A functionally conserved basic residue in glutathione transferases interacts with the glycine moiety of glutathione and is pivotal for enzyme catalysis

Biochemical Journal

Volumn 406, Issue 2, 2007, Pages 247-256

  Vararattanavech, Ardcharaporn ^a   Ketterman, Albert J ^a  

^a MAHIDOL UNIVERSITY   (Thailand)

Author keywords

Base assisted deprotonation model; Conserved active site residue; Delta class GST; Enzyme catalysis; Glutathione transferase (GST); Glycine moiety of glutathione (GSH)

Indexed keywords

CATALYSIS; DEPROTONATION; ENZYME ACTIVITY; HYDROGEN BONDS; IONIZATION; MATHEMATICAL MODELS;

BASE-ASSISTED DEPROTONATION MODELS; CONSERVED ACTIVE-SITE RESIDUE; DELTA CLASS GST; ENZYME CATALYSIS; GLUTATHIONE TRANSFERASE (GST); GLYCINE MOIETY OF GLUTATHIONE (GSH);

ENZYME KINETICS;

CYSTEINE; GLUTAMINE; GLUTATHIONE; GLUTATHIONE TRANSFERASE; GLYCINE; HISTIDINE;

ARTICLE; CATALYSIS; ENZYME SPECIFICITY; HYDROGEN BOND; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION;

BINDING SITES; CATALYSIS; DINITROCHLOROBENZENE; ENZYME STABILITY; GLUTATHIONE; GLUTATHIONE TRANSFERASE; GLYCINE; HYDROGEN BONDING; HYDROGEN-ION CONCENTRATION; KINETICS; MODELS, MOLECULAR; MUTATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SUBSTRATE SPECIFICITY; TEMPERATURE; VISCOSITY;

EID: 34548169608     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20070422     Document Type: Article

References (47)

