Multidrug-exporting secondary transporters

Current Opinion in Structural Biology

Volumn 13, Issue 4, 2003, Pages 443-452

  Murakami, Satoshi ^a,b   Yamaguchi, Akihito ^a,b  

^a OSAKA UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN;

CYTOPLASM; ESCHERICHIA COLI; GRAM NEGATIVE BACTERIUM; MEMBRANE CHANNEL; MULTIDRUG RESISTANCE; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN TRANSPORT; REVIEW;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA;

EID: 0042430540     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-440X(03)00109-X     Document Type: Review

References (50)

1. Nikaido H. Antibiotic resistance caused by Gram-negative multidrug efflux pumps. Clin Infect Dis. 27:1998;S32-S41.
2. Hancock R.E., Woodruff W.A. Roles of porin and β-lactamase in β-lactam resistance of Pseudomonas aeruginosa. Rev Infect Dis. 10:1988;770-775.
3. Poole K., Krebes K., McNally C., Neshat S. Multiple antibiotic resistance in Pseudomonas aeruginosa: evidence for involvement of efflux operon. J Bacteriol. 175:1993;7363-7372.
4. Okusu H., Ma D., Nikaido H. AcrAB efflux pump plays a major role in the antibiotic resistance phenotype of Escherichia coli multiple-antibiotic-resistance (Mar) mutants. J Bacteriol. 178:1996;306-308.
5. Zgurskaya H.I., Nikaido H. Multidrug resistance mechanisms: drug efflux across two membranes. Mol Microbiol. 37:2000;219-225.
6. Paulsen I.T., Sliwinski M.K., Saier M.H. Microbial genome analysis: global comparisons of transport capabilities based on phylogenies, bioenergetics and substrate specificities. J Mol Biol. 277:1998;573-592.
7. Paulsen I.T., Nguyen L., Sliwinski M.K., Rabus R., Saier M.H. Microbial genome analysis: comparative transport capabilities in eighteen prokaryotes. J Mol Biol. 301:2000;75-100.
8. Nishino K., Yamaguchi A. Analysis of a complete library of putative drug transporter genes in Escherichia coli. J Bacteriol. 183:2001;5803-5812.
9. Nikaido H. Multidrug efflux pumps of Gram-negative bacteria. J Bacteriol. 178:1996;5853-5859.
10. Van Veen H.W., Konings W.N. Drug efflux proteins in multidrug resistant bacteria. Biol Chem. 378:1997;769-777.
11. Putman M., van Veen H.W., Konings W.N. Molecular properties of bacterial multidrug transporters. Microbiol Mol Biol Rev. 64:2000;672-693.
12. Brown M.H., Paulsen I.T., Skurray R.A. The multidrug efflux protein NorM is a prototype of a new family of transporters. Mol Microbiol. 31:1999;394-395.
13. McMurry L., Petrucci R.E. Jr., Levy S.B. Active efflux of tetracycline encoded by four genetically different tetracycline resistance determinants in Escherichia coli. Proc Natl Acad Sci USA. 77:1980;3974-3977.
14. Yamaguchi A., Udagawa T., Sawai T. Transport of divalent cations with tetracycline as mediated by the transposon Tn10-encoded tetracycline resistance protein. J Biol Chem. 265:1990;4809-4813.
15. Sulavik M.C., Houseweart C., Cramer C., Jiwani N., Murgolo N., Greene J., DiDomenico B., Shaw K.J., Miller G.H., Hare R., Shimer G. Antibiotic susceptibility profiles of Escherichia coli strains lacking multidrug efflux pump genes. Antimicrob Agents Chemother. 45:2001;1126-1136.
16. Rouch D.A., Cram D.S., DiBerardino D., Littlejohn T.G., Skurry R.A. Efflux-mediated antiseptic resistance gene qac A from Staphylococcus aureus: common ancestry with tetracycline- and sugar-transport proteins. Mol Microbiol. 4:1990;2051-2062.
17. Neyfakh A.A., Borsch C.M., Kaatz G.W. Fluoroquinolone resistance protein NorA of Staphylococcus aureus is a multidrug efflux transporter. Antimicrob Agents Chemother. 37:1993;128-129.
