Glutathione degradation by the alternative pathway (DUG pathway) in Saccharomyces cerevisiae is initiated by (Dug2p-Dug3p)2 complex, a novel glutamine amidotransferase (GATase) enzyme acting on glutathione

Journal of Biological Chemistry

Volumn 287, Issue 12, 2012, Pages 8920-8931

  Kaur, Hardeep ^a   Ganguli, Dwaipayan ^a,c   Bachhawat, Anand K ^a,b  

^a INSTITUTE OF MICROBIAL TECHNOLOGY   (India)

^b INDIAN INSTITUTE OF SCIENCE EDUCATION AND RESEARCH MOHALI   (India)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GEL-FILTRATION CHROMATOGRAPHY; GLUTATHIONES; HOMODIMERIZE; IN-VITRO; MICHAELIS-MENTEN KINETIC; N-TERMINALS; PEPTIDASE ACTIVITY; RECONSTITUTION ASSAY; SULFUR LIMITATION;

AMINO ACIDS; DEGRADATION; ENZYMES; GEL PERMEATION CHROMATOGRAPHY; GENES; MOLECULAR WEIGHT; OLIGOMERS; YEAST;

PEPTIDES;

CYSTEINYLGLYCINE; FUNGAL PROTEIN; GLUTAMIC ACID; GLUTAMINE AMIDOTRANSFERASE; GLUTATHIONE; PROTEIN DUG1; PROTEIN DUG2; PROTEIN DUG2P; PROTEIN DUG3; PROTEIN DUG3P; SULFUR; TRANSFERASE; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; COMPLEX FORMATION; CONTROLLED STUDY; DIMERIZATION; DUG1 GENE; DUG2 GENE; DUG3 GENE; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME PURIFICATION; ESCHERICHIA COLI; FUNGAL GENE; FUNGAL METABOLISM; GEL FILTRATION CHROMATOGRAPHY; IN VITRO STUDY; MICHAELIS MENTEN KINETICS; MOLECULAR WEIGHT; MUTATIONAL ANALYSIS; NONHUMAN; NUTRIENT LIMITATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; CARBON-NITROGEN LIGASES; DIPEPTIDASES; GLUTAMIC ACID; GLUTATHIONE; KINETICS; MOLECULAR SEQUENCE DATA; PEPTIDE HYDROLASES; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SUBSTRATE SPECIFICITY; SULFUR; TRANSAMINASES;

FUNGI; SACCHAROMYCES CEREVISIAE;

EID: 84858587958     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.327411     Document Type: Article

References (38)

