Ubiquinone limits oxidative stress in Escherichia coli

Microbiology

Volumn 146, Issue 4, 2000, Pages 787-796

  Søballe, Britta ^a   Poole, Robert K ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Escherichia coli; Oxidative stress; Peroxide; Superoxide; Ubiquinone

Indexed keywords

CATALASE; CYSTEINE; HYDROGEN PEROXIDE; UBIQUINONE;

ARTICLE; BACTERIAL MEMBRANE; BACTERIUM MUTANT; ENZYME ACTIVITY; ESCHERICHIA COLI; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; MAMMALIA; NEGIBACTERIA; PROKARYOTA;

EID: 0034088408     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/00221287-146-4-787     Document Type: Article

References (46)

1. Afanas'ev, I. B., Korkina, L. G., Suslova, T. B. & Soodaeva, S. K. (1990). Are quinones producers or scavengers of superoxide ion in cells? Arch Biochem Biophys 281, 245-250.
2. Bader, M., Muse, W., Ballou, D. P., Gassner, C. & Bardwell, C. A. (1999). Oxidative protein folding is driven by the electron transport system. Cell 98, 217-227.
3. Beyer, R. E., Segura-Aguilar, J., Di Bernard, S. & 7 other authors (1996). The role of DT-diaphorase in the maintenance of the reduced antioxidant form of coenzyme Q in membrane systems. Proc Natl Acad Sci USA 93, 2528-2532.
4. Collis, C. M. & Grigg, G. W. (1989). An Escherichia coli mutant resistant to phleomycin, bleomycin and heat inactivation is defective in ubiquinone synthesis. J Bacteriol 171, 4792-4798.
5. Compan, I. & Touati, D. (1993). Interaction of six global regulators in expression of manganese superoxide dismutase in Escherichia coli K-12. J Bacteriol 175, 1687-1696.
6. Demple, B. (1991). Regulation of bacterial oxidative stress genes. Annu Rev Genet 25, 315-337.
7. D'mello, R., Hill, S. & Poole, R. K. (1996). The cytochrome bd quinol oxidase in Escherichia coli has an extremely high oxygen affinity and two oxygen-binding haems: implications for regulation of activity in vivo by oxygen inhibition. Microbiology 142, 755-763.
8. Do, T. Q., Schultz, J. R. & Clarke, C. (1996). Enhanced sensitivity of ubiquinone-deficient mutants of Saccharomyces cerevisiae to products of autoxidized polyunsaturated fatty acids. Proc Natl Acad Sci USA 93, 7534-7539.
9. Ernster, L. & Daliner, G. (1995). Biochemical, physiological and medical aspects of ubiquinone function. Biochim Biophys Acta 1271, 195-204.
10. Forsmark-Andrée, P., Dallner, G. & Ernster, L. (1995). Endogenous ubiquinol prevents protein modification accompanying lipid peroxidation in beef heart submitochondrial particles. Free Radic Biol Med 19, 749-757.
11. Gennis, R. B. & Stewart, V. (1996). Respiration. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn, pp. 217-261. Edited by F. C. Neidhardt and others. Washington, DC: American Society for Microbiology.
12. Goldman, B. S., Gabbert, K. K. & Kranz, R. G. (1996a). Use of heme reporters for studies of cytochrome biosynthesis and heme transport. J Bacteriol 178, 6338-6347.
13. Goldman, B. S., Gabbert, K. K. & Kranz, R. G. (1996b). The temperature-sensitive growth and survival phenotypes of Escherichia coli cydDC and cydAB strains are due to deficiencies in cytochrome bd and are corrected by exogenous catalase and reducing agents. J Bacteriol 178, 6348-6351.
14. Gonzalez-Flecha, B. & Demple, B. (1994). Intracellular generation of superoxide as a by-product of Vibrio harveyi luciferase expressed in Escherichia coli. J Bacteriol 176, 2293-2299.
15. Gonzalez-Flecha, B. & Demple, B. (1995). Metabolic sources of hydrogen peroxide in aerobically growing Escherichia coli. J Biol Chem 270, 13681-13687.
16. Hsu, A., Poon, W. W., Shepherd, J. A., Myles, D. C. & Clarke, C. (1996). Complementation of coq3 mutant yeast by mitochondrial targeting of the Escherichia coli UbiG polypeptide: evidence that UbiG catalyzes both O-methylation steps in ubiquinone biosynthesis. Biochemistry 35, 9797-9806.
17. Imlay, J. A. (1995). A metabolic enzyme that rapidly produces superoxide, fumarate reductase of Escherichia coli. J Biol Chem 270, 19767-19777.
18. Imlay, J. A. & Fridovich, I. (1991). Assay of metabolic superoxide production in Escherichia coli. J Biol Chem 266, 6957-6965.
19. Kalén, A., Norling, B., Appelkvist, E.-L. & Dallner, G. (1989). Ubiquinone biosynthesis by the microsomal fraction from rat liver. Biochim Biophys Acta 926, 70-78.
20. Kimura, T. & Nishioka, H. (1997). Intracellular generation of superoxide by copper sulphate in Escherichia coli. Mutation Res 389, 237-242.
21. Kobayashi, T. & Ito, K. (1999). Respiratory chain strongly oxidizes the CXXC motif of DsbB in the Escherichia coli disulfide bond formation pathway. EMBO J 18, 1192-1198.
22. Kobayashi, T., Kishigama, S., Sone, M., Inokuchi, H., Mogi, T. & Ito, K. (1997). Respiratory chain is required to maintain oxidised states of the DsbA-DsbB disulfide bond formation system in aerobically growing Escherichia coli. Proc Natl Acad Sci USA 94, 11857-11862.
