Oxidative protein damage causes chromium toxicity in yeast

Microbiology

Volumn 151, Issue 6, 2005, Pages 1939-1948

  Sumner, Edward R ^a   Shanmuganathan, Anupama ^b   Sideri, Theodora C ^a   Willets, Sylvia A ^a   Houghton, John E ^b   Avery, Simon V ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b GEORGIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBONYL DERIVATIVE; CHROMIUM; COPPER ZINC SUPEROXIDE DISMUTASE; FUNGAL DNA; FUNGAL PROTEIN; GLYCOLYTIC ENZYME; HEAT SHOCK PROTEIN; HYDROPEROXIDE DERIVATIVE; METHIONINE SULFOXIDE REDUCTASE; PROTEIN SOD1; UNCLASSIFIED DRUG;

ARTICLE; BACTERIUM MUTANT; CARBONYLATION; CYTOTOXICITY; ENZYME ACTIVITY; GENE OVEREXPRESSION; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MODIFICATION; SACCHAROMYCES CEREVISIAE; YEAST CELL;

AEROBIOSIS; ANAEROBIOSIS; CHROMIUM; DNA GLYCOSYLASES; DNA REPAIR; DNA-DIRECTED DNA POLYMERASE; GENE DELETION; GLUTATHIONE PEROXIDASE; OXIDATION-REDUCTION; OXIDOREDUCTASES; PHOSPHOLIPIDS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUPEROXIDE DISMUTASE;

SACCHAROMYCES CEREVISIAE;

EID: 21344466558     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.27945-0     Document Type: Article

References (53)

