The multifaceted capacity of Dps proteins to combat bacterial stress conditions: Detoxification of iron and hydrogen peroxide and DNA binding

Biochimica et Biophysica Acta - General Subjects

Volumn 1800, Issue 8, 2010, Pages 798-805

  Chiancone, Emilia ^a   Ceci, Pierpaolo ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Dps (DNA binding proteins from starved cells) protein; Dps DNA interaction; Ferroxidase activity; Microbial survival; Protection under oxidative damage condition; Review

Indexed keywords

DNA; DPS PROTEIN; FERRITIN; HYDROGEN PEROXIDE; HYDROXYL RADICAL; IRON;

ANTIBIOTIC RESISTANCE; DETOXIFICATION; DNA BINDING; FENTON REACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; REVIEW;

ADAPTATION, BIOLOGICAL; AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; DNA, BACTERIAL; DNA-BINDING PROTEINS; HUMANS; HYDROGEN PEROXIDE; IRON; METABOLIC DETOXICATION, DRUG; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; SEQUENCE HOMOLOGY, AMINO ACID; STRESS, PHYSIOLOGICAL;

BACTERIA (MICROORGANISMS);

EID: 77953809155     PISSN: 03044165     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbagen.2010.01.013     Document Type: Review

References (57)

1. Almiron M., Link A.J., Deirdre F., Kolter R. A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli. Genes Dev. 1992, 6:2646-2654.
2. Martinez A., Kolter R. Protection of DNA during oxidative stress by the nonspecific DNA-binding protein Dps. J. Bacteriol. 1997, 179:5188-5194.
3. Wolf S.G., Frenkiel D., Arad T., Finkel S.E., Kolter R., Minsky A. DNA protection by stress-induced biocrystallization. Nature 1999, 400:83-85.
4. Frenkiel-Krispin D., Levin-Zaidman S., Shimoni E., Gg Wolf S., Wachtel E.J., Arad T., Finkel S.E., Kolter R., Minsky A. Regulated phase transitions of bacterial chromatin: a non-enzymatic pathway for generic DNA protection. EMBO J. 2001, 20:1184-1191.
5. Altuvia S., Almirón M., Huisman G., Kolter R., Storz G. The dps promoter is activated by OxyR during growth and by IHF and sigma S in stationary phase. Mol. Microbiol. 1994, 13:265-272.
6. Ilari A., Stefanini S., Chiancone E., Tsernoglou D. The dodecameric ferritin from Listeria innocua contains a novel intersubunit iron-binding site. Nat. Struct. Biol. 2000, 7:38-43.
7. Evans D.J., Evans D.G., Lampert H.C., Nakano H. Identification of four new prokaryotic bacterioferritins, from Helicobacter pylori, Anabaena variabilis, Bacillus subtilis and Treponema pallidum, by analysis of gene sequences. Gene 1995, 153:123-127.
8. Grant R.A., Filman D.J., Finkel S.E., Kolter R., Hogle J.M. The crystal structure of Dps, a ferritin homolog that binds and protects DNA. Nat. Struct. Biol. 1998, 5:294-303.
9. Romão C.V., Mitchell E.P., 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. 2006, 11:891-902.
10. Bellapadrona G., Stefanini S., Zamparelli C., Theil E.C., 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. 2009, 284:19101-19109.
11. Ramsay B., Wiedenheft B., Allen M., Gauss G.H., Lawrence C.M., Young M., Douglas T. Dps-like protein from the hyperthermophilic archaeon Pyrococcus furiosus. J. Inorg. Biochem. 2006, 100:1061-1068.
12. Gauss G.H., Benas P., Wiedenheft B., Young M., Douglas T., Lawrence C.M. Structure of the DPS-like protein from Sulfolobus solfataricus reveals a bacterioferritin-like dimetal binding site within a DPS-like dodecameric assembly. Biochemistry 2006, 45:10815-10827.
13. Lawson D.M., Treffry A., Artymiuk A.P.J., Harrison P.M., Yewdall S.J., Luzzago A., Cesareni G., Levi S., Arosio P. Identification of the ferroxidase centre in ferritin. FEBS Lett. 1989, 254:207-210.
14. Zanotti G., Papinutto E., Dundon W., Battistutta R., Seveso M., Giudice G., Rappuoli R., Montecucco C. Structure of the neutrophil-activating protein from Helicobacter pylori. J. Mol. Biol. 2002, 323:125-130.
15. Kim S.G., Bhattacharyya G., Grove A., Lee Y.H. Crystal structure of Dps-1, a functionally distinct Dps protein from Deinococcus radiodurans. J. Mol. Biol. 2006, 361:105-114.
16. Ceci P., Ilari A., Falvo E., Chiancone E. The Dps 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. 2003, 278:20319-20326.
