Functional and biochemical characterisation of the Escherichia coli major facilitator superfamily multidrug transporter MdtM

Biochimie

Volumn 94, Issue 6, 2012, Pages 1334-1346

  Holdsworth, Scarlett R ^a   Law, Christopher J ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

Antibiotic resistance; Ethidium bromide efflux assays; Integral membrane protein; Major facilitator superfamily; Multidrug efflux

Indexed keywords

ARGININE; ASPARTIC ACID; CHLORAMPHENICOL; DETERGENT; DODECYL BETA DEXTRO MALTOPYRANOSIDE; ETHIDIUM BROMIDE; GLYCOPROTEIN P; PROTEIN MDTM; UNCLASSIFIED DRUG;

ARTICLE; ESCHERICHIA COLI; GROWTH INHIBITION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MULTIDRUG RESISTANCE; NONHUMAN; PROTEIN STABILITY; SITE DIRECTED MUTAGENESIS;

AMINO ACID SEQUENCE; ANTIPORTERS; DRUG RESISTANCE, MULTIPLE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MEMBRANE TRANSPORT PROTEINS; MUTAGENESIS, SITE-DIRECTED;

ESCHERICHIA COLI;

EID: 84860480499     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2012.03.001     Document Type: Article

References (66)

1. X.Z. Li, and H. Nikaido Efflux-mediated drug resistance in bacteria Drugs 64 2004 159 204 (Pubitemid 38186964)
2. A.A. Neyfakh Mystery of multidrug transporters: the answer can be simple Mol. Microbiol. 44 2002 1123 1130 (Pubitemid 34595747)
3. O. Lewinson, J. Adler, N. Sigal, and E. Bibi Promiscuity in multidrug recognition and transport: the bacterial MFS Mdr transporters Mol. Microbiol. 61 2006 277 284 (Pubitemid 44356562)
4. T.A. Krulwich, O. Lewinson, E. Padan, and E. Bibi Do physiological roles foster persistence of drug/multidrug-efflux transporters? A case study Nat. Rev. Microbiol. 3 2005 566 572 (Pubitemid 40903879)
5. A.A. Neyfakh Natural functions of bacterial multidrug transporters Trends Microbiol. 5 1997 309 313 (Pubitemid 27362292)
6. M.C. Sulavik, C. Houseweart, C. Cramer, N. Jiwani, N. Murgolo, J. Greene, B. DiDomenico, K.J. Shaw, G.H. Miller, R. Hare, and G. Shimer Antibiotic susceptibility profiles of Escherichia coli strains lacking multidrug efflux pump genes Antimicrob. Agents Chemother. 45 2001 1126 1136 (Pubitemid 32230993)
7. K. Nishino, and A. Yamaguchi Analysis of a complete library of putative drug transporter genes in Escherichia coli J. Bacteriol. 183 2001 5803 5812 (Pubitemid 32917397)
8. H. Nikaido, and H.I. Zgurskaya AcrAB and related multidrug efflux pumps of Escherichia coli J. Mol. Microbiol. Biotechnol. 3 2001 215 218 (Pubitemid 32257906)
9. N. Tal, and S. Schuldiner A coordinated network of transporters with overlapping specificities provides a robust survival strategy Proc. Natl. Acad. Sci. U S A 106 2009 9051 9056
10. V.W. Soo, P. Hanson-Manful, and W.M. Patrick Artificial gene amplification reveals an abundance of promiscuous resistance determinants in Escherichia coli Proc. Natl. Acad. Sci. U S A 108 2011 1484 1489
11. C.J. Law, P.C. Maloney, and D.N. Wang Ins and outs of major facilitator superfamily antiporters Annu. Rev. Microbiol. 62 2008 289 305
12. M.H. Saier Jr., J.T. Beatty, A. Goffeau, K.T. Harley, W.H. Heijne, S.C. Huang, D.L. Jack, P.S. Jahn, K. Lew, J. Liu, S.S. Pao, I.T. Paulsen, T.T. Tseng, and P.S. Virk The major facilitator superfamily J. Mol. Microbiol. Biotechnol. 1 1999 257 279 (Pubitemid 129491947)
13. J. Abramson, I. Smirnova, V. Kasho, G. Verner, H.R. Kaback, and S. Iwata Structure and mechanism of the lactose permease of Escherichia coli Science 301 2003 610 615 (Pubitemid 36927939)