1. Ackerley, D. F., Gonzalez, C. F., Keyhan, M., Blake, R. & Matin, A. (2004). Mechanism of chromate reduction by the Escherichia coli protein, NfsA, and the role of different chromate reductases in minimizing oxidative stress during chromate reduction. Environ Microbiol 6, 851-860.
2. Aiyar, J., Berkovits, H. J., Floyd, R. A. & Wetterhahn, K. E. (1991). Reaction of chromium(VI) with glutathione or with hydrogen peroxide: identification of reactive intermediates and their role in chromium(VI)-induced DNA damage. Environ Health Perspect 92, 53-62.
3. Ausubel, F., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A. & Struhl, K. (2004). Current Protocols in Molecular Biology. New York: Wiley.
4. Avery, A. M. & Avery, S. V. (2001). Saccharomyces cerevisiae expresses three phospholipid hydroperoxide glutathione peroxidases. J Biol Chem 276, 33730-33735.
5. Avery, A. M., Willetts, S. A. & Avery, S. V. (2004). Genetic dissection of the phospholipid hydroperoxidase activity of yeast Gpx3 reveals its functional importance. J Biol Chem 279, 46652-46658.
6. Avery, S. V. (2001). Metal toxicity in yeasts and the role of oxidative stress. Adv Appl Microbiol 49, 111-142.
7. Avery, S. V., Howlett, N. G. & Radice, S. (1996). Copper toxicity towards Saccharomyces cerevisiae: dependence on plasma-membrane fatty acid composition. Appl Environ Microbiol 62, 3960-3966.
8. Cabiscol, E., Piulats, E., Echave, P., Herrero, E. & Ros, J. (2000). Oxidative stress promotes specific protein damage in Saccharomyces cerevisiae. J Biol Chem 275, 27393-27398.
9. Cervantes, C., Campos-Garcia, J., Devars, S., Gutierrez-Corona, F., Loza-Tavera, H., Torres-Guzman, J. C. & Moreno-Sanchez, R. (2001). Interactions of chromium with microorganisms and plants. FEMS Microbiol Rev 25, 335-347.
10. Cheng, L., Liu, S. J. & Dixon, K. (1998). Analysis of repair and mutagenesis of chromium-induced DNA damage in yeast, mammalian cells, and transgenic yeast. Environ Health Perspect Suppl 4 106, 1027-1032.
11. Ciriolo, M. R., Civitareale, P., Carri, M. T., Demartino, A., Galiazzo, F. & Rotilio, G. (1994). Purification and characterization of Ag,Zn-superoxide dismutase from Saccharomyces cerevisiae exposed to silver. J Biol Chem 269, 25783-25787.
12. Costa, W. M. V., Amorim, M. A., Quintanilha, A. & Moraclas-Ferreira, P. (2002). Hydrogen peroxide-induced carbonylation of key metabolic enzymes in Saccharomyces cerevisiae: the involvement of the oxidative stress response regulators Yap1 and Skn7. Free Rad Biol Med 33, 1507-1515.
13. Culotta, V. C., Joh, H. D., Lin, S. J., Slekar, K. H. & Strain, J. (1995). A physiological role for Saccharomyces cerevisiae copper/zinc superoxide dismutase in copper buffering. J Biol Chem 270, 29991-29997.
14. Dayan, A. D. & Paine, A. J. (2001). Mechanisms of chromium toxicity, carcinogenicity and allergenicity: review of the literature from 1985 to 2000. Human Exp Toxicol 20, 439-451.
15. 2 receptor and redox-transducer in gene activation. Cell 111, 471-481.
16. Feng, W. Y., Li, B., Liu, J., Chai, Z. F., Zhang, P. Q., Gao, Y. X. & Zhao, J. J. (2003). Study of chromium-containing proteins in subcellular fractions of rat liver by enriched stable isotopic tracer technique and gel filtration chromatography. Anal Bioanal Chem 375, 363-368.
17. Fernandes, M. A. S., Santos, M. S., Alpoim, M. C., Madeira, V. M. C. & Vicente, J. A. F. (2002). Chromium(VI) interaction with plant and animal mitochondrial bioenergetics: a comparative study. J Biochem Mol Toxicol 16, 53-63.
18. Gadd, G. M. (1992). Metals and microorganisms - a problem of definition. FEMS Microbiol Lett 100, 197-203.
19. Gietz, R. D. & Woods, R. A. (2002). Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol 350, 87-96.
20. 2 stimulon in Saccharomyces cerevisiae. J Biol Chem 273, 22480-22489.
21. Grune, T., Reinheckel, T. & Davies, K. J. A. (1997). Degradation of oxidized proteins in mammalian cells. Faseb J 11, 526-534.
22. Halliwell, B. & Gutteridge, J. M. C. (1999). Free Radicals in Biology and Medicine, 3rd edn. Oxford: Oxford University Press.
23. Haracska, L., Yu, S. L., Johnson, R. E., Prakash, L. & Prakash, S. (2000). Efficient and accurate replication in the presence of 7,8-dihydro-8-oxoguanine by DNA polyrnerase η. Nat Genet 25, 458-461.
24. Henderson, G. (1989). A comparison of the effects of chromate, molybdate and cadmium oxide on respiration in the yeast Saccharomyces cerevisiae. Biol Met 2, 83-88.
25. Hodges, N. J. & Chipman, J. K. (2002). Down-regulation of the DNA-repair endonuclease 8-oxo-guanine DNA glycosylase I (hOGGI) by sodium dichromate in cultured human A549 lung carcinoma cells. Carcinogenesis 23, 55-60.
26. Howlett, N. G. & Avery, S. V. (1997). Induction of lipid peroxidation during heavy metal stress in Saccharomyces cerevisiae and influence of plasma membrane fatty acid unsaturation. Appl Environ Microbiol 63, 2971-2976.
27. Jamieson, D. J. (1998). Oxidative stress responses of the yeast Saccharomyces cerevisiae. Yeast 14, 1511-1527.
28. Kasprzak, K. S. (2002). Oxidative DNA and protein damage in metal-induced toxicity and carcinogenesis. Free Rad Biol Med 32, 958-967.
