The Campylobacter jejuni thiol peroxidases Tpx and Bcp both contribute to aerotolerance and peroxide-mediated stress resistance but have distinct substrate specificities

Journal of Bacteriology

Volumn 190, Issue 15, 2008, Pages 5279-5290

  Atack, John M ^a   Harvey, Philippa ^b   Jones, Michael A ^c   Kelly, David J ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

^c UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; HYDROGEN PEROXIDE; OXYGEN; PEROXIDASE; PEROXIDE; PROTEIN BCP; PROTEIN TPX; RECOMBINANT ENZYME; SUPEROXIDE;

AERATION; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BCP GENE; CAMPYLOBACTER JEJUNI; CELL VIABILITY; CONTROLLED STUDY; DISK DIFFUSION; ENZYME ACTIVITY; GENE MUTATION; IMMUNOBLOTTING; LIPID PEROXIDATION; MUTANT; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CARBONYLATION; QUANTITATIVE ANALYSIS; TPX GENE; WILD TYPE;

ADAPTATION, PHYSIOLOGICAL; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; CAMPYLOBACTER JEJUNI; GENE DELETION; LIPID PEROXIDATION; MICROBIAL VIABILITY; OXIDANTS; OXIDATION-REDUCTION; OXIDATIVE STRESS; PEROXIDASES; PEROXIDES; PROTEIN CARBONYLATION; SUBSTRATE SPECIFICITY; SULFHYDRYL COMPOUNDS;

AVES; CAMPYLOBACTER JEJUNI; MAMMALIA;

EID: 48149094202     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00100-08     Document Type: Article

References (46)

