Strategies to Characterize the Mechanisms of Action and the Active Sites of Glutathione S-Transferases: A Review

References

• Ishikawa T. The ATP-dependent glutathione S-conjugate export pump. Trends Biochem. Sci. 1992; 17: 463–468
   PubMed Web of Science ®Google Scholar
• Commandeur J. N. M., Stijntjes G. J., Vermeulen N. P. E. Enzymes and transport systems involved in the formation and disposition of glutathione S-conjugates. Pharmacol. Rev. 1995; 47: 271–330
   PubMed Web of Science ®Google Scholar
• Mannervik B., Alin P., Guthenberg C., Jensson H., Tahir M. K., Warholm M., Jornvall H. Identification of three classes of cytosolic glutathione transferase common to several mammalian species: correlation between structural data and enzymatic properties. Proc. Natl. Acad. Sci. USA 1985; 82: 7202–7206
   PubMed Web of Science ®Google Scholar
• Meyer D. J., Coles B., Pemble S. E., Gilmore K. S., Fraser G. M., Ketterer B. Theta, a new class of glutathione transferases purified from rat and man. Biochem. J. 1991; 274: 409–414
   PubMed Web of Science ®Google Scholar
• Buetler T. M., Eaton D. L. Glutathione S-transferases: amino acid sequence comparison, classification and phylogenetic relationship. Environ. Carcinogen. Ecotoxicol. Rev. 1992; C10: 181–203
   Google Scholar
• De Jong J. L., Morgenstern R., Jornvall H., De Pierre J. W., Tu C. -P. D. Gene expression of rat and human microsomal glutathione S-transferases. J. Biol. Chem. 1988; 263: 8430–8436
   PubMed Web of Science ®Google Scholar
• Hayes J. D., Pulford D. J. The glutathione S-transferase supergene family: regulation of GST* and the contribution of the isoenzymes to cancer chemoprotection and drug resistance. Crit. Rev. Biochem. Molec. Biol. 1995; 30: 445–600
   PubMed Web of Science ®Google Scholar
• Litwack G., Ketterer B., Arias I. M. Ligandin: a hepatic protein which binds steroids, bilirubin, carcinogens and a number of organic anions. Nature 1971; 234: 466–467
   PubMed Web of Science ®Google Scholar
• Bhargava M. M., Listowsky I., Arias I. M. Ligandin: bilirubin binding and glutathione S-transferase activity are independent processes. J. Biol. Chem. 1978; 253: 4112–4115
   PubMed Web of Science ®Google Scholar
• Jernström B., Babson J. R., Moldéus P., Homgren A., Reed D. J. Glutathione conjugation and DNA-binding of ()-trans-7,8-dihydroxy-7,8-dihydrobenzo[a]pyrene and ()-7β,8α-dihydroxy-9α, 10α-epoxy-7,8,9,10-tetrahydrobenzo[a]pyrene in isolated rat hepatocytes. Carcinogenesis 1982; 3: 861–866
   PubMed Web of Science ®Google Scholar
• Raney K. D., Meyer D. J., Ketterer B., Harris T. M., Guengerich F. P. Glutathione conjugation of aflatoxin B1exo- and endo-epoxides by rat and human glutathione S-transferases. Chem. Res. Toxicol. 1992; 5: 470–478
   PubMed Web of Science ®Google Scholar
• Te Koppele J. M., Coles B., Ketterer B., Mulder G. J. Stereoselectivity of rat liver glutathione transferase isoenzymes for α-bromoisovaleric acid and α-bromoisovalerylurea enantiomers. Biochem. J. 1988; 252: 137–142
   PubMed Web of Science ®Google Scholar
• Mulders T. M. T., Van Ommen B., Van Bladeren P. J., Breimer D. D., Mulder G. J. Stereoselectivity of human liver and intestinal cytosolic fractions as well as purified human glutathione S-transferase isoenzymes towards 2-bromoisovalerylurea enantiomers. Biochem. Pharmacol. 1993; 46: 1775–1780
   PubMed Web of Science ®Google Scholar
