Metal Export by CusCFBA, the Periplasmic Cu(I)/Ag(I) Transport System of Escherichia coli

Current Topics in Membranes

Volumn 69, Issue , 2012, Pages 163-196

  Mealman, Tiffany D ^a   Blackburn, Ninian J ^b   McEvoy, Megan M ^a  

^a University of Arizona   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Bacterial transporters; Copper resistance; Cus; Metal transfer; Periplasm

Indexed keywords

EID: 84867158886     PISSN: 10635823     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-394390-3.00007-0     Document Type: Chapter

References (100)

1. Abajian C., Yatsunyk L.A., Ramirez B.E., Rosenzweig A.C. Yeast cox17 solution structure and Copper(I) binding. The Journal of Biological Chemistry 2004, 279(51):53584-53592.
2. Achila D., Banci L., Bertini I., Bunce J., Ciofi-Baffoni S., Huffman D.L. Structure of human Wilson protein domains 5 and 6 and their interplay with domain 4 and the copper chaperone HAM in copper uptake. Proceedings of the National Academy of Sciences of the United States of America 2006, 103(15):5729-5734.
3. Akama H., Kanemaki M., Yoshimura M., Tsukihara T., Kashiwagi T., Yoneyama H., et al. Crystal structure of the drug discharge outer membrane protein, OprM, of Pseudomonas aeruginosa: dual modes of membrane anchoring and occluded cavity end. The Journal of Biological Chemistry 2004, 279(51):52816-52819.
4. Akama H., Matsuura T., Kashiwagi S., Yoneyama H., Narita S., Tsukihara T., et al. Crystal structure of the membrane fusion protein, MexA, of the multidrug transporter in Pseudomonas aeruginosa. The Journal of Biological Chemistry 2004, 279(25):25939-25942.
5. Arnesano F., Banci L., Bertini I., Huffman D.L., O'Halloran T.V. Solution structure of the Cu(I) and Apo forms of the yeast metallochaperone, Atx1. Biochemistry 2001, 40(6):1528-1539.
6. Arnesano F., Banci L., Bertini I., Thompsett A.R. Solution structure of CopC: a cupredoxin-like protein involved in copper homeostasis. Structure 2002, 10(10):1337-1347.
7. Bagai I., Liu W., Rensing C., Blackburn N.J., McEvoy M.M. Substrate-linked conformational change in the periplasmic component of a Cu(I)/Ag(I) efflux system. The Journal of Biological Chemistry 2007, 282(49):35695-35702.
8. Bagai I., Rensing C., Blackburn N.J., McEvoy M.M. Direct metal transfer between periplasmic proteins identifies a bacterial copper chaperone. Biochemistry 2008, 47(44):11408-11414.
9. Banci L., Bertini I., Cantini F., Felli I.C., Gonnelli L., Hadjiliadis N., et al. The Atx1-Ccc2 complex is a metal-mediated protein-protein interaction. Nature Chemical Biology 2006, 2(7):367-368.
10. Banci L., Bertini I., Ciofi-Baffoni S., Del Conte R., Gonnelli L. Understanding copper trafficking in bacteria: interaction between the copper transport protein CopZ and the N-terminal domain of the copper ATPase CopA from Bacillus subtilis. Biochemistry 2003, 42(7):1939-1949.
11. Banci L., Bertini I., Ciofi-Baffoni S., Huffman D.L., O'Halloran T.V. Solution structure of the yeast copper transporter domain Ccc2a in the apo and Cu(I)-loaded states. The Journal of Biological Chemistry 2001, 276(11):8415-8426.
12. Banci L., Bertini I., Ciofi-Baffoni S., Katsari E., Katsaros N., Kubicek K., et al. A copper(I) protein possibly involved in the assembly of CuA center of bacterial cytochrome c oxidase. Proceedings of the National Academy of Sciences of the United States of America 2005, 102(11):3994-3999.
13. Bavro V.N., Pietras Z., Furnham N., Perez-Cano L., Fernandez-Recio J., Pei X.Y., et al. Assembly and channel opening in a bacterial drug efflux machine. Molecular Cell 2008, 30(1):114-121.
