New substrates on the block: Clinically relevant resistances for EmrE and homologues

Journal of Bacteriology

Volumn 194, Issue 24, 2012, Pages 6766-6770

  Nasie, Iris ^a   Steiner Mordoch, Sonia ^a   Schuldiner, Shimon ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; EBRAB PROTEIN; EMRE PROTEIN; STREPTOMYCIN; TOBRAMYCIN; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; ARTICLE; DEINOCOCCUS RADIODURANS; HYDROPHILICITY; MULTIDRUG RESISTANCE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FAMILY; RADIATION; TEMPERATURE;

AMINO ACID SEQUENCE; ANTIPORTERS; BACTERIAL PROTEINS; DEINOCOCCUS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; SEQUENCE ALIGNMENT; STREPTOMYCIN; TOBRAMYCIN;

EID: 84870700313     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01318-12     Document Type: Article

References (36)

1. Adam Y, Tayer N, Rotem D, Schreiber G, Schuldiner S. 2007. The fast release of sticky protons: kinetics of substrate binding and proton release in a multidrug transporter. Proc. Natl. Acad. Sci. U. S. A. 104:17989-17994.
2. Bay DC, Turner RJ. 2009. Diversity and evolution of the small multidrug resistance protein family. BMC Evol. Biol. 9:140. doi:10.1186/1471-2148-9-140.
3. Chang AC, Cohen SN. 1978. Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J. Bacteriol. 134:1141-1156.
4. Chung YJ, Saier MH, Jr. 2001. SMR-type multidrug resistance pumps. Curr. Opin. Drug Discov. Devel. 4:237-245.
5. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645.
6. Elbaz Y, Salomon T, Schuldiner S. 2008. Identification of a glycine motif required for packing in EmrE, a multidrug transporter from Escherichia coli. J. Biol. Chem. 283:12276-12283.
7. Elbaz Y, Tayer N, Steinfels E, Steiner-Mordoch S, Schuldiner S. 2005. Substrate-induced tryptophan fluorescence changes in EmrE, the smallest ion-coupled multidrug transporter. Biochemistry 44:7369-7377.
8. Goldberg EB, et al. 1987. Characterization of a Na+/H+ antiporter gene of Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 84:2615-2619.
9. Gottesman MM, Fojo T, Bates SE. 2002. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat. Rev. Cancer 2:48-58.
10. Hayes JD, Wolf CR. 1990. Molecular mechanisms of drug resistance. Biochem. J. 272:281-295.
11. Jack DL, Storms ML, Tchieu JH, Paulsen IT, Saier MH, Jr. 2000. A broad-specificity multidrug efflux pump requiring a pair of homologous SMR-type proteins. J. Bacteriol. 182:2311-2313.
12. Kikukawa T, Nara T, Araiso T, Miyauchi S, Kamo N. 2006. Twocomponent bacterial multidrug transporter, EbrAB: mutations making each component solely functional. Biochim. Biophys. Acta 1758:673-679.
13. Levy SB. 1992. Active efflux mechanisms for antimicrobial resistance. Antimicrob. Agents Chemother. 36:695-703.
14. Li XZ, Poole K, Nikaido H. 2003. Contributions of MexAB-OprM and an EmrE homolog to intrinsic resistance of Pseudomonas aeruginosa to aminoglycosides and dyes. Antimicrob. Agents Chemother. 47:27-33.
15. Masaoka Y, et al. 2000. A two-component multidrug efflux pump, EbrAB, in Bacillus subtilis. J. Bacteriol. 182:2307-2310.
16. Muth TR, Schuldiner S. 2000. A membrane-embedded glutamate is required for ligand binding to the multidrug transporter EmrE. EMBO J. 19:234-240.
17. Nasie I, Steiner-Mordoch S, Gold A, Schuldiner S. 2010. Topologically random insertion of EmrE supports a pathway for evolution of inverted repeats in ion-coupled transporters. J. Biol. Chem. 285:15234-15244.
18. Neu HC. 1992. The crisis in antibiotic resistance. Science 257:1064-1073.
19. Nikaido H. 1998. Multiple antibiotic resistance and efflux. Curr. Opin. Microbiol. 1:516-523.
20. Nikaido H. 1994. Prevention of drug access to bacterial targets: permeability barriers and active efflux. Science 264:382-388.
21. Ninio S, Rotem D, Schuldiner S. 2001. Functional analysis of novel multidrug transporters from human pathogens. J. Biol. Chem. 276:48250-48256.
22. Nishino K, Yamaguchi A. 2001. Analysis of a complete library of putative drug transporter genes in Escherichia coli. J. Bacteriol. 183:5803-5812.
23. Rapp M, Granseth E, Seppala S, von Heijne G. 2006. Identification and evolution of dual-topology membrane proteins. Nat. Struct. Mol. Biol. 13:112-116.
24. Rosenbusch JP. 2001. Stability of membrane proteins: relevance for the selection of appropriate methods for high-resolution structure determinations. J. Struct. Biol. 136:144-157.
25. Schuldiner S. 2007. When biochemistry meets structural biology: the cautionary tale of EmrE. Trends Biochem. Sci. 32:252-258.
26. Schuldiner S. 2009. EmrE, a model for studying evolution and mechanism of ion-coupled transporters. Biochim. Biophys. Acta 1794:748-762.
27. Soskine M, Adam Y, Schuldiner S. 2004. Direct evidence for substrateinduced proton release in detergent-solubilized EmrE, a multidrug transporter. J. Biol. Chem. 279:9951-9955.
28. Tabor S, Richardson CC. 1985. A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc. Natl. Acad. Sci. U. S. A. 82:1074-1078.
29. Taglicht D, Padan E, Schuldiner S. 1991. Overproduction and purification of a functional Na+/H+ antiporter coded by nhaA (ant) from Escherichia coli. J. Biol. Chem. 266:11289-11294.
30. Tal N, Schuldiner S. 2009. A coordinated network of transporters with overlapping specificities provides a robust survival strategy. Proc. Natl. Acad. Sci. U. S. A. 106:9051-9056.
31. Yerushalmi H, Lebendiker M, Schuldiner S. 1995. EmrE, an Escherichia coli 12-kDa multidrug transporter, exchanges toxic cations andH+ and is soluble in organic solvents. J. Biol. Chem. 270:6856-6863.
32. Yerushalmi H, Lebendiker M, Schuldiner S. 1996. Negative dominance studies demonstrate the oligomeric structure of EmrE, a multidrug antiporter from Escherichia coli. J. Biol. Chem. 271:31044-31048.
33. Yerushalmi H, Schuldiner S. 2000. A common binding site for substrates and protons in EmrE, an ion-coupled multidrug transporter. FEBS Lett. 476:93-97.
34. Yerushalmi H, Schuldiner S. 2000. A model for coupling of H(*) and substrate fluxes based on "time-sharing" of a common binding site. Biochemistry 39:14711-14719.
35. Yerushalmi H, Schuldiner S. 2000. An essential glutamyl residue in EmrE, a multidrug antiporter from Escherichia coli. J. Biol. Chem. 275: 5264-5269.
36. Zhang Z, et al. 2007. Functional characterization of the heterooligomeric EbrAB multidrug efflux transporter of Bacillus subtilis. Biochemistry 46: 5218-5225.