Modulation of substrate efflux in bacterial small multidrug resistance proteins by mutations at the dimer interface

Journal of Bacteriology

Volumn 193, Issue 21, 2011, Pages 5929-5935

  Poulsen, Bradley E ^a,b   Cunningham, Fiona ^a,b   Lee, Kate K Y ^a   Deber, Charles M ^a,b  

^a HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; DIMER; ETHIDIUM BROMIDE; ISOLEUCINE; LEUCINE; METHIONINE; MULTIDRUG RESISTANCE PROTEIN; PHENYLALANINE; SMALL MULTIDRUG RESISTANCE PROTEIN; UNCLASSIFIED DRUG; VALINE;

ARTICLE; CONTROLLED STUDY; DIMERIZATION; GENE MUTATION; GENETIC CONSERVATION; HALOBACTERIUM SALINARUM; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN FUNCTION; SEQUENCE HOMOLOGY;

AMINO ACID MOTIFS; AMINO ACID SUBSTITUTION; ANTI-BACTERIAL AGENTS; DRUG RESISTANCE, BACTERIAL; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ETHIDIUM; HALOBACTERIUM SALINARUM; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; MUTATION, MISSENSE; P-GLYCOPROTEINS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION;

BACTERIA (MICROORGANISMS); HALOBACTERIUM SALINARUM;

EID: 80055060267     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.05846-11     Document Type: Article

References (31)