14. Chakravorty D.K., Wang B., Ucisik M.N., Merz K.M. Insight into the cation-pi interaction at the metal binding site of the copper metallochaperone CusF. Journal of the American Chemical Society 2011, 133(48):19330-19333.
15. Chen K., Yuldasheva S., Penner-Hahn J.E., O'Halloran T.V. An atypical linear Cu(I)-S2 center constitutes the high-affinity metal-sensing site in the CueR metalloregulatory protein. Journal of the American Chemical Society 2003, 125(40):12088-12089.
16. Conroy O., Kim E.H., McEvoy M.M., Rensing C. Differing ability to transport nonmetal substrates by two RND-type metal exporters. FEMS Microbiology Letters 2010, 308(2):115-122.
17. Davis A.V., O'Halloran T.V. A place for thioether chemistry in cellular copper ion recognition and trafficking. Nature Chemical Biology 2008, 4(3):148-151.
18. De Angelis F., Lee J.K., O'Connell J.D., Miercke L.J., Verschueren K.H., Srinivasan V., et al. Metal-induced conformational changes in ZneB suggest an active role of membrane fusion proteins in efflux resistance systems. Proceedings of the National Academy of Sciences of the United States of America 2010, 107(24):11038-11043.
19. Deniaud A., Goulielmakis A., Coves J., Pebay-Peyroula E. Differences between CusA and AcrB crystallisation highlighted by protein flexibility. PLoS One 2009, 4(7):e6214.
20. Dibrov P., Dzioba J., Gosink K.K., Hase C.C. Chemiosmotic mechanism of antimicrobial activity of Ag(+) in Vibrio cholerae. Antimicrobial Agents Chemotherapy 2002, 46(8):2668-2670.
21. Dinh T., Paulsen I.T., Saier M.H. A family of extracytoplasmic proteins that allow transport of large molecules across the outer membranes of gram-negative bacteria. Journal of Bacteriology 1994, 176(13):3825-3831.
22. Egler M., Grosse C., Grass G., Nies D.H. Role of the extracytoplasmic function protein family sigma factor RpoE in metal resistance of Escherichia coli. Journal of Bacteriology 2005, 187(7):2297-2307.
23. Espirito Santo C., Lam E.W., Elowsky C.G., Quaranta D., Domaille D.W., Chang C.J., et al. Bacterial killing by dry metallic copper surfaces. Applied Environmental Microbiology 2011, 77(3):794-802.
24. Franke S., Grass G., Nies D.H. The product of the ybdE gene of the Escherichia coli chromosome is involved in detoxification of silver ions. Microbiology 2001, 147(Pt 4):965-972.
25. Franke S., Grass G., Rensing C., Nies D.H. Molecular analysis of the copper-transporting efflux system CusCFBA of Escherichia coli. Journal of Bacteriology 2003, 185(13):3804-3812.
26. Goldberg M., Pribyl T., Juhnke S., Nies D.H. Energetics and topology of CzcA, a cation/proton antiporter of the resistance-nodulation-cell division protein family. The Journal of Biological Chemistry 1999, 274(37):26065-26070.
27. Grass G., Rensing C. CueO is a multi-copper oxidase that confers copper tolerance in Escherichia coli. Biochemistry and Biophysics Research Communications 2001, 286(5):902-908.
28. Grass G., Rensing C. Genes involved in copper homeostasis in Escherichia coli. Journal of Bacteriology 2001, 183(6):2145-2147.
29. Gudipaty S.A., Larsen A.S., Rensing C., McEvoy M.M. Regulation of Cu(I)/Ag(I) efflux genes in Escherichia coli by the sensor kinase CusS. FEMS Microbiology Letters 2012.
30. Gupta A., Matsui K., Lo J.F., Silver S. Molecular basis for resistance to silver cations in Salmonella. Nature Medicine 1999, 5(2):183-188.
