Campylobacter jejuni Dps protein binds DNA in the presence of iron or hydrogen peroxide

Journal of Bacteriology

Volumn 195, Issue 9, 2013, Pages 1970-1978

  Huergo, Luciano F ^a,b   Rahman, Hossinur ^a   Ibrahimovic, Adis ^a   Day, Christopher J ^a   Korolik, Victoria ^a  

^a GRIFFITH UNIVERSITY   (Australia)

^b FEDERAL UNIVERSITY OF PARANÁ   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; CYSTEINE; DPS PROTEIN; HYDROGEN PEROXIDE; HYDROXYL RADICAL; IRON; SERINE;

ARTICLE; BACTERIAL COLONIZATION; CAMPYLOBACTER JEJUNI; CONTROLLED STUDY; ENZYME DENATURATION; GENOTYPE; IN VITRO STUDY; IN VIVO STUDY; MUTANT; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DNA BINDING; PROTEIN DNA INTERACTION; PROTEIN EXPRESSION; PROTEIN PURIFICATION; SITE DIRECTED MUTAGENESIS;

BACTERIAL PROTEINS; CAMPYLOBACTER JEJUNI; CYTOCHROME B GROUP; DNA, BACTERIAL; DNA-BINDING PROTEINS; FERRITINS; HYDROGEN PEROXIDE; IRON; PROTEIN BINDING;

CAMPYLOBACTER JEJUNI;

EID: 84876191281     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00059-13     Document Type: Article

References (51)