• Booth J., Boyland E., Sims P. An enzyme from rat liver catalyzing conjugation with glutathione. Biochem. J. 1961; 79: 516–524
   PubMed Web of Science ®Google Scholar
• Lundblad R. L. Techniques in Protein Modification. CRC Press, London 1995
   Google Scholar
• Carne T., Tipping E., Ketterer B. The binding and catalytic activities of forms of ligandin after modification of its thiol groups. Biochem. J. 1979; 177: 433–439
   PubMed Web of Science ®Google Scholar
• Van B., Ommen J., Ploemen H. T. M., Ruven H. J., Vos R. M. E., Bogaards J. J. P., Van Berkel W. J. H., Van Bladeren P. J. Studies on the active site of rat glutathione S-transferase isoenzyme 4–4. Chemical modification by tetrachloro-1,4-benzoquinone and its glutathione conjugate. Eur. J. Biochem. 1989; 181: 423–429
   PubMedGoogle Scholar
• Mc Carthy R. M., Sheehan D. Cysteine plays a role in catalysis in glutathione S-transferase 1–1. Biochem. Soc. Trans. 1995; 23: 388S
   PubMed Web of Science ®Google Scholar
• Ploemen J. H. T. M., Van Ommen B., Van Bladeren P. J. Irreversible inhibition of human glutathione S-transferase isoenzymes by tetrachloro-1,4-benzoquinone and its glutathione conjugate. Biochem. Pharmacol. 1996; 41: 1665–1669
   Google Scholar
• Tamai K., Satoh K., Tsuchida S., Hatayama I., Maki T., Sato K. Specific inactivation of glutathione S-transferases in class pi by SH-modifiers. Biochem. Biophys. Res. Commun. 1990; 167: 331–338
   PubMed Web of Science ®Google Scholar
• Del Boccio G., Pennelli A., Whitehead E. P., Lo Bello M., Petruzzelli R., Federici G., Ricci G. Interaction of glutathione transferase from horse erythrocytes with 7-chloro-4-nitrobenzo-2-oxa-1,3-diazole. J. Biol. Chem. 1991; 266: 13777–13782
   PubMed Web of Science ®Google Scholar
• J-Hsieh C., Huang S-C., Chen W-L., Lai Y-C., Tam M. F. Cysteine-86 is not needed for the enzymic activity of glutathione S-transferase 3–3. Biochem. J. 1991; 278: 293–297
   PubMed Web of Science ®Google Scholar
• Chang L-H., Wang L-Y., Tam M. F. The single cysteine residue on an alpha family chick liver glutathione S-transferase CL 3–3 is not functionally important. Biochem. Biophys. Res. Commun. 1991; 180: 323–328
   PubMed Web of Science ®Google Scholar
• Phillips M. F., Mantle T. J. Inactivation of mouse liver glutathione S-transferase YfYf (Pi class) by ethacrynic acid and 5,5α-dithiobis-(2-nitrobenzoic acid). Biochem. J. 1993; 294: 57–62
   PubMed Web of Science ®Google Scholar
• Ploemen J. H. T. M., Van Schanke A., Van Ommen B., Van Bladeren P. J. Reversible conjugation of ethacrynic acid with glutathione and human glutathione S-transferase P1–1. Cancer Res. 1994; 54: 915–919
   PubMed Web of Science ®Google Scholar
• Wang R. W., Newton D. J., Pickett C. B., Lu A. Y. H. Site-directed mutagenesis of glutathione S-transferase YaYa: functional studies of histidine, cysteine and trypthophane mutants. Arch. Biochem. Biophys. 1992; 297: 86–91
   PubMed Web of Science ®Google Scholar
• Widersten M., Holmström E., Mannervik B. Cysteine residues are not essential for the catalytic activity of human class mu glutathione transferase M la-la. FEBS Lett. 1991; 293: 156–159
   PubMed Web of Science ®Google Scholar
• Kong K.-H., Inoue H., Takahashi K. Non-essentiality of cysteine and histidine residues for the activity of human class pi glutathione S-transferase. Biochem. Biophys. Res. Commun. 1991; 181: 748–755
