Two proton translocation pathways in a secondary active multidrug transporter

Journal of Molecular Microbiology and Biotechnology

Volumn 12, Issue 3-4, 2007, Pages 197-209

  Bapna, Akanksha ^a   Federici, Luca ^b   Venter, Henrietta ^a   Velamakanni, Saroj ^a   Luisi, Ben ^a   Fan, Tai Ping ^a   Van Veen, Hendrik W ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CHIETI   (Italy)

Author keywords

Carboxylate; Lactococcus lactis; Multidrug resistance; Proton coupling; Secondary active drug transport

Indexed keywords

ABC TRANSPORTER; ANTIPORTER; CARRIER PROTEIN; ETHIDIUM; GLYCEROL DERIVATIVE; GLYCOPROTEIN P; PROTON;

AMINO TERMINAL SEQUENCE; BACTERIAL STRAIN; CARBOXY TERMINAL SEQUENCE; CONFERENCE PAPER; CRYSTAL STRUCTURE; CYTOPLASM; ESCHERICHIA COLI; FLUORESCENCE; GENE TRANSLOCATION; LIPOPHILICITY; MEMBRANE VESICLE; MUTAGENESIS; NONHUMAN; PLASMID; PREDICTION; PROTEIN DETERMINATION; PROTEIN STRUCTURE; PROTON TRANSPORT; SEQUENCE HOMOLOGY; THREE DIMENSIONAL IMAGING; ULTRASTRUCTURE; WESTERN BLOTTING;

AMINO ACID SUBSTITUTION; ANTIPORTERS; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; ESCHERICHIA COLI; ETHIDIUM; LACTOCOCCUS LACTIS; MEMBRANE TRANSPORT PROTEINS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PROTEIN STRUCTURE, TERTIARY; PROTONS;

ESCHERICHIA COLI; LACTOCOCCUS LACTIS;

EID: 34250868387     PISSN: 14641801     EISSN: None     Source Type: Journal    
DOI: 10.1159/000099641     Document Type: Conference Paper

References (48)

