Lipid bilayer composition influences small multidrug transporters

BMC Biochemistry

Volumn 9, Issue 1, 2008, Pages

  Charalambous, Kalypso ^a   Miller, David ^b   Curnow, Paul ^b   Booth, Paula J ^b  

^a UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; GLYCOPROTEIN P; MEMBRANE PROTEIN; PHOSPHATIDYLETHANOLAMINE; PROTEIN EMRE; PROTEIN TBSMR; UNCLASSIFIED DRUG; ANTIPORTER; EMRE PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN; VIOLOGEN;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; LIPID BILAYER; LIPID COMPOSITION; MEMBRANE TRANSPORT; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN TRANSPORT; CHEMISTRY; ESCHERICHIA COLI; METABOLISM; METHYLATION; MULTIDRUG RESISTANCE; TRANSPORT AT THE CELLULAR LEVEL;

ESCHERICHIA COLI; MYCOBACTERIUM TUBERCULOSIS;

ANTIPORTERS; BIOLOGICAL TRANSPORT; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; LIPID BILAYERS; METHYLATION; VIOLOGENS;

EID: 58149097062     PISSN: None     EISSN: 14712091     Source Type: Journal    
DOI: 10.1186/1471-2091-9-31     Document Type: Article

References (48)

1. The SMR family: a novel family of multidrug efflux proteins involved with the efflux of lipophilic drugs. I Paulsen R Skurray R Tam M Saier R Turner J Weiner E Goldberg L Grinius, Mol Microbiol 1996 19 1167 1175 10.1111/j.1365-2958.1996.tb02462.x 8730859
2. Determining the Secondary Structure and Orientation of EmrE, a Multi-Drug Transporter, Indicates a Transmembrane Four-Helix Bundle. I Arkin W Russ M Lebendiker S Schuldiner, Biochemistry 1996 35 7233 7238 10.1021/bi960094i 8679552
3. The projection structure of EmrE, a proton-linked multidrug transporter from Escherichia coli, at 7 angstroms resolution. CG Tate ERS Kunji M Lebendiker S Schuldiner, EMBO J 2001 20 77 81 11226157 10.1093/emboj/20.1.77
4. Three-dimensional structure of the bacterial multidrug transporter EmrE shows it is an asymmetric homodimer. I Ubarretxena-Belandia JM Baldwin S Schuldiner CG Tate, EMBO J 2003 22 23 6175 6181 14633977 10.1093/emboj/cdg611
5. A membrane-embedded glutamate is required for ligand binding to the multidrug transporter EmrE. TR Muth S Schuldiner, EMBO J 2000 19 234 240 10637227 10.1093/emboj/19.2.234
6. Direct evidence for substrate-induced proton release in detergent-solubilized EmrE, a multidrug transporter. M Soskine Y Adam S Schuldiner, J Biol Chem 2004 279 11 9951 9955 10.1074/jbc.M312853200 14701800
7. Functional analysis of novel multidrug transporters from human pathogens. S Ninio D Rotem S Schuldiner, J Biol Chem 2001 276 48250 48256 11574548
8. + and Is Soluble in Organic Solvents. H Yerushalmi M Lebendiker S Schuldiner, Journal of Biological Chemistry 1995 270 12 6856 6863 10.1074/jbc.270.12.6856 7896833
9. The Escherichia coli multidrug transporter EmrE is a dimer in the detergent-solubilised state. PJ Butler I Ubarretxena-Belandia T Warne CG Tate, J Mol Biol 2004 340 4 797 808 10.1016/j.jmb.2004.05.014 15223321
10. When biochemistry meets structural biology: the cautionary tale of EmrE. S Schuldiner, Trends Biochem Sci 2007 32 6 252 258 10.1016/j.tibs.2007.04.002 17452106
11. On parallel and antiparallel topology of a homodimeric multidrug transporter. M Soskine S Mark N Tayer R Mizrachi S Schuldiner, J Biol Chem 2006 281 47 36205 36212 10.1074/jbc.M607186200 17003034
12. Emulating membrane protein evolution by rational design. M Rapp S Seppala E Granseth G von Heijne, Science 2007 315 5816 1282 1284 10.1126/science. 1135406 17255477
13. X-ray structure of EmrE supports dual topology model. YJ Chen O Pornillos S Lieu C Ma AP Chen G Chang, Proc Natl Acad Sci USA 2007 104 48 18999 19004 18024586
