Mechanism of ATPase-mediated Cu+ export and delivery to periplasmic chaperones: The interaction of Escherichia coli CopA and CusF

Journal of Biological Chemistry

Volumn 289, Issue 30, 2014, Pages 20492-20501

  Padilla Benavides, Teresita ^a   Thompson, Alayna M George ^b   McEvoy, Megan M ^b   Argüello, José M ^a  

^a United States   (United States)

^b The University of Arizona   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOPHYSICS; COPPER; ENZYMES; HYDROLYSIS;

COPPER HOMEOSTASIS; EXTRACELLULAR LOOPS; METAL TRANSFERS; PERIPLASMIC CHAPERONE; SPECIFIC INTERACTION; STRUCTURAL PLATFORM; TRANSFER EFFICIENCY; TRANSMEMBRANE TRANSPORT;

ESCHERICHIA COLI;

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; CATION TRANSPORT PROTEIN; CHAPERONE; COPPER; COPPER-TRANSPORTING ATPASES; CUSC PROTEIN, E COLI; CUSF PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN; MEMBRANE PROTEIN; PERIPLASMIC PROTEIN;

ESCHERICHIA COLI; GENETICS; ION TRANSPORT; METABOLISM; MUTATION; PHYSIOLOGY; PROTEIN SECONDARY STRUCTURE;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; CATION TRANSPORT PROTEINS; COPPER; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; ION TRANSPORT; MEMBRANE PROTEINS; MOLECULAR CHAPERONES; MUTATION; PERIPLASMIC PROTEINS; PROTEIN STRUCTURE, SECONDARY;

EID: 84905402461     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.577668     Document Type: Article

References (47)

