The two Dps of Edwardsiella tarda are involved in resistance against oxidative stress and host infection

Fish and Shellfish Immunology

Volumn 31, Issue 6, 2011, Pages 985-992

  Zheng, Wen jiang ^a,b   Hu, Yong hua ^a   Sun, Li ^a  

^a INSTITUTE OF OCEANOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

Dps; Edwardsiella tarda; Ferritin; Oxidative stress; Virulence

Indexed keywords

BACTERIA (MICROORGANISMS); EDWARDSIELLA TARDA;

EID: 81255142612     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2011.08.018     Document Type: Article

References (51)

1. Almirón M., Link A.J., Furlong D., Kolter R. A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli. Genes Dev 1992, 6:2646-2654.
2. 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.
3. Kauko A., Haataja S., Pulliainen A.T., Finne J. Papageorgiou AC. Crystal structure of Streptococcus suis Dps-like peroxide resistance protein Dpr: implications for iron incorporation. J Mol Biol 2004, 338:547-558.
4. 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.
5. 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.
6. Zeth K., Offermann S., Essen L.O., 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 2004, 101:13780-13785.
7. 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.
8. Calhoun L.N., Kwon Y.M. Structure, function and regulation of the DNA-binding protein Dps and its role in acid and oxidative stress resistance in Escherichia coli: a review. J Appl Microbiol 2011, 110:375-386.
9. Haikarainen T., Papageorgiou A.C. Dps-like proteins: structural and functional insights into a versatile protein family. Cell Mol Life Sci 2010, 67:341-351.
10. Zhao G., Ceci P., Ilari A., Giangiacomo L., Laue T.M., Chiancone E., et al. Iron and hydrogen peroxide detoxification properties of DNA-binding protein from starved cells. J Biol Chem 2002, 277:27689-27696.
11. 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.
12. Chen L., Helmann J.D. Bacillus subtilis MrgA is a Dps (PexB) homologue: evidence for metalloregulation of an oxidative-stress gene. Mol Microbiol 1995, 18:295-300.
13. 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.
14. 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.
15. Dundon W.G., Nishioka H., Polenghi A., Papinutto E., Zanotti G., Montemurro P., et al. The neutrophil-activating protein of Helicobacter pylori. Int J Med Microbiol 2001, 291:545-550.
16. 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.
17. Bozzi M., Mignogna G., Stefanini S., Barra D., Longhi C., Valenti P., et al. 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.
18. 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. J Biol Chem 2003, 278:20319-20326.
19. 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.
20. 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.
21. Yamamoto Y., Poole L.B., Hantgan R.R., Kamio Y. An iron-binding protein, Dpr, from Streptococcus mutans prevents iron-dependent hydroxyl radical formation in vitro. J Bacteriol 2002, 184:2931-2939.
22. Thieme D., Grass G. The Dps protein of Escherichia coli is involved in copper homeostasis. Microbiol Res 2010, 165:108-115.
23. Chiancone E., 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 2010, 1800:798-805.
24. Hébraud M., Guzzo J. The main cold shock protein of Listeria monocytogenes belongs to the family of ferritin-like proteins. FEMS Microbial Lett 2000, 190:29-34.
25. Nair S., Finkel S.E. Dps protects cells against multiple stresses during stationary phase. J Bacteriol 2004, 186:4192-4198.
26. Nicodeme M., Perrin C., Hols P., Bracquart P., Gaillard J.L. Identification of an iron-binding protein of the Dps family expressed by Streptococcus thermophilus. Curr Microbiol 2004, 48:51-56.
27. Ingmer H. Dps and bacterial Chromatin. Bacterial chromatin 2010, 175-201. Springer Press, Dordrecht, The Netherlands. R.T. Dame, C.J. Dorman (Eds.).
28. Nelson J., Nelson C., Carter J. Extraintestinal manifestations of Edwardsiella tarda infection: a 10-year retrospective review. J La State Med Soc 2009, 161:103-106.
29. Sun K., Wang H., Zhang M., Xiao Z., Sun L. Genetic mechanisms of multi-antimicrobial resistance in a pathogenic Edwardsiella tarda strain. Aquaculture 2009, 289:134-139.