1. Abramson J, Smirnova I, Kasho V, Verner G, Kaback HR, Iwata S: Structure and mechanism of the lactose permease of Escherichia coli. Science 2003; 301: 610-615.
2. Balakrishnan L, Venter H, Shilling RA, Van Veen HW: Reversible transport by the ATP-binding cassette multidrug export pump LmrA: ATP synthesis at the expense of downhill ethidium uptake. J Biol Chem 2004; 279: 11273-11280.
3. Bolhuis H, Poelarends G, Van Veen HW, Poolman B, Driessen AJ, Konings WN: The lactococcal LmrP gene encodes a proton motive force-dependent drug transporter. J Biol Chem 1995; 270: 26092-26098.
4. Bolhuis H, Van Veen HW, Brands JR, Putman M, Poolman B, Driessen AJ, Konings WN: Energetics and mechanism of drug transport mediated by the lactococcal multidrug transporter LmrP. J Biol Chem 1996; 271: 24123-24128.
5. Borst P, Elferink RO: Mammalian ABC transporters in health and disease. Annu Rev Biochem 2002; 71: 537-592.
6. De Ruyter P, Kuipers O, De Vos W: Controlled gene expression systems for Lactococcus lactis with the food-grade inducer nisin. Appl Environ Microbiol 1996; 62: 3662-3667.
7. Edgar R, Bibi E: A single membrane-embedded negative charge is critical for recognizing positively charged drugs by the Escherichia coli multidrug resistance protein MdfA. EMBO J 1999; 18: 822-832.
8. Eisenberg D, Luthy R, Bowie JU: VERIFY3D: assessment of protein models with three-dimensional profiles. Methods Enzymol 1997; 277: 396-404.
9. Gbaguidi B, Mazurkiewicz P, Konings WN, Driessen AJ, Ruysschaert JM, Vigano C: Proton motive force mediates a reorientation of the cytosolic domains of the multidrug transporter LmrP. Cell Mol Life Sci 2004; 61:2646-2657.
10. Guan L, Kaback HR: Lessons from lactose permease. Annu Rev Biophys Biomol Struct 2006; 35: 67-91.
11. Hirai T, Heymann JA, Shi D, Sarker R, Maloney PC, Subramaniam S: Three-dimensional structure of a bacterial oxalate transporter. Nat Struct Biol 2002; 9: 597-600.
12. Huang Y, Lemieux MJ, Song J, Auer M, Wang DN: Structure and mechanism of the glycerol-3-phosphate transporter from Escherichia coli. Science 2003; 301: 616-620.
13. Iwata S, Ostermeier C, Ludwig B, Michel H: Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 1995; 376: 660-669.
14. Janvilisri T, Venter H, Shahi S, Reuter G, Balakrishnan L, Van Veen HW: Sterol transport by the human breast cancer resistance protein (ABCG2) expressed in Lactococcus lactis. J Biol Chem 2003; 278: 20645-20651.
15. Kaback HR, Sahin-Toth M, Weinglass AB: The kamikaze approach to membrane transport. Nat Rev Mol Cell Biol 2001; 2: 610-620.
16. Konings WN: Microbial transport: adaptations to natural environments. Antonie Van Leeuwenhoek 2006; 90: 325-342.
17. Laskowski RA, Moss DS, Thornton JM: Mainchain bond lengths and bond angles in protein structures. J Mol Biol 1993; 231: 1049-1067.
18. Lewinson O, Adler J, Sigal N, Bibi E: Promiscuity in multidrug recognition and transport: the bacterial MFS Mdr transporters. Mol Microbiol 2006; 61: 277-284.
19. Macpherson A, Jones-Mortimer M, Horne P, Henderson P: Identification of the GalP galactose transport protein of Escherichia coli. J Biol Chem 1983; 258: 4390-4396.
20. Mazurkiewicz P, Driessen AJ, Konings WN: Energetics of wild-type and mutant multidrug resistance secondary transporter LmrP of Lactococcus lactis. Biochim Biophys Acta 2004a;1658: 252-261.
21. Mazurkiewicz P, Konings WN, Poelarends GJ: Acidic residues in the lactococcal multidrug efflux pump LmrP play critical roles in transport of lipophilic cationic compounds. J Biol Chem 2002; 277: 26081-26088.
22. Mazurkiewicz P, Poelarends GJ, Driessen AJ, Konings WN: Facilitated drug influx by an energy-uncoupled secondary multidrug transporter. J Biol Chem 2004b;279: 103-108.
23. McKeegan KS, Borges-Walmsley MI, Walmsley AR: The structure and function of drug pumps: an update. Trends Microbiol 2003; 11: 21-29.
24. Mizuguchi K, Deane CM, Blundell TL, Johnson MS, Overington JP: JOY: protein sequence-structure representation and analysis. Bioinformatics 1998; 14: 617-623.
25. Muth TR, Schuldiner S: A membrane-embedded glutamate is required for ligand binding to the multidrug transporter EmrE. EMBO J 2000; 19: 234-240.