31. Halliwell B., Gutteridge J.M.C. Oxygen-toxicity, oxygen radicals, transition-metals and disease. Biochemical Journal 1984, 219(1):1-14.
32. Halliwell B., Gutteridge J.M.C. Role of free-radicals and catalytic metal-ions in human-disease-an overview. Methods in Enzymology 1990, 186:1-85.
33. Higgins M.K., Bokma E., Koronakis E., Hughes C., Koronakis V. Structure of the periplasmic component of a bacterial drug efflux pump. Proceedings of the National Academy of Sciences of the United States of America 2004, 101(27):9994-9999.
34. Janganan T.K., Zhang L., Bavro V.N., Matak-Vinkovic D., Barrera N.P., Burton M.F., et al. Opening of the outer membrane protein channel in tripartite efflux pumps is induced by interaction with the membrane fusion partner. The Journal of Biological Chemistry 2011, 286(7):5484-5493.
35. Jiang J., Nadas I.A., Kim M.A., Franz K.J. A Mets motif peptide found in copper transport proteins selectively binds Cu(I) with methionine-only coordination. Inorganic Chemistry 2005, 44(26):9787-9794.
36. Kim H.M., Xu Y., Lee M., Piao S., Sim S.H., Ha N.C., et al. Functional relationships between the AcrA hairpin tip region and the TolC aperture tip region for the formation of the bacterial tripartite efflux pump AcrAB-TolC. Journal of Bacteriology 2010, 192(17):4498-4503.
37. Kittleson J.T., Loftin I.R., Hausrath A.C., Engelhardt K.P., Rensing C., McEvoy M.M. Periplasmic metal-resistance protein CusF exhibits high affinity and specificity for both CuI and AgI. Biochemistry 2006, 45(37):11096-11102.
38. Koronakis V., Sharff A., Koronakis E., Luisi B., Hughes C. Crystal structure of the bacterial membrane protein TolC central to multidrug efflux and protein export. Nature 2000, 405(6789):914-919.
39. Kulathila R., Indic M., van den Berg B. Crystal structure of Escherichia coli CusC, the outer membrane component of a heavy metal efflux pump. PLoS One 2011, 6(1):e15610.
40. Lamb A.L., Wernimont A.K., Pufahl R.A., Culotta V.C., O'Halloran T.V., Rosenzweig A.C. Crystal structure of the copper chaperone for superoxide dismutase. Nature Structural Biology 1999, 6(8):724-729.
41. Lim S.P., Nikaido H. Kinetic parameters of efflux of penicillins by the multidrug efflux transporter AcrAB-TolC of Escherichia coli. Antimicrobial Agents and Chemotherapy 2010, 54(5):1800-1806.
42. Lobedanz S., Bokma E., Symmons M.F., Koronakis E., Hughes C., Koronakis V. A periplasmic coiled-coil interface underlying TolC recruitment and the assembly of bacterial drug efflux pumps. Proceedings of the National Academy of Sciences of the United States of America 2007, 104(11):4612-4617.
43. Loftin I.R., Blackburn N.J., McEvoy M.M. Tryptophan Cu(I)-pi interaction fine-tunes the metal binding properties of the bacterial metallochaperone CusF. Journal of Biological Inorganic Chemistry 2009, 14(6):905-912.
44. Loftin I.R., Franke S., Blackburn N.J., McEvoy M.M. Unusual Cu(I)/Ag(I) coordination of Escherichia coli CusF as revealed by atomic resolution crystallography and X-ray absorption spectroscopy. Protein Science 2007, 16(10):2287-2293.
45. Loftin I.R., Franke S., Roberts S.A., Weichsel A., Heroux A., Montfort W.R., et al. A novel copper-binding fold for the periplasmic copper resistance protein CusF. Biochemistry 2005, 44(31):10533-10540.
46. Lomovskaya O., Zgurskaya H.I., Totrov M., Watkins W.J. Waltzing transporters and 'the dance macabre' between humans and bacteria. Nature Reviews Drug Discovery 2007, 6(1):56-65.
