Cu, Zn superoxide dismutase and NADP(H)homeostasis are required for tolerance of endoplasmic reticulum stress in Saccharomyces cerevisiae

Molecular Biology of the Cell

Volumn 20, Issue 5, 2009, Pages 1493-1508

  Tan, Shi Xiong ^a   Teo, Mariati ^a   Lam, Yuen T ^a   Dawes, Ian W ^a   Perrone, Gabriel G ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; DITHIOTHREITOL; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; TUNICAMYCIN;

ARTICLE; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; HOMEOSTASIS; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SACCHAROMYCES CEREVISIAE;

CELL SURVIVAL; DITHIOTHREITOL; ENDOPLASMIC RETICULUM; GENE DELETION; GLUTATHIONE; GLYCOPROTEINS; HOMEOSTASIS; MOLECULAR CHAPERONES; NADP; OXIDOREDUCTASES ACTING ON SULFUR GROUP DONORS; OXYGEN; PENTOSE PHOSPHATE PATHWAY; PROTEIN FOLDING; REACTIVE OXYGEN SPECIES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; STRESS, PHYSIOLOGICAL; SUPEROXIDE DISMUTASE; TRANSKETOLASE; TUNICAMYCIN;

SACCHAROMYCES CEREVISIAE;

EID: 65249134998     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E08-07-0697     Document Type: Article

References (74)

