Distinct characteristics of OxyR2, a new OxyR-type regulator, ensuring expression of Peroxiredoxin 2 detoxifying low levels of hydrogen peroxide in Vibrio vulnificus

Molecular Microbiology

Volumn 93, Issue 5, 2014, Pages 992-1009

  Kim, Suyeon ^a   Bang, Ye Ji ^a   Kim, Dukyun ^a   Lim, Jong Gyu ^a   Oh, Man Hwan ^b   Choi, Sang Ho ^a  

^a Seoul National University   (South Korea)

^b Dankook University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; HYDROGEN PEROXIDE; PEROXIREDOXIN 2; PROTEIN OXYR2; UNCLASSIFIED DRUG; PEROXIREDOXIN; REPRESSOR PROTEIN;

ALKYLATION; AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; DISULFIDE BOND; GEL MOBILITY SHIFT ASSAY; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; OXIDATION; PLASMID; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MULTIMERIZATION; RNA PURIFICATION; RNA TRANSCRIPTION; SEQUENCE HOMOLOGY; SITE DIRECTED MUTAGENESIS; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION; VIBRIO VULNIFICUS; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; PROMOTER REGION; SEQUENCE ALIGNMENT;

ESCHERICHIA; VIBRIO VULNIFICUS;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BINDING SITES; GENE EXPRESSION REGULATION, BACTERIAL; HYDROGEN PEROXIDE; MOLECULAR SEQUENCE DATA; PEROXIREDOXINS; PROMOTER REGIONS, GENETIC; REPRESSOR PROTEINS; SEQUENCE ALIGNMENT; VIBRIO VULNIFICUS;

EID: 84906937468     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12712     Document Type: Article

References (40)

