3nsc › Citations

Crystal structures of multicopper oxidase CueO bound to copper(I) and silver(I): functional role of a methionine-rich sequence.

Singh SK, Roberts SA, McDevitt SF, Weichsel A, Wildner GF, Grass GB, Rensing C, Montfort WR
J Biol Chem 286 37849-57 (2011)
Related entries: 3nsd, 3nsf, 3nsy, 3nt0, 3od3

Cited: 41 times
EuropePMC logo PMID: 21903583

Abstract

The multicopper oxidase CueO oxidizes toxic Cu(I) and is required for copper homeostasis in Escherichia coli. Like many proteins involved in copper homeostasis, CueO has a methionine-rich segment that is thought to be critical for copper handling. How such segments function is poorly understood. Here, we report the crystal structure of CueO at 1.1 Å with the 45-residue methionine-rich segment fully resolved, revealing an N-terminal helical segment with methionine residues juxtaposed for Cu(I) ligation and a C-terminal highly mobile segment rich in methionine and histidine residues. We also report structures of CueO with a C500S mutation, which leads to loss of the T1 copper, and CueO with six methionines changed to serine. Soaking C500S CueO crystals with Cu(I), or wild-type CueO crystals with Ag(I), leads to occupancy of three sites, the previously identified substrate-binding site and two new sites along the methionine-rich helix, involving methionines 358, 362, 368, and 376. Mutation of these residues leads to a ∼4-fold reduction in k(cat) for Cu(I) oxidation. Ag(I), which often appears with copper in nature, strongly inhibits CueO oxidase activities in vitro and compromises copper tolerance in vivo, particularly in the absence of the complementary copper efflux cus system. Together, these studies demonstrate a role for the methionine-rich insert of CueO in the binding and oxidation of Cu(I) and highlight the interplay among cue and cus systems in copper and silver homeostasis.

Articles - 3nsc mentioned but not cited (1)

  1. Crystal structures of multicopper oxidase CueO bound to copper(I) and silver(I): functional role of a methionine-rich sequence. Singh SK, Roberts SA, McDevitt SF, Weichsel A, Wildner GF, Grass GB, Rensing C, Montfort WR. J Biol Chem 286 37849-37857 (2011)


Reviews citing this publication (9)

  1. Copper homeostasis at the host-pathogen interface. Hodgkinson V, Petris MJ. J Biol Chem 287 13549-13555 (2012)
  2. Bacterial multidrug efflux transporters. Delmar JA, Su CC, Yu EW. Annu Rev Biophys 43 93-117 (2014)
  3. Molecular basis of active copper resistance mechanisms in Gram-negative bacteria. Bondarczuk K, Piotrowska-Seget Z. Cell Biol Toxicol 29 397-405 (2013)
  4. Resistance mechanisms of Mycobacterium tuberculosis against phagosomal copper overload. Rowland JL, Niederweis M. Tuberculosis (Edinb) 92 202-210 (2012)
  5. Laccases of prokaryotic origin: enzymes at the interface of protein science and protein technology. Martins LO, Durão P, Brissos V, Lindley PF. Cell Mol Life Sci 72 911-922 (2015)
  6. Heavy Metal Toxicity in Armed Conflicts Potentiates AMR in A. baumannii by Selecting for Antibiotic and Heavy Metal Co-resistance Mechanisms. Bazzi W, Abou Fayad AG, Nasser A, Haraoui LP, Dewachi O, Abou-Sitta G, Nguyen VK, Abara A, Karah N, Landecker H, Knapp C, McEvoy MM, Zaman MH, Higgins PG, Matar GM. Front Microbiol 11 68 (2020)
  7. Heavy metal transport by the CusCFBA efflux system. Delmar JA, Su CC, Yu EW. Protein Sci 24 1720-1736 (2015)
  8. Ag+ Complexes as Potential Therapeutic Agents in Medicine and Pharmacy. Hecel A, Kolkowska P, Krzywoszynska K, Szebesczyk A, Rowinska-Zyrek M, Kozlowski H. Curr Med Chem 26 624-647 (2019)
  9. Molecular regulation of conditioning film formation and quorum quenching in sulfate reducing bacteria. Raya D, Shreya A, Kumar A, Giri SK, Salem DR, Gnimpieba EZ, Gadhamshetty V, Dhiman SS. Front Microbiol 13 1008536 (2022)

