Alkyl Hydroperoxide Reductase Dependent on Thioredoxin-Like Protein from Pyrococcus horikoshii

Yasuhiro Kashima; Kazuhiko Ishikawa

doi:10.1093/jb/mvg109

Alkyl Hydroperoxide Reductase Dependent on Thioredoxin-Like Protein from Pyrococcus horikoshii

Author information

Keywords: alkyl hydroperoxide reductase, hyperthermophilic archaea, oxidative stress, Pyrococcus horikoshii, thioredoxin system

JOURNAL FREE ACCESS

2003 Volume 134 Issue 1 Pages 25-29

DOI https://doi.org/10.1093/jb/mvg109

Details

Published: 2003 Received: February 25, 2003 Available on J-STAGE: June 30, 2008 Accepted: May 14, 2003 Advance online publication: - Revised: -
Correction information
Date of correction: June 30, 2008 Reason for correction: - Correction: ABSTRACT Details: Wrong : Pyrococcus horikoshii is an obligate anaerobic hyperthermophilic archaeon. In P. horikoshii cells, a hydroperoxide reductase homologue ORF (PH 1217) was found to be induced by oxygen. The recombinant protein, which was expressed in E. coli under aerobic conditions, exhibited no activity. However, the recombinant protein prepared under semi-anaerobic conditions exhibited alkyl hydroperoxide reductase activity. Furthermore, it was clarified that it was coupled with the thioredoxin-like system in P. horikoshii. Western blot analysis revealed that the protein was induced by oxygen and hydrogen peroxide. This protein seems to be sensitive to oxygen but forms a thioredoxin-dependent system to eliminate reactive oxygen species in P. horikoshii.
Right : Pyrococcus horikoshii is an obligate anaerobic hyperthermophilic archaeon. In P. horikoshii cells, a hydroperoxide reductase homologue ORF (PH1217) was found to be induced by oxygen. The recombinant protein, which was expressed in E. coli under aerobic conditions, exhibited no activity. However, the recombinant protein prepared under semi-anaerobic conditions exhibited alkyl hydroperoxide reductase activity. Furthermore, it was clarified that it was coupled with the thioredoxin-like system in P. horikoshii. Western blot analysis revealed that the protein was induced by oxygen and hydrogen peroxide. This protein seems to be sensitive to oxygen but forms a thioredoxin-dependent system to eliminate reactive oxygen species in P. horikoshii.

Date of correction: June 30, 2008 Reason for correction: - Correction: AFFILIATION Details: Wrong :
1) Special Division of Human Life Technology, National Institute of Advanced Industrial Science and Technology

Right :
1) Special Division of Human Life Technology, National Institute of Advanced Industrial Science and Technology (AIST Kansai)

