Saccharomyces cerevisiae cells have three Omega class glutathione S-transferases acting as 1-Cys thiol transferases

Biochemical Journal

Volumn 398, Issue 2, 2006, Pages 187-196

  Garcerá, Ana ^a   Barreto, Lina ^a   Piedrafita, Lidia ^a   Tamarit, Jordi ^a   Herrero, Enrique ^a  

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

Author keywords

Deglutathionylation; Glutaredoxin (Grx); Glutathione peroxidase; Glutathione S transferase (GST); Redox regulation; Thiol oxidoreductase

Indexed keywords

ALCOHOLS; ENZYME KINETICS; PROTEINS; REDOX REACTIONS; SUBSTRATES; YEAST;

DEGLUTATHIONYLATION; GLUTAREDOXIN (GRX); GLUTATHIONE PEROXIDASE; REDOX REGULATION; THIOL OXIDOREDUCTASE;

CELL CULTURE;

1 CYS THIOL TRANSFERASE; CUMENE HYDROPEROXIDE; CYSTEINE; GLUTAREDOXIN; GLUTATHIONE PEROXIDASE; OMEGA CLASS GLUTATHIONE S TRANSFERASE; TRANSFERASE; UNCLASSIFIED DRUG; 1 CYS THIOL TRANSFERASE PROTEIN, S CEREVISIAE; 1-CYS THIOL TRANSFERASE PROTEIN, S CEREVISIAE; GLUTATHIONE; GLUTATHIONE TRANSFERASE; OXIDOREDUCTASE; RECOMBINANT PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; THIOL DERIVATIVE;

ARTICLE; ENZYME ACTIVITY; GENOME; IN VIVO STUDY; PRIORITY JOURNAL; PROTEIN PURIFICATION; SACCHAROMYCES CEREVISIAE; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; CLASSIFICATION; ENZYME SPECIFICITY; ENZYMOLOGY; GENE EXPRESSION; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHYLOGENY; SEQUENCE ALIGNMENT;

SACCHAROMYCES CEREVISIAE;

AMINO ACID SEQUENCE; ANIMALS; CONSERVED SEQUENCE; CYSTEINE; GENE EXPRESSION; GENOME, FUNGAL; GLUTATHIONE; GLUTATHIONE PEROXIDASE; GLUTATHIONE TRANSFERASE; HUMANS; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES; OXIDOREDUCTASES; PHYLOGENY; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ALIGNMENT; SUBSTRATE SPECIFICITY; SULFHYDRYL COMPOUNDS;

EID: 33748347924     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20060034     Document Type: Article

References (46)