26. Nikaido H: Preventing drug access to targets: cell surface permeability barriers and active efflux in bacteria. Semin Cell Dev Biol 2001; 12: 215-223.
27. Paternostre MT, Roux M, Rigaud JL: Mechanisms of membrane protein insertion into liposomes during reconstitution procedures involving the use of detergents. 1. Solubilization of large unilamellar liposomes (prepared by reverse-phase evaporation) by triton X-100, octyl glucoside, and sodium cholate. Biochemistry 1988; 27: 2668-2677.
28. Paulsen IT, Brown MH, Skurray RA: Proton-dependent multidrug efflux systems. Microbiol Rev 1996; 60: 575-608.
29. Putman M, Van Veen HW, Konings WN: Molecular properties of bacterial multidrug transporters. Microbiol Mol Biol Rev 2000; 64: 672-693.
30. Putman M, Van Veen HW, Poolman B, Konings WN: Restrictive use of detergents in the functional reconstitution of the secondary multidrug transporter LmrP. Biochemistry 1999; 38: 1002-1008.
31. Reuter G, Janvilisri T, Venter H, Shahi S, Balakrishnan L, Van Veen HW: The ATP binding cassette multidrug transporter LmrA and lipid transporter MsbA have overlapping substrate specificities. J Biol Chem 2003; 278: 35193-35198.
32. Saidijam M, Benedetti G, Ren Q, Xu Z, Hoyle CJ, Palmer SL, Ward A, Bettaney KE, Szakonyi G, Meuller J, Morrison S, Pos MK, Butaye P, Walravens K, Langton K, Herbert RB, Skurray RA, Paulsen IT, O'Reilly J, Rutherford NG, Brown MH, Bill RM, Henderson PJF: Microbial drug efflux proteins of the major facilitator superfamily. Curr Drug Targets 2006; 7: 793-811.
33. Saier MH Jr: Vectorial metabolism and the evolution of transport systems. J Bacteriol 2000; 182: 5029-5035.
34. Saier MH Jr, Paulsen IT, Sliwinski MK, Pao SS, Skurray RA, Nikaido H: Evolutionary origins of multidrug and drug-specific efflux pumps in bacteria. FASEB J 1998; 12: 265-274.
35. Sali A, Blundell TL: Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 1993; 234: 779-815.
36. Salje J, Ludwig B, Richter OM: Is a third proton-conducting pathway operative in bacterial cytochrome c oxidase? Biochem Soc Trans 2005; 33: 829-831.
37. Sanner MF: Python: a programming language for software integration and development. J Mol Graphics Mod 1999; 17: 57-61.
38. Shi J, Blundell TL, Mizuguchi K: FUGUE: sequence-structure homology recognition using environment-specific substitution tables and structure-dependent gap penalties. J Mol Biol 2001; 310: 243-257.
39. Shilling R, Federici L, Walas F, Venter H, Velamakanni S, Woebking B, Balakrishnan L, Luisi B, Van Veen HW: A critical role of a carboxylate in proton conduction by the ATP-binding cassette multidrug transporter LmrA. FASEB J 2005; 19: 1698-1700.
40. Stebbings LA, Mizuguchi K: HOMSTRAD: recent developments of the homologous protein structure alignment database. Nucleic Acids Res 2004; 32:D203-D207.
41. + antiport: complete cysteine-scanning mutagenesis and the protein engineering approach. Curr Opin Chem Biol 2003; 7: 570-579.
42. Van Veen HW: Towards the molecular mechanism of prokaryotic and eukaryotic multidrug transporters. Semin Cell Dev Biol 2001; 12: 239-245.
43. Van Veen HW, Konings WN: Multidrug transporters from bacteria to man: similarities in structure and function. Semin Cancer Biol 1997; 8: 183-191.
44. Venter H, Shahi S, Balakrishnan L, Velamakanni S, Bapna A, Woebking B, van Veen HW: Similarities between ATP-dependent and ion-coupled multidrug transporters. Biochem Soc Trans 2005; 33: 1008-1011.
45. Venter H, Shilling RA, Velamakanni S, Balakrishnan L, Van Veen HW: An ABC transporter with a secondary-active multidrug translocator domain. Nature 2003; 426: 866-870.
46. Woebking B, Reuter G, Shilling RA, Velamakanni S, Shahi S, Venter H, Balakrishnan L, Van Veen HW: Drug-lipid A interactions on the Escherichia coli ABC transporter MsbA. J Bacteriol 2005; 187: 6363-6369.
47. + and substrate fluxes based on 'time-sharing' of a common binding site. Biochemistry 2000; 39: 14711-14719.
48. Yin Y, He X, Szewczyk P, Nguyen T, Chang G: Structure of the multidrug transporter EmrD from Escherichia coli. Science 2006; 312: 741-744.