   PubMed Web of Science ®Google Scholar
• Nishihira J., Ishibashi T., Sakai M., Nishi S., Kumazaki T., Hatanaka Y., Tsuda S., Hikichi K. Characterization of cysteine residues of glutathione S-transferase P: evidence for steric hindrance of substrate binding by a bulky adduct to cysteine 47. Biochem. Biophys. Res. Commun. 1992; 188: 424–432
   PubMed Web of Science ®Google Scholar
• Rose M. S., Lock E. A. The interaction of triethyltin with a component of guinea-pig liver supernatant. Evidence for histidine in the binding sites. Biochem. J. 1970; 120: 151–157
   PubMed Web of Science ®Google Scholar
• Awasthi Y. C., Bhatnagar A., Singh S. V. Evidence for the involvement of histidine at the active site of glutathione S-transferase PS from human liver. Biochem. Biophys. Res. Commun. 1987; 143: 965–970
   PubMed Web of Science ®Google Scholar
• Zhang P., Graminski G. F., Armstrong R. N. Are the histidine residues of glutathione S-transferase important in catalysis? An assessment by 13C NMR spectroscopy and site-specific mutagenesis. J. Biol. Chem. 1991; 266: 19475–19479
   PubMed Web of Science ®Google Scholar
• Chang L. H., Tam M. F. Site-directed mutagenesis and chemical modification of histidine residues on an α-class chick liver glutathione S-transferase CL 3–3. Eur. J. Biochem. 1993; 211: 805–811
   PubMedGoogle Scholar
• Walker J., Crowley P., Barrett J. Chemical modification of a cloned glutathione S-transferase from Schistosoma japonicum: evidence for an essential histidine residue. Exp. Parasitol. 1995; 80: 616–623
   PubMed Web of Science ®Google Scholar
• Lo Bello M., Petruzzelli R., Reale L., Ricci G., Barra D., Federici G. Chemical modification of human placental glutathione transferase by pyridoxal 5α-phosphate. Biochim. Biophys. Acta 1992; 1121: 167–172
   PubMed Web of Science ®Google Scholar
• Reinemer P., Dirr H. W., Ladenstein R., Huber R., Lo Bello M., Federici G., Parker M. W. Three-dimensional structure of class glutathione S-transferase from human placenta in complex with S-hexylglutathione at 2.8 Å resolution. J. Molec. Biol. 1992; 227: 214–226
   PubMed Web of Science ®Google Scholar
• Xia C., Meyer D. J., Chen H., Reinemer P., Huber R., Ketterer B. Chemical modification of GSH transferase P1–1 confirms the presence of Arg-13, Lys-44 and one carboxylate group in the GSH-binding domain of the active site. Biochem. J. 1993; 293: 357–362
   PubMed Web of Science ®Google Scholar
• Reinemer P., Dirr H. W., Ladenstein R., Schäffer J., Gallay O., Huber R. The three-dimensional structure of class glutathione S-transferase in complex with glutathione sulfonate at 2.3 Å resolution. EMBO J. 1991; 10: 1997–2005
   PubMed Web of Science ®Google Scholar
• Dirr H. W., Reinemer P., Huber R. Refined crystal structure of porcine, class glutathione S-transferase (pGST P1–1) at 2.1 Å resolution. J. Molec. Biol. 1994; 243: 72–92
   PubMed Web of Science ®Google Scholar
• Widersten M., Kolm R. H., Björnestedt R., Mannervik B. Contribution of five amino acid residues in the glutathione binding site to the function of glutathione transferase P1–1. Biochem. J. 1992; 285: 377–381
   PubMed Web of Science ®Google Scholar
• Manoharan T. W., Gulick A. M., Reinemer P., Dirr H. W., Huber R., Fahl W. W. Mutational substitution of residues implicated by crystal structure in binding the substrate glutathione to human glutathione S-transferase pi. J. Molec. Biol. 1992; 226: 319–322
