A Redox Switch in CopC: an Intriguing Copper Trafficking Protein That Binds Copper(I) and Copper(II) at Different Sites

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2003 Mar 26

PMID 12651950

Citations 56

Authors

Fabio Arnesano

Lucia Banci

Ivano Bertini

Stefano Mangani

Andrew R Thompsett

Affiliations

Soon will be listed here.

Abstract

The protein CopC from Pseudomonas syringae has been found capable of binding copper(I) and copper(II) at two different sites, occupied either one at a time or simultaneously. The protein, consisting of 102 amino acids, is known to bind copper(II) in a position that is now found consistent with a coordination arrangement including His-1, Glu-27, Asp-89, and His-91. A full solution structure analysis is reported here for Cu(I)-CopC. The copper(I) site is constituted by His-48 and three of the four Met residues (40, 43, 46, 51), which are clustered in a Met-rich region. Both copper binding sites have been characterized through extended x-ray absorption fine structure studies. They represent novel coordination environments for copper in proteins. The two sites are approximately 30 A far apart and have little affinity for the ion in the other oxidation state. Oxidation of Cu(I)-CopC or reduction of Cu(II)-CopC causes migration of copper from one site to the other. This behavior is observed both in NMR and EXAFS studies and indicates that CopC can exchange copper between two sites activated by a redox switch. CopC resides in the periplasm of Gram-negative bacteria where there is a multicopper oxidase, CopA, which may modulate the redox state of copper. CopC and CopA are coded in the same operon, responsible for copper resistance. These peculiar and novel properties of CopC are discussed with respect to their relevance for copper homeostasis.

Citing Articles

Biomimetic Pseudopeptides to Decipher the Interplay between Cu and Methionine-Rich Domains in Proteins.

Badillo-Gomez J, Suarez-Antuna I, Mazurenko I, Biaso F, Pecaut J, Lojou E Chemistry. 2024; 31(11):e202403896.

PMID: 39715023 PMC: 11840665. DOI: 10.1002/chem.202403896.

Bacterial Metallostasis: Metal Sensing, Metalloproteome Remodeling, and Metal Trafficking.

Capdevila D, Rondon J, Edmonds K, Rocchio J, Villarruel Dujovne M, Giedroc D Chem Rev. 2024; 124(24):13574-13659.

PMID: 39658019 PMC: 11672702. DOI: 10.1021/acs.chemrev.4c00264.

Characterization of three rapidly growing novel species with significant polycyclic aromatic hydrocarbon bioremediation potential.

Deng Y, Mou T, Wang J, Su J, Yan Y, Zhang Y Front Microbiol. 2023; 14:1225746.

PMID: 37744919 PMC: 10517868. DOI: 10.3389/fmicb.2023.1225746.

Orchestrating copper binding: structure and variations on the cupredoxin fold.

Guo J, Fisher O J Biol Inorg Chem. 2022; 27(6):529-540.

PMID: 35994119 DOI: 10.1007/s00775-022-01955-2.

Unique underlying principles shaping copper homeostasis networks.

Novoa-Aponte L, Arguello J J Biol Inorg Chem. 2022; 27(6):509-528.

PMID: 35802193 PMC: 9470648. DOI: 10.1007/s00775-022-01947-2.

References

Roberts S, Weichsel A, Grass G, Thakali K, Hazzard J, Tollin G . Crystal structure and electron transfer kinetics of CueO, a multicopper oxidase required for copper homeostasis in Escherichia coli. Proc Natl Acad Sci U S A. 2002; 99(5):2766-71. PMC: 122422. DOI: 10.1073/pnas.052710499. View

Outten F, Huffman D, Hale J, OHalloran T . The independent cue and cus systems confer copper tolerance during aerobic and anaerobic growth in Escherichia coli. J Biol Chem. 2001; 276(33):30670-7. DOI: 10.1074/jbc.M104122200. View

Banci L, Felli I, Kummerle R . Direct detection of hydrogen bonds in monomeric superoxide dismutase: biological implications. Biochemistry. 2002; 41(9):2913-20. DOI: 10.1021/bi011617b. View

Grass G, Rensing C . Genes involved in copper homeostasis in Escherichia coli. J Bacteriol. 2001; 183(6):2145-7. PMC: 95116. DOI: 10.1128/JB.183.6.2145-2147.2001. View

