Structure and pH-induced structural rearrangements of the putative multidrug efflux pump EmrD in liposomes probed by site-directed spin labeling

Biochemistry

Volumn 52, Issue 45, 2013, Pages 7964-7974

  Steed, P Ryan ^a   Zou, Ping ^a   Trone, Kristin E ^a   McHaourab, Hassane S ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONFORMATIONAL CHANGE; CONFORMATIONAL SWITCHES; ELECTRON PARAMAGNETIC RESONANCE SPECTROSCOPY; FUNCTIONAL INFORMATION; MAJOR FACILITATOR SUPERFAMILY; MULTIDRUG EFFLUX PUMPS; SITE-DIRECTED SPIN LABELING; STRUCTURAL REARRANGEMENT;

LIPOSOMES; MAGNETIC RESONANCE;

ELECTRON SPIN RESONANCE SPECTROSCOPY;

AMPICILLIN; BENZALKONIUM CHLORIDE; CARBONYL CYANIDE CHLOROPHENYLHYDRAZONE; CARRIER PROTEIN; DOXORUBICIN; EMRD PROTEIN; ETHIDIUM; FLUORESCEIN; HYDROGEN TRANSPORTER PROTEIN; LIPOSOME; MAJOR FACILITATOR SUPERFAMILY PROTEIN; MEMBRANE PROTEIN; MULTIDRUG RESISTANCE PROTEIN; PROPIDIUM IODIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL CELL; CELL ASSAY; CELL FUNCTION; CELL SURVIVAL; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG TRANSPORT; ELECTRON SPIN RESONANCE; IN VITRO STUDY; LIPOSOMAL DELIVERY; MOLECULAR DYNAMICS; NONHUMAN; PH; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SITE DIRECTED MUTAGENESIS; SPIN LABELING;

ELECTRON SPIN RESONANCE SPECTROSCOPY; ESCHERICHIA COLI PROTEINS; HYDROGEN-ION CONCENTRATION; LIPOSOMES; MEMBRANE TRANSPORT PROTEINS; SPIN LABELS;

EID: 84887571225     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi4012385     Document Type: Article

References (42)