   PubMed Web of Science ®Google Scholar
• Schasteen C. S., Krivak B. M., Reed D. J. Similarities in inactivation of glutathione S-transferases by arginine specific chemical modifying agents. Fed. Proc. 1983; 42: 2036
   Google Scholar
• Chen P.-S., Wang T.-C., Chang G.-G. Chemical modification of glutathione S-transferase from C6/36, an Aedes albopictus cell line. Insect Biochem. Molec. Biol. 1995; 25: 613–619
   Web of Science ®Google Scholar
• Kong K.-H., Nishida M., Inoue H., Takahashi K. Tyrosine-7 is an essential residue for the catalytic activity of human class pi glutathione S-transferase: chemical modification and site-directed mutagenesis studies. Biochem. Biophys. Res. Commun. 1992; 182: 1122–1129
   PubMed Web of Science ®Google Scholar
• Meyer D. J., Xia C., Coles B., Chen H., Reinemer P., Huber R., Ketterer B. Unusual reactivity of Tyr-7 of GSH transferase P1–1. Biochem. J. 1993; 293: 351–356
   PubMed Web of Science ®Google Scholar
• Kolm R. H., Sroga G. E., Mannervik B. Participation of the phenolic hydroxyl group of Tyr-8 in the catalytic mechanism of human glutathione transferase P1–1. Biochem. J. 1992; 285: 537–540
   PubMed Web of Science ®Google Scholar
• Liu S., Zhang P., Ji X., Johnson W. W., Gilliland G. L., Armstrong R. N. Contribution of tyrosine 6 to the catalytic mechanism of isoenzyme 3–3 of glutathione S-transferase. J. Biol. Chem. 1992; 267: 4296–4299
   PubMed Web of Science ®Google Scholar
• Nishihira J., Sakai M., Nishi S. Identification of ionizable groups essential for the enzyme catalysis on glutathione S-transferase P. Biochem. Biophys. Res. Commun. 1993; 194: 1466–1474
   PubMed Web of Science ®Google Scholar
• Nishihira J., Ishibashi T., Sakai M., Nishi S., Kumazaki T. Evidence for the involvement of tryptophane 38 in the active site of glutathione S-transferase P. Biochem. Biophys. Res. Commun. 1992; 185: 1069–1077
   PubMed Web of Science ®Google Scholar
• Van Ommen B., Den Besten C., Rutten A. L. M., Ploemen J. H. T. M., Vos R. M. E., Muller F., Van Bladeren P. J. Active site-directed irreversible inhibition of glutathione S-transferases by the glutathione conjugate of tetrachloro-1,4-benzoquinone. J. Biol. Chem. 1988; 263: 12939–12942
   PubMed Web of Science ®Google Scholar
• Ploemen J. H. T. M., Johnson W. W., Jespersen S., Vanderwall D., Van Ommen B., Van der Greef J., Van Bladeren P. J., Armstrong R. N. Active-site tyrosyl residues are targets in the irreversible inhibition of a class mu glutathione transferase by 2-(S-glutathionyl)-3,5,6-trichloro-1,4-benzoquinone. J. Biol. Chem. 1994; 269: 26890–26897
   PubMed Web of Science ®Google Scholar
• Hong J.-L., Liu L.-F., Wang L.-Y., Tsai S.-P., Hsieh C.-H., Hsiao C.-D., Tam M. F. Modification of glutathione S-transferase 3–3 mutants with 2-(S-glutathionyl)-3,5,6-trichloro-1,4-benzoquinone. Identification of the C-terminal tryptic fragments as part of the H-site and evidence that 2-(S-glutathionyl)-3,5,6-trichloro-1,4-benzoquinone is not specific for cysteine labelling. Biochem. J. 1994; 304: 825–831
   PubMed Web of Science ®Google Scholar
• Katusz R. M., Colman R. F. S-(4-Bromo-2,3-dioxobutyl)glutathione: a new affinity label for the 4–4 isoenzyme of rat liver glutathione S-transferase. Biochemistry 1991; 30: 11230–11238
   PubMed Web of Science ®Google Scholar