Date of correction: June 30, 2008 Reason for correction: - Correction: CITATION Details: Wrong : 1. Longo, V. D, Gralla, E. B., and Valentine, J. S. (1996) Superoxide dismutase activity is essential for stationaonahase survival in Saccharomyces cerevzsiae. Mitochondrial production of toxic oxygen species in vivo. J. Biol. Chem. 271, 12275-12280
2. Fridovich, I. (1995) Superoxide radical and superoxide dismutases. Annu, Rev. Biochem. 64, 97-112
3. Gort, A., Ferber, D. M., and Imlay, J. A. (1999) The regulation and role of the periplasmic copper, zinc, superoxide dismutase of Escherichia coli. Mol. Microbiol. 32, 179-191
4. Jenny, F. E. Jr, Verhagen, M. F., Cui, X., and Adams, M. W. (1999) Anaerobic microbes: oxygen detoxification without superoxide dismutase. Science 286, 306-309
5. Brown, S. M., Howell, M. L., Vasil, M. L., Anderson, A. J., and Hassett, D. J. (1995) Cloning and characterization of the katB gene of Pseudomonas aeruginosa encoding a hydrogen peroxide-inducible catalase: purification of KatB, cellular localization, and demonstration that it is essential for optimal resistance to hydrogen peroxide. J. Bacteriol. 177, 6536-6544
6. Hofmann, B., Hecht, H. J., and Flohe, L. (2002) Peroxiredoxins. Biol. Chem. 383, 347-364
7. Arner, E. S. and Holmgren, A. (2000) Physiological functions of thioredoxin and thioredoxin reductase. Eur. J. Biochem. 267, 6102-6109
8. Williams, C. H., Arscott, L. D., Muller, S., Lennon, B. W., Ludwig, M. L., Wang, P. E, Veine, D. M., Becker, K., and Schirmer, R. H. (2000) Thioredoxin reductase. Two modes of catalysis have evolved. Eur. J. Biochem. 267, 6110-6117
9. Holmgren, A. (1979) Reduction of disulfide by thioredoxin. J. Biol. Chem. 254, 9113-9119
10. Song, J. J., Rhee, J. G., Suntharalingam, M., Walsh, S. A., Spitz, D. R,, and Lee, Y. J. (2002) Role of glutaredoxin in metabolic oxidative stress. Glutaredoxin as a sensor of oxidative stress mediated by H₂O₂. J. Biol. Chem. 277, 46566-46575
11. Holmgren, A. and Aslund, F. (1995) Glutaredoxin. Methods Enzymol. 252, 283-292
12. Pueyo, C., Jurado, J., Prieto-Alamo, M. J., Monje-Casas, F., and Lopez-Barea, J. (2002) Multiplex reverse transcriptionpolymerase chain reaction for determining transcriptional regulation of thioredoxin and glutaredoxin pathways. Methods Enzymol. 347, 441-451
13. Imalay, J. and Linn, S. (1988) Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro. Science 240, 640-642
14. Jamieson, D. and Storz, G. (1997) Transcriptional regulators of oxidative stress responses in Oxidative Stress and Molecular Biology of Antioxidant Defenses. (Scandalios. J., ed.) pp. 91-115, Cold spring harbor Laboratory, Cold Spring Harbor, NY
15. 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
16. Reynolds, C. M., Meyer, J., and Poole, L. B. (2002) An NADH-dependent bacterial thioredoxin reductase-like protein in conjunction with a glutaredoxin homologue form a unique peroxiredoxin (AhpC) reducing system in Clostridium pasteurianum. Biochemistry 41, 1990-2001
17. Hillas, P. J., del Alba, F. S., Oyarzabal, J., Wilks, A., and de Montellano, P. R. O. (0000) The AhpC and AhpD antioxidant defense system of Mycobacterium tuberculosis. J. Biol. Chem. 275, 18801-18809
18. Baker, L. M. S., Raudonikiene, A., Hofmman, P. S., and Poole, L. B. (2001) Essential thioredoxin-dependent peroxiredoxin system from Helicobacter pylori: genetic and kinetic characterization. J. Bacteriol. 183, 1961-1973
19. 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
20. Poole, L. B. and Ellis, H. R. (1996) Flavin-dependent alkyl hydroperoxide reductase from Salmonella typhimulium, 1. Purification and enzymatic activities of overexpressed AhpF and AhpC proteins. Biochemistry 35, 56-64
21. Poole, L. B., Reynolds, C. M., Wood, Z. A., Karplus, P. A., Ellis, H. R., and Calzi, M. L. (2000) AhpF and other NADH: peroxiredoxin oxidoreductases, homologues of low M_r thioredoxin reductase. Eur. J. Biochem. 267, 6126-6133
22. Poole, L. B., Godzik, A., Nayeem, A., and Schmitt, J. D. (2000) AhpF can be dissected two functional units: tandem repeats of two thioredoxin-like folds in the N-terminus mediate electron transfer from the thioredoxin reductase-like C-terminus to AhpC. Biochemistry 39, 6602-6615
23. Blake, P. R., Park, J. B., Bryant, F. O., Aono, S., Magnuson, J. K, Eccleson, E., Howard, J. B., Summers, M. F., and Adams, M. W. W. (1991) Determinants of protein hyperthermostability: purification and amino acid sequence of rubredoxin from the hyperthermophilic archaebacterium Pyrococcus furiosus and secondary structure of the zinc adduct by NMR. Biochemistry 30, 10885-10895
24. Kesen, M. and Adams, M. W. W. (1999) A hyperactive NAD (P) H: rubredoxin oxidoreductase from the hyperthermophilic archaeon Pyrococcus furiosus. J. Bacteriol. 181, 5530-5533
25. Meade, H. M., Long, S. R., Ruvkun, G. B., Brown, S. E., and Ausubel, F. M. (1982) Physical and genetic characterization of symbiotic and auxotrophic mutants of Rhizobium meliloti induced by transposon Tn 5 mutagenesis. J. Bacteriol. 149, 114-22
26. Pedrajas, J. R., Miranda-Vizuete, A., Javanmardy, N., Gustafsson, J. A., and Spyrou, G. (2000) Mitochondria of Saccharomyces cerevisiae contain one-conserved cysteine type peroxiredoxin with thioredoxin peroxidase activity. J. Biol. Chem. 275, 16296-16301
27. Prieto-Almano, M. J., Jurado, J., Gallardo-Madueno, R., Monje-Casas, F., Holmgren, A., and Pueyo, C. (2000) Transcriptionalregulation of glutaredoxin and thioredoxin pathways, and related enzymes in response to oxidative stress. J. Biol. Chem. 275, 13398-13405
28. Thurman, R. G., Ley, H. G., and Scholz, R. (1972) Hepatic microsomal ethanol oxidation. Hydrogen peroxide formation and the role of catalase. Eur. J. Biochem. 25, 420-430