1. Alic, N., Felder, T., Temple, M. D., Gloeckner, C., Higgins, V. J., Briza, P., and Dawes, I. W.(2004). Genome-wide transcriptional responses to a lipid hydroperoxide: adaptation occurs without induction of oxidant defenses. Free Radic. Biol. Med. 37, 23-35.
2. Barnes, G., Hansen, W. J., Holcomb, C. L., and Rine, J.(1984). Asparagine-linked glycosylation in Saccharomyces cerevisiae: genetic analysis of an early step. Mol. Cell. Biol. 4, 2381-2388.
3. Bonilla, M., and Cunningham, K. W.(2003). Mitogen-activated protein kinase stimulation of Ca(2 +)signaling is required for survival of endoplasmic reticulum stress in yeast. Mol. Biol. Cell 14, 4296-4305.
4. Bonilla, M., Nastase, K. K., and Cunningham, K. W.(2002). Essential role of calcineurin in response to endoplasmic reticulum stress. EMBO J. 21, 2343-2353.
5. Chen, Y., Feldman, D. E., Deng, C., Brown, J. A., De Giacomo, A. F., Gaw, A. F., Shi, G., Le, Q. T., Brown, J. M., and Koong, A. C.(2005). Identification of mitogen-activated protein kinase signaling pathways that confer resistance to endoplasmic reticulum stress in Saccharomyces cerevisiae. Mol. Cancer Res. 3, 669-677.
6. Collinson, L. P., and Dawes, I. W.(1992). Inducibility of the response of yeast cells to peroxide stress. J. Gen. Microbiol. 138, 329-335.
7. Cox, J. S., Shamu, C. E., and Walter, P.(1993). Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell 73, 1197-1206.
8. Cox, J. S., and Walter, P.(1996). A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell 87, 391-404.
9. Culotta, V. C.(2000). Superoxide dismutase, oxidative stress, and cell metabolism. Curr. Top. Cell Regul. 36, 117-132.
10. Culotta, V. C., Klomp, L. W., Strain, J., Casareno, R. L., Krems, B., and Gitlin, J. D.(1997). The copper chaperone for superoxide dismutase. J. Biol. Chem. 272, 23469-23472.
11. Cuozzo, J. W., and Kaiser, C. A.(1999). Competition between glutathione and protein thiols for disulphide-bond formation. Nat. Cell Biol. 1, 130-135.
12. Deere, D., Shen, J., Vesey, G., Bell, P., Bissinger, P., and Veal, D.(1998). Flow cytometry and cell sorting for yeast viability assessment and cell selection. Yeast 14, 147-160.
13. Drakulic, T., Temple, M. D., Guido, R., Jarolim, S., Breitenbach, M., Attfield, P. V., and Dawes, I. W.(2005). Involvement of oxidative stress response genes in redox homeostasis, the level of reactive oxygen species, and ageing in Saccharomyces cerevisiae. FEMS Yeast Res. 12, 1215-1228.
14. Flattery-O'Brien, J., Collinson, L. P., and Dawes, I. W.(1993). Saccharomyces cerevisiae has an inducible response to menadione which differs from that to hydrogen peroxide. J. Gen. Microbiol. 139, 501-507.
15. Gao, C. Y., and Pinkham, J. L.(2000). Tightly regulated, beta-estradiol dose-dependent expression system for yeast. Biotechniques 29, 1226-1231.
16. Gibon, Y., and Larher, F.(1997). Cycling assay for nicotinamide adenine dinucleotides: NaCl precipitation and ethanol solubilization of the reduced tetrazolium. Anal. Biochem. 251, 153-157.
17. Gralla, E. B., and Valentine, J. S.(1991). Null mutants of Saccharomyces cerevisiae Cu, Zn superoxide dismutase: characterization and spontaneous mutation rates. J. Bacteriol. 173, 5918-5920.
18. Grant, C. M.(2001). Role of the glutathione/glutaredoxin and thioredoxin systems in yeast growth and response to stress conditions. Mol. Microbiol. 39, 533-541.
19. Grant, C. M., Collinson, L. P., Roe, J. H., and Dawes, I. W.(1996a). Yeast glutathione reductase is required for protection against oxidative stress and is a target gene for yAP-1 transcriptional regulation. Mol. Microbiol 21, 171-179.
20. Grant, C. M., MacIver, F. H., and Dawes, I. W.(1996b). Glutathione is an essential metabolite required for resistance to oxidative stress in the yeast Saccharomyces cerevisiae. Curr. Genet. 29, 511-515.
21. Grant, C. M., Perrone, G., and Dawes, I. W.(1998). Glutathione and catalase provide overlapping defenses for protection against hydrogen peroxide in the yeast Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 253, 893-898.
22. Gross, E., Sevier, C. S., Heldman, N., Vitu, E., Bentzur, M., Kaiser, C. A., Thorpe, C., and Fass, D.(2006). Generating disulfides enzymatically: reaction products and electron acceptors of the endoplasmic reticulum thiol oxidase Ero1p. Proc. Natl. Acad. Sci. USA 103, 299-304.
23. Harding, H. P. et al.(2003). An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell 11, 619-633.
24. Hauptmann, P., Riel, C., Kunz-Schughart, L. A., Frohlich, K. U., Madeo, F., and Lehle, L.(2006). Defects in N-glycosylation induce apoptosis in yeast. Mol. Microbiol 59, 765-778.