1. Atack, J. M., and D. J. Kelly. 2006. Structure, mechanism and physiological roles of bacterial cytochrome c peroxidases. Adv. Microb. Physiol. 52:73-106.
2. Baillon, M.-L. A., A. H. M. van Vliet, J. M. Ketley, C. Constantinidou, and C. W. Penn. 1999. An iron-regulated alkyl hydroperoxide reductase (AhpC) confers aerotolerance and oxidative stress resistance to the microaerophilic pathogen Campylobacter jejuni. J. Bacteriol. 181:4798-4804.
3. Bryk, R., P. Griffin, and C. Nathan. 2000. Peroxynitrite reductase activity of bacterial peroxiredoxins. Nature 407:211-215.
4. Cha, M., H. Kim, and I. Kim. 1995. Thioredoxin-linked "thiol peroxidase" from periplasmic space of Escherichia coli. J. Biol. Chem. 270:28635-28641.
5. Cha, M., H. Kim, and I. Kim. 1996. Mutation and mutagenesis of thiol peroxidase of Escherichia coli and a new type of thiol peroxidase family. J. Bacteriol. 178:5610-5614.
6. Cha, M., W. Kim, C. Lim, K. Kim, and I. Kim. 2004. Escherichia coli periplasmic thiol peroxidase acts as lipid hydroperoxide peroxidase and the principal antioxidative function during anaerobic growth. J. Biol. Chem. 279:8769-8778.
7. Chelikani, P., I. Fita, and P. C. Loewen. 2004. Diversity of structures and properties among catalases. Cell. Mol. Life Sci. 61:192-208.
8. Chuang, M.-H., M.-S. Wu, W.-L. Lo, J.-T. Lin, C.-H. Wong, and S.-H. Chiou. 2006. The antioxidant protein alkylhydroperoxide reductase of Helicobacter pylori switches from a peroxide reductase to a molecular chaperone function. Proc. Natl. Acad. Sci. USA 103:2552-2557.
9. Comtois, S. L., M. D. Gidley, and D. J. Kelly. 2003. Role of the thioredoxin system and the thiol-peroxidases Tpx and Bcp in mediating resistance to oxidative and nitrosative stress in Helicobacter pylori. Microbiology 149:121-129.
10. Ellis, H. R., and L. B. Poole. 1997. Roles for the two cysteine residues of AhpC in catalysis of peroxide reduction by alkyl hydroperoxide reductase from Salmonella typhimurium. Biochemistry 36:13349- 13356.
11. Elvers, K. T., G. Wu, N. J. Gilberthorpe, R. K. Poole, and S. F. Park. 2004. Role of an inducible single-domain hemoglobin in mediating resistance to nitric oxide and nitrosative stress in Campylobacter jejuni and Campylobacter coli. J. Bacteriol. 186:5332-5341.
12. Elvers, K. T., S. M. Turner, L. M. Wainwright, G. Marsden, J. Hinds, J. A. Cole, R. K. Poole, C. W. Penn, and S. F. Park. 2005. NssR, a member of the Crp-Fnr superfamily from Campylobacter jejuni, regulates a nitrosative stress-responsive regulon that includes both a single-domain and a truncated haemoglobin. Mol. Microbiol. 57:735-750.
13. Grant, K., and S. Park. 1995. Molecular characterization of KatA from Campylobacter jejuni and generation of a catalase-deficient mutant of Campylobacter coli by interspecific allelic exchange. Microbiology 141:1369-1376.
14. Hillas, P. J., F. S. del Alba, J. Oyarzabal, A. Wilks, and P. R. Ortiz de Montellano. 2000. The AhpC and AhpD antioxidant defense system of Mycobacterium tuberculosis. J. Biol. Chem. 275:18801-18809.
15. Hofreuter, D., J. Tsai, R. O. Watson, V. Novik, B. Altman, M. Benitez, C. Clark, C. Perbost, T. Jarvie, L. Du, and J. E. Galan. 2006. Unique features of a highly pathogenic Campylobacter jejuni strain. Infect. Immun. 74:4694-4707.
16. Imlay, J. A. 2003. Pathways of oxidative damage. Annu. Rev. Microbiol. 57:395-418.
17. Jeong, W., M.-K. Cha, and I.-H. Kim. 2000. Thioredoxin-dependent hydroperoxide peroxidase activity of bacterioferritin comigratory protein (BCP) as a new member of the thiol-specific antioxidant protein (TSA)/alkyl hydroperoxide peroxidase C (AhpC) family. J. Biol. Chem. 275:2924-2930.
18. Ketley, J. 1997. Pathogenesis of enteric infection by Campylobacter. Microbiology 143:5-21.
19. Levine, R. 1983. Oxidative modification of glutamine synthetase. I. Inactivation is due to loss of one histidine residue. J. Biol. Chem. 258:11823-11827.
20. Levine, R., D. Garland, C. Oliver, A. Amici, I. Climent, A. Lenz, B. Ahn, S. Shaltiel, and E. Stadtman. 1990. Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol. 186:464-478.
21. Markwell, M. A. K., S. M. Haas, L. L. Bieber, and N. E. Tolbert. 1978. A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal. Biochem. 87:206-210.
22. Master, S. S., B. Springer, P. Sander, E. C. Boettger, V. Deretic, and G. S. Timmins. 2002. Oxidative stress response genes in Mycobacterium tuberculosis: role of ahpC in resistance to peroxynitrite and stage-specific survival in macrophages. Microbiology 148:3139-3144.