1. Argüello, J. M., Raimunda, D., and Padilla-Benavides, T. (2013) Mechanisms of copper homeostasis in bacteria. Front. Cell Infect. Microbiol. 3, 73
2. Fraústo da Silva, J. J. R., and Williams, R. J. P. (2001) The Biological Chemistry of the Elements: The Inorganic Chemistry of Life, 2nd Ed., Oxford University Press, Oxford
3. Rensing, C., and McDevitt, S. F. (2013) The copper metallome in prokaryotic cells. Met. Ions Life Sci. 12, 417-450
4. Macomber, L., and Imlay, J. A. (2009) The iron-sulfur clusters of dehydratases are primary intracellular targets of copper toxicity. Proc. Natl. Acad. Sci. U. S. A. 106, 8344-8349
5. Valko, M., Morris, H., and Cronin, M. T. (2005) Metals, toxicity and oxidative stress. Curr. Med. Chem. 12, 1161-1208
6. O'Halloran, T. V., and Culotta, V. C. (2000) Metallochaperones, an intracellular shuttle service for metal ions. J. Biol. Chem. 275, 25057-25060
7. Osman, D., and Cavet, J. S. (2008) Copper homeostasis in bacteria. Adv. Appl. Microbiol. 65, 217-247
8. Kim, E. H., Rensing, C., and McEvoy, M. M. (2010) Chaperone-mediated copper handling in the periplasm. Nat. Prod. Rep. 27, 711-719
9. Rae, T. D., Schmidt, P. J., Pufahl, R. A., Culotta, V. C., and O'Halloran, T. V. (1999) Undetectable intracellular free copper: the requirement of a copper chaperone for superoxide dismutase. Science 284, 805-808
10. + to transmembrane transport sites. Proc. Natl. Acad. Sci. U. S. A. 105, 5992-5997
11. Mealman, T. D., Bagai, I., Singh, P., Goodlett, D. R., Rensing, C., Zhou, H., Wysocki, V. H., and McEvoy, M. M. (2011) Interactions between CusF and CusB identified by NMR spectroscopy and chemical cross-linking coupled to mass spectrometry. Biochemistry 50, 2559-2566
12. Argüello, J. M. (2003) Identification of ion-selectivity determinants in heavy-metal transport P1b-type ATPases. J. Membr. Biol. 195, 93-108
13. Hernández-Montes, G., Argüello, J. M., and Valderrama, B. (2012) Evolution and diversity of periplasmic proteins involved in copper homeostasis in γ-proteobacteria. BMC Microbiol. 12, 249-263
14. +-ATPases: distinct efflux rates adapted to different function. Biometals 24, 467-475
15. Lutsenko, S., Barnes, N. L., Bartee, M. Y., and Dmitriev, O. Y. (2007) Function and regulation of human copper-transporting ATPases. Physiol. Rev. 87, 1011-1046
16. Argüello, J. M., González-Guerrero, M., and Raimunda, D. (2011) Bacterial transition metal P1b-ATPases: transport mechanism and roles in virulence. Biochemistry 50, 9940-9949
17. + efflux ATPases in Pseudomonas aeruginosa. Mol. Microbiol. 78, 1246-1258
18. Osman, D., Patterson, C. J., Bailey, K., Fisher, K., Robinson, N. J., Rigby, S. E., and Cavet, J. S. (2013) The copper supply pathway to a Salmonella Cu, Zn-superoxide dismutase (SodCII) involves P1B-type ATPase copper efflux and periplasmic CueP. Mol. Microbiol. 87, 466-477
19. +-ATPases. J. Biol. Chem. 283, 29753-29759
20. Gourdon, P., Liu, X. Y., Skjørringe, T., Morth, J. P., Møller, L. B., Pedersen, B. P., and Nissen, P. (2011) Crystal structure of a copper-transporting PiB-type ATPase. Nature 475, 59-64
21. + chaperones and the role of transient metal-binding sites. J. Biol. Chem. 288, 69-78
22. Kim, E. H., Nies, D. H., McEvoy, M. M., and Rensing, C. (2011) Switch or funnel: How RND-type transport systems control periplasmic metal homeostasis. J. Bacteriol. 193, 2381-2387
23. Long, F., Su, C. C., Zimmermann, M. T., Boyken, S. E., Rajashankar, K. R., Jernigan, R. L., and Yu, E. W. (2010) Crystal structures of the CusA efflux pump suggest methionine-mediated metal transport. Nature 467, 484-488
24. Loftin, I. R., Franke, S., Roberts, S. A., Weichsel, A., Héroux, A., Montfort, W. R., Rensing, C., and McEvoy, M. M. (2005) Anovel copper-binding fold for the periplasmic copper resistance protein CusF. Biochemistry 44, 10533-10540
25. Kiefer, F., Arnold, K., Künzli, M., Bordoli, L., and Schwede, T. (2009) The SWISS-MODEL repository and associated resources. Nucleic Acids Res. 37, D387-392
26. Comeau, S. R., Gatchell, D. W., Vajda, S., and Camacho, C. J. (2004) ClusPro: an automated docking and discrimination method for the prediction of protein complexes. Bioinformatics 20, 45-50
27. Kozakov, D., Brenke, R., Comeau, S. R., and Vajda, S. (2006) PIPER: an FFT-based protein docking program with pairwise potentials. Proteins 65, 392-406
28. Franke, S., Grass, G., Rensing, C., and Nies, D. H. (2003) Molecular analysis of the copper-transporting efflux system CusCFBA of Escherichia coli. J. Bacteriol. 185, 3804-3812
29. Rensing, C., Fan, B., Sharma, R., Mitra, B., and Rosen, B. P. (2000) CopA: an Escherichia coli Cu (I)-translocating P-type ATPase. Proc. Natl. Acad. Sci. U. S. A. 97, 652-656
30. Studier, F. W. (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif. 41, 207-234
31. +-ATPase from the extremophile Archaeoglobus fulgidus. J. Biol. Chem. 277, 7201-7208
32. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254
33. 2+ transporting P1B4-atpase of Mycobacterium smegmatis. Mol. Microbiol. 84, 1139-1149
34. Lanzetta, P. A., Alvarez, L. J., Reinach, P. S., and Candia, O. A. (1979) An improved assay for nanomole amounts of inorganic phosphate. Anal. Biochem. 100, 95-97
35. + transport ATPases: requirement of nucleotide binding. J. Biol. Chem. 284, 20804-20811
36. Robinson, N. J., and Winge, D. R. (2010) Copper metallochaperones. Annu. Rev. Biochem. 79, 537-562
37. Boal, A. K., and Rosenzweig, A. C. (2009) Structural biology of copper trafficking. Chem. Rev. 109, 4760-4779
38. Rosenzweig, A. C. (2002) Metallochaperones: bind and deliver. Chem. Biol. 9, 673-677
39. Banci, L., Bertini, I., McGreevy, K. S., and Rosato, A. (2010) Molecular recognition in copper trafficking. Nat. Prod. Rep. 27, 695-710
40. Banci, L., Bertini, I., Cantini, F., Felli, I. C., Gonnelli, L., Hadjiliadis, N., Pierattelli, R., Rosato, A., and Voulgaris, P. (2006) The Atx1-Ccc2 complex is a metal-mediated protein-protein interaction. Nat. Chem. Biol. 2, 367-368
41. 1B-ATPases. Biometals 20, 233-248
42. +-ATPase CopA. Biochemistry 42, 11040-11047
43. Kershaw, C. J., Brown, N. L., Constantinidou, C., Patel, M. D., and Hobman, J. L. (2005) The expression profile of Escherichia coli K-12 in response to minimal, optimal and excess copper concentrations. Microbiology 151, 1187-1198
44. Kaplan, J. H. (2002) Biochemistry of Na, K-ATPase. Annu. Rev. Biochem. 71, 511-535
45. +-ATPases present in Sinorhizobium meliloti. Microbiology 160, 1237-1251
46. Otoikhian, A., Barry, A. N., Mayfield, M., Nilges, M., Huang, Y., Lutsenko, S., and Blackburn, N. J. (2012) Lumenal loop M672-P707 of the Menkes protein (ATP7A) transfers copper to peptidylglycine monooxygenase. J. Am. Chem. Soc. 134, 10458-10468
47. Olesen, C., Picard, M., Winther, A. M., Gyrup, C., Morth, J. P., Oxvig, C., Møller, J. V., and Nissen, P. (2007) The structural basis of calcium transport by the calcium pump. Nature 450, 1036-1042