Structural and thermodynamic characterization of metal ion binding in Streptococcus suis Dpr

Journal of Molecular Biology

Volumn 405, Issue 2, 2011, Pages 448-460

  Haikarainen, Teemu ^a   Thanassoulas, Angelos ^b   Stavros, Philemon ^b   Nounesis, George ^b   Haataja, Sauli ^a   Papageorgiou, Anastassios C ^a  

^a UNIVERSITY OF TURKU   (Finland)

^b INSTITUTE OF NANOSCIENCE AND NANOTECHNOLOGY   (Greece)

Author keywords

Dps protein; ferritin; ferroxidase; isothermal titration calorimetry; metal binding

Indexed keywords

BACTERIAL PROTEIN; COBALT; COPPER ION; MAGNESIUM ION; MANGANESE; METAL ION; NICKEL; PROTEIN DPS LIKE PEROXIDE RESISTANCE; UNCLASSIFIED DRUG; ZINC ION;

ARTICLE; BINDING SITE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STRUCTURE; STREPTOCOCCUS SUIS; THERMODYNAMICS;

STREPTOCOCCUS SUIS;

EID: 78650895836     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.10.058     Document Type: Article

References (41)

1. Almirón M., Link A.J., Furlong D., and Kolter R. A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli Genes Dev. 6 1992 2646 2654
2. Haikarainen T., and Papageorgiou A. Dps-like proteins: structural and functional insights into a versatile protein family Cell Mol. Life Sci. 67 2010 341 351
3. Chiancone E., and Ceci P. The multifaceted capacity of Dps proteins to combat bacterial stress conditions: detoxification of iron and hydrogen peroxide and DNA binding Biochim. Biophys. Acta 1800 2010 798 805
4. Galvez N., Sanchez P., and Dominguez-Vera J.M. Preparation of Cu and CuFe Prussian Blue derivative nanoparticles using the apoferritin cavity as nanoreactor Dalton Trans. 2005 2492 2494
5. Douglas T., and Stark V.T. Nanophase cobalt oxyhydroxide mineral synthesized within the protein cage of ferritin Inorg. Chem. 39 2000 1828 1830
6. Okuda M., Iwahori K., Yamashita I., and Yoshimura H. Fabrication of nickel and chromium nanoparticles using the protein cage of apoferritin Biotechnol. Bioeng. 84 2003 187 194
7. Kasyutich O., Ilari A., Fiorillo A., Tatchev D., Hoell A., and Ceci P. Silver ion incorporation and nanoparticle formation inside the cavity of Pyrococcus furiosus ferritin: structural and size-distribution analyses J. Am. Chem. Soc. 132 2010 3621 3627
8. Ilari A., Stefanini S., Chiancone E., and Tsernoglou D. The dodecameric ferritin from Listeria innocua contains a novel intersubunit iron-binding site Nat. Struct. Biol. 7 2000 38 43
9. Ren B., Tibbelin G., Kajino T., Asami O., and Ladenstein R. The multi-layered structure of Dps with a novel di-nuclear ferroxidase center J. Mol. Biol. 329 2003 467 477
10. Zeth K., Offermann S., Essen L.O., and Oesterhelt D. Iron-oxo clusters biomineralizing on protein surfaces: structural analysis of Halobacterium salinarum DpsA in its low- and high-iron states Proc. Natl Acad. Sci. USA 101 2004 13780 13785
11. Romao C.V., Mitchell E.P., and McSweeney S. The crystal structure of Deinococcus radiodurans Dps protein (DR2263) reveals the presence of a novel metal centre in the N terminus J. Biol. Inorg. Chem. 11 2006 891 902
12. Havukainen H., Haataja S., Kauko A., Pulliainen A.T., Salminen A., and Haikarainen T. Structural basis of the zinc- and terbium-mediated inhibition of ferroxidase activity in Dps ferritin-like proteins Protein Sci. 17 2008 1513 1521
13. Alaleona F., Franceschini S., Ceci P., Ilari A., and Chiancone E. Thermosynechoccus elongatus DpsA binds Zn(II) at a unique three histidine-containing ferroxidase center and utilizes O(2) as iron oxidant with very high efficiency, unlike the typical Dps proteins FEBS J. 277 2010 903 917
14. Haikarainen T., Tsou C.C., Wu J.J., and Papageorgiou A.C. Structural characterization and biological implications of di-zinc binding in the ferroxidase center of Streptococcus pyogenes Dpr Biochem. Biophys. Res. Commun. 398 2010 361 365
15. Thieme D., and Grass G. The Dps protein of Escherichia coli is involved in copper homeostasis Microbiol. Res. 165 2010 108 115
16. Tsou C.C., Chiang-Ni C., Lin Y.S., Chuang W.J., Lin M.T., Liu C.C., and Wu J.J. An iron-binding protein, Dpr, decreases hydrogen peroxide stress and protects Streptococcus pyogenes against multiple stresses Infect. Immun. 76 2008 4038 4045
17. Kauko A., Pulliainen A.T., Haataja S., Meyer-Klaucke W., Finne J., and Papageorgiou A.C. Iron incorporation in Streptococcus suis Dps-like peroxide resistance protein Dpr requires mobility in the ferroxidase center and leads to the formation of a ferrihydrite-like core J. Mol. Biol. 364 2006 97 109