• Johnson W. W., Liu S., Ji X., Gilliland G. L., Armstrong R. N. Tyrosine 115 participates both in chemical and physical steps of the catalytic mechanism of a glutathione S-transferase. J. Biol. Chem. 1993; 268: 11508–11511
   PubMed Web of Science ®Google Scholar
• Pennington C. J., Rule G. S. Mapping the substrate-binding site of a human class mu glutathione transferase using nuclear magnetic resonance spectroscopy. Biochemistry 1992; 31: 2912–2920
   PubMed Web of Science ®Google Scholar
• Katusz R. M., Bono B., Colman R. F. Identification of Tyr115 labeled by S-(4-bromo-2,3-dioxobutyl)glutathione in the hydrophobic substrate binding site of glutathione S-transferase, isoenzyme 3–3. Arch. Biochem. Biophys. 1992; 298: 667–677
   PubMed Web of Science ®Google Scholar
• Katusz R. M., Bono B., Colman R. F. Affinity labeling of Cys111 of glutathione S-transferase, isoenzyme 1–1, by S-(4-bromo-2,3-dioxobutyl)-glutathione. Biochemistry 1992; 31: 8984–8990
   PubMed Web of Science ®Google Scholar
• Barycki J. J., Colman R. F. Affinity labeling of glutathione S-transferase, isozyme 4–4, by 4-(fluorosulfonyl)benzoic acid reveals Tyr115 to be an important determinant of xenobiotic substrate specificity. Biochemistry 1993; 32: 13002–13011
   PubMed Web of Science ®Google Scholar
• Wang J., Barycki J. J., Colman R. F. Tyrosine 8 contributes to catalysis but is not required for activity of rat liver glutathione S-transferase, 1–1. Protein Sci. 1996; 5: 1032–1042
   PubMed Web of Science ®Google Scholar
• Hu L., Colman R. F. Monobromobimane as an affinity label of the xenobiotic binding site of rat glutathione S-transferase 3–3. J. Biol. Chem. 1995; 270: 21875–21883
   PubMed Web of Science ®Google Scholar
• Vander Jagt D. L., Hunsaker L. A., Garcia K. B., Royer R. E. Isolation and characterization of the multiple glutathione S-transferases from human liver. Evidence for unique heme-binding sites. J. Biol. Chem. 1985; 260: 11603–11610
   PubMed Web of Science ®Google Scholar
• Liu L.-F., Hong J.-L., Tsai S.-P., Hsieh J.-C., Tam M. F. Reversible modification of rat liver glutathione S-transferase 3–3 with 1-chloro-2,4-dinitrobenzene: specific labelling of Tyr-115. Biochem. J. 1993; 296: 189–197
   PubMed Web of Science ®Google Scholar
• Van der Aar E. M., Tan K. T., Commandeur J. N. M., Vermeulen N. P. E. Affinity parameters of 2-substituted 1-chloro-4-nitrobenzenes for the active site of rat glutathione S-transferase 4–4, unpublished
   Google Scholar
• Hammes G. G. Enzyme Catalysis and Regulation, B. Horecker, N. O. Kaplan, J. Marmur, H. A. Scheraga. Academic Press, New York 1982
   Google Scholar
• Glazer A. N. The chemical modification of proteins by group-specific and site-specific reagents. The Proteins, H. Neurath, R. L. Hill. Academic Press, New York 1976; 2–103
   Google Scholar
• Seddon A. P., Bunni M., Douglas K. T. Photoaffinity labelling by S-(p-azidophenacyl)glutathione of glyoxalase II and glutathione S-transferase. Biochem. Biophys. Res. Commun. 1980; 95: 446–452
   PubMed Web of Science ®Google Scholar
• Hoesch R. M., Boyer T. D. Localization of a portion of the active site of two rat liver glutathione S-transferases using a photoaffinity label. J. Biol. Chem. 1989; 264: 17712–17717
   PubMed Web of Science ®Google Scholar