47. Long F., Su C.C., Zimmermann M.T., Boyken S.E., Rajashankar K.R., Jernigan R.L., et al. Crystal structures of the CusA efflux pump suggest methionine-mediated metal transport. Nature 2010, 467(7314):484-488.
48. McHugh G.L., Moellering R.C., Hopkins C.C., Swartz M.N. Salmonella typhimurium resistant to silver nitrate, chloramphenicol, and ampicillin. Lancet 1975, 1(7901):235-240.
49. Mealman T.D., Bagai I., Singh P., Goodlett D.R., Rensing C., Zhou H., et al. Interactions between CusF and CusB identified by NMR spectroscopy and chemical cross-linking coupled to mass spectrometry. Biochemistry 2011, 50(13):2559-2566.
50. Mikolosko J., Bobyk K., Zgurskaya H.I., Ghosh P. Conformational flexibility in the multidrug efflux system protein AcrA. Structure 2006, 14(3):577-587.
51. Misra R., Bavro V.N. Assembly and transport mechanism of tripartite drug efflux systems. Biochimica et Biophysica Acta 2009, 1794(5):817-825.
52. Modali S.D., Zgurskaya H.I. The periplasmic membrane proximal domain of MacA acts as a switch in stimulation of ATP hydrolysis by MacB transporter. Molecular Microbiology 2011, 81(4):937-951.
53. Molteni C., Abicht H.K., Solioz M. Killing of bacteria by copper surfaces involves dissolved copper. Applied Environmental Microbiology 2010, 76(12):4099-4101.
54. Munson G.P., Lam D.L., Outten F.W., O'Halloran T.V. Identification of a copper-responsive two-component system on the chromosome of Escherichia coli K-12. Journal of Bacteriology 2000, 182(20):5864-5871.
55. Murakami S., Nakashima R., Yamashita E., Matsumoto T., Yamaguchi A. Crystal structures of a multidrug transporter reveal a functionally rotating mechanism. Nature 2006, 443(7108):173-179.
56. Murakami S., Nakashima R., Yamashita E., Yamaguchi A. Crystal structure of bacterial multidrug efflux transporter AcrB. Nature 2002, 419(6907):587-593.
57. Murzin A.G. OB (oligonucleotide/oligosaccharide binding)-fold: common structural and functional solution for non-homologous sequences. EMBO Journal 1993, 12(3):861-867.
58. Neilsen P.O., Zimmerman G.A., McIntyre T.M. Escherichia coli Braun lipoprotein induces a lipopolysaccharide-like endotoxic response from primary human endothelial cells. Journal of Immunology 2001, 167(9):5231-5239.
59. Nies D.H. The cobalt, zinc, and cadmium efflux system CzcABC from Alcaligenes eutrophus functions as a cation-proton antiporter in Escherichia coli. Journal of Bacteriology 1995, 177(10):2707-2712.
60. Nies D.H. Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiology Reviews 2003, 27(2-3):313-339.
61. Nies D.H., Nies A., Chu L., Silver S. Expression and nucleotide sequence of a plasmid-determined divalent cation efflux system from Alcaligenes eutrophus. Proceedings of the National Academy of Sciences of the United States of America 1989, 86(19):7351-7355.
62. Nikaido H. Structure and mechanism of RND-type multidrug efflux pumps. Advances in Enzymology and Related Areas of Molecular Biology 2011, 77:1-60.
63. Outten F.W., Huffman D.L., Hale J.A., O'Halloran T.V. The independent cue and cus systems confer copper tolerance during aerobic and anaerobic growth in Escherichia coli. The Journal of Biological Chemistry 2001, 276(33):30670-30677.
64. Piddock L.J. Multidrug-resistance efflux pumps-not just for resistance. Nature Reviews Microbiology 2006, 4(8):629-636.
65. Ralle M., Cooper M.J., Lutsenko S., Blackburn N.J. The Menkes disease protein binds copper via novel 2-coordinate Cu(I)-cysteinates in the N-terminal domain. Journal of the American Chemical Society 1998, 120(51):13525-13526.