25. Haynes, C. M., Titus, E. A., and Cooper, A. A.(2004). Degradation of mis-folded proteins prevents ER-derived oxidative stress and cell death. Mol. Cell 15, 767-776.
26. Hermann, H., Hacker, U., Bandlow, W., and Magdolen, V.(1992). pYLZ vectors: Saccharomyces cerevisiae/Escherichia coli shuttle plasmids to analyze yeast promoters. Gene 119, 137-141.
27. Hiller, M. M., Finger, A., Schweiger, M., and Wolf, D. H.(1996). ER degradation of a misfolded luminal protein by the cytosolic ubiquitin-proteasome pathway. Science 273, 1725-1728.
28. Holmgren, A.(1989). Thioredoxin and glutaredoxin systems. J. Biol. Chem. 264, 13963-13966.
29. Huang, T. T., Raineri, I., Eggerding, F., and Epstein, C. J.(2002). Transgenic and mutant mice for oxygen free radical studies. Methods Enzymol. 349, 191-213.
30. Ito, H., Fukuda, Y., Murata, K., and Kimura, A.(1983). Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153, 163-168.
31. Jamieson, D. J.(1992). Saccharomyces cerevisiae has distinct adaptive responses to both hydrogen peroxide and menadione. J. Bacteriol. 174, 6678-6681.
32. Jamsa, E., Simonen, M., and Makarow, M.(1994). Selective retention of secretory proteins in the yeast endoplasmic reticulum by treatment of cells with a reducing agent. Yeast 10, 355-370.
33. Juhnke, H., Krems, B., Kotter, P., and Entian, K. D.(1996). Mutants that show increased sensitivity to hydrogen peroxide reveal an important role for the pentose phosphate pathway in protection of yeast against oxidative stress. Mol. Gen. Genet. 252, 456-464.
34. Kawahara, T., Yanagi, H., Yura, T., and Mori, K.(1997). Endoplasmic reticulum stress-induced mRNA splicing permits synthesis of transcription factor Hac1p/Ern4p that activates the unfolded protein response. Mol. Biol. Cell 8, 1845-1862.
35. Kimata, Y., Ishiwata-Kimata, Y., Yamada, S., and Kohno, K.(2006). Yeast unfolded protein response pathway regulates expression of genes for anti-oxidative stress and for cell surface proteins. Genes Cells 11, 59-69.
36. Kincaid, M. M., and Cooper, A. A.(2007). ERADicate ER stress or die trying. Antioxid. Redox Signal. 9, 2373-2387.
37. Kukuruzinska, M. A., and Lennon, K.(1995). Diminished activity of the first N-glycosylation enzyme, dolichol-P-dependent N-acetylglucosamine-1-P transferase(GPT), gives rise to mutant phenotypes in yeast. Biochim. Biophys. Acta 1247, 51-59.
38. Liu, C. Y., and Kaufman, R. J.(2003). The unfolded protein response. J. Cell Sci. 116, 1861-1862.
39. Liu, Y., and Chang, A.(2008). Heat shock response relieves ER stress. EMBOJ. 27, 1049-1059.
40. Lowry, O. H., Passonneau, J. V., and Rock, M. K.(1961). The stability of pyridine nucleotides. J. Biol. Chem. 236, 2756-2759.
41. Madeo, F., Frohlich, E., Ligr, M., Grey, M., Sigrist, S. J., Wolf, D. H., and Frohlich, K. U.(1999). Oxygen stress: a regulator of apoptosis in yeast. J. Cell Biol. 145, 757-767.
42. Malhotra, J. D., and Kaufman, R. J.(2007). Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword? Antioxid. Redox Signal. 9, 2277-2293.
43. Maris, A. F., Assumpcao, A. L., Bonatto, D., Brendel, M., and Henriques, J. A.(2001). Diauxic shift-induced stress resistance against hydroperoxides in Sac-charomyces cerevisiae is not an adaptive stress response and does not depend on functional mitochondria. Curr. Genet 39, 137-149.
44. Mori, K., Kawahara, T., Yoshida, H., Yanagi, H., and Yura, T.(1996). Signalling from endoplasmic reticulum to nucleus: transcription factor with a basic-leucine zipper motif is required for the unfolded protein-response pathway. Genes Cells 1, 803-817.
45. Muller, E. G.(1996). A glutathione reductase mutant of yeast accumulates high levels of oxidized glutathione and requires thioredoxin for growth. Mol. Biol. Cell 7, 1805-1813.
46. Ng, C. H., Tan, S. X., Perrone, G. G., Thorpe, G. W., Higgins, V. J., and Dawes, I. W.(2008). Adaptation to hydrogen peroxide in Saccharomyces cerevisiae: the role of NADPH-generating systems and the SKN7 transcription factor. Free Radic. Biol. Med. 44, 1131-1145.
47. Niwa, M., Patil, C. K., DeRisi, J., and Walter, P.(2005). Genome-scale approaches for discovering novel nonconventional splicing substrates of the Ire1 nuclease. Genome Biol. 6, R3.
48. Nogae, I., and Johnston, M.(1990). Isolation and characterization of the ZWF1 gene of Saccharomyces cerevisiae, encoding glucose-6-phosphate dehydrogenase. Gene 96, 161-169.
49. Perrone, G. G., Grant, C. M., and Dawes, I. W.(2005). Genetic and environmental factors influencing glutathione homeostasis in Saccharomyces cerevisiae. Mol. Biol. Cell 16, 218-230.
50. Perrone, G. G., Tan, S. X., and Dawes, I. W.(2008). Reactive oxygen species and yeast apoptosis. Biochim. Biophys. Acta 1783, 1354-1368.
