Multimeric forms of the small multidrug resistance protein EmrE in anionic detergent

Biochimica et Biophysica Acta - Biomembranes

Volumn 1798, Issue 3, 2010, Pages 526-535

  Bay, Denice C ^a   Budiman, R Arief ^a   Nieh, Mu Ping ^b   Turner, Raymond J ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b NATIONAL RESEARCH COUNCIL CANADA   (Canada)

Author keywords

EmrE; Fluorescence; Multimerization; Quaternary ammonium compound (QAC); SDS Tricine PAGE; Small angle neutron scattering (SANS); Small multidrug resistance protein (SMR)

Indexed keywords

DETERGENT; DODECYL SULFATE SODIUM; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN E; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; CIRCULAR DICHROISM; CONTROLLED STUDY; ESCHERICHIA COLI; FLUORESCENCE SPECTROSCOPY; LIGAND BINDING; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FAMILY; PROTEIN SECONDARY STRUCTURE; PROTEIN TRANSPORT; SOLUBILIZATION;

ANTIPORTERS; CIRCULAR DICHROISM; DETERGENTS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MODELS, MOLECULAR; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; NEUTRON DIFFRACTION; ONIUM COMPOUNDS; ORGANOPHOSPHORUS COMPOUNDS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; SCATTERING, SMALL ANGLE; SODIUM DODECYL SULFATE; SOLUBILITY; SOLUTIONS; SPECTROMETRY, FLUORESCENCE;

ESCHERICHIA COLI;

EID: 76749116310     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2009.12.017     Document Type: Article

References (52)

