A peroxisomal glutathione transferase of Saccharomyces cerevisiae is functionally related to sulfur amino acid metabolism

Eukaryotic Cell

Volumn 5, Issue 10, 2006, Pages 1748-1759

  Barreto, Lina ^a   Garcerá, Ana ^a   Jansson, Kristina ^b   Sunnerhagen, Per ^b   Herrero, Enrique ^a  

^a Universitat de Lleida Facultat de Medicina Sabadell   (Spain)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; GLUTATHIONE; GLUTATHIONE TRANSFERASE; MESSENGER RNA; MUTANT PROTEIN; OLEIC ACID; OXIDIZING AGENT; SULFUR AMINO ACID;

AMINO ACID SEQUENCE; ARTICLE; BIOSYNTHESIS; CHEMISTRY; CYTOLOGY; CYTOSOL; DOWN REGULATION; DRUG EFFECT; ENZYMOLOGY; FUNGAL GENE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; MUTATION; PEROXISOME; PHENOTYPE; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT; UPREGULATION;

AMINO ACID SEQUENCE; AMINO ACIDS, SULFUR; CYTOSOL; DOWN-REGULATION; GENE EXPRESSION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, FUNGAL; GENES, FUNGAL; GLUCOSE; GLUTATHIONE; GLUTATHIONE TRANSFERASE; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; MUTATION; OLEIC ACID; OXIDANTS; PEROXISOMES; PHENOTYPE; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT; UP-REGULATION;

SACCHAROMYCES CEREVISIAE;

EID: 33750380347     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00216-06     Document Type: Article

References (82)

