Glutathione degradation is a key determinant of glutathione homeostasis

Journal of Biological Chemistry

Volumn 287, Issue 7, 2012, Pages 4552-4561

  Baudouin Cornu, Peggy ^a   Lagniel, Gilles ^a   Kumar, Chitranshu ^b,c   Huang, Meng Er ^b   Labarre, Jean ^a  

^a SERVICE DE CHIMIE BIOORGANIQUE ET DE MARQUAGE   (France)

^b CNRS UMR3348   (France)

^c Glenmark Pharmaceuticals Limited   (India)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSOLIC; DEGRADATION ACTIVITY; EUKARYOTIC CELLS; GLUTATHIONES; IN-VIVO; INTRACELLULAR CONCENTRATION; KEY DETERMINANTS; MUTANT CELLS; STANDARD CONDITIONS; SULFUR DEPRIVATION; SULFUR SOURCE; SYNTHESIS RATE; TRANSCRIPTIONAL LEVELS;

CADMIUM; MATHEMATICAL MODELS; METABOLISM; PEPTIDES; PHYSIOLOGY; SULFUR; TRANSCRIPTION; YEAST;

DEGRADATION;

CADMIUM; DIPEPTIDASE; DUG1 PROTEIN; DUG2 PROTEIN; DUG3 PROTEIN; GAMMA GLUTAMYLTRANSFERASE; GLUTATHIONE; SULFUR; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; GLUTATHIONE METABOLISM; HALF LIFE TIME; METABOLISM; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; SULFATE METABOLISM; TRANSCRIPTION REGULATION;

BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CADMIUM; CARBON-NITROGEN LIGASES; DIPEPTIDASES; GENE DELETION; GLUTATHIONE; HALF-LIFE; HOMEOSTASIS; MULTIENZYME COMPLEXES; PEPTIDE HYDROLASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SULFUR;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 84856934666     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.315705     Document Type: Article

References (47)