23. 2 production in pigeon heart mitochondria. FEBS Lett 18, 261-264.
24. Markwell, M. A. K., Haas, S. M., Bieber, L. L. & Tolbert, N. E. (1978). A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal Biochem 87, 206-210.
25. Messner, K. R. & Imlay, J. A. (1999). The identification of primary sites of superoxide and hydrogen peroxide formation in the aerobic respiratory chain and sulfite reductase complex of Escherichia coli. J Biol Chem 274, 10119-10128.
26. Missiakas, D. & Raina, S. (1997). Protein folding in the bacterial periplasm. J Bacteriol 179, 2465-2471.
27. Nakayama, T., Hashimoto, M. & Hashimoto, K. (1997). Superoxide dismutase inhibition of oxidation of ubiquinol and concomitant formation of hydrogen peroxide. Biosci Biotechnol Biochem 61, 2034-2038.
28. Okada, K., Kainou, T., Matsuda, H. & Kawamukai, M. (1998). Biological significance of the side chain length in Saccharomyces cerevisiae. FEBS Lett 431, 241-244.
29. Olsson, J. M., Xia, L., Eriksson, L. C. & Bjornstedt, M. (1999). Ubiquinone is reduced by lipoamide dehydrogenase and this reaction is potently stimulated by zinc. FEBS Lett 448, 190-192.
30. Papa, S., Guerrieri, F. & Capitanio, N. (1997). A possible role of slips in cytochrome c oxidase in the antioxygen defense system of the cell. Biosci Rep 17, 23-31.
31. Poole, R. K. & Ingledew, W. J. (1987). Pathways of electrons to oxygen. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology, pp. 170-200. Edited by F. C. Neidhardt and others. Washington, DC: American Society for Microbiology.
32. Poole, R. K., Anjum, M. F., Membrillo-Hernández, J., Kim, S. O., Hughes, M. N. & Stewart, V. (1996). Nitric oxide, nitrite, and Fnr regulation of hmp (flavohemoglobin) gene expression in Escherichia coli K-12. J Bacteriol 178, 5487-5492.
33. Poon, W. W., Barkovich, R. J., Hsu, A. Y., Frankel, A., Lee, P. T., Shepherd, J. N., Myles, D. C. & Clarke, C. F. (1999). Yeast and rat Coq3 and Escherichia coli UbiG polypeptides catalyze both O-methyltransferase steps in coenzyme Q biosynthesis. J Biol Chem 274, 21665-21672.
34. Rosner, J. L. & Storz, G. (1997). Regulation of bacterial responses to oxidative stress. Curr Top Cell Regul 35, 163-175.
35. Skulachev, V. P. (1997). Membrane-linked systems preventing superoxide formation. Biosci Rep 17, 347-366.
36. Søballe, B. & Poole, R. K. (1997). Aerobic and anaerobic regulation of the ubiCA operon, encoding the first two committed steps of ubiquinone biosynthesis in Escherichia coli. FEBS Lett 414, 373-376.
37. Søballe, B. & Poole, R. K. (1998). Requirement for ubiquinone downstream of cytochrome(s) b in the oxygen-terminated respiratory chains of Escherichia coli K-12 revealed using a null mutant allele of ubiCA. Microbiology 144, 361-373.
38. Søballe, B. & Poole, R. K. (1999). Microbial ubiquinones: multiple roles in respiration, gene regulation and oxidative stress management. Microbiology 145, 1817-1830.
39. Stroobant, P., Young, I. G. & Gibson, F. (1972). Mutants of Escherichia coli K-12 blocked in the final reaction of ubiquinone biosynthesis: characterization and genetic analysis. J Bacteriol 109, 134-139.
40. Suzuki, K., Okada, K., Kamiya, Y., Zhu, X. F., Nakagawa, T., Kawamukai, M. & Matsuda, H. (1997). Analysis of the decaprenyl diphosphate synthase (dps) gene in fission yeast suggests a role of ubiquinone as an antioxidant. J Biochem 121, 496-505.
41. Thorn, J. M., Barton, J. D., Dixon, N. E., Ollis, D. L. & Edwards, K. J. (1995). Crystal structure of Escherichia coli QOR quinone oxidoreductase complexed with NADPH. J Mol Biol 249, 785-799.
42. Touati, D. (1988). Transcriptional and posttranscriptional regulation of manganese superoxide dismutase biosynthesis in Escherichia coli, studied with operon and protein fusions. J Bacteriol 170, 2511-2520.
43. Wall, D., Delaney, J. M., Fayet, O., Lipinska, B., Yamamoto, T. & Georgopoulos, C. (1992). arc-dependent thermal regulation and extragenic suppression of the Escherichia coli cytochrome d operon. J Bacteriol 174, 6554-6562.
44. Wallace, B. J. & Young, I. G. (1977). Role of quinones in electron transport to oxygen and nitrate in Escherichia coli: studies with a double quinone mutant. Biochim Biophys Acta 461, 84-100.
45. Wu, G., Williams, H. D., Zamanian, M., Gibson, F. & Poole, R. K. (1992). Isolation and characterization of Escherichia coli mutants affected in aerobic respiration: the cloning and nucleotide sequence of ubiG. Identification of an S-adenosylmethionine-binding motif in proteins, RNA, and small-molecule methyltransferases. J Gen Microbiol 138, 2101-2112.
46. Zeng, H., Snavely, P., Zamorano, P. & Javor, G. T. (1998). Low ubiquinone content in Escherichia coli causes thiol hypersensitivity. J Bacteriol 180, 3681-3685.