E. coli multidrug transporter MdfA is a monomer

Biochemistry

Volumn 46, Issue 17, 2007, Pages 5200-5208

  Sigal, Nadejda ^a   Lewinson, Oded ^a,b   Wolf, Sharon G ^a   Bibi, Eitan ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b California Institute of Technology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ELECTRON CRYSTALLOGRAPHY; METAL AFFINITY CHROMATOGRAPHY; MULTIDRUG EXPORT; TOXIC COMPOUNDS;

AFFINITY CHROMATOGRAPHY; CRYSTALLOGRAPHY; ESCHERICHIA COLI; POSITIVE IONS; SIZE EXCLUSION CHROMATOGRAPHY; TOXIC MATERIALS; TWO DIMENSIONAL;

DRUG PRODUCTS;

BETA DODECYL MALTOPYRANOSIDE; CARRIER PROTEIN; MONOMER; PHOSPHOLIPID; PROTEIN MDFA; PYRANOSIDE; TETRAPHENYLPHOSPHONIUM; UNCLASSIFIED DRUG;

AFFINITY CHROMATOGRAPHY; ARTICLE; CRYSTAL STRUCTURE; ESCHERICHIA COLI; GEL PERMEATION CHROMATOGRAPHY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PURIFICATION; PROTEOLIPOSOME; SOLUBILIZATION;

CHROMATOGRAPHY, AFFINITY; CHROMATOGRAPHY, GEL; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CRYSTALLIZATION; DETERGENTS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MEMBRANE TRANSPORT PROTEINS; MICROSCOPY, ELECTRON;

EID: 34247621710     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi602405w     Document Type: Article

References (49)