14. Y. Huang, M.J. Lemieux, J. Song, M. Auer, and D.N. Wang Structure and mechanism of the glycerol-3-phosphate transporter from Escherichia coli Science 301 2003 616 620 (Pubitemid 36927940)
15. T. Hirai, J.A. Heymann, D. Shi, R. Sarker, P.C. Maloney, and S. Subramaniam Three-dimensional structure of a bacterial oxalate transporter Nat. Struct. Biol. 9 2002 597 600 (Pubitemid 34816140)
16. Y. Yin, X. He, P. Szewczyk, T. Nguyen, and G. Chang Structure of the multidrug transporter EmrD from Escherichia coli Science 312 2006 741 744
17. S. Dang, L. Sun, Y. Huang, F. Lu, Y. Liu, H. Gong, J. Wang, and N. Yan Structure of a fucose transporter in an outward-open conformation Nature 467 2010 734 738
18. N. Fluman, and E. Bibi Bacterial multidrug transport through the lens of the major facilitator superfamily Biochim. Biophys. Acta 1794 2009 738 747
19. R. Edgar, and E. Bibi MdfA, an Escherichia coli multidrug resistance protein with an extraordinarily broad spectrum of drug recognition J. Bacteriol. 179 1997 2274 2280 (Pubitemid 27146882)
20. J. Adler, and E. Bibi Promiscuity in the geometry of electrostatic interactions between the Escherichia coli multidrug resistance transporter MdfA and cationic substrates J. Biol. Chem. 280 2005 2721 2729 (Pubitemid 40189378)
21. J. Adler, and E. Bibi Determinants of substrate recognition by the Escherichia coli multidrug transporter MdfA identified on both sides of the membrane J. Biol. Chem. 279 2004 8957 8965 (Pubitemid 38295957)
22. J. Adler, O. Lewinson, and E. Bibi Role of a conserved membrane-embedded acidic residue in the multidrug transporter MdfA Biochemistry 43 2004 518 525 (Pubitemid 38082575)
23. R. Edgar, and E. Bibi A single membrane-embedded negative charge is critical for recognizing positively charged drugs by the Escherichia coli multidrug resistance protein MdfA EMBO J. 18 1999 822 832 (Pubitemid 29082262)
24. O. Lewinson, J. Adler, G.J. Poelarends, P. Mazurkiewicz, A.J. Driessen, and E. Bibi The Escherichia coli multidrug transporter MdfA catalyzes both electrogenic and electroneutral transport reactions Proc. Natl. Acad. Sci. U S A 100 2003 1667 1672 (Pubitemid 36254505)
25. N. Sigal, E. Vardy, S. Molshanski-Mor, A. Eitan, Y. Pilpel, S. Schuldiner, and E. Bibi 3D model of the Escherichia coli multidrug transporter MdfA reveals an essential membrane-embedded positive charge Biochemistry 44 2005 14870 14880 (Pubitemid 41612266)
26. N. Sigal, O. Lewinson, S.G. Wolf, and E. Bibi E. coli multidrug transporter MdfA is a monomer Biochemistry 46 2007 5200 5208 (Pubitemid 46683018)
27. K. Nishino, T. Latifi, and E.A. Groisman Virulence and drug resistance roles of multidrug efflux systems of Salmonella enterica serovar Typhimurium Mol. Microbiol. 59 2006 126 141
28. A. Krogh, B. Larsson, G. von Heijne, and E.L. Sonnhammer Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes J. Mol. Biol. 305 2001 567 580 (Pubitemid 33032862)
29. M.A. Larkin, G. Blackshields, N.P. Brown, R. Chenna, P.A. McGettigan, H. McWilliam, F. Valentin, I.M. Wallace, A. Wilm, R. Lopez, J.D. Thompson, T.J. Gibson, and D.G. Higgins Clustal W and Clustal X version 2.0 Bioinformatics 23 2007 2947 2948 (Pubitemid 350162903)
30. L.M. Guzman, D. Belin, M.J. Carson, and J. Beckwith Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter J. Bacteriol. 177 1995 4121 4130