14. Mycobacterium and other actinomycetes. P Brennan, Microbial Lipids London: Academic Press, Ratledge C, Wilkinson SG, 1998 I 203 298
15. Compartmentalization of lipid biosynthesis in mycobacteria. YS Morita R Velasquez E Taig RF Waller JH Patterson D Tull SJ Williams H Billman-Jacobe MJ McConville, J Biol Chem 2005 280 22 21645 21652 10.1074/jbc.M414181200 15805104
16. Intrinsic curvature hypothesis for biomembrane lipid composition: a role for nonbilayer lipids. SM Gruner, Proc Natl Acad Sci USA 1985 82 3665 3669 3858841 10.1073/pnas.82.11.3665
17. Elastic properties of lipid bilayers: theory and possible experiments. W Helfrich, Z Naturforsch [C] 1973 28 11 693 703 4273690
18. Structure of the inverted hexagonal (HII) phase, and non-lamellar phase transitions of lipids. JM Seddon, Biochim Biophys Acta 1990 1031 1 69 2407291
19. The activation energy for insertion of transmembrane alpha-helices is dependent on membrane composition. W Meijberg PJ Booth, J Mol Biol 2002 319 839 853 10.1016/S0022-2836(02)00342-X 12054874
20. Controlling the folding efficiency of an integral membrane protein. SJ Allen AR Curran RH Templer W Meijberg PJ Booth, J Mol Biol 2004 342 1293 1304 10.1016/j.jmb.2004.07.041 15351652
21. Probability of Alamethicin conductance states varies with nonlamellar tendency of bilayer phospholipids. SLBS Keller SM Gruner MW Tate I Vodyanoy VA Parsegian, Biophys J 1993 65 1 23 27 8369434
22. Correlation between the free energy of a channel-forming voltage-gated peptide and the spontaneous curvature of bilayer lipids. JR Lewis DS Cafiso, Biochemistry 1999 38 5932 5938 10.1021/bi9828167 10231547
23. Physical properties of the fluid lipid-bilayer component of cell membranes: a perspective. M Bloom E Evans OG Mouritsen, Q Rev Biophys 1991 24 3 293 397 1749824
24. Functional consequences of lipid packing stress. SM Bezrukov, Curr Op Coll Int Sci 2000 5 237 243 10.1016/S1359-0294(00)00061-3
25. The reconstitution and activity of the small multidrug transporter EmrE is modulated by non-bilayer lipid composition. P Curnow M Lorch K Charalambous PJ Booth, J Mol Biol 2004 343 213 222 10.1016/j.jmb.2004.08.032 15381431
26. A single carboxyl mutant of the multidrug transporter EmrE is fully functional. H Yerushalmi S Mordoch S Schuldiner, Journal of Biological Chemistry 2001 276 16 12744 12748 10.1074/jbc.M010979200 11278804
27. An amino acid cluster around the essential Glu-14 is part of the substrate- and proton-binding domain of EmrE, a multidrug transporter from Escherichia coli. N Gutman S Steiner-Mordoch S Schuldiner, J Biol Chem 2003 278 18 16082 16087 10.1074/jbc.M213120200 12590142
28. EmrE, a multidrug transporter from Escherichia coli, transports monovalent and divalent substrates with the same stoichiometry. D Rotem S Schuldiner, J Biol Chem 2004 279 47 48787 48793 10.1074/jbc.M408187200 15371426
29. The relationship between membrane fluidity and permeabilities to water, solutes, ammonia, and protons. MB Lande JM Donovan ML Zeidel, J Gen Physiol 1995 106 1 67 84 7494139 10.1085/jgp.106.1.67
30. Reconstituting the barrier properties of a water-tight epithelial membrane by design of leaflet-specific liposomes. WG Hill ML Zeidel, J Biol Chem 2000 275 39 30176 30185 10.1074/jbc.M003494200 10903312
31. Effect of cardiolipin on proton permeability of phospholipid liposomes: the role of hydration at the lipid-water interface. QP Chen QT Li, Arch Biochem Biophys 2001 389 2 201 206 10.1006/abbi.2001.2319 11339809
32. Transmembrane electron transfer mediated by a viologen: a mechanism involving diffusion of doubly reduced viologen formed by disproportionation of viologen radical. L Hammarstrom M Almgren T Norby, J Phys Chem 1992 96 5017 5024 10.1021/j100191a052