Right : 1. Longo, V. D, Gralla, E. B., and Valentine, J. S. (1996) Superoxide dismutase activity is essential for stationary phase survival in Saccharomyces cerevzsiae. Mitochondrial production of toxic oxygen species in vivo. J. Biol. Chem. 271, 12275-12280
2. Fridovich, I. (1995) Superoxide radical and superoxide dismutases. Annu, Rev. Biochem. 64, 97-112
3. Gort, A., Ferber, D. M., and Imlay, J. A. (1999) The regulation and role of the periplasmic copper, zinc, superoxide dismutase of Escherichia coli. Mol. Microbiol. 32, 179-191
4. Jenny, F. E. Jr, Verhagen, M. F., Cui, X., and Adams, M. W. (1999) Anaerobic microbes: oxygen detoxification without superoxide dismutase. Science 286, 306-309
5. Brown, S. M., Howell, M. L., Vasil, M. L., Anderson, A. J., and Hassett, D. J. (1995) Cloning and characterization of the katB gene of Pseudomonas aeruginosa encoding a hydrogen peroxide-inducible catalase: purification of KatB, cellular localization, and demonstration that it is essential for optimal resistance to hydrogen peroxide. J. Bacteriol. 177, 6536-6544
6. Hofmann, B., Hecht, H. J., and Flohe, L. (2002) Peroxiredoxins. Biol. Chem. 383, 347-364
7. Arner, E. S. and Holmgren, A. (2000) Physiological functions of thioredoxin and thioredoxin reductase. Eur. J. Biochem. 267, 6102-6109
8. Williams, C. H., Arscott, L. D., Muller, S., Lennon, B. W., Ludwig, M. L., Wang, P. E, Veine, D. M., Becker, K., and Schirmer, R. H. (2000) Thioredoxin reductase. Two modes of catalysis have evolved. Eur. J. Biochem. 267, 6110-6117
9. Holmgren, A. (1979) Reduction of disulfide by thioredoxin. J. Biol. Chem. 254, 9113-9119
10. Song, J. J., Rhee, J. G., Suntharalingam, M., Walsh, S. A., Spitz, D. R,, and Lee, Y. J. (2002) Role of glutaredoxin in metabolic oxidative stress. Glutaredoxin as a sensor of oxidative stress mediated by H₂O₂. J. Biol. Chem. 277, 46566-46575
11. Holmgren, A. and Aslund, F. (1995) Glutaredoxin. Methods Enzymol. 252, 283-292
12. Pueyo, C., Jurado, J., Prieto-Alamo, M. J., Monje-Casas, F., and Lopez-Barea, J. (2002) Multiplex reverse transcription-polymerase chain reaction for determining transcriptional regulation of thioredoxin and glutaredoxin pathways. Methods Enzymol. 347, 441-451
13. Imalay, J. and Linn, S. (1988) Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro. Science 240, 640-642
14. Jamieson, D. and Storz, G. (1997) Transcriptional regulators of oxidative stress responses in Oxidative Stress and Molecular Biology of Antioxidant Defenses. (Scandalios. J., ed.) pp. 91-115, Cold spring harbor Laboratory, Cold Spring Harbor, NY
15. 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
16. Reynolds, C. M., Meyer, J., and Poole, L. B. (2002) An NADH-dependent bacterial thioredoxin reductase-like protein in conjunction with a glutaredoxin homologue form a unique peroxiredoxin (AhpC) reducing system in Clostridium pasteurianum. Biochemistry 41, 1990-2001
17. Hillas, P. J., del Alba, F. S., Oyarzabal, J., Wilks, A., and de Montellano, P. R. O. (0000) The AhpC and AhpD antioxidant defense system of Mycobacterium tuberculosis. J. Biol. Chem. 275, 18801-18809
18. Baker, L. M. S., Raudonikiene, A., Hofmman, P. S., and Poole, L. B. (2001) Essential thioredoxin-dependent peroxiredoxin system from Helicobacter pylori: genetic and kinetic characterization. J. Bacteriol. 183, 1961-1973