1. Adamis, P. D. B., D. S. Gomes, M. L. C. C. Pinto, A. D. Panek, and E. C. A. Eleuterio. 2004. The role of glutathione transferases in cadmium stress. Toxicol. Lett. 154:81-88.
2. Armstrong, R. N. 1997. Structure, catalytic mechanism, and evolution of the glutathione transferases. Chem. Res. Toxicol. 10:2-18.
3. Avery, S. V. 2001. Metal toxicity in yeasts and the role of oxidative stress. Adv. Appl. Microbiol. 49:111-142.
4. Awasthi, Y. C., G. A. S. Ansari, and S. Awasthi. 2005. Regulation of 4-hydroxynonenal mediated signaling by glutathione S-transferases. Methods Enzymol. 401:379-407.
5. Blaiseau, P. L., and D. Thomas. 1998. Multiple transcriptional activation complexes tether the yeast activator Met4 to DNA. EMBO J. 17:6327-6336.
6. Board, P. G., M. Coggan, G. Chelvanagayam, S. Easteal, L. S. Jermiin, G. K. Schulte, D. E. Danley, L. R. Hoth, M. C. Griffor, A. V. Kamath, M. H. Rosner, B. A. Chrunyk, D. E. Perregaux, C. A. Gabel, K. F. Geoghegan, and J. Pandit. 2000. Identification, characterization, and crystal structure of the omega class glutathione transferases. J. Biol. Chem. 275:248-24806.
7. Breitinger, U., T. Clausen, S. Ehlert, R. Huber, B. Laber, F. Schmidt, E. Pohl, and A. Messerchmidt. 2001. The three-dimensional structure of cystathionine β-lyase from Arabidopsis and its substrate specificity. Plant Physiol. 126:631-642.
8. Breitling, R., O. Sharif, M. L. Hartman, and S. K. Krisans. 2002. Loss of compartmentalization causes misregulation of lysine biosynthesis in peroxisome-deficient yeast cells. Eukaryot. Cell 1:978-986.
9. Brennan, R. J., and R. H. Schiestl. 1996. Cadmium is an inducer of oxidative stress in yeast. Mutat. Res. 356:171-178.
10. Cherest, H., and Y. Surdin-Kerjan. 1992. Genetic analysis of a new mutation conferring cysteine auxotrophy in Saccharomyces cerevisiae: updating of the sulfur metabolism pathway. Genetics 130:51-58.
11. Choi, J. H., W. Lou, and A. Vancura. 1998. A novel membrane-bound glutathione S-transferase functions in the stationary phase of the yeast Saccharomyces cerevisiae. J. Biol. Chem. 273:29915-29922.
12. Churin, Y., S. Schilling, and H. Börner. 1999. A gene encoding glutathione peroxidase homologues in Hordeum vulgare (barley). FEBS Lett. 459:33-38.
13. Claros, M. G., and P. Vincens. 1996. Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur. J. Biochem. 241:770-786.
14. Collinson, E. J., and C. M. Grant. 2003. Role of yeast glutaredoxins as glutathione S-transferases. J. Biol. Chem. 278:22492-22497.
15. Collinson, E. J., G. L. Wheeler, E. Ocón-Garrido, A. M. Avery, S. V. Avery, and C. M. Grant. 2002. The yeast glutaredoxins are active as glutathione peroxidases. J. Biol. Chem. 277:16712-16717.
16. Del Rio, L. A., F. J. Corpas, L. M. Sandalio, J. M. Palma, and J. B. Barroso. 2003. Plant peroxisomes, reactive oxygen metabolism, and nitric oxide. IUBMB Life 55:71-81.
17. Deponte, M., and K. Becker. 2005. Glutathione S-transferase from malarial parasites: structural and functional aspects. Methods Enzymol. 401:241-253.
18. Diekert, K., A. I. P. M. de Kroon, G. Kispal, G., and R. Lill. 2001. Isolation and subfractionation of mitochondria from the yeast Saccharomyces cerevisiae. Methods Cell Biol. 65:37-51.
19. Dormer, U. H., J. Westwater, N. F. McLaren, N. A. Kent, J. Mellor, and D. J. Jamieson. 2000. Cadmium-inducible expression of the yeast GSH1 gene requires a functional sulfur-amino acid regulatory network. J. Biol. Chem. 42:32611-32616.
20. Dujon, B. 2005. Hemiascomycetous yeasts at the forefront of comparative genomics. Curr. Opin. Gen. Dev. 15:1-7.
21. Erdmann, R., and S. J. Gould. 2002. Visualization and purification of yeast peroxisomes. Methods Enzymol. 351:365-381.
