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The X-ray structure of the zinc transporter ZnuA from Salmonella enterica discloses a unique triad of zinc-coordinating histidines.

Ilari A, Alaleona F, Petrarca P, Battistoni A, Chiancone E
J Mol Biol 409 630-41 (2011)
Related entries: 2xqv, 2xy4

Cited: 26 times
EuropePMC logo PMID: 21530543

Abstract

ZnuA is the soluble component of the high-affinity ZnuABC zinc transporter belonging to the cluster 9 group of ATP-binding cassette-type periplasmic Zn- and Mn-binding proteins. In Gram-negative bacteria, the ZnuABC system is essential for zinc uptake and homeostasis and is an important determinant of bacterial resistance to the host defense mechanisms. The cluster 9 members share a two (α/β)(4) domain architecture with a long α-helix connecting the two domains. In the Zn-specific proteins, the so-called α3c and the α4 helices are separated by an insert of variable length, rich in histidine and negatively charged residues. This distinctive His-rich loop is proposed to play a role in the management of zinc also due to its location at the entrance of the metal binding site located at the domain interface. The known Synechocystis 6803 and Escherichia coli ZnuA structures show the same metal coordination involving three conserved histidines and a glutamic acid or a water molecule as fourth ligand. The structures of Salmonella enterica ZnuA, with a partially or fully occupied zinc binding site, and of a deletion mutant missing a large part of the His-rich loop revealed unexpected differences in the metal-coordinating ligands, as histidine 140 from the mobile (at the C-terminal) part of the loop substitutes the conserved histidine 60. This unforeseen coordination is rendered possible by the "open conformation" of the two domains. The possible structural determinants of these peculiarities and their functional relevance are discussed.

Reviews citing this publication (6)

  1. Metal limitation and toxicity at the interface between host and pathogen. Becker KW, Skaar EP. FEMS Microbiol Rev 38 1235-1249 (2014)
  2. Competition for zinc binding in the host-pathogen interaction. Cerasi M, Ammendola S, Battistoni A. Front Cell Infect Microbiol 3 108 (2013)
  3. Manganese uptake and streptococcal virulence. Eijkelkamp BA, McDevitt CA, Kitten T. Biometals 28 491-508 (2015)
  4. Functional Regulation of the Plasma Protein Histidine-Rich Glycoprotein by Zn2+ in Settings of Tissue Injury. Priebatsch KM, Kvansakul M, Poon IK, Hulett MD. Biomolecules 7 E22 (2017)
  5. Host-imposed manganese starvation of invading pathogens: two routes to the same destination. Morey JR, McDevitt CA, Kehl-Fie TE. Biometals 28 509-519 (2015)
  6. How Zinc-Binding Systems, Expressed by Human Pathogens, Acquire Zinc from the Colonized Host Environment: A Critical Review on Zincophores. Bellotti D, Rowińska-Żyrek M, Remelli M. Curr Med Chem 28 7312-7338 (2021)

Articles citing this publication (20)