1. 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
2. Ketterer, B. (2001) A bird's eye view of the glutathione transferase field. Chem. Biol. Interact. 138, 27-42
3. Mannervik, B., Awasthi, Y. C., Board, P. G., Hayes, J. D., Di Ilio, C., Ketterer, B., Listowsky, I., Morgenstern, R., Muramatsu, M., Pearson, W. R. et al. (1992) Nomenclature for human glutathione transferases. Biochem. J. 282, 305-306
4. Hayes, J. D., Flanagan, J. U. and Jowsey, I. R. (2005) Glutathione transferases. Annu. Rev. Pharmacol. Toxicol. 45, 51-88
5. Mannervik, B. and Danielson, U. H. (1988) Glutathione transferases - structure and catalytic activity. CRC Crit. Rev. Biochem. 23, 283-337
6. Armstrong, R. N. (1997) Structure, catalytic mechanism, and evolution of the glutathione transferases. Chem. Res. Toxicol. 10, 2-18
7. Wilce, M. C. J., Board, P. G., Feil, S. C. and Parker, M. W. (1995) Crystal structure of a theta-class glutathione transferase. EMBO J. 14, 2133-2143
8. Dirr, H., Reinemer, P. and Huber, R. (1994) X-ray crystal structures of cytosolic glutathione S-transferases. Implications for protein architecture, substrate recognition and catalytic function. Eur. J. Biochem. 220, 645-661
9. Rossjohn, J., Feil, S. C., Wilce, M. C. J., Sexton, J., Spithill, T. W. and Parker, M. W. (1997) Crystallization, structural determination and analysis of a novel parasite vaccine candidate: Fasciola hepatica glutathione S-transferase. J. Mol. Biol. 273, 857-872
10. Stenberg, G., Board, P. G., Carlberg, I. and Mannervik, B. (1991) Effects of directed mutagenesis on conserved arginine residues in a human class Alpha glutathione transferase. Biochem. J. 274, 549-555
11. Lin, S., Zhang, P., Ji, X., Johnson, W. W., Gilliland, G. L. and Armstrong, R. N. (1992) Contribution of tyrosine 6 to the catalytic mechanism of isoenzyme 3-3 of glutathione S-transferase. J. Biol. Chem. 267, 4296-4299
12. Kolm, R. H., Sroga, G. E. and Mannervik, B. (1992) Participation of the phenolic hydroxyl group of Tyr-8 in the catalytic mechanism of human glutathione transferase P1-1. Biochem. J. 285, 537-540
13. Caccuri, A. M., Antonini, G., Nicotra, M., Battistoni, A., Lo Bello, M., Board, P. G., Parker, M. W. and Ricci, G. (1997) Catalytic mechanism and role of hydroxyl residues in the active site of theta class glutathione S-transferases. Investigation of Ser-9 and Tyr-113 in a glutathione S-transferase from the Australian sheep blowfly, Lucilia cuprina. J. Biol. Chem. 272, 29681-29686
14. Tan, K.-L., Chelvanayagam, G., Parker, M. W. and Board, P. G. (1996) Mutagenesis of the active site of the human Theta-class glutathione transferase GSTT2-2: catalysis with different substrates involves different residues. Biochem. J. 319, 315-321
15. Winayanuwattikun, P. and Ketterman, A. J. (2004) Catalytic and structural contributions for glutathione binding residues in a Delta class glutathione S-transferase. Biochem. J. 382, 751-757
16. 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
17. Winayanuwattikun, P. and Ketterman, A. J. (2007) Glutamate 64, a newly identified residue of the functionally conserved electron-sharing network contributes to catalysis and structural integrity of glutathione transferases. Biochem. J. 402, 339-348
18. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C. and Ferrin, T. E. (2004) UCSF chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612
19. Vararattanavech, A. and Ketterman, A. (2003) Multiple roles of glutathione binding-site residues of glutathione S-transferase. Protein Peptide Lett. 10, 441-448
20. Vararattanavech, A., Prommeenate, P. and Ketterman, A. J. (2006) The structural roles of a conserved small hydrophobic core in the active site and an ionic bridge in domain I of Delta class glutathione S-transferase. Biochem. J. 393, 89-95
21. Habig, W. H., Pabst, M. J. and Jakoby, W. B. (1974) Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J. Biol. Chem. 249, 7130-7139
22. Segel, I. H. (1993) Enzyme Kinetics, Behavior and Analysis of Rapid Equilibrium and Steady-state Enzyme Systems, John Wiley and Sons, New York
23. Jirajaroenrat, K., Pongjaroenkit, S., Krittanai, C., Prapanthadara, L. and Ketterman, A. J. (2001) Heterologous expression and characterization of alternatively spliced glutathione S-transferases from a single Anopheles gene. Insect Biochem. Mol. Biol. 31, 867-875
24. Caccuri, A. M., Ascenzi, P., Lo Bello, M., Federici, G., Battistoni, A., Mazzetti, P. and Ricci, G. (1994) Are the steady state kinetics of glutathione transferase always dependent on the deprotonation of the bound glutathione? New insights in the kinetic mechanism of GST P1-1. Biochem. Biophys. Res. Commun. 200, 1428-1434
25. Wolf, A. V., Brown, M. G. and Prentiss, P. G. (1985) Handbook of Chemistry and Physics, CRC Press, Boca Raton, FL
26. Armstrong, R. N., Rife, C. and Wang, Z. (2001) Structure, mechanism and evolution of thiol transferases. Chem. Biol. Interact. 133, 167-169