1. Ballatori, N., Krance, S. M., Notenboom, S., Shi, S., Tieu, K., and Hammond, C. L. (2009) Glutathione dysregulation and the etiology and progression of human diseases. Biol. Chem. 390, 191-214
2. Lu, S. C. (1999) Regulation of hepatic glutathione synthesis. Current concepts and controversies. FASEB J. 13, 1169-1183
3. Lu, S. C. (2009) Regulation of glutathione synthesis. Mol. Aspects Med. 30, 42-59
4. Bourbouloux, A., Shahi, P., Chakladar, A., Delrot, S., and Bachhawat, A. K. (2000) Hgt1p, a high affinity glutathione transporter from the yeast Saccharomyces cerevisiae. J. Biol. Chem. 275, 13259-13265 (Pubitemid 30257381)
5. Rebbeor, J. F., Connolly, G. C., Dumont, M. E., and Ballatori, N. (1998) ATP-dependent transport of reduced glutathione on YCF1, the yeast orthologue of mammalian multidrug resistance- associated proteins. J. Biol. Chem. 273, 33449-33454 (Pubitemid 29005726)
6. Jaspers, C. J., Gigot, D., and Penninckx, M. J. (1985) Pathways of glutathione degradation in the yeast Saccharomyces cerevisiae. Phytochemistry 24, 703-707
7. Kumar, C., Sharma, R., and Bachhawat, A. K. (2003) Utilization of glutathione as an exogenous sulfur source is independent of γ-glutamyl- transpeptidase in the yeast Saccharomyces cerevisiae. Evidence for an alternative gluathione degradation pathway. FEMS Microbiol. Lett. 219, 187-194 (Pubitemid 36302596)
8. Elskens, M. T., Jaspers, C. J., and Penninckx, M. J. (1991) Glutathione as an endogenous sulfur source in the yeast Saccharomyces cerevisiae. J. Gen. Microbiol. 137, 637-644
9. Mehdi, K., and Penninckx, M. J. (1997) An important role for glutathione and γ-glutamyl-transpeptidase in the supply of growth requirements during nitrogen starvation of the yeast Saccharomyces cerevisiae. Microbiology 143, 1885-1889 (Pubitemid 27290278)
10. Ganguli, D., Kumar, C., and Bachhawat, A. K. (2007) The alternative pathway of glutathione degradation is mediated by a novel protein complex involving three new genes in Saccharomyces cerevisiae. Genetics 175, 1137-1151 (Pubitemid 46798219)
11. Kaur, H., Kumar, C., Junot, C., Toledano, M. B., and Bachhawat, A. K. (2009) Dug1p Is a Cys-Gly peptidase of the γ-glutamyl cycle of Saccharomyces cerevisiae and represents a novel family of Cys-Gly peptidases. J. Biol. Chem. 284, 14493-14502
12. Thomas, D., and Surdin-Kerjan, Y. (1997) Metabolism of sulfur amino acids in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 61, 503-532 (Pubitemid 28006958)
13. Baudouin-Cornu, P., and Labarre, J. (2006) Regulation of the cadmium stress response through SCF-like ubiquitin ligases. Comparison between Saccharomyces cerevisiae, Schizosaccharomyces pombe, and mammalian cells. Biochimie 88, 1673-1685 (Pubitemid 44781266)
14. Lee, T. A., Jorgensen, P., Bognar, A. L., Peyraud, C., Thomas, D., and Tyers, M. (2010) Dissection of combinatorial control by the Met4 transcriptional complex. Mol. Biol. Cell 21, 456-469
15. Pereira, Y., Lagniel, G., Godat, E., Baudouin-Cornu, P., Junot, C., and Labarre, J. (2008) Chromate causes sulfur starvation in yeast. Toxicol. Sci. 106, 400-412
16. Fauchon, M., Lagniel, G., Aude, J. C., Lombardia, L., Soularue, P., Petat, C., Marguerie, G., Sentenac, A., Werner, M., and Labarre, J. (2002) Sulfur sparing in the yeast proteome in response to sulfur demand. Mol. Cell 9, 713-723 (Pubitemid 34454884)
17. Barbey, R., Baudouin-Cornu, P., Lee, T. A., Rouillon, A., Zarzov, P., Tyers, M., and Thomas, D. (2005) Inducible dissociation of SCF(Met30) ubiquitin ligase mediates a rapid transcriptional response to cadmium. EMBO J. 24, 521-532 (Pubitemid 40343254)
18. Wallis, J. W., Chrebet, G., Brodsky, G., Rolfe, M., and Rothstein, R. (1989) A hyper-recombination mutation in Saccharomyces cerevisiae identifies a novel eukaryotic topoisomerase. Cell 58, 409-419 (Pubitemid 19191422)
19. Thomas, D., Becker, A., and Surdin-Kerjan, Y. (2000) Reverse methionine biosynthesis from S-adenosylmethionine in eukaryotic cells. J. Biol. Chem. 275, 40718-40724 (Pubitemid 32054889)
20. Mortimer, R. K., and Johnston, J. R. (1986) Genealogy of principal strains of the yeast genetic stock center. Genetics 113, 35-43 (Pubitemid 16042668)
21. Brachmann, C. B., Davies, A., Cost, G. J., Caputo, E., Li, J., Hieter, P., and Boeke, J. D. (1998) Designer deletion strains derived from Saccharomyces cerevisiae S288C. A useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14, 115-132 (Pubitemid 28062863)
22. Lafaye, A., Junot, C., Pereira, Y., Lagniel, G., Tabet, J. C., Ezan, E., and Labarre, J. (2005) Combined proteome and metabolite-profiling analyses reveal surprising insights into yeast sulfur metabolism. J. Biol. Chem. 280, 24723-24730 (Pubitemid 40934561)