Guntert P, Mumenthaler C, Wuthrich K . Torsion angle dynamics for NMR structure calculation with the new program DYANA. J Mol Biol. 1997; 273(1):283-98. DOI: 10.1006/jmbi.1997.1284. View

Puig S, Lee J, Lau M, Thiele D . Biochemical and genetic analyses of yeast and human high affinity copper transporters suggest a conserved mechanism for copper uptake. J Biol Chem. 2002; 277(29):26021-30. DOI: 10.1074/jbc.M202547200. View

Rae T, Schmidt P, Pufahl R, Culotta V, OHalloran T . Undetectable intracellular free copper: the requirement of a copper chaperone for superoxide dismutase. Science. 1999; 284(5415):805-8. DOI: 10.1126/science.284.5415.805. View

Eccles C, Guntert P, Billeter M, Wuthrich K . Efficient analysis of protein 2D NMR spectra using the software package EASY. J Biomol NMR. 1991; 1(2):111-30. DOI: 10.1007/BF01877224. View

Hassett R, Kosman D . Evidence for Cu(II) reduction as a component of copper uptake by Saccharomyces cerevisiae. J Biol Chem. 1995; 270(1):128-34. DOI: 10.1074/jbc.270.1.128. View

10.

Arnesano F, Banci L, Bertini I, Thompsett A . Solution structure of CopC: a cupredoxin-like protein involved in copper homeostasis. Structure. 2002; 10(10):1337-47. DOI: 10.1016/s0969-2126(02)00858-4. View

11.

Arnesano F, Banci L, Bertini I, Cantini F, Ciofi-Baffoni S, Huffman D . Characterization of the binding interface between the copper chaperone Atx1 and the first cytosolic domain of Ccc2 ATPase. J Biol Chem. 2001; 276(44):41365-76. DOI: 10.1074/jbc.M104807200. View

12.

Eisses J, Stasser J, Ralle M, Kaplan J, Blackburn N . Domains I and III of the human copper chaperone for superoxide dismutase interact via a cysteine-bridged Dicopper(I) cluster. Biochemistry. 2000; 39(25):7337-42. DOI: 10.1021/bi000690j. View

13.

Cooksey D . Molecular mechanisms of copper resistance and accumulation in bacteria. FEMS Microbiol Rev. 1994; 14(4):381-6. DOI: 10.1111/j.1574-6976.1994.tb00112.x. View

14.

Guntert P, Braun W, Wuthrich K . Efficient computation of three-dimensional protein structures in solution from nuclear magnetic resonance data using the program DIANA and the supporting programs CALIBA, HABAS and GLOMSA. J Mol Biol. 1991; 217(3):517-30. DOI: 10.1016/0022-2836(91)90754-t. View

15.

Koradi R, Billeter M, Wuthrich K . MOLMOL: a program for display and analysis of macromolecular structures. J Mol Graph. 1996; 14(1):51-5, 29-32. DOI: 10.1016/0263-7855(96)00009-4. View

16.

Silver S . Bacterial resistances to toxic metal ions--a review. Gene. 1996; 179(1):9-19. DOI: 10.1016/s0378-1119(96)00323-x. View

17.

Briganti F, Mangani S, Pedocchi L, Scozzafava A, Golovleva L, Jadan A . XAS characterization of the active sites of novel intradiol ring-cleaving dioxygenases: hydroxyquinol and chlorocatechol dioxygenases. FEBS Lett. 1998; 433(1-2):58-62. DOI: 10.1016/s0014-5793(98)00884-9. View

18.

Lee L, Rance M, Chazin W, Palmer 3rd A . Rotational diffusion anisotropy of proteins from simultaneous analysis of 15N and 13C alpha nuclear spin relaxation. J Biomol NMR. 1997; 9(3):287-98. DOI: 10.1023/a:1018631009583. View

19.

Huffman D, Huyett J, Outten F, Doan P, Finney L, Hoffman B . Spectroscopy of Cu(II)-PcoC and the multicopper oxidase function of PcoA, two essential components of Escherichia coli pco copper resistance operon. Biochemistry. 2002; 41(31):10046-55. DOI: 10.1021/bi0259960. View

20.

Puig S, Rees E, Thiele D . The ABCDs of periplasmic copper trafficking. Structure. 2002; 10(10):1292-5. DOI: 10.1016/s0969-2126(02)00863-8. View