Glutathione and catalase provide overlapping defenses for protection against respiration-generated hydrogen peroxide in Haemophilus influenzae

Journal of Bacteriology

Volumn 185, Issue 18, 2003, Pages 5555-5562

  Vergauwen, Bjorn ^a   Pauwels, Frederik ^a   Van Beeumen, Jozef J ^a  

^a GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CATALASE; GLUTATHIONE; HYDROGEN PEROXIDE; SCAVENGER;

AEROBIC METABOLISM; ARTICLE; ESCHERICHIA COLI; HAEMOPHILUS INFLUENZAE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL;

AEROBIOSIS; CATALASE; CELL DIVISION; CULTURE MEDIA; GLUTATHIONE; HAEMOPHILUS INFLUENZAE; HYDROGEN PEROXIDE; MUTATION; OXIDATION-REDUCTION;

ESCHERICHIA COLI; EUKARYOTA; HAEMOPHILUS; HAEMOPHILUS INFLUENZAE; NEGIBACTERIA;

EID: 0042838106     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.185.18.5555-5562.2003     Document Type: Article

References (45)

1. Abe, K., N. Makino, and F. K. Anan. 1979. pH dependency of kinetic parameters and reaction mechanism of beef liver catalase. J. Biochem. 85:473-479.
2. Bishai, W. R., N. S. Howard, J. A. Winkelstein, and H. O. Smith. 1994. Characterization and virulence analysis of catalase mutants of Haemophilus influenzae. Infect. Immun. 62:4855-4860.
3. Bishai, W. R., H. O. Smith, and G. J. Barcak. 1994. A peroxide/ascorbate-inducible catalase from Haemophilus influenzae is homologous to the Escherichia coli katE gene product. J. Bacteriol. 176:2914-2921.
4. Brawn, K., and I. Fridovich. 1981. DNA strand scission by enzymically generated oxygen radicals. Arch. Biochem. Biophys. 206:414-419.
5. Chance, B., H. Sies, and A. Boveris. 1979. Hydroperoxide metabolism in mammalian organs. Physiol. Rev. 59:527-605.
6. del Rio, L. A., L. M. Sandalio, J. M. Palma, P. Bueno, and F. J. Corpas. 1992. Metabolism of oxygen radicals in peroxisomes and cellular implications. Free Radic. Biol. Med. 13:557-580.
7. Fleischmann, R. D., M. D. Adams, O. White, R. A. Clayton, E. F. Kirkness, A. R. Kerlavage, C. J. Bult, J. F. Tomb, B. A. Dougherty, J. M. Merrick, et al. 1995. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269:496-512.
8. Garcia-Ruiz, C., A. Colell, A. Morales, N. Kaplowitz, and J. C. Fernandez-Checa. 1995. Role of oxidative stress generated from the mitochondrial electron transport chain and mitochondrial glutathione status in loss of mitochondrial function and activation of transcription factor nuclear factor-κB: studies with isolated mitochondria and rat hepatocytes. Mol. Pharmacol. 48:825-834.
9. Gonzalez-Flecha, B., and B. Demple. 1995. Metabolic sources of hydrogen peroxide in aerobically growing Escherichia coli. J. Biol. Chem. 270:13681-13687.
10. Grant, C. M., G. Perrone, and I. W. Dawes. 1998. Glutathione and catalase provide overlapping defenses for protection against hydrogen peroxide in the yeast Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 253:893-898.
11. 2 and gamma radiation. J. Bacteriol. 168:1026-1029.
12. Greenwald, R. A. 1985. Therapeutic benefits of oxygen radical scavenger treatments remain unproven. J. Free Radic. Biol. Med. 1:173-177.
13. Halliwell, B. 1991. Reactive oxygen species in living systems: source, biochemistry, and role in human disease. Am. J. Med. 91:14S-22S.