1. Grinius L., Dreguniene G., Goldberg E.B., Liao C.H., and Projan S.J. A staphylococcal multidrug resistance gene product is a member of a new protein family. Plasmid 27 (1992) 119-129
2. Littlejohn T.G., Paulsen I.T., Gillespie M.T., Tennent J.M., Midgley M., Jones I.G., Purewal A.S., and Skurray R.A. Substrate specificity and energetics of antiseptic and disinfectant resistance in Staphylococcus aureus. FEMS Microbiol. Lett. 74 (1992) 259-265
3. Yerushalmi H., Lebendiker M., and Schuldiner S. EmrE, an Escherichia coli 12-kDa multidrug transporter, exchanges toxic cations and H+ and is soluble in organic solvents. J. Biol. Chem. 270 (1995) 6856-6863
4. Jack D.L., Yang N.M., and Saier Jr. M.H. The drug/metabolite transporter superfamily. Eur. J. Biochem. 268 (2001) 3620-3639
5. Saier Jr. M.H., and Paulsen I.T. Phylogeny of multidrug transporters. Semin. Cell Dev. Biol. 12 (2001) 205-213
6. Rosser S.J., and Young H.K. Identification and characterization of class 1 integrons in bacteria from an aquatic environment. J. Antimicrob. Chemother. 44 (1999) 11-18
7. Rodriguez I., Martin M.C., Mendoza M.C., and Rodicio M.R. Class 1 and class 2 integrons in non-prevalent serovars of Salmonella enterica: structure and association with transposons and plasmids. J. Antimicrob. Chemother. 58 (2006) 1124-1132
8. Bay D.C., Rommens K.L., and Turner R.J. Small multidrug resistance proteins: a multidrug transporter family that continues to grow. Biochim. Biophys. Acta 1778 (2008) 1814-1838
9. Schuldiner S. EmrE, a model for studying evolution and mechanism of ion coupled transporters. Biochim. Biophys. Acta 1794 (2009) 748-762
10. Chen Y.J., Pornillos O., Lieu S., Ma C., Chen A.P., and Chang G. X-ray structure of EmrE supports dual topology model. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 18999-19004
11. Tate C.G., Kunji E.R., Lebendiker M., and Schuldiner S. The projection structure of EmrE, a proton-linked multidrug transporter from Escherichia coli, at 7 A resolution. Embo J. 20 (2001) 77-81
12. Tate C.G., Ubarretxena-Belandia I., and Baldwin J.M. Conformational changes in the multidrug transporter EmrE associated with substrate binding. J. Mol. Biol. 332 (2003) 229-242
13. Ubarretxena-Belandia I., Baldwin J.M., Schuldiner S., and Tate C.G. Three-dimensional structure of the bacterial multidrug transporter EmrE shows it is an asymmetric homodimer. Embo J. 22 (2003) 6175-6181
14. Tate C.G. Comparison of three structures of the multidrug transporter EmrE. Curr. Opin. Struct. Biol. 16 (2006) 457-464
15. Schuldiner S. Controversy over EmrE structure. Science 317 (2007) 748-751 author reply 748-51.
16. Schuldiner S. When biochemistry meets structural biology: the cautionary tale of EmrE. Trends Biochem. Sci. 32 (2007) 252-258
17. Miller C. Pretty structures, but what about the data?. Science 315 (2007) 459
18. Korkhov V.M., and Tate C.G. An emerging consensus for the structure of EmrE. Acta Crystallogr. D Biol. Crystallogr. 65 (2009) 186-192
19. Rotem D., Sal-man N., and Schuldiner S. In vitro monomer swapping in EmrE, a multidrug transporter from Escherichia coli, reveals that the oligomer is the functional unit. J. Biol. Chem. 276 (2001) 48243-48249
20. Yerushalmi H., and Schuldiner S. An essential glutamyl residue in EmrE, a multidrug antiporter from Escherichia coli. J. Biol. Chem. 275 (2000) 5264-5269
21. Muth T.R., and Schuldiner S. A membrane-embedded glutamate is required for ligand binding to the multidrug transporter EmrE. Embo J. 19 (2000) 234-240
22. Sikora C.W., and Turner R.J. Investigation of ligand binding to the multidrug resistance protein EmrE by isothermal titration calorimetry. Biophys. J. 88 (2005) 475-482
23. Song J., Lee M.S., Carlberg I., Vener A.V., and Markley J.L. Micelle-induced folding of spinach thylakoid soluble phosphoprotein of 9 kDa and its functional implications. Biochemistry 45 (2006) 15633-15643
24. Federkeil S.L., Winstone T.L., Jickling G., and Turner R.J. Examination of EmrE conformational differences in various membrane mimetic environments. Biochem. Cell Biol. 81 (2003) 61-70
25. Korkhov V.M., and Tate C.G. Electron crystallography reveals plasticity within the drug binding site of the small multidrug transporter EmrE. J. Mol. Biol. 377 (2008) 1094-1103
26. Winstone T.L., Duncalf K.A., and Turner R.J. Optimization of expression and the purification by organic extraction of the integral membrane protein EmrE. Protein Expr. Purif. 26 (2002) 111-121
27. Hayter J.B., and Penfold J. Self-consistent structural and dynamic study of concentrated micelles solutions. J. Chem. Soc., Faraday Trans. 1 77 (1981) 1851-1863
