a contiguous channel for protein export from E. coli: reversible bridging of an IM translocase to an OM exit pore. EMBO J. 17 (1998) 6487-6496
5. Eswaran J., Koronakis E., Higgins M.K., Hughes C., and Koronakis V. Three's company: component structures bring a closer view of tripartite drug efflux pumps. Curr. Opin. Struct. Biol. 14 (2004) 741-747
6. Touze T., Eswaran J., Bokma E., Koronakis E., Hughes C., and Koronakis V. Interactions underlying assembly of the Escherichia coli AcrAB-TolC multidrug efflux system. Mol. Microbiol. 53 (2004) 697-706
7. Fralick J.A. Evidence that TolC is required for functioning of the Mar/AcrAB efflux pump of Escherichia coli. J. Bacteriol. 178 (1996) 5803-5805
8. Masuda N., Sakagawa E., Ohya S., Gotoh N., Tsujimoto H., and Nishino T. Substrate specificities of MexAB-OprM, MexCD-OprJ, and MexXY-OprM efflux pumps in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 44 (2000) 3322-3327
9. Koronakis V., Sharff A., Koronakis E., Luisi B., and Hughes C. Crystal structure of the bacterial membrane protein TolC central to multidrug efflux and protein export. Nature 405 (2000) 914-919
10. Andersen C., Koronakis E., Bokma E., Eswaran J., Humphreys D., Hughes C., and Koronakis V. Transition to the open state of the TolC periplasmic tunnel entrance. Proc. Natl. Acad. Sci. USA 99 (2002) 11103-11108
11. Akama H., Kanemaki M., Yoshimura M., Tsukihara T., Kashiwagi T., Yoneyama H., Narita S., Nakagawa A., and Nakae T. Crystal structure of the drug discharge outer membrane protein, OprM, of Pseudomonas aeruginosa: dual modes of membrane anchoring and occluded cavity end. J. Biol. Chem. 279 (2004) 52816-52819
12. Murakami S., Nakashima R., Yamashita E., and Yamaguchi A. Crystal structure of bacterial multidrug efflux transporter AcrB. Nature 419 (2002) 587-593
13. Tamura N., Murakami S., Oyama Y., Ishiguro M., and Yamaguchi A. Direct interaction of multidrug efflux transporter AcrB and outer membrane channel TolC detected via site-directed disulfide cross-linking. Biochemistry 44 (2005) 11115-11121
14. Higgins M.K., Bokma E., Koronakis E., Hughes C., and Koronakis V. Structure of the periplasmic component of a bacterial drug efflux pump. Proc. Natl. Acad. Sci. USA 101 (2004) 9994-9999
15. Akama H., Matsuura T., Kashiwagi S., Yoneyama H., Narita S., Tsukihara T., Nakagawa A., and Nakae T. Crystal structure of the membrane fusion protein, MexA, of the multidrug transporter in Pseudomonas aeruginosa. J. Biol. Chem. 279 (2004) 25939-25942
16. Mikolosko J., Bobyk K., Zgurskaya H.I., and Ghosh P. Conformational flexibility in the multidrug efflux system protein AcrA. Structure 14 (2006) 577-587
17. Tikhonova E.B., Wang Q., and Zgurskaya H.I. Chimeric analysis of the multicomponent multidrug efflux transporters from gram-negative bacteria. J. Bacteriol. 184 (2002) 6499-6507
18. Miyazaki K. Random DNA fragmentation with endonuclease V: application to DNA shuffling. Nucleic Acids Res. 30 (2002) e139
19. Stemmer W.P. Rapid evolution of a protein by DNA shuffling. Nature 370 (1994) 389-391
20. Neylon C. Chemical and biochemical strategies for the randomization of protein encoding DNA sequences: library construction methods for directed evolution. Nucleic Acids Res. 32 (2004) 1448-1459
21. Srikumar R., Kon T., Gotoh N., and Poole K. Expression of Pseudomonas aeruginosa multidrug efflux pumps MexA-MexB-OprM and MexC-MexD-OprJ in a multidrug-sensitive Escherichia coli strain. Antimicrob. Agents Chemother. 42 (1998) 65-71
22. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., and Higgins D.G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25 (1997) 4876-4882
23. Vediyappan G., Borisova T., and Fralick J.A. Isolation and characterization of VceC gain-of-function mutants that can function with the AcrAB multiple-drug-resistant efflux pump of Escherichia coli. J. Bacteriol. 188 (2006) 3757-3762
24. Andersen C., Koronakis E., Hughes C., and Koronakis V. An aspartate ring at the TolC tunnel entrance determines ion selectivity and presents a target for blocking by large cations. Mol. Microbiol. 44 (2002) 1131-1139
25. Eda S., Maseda H., Yoshihara E., and Nakae T. Assignment of the outer-membrane-subunit-selective domain of the membrane fusion protein in the tripartite xenobiotic efflux pump of Pseudomonas aeruginosa. FEMS Lett. 254 (2006) 101-107
26. Vaccaro L., Koronakis V., and Sansom M.S.P. Flexibility in a drug transport accessory protein: molecular dynamics simulations of MexA. Biophys. J. 91 (2006) 558-564