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Promiscuous nickel import in human pathogens: structure, thermodynamics, and evolution of extracytoplasmic nickel-binding proteins.

Lebrette H, Brochier-Armanet C, Zambelli B, de Reuse H, Borezée-Durant E, Ciurli S, Cavazza C
Structure 22 1421-32 (2014)
Related entries: 4oer, 4oes, 4oet, 4oeu, 4oev, 4ofl

Cited: 16 times
EuropePMC logo PMID: 25199691

Abstract

In human pathogenic bacteria, nickel is required for the activation of two enzymes, urease and [NiFe]-hydrogenase, necessary for host infection. Acquisition of Ni(II) is mediated by either permeases or ABC-importers, the latter including a subclass that involves an extracytoplasmic nickel-binding protein, Ni-BP. This study reports on the structure of three Ni-BPs from a diversity of human pathogens and on the existence of three new nickel-binding motifs. These are different from that previously described for Escherichia coli Ni-BP NikA, known to bind nickel via a nickelophore, and indicate a variegated ligand selectivity for Ni-BPs. The structures are consistent with ligand affinities measured in solution by calorimetry and challenge the hypothesis of a general requirement of nickelophores for nickel uptake by canonical ABC importers. Phylogenetic analyses showed that Ni-BPs have different evolutionary origins and emerged independently from peptide-binding proteins, possibly explaining the promiscuous behavior of this class of Ni(II) carriers.

Reviews citing this publication (5)

  1. Selective substrate uptake: The role of ATP-binding cassette (ABC) importers in pathogenesis. Tanaka KJ, Song S, Mason K, Pinkett HW. Biochim Biophys Acta Biomembr 1860 868-877 (2018)
  2. Microbial nickel: cellular uptake and delivery to enzyme centers. Zeer-Wanklyn CJ, Zamble DB. Curr Opin Chem Biol 37 80-88 (2017)
  3. Nickel recognition by bacterial importer proteins. Chivers PT. Metallomics 7 590-595 (2015)
  4. The Key Element Role of Metallophores in the Pathogenicity and Virulence of Staphylococcus aureus: A Review. Ghssein G, Ezzeddine Z. Biology (Basel) 11 1525 (2022)
  5. Metal homeostasis in pathogenic Epsilonproteobacteria: mechanisms of acquisition, efflux, and regulation. Kelley BR, Lu J, Haley KP, Gaddy JA, Johnson JG. Metallomics 13 mfaa002 (2021)

Articles citing this publication (11)

  1. The Metallophore Staphylopine Enables Staphylococcus aureus To Compete with the Host for Zinc and Overcome Nutritional Immunity. Grim KP, San Francisco B, Radin JN, Brazel EB, Kelliher JL, Párraga Solórzano PK, Kim PC, McDevitt CA, Kehl-Fie TE. mBio 8 e01281-17 (2017)
  2. Characterization in Helicobacter pylori of a Nickel Transporter Essential for Colonization That Was Acquired during Evolution by Gastric Helicobacter Species. Fischer F, Robbe-Saule M, Turlin E, Mancuso F, Michel V, Richaud P, Veyrier FJ, De Reuse H, Vinella D. PLoS Pathog 12 e1006018 (2016)
  3. Structure and mechanism of a group-I cobalt energy coupling factor transporter. Bao Z, Qi X, Hong S, Xu K, He F, Zhang M, Chen J, Chao D, Zhao W, Li D, Wang J, Zhang P. Cell Res 27 675-687 (2017)
  4. Mechanistic insights into staphylopine-mediated metal acquisition. Song L, Zhang Y, Chen W, Gu T, Zhang SY, Ji Q. Proc Natl Acad Sci U S A 115 3942-3947 (2018)
  5. Novel insights into nickel import in Staphylococcus aureus: the positive role of free histidine and structural characterization of a new thiazolidine-type nickel chelator. Lebrette H, Borezée-Durant E, Martin L, Richaud P, Boeri Erba E, Cavazza C. Metallomics 7 613-621 (2015)
  6. Crystal structure of the putative peptide-binding protein AppA from Clostridium difficile. Hughes A, Wilson S, Dodson EJ, Turkenburg JP, Wilkinson AJ. Acta Crystallogr F Struct Biol Commun 75 246-253 (2019)
  7. ATP-Binding Cassette Transporters: Snap-on Complexes? Younus I, Kochkina S, Choi CC, Sun W, Ford RC. Subcell Biochem 99 35-82 (2022)
  8. Biochemical studies highlight determinants for metal selectivity in the Escherichia coli periplasmic solute binding protein NikA. Law WWH, Kanelis V, Zamble DB. Metallomics 14 mfac084 (2022)
  9. In vitro maturation of NiSOD reveals a role for cytoplasmic histidine in processing and metalation. Basak P, Cabelli DE, Chivers PT, Farquhar ER, Maroney MJ. Metallomics 15 mfad054 (2023)
  10. Metal selectivity and translocation mechanism characterization in proteoliposomes of the transmembrane NiCoT transporter NixA from Helicobacter pylori. Hernandez JA, Micus PS, Sunga SAL, Mazzei L, Ciurli S, Meloni G. Chem Sci 15 651-665 (2024)
  11. Synthesis, Structure, and Characterization of Tris(1-ethyl-4-isopropyl-imidazolyl-κN)phosphine Nickel(II) Complexes. Banerjee A, Li J, Easley CR, Brennessel WW, Loloee R, Chavez FA. Inorganica Chim Acta 489 170-179 (2019)


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