22. Estruch, F. 2000. Stress-controlled transcription factors, stress-induced genes and stress tolerance in budding yeast. FEMS Microbiol. Rev. 24:469-486.
23. Fauchon, M., G. Lagniel, J. C. Aude, L. Lombardia, P. Soularue, C. Petat, G. Marguerie, A. Sentenae, M. Werner, and J. Labarre. 2002. Sulfur sparing in the yeast proteome in response to sulfur demand. Mol. Cell 9:713-723.
24. Gabaldón, T., B. Snel, F. Zimmeren, W. Hemrika, H. Tabak, and M. A. Huynen. 2006. Origin and evolution of the peroxisomal proteome. Biol. Direct. 1:8.
25. Garcerá, A., L. Barreto, L. Piedrafita, J. Tamarit, and E. Herrero. 2006. Saccharomyces cerevisiae cells have three Omega-class glutathione transferases acting as 1-Cys thiol transferases. Biochem. J. 398:187-196.
26. Garí, E., L. Piedrafita, M. Aldea, and E. Herrero. 1997. A set of vectors with the tetracycline-regulatable promoter system for modulated gene expression in Saccharomyces cerevisiae. Yeast 13:837-848.
27. Gasch, A. P. 2003. The environmental stress response: a common yeast response to diverse environmental stresses, p. 11-70. In S. Hohman and P. W. H. Mager (ed.). Topics in current genetics: yeast stress responses. Springer-Verlag, Berlin, Germany.
28. Geraghty, M. T., D. Bassett, J. C. Morrell, G. J. Gatto, Jr., J. Bai, B. V. Geisbrecht, P. Hieter, and S. J. Gould. 1999. Detecting patterns of protein distribution and gene expression in silico. Proc. Natl. Acad. Sci. USA 96:2937-2942.
29. Gietz, R. D., and A. Sugino. 1988. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74:3065-3073.
30. Girardini, J., A. Amirante, K. Zemzoumi, and E. Serra. 2002. Characterization of an omega-class glutathione S-transferase from Schistosoma mansonii with glutaredoxin-like dehydroascorbate reductase and thiol transferase activities. Eur. J. Biochem. 269:5512-5521.
31. Goldstein, A. L., X. Pan, and J. H. McCusker. 1999. Heterologous URA3MX cassettes for gene replacement in Saccharomyces cerevisiae. Yeast 15:507-511.
32. Goldstein, A. L., and J. H. McCusker. 1999. Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15:1541-1553.
33. Hansen, J., and P. F. Johannesen. 2000. Cysteine is essential for transcriptional regulation of the sulfur assimilation genes in Saccharomyces cerevisiae. Mol. Gen. Genet. 263:535-542.
34. Hayes, J. D., J. U. Flanagan, and I. R. Jowsey. 2005. Glutathione transferases. Annu. Rev. Pharmacol. Toxicol. 45:51-88.
35. He, X. J., and J. S. Fassier. 2005. Identification of novel Yap1p and Skn7p binding sites involved in the oxidative stress response of Saccharomyces cerevisiae. Mol. Microbiol. 58:1454-1467.
36. Heiland, I., and R. Erdmann. 2005. Biogenesis of peroxisomes: topogenesis of the peroxisomal membrane and matrix proteins. FEBS J. 272:2362-2372.
37. Hesse, H., and R. Hoefgen. 2003. Molecular aspects of methionine biosynthesis. Trends Plant Sci. 8:259-262.
38. Hiltunen, J. K., A. M. Mursula, H. Rottensteiner, R. K. Wierenga, A. J. Kastaniotis, and A. Gurvitz. 2003. The biochemistry of peroxisomal β-oxidation in the yeast Saccharomyces cerevisiae. FEMS Microbiol. Rev. 27:35-64.
39. Horiguchi, H., H. Yurimoto, N. Kato, and Y. Sakai. 2001. Antioxidant system within yeast peroxisome: biochemical and physiological characterization of CbPmp20 in the methylotrophic yeast Candida boidinii. J. Biol. Chem. 276:14279-14288.
40. Islinger, M., G. H. Lüers, H. Zischka, M. Ueffing, and A. Völkl. 2006. Insights into the membrane proteome of rat liver peroxisomes: microsomal glutathione-S-transferase is shared by both subcellular compartments. Proteomics 6:804-816.
41. Jakubowski, W., T. Bilinski, and G. Bartosz. 2000. Oxidative stress during aging of stationary cultures of the yeast Saccharomyces cerevisiae. Free Radic. Biol. Med. 28:659-664.
