Cytosolic superoxide dismutase (SOD1) is critical for tolerating the oxidative stress of zinc deficiency in yeast

PLoS ONE

Volumn 4, Issue 9, 2009, Pages

  Wu, Chang Yi ^a   Steffen, Janet ^a   Eide, David J ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; CATALASE; CHAPERONE; COPPER; COPPER ZINC SUPEROXIDE DISMUTASE; CYTOCHROME C PEROXIDASE; GLUTAREDOXIN; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; GLUTATHIONE TRANSFERASE; MANGANESE SUPEROXIDE DISMUTASE; PEROXIREDOXIN; PROTEIN AHP1; PROTEIN DOT5; PROTEIN PRX1; PROTEIN TSA1; PROTEIN TSA2; REACTIVE OXYGEN METABOLITE; SULFIREDOXIN; THIOREDOXIN; THIOREDOXIN REDUCTASE; UNCLASSIFIED DRUG; ZINC; CCS1 PROTEIN, S CEREVISIAE; HYDROGEN PEROXIDE; SACCHAROMYCES CEREVISIAE PROTEIN; SUPEROXIDE DISMUTASE;

ARTICLE; CONTROLLED STUDY; CYTOSOL; ENZYME ACTIVITY; GENE OVEREXPRESSION; GROWTH; METALLATION; NONHUMAN; OXIDATIVE STRESS; PROTEIN DEPLETION; PROTEIN FUNCTION; YEAST; ZINC DEFICIENCY; CHEMISTRY; ENZYMOLOGY; GENE EXPRESSION REGULATION; METABOLISM; MUTATION; SACCHAROMYCES CEREVISIAE;

SACCHAROMYCES CEREVISIAE;

ANTIOXIDANTS; CYTOSOL; GENE EXPRESSION REGULATION, FUNGAL; HYDROGEN PEROXIDE; MOLECULAR CHAPERONES; MUTATION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUPEROXIDE DISMUTASE; ZINC;

EID: 70349487306     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0007061     Document Type: Article

References (49)

