Abstract
The proteins belonging to the Dps (DNA-binding proteins from starved cells) family play an important role within the bacterial defence system against oxidative stress. They act on Fe(II) and hydrogen peroxide that are potentially toxic in the presence of air. Fe(II) forms spontaneously insoluble Fe(III) and reacts with molecular oxygen or its reduced forms to yield the highly damaging hydroxyl radicals. All Dps proteins have the distinctive capacity to annul the toxic combination of iron and hydrogen peroxide as they use the latter compound to oxidise Fe(II). In addition to this intrinsic DNA protection capacity, several members of the family, including the archetypical Escherichia coli Dps, protect DNA physically by shielding it in large Dps-DNA complexes. The structural and functional characteristics that endow Dps proteins with the chemical and physical protection mechanism are presented and discussed also in the framework of the varied situations that may be encountered in different bacterial species.
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Almirón M, Link AJ, Furlong D, Kolter R (1992) A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli. Genes Dev 6: 2646–2554
Altuvia S, Almirón M, Huisman G, Kolter R, Storz G (1994) The dps promoter is activated by OxyR during growth and by IHF and sigma S in stationary phase. Mol Microbiol 13: 265–272
Martinez A, Kolter R (1997) Protection of DNA during oxidative stress by the nonspecific DNA-binding protein Dps. J Bacteriol 179: 5188–5194
Wolf SG, Frenkiel D, Arad T, Finkel SE, Kolter R, Minsky A (1999) DNA protection by stress-induced biocrystallization. Nature 400: 83–85
Frenkiel-Krispin D, Levin-Zaidman S, Shimoni E, Wolf SG, Wachtel EJ, Arad T, Finkel SE, Kolter R, Minsky A (2001) Regulated phase transitions of bacterial chromatin: a nonenzymatic pathway for generic DNA protection. EMBO J 20: 1184–1191
Lewin A, Moore GR, Le Brun NE (2005) Formation of protein-coated iron minerals. Dalton Trans 22: 3597–3610
Hoare RJ, Harrison PM, Hoy TG (1975) Structure of horse-spleen apoferritin at 6 Angstrom resolution. Nature 255: 653–654
Stillman TJ, Hempstead PD, Artymiuk PJ, Andrews SC, Hudson AJ, Treffry A, Guest JR, Harrison PM (2001) The high-resolution X-ray crystallographic structure of the ferritin (EcFtnA) of Escherichia coli; comparison with human H ferritin (HuHF) and the structures of the Fe(3+) and Zn(2+) derivatives. J Mol Biol 307: 587–603
Stefanini S, Desideri A, Vecchini P, Drakenberg T, Chiancone E (1989) Identification of the iron entry channels in apoferritin. Chemical modification and spectroscopic studies. Biochemistry 28: 378–382
Douglas T, Ripoll DR (1998) Calculated electrostatic gradients in recombinant human H-chain ferritin. Protein Sci 7: 1083–1091
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
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
Papinutto E, Dundon WG, Pitulis N, Battistutta R, Montecucco C, Zanotti G (2002) Structure of two iron-binding proteins from Bacillus anthracis. J Biol Chem 277: 15093–15098
Zeth K, Offermann S, Essen LO, Oesterhelt D (2004) 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: 13780–13785
Kim SG, Bhattacharyya G, Grove A, Lee YH (2006) Crystal structure of Dps-1, a functionally distinct Dps protein from Deinococcus radiodurans. J Mol Biol 361: 105–14
Romão CV, Mitchell EP, McSweeney S (2006) 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: 891–902
Cuypers MG, Mitchell EP, Romão CV, McSweeney SM (2007) The crystal structure of the Dps2 from Deinococcus radiodurans reveals an unusual pore profile with a non-specific metal binding site. J Mol Biol 371: 787–799
Kauko A, Haataja S, Pulliainen AT, Finne J, Papageorgiou AC (2004) Crystal structure of Streptococcus suis Dps-like peroxide resistance protein Dpr: implications for iron incorporation. J Mol Biol 338: 547–558
Ren B, Tibbelin G, Kajino T, Asami O, Ladenstein R (2003) The multi-layered structure of Dps with a novel di-nuclear ferroxidase center. J Mol Biol 329: 467–477
Zhao G, Ceci P, Ilari A, Giangiacomo L, Laue TM, Chiancone E, Chasteen ND (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
Su M, Cavallo S, Stefanini S, Chiancone E, Chasteen ND (2005) The so-called Listeria innocua ferritin is a Dps protein. Iron incorporation, detoxification, and DNA protection properties. Biochemistry 44: 5572–5578
Liu X, Kim K, Leighton T, Theil EC (2006) Paired Bacillus anthracis Dps (miniferritin) have different reactivities with peroxide. J Biol Chem 281: 27827–27835
Ilari A, Ceci P, Ferrari D, Rossi GL, Chiancone E (2002) Iron incorporation into Escherichia coli Dps gives rise to a ferritin-like microcrystalline core. J Biol Chem 277: 37619–37623
Yamamoto Y, Poole LB, Hantgan RR, Kamio Y (2002) An iron-binding protein, Dpr, from Streptococcusmutans prevents iron-dependent hydroxyl radical formation in vitro. J Bacteriol 184: 2931–2939
Ilari A, Latella MC, Ceci P, Ribacchi F, Su M, Giangiacomo L, Stefanini S, Chasteen ND, 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: 5579–87
Grant RA, Filman DJ, Finkel SE, Kolter R, Hogle JM (1998) The crystal structure of Dps, a ferritin homolog that binds and protects DNA. Nat Struct Biol 5: 294–303
Ceci P, Cellai S, Falvo E, Rivetti C, Rossi GL, 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
Ceci P, Ilari A, Falvo E, Chiancone E (2003) TheDps protein of Agrobacterium tumefaciens does not bind to DNA but protects it toward oxidative cleavage: X-ray crystal structure, iron binding, and hydroxyl-radical scavenging properties. J Biol Chem 278: 20319–20326
Gupta S, Chatterji D. Bimodal protection of DNA by Mycobacterium smegmatis DNA-binding protein from stationary phase cells. J Biol Chem 278: 5235–5241 (2003)
Ceci P, Ilari A, Falvo E, Giangiacomo L, Chiancone E (2005) Reassessment of protein stability, DNA binding, and protection of Mycobacterium smegmatis Dps. J Biol Chem 280: 34776–34785
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Chiancone, E. Dps proteins, an efficient detoxification and DNA protection machinery in the bacterial response to oxidative stress. Rend. Fis. Acc. Lincei 19, 261–270 (2008). https://doi.org/10.1007/s12210-008-0018-4
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DOI: https://doi.org/10.1007/s12210-008-0018-4