66. Ralle M., Lutsenko S., Blackburn N.J. X-ray absorption spectroscopy of the copper chaperone HAH1 reveals a linear two-coordinate Cu(I) center capable of adduct formation with exogenous thiols and phosphines. The Journal of Biological Chemistry 2003, 278(25):23163-23170.
67. Reffay M., Gambin Y., Benabdelhak H., Phan G., Taulier N., Ducruix A., et al. Tracking membrane protein association in model membranes. PLoS One 2009, 4(4):e5035.
68. Rensing C., Fan B., Sharma R., Mitra B., Rosen B.P. CopA: an Escherichia coli Cu(I)-translocating P-type ATPase. Proceedings of the National Academy of Sciences of the United States of America 2000, 97(2):652-656.
69. Rensing C., Grass G. Escherichia coli mechanisms of copper homeostasis in a changing environment. FEMS Microbiology Reviews 2003, 27(2-3):197-213.
70. Rensing C., Pribyl T., Nies D.H. New functions for the three subunits of the CzcCBA cation-proton antiporter. Journal of Bacteriology 1997, 179(22):6871-6879.
71. Roberts S.A., Weichsel A., Grass G., Thakali K., Hazzard J.T., Tollin G., et al. Crystal structure and electron transfer kinetics of CueO, a multicopper oxidase required for copper homeostasis in Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 2002, 99(5):2766-2771.
72. Robinson N.J., Winge D.R. Copper metallochaperones. Annual Reviews of Biochemistry 2010, 79:537-562.
73. Saier M.H. A functional-phylogenetic classification system for transmembrane solute transporters. Microbiology and Molecular Biology Reviews 2000, 64(2):354-411.
74. Saier M.H., Tam R., Reizer A., Reizer J. Two novel families of bacterial membrane proteins concerned with nodulation, cell division and transport. Molecular Microbiology 1994, 11(5):841-847.
75. Sarret G., Favier A., Coves J., Hazemann J.L., Mergeay M., Bersch B. CopK from Cupriavidus metallidurans CH34 binds Cu(I) in a tetrathioether site: characterization by X-ray absorption and NMR spectroscopy. Journal of the American Chemical Society 2010, 132(11):3770-3777.
76. Seeger M.A., Schiefner A., Eicher T., Verrey F., Diederichs K., Pos K.M. Structural asymmetry of AcrB trimer suggests a peristaltic pump mechanism. Science 2006, 313(5791):1295-1298.
77. Sennhauser G., Bukowska M.A., Briand C., Grutter M.G. Crystal structure of the multidrug exporter MexB from Pseudomonas aeruginosa. Journal of Molecular Biology 2009, 389(1):134-145.
78. Silver S. Bacterial silver resistance: molecular biology and uses and misuses of silver compounds. FEMS Microbiology Reviews 2003, 27(2-3):341-353.
79. Silver S., Phung L.T., Silver G. Silver as biocides in burn and wound dressings and bacterial resistance to silver compounds. Journal of Industrial Microbiology and Biotechnology 2006, 33(7):627-634.
80. Singh S.K., Grass G., Rensing C., Montfort W.R. Cuprous oxidase activity of CueO from Escherichia coli. Journal of Bacteriology 2004, 186(22):7815-7817.
81. Stasser J.P., Siluvai G.S., Barry A.N., Blackburn N.J. A multinuclear copper(I) cluster forms the dimerization interface in copper-loaded human copper chaperone for superoxide dismutase. Biochemistry 2007, 46(42):11845-11856.
82. Stroebel D., Sendra V., Cannella D., Helbig K., Nies D.H., Coves J. Oligomeric behavior of the RND transporters CusA and AcrB in micellar solution of detergent. Biochimica et Biophysica Acta 2007, 1768(6):1567-1573.
83. Su C.C., Long F., Zimmermann M.T., Rajashankar K.R., Jernigan R.L., Yu E.W. Crystal structure of the CusBA heavy-metal efflux complex of Escherichia coli. Nature 2011, 470(7335):558-562.
