The cus efflux system removes toxic ions via a methionine shuttle

Protein Science

Volumn 20, Issue 1, 2011, Pages 6-18

  Su, Chih Chia ^a   Long, Feng ^a   Yu, Edward W ^a  

^a IOWA STATE UNIVERSITY   (United States)

Author keywords

CusCBA efflux complex; Heavy metal efflux; Membrane fusion protein; Multidrug resistance; Outer membrane channel; Resistance nodulation cell division

Indexed keywords

ACRIFLAVINE; BENZALKONIUM; CARRIER PROTEIN; CHLORAMPHENICOL; COPPER; CRYSTAL VIOLET; DEOXYCHOLIC ACID; DODECYL SULFATE SODIUM; DOXORUBICIN; ENOXACIN; ERYTHROMYCIN; ETHIDIUM BROMIDE; MEMBRANE FUSION PROTEIN; METAL ION; METHIONINE; MINOCYCLINE; NALIDIXIC ACID; NORFLOXACIN; NOVOBIOCIN; OUTER MEMBRANE ANCHORED CHANNEL; PROTEIN CUSA; PROTEIN CUSB; RHODAMINE 6G; RIFAMPICIN; SILVER; SUBSTRATE BINDING INNER MEMBRANE TRANSPORTER; TAUROCHOLIC ACID; TETRACYCLINE; TETRAPHENYLPHOSPHONIUM; TRIMETHOPRIM; UNCLASSIFIED DRUG;

BINDING SITE; CRYSTAL STRUCTURE; ESCHERICHIA COLI; GENE STRUCTURE; GENETIC ANALYSIS; IN VITRO STUDY; IN VIVO STUDY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW;

COPPER; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; ION PUMPS; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; METALS, HEAVY; METHIONINE; PROTEIN BINDING; PROTEIN CONFORMATION; SILVER;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA;

EID: 78650791250     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.532     Document Type: Review

References (47)