29. Kim, Y. H., Berry, A. H., Spencer, D. S. & Stites, W. E. (2001). Comparing the effect on protein stability of methionine oxidation versus mutagenesis: steps toward engineering oxidative resistance in proteins. Prot Eng 14, 343-347.
30. Koc, A., Gasch, A. P., Rutherford, J. C., Kim, H. Y. & Gladyshev, V. N. (2004). Methionine sulfoxide reductase regulation of yeast lifespan reveals reactive oxygen species-dependent and -independent components of aging. Proc Natl Acad Sci U S A 101, 7999-8004.
31. Kryukov, G. V., Kumar, R. A., Koc, A., Sun, Z. H. & Gladyshev, V. N. (2002). Selenoprotein R is a zinc-containing stereo-specific methionine sulfoxide reductase. Proc Natl Acad Sci U S A 99, 4245-4250.
32. Levine, R. L., Moskovitz, J. & Stadtman, E. R. (2000). Oxidation of methionine in proteins: roles in antioxidant defense and cellular regulation. IUBMB Life 50, 301-307.
33. Lu, Y., Roe, J. A., Bender, C. J., Peisach, J., Banci, L., Bertini, I., Gralla, E. B. & Valentine, J. S. (1996). New type 2 copper-cysteinate proteins. Copper site histidine-to-cysteine mutants of yeast copper-zinc superoxide dismutase. Inorg Chem 35, 1692-1700.
34. Luo, H., Lu, Y., Shi, X., Mao, Y. & Delal, N. S. (1996). Chromium (IV)-mediated Fenton-like reaction causes DNA damage: implication to genotoxicity of chromate. Ann Clin Lab Sci 26, 185-191.
35. Moradas-Ferreira, P., Costa, V., Piper, P. & Mager, W. (1996). The molecular defences against reactive oxygen species in yeast. Mol Microbiol 19, 651-658.
36. Nguyen-Nhu, N. T. & Knoops, B. (2002). Alkyl hydroperoxide reductase 1 protects Saccharomyces cerevisiae against metal ion toxicity and glutathione depletion. Toxicol Lett 135, 219-228.
37. Nishida, C. R., Gralla, E. B. & Valentine, J. S. (1994). Characterization of three yeast copper-zinc superoxide dismutase mutants analogous to those coded for in familial amyotrophic lateral sclerosis. Proc Natl Acad Sci U S A 91, 9906-9910.
38. O'Brien, T., Xu, J. & Patierno, S. R. (2001). Effects of glutathione on chromium-induced DNA crosslinking and DNA polymerase arrest. Mol Cell Biochem 222, 173-182.
39. O'Brien, T. J., Fornsaglio, J. L., Ceryak, S. & Patierno, S. R. (2002). Effects of hexavalent chromium on the survival and cell cycle distribution of DNA repair-deficient S. cerevisiae. DNA Repair 1, 617-627.
40. Pesti, M., Gazdag, Z., Emri, T., Farkas, N., Koosz, Z., Belagy, J. & Pocsi, I. (2002). Chromate sensitivity in fission yeast is caused by increased glutathione reductase activity and peroxide overproduction. J Basic Microbiol 42, 408-419.
41. Pourahmad, J. & O'Brien, P. J. (2001). Biological reactive intermediates that mediate chromium (VI) toxicity. Biol React Intermed VI Adv Exp Med Biol 500, 203-207.
42. Ravichandran, V., Seres, T., Moriguchi, T., Thomas, J. A. & Johnston, R. B. (1994). S-thiolation of glyceraldehyde-3-phosphate dehydrogenase induced by the phagocytosis-associated respiratory burst in blood monocytes. J Biol Chem 269, 25010-25015.
43. Requena, J. R., Chao, C. C., Levine, R. L. & Stadtman, E. R. (2001). Glutamic and aminoadipic semialdehydes are the main carbonyl products of metal-catalyzed oxidation of proteins. Proc Natl Acad Sci U S A 98, 69-74.
44. Reynolds, M., Peterson, E., Quievryn, G. & Zhitkovich, A. (2004). Human nucleotide excision repair efficiently removes chromium-DNA phosphate adducts and protects cells against chromate toxicity. J Biol Chem 279, 30419-30424.
45. Shanmuganathan, A., Avery, S. V., Willetts, S. A. & Houghton, J. E. (2004). Copper-induced oxidative stress in Saccharomyces cerevisiae targets enzymes of the glycolytic pathway. FEBS Lett 556, 253-259.
46. Shenton, D. & Grant, C. M. (2003). Protein S-thiolation targets glycolysis and protein synthesis in response to oxidative stress in the yeast Saccharomyces cerevisiae. Biochem J 374, 513-519.
47. Shrivastava, H. Y. & Nair, B. U. (2000). Protein degradation by peroxide catalyzed by chromium (III): role of coordinated ligand. Biochem Biophys Res Commun 270, 749-754.
48. Shrivastava, H. Y. & Nair, B. U. (2004). Fluorescence resonance energy transfer from tryptophan to a chromium(III) complex accompanied by non-specific cleavage of albumin: a step forward towards the development of a novel photoprotease. J Inorg Biochem 98, 991-994.
49. Sumner, E. R., Avery, A. M., Houghton, J. E., Robins, R. A. & Avery, S. V. (2003). Cell cycle- and age-dependent activation of Sod1p drives the formation of stress-resistant cell subpopulations within clonal yeast cultures. Mol Microbiol 50, 857-870.
50. Swanson, R. L., Morey, N. J., Doetsch, P. W. & Jinks-Robertson, S. (1999). Overlapping specificities of base excision repair, nucleotide excision repair, recombination, and translesion synthesis pathways for DNA base damage in Saccharomyces cerevisiae. Mol Cell Biol 19, 2929-2935.
51. Wei, J. P. J., Srinivasan, C., Han, H., Valentine, J. S. & Gralla, E. B. (2001). Evidence for a novel role of copper-zinc superoxide dismutase in zinc metabolism. J Biol Chem 276, 44798-44803.
52. White, C., Sharman, A. K. & Gadd, G. M. (1998). An integrated microbial process for the bioremediation of soil contaminated with toxic metals. Nat Biotechnol 16, 572-575.
53. Willetts, S. A. (2004). Genetic and genomic approaches to understanding metal toxicity in Saccharomyces cerevisiae. PhD thesis, University of Nottingham.