Outer membrane protein OmpW participates with small multidrug resistance protein member EmrE in quaternary cationic compound efflux

Journal of Bacteriology

Volumn 196, Issue 10, 2014, Pages 1908-1914

  Beketskaia, Maria S ^a   Bay, Denice C ^a   Turner, Raymond J ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MICROBIAL PRODUCTS NOT CLASSIFIED ELSEWHERE; MULTIDRUG RESISTANCE PROTEIN; OUTER MEMBRANE PROTEIN; PARAQUAT; PROTEIN EMRE; PROTEIN OMPW; QUATERNARY CATIONIC COMPOUND; UNCLASSIFIED DRUG;

ALKALINITY; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; CONTROLLED STUDY; ESCHERICHIA COLI; GENE DELETION; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PHENOTYPE; PLASMID; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; WILD TYPE;

ANTI-BACTERIAL AGENTS; ANTIPORTERS; BACTERIAL OUTER MEMBRANE PROTEINS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; MICROBIAL SENSITIVITY TESTS; SUBSTRATE SPECIFICITY;

EID: 84898870049     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01483-14     Document Type: Article

References (32)

1. Piddock LJ. 2006. Clinically relevant chromosomally encoded multidrug resistance efflux pumps in bacteria. Clin. Microbiol. Rev. 19:382-402. http://dx.doi.org/10.1128/CMR.19.2.382-402.2006.
2. Poole K. 2005. Efflux-mediated antimicrobial resistance. J. Antimicrob. Chemother. 56:20-51. http://dx.doi.org/10.1093/jac/dki171.
3. Wong K, Ma J, Rothnie A, Biggin PC, Kerr ID. 2014. Towards understanding promiscuity in multidrug efflux pumps. Trends Biochem. Sci. 39:8-16. http://dx.doi.org/10.1016/j.tibs.2013.11.002.
4. Yen MR, Chen JS, Marquez JL, Sun EI, Saier MH. 2010. Multidrug resistance: phylogenetic characterization of superfamilies of secondary carriers that include drug exporters. Methods Mol. Biol. 637:47-64. http://dx.doi.org/10.1007/978-1-60761-700-6_3.
5. Ruggerone P, Murakami S, Pos KM, Vargiu AV. 2013. RND efflux pumps: structural information translated into function and inhibition mechanisms. Curr. Top. Med. Chem. 13:3079-3100. http://dx.doi.org/10.2174/15680266113136660220.
6. Pages JM, James CE, Winterhalter M. 2008. The porin and the permeating antibiotic: a selective diffusion barrier in Gram-negative bacteria. Nat. Rev. Microbiol. 6:893-903. http://dx.doi.org/10.1038/nrmicro1994.
7. Sigal N, Cohen-Karni D, Siemion S, Bibi E. 2006. MdfA from Escherichia coli, a model protein for studying secondary multidrug transport. J. Mol. Microbiol. Biotechnol. 11:308-317. http://dx.doi.org/10.1159/000095633.
8. Bay DC, Rommens KL, Turner RJ. 2008. Small multidrug resistance proteins: a multidrug transporter family that continues to grow. Biochim. Biophys. Acta 1778:1814-1838. http://dx.doi.org/10.1016/j.bbamem.2007.08.015.
9. Schuldiner S. 2009. EmrE, a model for studying evolution and mechanism of ion-coupled transporters. Biochim. Biophys. Acta 1794:748-762. http://dx.doi.org/10.1016/j.bbapap.2008.12.018.
10. Grinius LL, Goldberg EB. 1994. Bacterial multidrug resistance is due to a single membrane protein which functions as a drug pump. J. Biol. Chem. 269:29998-30004.
11. Littlejohn TG, Paulsen IT, Gillespie MT, Tennent JM, Midgley M, Jones IG, Purewal AS, Skurray RA. 1992. Substrate specificity and energetics of antiseptic and disinfectant resistance in Staphylococcus aureus. FEMS Microbiol. Lett. 74:259-265.
12. Muth TR, Schuldiner S. 2000. A membrane-embedded glutamate is required for ligand binding to the multidrug transporter EmrE. EMBO J. 19:234-240. http://dx.doi.org/10.1093/emboj/19.2.234.
13. + and substrate fluxes based on "time-sharing" of a common binding site. Biochemistry 39:14711-14719. http://dx.doi.org/10.1021/bi001892i.
14. Bay DC, Turner RJ. 2012. Small multidrug resistance protein EmrE reduces host pH and osmotic tolerance to metabolic quaternary cation osmoprotectants. J. Bacteriol. 194:5941-5948. http://dx.doi.org/10.1128/JB.00666-12.