28. Higgins J.S., and Benoît H.C. Polymers and Neutron Scattering (1994), Oxford University Press Inc., NY, USA
29. Kline S.R. Reduction and analysis of SANS and USANS data using IGOR Pro. J. Appl. Crystallogr. 39 (2006) 895-900
30. McHaourab H.S., Mishra S., Koteiche H.A., and Amadi S.H. Role of sequence bias in the topology of the multidrug transporter EmrE. Biochemistry 47 (2008) 7980-7982
31. Mordoch S.S., Granot D., Lebendiker M., and Schuldiner S. Scanning cysteine accessibility of EmrE, an H+-coupled multidrug transporter from Escherichia coli, reveals a hydrophobic pathway for solutes. J. Biol. Chem. 274 (1999) 19480-19486
32. Sharoni M., Steiner-Mordoch S., and Schuldiner S. Exploring the binding domain of EmrE, the smallest multidrug transporter. J. Biol. Chem. 280 (2005) 32849-32855
33. Elbaz Y., Steiner-Mordoch S., Danieli T., and Schuldiner S. In vitro synthesis of fully functional EmrE, a multidrug transporter, and study of its oligomeric state. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 1519-1524
34. Rotem D., Steiner-Mordoch S., and Schuldiner S. Identification of tyrosine residues critical for the function of an ion-coupled multidrug transporter. J. Biol. Chem. 281 (2006) 18715-18722
35. Elbaz Y., Tayer N., Steinfels E., Steiner-Mordoch S., and Schuldiner S. Substrate-induced tryptophan fluorescence changes in EmrE, the smallest ion-coupled multidrug transporter. Biochemistry 44 (2005) 7369-7377
36. Ubarretxena-Belandia I., and Tate C.G. New insights into the structure and oligomeric state of the bacterial multidrug transporter EmrE: an unusual asymmetric homo-dimer. FEBS Lett. 564 (2004) 234-238
37. Rainey J.K., Fliegel L., and Sykes B.D. Strategies for dealing with conformational sampling in structural calculations of flexible or kinked transmembrane peptides. Biochem. Cell Biol. 84 (2006) 918-929
38. Yerushalmi H., Lebendiker M., and Schuldiner S. Negative dominance studies demonstrate the oligomeric structure of EmrE, a multidrug antiporter from Escherichia coli. J. Biol. Chem. 271 (1996) 31044-31048
39. Winstone T.L., Jidenko M., le Maire M., Ebel C., Duncalf K.A., and Turner R.J. Organic solvent extracted EmrE solubilized in dodecyl maltoside is monomeric and binds drug ligand. Biochem. Biophys. Res. Commun. 327 (2005) 437-445
40. Venkatraman J., Nagana Gowda G.A., and Balaram P. Structural analysis of synthetic peptide fragments from EmrE, a multidrug resistance protein, in a membrane-mimetic environment. Biochemistry 41 (2002) 6631-6639
41. Butler P.J., Ubarretxena-Belandia I., Warne T., and Tate C.G. The Escherichia coli multidrug transporter EmrE is a dimer in the detergent-solubilised state. J. Mol. Biol. 340 (2004) 797-808
42. Grinius L.L., and Goldberg E.B. Bacterial multidrug resistance is due to a single membrane protein which functions as a drug pump. J. Biol. Chem. 269 (1994) 29998-30004
43. Torres J., and Arkin I.T. Recursive use of evolutionary conservation data in molecular modeling of membrane proteins A model of the multidrug H+ antiporter EmrE. Eur. J. Biochem. 267 (2000) 3422-3431
44. Arkin I.T., Russ W.P., Lebendiker M., and Schuldiner S. Determining the secondary structure and orientation of EmrE, a multi-drug transporter, indicates a transmembrane four-helix bundle. Biochemistry 35 (1996) 7233-7238
45. Rath A., Glibowicka M., Nadeau V.G., Chen G., and Deber C.M. Detergent binding explains anomalous SDS-PAGE migration of membrane proteins. Proc. Natl. Acad. Sci. U. S. A. 106 (2009) 1760-1765
46. Miller D., Charalambous K., Rotem D., Schuldiner S., Curnow P., and Booth P.J. In vitro unfolding and refolding of the small multidrug transporter EmrE. J. Mol. Biol. 393 (2009) 815-832
47. Adam Y., Tayer N., Rotem D., Schreiber G., and Schuldiner S. 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 (2007) 17989-17994
48. Furste J.P., Pansegrau W., Frank R., Blocker H., Scholz P., Bagdasarian M., and Lanka E. Molecular cloning of the plasmid RP4 primase region in a multi-host-range tacP expression vector. Gene 48 (1986) 119-131
49. Stoscheck C.M. Quantitation of protein. Methods Enzymol. 182 (1990) 50-68
50. Ladner C.L., Yang J., Turner R.J., and Edwards R.A. Visible fluorescent detection of proteins in polyacrylamide gels without staining. Anal. Biochem. 326 (2004) 13-20
51. Lobley A., Whitmore L., and Wallace B.A. DICHROWEB: an interactive website for the analysis of protein secondary structure from circular dichroism spectra. Bioinformatics 18 (2002) 211-212
52. Whitmore L., and Wallace B.A. DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res. 32 (2004) W668-W673