1. Hao Q, Maret W (2005) Imbalance between pro-oxidant and pro-antioxidant functions of zinc in disease. J Alzheimers Dis 8: 161-170; discussion 209-115.
2. Powell SR (2000) The antioxidant properties of zinc. J Nutr 130: 1447S-1454S.
3. Bossy-Wetzel E, Talantova MV, Lee WD, Scholzke MN, Harrop A, et al. (2004) Crosstalk between nitric oxide and zinc pathways to neuronal cell death involving mitochondrial dysfunction and p38-activated K+ channels. Neuron 41: 351-365.
4. Dineley KE, Richards LL, Votyakova TV, Reynolds IJ (2005) Zinc causes loss of membrane potential and elevates reactive oxygen species in rat brain mitochondria. Mitochondrion 5: 55-65.
5. Ho E (2004) Zinc deficiency, DNA damage and cancer risk. J Nutr Biochem 15: 572-578.
6. Maret W (2007) Cellular zinc and redox buffering capacity of metallothionein/thionein in health and disease. Mol Med 13: 371-375.
7. Burke JP, Fenton MR (1985) Effect of a zinc-deficient diet on lipid peroxidation in liver and tumor subcellular membranes. Proc Soc Exp Biol Med 179: 187-191.
8. Oteiza PI, Olin KL, Fraga CG, Keen CL (1995) Zinc deficiency causes oxidative damage to proteins, lipids and DNA in rat testes. J Nutr 125: 823-829.
9. Ho E, Ames BN (2002) Low intracellular zinc induces oxidative DNA damage, disrupts p53, NFkappa B, and AP1 DNA binding, and affects DNA repair in a rat glioma cell line. Proc Natl Acad Sci U S A 99: 16770-16775.
10. Ho E, Courtemanche C, Ames BN (2003) Zinc deficiency induces oxidative DNA damage and increases p53 expression in human lung fibroblasts. J Nutr 133: 2543-2548.
11. Ames BN, Wakimoto P (2002) Are vitamin and mineral deficiencies a major cancer risk? Nat Rev Cancer 2: 694-704.
12. International Zinc Consultative Group (2004) Assessment of the risk of zinc deficiency in populations and options for its control. Food Nutr Bull 25: S94-203.
13. Wu CY, Bird AJ, Winge DR, Eide DJ (2007) Regulation of the yeast TSA1 peroxiredoxin by ZAP1 is an adaptive response to the oxidative stress of zinc deficiency. J Biol Chem 282: 2184-2195.
14. Wu CY, Bird AJ, Chung LM, Newton MA, Winge DR, et al. (2008) Differential control of Zap1-regulated genes in response to zinc deficiency in Saccharomyces cerevisiae. BMC Genomics 9: 370.
15. Eide DJ (2009) Homeostatic and Adaptive Responses to Zinc Deficiency in Saccharomyces cerevisiae. J Biol Chem 284: 18565-18569.
16. Wei JP, Srinivasan C, Han H, Valentine JS, Gralla EB (2001) Evidence for a novel role of copper-zinc superoxide dismutase in zinc metabolism. J Biol Chem 276: 44798-44803.
17. Gitan RS, Luo H, Rodgers J, Broderius M, Eide D (1998) Zinc-induced inactivation of the yeast ZRT1 zinc transporter occurs through endocytosis and vacuolar degradation. J Biol Chem 273: 28617-28624.
18. Luk E, Yang M, Jensen LT, Bourbonnais Y, Culotta VC (2005) Manganese activation of superoxide dismutase 2 in the mitochondria of Saccharomyces cerevisiae. J Biol Chem 280: 22715-22720.
19. Carroll MC, Girouard JB, Ulloa JL, Subramaniam JR, Wong PC, et al. (2004) Mechanisms for activating Cu- and Zn-containing superoxide dismutase in the absence of the CCS Cu chaperone. Proc Natl Acad Sci U S A 101: 5964-5969.
20. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
21. Gralla EB, Kosman DJ (1992) Molecular genetics of superoxide dismutases in yeasts and related fungi. Adv Genet 30: 251-319.
22. Culotta VC, Klomp LWJ, Strain J, Casareno RLB, Krems B, et al. (1997) The copper chaperone for superoxide dismutase. J Biol Chem 272: 23469-23472.
23. Rae TD, Schmidt PJ, Pufahl RA, Culotta VC, O'Halloran TV (1999) Undetectable intracellular free copper: The requirement of a copper chaperone for superoxide dismutase. Science 284: 805-808.
24. Chang EC, Kosman DJ (1989) Intracellular Mn (II)-associated superoxide scavenging activity protects Cu,Zn superoxide dismutase-deficient Saccharomyces cerevisiae against dioxygen stress. J Biol Chem 264: 12172-12178.
25. Halliwell B, Whiteman M (2004) Measuring reactive species and oxidative damage in vivo and in cell culture: how should you do it and what do the results mean? Br J Pharmacol 142: 231-255.
26. Bermingham-McDonogh O, Gralla EB, Valentine JS (1988) The copper, zinc-superoxide dismutase gene of Saccharomyces cerevisiae: cloning, sequencing, and biological activity. Proc Natl Acad Sci U S A 85: 4789-4793.
27. Tan SX, Teo M, Lam YT, Dawes IW, Perrone GG (2009) Cu, Zn superoxide dismutase and NADP(H) homeostasis are required for tolerance of endoplasmic reticulum stress in Saccharomyces cerevisiae. Mol Biol Cell 20: 1493-1508.