18. Bolhuis H., Poelarends G., van Veen H.W., Poolman B., Driessen A.J., Konings W.N. The lactococcal lmrP gene encodes a proton motive force-dependent drug transporter. J Biol Chem. 270:1995;26092-26098.
19. Dean M., Rzhetsky A., Alikmets R. The human ATP-binding cassette (ABC) transporter superfamily. Genome Res. 11:2000;1156-1166.
20. Van Veen H.W., Callaghan R., Soceneantu L., Sardini A., Konings W.N., Higgins C.F. A bacterial antibiotic-resistance gene that complements the human multidrug-resistance P-glycoprotein gene. Nature. 391:1998;291-295.
21. Kobayashi N., Nishino K., Yamaguchi A. Novel macrolide-specific ABC-type efflux transporter in Escherichia coli. J Bacteriol. 183:2001;5639-5644.
22. Dinh T., Paulsen I.T., Saier M.H. Jr. A family of extracytoplasmic proteins that allow transport of large molecules across the outer membranes of Gram-negative bacteria. J Bacteriol. 176:1994;3825-3831.
23. Paulsen I.T., Park J.H., Cjoi P.S., Saier M.H. Jr. A family of Gram-negative bacterial outer membrane factors that function in the export of proteins, carbohydrates, drugs and heavy metals from Gram-negative bacteria. FEMS Microbiol Lett. 156:1997;1-8.
24. Zgurskaya H.I., Nikaido H. Bypassing the periplasm: reconstitution of the AcrAB multidrug efflux pump of Escherichia coli. Proc Natl Acad Sci USA. 96:1999;7190-7195.
25. Nikaido H. How do exported proteins and antibiotics bypass the periplasm in Gram-negative bacterial cells? Trends Microbiol. 8:2000;489-493.
26. Poole K. Multidrug efflux pumps and antimicrobial resistance in Pseudomonas aeruginosa and related organisms. J Mol Microbiol Biotechnol. 3:2001;255-264.
27. Nishino K, Yamada J, Hirakawa H, Hirata T, Yamaguchi A: Roles of TolC-dependent type multidrug transporters in Escherichia coli resistance to β-lactam antibiotics. Antimicrob Agents Chemother 2003, 47 in press.
28. Nikaido H., Zgurskaya H.I. AcrB and related multidrug efflux pumps of Escherichia coli. J Mol Microbiol Biotechnol. 3:2001;215-218.
29. Dutt A., Heath L.A., Nelson J.A. P-glycoprotein and organic cation secretion by the mammalian kidney. J Pharmacol Exp Ther. 269:1994;1254-1260.
30. Keppler D., Cui Y., Konig J., Nies A. Export pumps for anionic conjugates encoded by MRP genes. Adv Enzyme Regul. 39:1999;237-246.
31. Bolhuis H., van Veen H.W., Molenaar D., Poolman B., Driessen A.J., Konings W.N. Multidrug resistance in Lactococcus lactis: evidence for ATP-dependent drug extrusion from the inner leaflet of the cytoplasmic membrane. EMBO J. 15:1996;4239-4245.
32. Bolhuis H., van Veen H.W., Brands J.R., Putman M., Poolman B., Driessen A.J., Konings W.N. Energetics and mechanisms of drug transport mediated by the lactococcal multidrug transporter LmrP. J Biol Chem. 271:1996;24123-24128.
33. Li X.Z., Ma D., Livermore D.M., Nikaido H. Role of efflux pump(s) in intrinsic resistance of Pseudomonas aeruginosa: active efflux as a contributing factor to β-lactam resistance. Antimicrob Agents Chemother. 38:1994;1742-1752.
34. Koronakis V., Sharff A., Koronakis E., Luisi B., Hughes C. Crystal structure of the bacterial membrane protein TolC central multidrug efflux and protein export. Nature. 405:2000;914-919.
35. Zgurskaya H.I., Nikaido H. AcrA is a highly asymmetric protein capable of spanning the periplasm. J Mol Biol. 285:1999;409-420.
36. Murakami S., Nakashima R., Yamashita E., Yamaguchi A. Crystal structure of bacterial multidrug efflux transporter AcrB. Nature. 419:2002;587-593 We report the first crystal structure determination of a multidrug efflux transporter. This is also the first structure of a proton-coupled active transporter. It is a trimer that looks like a jellyfish. It has three vestibules open to periplasm for taking up substrates and a top funnel that might directly dock with TolC.
