1887

Abstract

Iron is an essential micronutrient for living organisms as it is involved in a broad variety of important biological processes. However, free iron inside the cell could be potentially toxic, generating hydroxyl radicals through the Fenton reaction. Dps (DNA-binding protein from starved cells) belongs to a subfamily of ferritins and can store iron atoms inside the dodecamer. The presence of a ferroxidase centre, composed of highly conserved residues, is a signature of this protein family. In this study, we analysed the role of two conserved histidine residues (H25 and H37) located at the ferroxidase centre of the Dps protein by replacing them with glycine residues. The H25G/H37G substituted variant showed reduced iron binding and ferroxidase activities in comparison with wt Dps, while DNA-binding activity remained unaffected. We also found that both CjDps wt and CjDps H25G/H37G were able to bind manganese atoms. These results indicate that the H25 and H37 residues at the ferroxidase centre of Dps are not strictly required for metal binding and oxidation.

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2016-01-01
2019-10-21
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References

  1. Acheson D. , Allos B. M. . ( 2001;). Campylobacter jejuni infections: update on emerging issues and trends. Clin Infect Dis 32: 1201–1206 [CrossRef] [PubMed].
    [Google Scholar]
  2. Almirón M. , Link A. J. , Furlong D. , Kolter R. . ( 1992;). A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli . Genes Dev 6: 2646–2654 [CrossRef] [PubMed].
    [Google Scholar]
  3. Altekruse S. F. , Stern N. J. , Fields P. I. , Swerdlow D. L. . ( 1999;). Campylobacter jejuni – an emerging foodborne pathogen. Emerg Infect Dis 5: 28–35 [PubMed].[CrossRef]
    [Google Scholar]
  4. Andrews S. C. , Robinson A. K. , Rodríguez-Quiñones F. . ( 2003;). Bacterial iron homeostasis. FEMS Microbiol Rev 27: 215–237 [CrossRef] [PubMed].
    [Google Scholar]
  5. Ardini M. , Fiorillo A. , Fittipaldi M. , Stefanini S. , Gatteschi D. , Ilari A. , Chiancone E. . ( 2013;). Kineococcus radiotolerans Dps forms a heteronuclear Mn-Fe ferroxidase center that may explain the Mn-dependent protection against oxidative stress. Biochim Biophys Acta 1830: 3745–3755.[CrossRef]
    [Google Scholar]
  6. Arnold A. R. , Barton J. K. . ( 2013;). DNA protection by the bacterial ferritin Dps via DNA charge transport. J Am Chem Soc 135: 15726–15729 [CrossRef] [PubMed].
    [Google Scholar]
  7. Blaser M. J. . ( 1997;). Epidemiologic and clinical features of Campylobacter jejuni infections. J Infect Dis 176: (Suppl. 2), S103–S105 [CrossRef] [PubMed].
    [Google Scholar]
  8. Bou-Abdallah F. . ( 2010;). The iron redox and hydrolysis chemistry of the ferritins. Biochim Biophys Acta 1800: 719–731.[CrossRef]
    [Google Scholar]
  9. Bozzi M. , Mignogna G. , Stefanini S. , Barra D. , Longhi C. , Valenti P. , Chiancone E. . ( 1997;). A novel non-heme iron-binding ferritin related to the DNA-binding proteins of the Dps family in Listeria innocua . J Biol Chem 272: 3259–3265 [CrossRef] [PubMed].
    [Google Scholar]
  10. Ceci P. , Cellai S. , Falvo E. , Rivetti C. , Rossi G. L. , Chiancone E. . ( 2004;). DNA condensation and self-aggregation of Escherichia coli Dps are coupled phenomena related to the properties of the N-terminus. Nucleic Acids Res 32: 5935–5944 [CrossRef] [PubMed].
