Engineered disulfide bonds support the functional rotation mechanism of multidrug efflux pump AcrB

Nature Structural and Molecular Biology

Volumn 15, Issue 2, 2008, Pages 199-205

  Seeger, Markus A ^a,b,d   Von Ballmoos, Christoph ^b   Eicher, Thomas ^a   Brandstätter, Lorenz ^a   Verrey, François ^a   Diederichs, Kay ^c   Pos, Klaas M ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITY OF KONSTANZ   (Germany)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINE; CYSTEINE; DISULFIDE; HYBRID PROTEIN; N PHENYLNAPHTHYLAMINE; PROTEIN ACRA; PROTEIN ACRB; TOLC PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DISULFIDE BOND; ENGINEERING; ESCHERICHIA COLI; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL;

1-NAPHTHYLAMINE; AMINO ACID SUBSTITUTION; ANTI-BACTERIAL AGENTS; CYSTEINE; DISULFIDES; DITHIOTHREITOL; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE DELETION; MICROBIAL SENSITIVITY TESTS; MODELS, MOLECULAR; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; MUTAGENESIS, SITE-DIRECTED; MUTANT PROTEINS; PROTEIN STRUCTURE, TERTIARY; REDUCING AGENTS;

ESCHERICHIA COLI;

EID: 38849185972     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1379     Document Type: Article

References (33)

1. Poole, K. Efflux-mediated multiresistance in Gram-negative bacteria. Clin. Microbiol. Infect. 10, 12-26 (2004).
2. Zgurskaya, H.I. & Nikaido, H. Multidrug resistance mechanisms: drug efflux across two membranes. Mol. Microbiol. 37, 219-225 (2000).
3. Murakami, S. & Yamaguchi, A. Multidrug-exporting secondary transporters. Curr. Opin. Struct. Biol. 13, 443-452 (2003).
4. Eswaran, J., Koronakis, E., Higgins, M.K., Hughes, C. & Koronakis, V. Three's company: component structures bring a closer view of tripartite drug efflux pumps. Curr. Opin. Struct. Biol. 14, 741-747 (2004).
5. Koronakis, V., Sharff, A., Koronakis, E., Luisi, B. & Hughes, C. Crystal structure of the bacterial membrane protein TolC central to multidrug efflux and protein export. Nature 405, 914-919 (2000).
6. Murakami, S., Nakashima, R., Yamashita, E. & Yamaguchi, A. Crystal structure of bacterial multidrug efflux transporter AcrB. Nature 419, 587-593 (2002).
7. Pos, K.M., Schiefner, A., Seeger, M.A. & Diederichs, K. Crystallographic analysis of AcrB. FEBS Lett. 564, 333-339 (2004).
8. Murakami, S., Nakashima, R., Yamashita, E., Matsumoto, T. & Yamaguchi, A. Crystal structures of a multidrug transporter reveal a functionally rotating mechanism. Nature 443, 173-179 (2006).
9. Seeger, M.A. et al. Structural asymmetry of AcrB trimer suggests a peristaltic pump mechanism. Science 313, 1295-1298 (2006).
10. Mikolosko, J., Bobyk, K., Zgurskaya, H.I. & Ghosh, P. Conformational flexibility in the multidrug efflux system protein AcrA. Structure 14, 577-587 (2006).
11. Andersen, C. et al. Transition to the open state of the TolC periplasmic tunnel entrance. Proc. Natl. Acad. Sci. USA 99, 11103-11108 (2002).
12. Tikhonova, E.B. & Zgurskaya, H.I. AcrA, AcrB, and TolC of Escherichia coli form a stable intermembrane multidrug efflux Complex. J. Biol. Chem. 279, 32116-32124 (2004).
13. Touze, T. et al. Interactions underlying assembly of the Escherichia coli AcrAB-TolC multidrug efflux system. Mol. Microbiol. 53, 697-706 (2004).
14. Lobedanz, S. et al. A periplasmic coiled-coil interface underlying TolC recruitment and the assembly of bacterial drug efflux pumps. Proc. Natl. Acad. Sci. USA 104, 4612-4617 (2007).
15. Tikhonova, E.B., Wang, Q. & Zgurskaya, H.I. Chimeric analysis of the multicomponent multidrug efflux transporters from Gram-negative bacteria. J. Bacteriol. 184, 6499-6507 (2002).
16. Eda, S., Maseda, H. & Nakae, T. 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 (2003).
17. Pos, K.M. & Diederichs, K. Purification, crystallization and preliminary diffraction studies of AcrB, an inner-membrane multi-drug efflux protein. Acta Crystallogr. D Biol. Crystallogr. 58, 1865-1867 (2002).
18. Yu, E.W., McDermott, G., Zgurskaya, H.I., Nikaido, H. & Koshland, D.E., Jr. Structural basis of multiple drug-binding capacity of the AcrB multidrug efflux pump. Science 300, 976-980 (2003).
19. Sennhauser, G., Amstutz, P., Briand, C., Storchenegger, O. & Grutter, M.G. Drug export pathway of multidrug exporter AcrB revealed by DARPin inhibitors. PLoS Biol. 5, Acta Crystallogr. D Biol. Crystallogr. 5, e7 (2007).
20. Abrahams, J.P., Leslie, A.G., Lutter, R. & Walker, J.E. Structure at 2.8 A resolution of F1-ATPase from bovine heart mitochondria. Nature 370, 621-628 (1994).
21. Nikaido, H. Multidrug efflux pumps of Gram-negative bacteria. J. Bacteriol. 178, 5853-5859 (1996).
22. Lomovskaya, O. et al. Identification and characterization of inhibitors of multidrug resistance efflux pumps in Pseudomonas aeruginosa: novel agents for combination therapy. Antimicrob. Agents Chemother. 45, 105-116 (2001).
23. Colonna-Cesari, F. & Sander, C. Excluded volume approximation to protein-solvent interaction. The solvent contact model. Biophys. J. 57, 1103-1107 (1990).
24. Dombkowski, A.A. & Crippen, G.M. Disulfide recognition in an optimized threading potential. Protein Eng. 13, 679-689 (2000).
25. Murakami, S., Tamura, N., Saito, A., Hirata, T. & Yamaguchi, A. Extramembrane central pore of multidrug exporter AcrB in Escherichia coli plays an important role in drug transport. J. Biol. Chem. 279, 3743-3748 (2004).
26. Woodcock, D.M. et al. Quantitative evaluation of Escherichia coli host strains for tolerance to cytosine methylation in plasmid and phage recombinants. Nucleic Acids Res. 17, 3469-3478 (1989).
27. Miroux, B. & Walker, J.E. Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J. Mol. Biol. 260, 289-298 (1996).
28. Sambrook, J., Fritsch, E.F. & Maniatis, T. Molecular Cloning: A Laboratory Manual (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, USA, 1989).
29. Datsenko, K.A. & Wanner, B.L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97, 6640-6645 (2000).
30. Schagger, H. & von Jagow, G. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166, 368-379 (1987).
31. Molloy, P.L. Electrophoretic mobility shift assays. Methods Mol. Biol. 130, 235-246 (2000).
32. Kyhse-Andersen, J. Electroblotting of multiple gels: a simple apparatus without buffer tank for rapid transfer of proteins from polyacrylamide to nitrocellulose. J. Biochem. Biophys. Methods 10, 203-209 (1984).
33. Kraft, P., Mills, J. & Dratz, E. Mass spectrometric analysis of cyanogen bromide fragments of integral membrane proteins at the picomole level: application to rhodopsin. Anal. Biochem. 292, 76-86 (2001).