42. Kumar, A., L. John, M. M. Alam, A. Gupta, G. Sharma, B. Pillai, and S. Sengupta. 2006. Homocysteine- and cysteine-mediated growth defect is not associated with induction of oxidative stress response genes in yeast. Biochem. J. 396:61-69.
43. Kuras, L., R. Barbey, and D. Thomas. 1997. Assembly of a bZIP-bHLH transcription activation complex: formation of the yeast Cbf1-Met4-Met28 complex is regulated through Met28 stimulation of Cbf1 DNA binding. EMBO J. 16:2441-2451.
44. Lametschwandtner, G., C. Brocard, M. Fransen, P. van Veldhoven, J. Berger, and A. Hartig. 1998. The difference in recognition of terminal tripeptides as peroxisomal targeting signal I between yeast and human is due to different affinities of their receptor Pex5p to the cognate signal and to residues adjacent to it. J. Biol. Chem. 273:33635-33643.
45. Li, Z., Y. Lu, R. Zhen, M. Szczypka, D. Thiele, and P. A. Rea. 1997. A new pathway for vacuolar cadmium sequestration in Saccharomyces cerevisiae: YCF1-catalyzed transport of bis(glutathionate)cadmium. Proc. Natl. Acad. Sci. USA 94:42-47.
46. Mannervik, B., P. G. Board, J. D. Hayes, I. Listowsky, and W. R. Pearson. 2005. Nomenclature for mammalian soluble glutathione transferases. Methods Enzymol. 401:1-8.
47. McGoldrick, S., S. M. O'Sullivan, and D. Sheehan. 2005. Glutathione transferase-like proteins encoded in genomes of yeasts and fungi: insights into evolution of a multifunctional protein superfamily. FEMS Microbiol. Lett. 242:1-12.
48. Menant, A., P. Baudouin-Cornu, C. Peyraud, M. Tyers, and D. Thomas. 2006. Determinants of the ubiquitin-mediated degradation of the Met4 transcription factor. J. Biol. Chem. 281:11744-11754.
49. Molina, M. M., G. Bellí, M. A. de la Torre, M. T. Rodríguez-Manzaneque, and E. Herrero, E. 2004. Nuclear monothiol glutaredoxins of Saccharomyces cerevisiae can function as mitochondrial glutaredoxins. J. Biol. Chem. 279:1923-51930.
50. Morel, F., C. Rauch, E. Petit, A. Piton, N. Theret, B. Coles, and A. Guillouzo. 2004. Gene and protein characterization of the human glutathione S-transferase kappa and evidence for a peroxisomal localization. J. Biol. Chem. 279:16246-16253.
51. Oakley, A. J. 2005. Glutathione transferases: new functions. Curr. Opin. Struct. Biol. 15:716-723.
52. Petersen, J. G., M. C. Kielland-Brandt, T. Nilsson-Tillgren, C. Bornaes, and S. Holmberg. 1988. Molecular genetics of serine and threonine catabolism in Saccharomyces cerevisiae. Genetics 119:527-534.
53. Pócsi, I., R. A. Prade, and M. J. Penninckx. 2004. Glutathione, altruistic metabolite in fungi. Adv. Microb. Physiol. 49:1-76.
54. Puig, O., F. Caspary, G. Rigaut, B. Rutz, E. Bouveret, E. Bragado-Nilsson, M. Wilm, and B. Seraphin. 2001. The tandem affinity purification (TAP) method: a general procedure of protein complex purification. Methods 24:218-229.
55. Purdue, P. E., and P. B. Lazarow. 2001. Peroxisome biogenesis. Annu. Rev. Cell Dev. Biol. 17:701-752.
56. Rai, R., and T. G. Cooper. 2005. In vivo specificity of Ure2 protection from heavy metal ion and oxidative cellular damage in Saccharomyces cerevisiae. Yeast 22:343-358.
57. Rai, R., J. J. Tate, and T. G. Cooper. 2003. Ure2, a prion precursor with homology to glutathione S-transferase, protects Saccharomyces cerevisiae cells from heavy metal ion and oxidant toxicity. J. Biol. Chem. 278:12826-12833.
58. Ravanel, S., D. Job, and R. Douce. 1996. Purification and properties of cystathionine β-lyase from Arabidopsis thaliana overexpressed in Escherichia coli. Biochem. J. 320:383-392.
59. Rodríguez-Manzaneque, M. T., J. Tamarit, J. G. Bellí, J. Ros, and E. Herrero. 2002. Grx5 is a mitochondrial glutaredoxin required for the maturation of iron/sulfur enzymes. Mol. Biol. Cell 13:1109-1121.