Articles citing this publication (31)

  1. A multicopper oxidase is required for copper resistance in Mycobacterium tuberculosis. Rowland JL, Niederweis M. J Bacteriol 195 3724-3733 (2013)
  2. Bacterial killing in macrophages and amoeba: do they all use a brass dagger? German N, Doyscher D, Rensing C. Future Microbiol 8 1257-1264 (2013)
  3. Copper complexation screen reveals compounds with potent antibiotic properties against methicillin-resistant Staphylococcus aureus. Haeili M, Moore C, Davis CJ, Cochran JB, Shah S, Shrestha TB, Zhang Y, Bossmann SH, Benjamin WH, Kutsch O, Wolschendorf F. Antimicrob Agents Chemother 58 3727-3736 (2014)
  4. A comprehensive platform to investigate protein-metal ion interactions by affinity capillary electrophoresis. Alhazmi HA, Nachbar M, Albishri HM, Abd El-Hady D, Redweik S, El Deeb S, Wätzig H. J Pharm Biomed Anal 107 311-317 (2015)
  5. SilE is an intrinsically disordered periplasmic "molecular sponge" involved in bacterial silver resistance. Asiani KR, Williams H, Bird L, Jenner M, Searle MS, Hobman JL, Scott DJ, Soultanas P. Mol Microbiol 101 731-742 (2016)
  6. The mechanism of copper uptake by tyrosinase from Bacillus megaterium. Kanteev M, Goldfeder M, Chojnacki M, Adir N, Fishman A. J Biol Inorg Chem 18 895-903 (2013)
  7. Bactericidal potential of silver nanoparticles synthesized using cell-free extract of Comamonas acidovorans: in vitro and in silico approaches. Rudakiya DM, Pawar K. 3 Biotech 7 92 (2017)
  8. Crystal structure of the multicopper oxidase from the pathogenic bacterium Campylobacter jejuni CGUG11284: characterization of a metallo-oxidase. Silva CS, Durão P, Fillat A, Lindley PF, Martins LO, Bento I. Metallomics 4 37-47 (2012)
  9. New silver nanoparticles induce apoptosis-like process in E. coli and interfere with mammalian copper metabolism. Orlov IA, Sankova TP, Babich PS, Sosnin IM, Ilyechova EY, Kirilenko DA, Brunkov PN, Ataev GL, Romanov AE, Puchkova LV. Int J Nanomedicine 11 6561-6574 (2016)
  10. The functional roles of the three copper sites associated with the methionine-rich insert in the multicopper oxidase CueO from E. coli. Cortes L, Wedd AG, Xiao Z. Metallomics 7 776-785 (2015)
  11. Structural analysis and biochemical properties of laccase enzymes from two Pediococcus species. Olmeda I, Casino P, Collins RE, Sendra R, Callejón S, Huesa J, Soares AS, Ferrer S, Pardo I. Microb Biotechnol 14 1026-1043 (2021)
  12. Assessing the genetic diversity of Cu resistance in mine tailings through high-throughput recovery of full-length copA genes. Li X, Zhu YG, Shaban B, Bruxner TJ, Bond PL, Huang L. Sci Rep 5 13258 (2015)
  13. Elucidation of the crystal structure of Coriolopsis caperata laccase: restoration of the structure and activity of the native enzyme from the T2-depleted form by copper ions. Glazunova OA, Polyakov KM, Fedorova TV, Dorovatovskii PV, Koroleva OV. Acta Crystallogr D Biol Crystallogr 71 854-861 (2015)
  14. Atomic differentiation of silver binding preference in protein targets: Escherichia coli malate dehydrogenase as a paradigm. Wang H, Yang X, Wang M, Hu M, Xu X, Yan A, Hao Q, Li H, Sun H. Chem Sci 11 11714-11719 (2020)
  15. Crystal structure of the CueO mutants at Glu506, the key amino acid located in the proton transfer pathway for dioxygen reduction. Komori H, Kajikawa T, Kataoka K, Higuchi Y, Sakurai T. Biochem Biophys Res Commun 438 686-690 (2013)