31. K.A. Datsenko, and B.L. Wanner One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products Proc. Natl. Acad. Sci. U S A 97 2000 6640 6645 (Pubitemid 30412767)
32. T. Baba, T. Ara, M. Hasegawa, Y. Takai, Y. Okumura, M. Baba, K.A. Datsenko, M. Tomita, B.L. Wanner, and H. Mori Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection Mol. Syst. Biol. 2 2006 2006 0008
33. O. Beja, and E. Bibi Functional expression of mouse Mdr1 in an outer membrane permeability mutant of Escherichia coli Proc. Natl. Acad. Sci. U S A 93 1996 5969 5974 (Pubitemid 26190786)
34. M. Auer, M.J. Kim, M.J. Lemieux, A. Villa, J. Song, X.D. Li, and D.N. Wang High-yield expression and functional analysis of Escherichia coli glycerol-3-phosphate transporter Biochemistry 40 2001 6628 6635 (Pubitemid 32552786)
35. H. Toyota, M. Hosokawa, I. Urabe, and T. Yomo Emergence of polyproline II-like structure at early stages of experimental evolution from random polypeptides Mol. Biol. Evol. 25 2008 1113 1119
36. T.I. Brelidze, A.E. Carlson, D.R. Davies, L.J. Stewart, and W.N. Zagotta Identifying regulators for EAG1 channels with a novel electrophysiology and tryptophan fluorescence based screen PloS One 5 2010
37. S.L. Ginn, M.H. Brown, and R.A. Skurray The TetA(K) tetracycline/H(+) antiporter from Staphylococcus aureus: mutagenesis and functional analysis of motif C J. Bacteriol. 182 2000 1492 1498 (Pubitemid 30121111)
38. G. von Heijne Membrane protein structure prediction. Hydrophobicity analysis and the positive-inside rule J. Mol. Biol. 225 1992 487 494
39. A. Rath, M. Glibowicka, V.G. Nadeau, G. Chen, and C.M. Deber Detergent binding explains anomalous SDS-PAGE migration of membrane proteins Proc. Natl. Acad. Sci. U S A 106 2009 1760 1765
40. X.D. Li, A. Villa, C. Gownley, M.J. Kim, J. Song, M. Auer, and D.N. Wang Monomeric state and ligand binding of recombinant GABA transporter from Escherichia coli FEBS Lett. 494 2001 165 169 (Pubitemid 32322676)
41. J.M. Boulter, and D.N. Wang Purification and characterization of human erythrocyte glucose transporter in decylmaltoside detergent solution Protein Expr. Purif. 22 2001 337 348 (Pubitemid 32608561)
42. A.R. Ferre-D'Amare, and S.K. Burley Use of dynamic light scattering to assess crystallizability of macromolecules and macromolecular assemblies Structure 2 1994 357 359
43. M.H. Brown, and R.A. Skurray Staphylococcal multidrug efflux protein QacA J. Mol. Microbiol. Biotechnol. 3 2001 163 170 (Pubitemid 32257899)
44. A.A. Neyfakh, C.M. Borsch, and G.W. Kaatz Fluoroquinolone resistance protein NorA of Staphylococcus aureus is a multidrug efflux transporter Antimicrob. Agents Chemother. 37 1993 128 129 (Pubitemid 23019184)
45. O. Lomovskaya, and K. Lewis Emr, an Escherichia coli locus for multidrug resistance Proc. Natl. Acad. Sci. U S A 89 1992 8938 8942
46. A. Kumar, and H.P. Schweizer Bacterial resistance to antibiotics: active efflux and reduced uptake Adv. Drug Deliv. Rev. 57 2005 1486 1513 (Pubitemid 40984603)
47. Y. Morita, A. Kataoka, S. Shiota, T. Mizushima, and T. Tsuchiya NorM of Vibrio parahaemolyticus is an Na(+)-driven multidrug efflux pump J. Bacteriol. 182 2000 6694 6697 (Pubitemid 32249252)
48. E.B. Tikhonova, and H.I. Zgurskaya AcrA, AcrB, and TolC of Escherichia coli form a stable intermembrane multidrug efflux complex J. Biol. Chem. 279 2004 32116 32124 (Pubitemid 39014658)
49. K. Nishino, E. Nikaido, and A. Yamaguchi Regulation and physiological function of multidrug efflux pumps in Escherichia coli and Salmonella Biochim. Biophys. Acta 1794 2009 834 843