  1. Imperfect coordination chemistry facilitates metal ion release in the Psa permease. Couñago RM, Ween MP, Begg SL, Bajaj M, Zuegg J, O'Mara ML, Cooper MA, McEwan AG, Paton JC, Kobe B, McDevitt CA. Nat Chem Biol 10 35-41 (2014)
  2. Advances in the molecular understanding of biological zinc transport. Blindauer CA. Chem Commun (Camb) 51 4544-4563 (2015)
  3. New insights into histidine triad proteins: solution structure of a Streptococcus pneumoniae PhtD domain and zinc transfer to AdcAII. Bersch B, Bougault C, Roux L, Favier A, Vernet T, Durmort C. PLoS One 8 e81168 (2013)
  4. The Salmonella enterica ZinT structure, zinc affinity and interaction with the high-affinity uptake protein ZnuA provide insight into the management of periplasmic zinc. Ilari A, Alaleona F, Tria G, Petrarca P, Battistoni A, Zamparelli C, Verzili D, Falconi M, Chiancone E. Biochim Biophys Acta 1840 535-544 (2014)
  5. The Acinetobacter baumannii Znu System Overcomes Host-Imposed Nutrient Zinc Limitation. Hesse LE, Lonergan ZR, Beavers WN, Skaar EP. Infect Immun 87 e00746-19 (2019)
  6. Transcriptional Regulation, Metal Binding Properties and Structure of Pden1597, an Unusual Zinc Transport Protein from Paracoccus denitrificans. Handali M, Neupane DP, Roychowdhury H, Yukl ET. J Biol Chem 290 11878-11889 (2015)
  7. Identification, Functional Characterization, and Regulon Prediction of the Zinc Uptake Regulator (zur) of Bacillus anthracis - An Insight Into the Zinc Homeostasis of the Pathogen. Kandari D, Gopalani M, Gupta M, Joshi H, Bhatnagar S, Bhatnagar R. Front Microbiol 9 3314 (2018)
  8. Mechanisms of zinc binding to the solute-binding protein AztC and transfer from the metallochaperone AztD. Neupane DP, Avalos D, Fullam S, Roychowdhury H, Yukl ET. J Biol Chem 292 17496-17505 (2017)
  9. Metal binding is critical for the folding and function of laminin binding protein, Lmb of Streptococcus agalactiae. Ragunathan P, Sridaran D, Weigel A, Shabayek S, Spellerberg B, Ponnuraj K. PLoS One 8 e67517 (2013)
  10. Characterization of a novel zinc transporter ZnuA acquired by Vibrio parahaemolyticus through horizontal gene transfer. Liu M, Yan M, Liu L, Chen S. Front Cell Infect Microbiol 3 61 (2013)
  11. Crystal structure of a periplasmic solute binding protein in metal-free, intermediate and metal-bound states from Candidatus Liberibacter asiaticus. Sharma N, Selvakumar P, Bhose S, Ghosh DK, Kumar P, Sharma AK. J Struct Biol 189 184-194 (2015)
  12. Zinc ion coordination as a modulating factor of the ZnuA histidine-rich loop flexibility: a molecular modeling and fluorescence spectroscopy study. Castelli S, Stella L, Petrarca P, Battistoni A, Desideri A, Falconi M. Biochem Biophys Res Commun 430 769-773 (2013)
  13. A Trap-Door Mechanism for Zinc Acquisition by Streptococcus pneumoniae AdcA. Luo Z, Morey JR, Deplazes E, Motygullina A, Tan A, Ganio K, Neville SL, Eleftheriadis N, Isselstein M, Pederick VG, Paton JC, Cordes T, Harmer JR, Kobe B, McDevitt CA. mBio 12 e01958-20 (2021)
  14. Molecular dynamics simulation of metal free structure of Lmb, a laminin-binding adhesin of Streptococcus agalactiae: metal removal and its structural implications. Sridharan U, Ragunathan P, Spellerberg B, Ponnuraj K. J Biomol Struct Dyn 37 714-725 (2019)
  15. Crystal structures of AztD provide mechanistic insights into direct zinc transfer between proteins. Neupane DP, Fullam SH, Chacón KN, Yukl ET. Commun Biol 2 308 (2019)
  16. Structure and metal-binding properties of PA4063, a novel player in periplasmic zinc trafficking by Pseudomonas aeruginosa. Fiorillo A, Battistoni A, Ammendola S, Secli V, Rinaldo S, Cutruzzolà F, Demitri N, Ilari A. Acta Crystallogr D Struct Biol 77 1401-1410 (2021)
  17. Zinc-dependent interaction between JAB1 and pre-S2 mutant large surface antigen of hepatitis B virus and its implications for viral hepatocarcinogenesis. Hsu JL, Chuang WJ, Su IJ, Gui WJ, Chang YY, Lee YP, Ai YL, Chuang DT, Huang W. J Virol 87 12675-12684 (2013)
  18. Structure and Metal Binding Properties of Chlamydia trachomatis YtgA. Luo Z, Neville SL, Campbell R, Morey JR, Menon S, Thomas M, Eijkelkamp BA, Ween MP, Huston WM, Kobe B, McDevitt CA. J Bacteriol 202 e00580-19 (2019)
  19. Conformational flexibility in the zinc solute-binding protein ZnuA. Yekwa EL, Serrano FA, Yukl E. Acta Crystallogr F Struct Biol Commun 78 128-134 (2022)
  20. Site 2 of the Yersinia pestis substrate-binding protein YfeA is a dynamic surface metal-binding site. Radka CD, Aller SG. Acta Crystallogr F Struct Biol Commun 77 286-293 (2021)


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