    [Google Scholar]
  11. Ceci P. , Mangiarotti L. , Rivetti C. , Chiancone E. . ( 2007;). The neutrophil-activating Dps protein of Helicobacter pylori, HP-NAP, adopts a mechanism different from Escherichia coli Dps to bind and condense DNA. Nucleic Acids Res 35: 2247–2256 [CrossRef] [PubMed].
    [Google Scholar]
  12. Chiancone E. , Ceci P. . ( 2010;). The multifaceted capacity of Dps proteins to combat bacterial stress conditions: Detoxification of iron and hydrogen peroxide and DNA binding. Biochim Biophys Acta 1800: 798–805 [CrossRef] [PubMed].
    [Google Scholar]
  13. Dundon W. G. , Nishioka H. , Polenghi A. , Papinutto E. , Zanotti G. , Montemurro P. , Del Giudice G. , Rappuoli R. , Montecucco C. . ( 2001;). The neutrophil-activating protein of Helicobacter pylori . Int J Med Microbiol 291: 545–550 [CrossRef] [PubMed].
    [Google Scholar]
  14. Franceschini S. , Ceci P. , Alaleona F. , Chiancone E. , Ilari A. . ( 2006;). Antioxidant Dps protein from the thermophilic cyanobacterium Thermosynechococcus elongatus . FEBS J 273: 4913–4928 [CrossRef] [PubMed].
    [Google Scholar]
  15. Ghisaidoobe A.B.T. , Chung S. J. . ( 2014;). Intrinsic tryptophan fluorescence in the detection and analysis of proteins: a focus on Förster resonance energy transfer techniques. Int J Mol Sci 15: 22518–22538 [CrossRef] [PubMed].
    [Google Scholar]
  16. Haikarainen T. , Papageorgiou A. C. . ( 2010;). Dps-like proteins: structural and functional insights into a versatile protein family. Cell Mol Life Sci 67: 341–351 [CrossRef] [PubMed].
    [Google Scholar]
  17. Haikarainen T. , Thanassoulas A. , Stavros P. , Nounesis G. , Haataja S. , Papageorgiou A. C. . ( 2011;). Structural and thermodynamic characterization of metal ion binding in Streptococcus suis Dpr. J Mol Biol 405: 448–460 [CrossRef] [PubMed].
    [Google Scholar]
  18. Havukainen H. , Haataja S. , Kauko A. , Pulliainen A. T. , Salminen A. , Haikarainen T. , Finne J. , Papageorgiou A. C. . ( 2008;). Structural basis of the zinc- and terbium-mediated inhibition of ferroxidase activity in Dps ferritin-like proteins. Protein Sci 17: 1513–1521 [CrossRef] [PubMed].
    [Google Scholar]
  19. Huergo L. F. , Noindorf L. , Gimenes C. , Lemgruber R.S.P. , Cordellini D. F. , Falarz L. J. , Cruz L. M. , Monteiro R. A. , Pedrosa F. O. , other authors . ( 2010;). Proteomic analysis of Herbaspirillum seropedicae reveals ammonium-induced AmtB-dependent membrane sequestration of PII proteins. FEMS Microbiol Lett 308: 40–47 [CrossRef] [PubMed].
    [Google Scholar]
  20. Huergo L. F. , Rahman H. , Ibrahimovic A. , Day C. J. , Korolik V. . ( 2013;). Campylobacter jejuni Dps protein binds DNA in the presence of iron or hydrogen peroxide. J Bacteriol 195: 1970–1978 [CrossRef] [PubMed].
    [Google Scholar]
  21. Ilari A. , Stefanini S. , Chiancone E. , Tsernoglou D. . ( 2000;). The dodecameric ferritin from Listeria innocua contains a novel intersubunit iron-binding site. Nat Struct Biol 7: 38–43 [CrossRef] [PubMed].
    [Google Scholar]
  22. Ilari A. , Ceci P. , Ferrari D. , Rossi G. L. , Chiancone E. . ( 2002;). Iron incorporation into Escherichia coli Dps gives rise to a ferritin-like microcrystalline core. J Biol Chem 277: 37619–37623 [CrossRef] [PubMed].
