Structural contributions of Delta class glutathione transferase active-site residues to catalysis

Biochemical Journal

Volumn 428, Issue 1, 2010, Pages 25-32

  Wongsantichon, Jantana ^a   Robinson, Robert C ^b   Ketterman, Albert J ^a  

^a MAHIDOL UNIVERSITY   (Thailand)

^b INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

Author keywords

Crystal structure; Glutathione transferase (GST); Structural motif; Structure function relationship; Substrate specificity

Indexed keywords

C-TERMINAL DOMAINS; CO-SUBSTRATE; CONFORMATIONAL STABILITIES; CRYSTALLOGRAPHIC STUDIES; DIMERIC ENZYME; DIMERIC STRUCTURE; GLUTATHIONE TRANSFERASE; HYDROPHOBIC SUBSTRATE; MOLECULAR REARRANGEMENT; PROTEIN STABILITY; SITE DIRECTED MUTAGENESIS; STRUCTURAL MOTIFS; STRUCTURE-FUNCTION RELATIONSHIP; SUBSTRATE SPECIFICITY; TOXIC COMPOUNDS; WILD-TYPE ENZYMES;

AROMATIC COMPOUNDS; AROMATIZATION; BINDING ENERGY; BIOCHEMISTRY; CATALYSIS; ENZYME KINETICS; ENZYMES; HYDROPHOBICITY; SUBSTRATES;

CRYSTAL STRUCTURE;

1 CHLORO 2,4 DINITROBENZENE; GLUTATHIONE TRANSFERASE; MUTANT PROTEIN; PHENYLALANINE; S HEXYLGLUTATHIONE; TYROSINE; RECOMBINANT PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; COMPLEX FORMATION; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; ENZYME ACTIVE SITE; ENZYME BINDING; ENZYME KINETICS; ENZYME SPECIFICITY; ENZYME STABILITY; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; ENZYME SUBUNIT; GENE MUTATION; HYDROPHOBICITY; MOLECULAR INTERACTION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN STABILITY; SITE DIRECTED MUTAGENESIS; STRUCTURE ACTIVITY RELATION; WILD TYPE; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; KINETICS; METABOLISM; PROTEIN CONFORMATION; X RAY CRYSTALLOGRAPHY;

BINDING SITES; CATALYSIS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; GLUTATHIONE TRANSFERASE; KINETICS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PHENYLALANINE; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; SUBSTRATE SPECIFICITY; TYROSINE;

EID: 77953416164     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20091939     Document Type: Article

References (46)