1. Silver S (2003) Bacterial silver resistance: molecular biology and uses and misuses of silver compounds. FEMS Microbiol Rev 27:341-353.
2. Percival SL, Bowler PG, Russell D (2005) Bacterial resistance to silver in wound care. J Hosp Infect 60: 1-7.
3. Ercal N, Gurer-Orhan H, Aykin-Burns N (2001) Toxic metals and oxidative stress part I: mechanisms involved in metal induced oxidative damage. Curr. Topics Med Chem 1:529-539.
4. Tseng TT, Gratwick KS, Kollman J, Park D, Nies DH, Goffeau A, Saier MH, Jr (1999) The RND permease superfamily: an ancient, ubiquitous and diverse family that includes human disease and development protein. J Mol Microbiol Biotechnol 1:107-125.
5. Nies DH (2003) Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev 27:313-339.
6. Zgurskaya H, Nikaido H (1999) Bypassing the periplasm: reconstitution of the AcrAB multidrug efflux pump of Escherichia coli. Proc Natl Acad Sci USA 96: 7190-7195.
7. Nishino K, Yamaguchi A (2001) Analysis of a complete library of putative drug transporter genes in Escherichia coli. J Bacteriol 183:5803-5812.
8. Murakami S, Nakashima R, Yamashita E, Yamaguchi, A (2002) Crystal structure of bacterial multidrug efflux transporter AcrB. Nature 419:587-593.
9. Yu EW, McDermott G, Zgruskaya HI, Nikaido H, Koshland DE, Jr (2003) Structural basis of multiple drug binding capacity of the AcrB multidrug efflux pump. Science 300:976-980.
10. Yu EW, Aires JR, McDermott G, Nikaido H (2005) A periplasmic drug-binding site of the AcrB multidrug efflux pump: a crystallographic and site-directed mutagenesis study. J Bacteriol 187:6804-6815.
11. Murakami S, Nakashima R, Yamashita E, Matsumoto T, Yamaguchi A (2006) Crystal structures of a multidrug transporter reveal a functionally rotating mechanism. Nature 443:173-179.
12. Seeger MA, Schiefner A, Eicher T, Verrey F, Dietrichs K, Pos KM (2006) Structural asymmetry of AcrB trimer suggests a peristaltic pump mechanism. Science 313: 1295-1298.
13. Sennhauser G, Amstutz P, Briand C, Storchengegger O, Grütter MG (2007) Drug export pathway of multidrug exporter AcrB revealed by DARPin inhibitors. PLoS Biol 5:e7.
14. Das D, Xu QS, Lee JY, Ankoudinova I, Huang C, Lou Y, Degiovanni A, Kim R, Kim SH (2007) Crystal structure of the multidrug efflux transporter AcrB at 3.1 Å resolution reveals the N-terminal region with conserved amino acids. J Struct Biol 158:494-502.
15. Su C-C, Li M, Gu R, Takatsuka Y, McDermott G, Nikaido H, Yu EW (2006) Conformation of the AcrB multidrug efflux pump in mutants of the putative proton relay pathway. J Bacteriol 188:7290-7296.
16. Törnroth-Horsefield S, Gourdon P, Horsefield R, Brive L, Yamamoto N, Mori H, Snijder A, Neutze R (2007) Crystal structure of AcrB in complex with a single transmembrane subunit reveals another twist. Structure 15:1663-1673.
17. Rosenberg EY, Ma D, Nikaido H (2000) AcrD of Escherichia coli is an aminoglycoside efflux pump. J Bacteriol 182:1754-1756.
18. Aires JR, Nikaido H (2005) Aminoglycosides are captured from both periplasm and cytoplasm by the AcrD multidrug efflux transporter of Escherichia coli. J Bacteriol 187:1923-1929.
19. Ma D, Cook DN, Alberti M, Pon NG, Nikaido H, Hearst E (1993) Molecular cloning of acrA and acrE genes of Escherichia coli. J Bacteriol 175:6299-6313.
20. Lau SY, Zgurskaya HI (2005) Cell division defects in Escherichia coli deficient in the multidrug efflux transporter AcrEF-TolC. J Bacteriol 187:7815-7825.
21. Baranova N, Nikaido H (2002) The BaeSR two-component regulatory system activates transcription of yegMNOB (mdtABCD) transporter gene cluster in Escherichia coli and increases its resistance to novobiocin and deoxycholate. J Bacteriol 184:4168-4176.
22. Nagakubo S, Nishino K, Hirata T, Yamaguchi A (2002) The putative response regulator BaeR stimulates multidrug resistance of Escherichia coli via a novel multidrug exporter system, MdtABC. J Bacteriol 184:4161-4167.
23. Bohnert JA, Schuster S, Fähnrich E, Trittler R., Kern WV (2007) Altered spectrum of multidrug resistance associated with a single point mutation in the Escherichia coli RND-type MDR efflux pump YhiV (MdtF). J Antimicrob Chemother 6:1216-1222.
24. Kobayashi A, Hirakawa H, Hirata T, Nishino K, Yamaguchi A (2001) Growth phase-dependent expression of drug exporters in Escherichia coli and its contribution to drug tolerance. J Bacteriol 16:5693-5703.
25. Franke S, Grass G, Nies DH (2001) The product of the ybdE gene of the Escherichia coli chromosome is involved in detoxification of silver ions. Microbiol 147: 965-972. (Pubitemid 32401336)