    [Google Scholar]
  23. Ilari A. , Latella M. C. , Ceci P. , Ribacchi F. , Su M. , Giangiacomo L. , Stefanini S. , Chasteen N. D. , Chiancone E. . ( 2005;). The unusual intersubunit ferroxidase center of Listeria innocua Dps is required for hydrogen peroxide detoxification but not for iron uptake. A study with site-specific mutants. Biochemistry 44: 5579–5587 [CrossRef] [PubMed].
    [Google Scholar]
  24. Ilbert M. , Bonnefoy V. . ( 2013;). Insight into the evolution of the iron oxidation pathways. Biochim Biophys Acta Biochem Biophys Acta 1827: 161–175.[CrossRef]
    [Google Scholar]
  25. Ishikawa T. , Mizunoe Y. , Kawabata S. , Takade A. , Harada M. , Wai S. N. , Yoshida S. . ( 2003;). The iron-binding protein Dps confers hydrogen peroxide stress resistance to Campylobacter jejuni . J Bacteriol 185: 1010–1017 [CrossRef] [PubMed].
    [Google Scholar]
  26. Jeong K. C. , Hung K. F. , Baumler D. J. , Byrd J. J. , Kaspar C. W. . ( 2008;). Acid stress damage of DNA is prevented by Dps binding in Escherichia coli O157 : H7. BMC Microbiol 8: 181 [CrossRef] [PubMed].
    [Google Scholar]
  27. Lawson D. M. , Treffry A. , Artymiuk P. J. , Harrison P. M. , Yewdall S. J. , Luzzago A. , Cesareni G. , Levi S. , Arosio P. . ( 1989;). Identification of the ferroxidase centre in ferritin. FEBS Lett 254: 207–210 [CrossRef] [PubMed].
    [Google Scholar]
  28. Lee J.-W. , Helmann J. D. . ( 2006;). The PerR transcription factor senses H2O2 by metal-catalysed histidine oxidation. Nature 440: 363–367 [CrossRef] [PubMed].
    [Google Scholar]
  29. Leong L. M. , Tan B. H. , Ho K. K. . ( 1992;). A specific stain for the detection of nonheme iron proteins in polyacrylamide gels. Anal Biochem 207: 317–320 [CrossRef] [PubMed].
    [Google Scholar]
  30. Litwin C. M. , Calderwood S. B. . ( 1993;). Role of iron in regulation of virulence genes. Clin Microbiol Rev 6: 137–149 [PubMed].
    [Google Scholar]
  31. Martinez A. , Kolter R. . ( 1997;). Protection of DNA during oxidative stress by the nonspecific DNA-binding protein Dps. J Bacteriol 179: 5188–5194 [PubMed].
    [Google Scholar]
  32. Moure V. R. , Razzera G. , Araújo L. M. , Oliveira M.A.S. , Gerhardt E.C.M. , Müller-Santos M. , Almeida F. , Pedrosa F. O. , Valente A. P. , other authors . ( 2012;). Heat stability of proteobacterial PII protein facilitate purification using a single chromatography step. Protein Expr Purif 81: 83–88 [CrossRef] [PubMed].
    [Google Scholar]
  33. Nair S. , Finkel S. E. . ( 2004;). Dps protects cells against multiple stresses during stationary phase. J Bacteriol 186: 4192–4198 [CrossRef] [PubMed].
    [Google Scholar]
  34. Niesen F. H. , Berglund H. , Vedadi M. . ( 2007;). The use of differential scanning fluorimetry to detect ligand interactions that promote protein stability. Nat Protoc 2: 2212–2221 [CrossRef] [PubMed].
    [Google Scholar]
  35. Nyati K. K. , Nyati R. . ( 2013;). Role of Campylobacter jejuni infection in the pathogenesis of Guillain-Barré syndrome: an update. BioMed Res Int 2013: 852195 [CrossRef] [PubMed].