14. Hassett, D. J., E. Alsabbagh, K. Parvatiyar, M. L. Howell, R. W. Wilmott, and U. A. Ochsner. 2000. A protease-resistant catalase, KatA, released upon cell lysis during stationary phase is essential for aerobic survival of a Pseudomonas aeruginosa oxyR mutant at low cell densities. J. Bacteriol. 182:4557-4563.
15. Herriott, R. M., E. M. Meyer, and M. Vogt. 1970. Defined nongrowth media for stage II development of competence in Haemophilus influenzae. J. Bacteriol. 101:517-524.
16. Inoue, Y., T. Matsuda, K. Sugiyama, S. Izawa, and A. Kimura. 1999. Genetic analysis of glutathione peroxidase in oxidative stress response of Saccharomyces cerevisiae. J. Biol. Chem. 274:27002-27009.
17. Izawa, S., Y. Inoue, and A. Kimura. 1995. Oxidative stress response in yeast: effect of glutathione on adaptation to hydrogen peroxide stress in Saccharomyces cerevisiae. FEBS Lett. 368:73-76.
18. Jacobson, F. S., R. W. Morgan, M. F. Christman, and B. N. Ames. 1989. An alkyl hydroperoxide reductase from Salmonella typhimurium involved in the defense of DNA against oxidative damage: purification and properties. J. Biol. Chem. 264:1488-1496.
19. Jain, A., J. Martensson, E. Stole, P. A. Auld, and A. Meister. 1991. Glutathione deficiency leads to mitochondrial damage in brain. Proc. Natl. Acad. Sci. USA 88:1913-1917.
20. Kinoshita, H., H. Atomi, M. Ueda, and A. Tanaka. 1994. Characterization of the catalase of the n-alkane-utilizing yeast Candida tropicalis functionally expressed in Saccharomyces cerevisiae. Appl. Microbiol. Biotechnol. 40:682-686.
21. Lesko, S. A., R. J. Lorentzen, and P. O. Ts'o. 1980. Role of superoxide in deoxyribonucleic acid strand scission. Biochemistry 19:3023-3028.
22. Loewen, P. C., and R. Hengge-Aronis. 1994. The role of the sigma factor sigma S (KatF) in bacterial global regulation. Annu. Rev. Microbiol. 48:53-80.
23. Meister, A., and M. E. Anderson. 1983. Glutathione. Annu. Rev. Biochem. 52:711-760.
24. Mongkolsuk, S., W. Whangsuk, P. Vattanaviboon, S. Loprasert, and M. Fuangthong. 2000. A Xanthomonas alkyl hydroperoxide reductase subunit C (ahpC) mutant showed an altered peroxide stress response and complex regulation of the compensatory response of peroxide detoxification enzymes. J. Bacteriol. 182:6845-6849.
25. Moxon, E. R. 1986. The carrier state: Haemophilus influenzae. J. Antimicrob. Chemother. 18(Suppl. A):17-24.
26. Niimura, Y., L. B. Poole, and V. Massey. 1995. Amphibacillus xylanus NADH oxidase and Salmonella typhimurium alkyl-hydroperoxide reductase flavoprotein components show extremely high scavenging activity for both alkyl hydroperoxide and hydrogen peroxide in the presence of S. typhimurium alkyl-hydroperoxide reductase 22-kDa protein component. J. Biol. Chem. 270:25645-25650.
27. Ochsner, U. A., M. L. Vasil, E. Alsabbagh, K. Parvatiyar, and D. J. Hassett. 2000. Role of the Pseudomonas aeruginosa oxyR-recG operon in oxidative stress defense and DNA repair: OxyR-dependent regulation of katB-ankB, ahpB, and ahpC-ahpF. J. Bacteriol. 182:4533-4544.
28. Oktyabrsky, O. N., G. V. Smirnovam, and N. G. Muzyka. 2001. Role of glutathione in regulation of hydroperoxidase I in growing Escherichia coli. Free Radic. Biol. Med. 31:250-255.
29. Park, S. G., M. K. Cha, W. Jeong, and I. H. Kim. 2000. Distinct physiological functions of thiol peroxidase isoenzymes in Saccharomyces cerevisiae. J. Biol. Chem. 275:5723-5732.