19. 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
20. Poole, L. B. and Ellis, H. R. (1996) Flavin-dependent alkyl hydroperoxide reductase from Salmonella typhimulium, 1. Purification and enzymatic activities of overexpressed AhpF and AhpC proteins. Biochemistry 35, 56-64
21. Poole, L. B., Reynolds, C. M., Wood, Z. A., Karplus, P. A., Ellis, H. R., and Calzi, M. L. (2000) AhpF and other NADH: peroxiredoxin oxidoreductases, homologues of low M_r thioredoxin reductase. Eur. J. Biochem. 267, 6126-6133
22. Poole, L. B., Godzik, A., Nayeem, A., and Schmitt, J. D. (2000) AhpF can be dissected two functional units: tandem repeats of two thioredoxin-like folds in the N-terminus mediate electron transfer from the thioredoxin reductase-like C-terminus to AhpC. Biochemistry 39, 6602-6615
23. Blake, P. R., Park, J. B., Bryant, F. O., Aono, S., Magnuson, J. K, Eccleson, E., Howard, J. B., Summers, M. F., and Adams, M. W. W. (1991) Determinants of protein hyperthermostability: purification and amino acid sequence of rubredoxin from the hyperthermophilic archaebacterium Pyrococcus furiosus and secondary structure of the zinc adduct by NMR. Biochemistry 30, 10885-10895
24. Kesen, M. and Adams, M. W. W. (1999) A hyperactive NAD (P) H: rubredoxin oxidoreductase from the hyperthermophilic archaeon Pyrococcus furiosus. J. Bacteriol. 181, 5530-5533
25. Meade, H. M., Long, S. R., Ruvkun, G. B., Brown, S. E., and Ausubel, F. M. (1982) Physical and genetic characterization of symbiotic and auxotrophic mutants of Rhizobium meliloti induced by transposon Tn5 mutagenesis. J. Bacteriol. 149, 114-22
26. Pedrajas, J. R., Miranda-Vizuete, A., Javanmardy, N., Gustafsson, J. A., and Spyrou, G. (2000) Mitochondria of Saccharomyces cerevisiae contain one-conserved cysteine type peroxiredoxin with thioredoxin peroxidase activity. J. Biol. Chem. 275, 16296-16301
27. Prieto-Almano, M. J., Jurado, J., Gallardo-Madueno, R., Monje-Casas, F., Holmgren, A., and Pueyo, C. (2000) Transcriptional regulation of glutaredoxin and thioredoxin pathways, and related enzymes in response to oxidative stress. J. Biol. Chem. 275, 13398-13405
28. Thurman, R. G., Ley, H. G., and Scholz, R. (1972) Hepatic microsomal ethanol oxidation. Hydrogen peroxide formation and the role of catalase. Eur. J. Biochem. 25, 420-430

Date of correction: June 30, 2008 Reason for correction: - Correction: PDF FILE Details: -

Abstract

Pyrococcus horikoshii is an obligate anaerobic hyperthermophilic archaeon. In P. horikoshii cells, a hydroperoxide reductase homologue ORF (PH1217) was found to be induced by oxygen. The recombinant protein, which was expressed in E. coli under aerobic conditions, exhibited no activity. However, the recombinant protein prepared under semi-anaerobic conditions exhibited alkyl hydroperoxide reductase activity. Furthermore, it was clarified that it was coupled with the thioredoxin-like system in P. horikoshii. Western blot analysis revealed that the protein was induced by oxygen and hydrogen peroxide. This protein seems to be sensitive to oxygen but forms a thioredoxin-dependent system to eliminate reactive oxygen species in P. horikoshii.

Corresponding author

Correction information

Register with J-STAGE for free!