    [Google Scholar]
  36. Pang B. , Hong W. , Kock N. D. , Swords W. E. . ( 2012;). Dps promotes survival of nontypeable Haemophilus influenzae in biofilm communities in vitro and resistance to clearance in vivo . Front Cell Infect Microbiol 2: 58 [CrossRef] [PubMed].
    [Google Scholar]
  37. Roy S. , Saraswathi R. , Gupta S. , Sekar K. , Chatterji D. , Vijayan M. . ( 2007;). Role of N and C-terminal tails in DNA binding and assembly in Dps: structural studies of Mycobacterium smegmatis Dps deletion mutants. J Mol Biol 370: 752–767 [CrossRef] [PubMed].
    [Google Scholar]
  38. Sanchuki H.B.S. , Valdameri G. , Moure V. R. , Oliveira M. A. , Pedrosa F. O. , Souza E. M. , Korolik V. , Huergo L. F. . ( 2015;). Purification of the Campylobacter jejuni Dps protein assisted by its high melting temperature. Protein Expr Purif 111: 105–110 [CrossRef] [PubMed].
    [Google Scholar]
  39. Su M. , Cavallo S. , Stefanini S. , Chiancone E. , Chasteen N. D. . ( 2005;). The so-called Listeria innocua ferritin is a Dps protein. Iron incorporation, detoxification, and DNA protection properties. Biochemistry 44: 5572–5578 [CrossRef] [PubMed].
    [Google Scholar]
  40. Theoret J. R. , Cooper K. K. , Glock R. D. , Joens L. A. . ( 2011;). Campylobacter jejuni Dps homolog has a role in intracellular survival and in the development of campylobacterosis in neonate piglets. Foodborne Pathog Dis 8: 1263–1268 [CrossRef] [PubMed].
    [Google Scholar]
  41. Touati D. . ( 2000;). Iron and oxidative stress in bacteria. Arch Biochem Biophys 373: 1–6 [CrossRef] [PubMed].
    [Google Scholar]
  42. Tsuruta O. , Yokoyama H. , Fujii S. . ( 2012;). A new crystal lattice structure of Helicobacter pylori neutrophil-activating protein (HP-NAP). Acta Crystallogr F Struct Biol Cryst Commun 68: 134–140 [CrossRef] [PubMed].
    [Google Scholar]
  43. Vivian J. T. , Callis P. R. . ( 2001;). Mechanisms of tryptophan fluorescence shifts in proteins. Biophys J 80: 2093–2109 [CrossRef] [PubMed].
    [Google Scholar]
  44. Wei X. , Mingjia H. , Xiufeng L. , Yang G. , Qingyu W. . ( 2007;). Identification and biochemical properties of Dps (starvation-induced DNA binding protein) from cyanobacterium Anabaena sp. PCC 7120. IUBMB Life 59: 675–681 [CrossRef] [PubMed].
    [Google Scholar]
  45. Yokoyama H. , Fujii S. . ( 2014;). Structures and metal-binding properties of Helicobacter pylori neutrophil-activating protein with a di-nuclear ferroxidase center. Biomolecules 4: 600–615 [CrossRef] [PubMed].
    [Google Scholar]
  46. Zhao G. , Ceci P. , Ilari A. , Giangiacomo L. , Laue T. M. , Chiancone E. , Chasteen N. D. . ( 2002;). Iron and hydrogen peroxide detoxification properties of DNA-binding protein from starved cells. A ferritin-like DNA-binding protein of Escherichia coli . J Biol Chem 277: 27689–27696 [CrossRef] [PubMed].
    [Google Scholar]
  47. Zheng H. , Chruszcz M. , Lasota P. , Lebioda L. , Minor W. . ( 2008;). Data mining of metal ion environments present in protein structures. J Inorg Biochem 102: 1765–1776 [CrossRef] [PubMed].
    [Google Scholar]
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