1. Åslund, F., Beckwith, M., Zheng, J., and Storz, G. (1999) Regulation of the OxyR transcription factor by hydrogen peroxide and the cellular thiol - disulfide status. Proc Natl Acad Sci USA 96: 6161-61665.
2. Baek, W.K., Lee, H.S., Oh, M.H., Koh, M.J., Kim, K.S., and Choi, S.H. (2009) Identification of the Vibrio vulnificus ahpCl gene and its influence on survival under oxidative stress and virulence. J Microbiol 47: 624-632.
3. Bang, Y.J., Oh, M.H., and Choi, S.H. (2012) Distinct characteristics of two 2-Cys peroxiredoxins of Vibrio vulnificus suggesting differential roles in detoxifying oxidative stress. J Biol Chem 287: 42516-42524.
4. Bsat, N., Chen, L., and Helmann, J.D. (1996) Mutation of the Bacillus subtilis alkyl hydroperoxide reductase (ahpCF) operon reveals compensatory interactions among hydrogen peroxide stress genes. J Bacteriol 178: 6579-6586.
5. Choi, H.J., Kim, S.J., Mukhopadhyay, P., Cho, S., Woo, J.R., Storz, G., and Ryu, S.E. (2001) Structural basis of the redox switch in the OxyR transcription factor. Cell 105: 103-113.
6. Christman, M.F., Morgan, R.W., Jacobson, F.S., and Ames, B.N. (1985) Positive control of a regulon for defenses against oxidative stress and some heat-shock proteins in Salmonella typhimurium. Cell 41: 753-762.
7. Chung, K.J., Cho, E.J., Kim, M.K., Kim, Y.R., Kim, S.H., Yang, H.Y., etal. (2010) RtxA1-induced expression of the small GTPase Rac2 plays a key role in the pathogenicity of Vibrio vulnificus. J Infect Dis 201: 97-105.
8. Dubbs, J.M., and Mongkolsuk, S. (2012) Peroxide-sensing transcriptional regulators in bacteria. J Bacteriol 194: 5495-5503.
9. Goo, S.Y., Lee, H.-J., Kim, W.H., Han, K.-L., Park, D.-K., Lee, H.-J., etal. (2006) Identification of OmpU of Vibrio vulnificus as a fibronectin-binding protein and its role in bacterial pathogenesis. Infect Immun 74: 5586-5594.
10. Hall, A., Karplus, P.A., and Poole, L.B. (2009) Typical 2-Cys peroxiredoxins-structures, mechanisms and functions. FEBS J 276: 2469-2477.
11. Jacobson, F.S., Morgan, R.W., Christman, M.F., and Ames, B.N. (1989) An alkyl hydroperoxide reductase from Salmonella typhimurium involved in the defense of DNA against oxidative damage. J Biol Chem 264: 1488-1496.
12. Kelley, L.A., and Sternberg, M.J. (2009) Protein structure prediction on the web: a case study using the Phyre server. Nat Protoc 4: 363-371.
13. Kim, B.S., Hwang, J., Kim, M.H., and Choi, S.H. (2011) Cooperative regulation of the Vibrio vulnificus nan gene cluster by NanR protein, cAMP receptor protein, and N-acetylmannosamine 6-phosphate. J Biol Chem 286: 40889-40899.
14. Kim, S.O., Merchant, K., Nudelman, R., Beyer, W.F., Jr, Keng, T., DeAngelo, J., etal. (2002) OxyR: a molecular code for redox-related signaling. Cell 109: 383-396.
15. Kong, I.S., Bates, T.C., Hulsmann, A., Hassan, H., Smith, B.E., and Oliver, J.D. (2004) Role of catalase and oxyR in the viable but nonculturable state of Vibrio vulnificus. FEMS Microbiol Ecol 50: 133-142.
16. Kullik, I., Stevens, J., Toledano, M.B., and Storz, G. (1995a) Mutational analysis of the redox-sensitive transcriptional regulator OxyR: regions important for DNA binding and multimerization. J Bacteriol 177: 1285-1291.
17. Kullik, I., Toledano, M.B., Tartaglia, L.A., and Storz, G. (1995b) Mutational analysis of the redox-sensitive transcriptional regulator OxyR: regions important for oxidation and transcriptional activation. J Bacteriol 177: 1275-1284.
18. Kunisaki, H., and Tanji, Y. (2010) Intercrossing of phage genomes in a phage cocktail and stable coexistence with Escherichia coli O157:H7 in anaerobic continuous culture. Appl Microbiol Biotechnol 85: 1533-1540.
19. Lee, C., Lee, S.M., Mukhopadhyay, P., Kim, S.J., Lee, S.C., Ahn, W.S., etal. (2004) Redox regulation of OxyR requires specific disulfide bond formation involving a rapid kinetic reaction path. Nat Struct Mol Biol 11: 1179-1185.
20. Lim, J.G., and Choi, S.H. (2014) IscR is a global regulator essential for the pathogenesis of Vibrio vulnificus and induced by host cells. Infect Immun 82: 569-578.
21. Miller, R.A., and Britigan, B.E. (1997) Role of oxidants in microbial pathophysiology. Clin Microbiol Rev 10: 1-18.
22. Miller, V.L., and Mekalanos, J.J. (1988) A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J Bacteriol 170: 2575-2583.
23. Milton, D.L., O'Toole, R., Horstedt, P., and Wolf-Watz, H. (1996) Flagellin A is essential for the virulence of Vibrio anguillarum. J Bacteriol 178: 1310-1319.
24. Netto, L.E., de Oliveira, M.A., Monteiro, G., Demasi, A.P., Cussiol, J.R., Discola, K.F., etal. (2007) Reactive cysteine in proteins: protein folding, antioxidant defense, redox signaling and more. Comp Biochem Physiol C Toxicol Pharmacol 146: 180-193.
25. Oh, M.H., Jeong, H.G., and Choi, S.H. (2008) Proteomic identification and characterization of Vibrio vulnificus proteins induced upon exposure to INT-407 intestinal epithelial cells. J Microbiol Biotechnol 18: 968.
26. Oh, M.H., Lee, S.M., Lee, D.H., and Choi, S.H. (2009) Regulation of the Vibrio vulnificus hupA gene by temperature alteration and cyclic AMP receptor protein and evaluation of its role in virulence. Infect Immun 77: 1208-1215.
27. Oka, A., Sugisaki, H., and Takanami, M. (1981) Nucleotide sequence of the kanamycin resistance transposon Tn903. J Mol Biol 147: 217-226.
28. Sambrook, J., and Russell, D. (2001) Molecular Cloning: A Laboratory Manual, 3rd edn. New York: Cold Spring Horbor laboratory Press.
29. Seaver, L.C., and Imlay, J.A. (2001) Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. J Bacteriol 183: 7173-7181.
30. Seth, D., Hausladen, A., Wang, Y.J., and Stamler, J.S. (2012) Endogenous protein S-nitrosylation in E. coli: regulation by OxyR. Science 336: 470-473.
31. Storz, G., and Zheng, M. (2000) Oxidative stress. In Bacterial Stress Responses. Storz, G., and Hengge-Aronis, R. (eds). Washington, DC: ASM Press, pp. 47-59.
32. Storz, G., Jacobson, F., Tartaglia, L., Morgan, R., Silveira, L., and Ames, B. (1989) An alkyl hydroperoxide reductase induced by oxidative stress in Salmonella typhimurium and Escherichia coli: genetic characterization and cloning of ahp. J Bacteriol 171: 2049-2055.
33. Storz, G., Tartaglia, L.A., and Ames, B.N. (1990) Transcriptional regulator of oxidative stress-inducible genes: direct activation by oxidation. Science 248: 189-194.
34. Tao, K., Makino, K., Yonei, S., Nakata, A., and Shinagawa, H. (1991) Purification and characterization of the Escherichia coli OxyR protein, the positive regulator for a hydrogen peroxide-inducible regulon. J Biochem 109: 262-266.
35. Tao, K., Fujita, N., and Ishihama, A. (1993) Involvement of the RNA polymerase α subunit C-terminal region in co-operative interaction and transcriptional activation with OxyR protein. Mol Microbiol 7: 859-864.
36. Toledano, M.B., Kullik, I., Trinh, F., Balrd, P.T., Schnelder, T.D., and Storz, G. (1994) Redox-dependent shift of OxyR-DNA contacts along an extended DNA-binding site: a mechanism for differential promoter selection. Cell 78: 897-909.
37. Wang, X., Mukhopadhyay, P., Wood, M.J., Outten, F.W., Opdyke, J.A., and Storz, G. (2006) Mutational analysis to define an activating region on the redox-sensitive transcriptional regulator OxyR. J Bacteriol 188: 8335-8342.
38. Zaim, J., and Kierzek, A.M. (2003) The structure of full-length LysR-type transcriptional regulators. Modeling of the full-length OxyR transcription factor dimer. Nucleic Acids Res 31: 1444-1454.
39. Zheng, M., Aslund, F., and Storz, G. (1998) Activation of the OxyR transcription factor by reversible disulfide bond formation. Science 279: 1718-1722.
40. Zheng, M., Wang, X., Templeton, L.J., Smulski, D.R., LaRossa, R.A., and Storz, G. (2001) DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J Bacteriol 183: 4562-4570.