33. Probing the interface between membrane proteins and membrane lipids by X-ray crystallography. PK Fyfe KE McAuley AW Roszak NW Isaacs RJ Cogdell MR Jones, Trends Biochem Sci 2001 26 106 112 10.1016/S0968-0004(00)01746-1 11166568
34. The phospholipid requirement for activity of the lactose carrier of Escherichia Coli. CC Chen TH Wilson, J Biol Chem 1984 259 10150 10158 6381481
35. Phosphlipid-assisted protein folding: phosphatidylethanolamine is required at a late step of the conformational maturation of the polytopic membrane protein lactose permease. M Bogdanov W Dowhan, EMBO J 1998 17 5255 5264 9736605 10.1093/emboj/17.18.5255
36. Lipid-assisted protein folding. M Bogdanov W Dowhan, J Biol Chem 1999 274 36827 36830 10.1074/jbc.274.52.36827 10601231
37. Reversible topological organization within a polytopic membrane protein is governed by a change in membrane phospholipid composition. W Zhang M Bogdanov J Pi AJ Pittard W Dowhan, J Biol Chem 2003 278 50 50128 50135 10.1074/jbc.M309840200 14525982
38. Topology of polytopic membrane protein subdomains is dictated by membrane phospholipid composition. X Wang M Bogdanov W Dowhan, Embo J 2002 21 21 5673 5681 12411485 10.1093/emboj/cdf571
39. Phospholipids as determinants of membrane protein topology. Phosphatidylethanolamine is required for the proper topological organization of the gamma-aminobutyric acid permease (GabP) of Escherichia coli. W Zhang HA Campbell SC King W Dowhan, J Biol Chem 2005 280 28 26032 26038 10.1074/jbc.M504929200 15890647
40. Conformational changes in a bacterial multidrug transporter are phosphatidylethanolamine-dependent. B Gbaguidi P Hakizimana G Vandenbussche JM Ruysschaert, Cell Mol Life Sci 2007 64 12 1571 1582 10.1007/s00018-007-7031-0 17530171
41. Interactions between phosphatidylethanolamine headgroup and LmrP, a multidrug transporter: a conserved mechanism for proton gradient sensing? P Hakizimana M Masureel B Gbaguidi JM Ruysschaert C Govaerts, J Biol Chem 2008 283 14 9369 9376 10.1074/jbc.M708427200 18234676
42. The membrane lipid environment modulates drug interactions with the P-glycoprotein multidrug transporter. Y Romsicki FJ Sharom, Biochemistry 1999 38 21 6887 6896 10.1021/bi990064q 10346910
43. Insertion kinetics of a denatured alpha helical membrane protein into phospholipid bilayer vesicles. M Lorch PJ Booth, J Mol Biol 2004 344 1109 1121 10.1016/j.jmb.2004.09.090 15544815
44. Modulation of folding and assembly of the membrane protein bacteriorhodopsin by intermolecular forces within the lipid bilayer. AR Curran RH Templer PJ Booth, Biochemistry 1999 38 9328 9336 10.1021/bi982322+ 10413507
45. Complete genome sequence of Methanobacterium thermoautotrophicum deltaH: functional analysis and comparative genomics. DR Smith LA Doucette-Stamm C Deloughery H Lee J Dubois T Aldredge R Bashirzadeh DCR Blakely K Gilbert D Harrison L Hoang P Keagle W Lumm B Pothier D Qiu R Spadafora R Vicaire Y Wang J Wierzbowski R Gibson N Jiwani A Caruso D Bush JN Reeve, J Bacteriol 1997 179 7135 7155 9371463
46. A membrane-associated form of sucrose synthase and its potential role in synthesis of cellulose and callose in plants. Y Amor CH Haigler S Johnson M Wainscott DP Delmer, Proc Natl Acad Sci USA 1995 92 20 9353 9357 7568131 10.1073/pnas.92.20.9353
47. Rapid immunodetection on polyvinylidene fluoride membrane blots without blocking. MA Mansfield, Anal Biochem 1995 229 1 140 143 10.1006/abio.1995.1391 8533884
48. Ectopic expression of alkaline phosphatase in proximal tubular brush border membrane of human renal cell carcinoma. R Prasad S Lambe P Kaler S Pathania S Kumar S Attri SK Singh, Biochim Biophys Acta 2005 1741 3 240 245 16081252