1. Ketterer, B. (2001) A bird's eye view of the glutathione transferase field. Chem. Biol. Interact. 138, 27-42
2. Beckett, G. J. and Hayes, J. D. (1993) Glutathione S-transferases: biomedical applications. Adv. Clin. Chem. 30, 281-380
3. Widersten, M., Kolm, R. H., Björnestedt, R. and Mannervik, B. (1992) Contribution of five amino acid residues in the glutathione binding site to the function of human glutathione transferase P1-1. Biochem. J. 285, 377-381
4. Casalone, E., Allocati, N., Ceccarelli, I., Masulli, M., Rossjohn, J., Parker, M. W. and Di Ilio, C. (1998) Site-directed mutagenesis of the Proteus mirabilis glutathione transferase B1-1 G-site. FEBS Lett. 423, 122-124 (Pubitemid 28343193)
5. Andújar-Sánchez, M., Clemente-Jiménez, J. M., Las Heras-Vázquez, F. J., Rodríguez-Vico, F., Cámara-Artigas, A. and Jara-Pérez, V. (2003) Thermodynamics of glutathione binding to the tyrosine 7 to phenylalanine mutant of glutathione S-transferase from Schistosoma japonicum. Int. J. Biol. Macromol. 32, 77-82
6. 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 (Pubitemid 39243942)
7. 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
8. Ralat, L. A. and Colman, R. F. (2004) Glutathione S-transferase Pi has at least three distinguishable xenobiotic substrate sites close to its glutathione binding site. J. Biol. Chem. 279, 50204-50213
9. 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
10. Mannervik, B., Board, P. G., Hayes, J. D., Listowsky, I. and Pearson, W. R. (2005) Nomenclature for mammalian soluble glutathione transferases. Methods Enzymol. 401, 1-8 (Pubitemid 43052383)
11. Jakobson, I., Askelöf, P., Warholm, M. and Mannervik, B. (1977) A steady-state-kinetic random mechanism for glutathione S-transferase A from rat liver. A model involving kinetically significant enzyme-product complexes in the forward reaction. Eur. J. Biochem. 77, 253-262
12. Mannervik, B., Ålin, P., Guthenberg, C., Jensson, H., Tahir, M. K., Warholm, M. and Jörnvall, H. (1985) Identification of three classes of cytosolic glutathione transferase common to several mammalian species: correlation between structural data and enzymatic properties. Proc. Natl. Acad. Sci. U.S.A. 82, 7202-7206
13. Ji, X., Von Rosenvinge, E. C., Johnson, W. W., Tomarev, S. I., Paitigorsky, J., Armstrong, R. N. and Gilliland, G. L. (1995) Three-dimensional structure, catalytic properties, and evolution of a sigma class glutathione transferase from squid, a progenitor of the lens S-crystallins of cephalopods. Biochemistry 34, 5317-5328
14. Meyer, D. J., Coles, B., Pemble, S. E., Gilmore, K. S., Fraser, G. M. and Ketterer, B. (1991) Theta, a new class of glutathione transferases purified from rat and man. Biochem. J. 274, 409-414
15. Board, P. G., Coggan, M., Chelvanayagam, 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
16. Board, P., Baker, R. T., Chelvanayagam, G. and Jermiin, L. S. (1997) Zeta, a novel class of glutathione transferases in a range of species from plants to humans. Biochem. J. 328, 929-935
17. Mignogna, G., Allocati, N., Aceto, A., Piccolomini, R., Di Ilio, C., Barra, D. and Martini, F. (1993) The amino acid sequence of glutathione transferase from Proteus mirabilis, a prototype of a new class of enzymes. Eur. J. Biochem. 211, 421-425
18. 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
19. Sawicki, R., Singh, S. P., Mondal, A. K., Beneš, H. and Zimniak, P. (2003) Cloning, expression and biochemical characterization of one Epsilon-class (GST-3) and ten Delta-class (GST-1) glutathione S-transferases from Drosophila melanogaster, and identification of additional nine members of the Epsilon class. Biochem. J. 370, 661-669
20. Dixon, D. P., Davis, B. G. and Edwards, R. (2002) Functional divergence in the glutathione transferase superfamily in plants. Identification of two classes with putative functions in redox homeostasis in Arabidopsis thaliana. J. Biol. Chem. 277, 30859-30869
21. Edwards, R., Dixon, D. P. and Walbot, V. (2000) Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health. Trends Plant Sci. 5, 193-198 (Pubitemid 30300842)
22. Droog, F. (1997) Plant glutathione S-transferases, a tale of Theta and Tau. J. Plant Growth Regul. 16, 95-107 (Pubitemid 27492930)
23. Konishi, T., Kato, K., Araki, T., Shiraki, K., Takagi, M. and Tamaru, Y. (2005) A new class of glutathione S-transferase from the hepatopancreas of the red sea bream, Pagrus major. Biochem. J. 388, 299-307
24. Chelvanayagam, G., Parker, M. W. and Board, P. G. (2001) Fly fishing for GSTs: a unified nomenclature for mammalian and insect glutathione transferases. Chem. Biol. Interact. 133, 256-260
25. Dixon, D. P., Lapthorn, A. and Edwards, R. (2002) Plant glutathione transferases. Genome Biol. 3, 3004.1-3004.10
26. Jemth, P., Stenberg, G., Chaga, G. and Mannervik, B. (1996) Heterologous expression, purification and characterization of rat class theta glutathione transferase T2-2. Biochem. J. 316, 131-136 (Pubitemid 26158212)
27. Hayes, J. D., Flanagan, J. U. and Jowsey, I. R. (2005) Glutathione transferases. Annu. Rev. Pharmacol. Toxicol. 45, 51-88
28. Oakley, A. J., Harnnoi, T., Udomsinprasert, R., Jirajaroenrat, K., Ketterman, A. J. and Wilce, M. C. J. (2001) The crystal structures of glutathione S-transferases isozymes 1-3 and 1-4 from Anopheles dirus species B. Protein Sci. 10, 2176-2185 (Pubitemid 32988634)
29. Lerksuthirat, T. and Ketterman, A. J. (2008) Characterization of putative hydrophobic substrate binding site residues of a Delta class glutathione transferase from Anopheles dirus. Arch. Biochem. Biophys. 479, 97-103
30. 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
31. Wongsantichon, J. and Ketterman, A. J. (2006) An intersubunit lock-and-key 'Clasp' motif in the dimer interface of Delta class glutathione transferase. Biochem. J. 394, 135-144
32. Vararattanavech, A. and Ketterman, A. (2003) Multiple roles of glutathione binding-site residues of glutathione S-transferase. Protein Peptide Lett. 10, 441-448 (Pubitemid 37143543)
33. 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
34. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Macromol. Crystallogr. Part A 276, 307-326
35. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr. Sect. D Biol. Crystallogr. 50, 760-763
36. 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. Cryst. 26, 283-291
37. Davis, I. W., Leaver-Fay, A., Chen, V. B., Block, J. N., Kapral, G. J., Wang, X., Murray, L. W., Arendall, III, W. B., Snoeyink, J., Richardson, J. S. and Richardson, D. C. (2007) MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35, W375-W383
38. 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
39. Reference deleted
40. Lo Bello, M., Oakley, A. J., Battistoni, A., Mazzetti, A. P., Nuccetelli, M., Mazzarese, G., Rossjohn, J., Parker, M. W. and Ricci, G. (1997) Multifunctional role of Tyr 108 in the catalytic mechanism of human glutathione transferase P1-1. Crystallographic and kinetic studies on the Y108F mutant enzyme. Biochemistry 36, 6207-6217
41. 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
42. Ji, X., Johnson, W. W., Sesay, M. A., Dickert, L., Prasad, S. M., Ammon, H. L., Armstrong, R. N. and Gilliland, G. L. (1994) Structure and function of the xenobiotic substrate binding site of a glutathione S-transferase as revealed by x-ray crystallographic analysis of product complexes with the diastereomers of 9-(S-glutathionyl)-10-hydroxy-9-10-dihydrophenanthrene. Biochemistry 33, 1043-1052
43. Piromjitpong, J., Wongsantichon, J. and Ketterman, A. J. (2007) Differences in the subunit interface residues of alternatively spliced glutathione transferases affects catalytic and structural functions. Biochem. J. 401, 635-644 (Pubitemid 46219257)
44. Vararattanavech, A. and Ketterman, A. J. (2007) A functionally conserved basic residue in glutathione transferases interacts with the glycine moiety of glutathione and is pivotal for enzyme catalysis. Biochem. J. 406, 247-256 (Pubitemid 47310955)
45. 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
46. Armougom, F., Moretti, S., Poirot, O., Audic, S., Dumas, P., Schaeli, B., Keduas, V. and Notredame, C. (2006) Expresso: automatic incorporation of structural information in multiple sequence alignments using 3D-Coffee. Nucleic Acids Res. 34, W604-W608