  16. Interaction of Copper Toxicity and Oxidative Stress in Campylobacter jejuni. Gardner SP, Olson JW. J Bacteriol 200 e00208-18 (2018)
  17. Activity-stability relationships revisited in blue oxidases catalyzing electron transfer at extreme temperatures. Roulling F, Godin A, Cipolla A, Collins T, Miyazaki K, Feller G. Extremophiles 20 621-629 (2016)
  18. Electron transfer rate analysis of a site-specifically wired copper oxidase. Schlesinger O, Pasi M, Dandela R, Meijler MM, Alfonta L. Phys Chem Chem Phys 20 6159-6166 (2018)
  19. Gene cloning, identification, and characterization of the multicopper oxidase CumA from Pseudomonas sp. 593. Yang S, Long Y, Yan H, Cai H, Li Y, Wang X. Biotechnol Appl Biochem 64 347-355 (2017)
  20. Maturation of Rhodobacter capsulatus Multicopper Oxidase CutO Depends on the CopA Copper Efflux Pathway and Requires the cutF Product. Öztürk Y, Blaby-Haas CE, Daum N, Andrei A, Rauch J, Daldal F, Koch HG. Front Microbiol 12 720644 (2021)
  21. Engineering of Laccase CueO for Improved Electron Transfer in Bioelectrocatalysis by Semi-Rational Design. Zhang L, Cui H, Dhoke GV, Zou Z, Sauer DF, Davari MD, Schwaneberg U. Chemistry 26 4974-4979 (2020)
  22. Lability and liability of endogenous copper pools. Outten FW, Munson GP. J Bacteriol 195 4553-4555 (2013)
  23. Copper Binding and Redox Activity of α-Synuclein in Membrane-Like Environment. Bacchella C, Camponeschi F, Kolkowska P, Kola A, Tessari I, Baratto MC, Bisaglia M, Monzani E, Bubacco L, Mangani S, Casella L, Dell'Acqua S, Valensin D. Biomolecules 13 287 (2023)
  24. Crystal structures of multicopper oxidase CueO G304K mutant: structural basis of the increased laccase activity. Wang H, Liu X, Zhao J, Yue Q, Yan Y, Gao Z, Dong Y, Zhang Z, Fan Y, Tian J, Wu N, Gong Y. Sci Rep 8 14252 (2018)
  25. Development and structural characterization of an engineered multi-copper oxidase reporter of protein-protein interactions. Sana B, Chee SMQ, Wongsantichon J, Raghavan S, Robinson RC, Ghadessy FJ. J Biol Chem 294 7002-7012 (2019)
  26. Mn(III) species formed by the multi-copper oxidase MnxG investigated by electron paramagnetic resonance spectroscopy. Tao L, Stich TA, Soldatova AV, Tebo BM, Spiro TG, Casey WH, Britt RD. J Biol Inorg Chem 23 1093-1104 (2018)
  27. Periplasmic oxidized-protein repair during copper stress in E. coli: A focus on the metallochaperone CusF. Vergnes A, Henry C, Grassini G, Loiseau L, El Hajj S, Denis Y, Galinier A, Vertommen D, Aussel L, Ezraty B. PLoS Genet 18 e1010180 (2022)
  28. Desulfovibrio DA2_CueO is a novel multicopper oxidase with cuprous, ferrous and phenol oxidase activity. Mancini S, Kumar R, Mishra V, Solioz M. Microbiology (Reading) 163 1229-1236 (2017)
  29. Antimicrobial properties of ternary eutectic aluminum alloys. Hahn C, Hans M, Hein C, Dennstedt A, Mücklich F, Rettberg P, Hellweg CE, Leichert LI, Rensing C, Moeller R. Biometals 31 759-770 (2018)
  30. Feasible Cluster Model Method for Simulating the Redox Potentials of Laccase CueO and Its Variant. Jiang Q, Cui Z, Wei R, Nie K, Xu H, Liu L. Front Bioeng Biotechnol 10 957694 (2022)
  31. Insights into the binding of Ag ions with SilE model peptides: an NMR and MS coupled approach. Zingale GA, Oliveri V, Grasso G. Metallomics 15 mfad015 (2023)


Quick links