1. Bolhuis, H., van Veen, H. W., Poolman, B., Driessen, A. J., and Konings, W. N. (1997) Mechanisms of multidrug transporters, FEMS Microbiol. Rev. 21, 55-84.
2. Putman, M., Van Veen, H. W., Degener, J. E., and Konings, W. N. (2000) Antibiotic resistance: era of the multidrug pump, Mol. Microbiol. 36, 772-773.
3. Edgar, R., and Bibi, E. (1997) MdfA, an Escherichia coli multidrug resistance protein with an extraordinarily broad spectrum of drug recognition, J. Bacteriol. 179, 2274-2280.
4. Jack, D. L., Storms, M. L., Tchieu, J. H., Paulsen, I. T., and Saier, M. H., Jr. (2000) A broad-specificity multidrug efflux pump requiring a pair of homologous SMR-type proteins, J. Bacteriol. 182, 2311-2313.
5. Lewis, K., Naroditskaya, V., Ferrante, A., and Fokina, I. (1994) Bacterial resistance to uncouplers, J. Bioenerg. Biomembr. 26, 639-646.
6. Zgurskaya, H. I., and Nikaido, H. (2000) Multidrug resistance mechanisms: drug efflux across two membranes, Mol. Microbiol. 37, 219-225.
7. Nikaido, H. (1994) Prevention of drug access to bacterial targets: permeability barriers and active efflux, Science 264, 382-388.
8. Paulsen, I. T. (2003) Multidrug efflux pumps and resistance: regulation and evolution, Curr. Opin. Microbiol. 6, 446-451.
9. Saier, M. H., Jr., and Paulsen, I. T. (2001) Phylogeny of multidrug transporters, Semin. Cell Dev. Biol. 12, 205-213.
10. Marger, M. D., and Saier, M. H., Jr. (1993) A major superfamily of transmembrane facilitators that catalyse uniport, symport and antiport, Trends Biochem. Sci. 18, 13-20.
11. Lewinson, O., Adler, J., Sigal, N., and Bibi, E. (2006) Promiscuity in multidrug recognition and transport: the bacterial MFS Mdr transporters, Mol. Microbiol. 61, 277-284.
12. Bibi, E., Adler, J., Lewinson, O., and Edgar, R. (2001) MdfA, an interesting model protein for studying multidrug transport, J. Mol. Microbiol. Biotechnol. 3, 171-177.
13. Sigal, N., Cohen-Karni, D., Siemion, S., and Bibi, E. (2006) MdfA from E. coli, a model protein for studying secondary multidrug transport, J. Mol. Microbiol. Biotechnol. 11, 308-317.
14. Jin, Q., Yuan, Z., Xu, J., Wang, Y., Shen, Y., Lu, W., Wang, J., Liu, H., Yang, J., Yang, F., Zhang, X., Zhang, J., Yang, G., Wu, H., Qu, D., Dong, J., Sun, L., Xue, Y., Zhao, A., Gao, Y., Zhu, J., Kan, B., Ding, K., Chen, S., Cheng, H., Yao, Z., He, B., Chen, R., Ma, D., Qiang, B., Wen, Y., Hou, Y., and Yu, J. (2002) Genome sequence of Shigella flexneri 2a: insights into pathogenicity through comparison with genomes of Escherichia coli K12 and O157, Nucleic Acids Res. 30, 4432-4441.
15. Parkhill, J., Dougan, G., James, K. D., Thomson, N. R., Pickard, D., Wain, J., Churcher, C., Mungall, K. L., Bentley, S. D., Holden, M. T., Sebaihia, M., Baker, S., Basham, D., Brooks, K., Chillingworth, T., Connerton, P., Cronin, A., Davis, P., Davies, R. M., Dowd, L., White, N., Farrar, J., Feltwell, T., Hamlin, N., Haque, A., Hien, T. T., Holroyd, S., Jagels, K., Krogh, A., Larsen, T. S., Leather, S., Moule, S., O'Gaora, P., Parry, C., Quail, M., Rutherford, K., Simmonds, M., Skelton, J., Stevens, K., Whitehead, S., and Barrell, B. G. (2001) Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18, Nature 413, 848-852.
16. Parkhill, J., Wren, B. W., Thomson, N. R., Titball, R. W., Holden, M. T., Prentice, M. B., Sebaihia, M., James, K. D., Churcher, C., Mungall, K. L., Baker, S., Basham, D., Bentley, S. D., Brooks, K., Cerdeno-Tarraga, A. M., Chillingworth, T., Cronin, A., Davies, R. M., Davis, P., Dougan, G., Feltwell, T., Hamlin, N., Holroyd, S., Jagels, K., Karlyshev, A. V., Leather, S., Moule, S., Oyston, P. C., Quail, M., Rutherford, K., Simmonds, M., Skelton, J., Stevens, K., Whitehead, S., and Barrell, B. G. (2001) Genome sequence of Yersinia pestis, the causative agent of plague, Nature 413, 523-527.
17. Lewinson, O., Adler, J., Poelarends, G. J., Mazurkiewicz, P., Driessen, A. J., and Bibi, E. (2003) The Escherichia coli multidrug transporter MdfA catalyzes both electrogenic and electroneutral transport reactions, Proc. Natl. Acad. Sci. U.S.A. 100, 1667-1672.
18. Mine, T., Monta, Y., Kataoka, A., Mizushima, T., and Tsuchiya, T. (1998) Evidence for chloramphenicol/H+ antiport in Cmr (MdfA) system of Escherichia coli and properties of the antiporter, J. Biochem. (Tokyo) 124, 187-193.
19. Lewinson, O., Padan, E., and Bibi, E. (2004) Alkalitolerance: a biological function for a multidrug transporter in pH homeostasis, Proc. Natl. Acad. Sci. U.S.A. 101, 14073-14078.
20. Adler, J., and Bibi, E. (2002) Membrane topology of the multidrug transporter MdfA: complementary gene fusion studies reveal a nonessential C-terminal domain, J. Bacteriol. 184, 3313-3320.
21. Edgar, R., and Bibi, E. (1999) A single membrane-embedded negative charge is critical for recognizing positively charged drugs by the Escherichia coli multidrug resistance protein MdfA, EMBO J. 18, 822-832.
22. Adler, J., and Bibi, E. (2004) Determinants of substrate recognition by the Escherichia coli multidrug transporter MdfA identified on both sides of the membrane, J. Biol. Chem. 279, 8957-8965.
23. Adler, J., and Bibi, E. (2005) Promiscuity in the geometry of electrostatic interactions between the Escherichia coli multidrug resistance transporter MdfA and cationic substrates, J. Biol. Chem. 280, 2721-2729.