1. Armstrong, R. N. (1997) Structure, catalytic mechanism, and evolution of the glutathione transferases. Chem. Res. Toxicol. 10, 2-18
2. Sheehan, D., Meade, G., Foley, V. M. and Dowd, C. A. (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
3. Hayes, J. D., Flanagan, J. U. and Jowsey, I. R. (2005) Glutathione transferases. Annu. Rev. Pharmacol. Toxicol. 45, 51-88
4. Oakley, A. J. (2005) Glutathione transferases: new functions. Curr. Opin. Struct. Biol. 15, 716-723
5. Morel, F., Rauch, C., Petit, E., Piton, A., Theret, N., Coles, B. and Guillouzo, A. (2004) Gene and protein characterization of the human glutathione S-transferase kappa and evidence for a peroxisomal localization. J. Biol. Chem. 279, 16246-16253
6. Board, P. G., Coggan, M., Chelvanagayam, G., Easteal, S., Jermiin, L. S., Schulte, G. K., Danley, D. E., Hoth, L. R., Griffor, M. C., Kamath, A. V. et al. (2000) Identification, characterization, and crystal structure of the Omega class glutathione transferases. J. Biol. Chem. 275, 24798-24806
7. Rouimi, P., Anglade, P., Benzekri, A., Costet, P., Debrauwer, L., Pineau, T. and Tulliez, J. (2001) Purification and characterization of a glutathione S-transferase Omega in pig: evidence for two distinct organ-specific transcripts. Biochem. J. 358, 257-262
8. Girardini, J., Amirante, A., Zemzoumi, K. and Serra, E. (2002) Characterization of an omega-class glutathione S-transferase from Schistosoma mansoni with glutaredoxin-like dehydroascorbate reductase and thiol transferase activities. Eur. J. Biochem. 269, 5512-5521
9. Whitbread, A. K., Masoumi, A., Tetlow, N., Schmuck, E., Coggan, M. and Board, P. G. (2005) Characterization of the Omega-class of glutathione transfrases. Methods Enzymol. 401, 78-99
10. Hurst, R., Bao, Y., Mannervik, B. and Williamson, G. (1998) Phospholipid hydroperoxide glutathione peroxidase activity of human glutathione transferases. Biochem. J. 332, 97-100
11. Zhao, T., Singhal, S. S., Piper, J. T., Cheng, J., Pandya, U., Clark-Wronski, J., Awasthi, S. and Awasthi, Y. C. (1999) The role of human glutathione S-transferases hGSTA1-1 and hGSTA2-2 in protection against oxidative stress. Arch. Biochem. Biophys. 367, 216-224
12. Prabhu, K. S., Reddy, P. V., Jones, E. C., Liken, A. D. and Reddy, C. C. (2004) Characterization of a class alpha glutathione S-transferase with glutathione peroxidase activity in human liver microsomes. Arch. Biochem. Biophys. 424, 72-80
13. Schmuck, E. M., Board, P. G., Whitbread, A. K., Tetlow, N., Blackburn, A. C. and Masoumi, A. (2005) Characterization of the monomethylarsonate reductase and dehydroascorbate reductase activities of Omega class glutathione transferase variants. Implications for arsenic metabolism and age-at-onset of Alzheimer's and Parkinson's diseases. Pharmacogenet. Genomics 15, 493-501
14. Dulhunty, A., Gage, P., Curtis, S., Chelvanayagam, G. and Board, P. (2001) The glutathione transferase structural family includes a nuclear chloride channel and a ryanodine receptor calcium release channel modulator. J. Biol. Chem. 276, 3319-3323
15. Laliberte, R. E., Perregaux, D. G., Hoth, L. R., Rosner, P. J., Jordan, C. K., Peese, K. M., Eggler, J. F., Dombroski, M. A., Geoghegan, K. F. and Gabel, C. A. (2003) Glutathione S-transferase omega 1-1 is a target of cytokine release inhibitory drugs and may be responsible for their effect on interleukin-1β posttranslational processing. J. Biol. Chem. 278, 16567-16578
16. Li, Y. J., Oliveira, S. A., Xu, O., Martin, E. R., Stenger, J. E., Scherzer, C. R., Hauser, M. A., Scott, W. K., Small, G. W., Nance, M. A. et al. (2003) Glutathione S-transferase omega-1 modifies age-ot-onset of Alzheimer disease and Parkinson disease. Human Mol. Genet. 12, 3259-3267
17. McGoldrick, S., O'Sullivan, S. M. and Sheehan, D. (2005) Glutatnione transferase-like proteins encoded in genomes of yeasts and fungi: insights into evolution of a multifunctional protein superfamily. FEMS Microbiol. Lett. 242, 1-12
18. Choi, J. H., Lou, W. and Vancura, A. (1998) A novel membrane-bound glutathione S-transferase functions in the stationary phase of the yeast Saccharomyces cerevisiae. J. Biol. Chem. 273, 29915-29922
19. Collinson, E. J. and Grant, C. M. (2003) Role of yeast glutaredoxins as glutathione S-transferases. J. Biol. Chem. 278, 22492-22497
20. Luikenhuis, S., Dawes, I. W. and Grant, C. M. (1998) The yeast Saccharomyces cerevisiae contains two glutaredoxin genes that are required for protection against reactive oxygen species. Mol. Biol. Cell 9, 1081-1091
21. Veal, E. A., Toone, W. M., Jones, N. and Morgan, B. A. (2002) Distinct roles for glutathione S-transferases in the oxidative stress response in Schizosaccharomyces pombe. J. Biol. Chem. 277, 35523-35531