1. Law, C. J., Maloney, P. C., and Wang, D.-N. (2008) Ins and outs of major facilitator superfamily antiporters Annu. Rev. Microbiol. 62, 289-305
2. Fluman, N. and Bibi, E. (2009) Bacterial multidrug transport through the lens of the major facilitator superfamily Biochim. Biophys. Acta 1794, 738-747
3. Yan, N. (2013) Structural advances for the major facilitator superfamily (MFS) transporters Trends Biochem. Sci. 38, 151-159
4. Forrest, L. R., Krämer, R., and Ziegler, C. (2011) The structural basis of secondary active transport mechanisms Biochim. Biophys. Acta 1807, 167-188
5. Mazurkiewicz, P., Konings, W. N., and Poelarends, G. J. (2002) Acidic residues in the lactococcal multidrug efflux pump LmrP play critical roles in transport of lipophilic cationic compounds J. Biol. Chem. 277, 26081-26088
6. 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
7. Fluman, N., Ryan, C. M., Whitelegge, J. P., and Bibi, E. (2012) Dissection of mechanistic principles of a secondary multidrug efflux protein Mol. Cell 47, 777-787
8. Gbaguidi, B., Mazurkiewicz, P., Konings, W. N., Driessen, a J. M., Ruysschaert, J. M., and Vigano, C. (2004) Proton motive force mediates a reorientation of the cytosolic domains of the multidrug transporter LmrP Cell. Mol. Life Sci. 61, 2646-2657
9. Varela, M. F., Sansom, C. E., and Griffith, J. K. (1995) Mutational analysis and molecular modelling of an amino acid sequence motif conserved in antiporters but not symporters in a transporter superfamily Mol. Membr. Biol. 12, 313-319
10. Yaffe, D., Radestock, S., Shuster, Y., Forrest, L. R., and Schuldiner, S. (2013) Identification of molecular hinge points mediating alternating access in the vesicular monoamine transporter VMAT2 Proc. Natl. Acad. Sci. U.S.A. 110, E1332-1341
11. Iwaki, S., Tamura, N., Kimura-Someya, T., Nada, S., and Yamaguchi, A. (2000) Cysteine-scanning mutagenesis of transmembrane segments 4 and 5 of the Tn10-encoded metal-tetracycline/H+ antiporter reveals a permeability barrier in the middle of a transmembrane water-filled channel J. Biol. Chem. 275, 22704-22712
12. 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
13. 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
14. 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
15. Baker, J., Wright, S. H., and Tama, F. (2012) Simulations of substrate transport in the multidrug transporter EmrD Proteins 1620-1632
16. Masureel, M., Martens, C., Stein, R. A., Mishra, S., Ruysschaert, J.-M., Mchaourab, H. S., and Govaerts, C. Protonation of acidic residues triggers the conformational switch in the secondary multidrug transporter LmrP. Nat. Chem. Biol. 2013, in press
17. Mchaourab, H. S., Steed, P. R., and Kazmier, K. (2011) Toward the fourth dimension of membrane protein structure: insight into dynamics from spin-labeling EPR spectroscopy Structure 19, 1549-1561
18. Zou, P. and Mchaourab, H. S. (2009) Alternating access of the putative substrate-binding chamber in the ABC transporter MsbA J. Mol. Biol. 393, 574-585
19. Amadi, S. T., Koteiche, H. A., Mishra, S., and Mchaourab, H. S. (2010) Structure, dynamics, and substrate-induced conformational changes of the multidrug transporter EmrE in liposomes J. Biol. Chem. 285, 26710-26718
20. Hubbell, W. L., Mchaourab, H. S., Altenbach, C., and Lietzow, M. A. (1996) Watching proteins move using site-directed spin labeling Structure 4, 779-783
21. Naroditskaya, V., Schlosser, M. J., Fang, N. Y., and Lewis, K. (1993) An E coli gene emrD is involved in adaptation to low energy shock Biochem. Biophys. Res. Commun. 196, 803-809
22. Nishino, K. and Yamaguchi, A. (2001) Analysis of a complete library of putative drug transporter genes in Escherichia coli J. Bacteriol. 183, 5803-5812
23. Steed, P. R., Stein, R. A., Mishra, S., Goodman, M. C., and Mchaourab, H. S. (2013) Na(+)-Substrate coupling in the multidrug antiporter NorM probed with a spin-labeled substrate Biochemistry 52, 5790-5799
24. Koteiche, H. A., Reeves, M. D., and Mchaourab, H. S. (2003) Structure of the substrate binding pocket of the multidrug transporter EmrE: site-directed spin labeling of transmembrane segment 1 Biochemistry 42, 6099-6105
25. Fillingame, R. H. (1976) Purification of the carbodiimide-reactive protein component of the ATP energy-transducing system of Escherichia coli J. Biol. Chem. 251, 6630-6637
26. Tal, N. and 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
27. Mchaourab, H. S., Lietzow, M. A., Hideg, K., and Hubbell, W. L. (1996) Motion of spin-labeled side chains in T4 lysozyme correlation with protein structure and dynamics Biochemistry 35, 7692-7704
28. Altenbach, C., Greenhalgh, D. A., Khorana, H. G., and Hubbell, W. L. (1994) A collision gradient method to determine the immersion depth of nitroxides in lipid bilayers: application to spin-labeled mutants of bacteriorhodopsin Proc. Natl. Acad. Sci. U.S.A. 91, 1667-1671
29. Altenbach, C., Froncisz, W., Hemker, R., Mchaourab, H. S., and Hubbell, W. L. (2005) Accessibility of nitroxide side chains: absolute Heisenberg exchange rates from power saturation EPR Biophys. J. 89, 2103-2112
30. Dong, J., Yang, G., and Mchaourab, H. S. (2005) Structural basis of energy transduction in the transport cycle of MsbA Science 308, 1023-1028
31. Hakizimana, P., Masureel, M., Gbaguidi, B., Ruysschaert, J.-M., and Govaerts, C. (2008) Interactions between phosphatidylethanolamine headgroup and LmrP, a multidrug transporter: a conserved mechanism for proton gradient sensing? J. Biol. Chem. 283, 9369-9376
32. Rabenstein, M. D. and Shin, Y. K. (1995) Determination of the distance between two spin labels attached to a macromolecule Proc. Natl. Acad. Sci. U.S.A. 92, 8239-8243
33. Paulsen, I. T., Brown, M. H., and Skurray, R. a. (1996) Proton-dependent multidrug efflux systems Microbiol. Rev. 60, 575-608
34. Putman, M., van Veen, H. W., Poolman, B., and Konings, W. N. (1999) Restrictive use of detergents in the functional reconstitution of the secondary multidrug transporter LmrP Biochemistry 38, 1002-1008
35. Angevine, C. M. and Fillingame, R. H. (2003) Aqueous access channels in subunit a of rotary ATP synthase J. Biol. Chem. 278, 6066-6074
36. Pao, S. S., Paulsen, I. T., and Saier, M. H. (1998) Major facilitator superfamily Microbiol. Rev. 62, 1-34
37. Jiang, D., Zhao, Y., Wang, X., Fan, J., Heng, J., Liu, X., Feng, W., Kang, X., Huang, B., Liu, J., and Zhang, X. C. (2013) Structure of the YajR transporter suggests a transport mechanism based on the conserved motif A Proc. Natl. Acad. Sci. U.S.A. 110, 14664-14669
38. Smirnova, I., Kasho, V., Choe, J.-Y., Altenbach, C., Hubbell, W. L., and Kaback, H. R. (2007) Sugar binding induces an outward facing conformation of LacY Proc. Natl. Acad. Sci. U.S.A. 104, 16504-16509
39. Radestock, S. and Forrest, L. R. (2011) The alternating-access mechanism of MFS transporters arises from inverted-topology repeats J. Mol. Biol. 407, 698-715
40. Bolhuis, H., van Veen, H. W., Brands, J. R., Putman, M., Poolman, B., Driessen, A. J., and Konings, W. N. (1996) Energetics and mechanism of drug transport mediated by the lactococcal multidrug transporter LmrP J. Biol. Chem. 271, 24123-24128
41. Putman, M., van Veen, H. W., Degener, J. E., and Konings, W. N. (2001) The lactococcal secondary multidrug transporter LmrP confers resistance to lincosamides, macrolides, streptogramins and tetracyclines Microbiology (Reading, U. K.) 147, 2873-2880
42. 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