23. Mostertz, J., and M. Hecker. 2003. Patterns of protein carbonylation following oxidative stress in wild-type and sigB Bacillus subtilis cells. Mol. Genet. Genomics 269:640-648.
24. Myers, J. D., and D. J. Kelly. 2005. A sulphite respiration system in the chemoheterotrophic human pathogen Campylobacter jejuni. Microbiology 151:233-242.
25. Olczak, A. A., R. W. Seyler, Jr., J. W. Olson, and R. J. Maier. 2003. Association of Helicobacter pylori antioxidant activities with host colonization proficiency. Infect. Immun. 71:580-583.
26. Park, S. F. 2002. The physiology of Campylobacter species and its relevance to their role as foodborne pathogens. Int. J. Food Microbiol. 74:177-188.
27. Parkhill, J., B. W. Wren, K. Mungall, J. M. Ketley, C. Churcher, D. Basham, T. Chillingworth, R. M. Davies, T. Feltwell, S. Holroyd, K. Jagels, A. V. Karlyshev, S. Moule, M. J. Pallen, C. W. Penn, M. A. Quail, M.-A. Rajandream, K. M. Rutherford, A. H. M. van Vliet, S. Whitehead, and B. G. Barrell. 2000. The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403:665-668.
28. Pearson, B. M., D. J. H. Gaskin, R. P. A. M. Segers, J. M. Wells, P. J. M. Nuijten, and A. H. M. van Vliet. 2007. The complete genome sequence of Campylobacter jejuni strain 81116 (NCTC11828). J. Bacteriol. 189:8402-8403.
29. Pesci, E. C., D. L. Cottle, and C. L. Pickett. 1994. Genetic, enzymatic, and pathogenic studies of the iron superoxide dismutase of Campylobacter jejuni. Infect. Immun. 62:2687-2694.
30. Pittman, M. S., K. T. Elvers, L. Lee, M. A. Jones, R. K. Poole, S. F. Park, and D. J. Kelly. 2007. Growth of Campylobacter jejuni on nitrate and nitrite: electron transport to NapA and NrfA via NrfH and distinct roles for NrfA and the globin Cgb in protection against nitrosative stress. Mol. Microbiol. 63:575-590.
31. Poole, L. B. 2005. Bacterial defenses against oxidants: mechanistic features of cysteine-based peroxidases and their flavoprotein reductases. Arch. Biochem. Biophys. 433:240-254.
32. Rho, B.-S., L.-W. Hung, J. M. Holton, D. Vigil, S.-I. Kim, M. S. Park, T. C. Terwilliger, and J.-D. Pedelacq. 2006. Functional and structural characterization of a thiol peroxidase from Mycobacterium tuberculosis. J. Mol. Biol. 361:850-863.
33. Rozen, S., and H. Skaletsky. 2000. Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 132:365-386.
34. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
35. Seaver, L. C., and J. A. Imlay. 2001. Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. J. Bacteriol. 183:7173-7181.
36. Shacter, E., J. E. Williams, M. Lim, and R. L. Levine. 1994. Differential susceptibility of plasma proteins to oxidative modification: examination by western blot immunoassay. Free Radic. Biol. Med. 17:429-437.
37. Sommerlad, S. M., and D. R. Hendrixson. 2007. Analysis of the roles of FlgP and FlgQ in flagellar motility of Campylobacter jejuni. J. Bacteriol. 189:179-186.
38. Stadtman, E. 1992. Protein oxidation and aging. Science 257:12211-1224.
39. Storz, G., and J. A. Imlay. 1999. Oxidative stress. Curr. Opin. Microbiol. 2:188-194.
40. Tauxe, R. V. 1992. Epidemiology of Campylobacter infections in the United States and other industrialized nations, p. 9-19. In I. Nachamkin, M. J. Blaser, and L. S. Tompkins (ed.), Campylobacter jejuni: current status and future trends. American Society for Microbiology. Washington, DC.
41. van Vliet, A. H. M., K. G. Wooldridge, and J. M. Ketley. 1998. Iron-responsive gene regulation in a Campylobacter jejuni fur mutant. J. Bacteriol. 180:5291-5298.
42. Wang, G., R. C. Conover, S. Benoit, A. A. Olczak, J. W. Olson, M. K. Johnson, and R. J. Maier. 2004. Role of a bacterial organic hydroperoxide detoxification system in preventing catalase inactivation. J. Biol. Chem. 279:51908-51914.
43. Wang, G., A. A. Olczak, J. P. Walton, and R. J. Maier. 2005. Contribution of the Helicobacter pylori thiol peroxidase bacterioferritin comigratory protein to oxidative stress resistance and host colonization. Infect. Immun. 73:378-384.
44. Wang, Y., and D. E. Taylor. 1990. Chloramphenicol resistance in Campylobacter coli: nucleotide sequence, expression, and cloning vector construction. Gene 94:23-28.
45. Wood, Z. A., E. Schroder, J. R. Harris, and L. B. Poole. 2003. Structure, mechanism and regulation of peroxiredoxins. Trends Biochem. Sci. 28:32-40.
46. Zhou, Y., X.-Y. Wan, H.-L. Wang, Z.-Y. Yan, Y. De Hou, and D.-Y. Jin. 1997. Bacterial scavengase p20 is structurally and functionally related to peroxiredoxins. Biochem. Biophys. Res. Commun. 233:848-852.