1. Blaser MJ. 1997. Epidemiologic and clinical features of Campylobacter jejuni infections. J. Infect. Dis. 176:S103-S105.
2. Allos BM. 1997. Association between Campylobacter infection and Guillain- Barre syndrome. J. Infect. Dis. 176:S125-S128.
3. Israeli E, Agmon-Levin N, Blank M, Chapman J, Shoenfeld Y. 2012. Guillain-Barre syndrome, a classical autoimmune disease triggered by infection or vaccination. Clin. Rev. Allergy Immunol. 42:121-130.
4. Zeth K. 2012. Dps biomineralizing proteins: multifunctional architects of nature. Biochem. J. 445:297-311.
5. Carrondo MA. 2003. Ferritins, iron uptake and storage from the bacterioferritin viewpoint. EMBO J. 22:1959 -1968.
6. Bou-Abdallah F. 2010. The iron redox and hydrolysis chemistry of the ferritins. Biochim. Biophys. Acta 1800:719 -731.
7. Almiron MA, Link 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.
8. Roy S, Saraswathi R, Chatterji D, Vijayan M. 2008. Structural studies on the second Mycobacterium smegmatis Dps: invariant and variable features of structure, assembly and function. J. Mol. Biol. 375:948 -959.
9. 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.
10. 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.
11. 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.
12. Martinez A, Kolter R. 1997. Protection of DNA during oxidative stress by the nonspecific DNA-binding protein Dps. J. Bacteriol. 179:5188 -5194.
13. Ceci P, Ilari A, Falvo E, Chiancone E. 2003. The Dps protein of Agrobacterium tumefaciens does not bind to DNA but protects it toward oxidative cleavage: X-ray crystal structure, iron binding, and hydroxylradical scavenging properties. J. Biol. Chem. 278:20319 -20326.
14. Tu WY, Pohl S, Gizynski K, Harwood CR. 2012. The iron-binding protein Dps2 confers peroxide stress resistance on Bacillus anthracis. J. Bacteriol. 194:925-931.
15. Nair S, Finkel SE. 2004. Dps protects cells against multiple stresses during stationary phase. J. Bacteriol. 186:4192- 4198.
16. Wang G, Hong Y, Olczak A, Maier SE, Maier RJ. 2006. Dual roles of Helicobacter pylori NapA in inducing and combating oxidative stress. Infect. Immun. 74:6839-6846.
17. Ishikawa T, Mizunoe Y, Kawabata S, Takade A, Harada M, Wai SN, Yoshida S. 2003. The iron-binding protein Dps confers hydrogen peroxide stress resistance to Campylobacter jejuni. J. Bacteriol. 185:1010 -1017.
18. Cooksley C, Jenks PJ, Green A, Cockayne A, Logan RP, Hardie KR. 2003. NapA protects Helicobacter pylori from oxidative stress damage, and its production is influenced by the ferric uptake regulator. J. Med. Microbiol. 52:461- 469.
19. Olczak AA, Wang G, Maier RJ. 2005. Up-expression of NapA and other oxidative stress proteins is a compensatory response to loss of major Helicobacter pylori stress resistance factors. Free Radic. Res. 39:1173-1182.
20. Jeong KC, Hung KF, Baumler DJ, Byrd JJ, Kaspar CW. 2008. Acid stress damage of DNA is prevented by Dps binding in Escherichia coli O157:H7. BMC Microbiol. 8:181. doi:10.1186/1471-2180-8-181.
21. Pang B, Hong W, Kock ND, Swords WE. 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. doi:10 .3389/fcimb.2012.00058.
22. Ceci P, Mangiarotti L, Rivetti C, Chiancone E. 2007. The neutrophilactivating 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.
23. 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.
24. 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.
25. 2 as a co-substrate for iron oxidation and reveals DPS-like DNA protection and binding activities. Biochem. J. 446:125-133.
26. 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 DNAbinding protein of Escherichia coli. J. Biol. Chem. 277:27689 -27696.
27. Wolf SG, Frenkiel D, Arad T, Finkel SE, Kolter R, Minsky A. 1999. DNA protection by stress-induced biocrystallization. Nature 400:83- 85.
28. Castruita M, Saito M, Schottel PC, Elmegreen LA, Myneni S, Stiefel EI, Morel FM. 2006. Overexpression and characterization of an iron storage and DNA-binding Dps protein from Trichodesmium erythraeum. Appl. Environ. Microbiol. 72:2918 -2924.
29. Stillman TJ, Upadhyay M, Norte VA, Sedelnikova SE, Carradus M, Tzokov S, Bullough PA, Shearman CA, Gasson MJ, Williams CH, Artymiuk PJ, Green J. 2005. 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. 57:1101-1112.
30. 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.
31. Bhattacharyya G, Grove A. 2007. The N-terminal extensions of Deinococcus radiodurans Dps-1 mediate DNA major groove interactions as well as assembly of the dodecamer. J. Biol. Chem. 282:11921-11930.
32. Nguyen KH, Grove A. 2012. Metal binding at the Deinococcus radiodurans Dps-1 N-terminal metal site controls dodecameric assembly and DNA binding. Biochemistry 51:6679-6689.
33. Zanotti G, Papinutto E, Dundon W, Battistutta R, Seveso M, Giudice G, Rappuoli R, Montecucco C. 2002. Structure of the neutrophil-activating protein from Helicobacter pylori. J. Mol. Biol. 323:125-130.
34. Theoret JR, Cooper KK, Glock RD, Joens LA. 2011. A 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.
35. Theoret JR, Cooper KK, Zekarias B, Roland KL, Law BF, Curtiss R, Joens LA. 2012. The Campylobacter jejuni Dps homologue is important for in vitro biofilm formation and cecal colonization of poultry and may serve as a protective antigen for vaccination. Clin. Vaccine Immunol. 19: 1426-1431.
36. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning. a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
37. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
38. Bradford MM. 1976. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248 -254.
39. Shacter E. 2000. Quantification and significance of protein oxidation in biological samples. Drug Metab. Rev. 32:307-326.
40. Rhee SG, Bae YS, Lee SR, Kwon J. 2000. Hydrogen peroxide: a key messenger that modulates protein phosphorylation through cysteine oxidation. Sci. STKE 2000:e1. doi:10.1126/stke.2000.53.pe1.
41. 2 sensors as archetypical redox signaling modules. Trends Biochem. Sci. 29:351-357.
42. Zheng M, Aslund F, Storz G. 1998. Activation of the OxyR transcription factor by reversible disulfide bond formation. Science 279:1718 -1721.
43. Choi H, Kim S, Mukhopadhyay P, Cho S, Woo J, Storz G, Ryu SE. 2001. Structural basis of the redox switch in the OxyR transcription factor. Cell 105:103-113.
44. Netto LE, Stadtman ER. 1996. The iron-catalyzed oxidation of dithiothreitol is a biphasic process: hydrogen peroxide is involved in the initiation of a free radical chain of reactions. Arch. Biochem. Biophys. 333:233- 242.
45. Grove A, Wilkinson SP. 2005. Differential DNA binding and protection by dimeric and dodecameric forms of the ferritin homolog Dps from Deinococcus radiodurans. J. Mol. Biol. 347:495-508.
46. Altuvia S, Almiron 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.
47. Nguyen KH, Smith LT, Xiao L, Bhattacharyya G, Grove A. 2012. On the stoichiometry of Deinococcus radiodurans Dps-1 binding to duplex DNA. Proteins 80:713-721.
48. Birk TT, Wik MT, Lametsch R, Knochel S. 2012. Acid stress response and protein induction in Campylobacter jejuni isolates with different acid tolerance. BMC Microbiol. 12:174. doi:10.1186/1471-2180-12-174.
49. Guazzaroni ME, Morgante V, Mirete S, González-Pastor JE. 15 October 2012. Novel acid resistance genes from the metagenome of the Tinto River, an extremely acidic environment. Environ. Microbiol. [Epub ahead of print.] doi:10.1111/1462-2920.12021.
50. Halsey TA, Vazquez-Torres A, Gravdahl DJ, Fang FC, Libby SJ. 2004. The ferritin-like Dps protein is required for Salmonella enterica serovar Typhimurium oxidative stress resistance and virulence. Infect. Immun. 72:1155-1158.
51. Skirrow MB. 1977. Campylobacter enteritis: a "new" disease. Br. Med. J. 2:9-11.