• Cooke R., Björnestedt R., Douglas K. T., Mc Kie J. H., King M. D., Coles B., Ketterer B., Mannervik B. Photoaffinity labelling of the active site of the rat glutathione transferases 3–3 and 1–1 and human glutathione transferase Al-1. Biochem. J. 1994; 302: 383–390
   PubMed Web of Science ®Google Scholar
• Ji X., Armstrong R. N., Gilliland G. L. Snapshots along the reaction coordinate of an SNAr reaction catalyzed by glutathione transferase. Biochemistry 1993; 32: 12949–12954
   PubMed Web of Science ®Google Scholar
• Sinning I., Kleywegt G. J., Cowan S. W., Reinemer P., Dirr H. W., Huber R., Gilliland G. L., Armstrong R. N., Ji X., Board P. G., Olin B., Mannervik B., Jones T. A. Structure determination and refinement of human alpha class glutathione transferase A1–1, and a comparison with the mu and pi class enzymes. J. Molec. Biol. 1993; 232: 192–212
   PubMed Web of Science ®Google Scholar
• Nishihira J., Sakai M., Nishi S., Hatanaka Y. Identification of the electrophilic substrate-binding site of glutathione S-transferase P by photo-affinity labeling. Eur. J. Biochem. 1995; 232: 106–110
   PubMedGoogle Scholar
• García-Sá I., Aez Párraga A., Phillips M. F., Mantle T. J., Coll M. Molecular structure at 1.8 Å of mouse liver class pi glutathione S-transferase complexed with S-(p-nitrobenzyl)glutathione and other inhibitors. J. Molec. Biol. 1994; 237: 298–314
   PubMed Web of Science ®Google Scholar
• Whalen R., Kempner E. S., Boyer T. D. Structural studies of a human pi class glutathione S-transferase. Photoaffinity labeling of the active site and target size analysis. Biochem. Pharmacol. 1996; 52: 281–288
   PubMed Web of Science ®Google Scholar
• Chen W.-L., Hsieh J.-C., Hong J.-L., Tsai S.-P., Tam M. F. Site-directed mutagenesis and chemical modification of cysteine residues of rat glutathione S-transferase 3–3. Biochem. J. 1992; 286: 205–210
   PubMed Web of Science ®Google Scholar
• Tamai K., Shen W., Tsuchida S., Hatayama I., Satoh K., Yasui A., Oikawa A., Sato K. Role of cysteine residues in the activity of rat glutathione transferase P (7–7). Biochem. Biophys. Res. Commit. 1991; 179: 790–797
   PubMed Web of Science ®Google Scholar
• Ricci G., Lo Bello M., Caccuri A. M., Pastore A., Nuccetelli M., Parker M. W., Federici G. Site-directed mutagenesis of human glutathione transferase P1–1. Mutation of Cys-47 induces a positive cooperativity in glutathione transferase P1–1. J. Biol. Chem. 1995; 270: 1243–1248
   PubMed Web of Science ®Google Scholar
• Vander Jagt D. L., Wilson S. P., Heidrich J. E. Purification and bilirubin binding properties of glutathione S-transferase from human placenta. FEBS Lett. 1981; 136: 319–321
   PubMed Web of Science ®Google Scholar
• Lo Bello M., Pastore A., Petruzzelli R., Parker M. W., Wilce M. C. J., Federici G., Ricci G. Conformational states of human placental glutathione transferase as probed by limited proteolysis. Biochem. Biophys. Res. Commun. 1993; 194: 804–810
   PubMed Web of Science ®Google Scholar
• Lo Bello M., Battistoni A., Mazzetti A. P., Board P. G., Muramatsu M., Federici G., Ricci G. Site-directed mutagenesis of human glutathione transferase P1–1. Spectral, kinetic and structural properties of Cys-47 and Lys-54 mutants. J. Biol. Chem. 1995; 270: 1249–1253
   PubMed Web of Science ®Google Scholar
• Wang R. W., Newton D. J., Pickett C. B., Lu A. Y. H. Site-directed mutagenesis of glutathione S-transferase YaYa: nonessential role of histidine in catalysis. Arch. Biochem. Biophys. 1991; 286: 574–578