27. Caccuri, A. M., Ascenzi, P., Antonini, G., Parker, M. W., Oakley, A. J., Chiessi, E., Nuccetelli, M., Battistoni, A., Bellizia, A. and Ricci, G. (1996) Structural flexibility modulates the activity of human glutathione transferase P1-1. Influence of a poor co-substrate on dynamics and kinetics of human glutathione transferase. J. Biol. Chem. 271, 16193-16198
28. Caccuri, A. M., Lo Bello, M., Nuccetelli, M., Rossi, P., Antonini, G., Federici, G. and Ricci, G. (1998) Proton release upon glutathione binding to glutathione transferase P1-1: kinetic analysis of a multistep glutathione binding process. Biochemistry 37, 3028-3034
29. Armstrong, R. N. (1997) Structure, catalytic mechanism, and evolution of the glutathione transferases. Chem. Res. Toxicol. 10, 2-18
30. Gustafsson, A., Pettersson, P. L., Grehn, L., Jemth, P. and Mannervik, B. (2001) Role of the glutamyl α-carboxylate of the substrate glutathione in the catalytic mechanism of human glutathione transferase A1-1. Biochemistry 40, 15835-15845
31. Widersten, M., Björnestedt, R. and Mannervik, B. (1996) Involvement of the carboxyl groups of glutathione in the catalytic mechanism of human glutathione transferase A1-1. Biochemistry 35, 7731-7742
32. Johnson, W. W., Liu, S., Ji, X., Gilliland, G. L. and Armstrong, R. N. (1993) Tyrosine 115 participates both in chemical and physical steps of the catalytic mechanism of a glutathione S-transferase. J. Biol. Chem. 268, 11508-11511
33. Ricci, G., Caccuri, A. M., Lo Bello, M., Rosato, N., Mei, G., Nicotra, M., Chiessi, E., Mazzetti, A. P. and Federici, G. (1996) Structural flexibility modulates the activity of human glutathione transferase P1-1. Role of helix 2 flexibility in the catalytic mechanism. J. Biol. Chem. 271, 16187-16192
34. Dirr, H. W., Little, T., Kuhnert, D. C. and Sayed, Y. (2005) A conserved N-capping motif contributes significantly to the stabilization and dynamics of the C-terminal region of class alpha glutathione transferases. J. Biol. Chem. 280, 19480-19487
35. Lo Bello, M., Nuccetelli, M., Chiessi, E., Lahm, A., Mazzetti, A. P., Parker, M. W., Tramontano, A., Federici, G. and Ricci, G. (1998) Mutations of Gly to Ala in human glutathione transferase P1-1 affect helix 2 (G-site) and induce positive cooperativity in the binding of glutathione. J. Mol. Biol. 284, 1717-1725
36. Labrou, N. E., Mello, L. V. and Clonis, Y. D. (2001) Functional and structural roles of the glutathione-binding residues in maize (Zea mays) glutathione S-transferase I. Biochem. J. 358, 101-110
37. Labrou, N. E., Mello, L. V. and Clonis, Y. D. (2001) The conserved Asn49 of maize glutathione S-transferase I modulates substrate binding, catalysis and intersubunit communication. Eur. J. Biochem. 268, 3950-3957
38. Principato, G. B., Danielson, U. H. and Mannervik, B. (1988) Relaxed thiol substrate specificity of glutathione transferase effected by a non-substrate glutathione derivative. FEBS Lett. 231, 155-158
39. Jemth, P. and Mannervik, B. (1999) Fast product formation and slow product release are important features in a hysteretic reaction mechanism of glutathione transferase T2-2. Biochemistry 38, 9982-9991
40. Wang, J., Barycki, J. J. and Colman, R. F. (1996) Tyrosine 8 contributes to catalysis but is not required for activity of rat liver glutathione S-transferase, 1-1. Protein Sci. 5, 1032-1042
41. Gustafsson, A., Etahadieh, M., Jemth, P. and Mannervik, B. (1999) The C-terminal region of human glutathione transferase A1-1 affects the rate of glutathione binding and the ionization of the active-site Tyr9. Biochemistry 38, 16268-16275
42. Labrou, N. E., Rigden, D. J. and Clonis, Y. D. (2003) Engineering the pH-dependence of kinetic parameters of maize glutathione S-transferase I by site-directed mutagenesis. Biomol. Eng. 21, 61-66
43. Patskovsky, Y. V., Patskovska, L. N. and Listowsky, I. (2000) The enhanced affinity for thiolate anion and activation of enzyme-bound glutathione is governed by an arginine residue of human Mu class glutathione S-transferases. J. Biol. Chem. 275, 3296-3304
44. Björnestedt, R., Tardioli, S. and Mannervik, B. (1995) The high activity of rat glutathione transferase 8-8 with alkene substrates is dependent on a glycine residue in the active site. J. Biol. Chem. 270, 29705-29709
45. Garcia-Viloca, M., Gao, J., Karplus, M. and Truhlar, D. G. (2004) How enzymes work: analysis by modern rate theory and computer simulations. Science 303, 186-195
46. Caccuri, A. M., Antonini, G., Board, P. G., Parker, M. W., Nicotra, M., Lo Bello, M., Federici, G. and Ricci, G. (1999) Proton release on binding of glutathione to Alpha, Mu and Delta class glutathione transferases. Biochem. J. 344, 419-425
47. Caccuri, A. M., Antonini, G., Board, P. G., Flanagan, J., Parker, M. W., Paolesse, R., Turella, P., Federici, G., Lo Bello, M. and Ricci, G. (2001) Human glutathione transferase T2-2 discloses some evolutionary strategies for optimization of substrate binding to the active site of glutathione transferases. J. Biol. Chem. 276, 5427-5431