51. Ron, D., and Walter, P.(2007). Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 8, 519-529.
52. Rose, M., and Botstein, D.(1983). Construction and use of gene fusions to lacZ(beta-galactosidase)that are expressed in yeast. Methods Enzymol. 101, 167-180.
53. Rosen, D. R. et al.(1993). Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362, 59-62.
54. Sanchez, R. J., Srinivasan, C., Munroe, W. H., Wallace, M. A., Martins, J., Kao, T. Y., Le, K., Gralla, E. B., and Valentine, J. S.(2005). Exogenous manganous ion at millimolar levels rescues all known dioxygen-sensitive phenotypes of yeast lacking CuZnSOD. J. Biol. Inorg. Chem. 10, 913-923.
55. Schafer, F. Q., and Buettner, G. R.(2001). Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic. Biol. Med. 30, 1191-1212.
56. Sevier, C. S., Qu, H., Heldman, N., Gross, E., Fass, D., and Kaiser, C. A.(2007). Modulation of cellular disulfide-bond formation and the ER redox environment by feedback regulation of Ero1. Cell 129, 333-344.
57. Slekar, K. H., Kosman, D. J., and Culotta, V. C.(1996). The yeast copper/zinc superoxide dismutase and the pentose phosphate pathway play overlapping roles in oxidative stress protection. J. Biol. Chem. 271, 28831-28836.
58. Spear, E. D., and Ng, D. T.(2003). Stress tolerance of misfolded carboxypeptidase Y requires maintenance of protein trafficking and degradative pathways. Mol. Biol. Cell 14, 2756-2767.
59. Stevens, T., Esmon, B., and Schekman, R.(1982). Early stages in the yeast secretory pathway are required for transport of carboxypeptidase Y to the vacuole. Cell 30, 439-448.
60. Sturtz, L. A., Diekert, K., Jensen, L. T., Lill, R., and Culotta, V. C.(2001). A fraction of yeast Cu, Zn-superoxide dismutase and its metallochaperone, CCS, localize to the intermembrane space of mitochondria. A physiological role for SOD1 in guarding against mitochondrial oxidative damage. J. Biol. Chem. 276, 38084-38089.
61. Takemori, Y., Sakaguchi, A., Matsuda, S., Mizukami, Y., and Sakurai, H.(2006). Stress-induced transcription of the endoplasmic reticulum oxi-doreductin gene ERO1 in the yeast Saccharomyces cerevisiae. Mol. Genet. Genomics 275, 89-96.
62. Temple, M. D., Perrone, G. G., and Dawes, I. W.(2005). Complex cellular responses to reactive oxygen species. Trends Cell Biol. 15, 319-326.
63. Thorpe, G. W., Fong, C. S., Alic, N., Higgins, V. J., and Dawes, I. W.(2004). Cells have distinct mechanisms to maintain protection against different reactive oxygen species: oxidative-stress-response genes. Proc. Natl. Acad. Sci. USA 101, 6564-6569.
64. Tong, A. H. et al.(2001). Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294, 2364-2368.
65. Travers, K. J., Patil, C. K., Wodicka, L., Lockhart, D. J., Weissman, J. S., and Walter, P.(2000). Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101, 249-258.
66. Trotter, E. W., and Grant, C. M.(2002). Thioredoxins are required for protection against a reductive stress in the yeast Saccharomyces cerevisiae. Mol. Microbiol. 46, 869-878.
67. Tu, B. P., and Weissman, J. S.(2004). Oxidative protein folding in eukaryotes: mechanisms and consequences. J. Cell Biol. 164, 341-346. Valls, L. A., Hunter, C. P., Rothman, J. H., and Stevens, T. H.(1987). Protein
68. sorting in yeast: the localization determinant of yeast vacuolar carboxypeptidase Y resides in the propeptide. Cell 48, 887-897.
69. Vandeputte, C., Guizon, I., Genestie-Denis, I., Vannier, B., and Lorenzon, G.(1994). A microtiter plate assay for total glutathione and glutathione disulfide contents in cultured/isolated cells: performance study of a new miniaturized protocol. Cell Biol. Toxicol. 10, 415-421.
70. Veal, E. A., Ross, S. J., Malakasi, P., Peacock, E., and Morgan, B. A.(2003). Ybp1 is required for the hydrogen peroxide-induced oxidation of the Yap1 transcription factor. J. Biol. Chem. 278, 30896-30904.
71. Wheals, A. E.(1982). Size control models of Saccharomyces cerevisiae cell proliferation. Mol. Cell. Biol. 2, 361-368.
72. White, C. W., Nguyen, D. H., Suzuki, K., Taniguchi, N., Rusakow, L. S., Avraham, K. B., and Groner, Y.(1993). Expression of manganese super-oxide dismutase is not altered in transgenic mice with elevated level of copper-zinc superoxide dismutase. Free Radic. Biol. Med. 15, 629-636.
73. Winzeler, E. A. et al.(1999). Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285, 901-906.
74. Zhao, H., Kalivendi, S., Zhang, H., Joseph, J., Nithipatikom, K., Vasquez-Vivar, J., and Kalyanaraman, B.(2003). Superoxide reacts with hydroethidine but forms a fluorescent product that is distinctly different from ethidium: potential implications in intracellular fluorescence detection of superoxide. Free Radic. Biol. Med. 34, 1359-1368.