30. Sambrook J., Fritsch E.F., Maniatis T. Molecular cloning: a laboratory manual 1989, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y. 2nd ed.
31. Zhang W.W., Sun L. Cloning, characterization and molecular application of a beta-agarase gene from Vibrio sp. strain V134. Appl Environ Microbiol 2007, 73:2825-2831.
32. Hu Y.H., Zheng W.J., Sun L. Identification and molecular analysis of a ferritin subunit from red drum (Sciaenops ocellatus). Fish Shellfish Immunol 2010, 28:678-686.
33. Milton D.L., O'Toole R., Hörstedt P., Wolf-Watz H. Flagellin A is essential for the virulence of Vibrio anguillarum. J Bacteriol 1996, 178:1310-1319.
34. Vh, a serine protease and a protective immunogen from a pathogenic Vibrio harveyi strain. Appl Environ Microbiol 2008, 74:6254-6262.
35. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254.
36. Zhang M., Jiao X., Hu Y., Sun L. Attenuation of Edwardsiella tarda virulence by small peptides that interfere with LuxS/autoinducer type 2 quorum sensing. Appl Environ Microbiol 2009, 75:3882-3890.
37. Liu C.S., Sun Y., Hu Y.H., Sun L. Identification and analysis of the immune effects of CpG motifs that protect Japanese flounder (Paralichthys olivaceus) against bacterial infection. Fish Shellfish Immunol 2010, 29:279-285.
38. Srinivasa Rao P.S., Lim T.M., Leung K.Y. Opsonized virulent Edwardsiella tarda strains are able to adhere to and survive and replicate within fish phagocytes but fail to stimulate reactive oxygen intermediates. Infect Immun 2001, 69:5689-5697.
39. Ali Azam T., Iwata A., Nishimura A., Ueda S., Ishihama A. Growth phase-dependent variation in protein composition of the Escherichia coli Nucleoid. J Bacteriol 1999, 181:6361-6370.
40. Cooksley C., Jenks P.J., Green A., Cockayne A., Logan R.P., Hardie K.R. NapA protects Helicobacter pylori from oxidative stress damage, and its production is influenced by the ferric uptake regulator. J Med Microbiol 2003, 52:461-469.
41. Polidoro M., de Biase D., Montagnini B., Guarrera L., Cavallo S., Valenti P., et al. The expression of the dodecameric ferritin in Listeria spp. is induced by iron limitation and stationary growth phase. Gene 2002, 296:121-128.
42. Mohamed W., Darji A., Domann E., Chiancone E., Chakraborty T. The ferritin-like protein Frm is a target for the humoral immune response to Listeria monocytogenes and is required for efficient bacterial survival. Mol Genet Genomics 2006, 275:344-353.
43. 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.
44. Colburn-Clifford J.M., Scherf J.M., Allen C. Ralstonia solanacearum Dps contributes to oxidative stress tolerance and to colonization of and virulence on tomato plants. Appl Environ Microbiol 2010, 76:7392-7399.
45. Dussurget O., Dumas E., Archambaud C., Chafsey I., Chambon C., Hébraud M., et al. Listeria monocytogenes ferritin protects against multiple stresses and is required for virulence. FEMS Microbial Lett 2005, 250:253-261.
46. Ishikawa T., Mizunoe Y., Kawabata S., Takade A., Harada M., Wai S.N., et al. The iron-binding protein Dps confers hydrogen peroxide stress resistance to Campylobacter jejuni. J Bacteriol 2003, 185:1010-1017.
47. 2 resistance mediated by Streptococcal Dpr. J Biol Chem 2003, 278:7996-8005.
48. Ueshima J., Shoji M., Ratnayake D.B., Abe K., Yoshida S., Yamamoto K., et al. Purification, gene cloning, gene expression, and mutants of Dps from the obligate anaerobe Porphyromonas gingivalis. Infect Immun 2003, 71:1170-1178.
49. Velayudhan J., Castor M., Richardson A., Main-Hestor K.L., Fang F.C. The role of ferritins in the physiology of Salmonella enterica sv. typhimurium: a unique role for ferritin B in iron-sulphur cluster repair and virulence. Mol Microbiol 2007, 63:1495-1507.
50. Olsen K.N., Larsen M.H., Gahan C.G., Kallipolitis B., Wolf X.A., Rea R., et al. The Dps-like protein Fri of Listeria monocytogenes promotes stress tolerance and intracellular multiplication in macrophage-like cells. Microbiology 2005, 151:925-933.
51. Mohamed W., Sethi S., Darji A., Mraheil M.A., Hain T., Chakraborty T. Antibody targeting the ferritin-like protein controls Listeria infection. Infect Immun 2010, 78:3306-3314.