17. Cuypers M.G., Mitchell E.P., Romão C.V., McSweeney S.M. The crystal structure of the Dps2 from Deinococcus radiodurans reveals an unusual pore profile with a non-specific metal binding site. J. Mol. Biol. 2007, 371:787-799.
18. Ren B., Tibbelin G., Kajino T., Asami O., Ladenstein R. The multi-layered structure of Dps with a novel di-nuclear ferroxidase center. J. Mol. Biol. 2003, 329:467-477.
19. Franceschini S., Ceci P., Alaleona F., Chiancone E., Ilari A. Antioxidant Dps protein from the thermophilic cyanobacterium Thermosynechococcus elongatus. FEBS J. 2006, 273:4913-4928.
20. Ilari A., Ceci P., Ferrari D., Rossi G.L., Chiancone E. Iron incorporation into Escherichia coli Dps gives rise to a ferritin-like microcrystalline core. J. Biol. Chem. 2002, 277:37619-37623.
21. Zhao G., Ceci P., Ilari A., Giangiacomo L., Laue T.M., Chiancone E., Chasteen N.D. 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. 2002, 277:27689-27696.
22. Ceci P., Cellai S., Falvo E., Rivetti C., Rossi G.L., Chiancone E. DNA condensation and self-aggregation of Escherichia coli Dps are coupled phenomena related to the properties of the N-terminus. Nucleic Acids Res. 2004, 32:5935-5944.
23. Stillman T.J., Upadhyay M., Norte V.A., Sedelnikova S.E., Carradus M., Tzokov S., Bullough P.A., Shearman C.A., Gasson M.J., Williams C.H., Artymiuk P.J., Green J. The crystal structures of Lactococcus lactis MG1363 Dps proteins reveal the presence of an N-terminal helix that is required for DNA binding. Mol. Microbiol. 2005, 57:1101-1112.
24. E. Chiancone, P. Ceci, Dps (DNA-binding proteins from starved cells) proteins. The aggregation on DNA and its role in microbial survival, Front Biosci 15 (2010) 122-131.
25. Roy S., Saraswathi R., Chatterji D., Vijayan M. Structural studies on the second Mycobacterium smegmatis Dps: invariant and variable features of structure, assembly and function. J. Mol. Biol. 2008, 375:948-959.
26. Grove A., Wilkinson S.P. Differential DNA binding and protection by dimeric and dodecameric forms of the ferritin homolog Dps from Deinococcus radiodurans. J. Mol. Biol. 2005, 347:495-508.
27. Bhattacharyya G., Grove A. The N-terminal extensions of Deinococcus radiodurans Dps-1 mediate DNA major groove interactions as well as assembly of the dodecamer. J. Biol. Chem. 2007, 282:11921-11930.
28. Gupta S., Chatterji D. Bimodal protection of DNA by Mycobacterium smegmatis DNA-binding protein from stationary phase cells. J. Biol. Chem. 2003, 278:5235-5241.
29. Roy S., Saraswathi R., Gupta S., Sekar K., Chatterji D., Vijayan M. 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. 2007, 370:752-767.
30. Ceci P., Ilari A., Falvo E., Giangiacomo L., Chiancone E. Reassessment of protein stability, DNA binding, and protection of Mycobacterium smegmatis Dps. J. Biol. Chem. 2005, 280:34776-34785.
31. Ceci P., Mangiarotti L., Rivetti C., Chiancone E. 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. 2007, 35:2247-2256.
32. Castruita M., Saito M., Schottel P.C., Elmegreen L.A., Myneni S., Stiefel E.I., Morel F.M. Overexpression and characterization of an iron storage and DNA-binding Dps protein from Trichodesmium erythraeum. Appl. Environ. Microbiol. 2006, 72:2918-2924.
33. Bozzi M., Mignogna G., Stefanini S., Barra D., Longhi C., Valenti P., Chiancone E. A novel non-heme iron-binding ferritin related to the DNA-binding proteins of the Dps family in Listeria innocua. J. Biol. Chem. 1997, 272:3259-3265.
34. Papinutto E., Dundon W.G., Pitulis N., Battistutta R., Montecucco C., Zanotti G. Structure of two iron-binding proteins from Bacillus anthracis. J. Biol. Chem. 2002, 277:15093-15098.
35. Ishikawa T., Mizunoe Y., Kawabata S., Takade A., Harada M., Wai S.N., Yoshida S. The iron-binding protein Dps confers hydrogen peroxide stress resistance to Campylobacter jejuni. J. Bacteriol. 2003, 185:1010-1017.
36. Zhao G., Bou-Abdallah F., Arosio P., Levi S., Janus-Chandler C., Chasteen N.D. Multiple pathways for mineral core formation in mammalian apoferritin. The role of hydrogen peroxide. Biochemistry 2003, 42:3142-3150.