60. Rouimi, P., P. Anglade, A. Benzekri, P. Costet, L. Debrauwer, T. Pineau, and J. Tulliez. 2001. Purification and characterization of a glutathione S-transferase Omega in pig: evidence for two distinct organ-specific transcripts. Biochem. J. 358:257-262.
61. Schafer, H., K. Nau, A. Sickmann, R. Erdmann, and H. E. Meyer. 2001. identification of peroxisomal membrane proteins of Saccharomyces cerevisiae by mass spectrometry. Electrophoresis 22:2955-2968.
62. Schrader, M., and H. D. Fahimi. 2004. Mammalian peroxisomes and reactive oxygen species. Histochem. Cell Biol. 122:383-393.
63. Sharma, K. G., D. L. Mason, G. Liu, P. A. Rea, A. K. Bachhawat, and S. Michaelis. 2002. Localization, regulation, and substrate transport properties of Bpt1p, a Saccharomyces cerevisiae MRP-type ABC transporter. Eukaryot. Cell 1:391-400.
64. Sheehan, D., G. Meade, V. M. Foley, and C. A. Dowd. 2001. Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily. Biochem. J. 360:1-16.
65. Sherman, F. 2002. Getting started with yeast. Methods Enzymol. 350:3-41.
66. Tatchell, K., and L. C. Robinson. 2002. Use of green fluorescent protein in living yeast cells. Methods Enzymol. 351:661-683.
67. Thomas, D., and Y. Surdin-Kerjan. 1997. Metabolism of sulfur amino acids in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 61:503-532.
68. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
69. Toledano, M. B., A. Delaunay, B. Biteau, D. Spector, and D. Azevedo. 2003. Oxidative stress responses in yeast, p. 241-303. In S. Hohman and P. W. H. Mager (ed.), Topics in current genetics: yeast stress responses. Springer-Verlag, Berlin, Germany.
70. Townsend, D. M., V. L. Findlay, and K. D. Tew. 2005. Glutathione S-transferases as regulators of kinase pathways and anticancer drug targets. Methods Enzymol. 401:287-307.
71. Van Helden, J. 2003. Regulatory sequence analysis tools. Nucleic Acids Res. 31:3593-3596.
72. Veal, E. A., W. M. Toone, N. Jones, and B. A. Morgan. 2002. Distinct roles for glutathione S-transferases in the oxidative stress response in Schizosaccharomyces pombe. J. Biol. Chem. 277:35523-35531.
73. Veenhuis, M., F. A. Salomons, and I. J. Van der Klei. 2000. Peroxisome biogenesis and degradation in yeast: a structure/function analysis. Microsc. Res. Technol. 51:584-600.
74. Viladevall, L., R. Serrano, A. Ruiz, G. Domenech, J. Giraldo, A. Barceló, and J. Ariño. 2004. Characterization of the calcium-mediated response to alkaline stress in Saccharomyces cerevisiae. J. Biol. Chem. 279:43614-43624.
75. Vuilleumier, S. 1997. Bacterial glutathione S-transferases: what are they good for? J. Bacteriol. 179:1431-1441.
76. Wach, A., A. Brachat, R. Pöhlmann, and P. Philippsen. 1994. New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 13:1793-1808.
77. Wanders, R. J. A., and H. R. Waterman. 2006. Biochemistry of mammalian peroxisomes revisited. Annu. Rev. Biochem. 75:295-332.
78. Warringer, J., and A. Blomberg. 2003. Automated screening in environmental arrays allows analysis of quantitative phenotypic profiles in Saccharomyces cerevisiae. Yeast 20:53-67.
79. Weiner, M. P., and L. Costa. 1995. Rapid PCR site-directed mutagenesis, p. 613-621. In C. W. Dieffenbach and G. S. Dveksler (ed.), PCR primer: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
80. Whitbread, A. K., A. Masoumi, N. Tetlow, E. Schmuck, M. Coggan, and P. G. Board. 2005. Characterization of the Omega-class of glutathione transferases. Methods Enzymol. 401:78-99.
81. Wong, S., G. Butler, and K. H. Wolfe. 2002. Gene order evolution and paleopolyploidy in hemiascomycete yeasts. Proc. Natl. Acad. Sci. USA 387:708-713.
82. Yi, E. C., M. Marelli, H. Lee, S. O. Purvine, R. Aebersold, J. D. Aitchison, and D. R. Goodlett. 2002. Approaching complete peroxisome characterization by gas-phase fractionation. Electrophoresis 23:3205-3216.