γ-glutamylcysteine synthetase-glutathione synthetase: Domain structure and identification of residues important in substrate and glutathione binding

Biochemistry

Volumn 45, Issue 35, 2006, Pages 10461-10473

  Janowiak, Blythe E ^a,b   Hayward, Michael A ^a   Peterson, Francis C ^a   Volkman, Brian F ^a   Griffith, Owen W ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIODIVERSITY; ENZYME INHIBITION; ENZYMES; ESCHERICHIA COLI; MUTAGENS; SUBSTRATES; SYNTHESIS (CHEMICAL);

GLUTAMYLCYSTEINE SYNTHETASE; GLUTATHIONE (GSH); PASTEURELLA MULTOCIDA; STREPTOCOCCUS AGALACTIAE;

ENZYME KINETICS;

ADENOSINE TRIPHOSPHATE; DEXTRO ALANINE; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE; GLUTATHIONE SYNTHASE;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CHIMERA; CONTROLLED STUDY; COVALENT BOND; ENTEROCOCCUS FAECALIS; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REGULATION; ENZYME SUBSTRATE COMPLEX; ESCHERICHIA COLI; NONHUMAN; PASTEURELLA MULTOCIDA; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN STRUCTURE; SITE DIRECTED MUTAGENESIS; STREPTOCOCCUS AGALACTIAE;

AMINO ACID SEQUENCE; BINDING SITES; CIRCULAR DICHROISM; DIPEPTIDES; ENTEROCOCCUS FAECALIS; GLUTAMATE-CYSTEINE LIGASE; GLUTATHIONE; GLUTATHIONE SYNTHASE; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROTEIN FOLDING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; STREPTOCOCCUS AGALACTIAE;

ENTEROCOCCUS FAECALIS; ESCHERICHIA COLI; PASTEURELLA MULTOCIDA; STREPTOCOCCUS AGALACTIAE;

EID: 33748256537     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi052483v     Document Type: Article

References (47)