50. I.T. Paulsen, and R.A. Skurray Topology, structure and evolution of two families of proteins involved in antibiotic and antiseptic resistance in eukaryotes and prokaryotes - an analysis Gene 124 1993 1 11 (Pubitemid 23065961)
51. I.T. Paulsen, R.A. Skurray, R. Tam, M.H. Saier Jr., R.J. Turner, J.H. Weiner, E.B. Goldberg, and L.L. Grinius The SMR family: a novel family of multidrug efflux proteins involved with the efflux of lipophilic drugs Mol. Microbiol. 19 1996 1167 1175 (Pubitemid 26111492)
52. S. Schuldiner, M. Lebendiker, and H. Yerushalmi EmrE, the smallest ion-coupled transporter, provides a unique paradigm for structure-function studies J. Exptl Biol. 200 1997 335 341 (Pubitemid 27126465)
53. T.R. Muth, and S. Schuldiner A membrane-embedded glutamate is required for ligand binding to the multidrug transporter EmrE EMBO J. 19 2000 234 240 (Pubitemid 30042705)
54. + symporter from Leishmania donovani J. Biol. Chem. 272 1997 24210 24215 (Pubitemid 27418621)
55. M.L. Zani, T. Pourcher, and G. Leblanc Mutagenesis of acidic residues in putative membrane-spanning segments of the melibiose permease of Escherichia coli. II. Effect on cationic selectivity and coupling properties J. Biol. Chem. 268 1993 3216 3221 (Pubitemid 23070947)
56. S. Vanni, P. Campomanes, M. Marcia, and U. Rothlisberger Ion binding and internal hydration in the multidrug resistance secondary active transporter NorM investigated by molecular dynamics simulations Biochemistry 51 2012 1281 1287
57. C.J. Law, J. Almqvist, A. Bernstein, R.M. Goetz, Y. Huang, C. Soudant, A. Laaksonen, S. Hovmoller, and D.N. Wang Salt-bridge dynamics control substrate-induced conformational change in the membrane transporter GlpT J. Mol. Biol. 378 2008 828 839
58. M. Fann, A.H. Davies, A. Varadhachary, T. Kuroda, C. Sevier, T. Tsuchiya, and P.C. Maloney Identification of two essential arginine residues in UhpT, the sugar phosphate antiporter of Escherichia coli J. Membr. Biol. 164 1998 187 195 (Pubitemid 28336996)
59. + antiporter of Escherichia coli Biochemistry 37 1998 5475 5480 (Pubitemid 28241928)
60. J. Abramson, S. Iwata, and H.R. Kaback Lactose permease as a paradigm for membrane transport proteins Mol. Membr. Biol. 21 2004 227 236 (Pubitemid 39208298)
61. M. Sahin-Toth, M.C. Lawrence, and H.R. Kaback Properties of permease dimer, a fusion protein containing two lactose permease molecules from Escherichia coli Proc. Natl. Acad. Sci. U.S.A 91 1994 5421 5425 (Pubitemid 24174339)
62. S.V. Ambudkar, V. Anantharam, and P.C. Maloney UhpT, the sugar phosphate antiporter of Escherichia coli, functions as a monomer J. Biol. Chem. 265 1990 12287 12292
63. C.G. Tate, I. Ubarretxena-Belandia, and J.M. Baldwin Conformational changes in the multidrug transporter EmrE associated with substrate binding J. Mol. Biol. 332 2003 229 242 (Pubitemid 36999743)
64. F.J. Sharom, R. Liu, Y. Romsicki, and P. Lu Insights into the structure and substrate interactions of the P-glycoprotein multidrug transporter from spectroscopic studies Biochim. Biophys. Acta 1461 1999 327 345
65. C.J. Law, G. Enkavi, D.N. Wang, and E. Tajkhorshid Structural basis of substrate selectivity in the glycerol-3-phosphate: phosphate antiporter GlpT Biophys. J. 97 2009 1346 1353
66. G.E. Dale, C. Oefner, and A. D'Arcy The protein as a variable in protein crystallization J. Struct. Biol. 142 2003 88 97 (Pubitemid 36457893)