30. Pauwels, F., B. Vergauwen, F. Vanrobaeys, B. Devreese, and J. J. Van Beeumen. 2003. Purification and characterization of a chimeric enzyme from Haemophilus influenzae Rd that exhibits glutathione-dependent peroxidase activity. J. Biol. Chem. 275:16658-16666.
31. Penninckx, M. 2000. A short review on the role of glutathione in the response of yeasts to nutritional, environmental, and oxidative stresses. Enzyme Microb. Technol. 26:737-742.
32. Potamitou, A., A. Holmgren, and A. Vlamis-Gardikas. 2002. Protein levels of Escherichia coli thioredoxins and glutaredoxins and their relation to null mutants, growth phase, and function. J. Biol. Chem. 277:18561-18567.
33. Regelsberger, G., C. Obinger, R. Zoder, F. Altmann, and G. A. Peschek. 1999. Purification and characterization of a hydroperoxidase from the cyanobacterium Synechocystis PCC 6803: identification of its gene by peptide mass mapping using matrix assisted laser desorption ionization time-of-flight mass spectrometry. FEMS Microbiol. Lett. 170:1-12.
34. Rocha, E. R., and C. J. Smith. 1999. Role of the alkyl hydroperoxide reductase (ahpCF) gene in oxidative stress defense of the obligate anaerobe Bacteroides fragilis. J. Bacteriol. 181:5701-5710.
35. Sasaki, K., S. Bannai, and N. Makino. 1998. Kinetics of hydrogen peroxide elimination by human umbilical vein endothelial cells in culture. Biochim. Biophys. Acta 1380:275-288.
36. 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.
37. Seaver, L. C., and J. A. Imlay. 2001. Hydrogen peroxide fluxes and compartmentalization inside growing Escherichia coli. J. Bacteriol. 183:7182-7189.
38. Tartaglia, L. A., G. Storz, and B. N. Ames. 1989. Identification and molecular analysis of oxyR-regulated promoters important for the bacterial adaptation to oxidative stress. J. Mol. Biol. 210:709-719.
39. Triggs-Raine, B. L., B. W. Doble, M. R. Mulvey, P. A. Sorby, and P. C. Loewen. 1988. Nucleotide sequence of katG, encoding catalase HPI of Escherichia coli. J. Bacteriol. 170:4415-4419.
40. Ursini, M. V., A. Parrella, G. Rosa, S. Salzano, and G. Martini. 1997. Enhanced expression of glucose-6-phosphate dehydrogenase in human cells sustaining oxidative stress. Biochem. J. 323:801-806.
41. Varma, S. D., and S. M. Morris. 1988. Peroxide damage to the eye lens in vitro prevention by pyruvate. Free Radic. Res. Commun. 4:283-290.
42. Vergauwen, B., F. Pauwels, M. Vaneechoutte, and J. J. Van Beeumen. 2003. Exogenous glutathione completes the defense against oxidative stress in Haemophilus influenzae. J. Bacteriol. 185:1572-1581.
43. Vergauwen, B., F. Pauwels, F. Jacquemotte, T. E. Meyer, M. A. Cusanovich, R. G. Bartsch, and J. J. Van Beeumen. 2001. Characterization of glutathione amide reductase from Chromatium gracile: identification of a novel thiol peroxidase (Prx/Grx) fueled by glutathione amide redox cycling. J. Biol. Chem. 276:20890-20897.
44. Vlamis-Gardikas, A., A. Potamitou, R. Zarivach, A. Hochman, and A. Holmgren. 2002. Characterization of Escherichia coli null mutants for glutaredoxin 2. J. Biol. Chem. 277:10861-10868.
45. von Ossowski, I., M. R. Mulvey, P. A. Leco, A. Borys, and P. C. Loewen. 1991. Nucleotide sequence of Escherichia coli katE, which encodes catalase HPII. J. Bacteriol. 173:514-520.