37. Chang G., Roth C.B. Structure of MsbA from E. coli: a homolog of the multidrug resistance ATP binding cassette (ABC) transporters. Science. 293:2001;1793-1800.
38. Locher K.P., Lee A.T., Rees D.C. The E. coli BtuCD structure: a framework for ABC transporter architecture and mechanism. Science. 296:2002;1091-1098 The authors report the crystal structure of the ABC transporter BtuCD, which takes up vitamin B12.
39. Elkins C.A., Nikaido H. 3D structure of AcrB: the archetypical multidrug efflux transporter of Escherichia coli likely captures substrates from periplasm. Drug Resist Updat. 6:2003;9-13 The authors review our three-dimensional structure determination of AcrB and emphasize the significance of the structure determination for understanding the multidrug exporting mechanism.
40. Elkins C.A., Nikaido H. Substrate specificity of the RND-type multidrug efflux pumps AcrB and AcrD of Escherichia coli is determined predominantly by two large periplasmic loops. J Bacteriol. 184:2002;6490-6498 On the basis of a loop exchange experiment, the authors report that the substrate specificity of the RND-type multidrug exporters AcrB and AcrD in E. coli is determined by large periplasmic loops.
41. Tikhonova E.B., Wang Q., Zgurskaya H.I. Chimeric analysis of the multicomponent multidrug efflux transporters from Gram-negative bacteria. J Bacteriol. 184:2002;6499-6507.
42. Eda S., Maeda H., Nakae T. An elegant means of self-protection in Gram-negative bacteria by recognizing and extruding xenobiotics from the periplasmic space. J Biol Chem. 278:2003;2085-2088.
43. Mao W., Warren M.S., Black D.S., Satou T., Murata T., Nishino T., Gotoh N., Lomovskaya O. On the mechanism of substrate specificity by resistance nodulation division (RND)-type multidrug resistance pumps: the large periplasmic loops of MexD from Pseudomonas aeruginosa are involved in substrate recognition. Mol Microbiol. 46:2002;889-901.
44. Yu E.W., McDermott G., Zgurskaya H.I., Nikaido H., Koshland D.E. Jr. Structural basis of multiple drug-binding capacity of the AcrB multidrug efflux pump. Science. 300:2003;976-980 A crystal structure determination of ligand-bound forms of AcrB with four different ligands. Three molecules of ligand bind simultaneously to the central cavity. Different ligands use different sets of residues of AcrB.
45. Schumacher M.A., Miller M.C., Grkovic S., Brown M.H., Skurry R.A., Brennan R.G. Structural mechanisms of QacR induction and multidrug recognition. Science. 294:2001;2158-2163.
46. Zheleznova E.E., Markham P.N., Neyfakh A.A., Brennan R.G. Structural basis of multidrug recognition by BmrR, a transcription activator of a multidrug transporter. Cell. 96:1999;353-362.
47. Neyfakh A.A. Mystery of multidrug transporters: the answer can be simple. Mol Microbiol. 44:2002;1123-1130 The author proposes his theory that multidrug recognition is due to the large hydrophobic substrate-binding site, which allows multiple binding. Substrates bind through a combination of hydrophobic effects and electrostatic attraction without hydrogen bonding.
48. Fujihira E., Tamura N., Yamaguchi A. Membrane topology of a multidrug efflux transporter AcrB in Escherichia coli. J Biochem. 131:2002;145-151 An experimental determination of the AcrB topology. This was the most significant step towards determining the structure of a multidrug exporter before the X-ray crystal structure determination.
49. Anderson C., Hughes C., Koronakis V. Protein export and drug efflux through bacterial channel-tunnels. Curr Opin Cell Biol. 13:2001;412-416.
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