37. 2 as oxidants. Biophys. Chem. 2005, 114:235-244.
38. Tonello F., Dundon W.G., Satin B., Molinari M., Tognon G., Grandi G., Del Giudice G., Rappuoli R., Montecucco C. The Helicobacter pylori neutrophil-activating protein is an iron-binding protein with dodecameric structure. Mol. Microbiol. 1999, 34:238-246.
39. Su M., Cavallo S., Stefanini S., Chiancone E., Chasteen N.D. The so-called Listeria innocua ferritin is a Dps protein, iron incorporation, detoxification, and DNA protection properties. Biochemistry 2005, 44:5572-5578.
40. Ilari A., Latella M.C., Ceci P., Ribacchi F., Su M., Giangiacomo L., Stefanini S., Chasteen N.D., Chiancone E. 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 2005, 44:5579-5587.
41. Halsey T.A., Vazquez-Torres A., Gravdahl D.J., Fang F.C., Libby S.J. The ferritin-like Dps protein is required for Salmonella enterica serovar Typhimurium oxidative stress resistance and virulence. Infect. Immun. 2004, 72:1155-1158.
42. Ueshima J., Shoji M., Ratnayake D.B., Abe K., Yoshida S., Yamamoto K., Nakayama K. Purification, gene cloning, gene expression, and mutants of Dps from the obligate anaerobe Porphyromonas gingivalis. Infect. Immun. 2003, 71:1170-1178.
43. Diaz P.I., Slakeski N., Reynolds E.C., Morona R., Rogers A.H., Kolenbrander P.E. Role of oxyR in the oral anaerobe Porphyromonas gingivalis. J. Bacteriol. 2006, 188:2454-2462.
44. Yamamoto Y., Higuchi M., Poole L.B., Kamio Y. Role of the dpr product in oxygen tolerance in Streptococcus mutans. J. Bacteriol. 2000, 182:3740-3747.
45. Higuchi M., Yamamoto Y., Kamio Y. Molecular biology of oxygen tolerance in lactic acid bacteria: functions of NADH oxidases and Dpr in oxidative stress. J. Biosci. Bioeng. 2000, 90:484-493.
46. Yang X., Chiancone E., Stefanini S., Ilari A., Chasteen N.D. Iron oxidation and hydrolysis reactions of a novel ferritin from Listeria innocua. Biochem. J. 2000, 349:783-786.
47. Pulliainen A.T., Kauko A., Haataja S., Papageorgiou A.C., Finne J. Dps/Dpr ferritin-like protein: insight into the mechanism of iron incorporation and evidences for a central role in cellular iron homeostasis in Streptococcus suis. Mol. Microbiol. 2005, 57:1086-1100.
48. Kauko A., Pulliainen A.T., Haataja S., Meyer-Klaucke W., Finne J., Papageorgiou A.C. Iron incorporation in Streptococcus suis Dps-like peroxide resistance protein Dpr requires mobility in the ferroxidase center and leads to formation of a ferrihydrite-like core. J. Mol. Biol. 2006, 364:97-109.
49. Liu X., Kim K., Leighton T., Theil E.C. Paired Bacillus anthracis Dps (mini-ferritin) have different reactivities with peroxide. J. Biol. Chem. 2006, 281:27827-27835.
50. Aubert C., Vos M.H., Mathis P., Eker A.P., Brettel K. Intraprotein radical transfer during photoactivation of DNA photolyase. Nature 2000, 405:586-590.
51. Fontecave M. Ribonucleotide reductase and radical reactions. Cell. Mol. Life Sci. 1998, 54:684-695.
52. Bellapadrona G., Ardini M., Ceci P., Stefanini S., Chiancone E. Dps proteins prevent Fenton mediated oxidative damage by trapping hydroxyl radicals within the protein shell. Free Radic. Biol. Med. 2010, 292-297.
53. Nair S., Finkel S.E. Dps protects cells against multiple stresses during stationary phase. J. Bacteriol. 2004, 186:4192-4198.
54. Ohniwa R.L., Morikawa K., Kim J., Ohta T., Ishihama A., Wada C., Takeyasu K. Dynamic state of DNA topology is essential for genome condensation in bacteria. EMBO J. 2006, 25:5591-5602.
55. Grainger D.C., Goldberg M.D., Lee D.J., Busby S.J. Selective repression by Fis and H-NS at the Escherichia coli dps promoter. Mol. Microbiol. 2008, 68:1366-1377.
56. Chodavarapu S., Gomez R., Vicente M., Kaguni J.M. Escherichia coli Dps interacts with DnaA protein to impede initiation: a model of adaptive mutation. Mol. Microbiol. 2008, 67:1331-1346.
57. Facey P.D., Hitchings M.D., Saavedra-Garcia P., Fernandez-Martinez L., Dyson P.J., Del Sol R. Streptomyces coelicolor Dps-like proteins: differential dual roles in response to stress during vegetative growth and in nucleoid condensation during reproductive cell division. Mol. Microbiol. 2009, 73:1186-1202.