1. Fahey, R. C., and Newton, G. L. (1987) Determination of low molecular weight thiols using monobromobimane fluorescent labeling and high-performance liquid chromatography. Methods Enzymol. 143, 85-96
2. Meister, A., and Anderson, M. E. (1983) Glutathione. Annu. Rev. Biochem. 52, 711-760 (Pubitemid 13030692)
3. Penninckx, M. J. (2002) An overview on glutathione in Saccharomyces versus non-conventional yeasts. FEMS Yeast Res. 2, 295-305
4. Barouki, R., Finidori, J., Chobert, M. N., Aggerbeck, M., Laperche, Y., and Hanoune, J. (1984) Biosynthesis and processing of γ-glutamyl transpeptidase in hepatoma tissue culture cells. J. Biol. Chem. 259, 7970-7974 (Pubitemid 14081220)
5. Griffith, O. W., and Meister, A. (1979) Translocation of intracellular glutathione to membrane-bound γ-glutamyl transpeptidase as a discrete step in the γ-glutamyl cycle: glutathionuria after inhibition of transpeptidase. Proc. Natl. Acad. Sci. U.S.A. 76, 268-272 (Pubitemid 9081758)
6. Nakano, Y., Okawa, S., Prieto, R., and Sekiya, J. (2006) Subcellular localization and possible functions of γ-glutamyltransferase in the radish (Raphanus sativus L.) plant. Biosci. Biotechnol. Biochem. 70, 1790-1793 (Pubitemid 44124945)
7. Mehdi, K., Thierie, J., and Penninckx, M. J. (2001) γ-Glutamyl transpeptidase in the yeast Saccharomyces cerevisiae and its role in the vacuolar transport and metabolism of glutathione. Biochem. J. 359, 631-637 (Pubitemid 33063388)
8. Jaspers, C. J., and Penninckx, M. J. (1984) Glutathione metabolism in yeast Saccharomyces cerevisiae: evidence that γ-glutamyl transpeptidase is a vacuolar enzyme. Biochimie 66, 71-74
9. 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 glutathione degradation pathway. FEMS Microbiol. Lett. 219, 187-194 (Pubitemid 36302596)
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. Stirnimann, C. U., Petsalaki, E., Russell, R. B., and Müller, C. W. (2010) WD40 proteins propel cellular networks. Trends Biochem. Sci. 35, 565-574
12. Smith, T. F., Gaitatzes, C., Saxena, K., and Neer, E. J. (1999) The WD repeat: a common architecture for diverse functions. Trends Biochem. Sci. 24, 181-185 (Pubitemid 29348450)
13. 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
14. Ito, S., Miyahara, R., Takahashi, R., Nagai, S., Takenaka, K., Wada, H., and Tanaka, F. (2009) Stromal aminopeptidase N expression: correlation with angiogenesis in non-small cell lung cancer. Gen. Thorac. Cardiovasc. Surg. 57, 591-598
15. Guthrie, C., and Fink, G. R. (1991) Guide to yeast genetics and molecular biology. Methods Enzymol. 194, 1-863
16. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning: a Laboratory Manual, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
17. Gyuris, J., Golemis, E., Chertkov, H., and Brent, R. (1993) Cdi1, a human G1 and S phase protein phosphatase that associates with Cdk2. Cell 75, 791-803 (Pubitemid 23346376)
18. Penninckx, M., Jaspers, C., and Wiame, J. M. (1980) Glutathione metabolism in relation to the amino acid permeation systems of the yeast Saccharomyces cerevisiae. Occurrence of γ-glutamyl transpeptidase: its regulation and the effects of permeation mutations on the enzyme cellular level. Eur. J. Biochem. 104, 119-123 (Pubitemid 10099515)
19. Ohkama-Ohtsu, N., Oikawa, A., Zhao, P., Xiang, C., Saito, K., and Oliver, D. J. (2008) A γ-glutamyl transpeptidase-independent pathway of glutathione catabolism to glutamate via 5-oxoproline in Arabidopsis. Plant Physiol. 148, 1603-1613 (Pubitemid 352847494)
20. Gaitonde, M. K. (1967) A spectrophotometric method for the direct determination of cysteine in the presence of other naturally occurring amino acids. Biochem. J. 104, 627-633
21. Guarente, L. (1983) Yeast promoters and lacZ fusions designed to study expression of cloned genes in yeast. Methods Enzymol. 101, 181-191
22. Jösch, C., Klotz, L. O., and Sies, H. (2003) Identification of cytosolic leucyl aminopeptidase (EC 3.4.11.1) as the major cysteinyl-glycine- hydrolyzing activity in rat liver. Biol. Chem. 384, 213-218 (Pubitemid 36348320)
23. Cappiello, M., Lazzarotti, A., Buono, F., Scaloni, A., D'Ambrosio, C., Amodeo, P., Méndez, B. L., Pelosi, P., Del Corso, A., and Mura, U. (2004) New role for leucyl aminopeptidase in glutathione turnover. Biochem. J. 378, 35-44 (Pubitemid 38304951)
24. Zalkin, H. (1993) The amidotransferases. Adv. Enzymol. Relat. Areas Mol. Biol. 66, 203-309
25. Massière, F., and Badet-Denisot, M. A. (1998) The mechanism of glutamine-dependent amidotransferases. Cell. Mol. Life Sci. 54, 205-222 (Pubitemid 28167481)
26. Muchmore, C. R., Krahn, J. M., Kim, J. H., Zalkin, H., and Smith, J. L. (1998) Crystal structure of glutamine phosphoribosylpyrophosphate amidotransferase from Escherichia coli. Protein Sci. 7, 39-51 (Pubitemid 28133744)
27. Mouilleron, S., Badet-Denisot, M. A., and Golinelli-Pimpaneau, B. (2006) Glutamine binding opens the ammonia channel and activates glucosamine-6P synthase. J. Biol. Chem. 281, 4404-4412 (Pubitemid 43847872)
28. Larsen, T. M., Boehlein, S. K., Schuster, S. M., Richards, N. G., Thoden, J. B., Holden, H. M., and Rayment, I. (1999) Three-dimensional structure of Escherichia coli asparagine synthetase B: a short journey from substrate to product. Biochemistry 38, 16146-16157 (Pubitemid 129520535)
29. Milewski, S. (2002) Glucosamine-6-phosphate synthase: the multi-facets enzyme. Biochim. Biophys. Acta 1597, 173-192
30. van den Heuvel, R. H., Curti, B., Vanoni, M. A., and Mattevi, A. (2004) Glutamate synthase: a fascinating pathway from L-glutamine to L-glutamate. Cell. Mol. Life Sci. 61, 669-681 (Pubitemid 38446411)
31. Smith, J. L. (1998) Glutamine PRPP amidotransferase: snapshots of an enzyme in action. Curr. Opin. Struct. Biol. 8, 686-694
32. Oinonen, C., and Rouvinen, J. (2000) Structural comparison of Ntn hydrolases. Protein Sci. 9, 2329-2337
33. Rawlings, N. D., Morton, F. R., and Barrett, A. J. (2006) MEROPS: the peptidase database. Nucleic Acids Res. 34, D270-D272
34. Springael, J. Y., and Penninckx, M. J. (2003) Nitrogen source regulation of yeast glutamyl transpeptidase-glutamyl transpeptidase synthesis involves the regulatory network including the GATA zinc-finger factors Gln3, Nil1/Gat1, and Gzf3. Biochem. J. 371, 589-595
35. Thomas, D., and Surdin-Kerjan, Y. (1997) Metabolism of sulfur amino acids in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 61, 503-532 (Pubitemid 28006958)
36. Thomas, D., Jacquemin, I., and Surdin-Kerjan, Y. (1992) MET4, a leucine zipper protein, and centromere-binding factor 1 are both required for transcriptional activation of sulfur metabolism in Saccharomyces cerevisiae. Mol. Cell. Biol. 12, 1719-1727
37. Kuras, L., Cherest, H., Surdin-Kerjan, Y., and Thomas, D. (1996) A heteromeric complex containing the centromere-binding factor 1 and two basic leucine zipper factors, Met4 and Met28, mediates the transcription activation of yeast sulfur metabolism. EMBO J. 15, 2519-2529 (Pubitemid 26151191)
38. Blaiseau, P. L., Isnard, A. D., Surdin-Kerjan, Y., and Thomas, D. (1997) Met31p and Met32p, two related zinc finger proteins, are involved in transcriptional regulation of yeast sulfur amino acid metabolism. Mol. Cell. Biol. 17, 3640-3648 (Pubitemid 27281839)