24. Sigal, N., Vardy, E., Molshanski-Mor, S., Eitan, A., Pilpel, Y., Schuldiner, S., and Bibi, E. (2005) 3D model of the Escherichia coli multidrug transporter MdfA reveals an essential membrane-embedded positive charge, Biochemistry 44, 14870-14880.
25. Lewinson, O., and Bibi, E. (2001) Evidence for simultaneous binding of dissimilar substrates by the Escherichia coli multidrug transporter MdfA, Biochemistry 40, 12612-12618.
26. Butler, P. J., Ubarretxena-Belandia, L, Warne, T., and Tate, C. G. (2004) The Escherichia coli multidrug transporter EmrE is a dimer in the detergent-solubilised state, J. Mol. Biol. 340, 797-808.
27. Jap, B. K., Zulauf, M., Scheybani, T., Hefti, A., Baumeister, W., Aebi, U., and Engel, A. (1992) 2D crystallization: from art to science, Ultramicroscopy 46, 45-84.
28. Kuhlbrandt, W. (1992) Two-dimensional crystallization of membrane proteins, Q. Rev. Biophys. 25, 1-49.
29. Levy, D., Mosser, G., Lambert, O., Moeck, G. S., Bald, D., and Rigaud, J. L. (1999) Two-dimensional crystallization on lipid layer: A successful approach for membrane proteins, J. Struct. Biol. 127, 44-52.
30. Walz, T., and Grigorieff, N. (1998) Electron crystallography of two-dimensional crystals of membrane proteins, J. Struct. Biol. 121, 142-161.
31. Crowther, R. A., Henderson, R., and Smith, J. M. (1996) MRC image processing programs, J. Struct. Biol. 116, 9-16.
32. Agard, D. A. (1983) A least-squares method for determining structure factors in three-dimensional tilted-view reconstructions, J. Mol. Biol. 167, 849-852.
33. Adler, J., Lewinson, O., and Bibi, E. (2004) Role of a conserved membrane-embedded acidic residue in the multidrug transporter MdfA, Biochemistry 43, 518-525.
34. Raetz, C. R., and Dowhan, W. (1990) Biosynthesis and function of phospholipids in Escherichia coli, J. Biol. Chem. 265, 1235-1238.
35. Eskandari, S., Wright, E. M., Kreman, M., Starace, D. M., and Zampighi, G. A. (1998) Structural analysis of cloned plasma membrane proteins by freeze-fracture electron microscopy, Proc. Natl. Acad. Sci. U.S.A. 95, 11235-11240.
36. Conroy, M. J., Jamieson, S. J., Blakey, D., Kaufmann, T., Engel, A., Fotiadis, D., Merrick, M., and Bullough, P. A. (2004) Electron and atomic force microscopy of the trimeric ammonium transporter AmtB, EMBO Rep. 5, 1153-1158.
37. Williams, K. A., Geldmacher-Kaufer, U., Padan, E., Schuldiner, S., and Kuhlbrandt, W. (1999) Projection structure of NhaA, a secondary transporter from Escherichia coli, at 4.0 Å resolution, EMBO J. 18, 3558-3563.
38. Heymann, J. A., Sarker, R., Hirai, T., Shi, D., Milne, J. L., Maloney, P. C., and Subramaniam, S. (2001) Projection structure and molecular architecture of OxlT, a bacterial membrane transporter, EMBO J. 20, 4408-4413.
39. Hacksell, I., Rigaud, J. L., Purhonen, P., Fourcher, T., Hebert, H., and Leblanc, G. (2002) Projection structure at 8 Å resolution of the melibiose permease, an Na-sugar co-transporter from Escherichia coli, EMBO J. 21, 3569-3574.
40. Huang, Y., Lemieux, M. J., Song, J., Auer, M., and Wang, D. N. (2003) Structure and mechanism of the glycerol-3-phosphate transporter from Escherichia coli, Science 301, 616-620.
41. Abramson, J., Smirnova, I., Kasho, V., Verner, G., Kaback, H. R., and Iwata, S. (2003) Structure and mechanism of the lactose permease of Escherichia coli, Science 301, 610-615.
42. Rosenberg, M. F., Kamis, A. B., Aleksandrov, L. A., Ford, R. C., and Riordan, J. R. (2004) Purification and crystallization of the cystic fibrosis transmembrane conductance regulator (CFTR), J. Biol. Chem. 279, 39051-39057.
43. Yin, Y., He, X., Szewczyk, P., Nguyen, T., and Chang, G. (2006) Structure of the multidrug transporter EmrD from Escherichia coli, Science 312, 741-744.
44. Lemieux, M. J., Song, J., Kim, M. J., Huang, Y., Villa, A., Auer, M., Li, X. D., and Wang, D. N. (2003) Three-dimensional crystallization of the Escherichia coli glycerol-3-phosphate transporter: a member of the major facilitator superfamily, Protein Sci. 12, 2748-2756.
45. Guan, L., Smirnova, I. N., Verner, G., Nagamori, S., and Kaback, H. R. (2006) Manipulating phospholipids for crystallization of a membrane transport protein, Proc. Natl. Acad. Sci. U.S.A. 103, 1723-1726.
46. Heuberger, E. H., Veenhoff, L. M., Duurkens, R. H., Friesen, R. H., and Poolman, B. (2002) Oligomeric state of membrane transport proteins analyzed with blue native electrophoresis and analytical ultracentrifugation, J. Mol. Biol. 317, 591-600.
47. Kaufmann, T. C., Engel, A., and Remigy, H. W. (2006) A novel method for detergent concentration determination, Biophys. J. 90, 310-317.
48. Ravaud, S., Do Cao, M. A., Jidenko, M., Ebel, C., Le Maire, M., Jault, J. M., Di Pietro, A., Haser, R., and Aghajari, N. (2006) The ABC transporter BmrA from Bacillus subtilis is a functional dimer when in a detergent-solubilized state, Biochem. J. 395, 345-353.
49. Vardy, E., Arkin, I. T., Gottschalk, K. E., Kaback, H. R., and Schuldiner, S. (2004) Structural conservation in the major facilitator superfamily as revealed by comparative modeling, Protein Sci. 13, 1832-1840.