22. Rodríguez-Manzaneque, M. T., Ros, J., Cabiscol, E., Sorribas, A. and Herrero, E. (1999) Grx5 glutaredoxin plays a central role in protection against protein oxidative damage in Saccharomyes cerevisiae. Mol. Cell. Biol. 19, 8180-8190
23. Bellí, G., Polaina, J., Tamarit, J., de la Torre, M. A., Rodríguez-Manzaneque, M. T., Ros, J. and Herrero, E. (2002) Structure-function analysis of yeast Grx5 monothiol glutaredoxin defines essential amino acids for the function of the protein. J. Biol. Chem. 277, 37590-37596
24. Rahlfs, S., Fischer, M. and Becker, K. (2001) Plasmodium falciparum possesses a classical glutaredoxin and a second, glutaredoxin-like protein with a PICOT homology domain. J. Biol. Chem. 276, 37133-37140
25. Tamarit, J., Bellí, G., Cabiscol, E, Herrero, E. and Ros, J. (2003) Biochemical characterization of yeast mitochondrial Grx5 monothiol glutaredoxin. J. Biol. Chem. 278, 25745-25751
26. Fernandes, A. P., Fladvad, M., Berndt, C., Andrésen, C., Lillig, C. H., Neubauer, P., Sunnerhagen, M., Holmgren, A. and Vlamis-Gardikas, A. (2005) A novel monothiol glutaredoxin (Grx4) from Escherichia coli can serve as a substrate for thioredoxin reductase. J. Biol. Chem. 280, 24544-24552
27. Collinson, E. J., Wheeler, G. L., Ocón-Garrido, E., Avery, A. M., Avery, S. V. and Grant, C. M. (2002) The yeasts glutaredoxins are active as glutathione peroxidases. J. Biol. Chem. 277, 16712-16717
28. Weiner, M. P. and Costa, L. (1995) Rapid PCR site-directed mutagenesis. In PCR Primer, a Laboratory Manual (Dieffenbach, C. W. and Dveksler, G. S., eds.), pp. 613-621, Cold Spring Harbor Laboratory Press, Cold Spring Harbor
29. Gietz, R. D. and Sugino, A. (1988) New yeast-Escterichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74, 3065-3073
30. Sherman, F. (2002) Getting started with yeast. Methods Enzymol. 350, 3-41
31. Habig, W. H., Pabst, M. J. and Jakoby, W. B. (1974) Glutathione S-transferases. J. Biol. Chem. 249, 7130-7139
32. Holmgren, A. and Aslund, F. (1995) Glutaredoxin. Methods Enzymol. 252, 283-292
33. Thompson, J. D., Higgins, D. G. and Gibson, T. J. (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
34. Combet, C., Blanchet, C., Geourjon, C. and Deléage, G. (2000) NPS@: network protein sequence analysis. Trends Biochem. Sci. 25, 147-150
35. Lussier, M., White, A. M., Sheraton, J., di Paolo, T., Treadwell, J., Southard, S. B., Horenstein, C. I., Chen-Weiner, J., Ram, A. F., Kapteyn, J. C. et al. (1997) Large scale identification of genes involved in cell surface biosynthesis and architecture in Saccharomyces cerevisiae. Genetics 147, 435-450
36. Blackwell, J. R. and Horgan, R. (1991) A novel strategy for the production of a highly expressed recombinant protein in an active form. FEBS Lett. 295, 10-12
37. Gasch, A. P., Spellman, P. T., Kao, C. M., Carmel-Harel, O., Eisen, M. B., Storz, G., Botstein, D. and Brown, P. O. (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell 11, 4241-4257
38. Winayanuwattikun, P. and Ketterman, A. J. (2005) An electron-sharing network involved in the catalytic mechanism is functionally conserved in different glutathione transferase classes. J. Biol. Chem. 280, 31776-31782
39. Martin, J. L. (1995) Thioredoxin - a fold for all reasons. Structure 3, 245-250
40. Ferrari, D. M. and Soling, H. D. (1999) The protein disulphide-isomerase family: unravelling a string of folds. Biochem. J. 339, 1-10
41. Fladvad, M., Bellanda, M., Fernandes, A. P., Mammi, S., Vlamis-Gardikas, A., Holmgren, A. and Sunnerhagen, M. (2005) Molecular mapping of functionalities in the solution structure of reduced Grx4, a monothiol glutaredoxin from Escherichia coli. J. Biol. Chem. 280, 24553-24561
42. Caccuri, A. M., Antonioni, G., Allocate, N., Di Ilio, C., De Maria, F., Innocenti, F., Parker, M. W., Masulli, M., Lo Bello, M., Turella, P., Federico, G. and Ricci, G. (2002) GSTB1-1 from Profeus mirabilis: a snapshot of an enzyme in the evolutionary pathway from a redox enzyme to a conjugating enzyme. J. Biol. Chem. 277, 18777-18784
43. Huh, W. K., Falvo, J. V., Gerke, L. C., Carroll, A. S., Howson, R. W., Weismann, J. S. and O'Shea, E. K. (2003) Global analysis of protein localization in budding yeast. Nature (London) 425, 686-691
44. Fernandes, A. P. and Holmgren, A. (2004) Glutaredoxins: glutathione-dependent redox enzymes with functions far beyond a simple thioredoxin backup system. Antioxid. Redox Signaling 6, 63-74
45. Molina, M. M., Bellí, G., de la Torre, M. A., Rodríguez- Manzaneque, M. T. and Herrero, E. (2004) Nuclear monothiol glutaredoxins of Saccharomyces cerevisiae can function as mitochondrial glutaredoxins. J. Biol. Chem. 279, 51923-51930
46. Bai, M., Zhou, J. M. and Perrett, S. (2004) The yeast prion protein Ure2 shows glutathione peroxidase activity in both native and fibrillar form. J. Biol. Chem. 279, 50025-50030