1. Bay, D. C., R. A. Budiman, M. P. Nieh, and R. J. Turner. 2010. Multimeric forms of the small multidrug resistance protein EmrE in anionic detergent. Biochim. Biophys. Acta 1798:526-535.
2. Bay, D. C., K. L. Rommens, and R. J. Turner. 2008. Small multidrug resistance proteins: a multidrug transporter family that continues to grow. Biochim. Biophys. Acta 1778:1814-1838.
3. Brunger, A. T., et al. 1998. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54:905-921.
4. Butler, P. J., I. Ubarretxena-Belandia, T. Warne, and C. G. Tate. 2004. The Escherichia coli multidrug transporter EmrE is a dimer in the detergentsolubilised state. J. Mol. Biol. 340:797-808.
5. Chen, Y. J., et al. 2007. X-ray structure of EmrE supports dual topology model. Proc. Natl. Acad. Sci. U. S. A. 104:18999-19004.
6. Cunningham, F., B. E. Poulsen, W. Ip, and C. M. Deber. 2011. Beta-branched residues adjacent to GG4 motifs promote the efficient association of glycophorin A transmembrane helices. Biopolymers 96:340-347.
7. Elbaz, Y., T. Salomon, and S. Schuldiner. 2008. Identification of a glycine motif required for packing in EmrE, a multidrug transporter from Escherichia coli. J. Biol. Chem. 283:12276-12283.
8. Elbaz, Y., S. Steiner-Mordoch, T. Danieli, and S. Schuldiner. 2004. In vitro synthesis of fully functional EmrE, a multidrug transporter, and study of its oligomeric state. Proc. Natl. Acad. Sci. U. S. A. 101:1519-1524.
9. Grinius, L. L., and E. B. Goldberg. 1994. Bacterial multidrug resistance is due to a single membrane protein which functions as a drug pump. J. Biol. Chem. 269:29998-30004.
10. Heir, E., G. Sundheim, and A. L. Holck. 1999. Identification and characterization of quaternary ammonium compound resistant staphylococci from the food industry. Int. J. Food Microbiol. 48:211-219.
11. Kikukawa, T., T. Nara, T. Araiso, S. Miyauchi, and N. Kamo. 2006. Twocomponent bacterial multidrug transporter, EbrAB: mutations making each component solely functional. Biochim. Biophys. Acta 1758:673-679.
12. Korkhov, V. M., and C. G. Tate. 2008. Electron crystallography reveals plasticity within the drug binding site of the small multidrug transporter EmrE. J. Mol. Biol. 377:1094-1103.
13. LePecq, J. B., and C. Paoletti. 1967. A fluorescent complex between ethidium bromide and nucleic acids. Physical-chemical characterization. J. Mol. Biol. 27:87-106.
14. Littlejohn, T. G., et al. 1992. Substrate specificity and energetics of antiseptic and disinfectant resistance in Staphylococcus aureus. FEMS Microbiol. Lett. 74:259-265.
15. Masaoka, Y., et al. 2000. A two-component multidrug efflux pump, EbrAB, in Bacillus subtilis. J. Bacteriol. 182:2307-2310.
16. Miller, D., et al. 2009. In vitro unfolding and refolding of the small multidrug transporter EmrE. J. Mol. Biol. 393:815-832.
17. Nikaido, H. 2009. Multidrug resistance in bacteria. Annu. Rev. Biochem. 78:119-146.
18. Ninio, S., and S. Schuldiner. 2003. Characterization of an archaeal multidrug transporter with a unique amino acid composition. J. Biol. Chem. 278:12000-12005.
19. Paulsen, I. T., et al. 1993. The 3' conserved segment of integrons contains a gene associated with multidrug resistance to antiseptics and disinfectants. Antimicrob. Agents Chemother. 37:761-768.
20. Poulsen, B. E., A. Rath, and C. M. Deber. 2009. The assembly motif of a bacterial small multidrug resistance protein. J. Biol. Chem. 284:9870-9875.
21. Rath, A., R. A. Melnyk, and C. M. Deber. 2006. Evidence for assembly of small multidrug resistance proteins by a "two-faced" transmembrane helix. J. Biol. Chem. 281:15546-15553.
22. Rotem, D., N. Sal-man, and S. Schuldiner. 2001. In vitro monomer swapping in EmrE, a multidrug transporter from Escherichia coli, reveals that the oligomer is the functional unit. J. Biol. Chem. 276:48243-48249.
23. Schuldiner, S. 2009. EmrE, a model for studying evolution and mechanism of ion-coupled transporters. Biochim. Biophys. Acta 1794:748-762.
24. Seppala, S., J. S. Slusky, P. Lloris-Garcera, M. Rapp, and G. von Heijne. 2010. Control of membrane protein topology by a single C-terminal residue. Science 328:1698-1700.
25. Soskine, M., S. Mark, N. Tayer, R. Mizrachi, and S. Schuldiner. 2006. On parallel and antiparallel topology of a homodimeric multidrug transporter. J. Biol. Chem. 281:36205-36212.
26. Soskine, M., S. Steiner-Mordoch, and S. Schuldiner. 2002. Crosslinking of membrane-embedded cysteines reveals contact points in the EmrE oligomer. Proc. Natl. Acad. Sci. U. S. A. 99:12043-12048.
27. Tate, C. G., E. R. Kunji, M. Lebendiker, and S. Schuldiner. 2001. The projection structure of EmrE, a proton-linked multidrug transporter from Escherichia coli, at 7 A resolution. EMBO J. 20:77-81.
28. Tate, C. G., I. Ubarretxena-Belandia, and J. M. Baldwin. 2003. Conformational changes in the multidrug transporter EmrE associated with substrate binding. J. Mol. Biol. 332:229-242.
29. Ubarretxena-Belandia, I., J. M. Baldwin, S. Schuldiner, and C. G. Tate. 2003. Three-dimensional structure of the bacterial multidrug transporter EmrE shows it is an asymmetric homodimer. EMBO J. 22:6175-6181.
30. Ubarretxena-Belandia, I., and C. G. Tate. 2004. New insights into the structure and oligomeric state of the bacterial multidrug transporter EmrE: an unusual asymmetric homo-dimer. FEBS Lett. 564:234-238.
31. Yerushalmi, H., M. Lebendiker, and S. Schuldiner. 1995. EmrE, an Escherichia coli 12-kDa multidrug transporter, exchanges toxic cations and H+ and is soluble in organic solvents. J. Biol. Chem. 270:6856-6863.