28. Garay-Arroyo A, Lledias F, Hansberg W, Covarrubias AA (2003) Cu, Zn-superoxide dismutase of Saccharomyces cerevisiae is required for resistance to hyperosmosis. FEBS Lett 539: 68-72.
29. Davidson JF, Whyte B, Bissinger PH, Schiestl RH (1996) Oxidative stress is involved in heat-induced cell death in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 93: 5116-5121.
30. Park JI, Grant CM, Davies MJ, Dawes IW (1998) The cytoplasmic Cu,Zn superoxide dismutase of saccharomyces cerevisiae is required for resistance to freeze-thaw stress. Generation of free radicals during freezing and thawing. J Biol Chem 273: 22921-22928.
31. Longo VD, Gralla EB, Valentine JS (1996) Superoxide dismutase activity is essential for stationary phase survival in Saccharomyces cerevisiae. Mitochondrial production of toxic oxygen species in vivo. J Biol Chem 271: 12275-12280.
32. Ghaemmaghami S, Huh WK, Bower K, Howson RW, Belle A, et al. (2003) Global analysis of protein expression in yeast. Nature 425: 737-741.
33. Hoffman EK, Wilcox HM, Scott RW, Siman R (1996) Proteasome inhibition enhances the stability of mouse Cu/Zn superoxide dismutase with mutations linked to familial amyotrophic lateral sclerosis. J Neurol Sci 139: 15-20.
34. Kabuta T, Suzuki Y, Wada K (2006) Degradation of amyotrophic lateral sclerosis-linked mutant Cu,Zn-superoxide dismutase proteins by macroautophagy and the proteasome. J Biol Chem 281: 30524-30533.
35. Hart PJ (2006) Pathogenic superoxide dismutase structure, folding, aggregation and turnover. Curr Opin Chem Biol 10: 131-138.
36. Culotta VC, Yang M, O'Halloran TV (2006) Activation of superoxide dismutases: putting the metal to the pedal. Biochim Biophys Acta 1763: 747-758.
37. Beckman JS, Estevez AG, Crow JP, Barbeito L (2001) Superoxide dismutase and the death of motoneurons in ALS. Trends Neurosci 24: S15-20.
38. Trumbull KA, Beckman JS (2009) A role for copper in the toxicity of zinc-deficient superoxide dismutase to motor neurons in Amyotrophic Lateral Sclerosis. Antioxid Redox Signal, in press.
39. Furukawa Y, Kaneko K, Yamanaka K, O'Halloran TV, Nukina N (2008) Complete loss of post-translational modifications triggers fibrillar aggregation of SOD1 in the familial form of amyotrophic lateral sclerosis. J Biol Chem 283: 24167-24176.
40. Banci L, Bertini I, Durazo A, Girotto S, Gralla EB, et al. (2007) Metal-free superoxide dismutase forms soluble oligomers under physiological conditions: a possible general mechanism for familial ALS. Proc Natl Acad Sci U S A 104: 11263-11267.
41. Crow JP, Sampson JB, Zhuang Y, Thompson JA, Beckman JS (1997) Decreased zinc affinity of amyotrophic lateral sclerosis-associated superoxide dismutase mutants leads to enhanced catalysis of tyrosine nitration by peroxynitrite. J Neurochem 69: 1936-1944.
42. Estevez AG, Crow JP, Sampson JB, Reiter C, Zhuang Y, et al. (1999) Induction of nitric oxide-dependent apoptosis in motor neurons by zinc-deficient superoxide dismutase. Science 286: 2498-2500.
43. Ermilova IP, Ermilov VB, Levy M, Ho E, Pereira C, et al. (2005) Protection by dietary zinc in ALS mutant G93A SOD transgenic mice. Neurosci Lett 379: 42-46.
44. Furukawa Y, O'Halloran TV (2005) Amyotrophic lateral sclerosis mutations have the greatest destabilizing effect on the apo- and reduced form of SOD1, leading to unfolding and oxidative aggregation. J Biol Chem 280: 17266-17274.
45. Deng HX, Shi Y, Furukawa Y, Zhai H, Fu R, et al. (2006) Conversion to the amyotrophic lateral sclerosis phenotype is associated with intermolecular linked insoluble aggregates of SOD1 in mitochondria. Proc Natl Acad Sci U S A 103: 7142-7147.
46. Furukawa Y, Fu R, Deng HX, Siddique T, O'Halloran TV (2006) Disulfide cross-linked protein represents a significant fraction of ALS-associated Cu, Zn-superoxide dismutase aggregates in spinal cords of model mice. Proc Natl Acad Sci U S A 103: 7148-7153.
47. Taysi S, Cikman O, Kaya A, Demircan B, Gumustekin K, et al. (2008) Increased oxidant stress and decreased antioxidant status in erythrocytes of rats fed with zinc-deficient diet. Biol Trace Elem Res 123: 161-167.
48. Sun JY, Jing MY, Weng XY, Fu LJ, Xu ZR, et al. (2005) Effects of dietary zinc levels on the activities of enzymes, weights of organs, and the concentrations of zinc and copper in growing rats. Biol Trace Elem Res 107: 153-165.
49. Lyons TJ, Gasch AP, Gaither LA, Botstein D, Brown PO, et al. (2000) Genome-wide characterization of the Zap1p zinc-responsive regulon in yeast. Proc Natl Acad Sci USA 97: 7957-7962.