1. Fahey, R. C., Newton, G. L., Arrick, B., Overdank-Bogart, T., and Aley, S. B. (1984) Entamoeba histolytica: a eukaryote without glutathione metabolism, Science 224, 70-72.
2. Newton, G. L., Arnold, K., Price, M. S., Sherrill, C., Delcardayre, S. B., Aharonowitz, Y., Cohen, G., Davies, J., Fahey, R. C., and Davis, C. (1996) Distribution of thiols in microorganisms: mycothiol is a major thiol in most actinomycetes, J. Bacteriol. 178, 1990-1995.
3. Fahey, R. C., Brown, W. C., Adams, W. B., and Worsham, M. B. (1978) Occurrence of glutathione in bacteria, J. Bacteriol. 133, 1126-1129.
4. Sherrill, C., and Fahey, R. C. (1998) Import and metabolism of glutathione by Streptococcus mutans, J. Bacteriol. 180, 1454-1459.
5. Janowiak, B. E., and Griffith, O. W. (2005) Glutathione synthesis in Streptococcus agalactiae. One protein accounts for gamma-glutamylcysteine synthetase and glutathione synthetase activities, J. Biol. Chem. 280, 11829-39.
6. Gopal, S., Borovok, I., Ofer, A., Yanku, M., Gohen, G., Goebel, W., Kreft, J., Aharonowitz, Y. (2005) A multidomain fusion protein in Listeria monocytogenes catalyzes the two primary activites for glutathione biosynthesis, J. Bacteriol. 187, 3839-3847.
7. Vergauwen, B., De Vos, D., and Beeumen, J. J. (2006) Characterization of the bifunctional γ-glutamate-cysteine ligase-glutathione synthetase (GshF) of Pasteurella multocida, J. Biol. Chem. 281, 4380-4394.
8. Strumeyer, D., and Bloch, K. (1962) gamma-L-glutamyl-L-cysteine from glutathione, Biochem. Prep. 9, 52-55.
9. Dougherty, W. G., Cary, S. M., and Parks, T. D. (1989) Molecular genetic analysis of a plant virus polyprotein cleavage site: a model, Virology 171, 356-364.
10. Waltner, J. K., Peterson, F. C., Lytle, B. L., and Volkman, B. F. (2005) Structure of the B3 domain from Arabidopsis thaliana protein At1g16640, Protein Sci. 14, 2478-2483.
11. Paulsen, I. T., Banerjei, L., Myers, G. S. A., Nelson, K. E., Seshadri, R., Read, T. D., Fouts, D. E., Eisen, J. A., Gill, S. R., Heidelberg, J. F., Tettelin, H., Dodson, R. J., Umayam, L., Brinkac, L., Beanan, M., Daugherty, S., DeBoy, R. T., Durkin, S., Kolonay, J., Madupu, R., Nelson, W., Vamathevan, J., Tran, B., Upton, J., Hansen, T., Shetty, J., Khouri, H., Utterback, T., Radune, D., Ketchum, K. A., Dougherty, B. A., Fraser, C. M. (2003) Role of mobile DNA in the evolution of vancomycin-resistant Enterococcus faecalis, Science 299, 2071-2074.
12. Weber, D. J., Gittis, A. G., Mullen, G. P., Abeygunawardana, C., Lattman, E. E., and Mildvan, A. S. (1992) NMR docking of a substrate into the X-ray structure of staphylococcal nuclease, Proteins 13, 275-287.
13. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem. 72, 248-254.
14. Pace, C. N., Vajdos, F., Fee, L., Grimsley, G., and Gray, T. (1995) How to measure and predict the molar absorption coefficient of a protein, Protein Sci. 4, 2411-2423.
15. Mori, S., Abeygunawardana, C., Johnson, M. O., and van Zijl, P. C. (1995) Improved sensitivity of HSQC spectra of exchanging protons at short interscan delays using a new fast HSQC (FHSQC) detection scheme that avoids water saturation, J. Magn. Reson. B 108, 94-98
16. [erratum: (1996) J. Magn. Reson. B 110, 321].
17. Pervushin, K., Riek, R., Wider, G., and Wuthrich, K. (1997) Attenuated T2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution, Proc. Natl. Acad. Sci. U.S.A. 94, 12366-12371.
18. Notredame, C., Higgins, D. G., and Heringa, J. (2000) T-coffee: a novel method for fast and accurate multiple sequence alignment, J. Mol. Biol. 302, 205-217.
19. Hibi, T., Nii, H., Nakatsu, T., Kimura, A., Kato, H., Hiratake, J., and Oda, J. (2004) Crystal structure of gamma-glutamylcysteine synthetase: insights into the mechanism of catalysis by a key enzyme for glutathione homeostasis, Proc. Natl. Acad. Sci. U.S.A. 101, 15052-15057.
20. Eswar, N., John, B., Mirkovic, N., Fiser, A., Ilyin, V. A., Pieper, U., Stuart, A. C., Marti-Renom, M. A., Madhusudhan, M. S., Yerkovich, B., and Sali, A. (2003) Tools for comparative protein structure modeling and analysis, Nucleic Acids Res. 31, 3375-3380.
21. Fiser, A., and Sali, A. (2003) Modeller: generation and refinement of homology-based protein structure models, Methods Enzymol. 374, 461-491.
22. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) PROCHECK: a program to check the stereochemical quality of protein structures, J. Appl. Crystallogr. 26, 283-291.