26. Franke S, Grass G, Rensing C, Nies DH (2003) Molecular analysis of the copper-transporting efflux system CusCFBA of Escherichia coli. J Bacteriol 185: 3804-3812.
27. Xue Y, Davis AV, Balakrishnan G, Stasser JP, Staehlin BM, Focia P, Spiro TG, Penner-Hahn JE, O'Halloran TV (2008) Cu(I) recognition via cation-p and methionine interactions in CusF. Nature Chem Biol 4: 107-109.
28. Loftin IR, Franke S, Blackburn NJ, McEvoy MM (2007) Unusual Cu(I)/Ag(I) coordination of Escherichia coli CusF as revealed by atomic resolution crystallography and x-ray absorption spectroscopy. Protein Sci 16: 2287-2293.
29. Sennhauser G, Bukowska MA, Briand C, Grütter M G (2009) Crystal structure of the multidrug exporter MexB from Pseudomonas aeruginosa. J Mol Biol 389: 134-145.
30. Koronakis V, Sharff A, Koronakis E, Luisi B, Hughes C (2000) Crystal structure of the bacterial membrane protein TolC central to multidrug efflux and protein export. Nature 405:914-919.
31. Akama H, Kanemaki M, Yoshimura M, Tsukihara T, Kashiwag T, Yoneyama H, Narita S, Nakagawa A, Nakae T (2004) Crystal structure of the drug discharge outer membrane protein, OprM, of Pseudomonas aeruginosa. J Biol Chem 279:52816-52819.
32. Mikolosko J, Bobyk K, Zgurskaya HI, Ghosh P (2006) Conformational flexibility in the multidrug efflux system protein AcrA. Structure 14:577-587.
33. Higgins MK, Bokma E, Koronakis E, Hughes C, Koronakis V (2004) Structure of the periplasmic component of a bacterial drug efflux pump. Proc Natl Acad Sci USA 101:9994-9999.
34. Akama H, Matsuura T, Kashiwag S, Yoneyama H, Narita S, Tsukihara T, Nakagawa A, Nakae T (2004) Crystal structure of the membrane fusion protein, MexA, of the multidrug transporter in Pseudomonas aeruginosa. J Biol Chem 279:25939-25942 (2004).
35. Symmons M, Bokma E, Koronakis E, Hughes C, Koronakis V (2009) The assembled structure of a complete tripartite bacterial multidrug efflux pump. Proc Natl Acad Sci USA 106:7173-7178.
36. Su C-C, Yang F, Long F, Reyon D, Routh MD, Kuo DW, Mokhtari AK, Van Ornam JD, Rabe KL, Hoy JA, Lee YJ, Rajashankar KR, Yu EW (2009) Crystal structure of the membrane fusion protein CusB from Escherichia coli. J Mol Biol 393:342-355.
37. Long F, Su C-C, Zimmermann MT, Boyken SE, Rajashankar KR, Jernigan RL, Yu EW (2010) Crystal structures of the CusA efflux pump suggest methioninemediated metal transport. Nature 467:484-488.
38. Yum S, Xu Y, Piao S, Sim S-H, Kim H-M, Jo W-S, Kim K-J, Kweon H-S, Jeong M-H, Lee K, Ha N-C (2009) Crystal structure of the periplasmic component of a tripartite macrolide-specific efflux pump. J Mol Biol 387: 1286-1297.
39. De Angelis F, Lee JK, O'Connell III JD, Miercke LJW, Verschueren KH, Srinivasan V, Bauvois C, Govaerts C, Robbins RA, Ruysschaert J-M, Stroud RM, Vandenbussche G (2010) Metal-induced conformational changes in ZneB suggest an active role of membrane fusion proteins in efflux resistance systems. Proc Natl Acad Sci USA 107:11038-11043.
40. Borges-Walmsley MI, Beauchamp J, Kelly SM, Jumel K, Candlish D, Harding SE, Price NC, Walmsley AR (2003) Identification of oligomerization and drug-binding domains of the membrane fusion protein EmrA. J Biol Chem 278:12903-12912.
41. Bagai I, Liu W, Rensing C, Blackburn NJ, McEvoy MM (2007) Substrate-linked conformational change in the periplasmic component of a Cu(I)/Ag(I) efflux system. J Biol Chem 282:35695-35702.
42. Zhou H, Thiele DJ (2001) Identification of a novel high affinity copper transport complex in the fission yeast Schizosaccharomyces pombe. J Biol Chem 276:20529-20535.
43. Jiang J, Nadas IA, Kim MA, Franz KJ (2005) A Mets motif peptide found in copper transport proteins selectively binds Cu(I) with methionine-only coordination. Inorg Chem 44:9787-9794.
44. Changela A, Chen K, Xue Y, Holschen J, Outten CE, O'Halloran TV, Mondragón A (2003) Molecular basis of metal-ion selectivity and zeptomolar sensitivity by CueR. Science 301:1383-1387.
45. Arnesano F, Banci L, Bertini I, Huffman DL, O'Halloran TV (2001) Solution structure of the Cu(I) and apo-forms of the yeast metallochaperone, Atx1. Biochemistry 40:1528-1539.
46. Goldberg M, Pribyl T, Juhuke S, Nies DH (1999) Energetics and topology of CzcA, a cation/proton antiporter of the resistance-nodulation-cell division protein family. J Biol Chem 274:26065-26070.
47. Piddock, LJV (2006) Clinically relevant chromosomally encoded multidrug resistance efflux pumps in bacteria. Clin Microbiol Rev 19:382-402.