15. Bay DC, Turner RJ. 2009. Diversity and evolution of the small multidrug resistance protein family. BMC Evol. Biol. 9:140. http://dx.doi.org/10.1186/1471-2148-9-140.
16. 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. http://dx.doi.org/10.1073/pnas.0902400106.
17. Sulavik MC, Houseweart C, Cramer C, Jiwani N, Murgolo N, Greene J, DiDomenico B, Shaw KJ, Miller GH, Hare R, Shimer G. 2001. Antibiotic susceptibility profiles of Escherichia coli strains lacking multidrug efflux pump genes. Antimicrob. Agents Chemother. 45:1126-1136. http://dx.doi.org/10.1128/AAC.45.4.1126-1136.2001.
18. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2:2006.2008. http://dx.doi.org/10.1038/msb4100050.
19. Sambrook J, Russell DW. 2001. Molecular cloning: a laboratory manual, vol. 1 to 3, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
20. Winstone TL, Duncalf KA, Turner RJ. 2002. Optimization of expression and the purification by organic extraction of the integral membrane protein EmrE. Protein Expr. Purif. 26:111-121. http://dx.doi.org/10.1016/S1046-5928(02)00525-9.
21. Furste JP, Pansegrau W, Frank R, Blocker H, Scholz P, Bagdasarian M, Lanka E. 1986. Molecular cloning of the plasmid RP4 primase region in a multi-host-range tacP expression vector. Gene 48:119-131. http://dx.doi.org/10.1016/0378-1119(86)90358-6.
22. Kitagawa M, Ara T, Arifuzzaman M, Ioka-Nakamichi T, Inamoto E, Toyonaga H, Mori H. 2005. Complete set of ORF clones of Escherichia coli ASKA library (a complete set of E. coli K-12 ORF archive): unique resources for biological research. DNA Res. 12:291-299. http://dx.doi.org/10.1093/dnares/dsi012.
23. Beernink PT, Tolan DR. 1992. Construction of a high-copy "ATG vector" for expression in Escherichia coli. Protein Expr. Purif. 3:332-336. http://dx.doi.org/10.1016/1046-5928(92)90009-L.
24. de Boer HA, Comstock LJ, Vasser M. 1983. The tac promoter: a functional hybrid derived from the trp and lac promoters. Proc. Natl. Acad. Sci. U. S. A. 80:21-25. http://dx.doi.org/10.1073/pnas.80.1.21.
25. Soskine M, Steiner-Mordoch S, Schuldiner S. 2002. Crosslinking of membrane-embedded cysteines reveals contact points in the EmrE oligomer. Proc. Natl. Acad. Sci. U. S. A. 99:12043-12048. http://dx.doi.org/10.1073/pnas.192392899.
26. + and is soluble in organic solvents. J. Biol. Chem. 270:6856-6863. http://dx.doi.org/10.1074/jbc.270.12.6856.
27. Molloy MP, Herbert BR, Slade MB, Rabilloud T, Nouwens AS, Williams KL, Gooley AA. 2000. Proteomic analysis of the Escherichia coli outer membrane. Eur. J. Biochem. 267:2871-2881. http://dx.doi.org/10.1046/j.1432-1327.2000.01296.x.
28. Gil F, Ipinza F, Fuentes J, Fumeron R, Villarreal JM, Aspee A, Mora GC, Vasquez CC, Saavedra C. 2007. The ompW porin gene mediates methyl viologen (paraquat) efflux in Salmonella enterica serovar typhimurium. Res. Microbiol. 158:529-536. http://dx.doi.org/10.1016/j.resmic.2007.05.004.
29. Morimyo M. 1988. Isolation and characterization of methyl viologensensitive mutants of Escherichia coli K-12. J. Bacteriol. 170:2136-2142.
30. Nandi B, Nandy RK, Sarkar A, Ghose AC. 2005. Structural features, properties and regulation of the outer-membrane protein W OmpW of Vibrio cholerae. Microbiology 151:2975-2986. http://dx.doi.org/10.1099/mic.0.27995-0.
31. Xu C, Wang S, Ren H, Lin X, Wu L, Peng X. 2005. Proteomic analysis on the expression of outer membrane proteins of Vibrio alginolyticus at different sodium concentrations. Proteomics 5:3142-3152. http://dx.doi.org/10.1002/pmic.200401128.
32. Villagra NA, Hidalgo AA, Santiviago CA, Saavedra CP, Mora GC. 2008. SmvA, and not AcrB, is the major efflux pump for acriflavine and related compounds in Salmonella enterica serovar Typhimurium. J. Antimicrob. Chemother. 62:1273-1276. http://dx.doi.org/10.1093/jac/dkn407.