23. Pontius, J., Richelle, J., and Wodak, S. J. (1996) Deviations from standard atomic volumes as a quality measure for protein crystal structures, J. Mol. Biol. 264, 121-136.
24. Melo, F., and Feytmans, E. (1998) Assessing protein structures with a nonlocal atomic interaction energy, J. Mol. Biol. 277, 1141-1152.
25. Colovos, C., and Yeates, T. O. (1993) Verification of protein structures: Patterns of nonbonded atomic interactions, Protein Sci. 2, 1511-1519.
26. Inoue, Y., Iba, Y., Yano, H., Murata, K., and Kimura, A. (1993) Functional analysis of the gamma-glutamylcysteine synthetase of Escherichia coli B: effect of substitution of His-150 to Ala, Appl. Microbiol. Biotechnol. 38, 473-477.
27. 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.
28. Griffith, O. W., and Mulcahy, R. T. (1999) The enzymes of glutathione synthesis: gamma-glutamylcysteine synthetase, Adv. Enzymol. Relat. Subj. Biochem. 73, 209-267.
29. Kelly, B. S., Antholine, W. E., and Griffith, O. W. (2002) Escherichia coli gamma-glutamylcysteine synthetase. Two active site metal ions affect substrate and inhibitor binding, J. Biol. Chem. 277, 50-58.
30. Misra, I., and Griffith, O. W. (1998) Expression and purification of human gamma-glutamylcysteine synthetase, Protein Expression Purif. 13, 268-276.
31. Fan, C., Moews, P. C., Walsh, C. T., and Knox, J. R. (1994) Vancomycin resistance: structure of D-alanine:D-alanine ligase at 2.3 Å resolution, Science 266, 439-443.
32. Hara, T., Kato, H., Katsube, Y., and Oda, J. (1996) A pseudomichaelis quaternary complex in the reverse reaction of a ligase: structure of Escherichia coli B glutathione synthetase complexed with ADP, glutathione, and sulfate at 2.0 Å resolution, Biochemistry 35, 11967-11974.
33. Fan, C., Moews, P. C., Shi, Y., Walsh, C. T., and Knox, J. R. (1995) A common fold for peptide synthetases cleaving ATP to ADP: glutathione synthetase and D-alanine:D-alanine ligase of Escherichia coli, Proc. Natl. Acad. Sci. U.S.A. 92, 1172-1176.
34. Shi, Y., and Walsh, C. T. (1995) Active site mapping of Escherichia coli D-Ala-D-Ala ligase by structure-based mutagenesis, Biochemistry 34, 2768-2776.
35. Tu, Z., and Anders, M. W. (1998) Expression and characterization of human glutamate-cysteine ligase, Arch. Biochem. Biophys. 354, 247-254.
36. Sekura, R., and Meister, A. (1977) gamma-Glutamylcysteine synthetase. Further purification, "half of the sites" reactivity, subunits, and specificity, J. Biol. Chem. 252, 2599-2605.
37. May, M. J., and Leaver, C. J. (1994) Arabidopsis thaliana gamma-glutamylcysteine synthetase is structurally unrelated to mammalian, yeast, and Escherichia coli homologs, Proc. Natl. Acad. Sci. U.S.A. 91, 10059-10063.
38. Lueder, D. V., and Phillips, M. A. (1996) Characterization of Trypanosoma brucei gamma-glutamylcysteine synthetase, an essential enzyme in the biosynthesis of trypanothione (diglutathionylspermidine), J. Biol. Chem. 271, 17485-17490.
39. Hussein, A. S., and Walter, R. D. (1995) Purification and characterization of gamma-glutamylcysteine synthetase from Ascaris suum, Mol. Biochem. Parasitol. 72, 57-64.
40. Brekken, D. L., and Phillips, M. A. (1998) Trypanosoma brucei gamma-glutamylcysteine synthetase. Characterization of the kinetic mechanism and the role of Cys-319 in cystamine inactivation, J. Biol. Chem. 273, 26317-26322.
41. 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.
42. Phlippen, N., Hoffmann, K., Fischer, R., Wolf, K., and Zimmermann, M. (2003) The glutathione synthetase of Schizosaccharomyces pombe is synthesized as a homodimer but retains full activity when present as a heterotetramer, J. Biol. Chem. 278, 40152-40161.
43. Huang, C. S., Moore, W. R., and Meister, A. (1988) On the active site thiol of gamma-glutamylcysteine synthetase: relationships to catalysis, inhibition, and regulation, Proc. Natl. Acad. Sci. U.S.A. 85, 2464-2468.
44. Huang, C.-S., Chang, L.-S., Anderson, M. E., and Meister, A. (1993) Catalytic and regulatory properties of the heavy subunit of rat kidney γ-glutamylcysteine synthetase, J. Biol. Chem. 268, 19675-19680.
45. Meister, A., and Anderson, M. E. (1983) Glutathione, Annu. Rev. Biochem. 52, 711-760.
46. Cayley, S., Lewis, B. A., Guttman, H. J., and Record, M. T., Jr. (1991) Characterization of the cytoplasm of Escherichia coli K-12 as a function of external osmolarity. Implications for protein-DNA interactions in vivo, J. Mol. Biol. 222, 281-300.
47. Griffith, O. W. (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine, Anal. Biochem. 106, 207-212.