18. Kauko A., Haataja S., Pulliainen A.T., Finne J., and Papageorgiou A.C. Crystal structure of Streptococcus suis Dps-like peroxide resistance protein Dpr: implications for iron incorporation J. Mol. Biol. 338 2004 547 558
19. Bellapadrona G., Stefanini S., Zamparelli C., Theil E.C., and Chiancone E. Iron translocation into and out of Listeria innocua Dps and size distribution of the protein-enclosed nanomineral are modulated by the electrostatic gradient at the 3-fold "ferritin-like" pores J. Biol. Chem. 284 2009 19101 19109
20. Haikarainen T., Tsou C.C., Wu J.J., and Papageorgiou A.C. Crystal structures of Streptococcus pyogenes Dpr reveal a dodecameric iron-binding protein with a ferroxidase site J. Biol. Inorg. Chem. 15 2010 183 194
21. Ilari A., Ceci P., Ferrari D., Rossi G.L., and Chiancone E. Iron incorporation into Escherichia coli Dps gives rise to a ferritin-like microcrystalline core J. Biol. Chem. 277 2002 37619 37623
22. Su M., Cavallo S., Stefanini S., Chiancone E., and Chasteen N.D. The so-called Listeria innocua ferritin is a Dps protein. Iron incorporation, detoxification, and DNA protection properties Biochemistry 44 2005 5572 5578
23. Bou-Abdallah F., Woodhall M.R., Velazquez-Campoy A., Andrews S.C., and Chasteen N.D. Thermodynamic analysis of ferrous ion binding to Escherichia coli ferritin EcFtnA Biochemistry 44 2005 13837 13846
24. Bou-Abdallah F., Adinolfi S., Pastore A., Laue T.M., and Dennis Chasteen N. Iron binding and oxidation kinetics in frataxin CyaY of Escherichia coli J. Mol. Biol. 341 2004 605 615
25. Bou-Abdallah F., Arosio P., Santambrogio P., Yang X., Janus-Chandler C., and Chasteen N.D. Ferrous ion binding to recombinant human H-chain ferritin. An isothermal titration calorimetry study Biochemistry 41 2002 11184 11891
26. Bou-Abdallah F., Arosio P., Levi S., Janus-Chandler C., and Chasteen N.D. Defining metal ion inhibitor interactions with recombinant human H- and L-chain ferritins and site-directed variants: an isothermal titration calorimetry study J. Biol. Inorg. Chem. 8 2003 489 497
27. Glusker J.P., Katz A.P., and Bock C.W. Metal ions in biological systems Rigaku J. 16 1999 8 16
28. Ha Y., Shi D., Small G.W., Theil E.C., and Allewell N.M. Crystal structure of bullfrog M ferritin at 2.8 Å resolution: analysis of subunit interactions and the binuclear metal center J. Biol. Inorg. Chem. 4 1999 243 256
29. Langlois d'Estaintot B., Santambrogio P., Granier T., Gallois B., Chevalier J.M., and Precigoux G. Crystal structure and biochemical properties of the human mitochondrial ferritin and its mutant Ser144Ala J. Mol. Biol. 340 2004 277 293
30. Kim S.G., Bhattacharyya G., Grove A., and Lee Y.H. Crystal structure of Dps-1, a functionally distinct Dps protein from Deinococcus radiodurans J. Mol. Biol. 361 2006 105 114
31. Dundon W.G., Polenghi A., Del Guidice G., Rappuoli R., and Montecucco C. Neutrophil-activating protein (HP-NAP) versus ferritin (Pfr): comparison of synthesis in Helicobacter pylori FEMS Microbiol. Lett. 199 2001 143 149
32. Price D., and Joshi J.G. Ferritin: a zinc detoxicant and a zinc ion donor Proc. Natl Acad. Sci. USA 79 1982 3116 3119
33. Haataja S., Penttinen A., Pulliainen A.T., Tikkanen K., Finne J., and Papageorgiou A.C. Expression, purification and crystallization of Dpr, a ferritin-like protein from the Gram-positive meningitis-associated bacterium Streptococcus suis Acta Crystallogr. Sect. D 58 2002 1851 1853
34. Kabsch W. XDS Acta Crystallogr. Sect. D 66 2010 125 132
35. Leslie A.G. The integration of macromolecular diffraction data Acta Crystallogr. Sect. D 62 2006 48 57
36. Collaborative Computational Project The CCP4 suite: programs for protein crystallography Acta Crystallogr. Sect. D 50 1994 760 763
37. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. Sect. D 53 1997 240 255
38. Winn M.D., Isupov M.N., and Murshudov G.N. Use of TLS parameters to model anisotropic displacements in macromolecular refinement Acta Crystallogr. Sect. D 57 2001 122 133
39. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics Acta Crystallogr. Sect. D 60 2004 2126 2132
40. Krissinel E., and Henrick K. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions Acta Crystallogr. Sect. D 60 2004 2256 2268
41. Wiseman T., Williston S., Brandts J.F., and Lin L.N. Rapid measurement of binding constants and heats of binding using a new titration calorimeter Anal. Biochem. 179 1989 131 137