23. Rahman, I., Kode, A., and Biswas, S. K. (2006) Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nat. Protoc. 1, 3159-3165
24. Baudouin-Cornu, P., Lagniel, G., Chédin, S., and Labarre, J. (2009) Development of a new method for absolute protein quantification on two-dimensional gels. Proteomics 9, 4606-4615
25. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, I. G., Smith, J. A., and Struhl, K. (2002) Short Protocols in Molecular Biology (5th Ed.), pp. 13-45-13-46, John Wiley & Sons, Inc., New York
26. 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 (Pubitemid 40024305)
27. Song, S. H., and Lim, C. J. (2008) Nitrogen depletion causes up-regulation of glutathione content and γ-glutamyl-transpeptidase in Schizosaccharomyces pombe. J. Microbiol. 46, 70-74
28. Huang, C. S., Moore, W. R., and Meister, A. (1988) On the active site thiol of γ-glutamylcysteine synthetase. Relationships to catalysis, inhibition, and regulation. Proc. Natl. Acad. Sci. U.S.A. 85, 2464-2468
29. Richman, P. G., and Meister, A. (1975) Regulation of γ-glutamyl- cysteine synthetase by nonallosteric feedback inhibition by glutathione. J. Biol. Chem. 250, 1422-1426
30. Jez, J. M., Cahoon, R. E., and Chen, S. (2004) Arabidopsis thaliana glutamate- cysteine ligase. Functional properties, kinetic mechanism, and regulation of activity. J. Biol. Chem. 279, 33463-33470 (Pubitemid 39066267)
31. Dennda, G., and Kula, M. R. (1986) Assay of the glutathione-synthesizing enzymes by high performance liquid chromatography. Biotechnol. Appl. Biochem. 8, 459-464
32. Biterova, E. I., and Barycki, J. J. (2010) Structural basis for feedback and pharmacological inhibition of Saccharomyces cerevisiae glutamate cysteine ligase. J. Biol. Chem. 285, 14459-14466
33. Grant, C. M., MacIver, F. H., and Dawes, I. W. (1997) Glutathione synthetase is dispensable for growth under both normal and oxidative stress conditions in the yeast Saccharomyces cerevisiae due to an accumulation of the dipeptide γ-glutamylcysteine. Mol. Biol. Cell 8, 1699-1707 (Pubitemid 27411135)
34. Russell, J. B. (2007) The energy spilling reactions of bacteria and other organisms. J. Mol. Microbiol. Biotechnol. 13, 1-11
35. Paolicchi, A., Tongiani, R., Tonarelli, P., Comporti, M., and Pompella, A. (1997) γ-Glutamyl-transpeptidase-dependent lipid peroxidation in isolated hepatocytes and HepG2 hepatoma cells. Free Radic. Biol. Med. 22, 853-860 (Pubitemid 27058349)
36. Paolicchi, A., Dominici, S., Pieri, L., Maellaro, E., and Pompella, A. (2002) Glutathione catabolism as a signaling mechanism. Biochem. Pharmacol. 64, 1027-1035 (Pubitemid 35232278)
37. Cuozzo, J. W., and Kaiser, C. A. (1999) Competition between glutathione and protein thiols for disufide bond formation. Nat. Cell Biol. 1, 130-135 (Pubitemid 129656016)
38. Vido, K., Spector, D., Lagniel, G., Lopez, S., Toledano, M. B., and Labarre, J. (2001) A proteome analysis of the cadmium response in Saccharomyces cerevisiae. J. Biol. Chem. 276, 8469-8474
39. Penninckx, M. J., and Jaspers, C. J. (1985) Molecular and kinetic properties of purified γ-glutamyl transpeptidase from yeast (Saccharomyces cerevisiae). Phytochemistry 24, 1913-1918
40. Ubiyvovk, V. M., Blazhenko, O. V., Gigot, D., Penninckx, M., and Sibirny, A. A. (2006) Role of γ-glutamyl-transpeptidase in detoxification of xenobiotics in the yeasts Hansenula polymorpha and Saccharomyces cerevisiae. Cell Biol. Int. 30, 665-671 (Pubitemid 44209331)
41. Wünschmann, J., Krajewski, M., Letzel, T., Huber, E. M., Ehrmann, A., Grill, E., and Lendzian, K. J. (2010) Dissection of glutathione conjugate turnover in yeast. Phytochemistry 71, 54-61
42. Kacser, H., and Burns, J. A. (1995) The control of flux. Biochem. Soc. Trans. 23, 341-366
43. Fell, D. A. (2005) Enzymes, metabolites, and fluxes. J. Exp. Bot. 56, 267-272
44. Fendt, S. M., Buescher, J. M., Rudroff, F., Picotti, P., Zamboni, N., and Sauer, U. (2010) Tradeoff between enzyme and metabolite efficiency maintains metabolic homeostasis upon perturbations in enzyme capacity. Mol. Syst. Biol. 6, 356
45. Messenguy, F., Colin, D., and ten Have, J. P. (1980) Regulation of compartmentation of amino acid pools in Saccharomyces cerevisiae and its effects on metabolic control. Eur. J. Biochem. 108, 439-447 (Pubitemid 11227409)
46. Godat, E., Madalinski, G., Muller, L., Heilier, J. F., Labarre, J., and Junot, C. (2010) Mass spectrometry-based methods for the determination of sulfur and related metabolite concentrations in cell extracts. Methods Enzymol. 473, 41-76
47. Spector, D., Labarre, J., and Toledano, M. B. (2001)Agenetic investigation of the essential role of glutathione. Mutations in the proline biosynthesis pathway are the only suppressors of glutathione auxotrophy in yeast. J. Biol. Chem. 276, 7011-7016