84. Su C.C., Yang F., Long F., Reyon D., Routh M.D., Kuo D.W., et al. Crystal structure of the membrane fusion protein CusB from Escherichia coli. Journal of Molecular Biology 2009, 393(2):342-355.
85. Symmons M.F., Bokma E., Koronakis E., Hughes C., Koronakis V. The assembled structure of a complete tripartite bacterial multidrug efflux pump. Proceedings of the National Academy of Sciences of the United States of America 2009, 106(17):7173-7178.
86. Tikhonova E.B., Zgurskaya H.I. AcrA, AcrB, and TolC of Escherichia coli form a stable intermembrane multidrug efflux complex. The Journal of Biological Chemistry 2004, 279(31):32116-32124.
87. Touze T., Eswaran J., Bokma E., Koronakis E., Hughes C., Koronakis V. Interactions underlying assembly of the Escherichia coli AcrAB-TolC multidrug efflux system. Molecular Microbiology 2004, 53(2):697-706.
88. Tseng T.T., Gratwick K.S., Kollman J., Park D., Nies D.H., Goffeau A., et al. The RND permease superfamily: an ancient, ubiquitous and diverse family that includes human disease and development proteins. Journal of Molecular Microbiology and Biotechnology 1999, 1(1):107-125.
89. Vaccaro L., Koronakis V., Sansom M.S. Flexibility in a drug transport accessory protein: molecular dynamics simulations of MexA. Biophysical Journal 2006, 91(2):558-564.
90. von Rozycki T., Nies D.H. Cupriavidus metallidurans: evolution of a metal-resistant bacterium. Antonie Van Leeuwenhoek 2009, 96(2):115-139.
91. Wang B., Weng J., Fan K., Wang W. Interdomain flexibility and pH-induced conformational changes of AcrA revealed by molecular dynamics simulations. Journal of Physical Chemistry B 2012.
92. Wernimont A.K., Huffman D.L., Finney L.A., Demeler B., O'Halloran T.V., Rosenzweig A.C. Crystal structure and dimerization equilibria of PcoC, a methionine-rich copper resistance protein from Escherichia coli. Journal of Biological Inorganic Chemistry 2003, 8(1-2):185-194.
93. Williams J.R., Morgan A.G., Rouch D.A., Brown N.L., Lee B.T. Copper-resistant enteric bacteria from United Kingdom and Australian piggeries. Applied Environmental Microbiology 1993, 59(8):2531-2537.
94. Xu Y., Lee M., Moeller A., Song S., Yoon B.Y., Kim H.M., et al. Funnel-like hexameric assembly of the periplasmic adapter protein in the tripartite multidrug efflux pump in Gram-negative bacteria. The Journal of Biological Chemistry 2011, 286(20):17910-17920.
95. Xue Y., Davis A.V., Balakrishnan G., Stasser J.P., Staehlin B.M., Focia P., et al. Cu(I) recognition via cation-pi and methionine interactions in CusF. Nature Chemical Biology 2008, 4(2):107-109.
96. Yum S., Xu Y., Piao S., Sim S.H., Kim H.M., Jo W.S., et al. Crystal structure of the periplasmic component of a tripartite macrolide-specific efflux pump. Journal of Molecular Biology 2009, 387(5):1286-1297.
97. Zgurskaya H.I., Nikaido H. Bypassing the periplasm: reconstitution of the AcrAB multidrug efflux pump of Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 1999, 96(13):7190-7195.
98. Zgurskaya H.I., Nikaido H. Multidrug resistance mechanisms: drug efflux across two membranes. Molecular Microbiology 2000, 37(2):219-225.
99. Zgurskaya H.I., Yamada Y., Tikhonova E.B., Ge Q., Krishnamoorthy G. Structural and functional diversity of bacterial membrane fusion proteins. Biochimica et Biophysica Acta 2009, 1794(5):794-807.
100. Zhou H., Thiele D.J. Identification of a novel high affinity copper transport complex in the fission yeast Schizosaccharomyces pombe. The Journal of Biological Chemistry 2001, 276(23):20529-20535.