   PubMed Web of Science ®Google Scholar
• Widersten M., Mannervik B. A structural role of histidine 15 in human glutathione transferase M1–1, an amino acid residue conserved in class Mu enzymes. Protein Eng. 1992; 5: 551–557
   PubMedGoogle Scholar
• Stenberg G., Board P. G., Carlberg I., Mannervik B. Effects of directed mutagenesis on conserved arginine residues in a human class alpha glutathione transferase. Biochem. J. 1991; 274: 549–555
   PubMed Web of Science ®Google Scholar
• Wang R. W., Newton D. J., Johnson A. R., Pickett C. B., Lu A. Y. H. Site-directed mutagenesis of glutathione S-transferase YaYa: mapping the glutathione binding site. J. Biol. Chem. 1993; 268: 23981–23985
   PubMed Web of Science ®Google Scholar
• Bjömestedt R., Stenberg G., Widersten M., Board P. G., Sinning I., Jones T. A., Mannervik B. Functional significance of arginine 15 in the active site of human class alpha glutathione transferase A1–1. J. Molec. Biol. 1995; 247: 765–773
   PubMed Web of Science ®Google Scholar
• Kong K.-H., Inoue H., Takahashi K. Site-directed mutagenesis of amino acid residues involved in the glutathione binding of human glutathione S-transferase P1–1. J. Biochem. 1992; 112: 725–728
   PubMed Web of Science ®Google Scholar
• Manoharan T. H., Gulick A. M., Puchalski R. B., Servais A. L., Fahl W. E. Structural studies on human glutathione S-transferase. Substitution mutations to determine amino acids necessary for binding glutathione. J. Biol. Chem. 1992; 267: 18940–18945
   PubMed Web of Science ®Google Scholar
• Stenberg G., Board P. G., Mannervik M. Mutation of an evolutionarily conserved tyrosine residue in the active site of a human class alpha glutathione transferase. FEBS Lett. 1991; 293: 153–155
   PubMed Web of Science ®Google Scholar
• Wang R. W., Newton D. J., Huskey S.-E. W., Mc Keever B. M., Pickett C. B., Lu A. Y. H. Site-directed mutagenesis of glutathione S-transferase YaYa. Important roles of tyrosine 9 and aspartic acid 101 in catalysis. J. Biol. Chem. 1992; 267: 19866–19871
   PubMed Web of Science ®Google Scholar
• Atkins W. M., Wang R. W., Bird A. W., Newton D. J., Lu A. Y. H. The catalytic mechanism of glutathione S-transferase (GST). Spectroscopic determination of the pKa of Tyr-9 in rat α1–1 GST. J. Biol. Chem. 1993; 268: 19188–19191
   PubMed Web of Science ®Google Scholar
• Dietze E. C., Wang R. W., Lu A. Y. H., Atkins W. M. Ligand effects on the fluorescence properties of tyrosine-9 in alpha 1–1 glutathione S-transferase. Biochemistry 1996; 35: 6745–6753
   PubMed Web of Science ®Google Scholar
• Xiao G., Liu S., Ji X., Johnson W. W., Chen J., Parsons J. F., Stevens W. J., Gilliland G. L., Armstrong R. N. First-sphere and second-sphere electrostatic effects in the active site of a class mu glutathione transferase. Biochemistry 1996; 35: 4753–4765
   PubMed Web of Science ®Google Scholar
• Liu S., Ji X., Gilliland G. L., Stevens W. J., Armstrong R. N. Second-sphere electrostatic effects in the active site of glutathione S-transferase. Observation of an on-face hydrogen bond between the side chain of threonine 13 and the α-cloud of tyrosine 6 and its influence on catalysis. J. Am. Chem. Soc. 1993; 115: 7910–7911
   Web of Science ®Google Scholar
• Kong K.-H., Takasu K., Inoue H., Takahashi K. Tyrosine-7 in human class pi glutathione S-transferase is important for lowering the pKa of the thiol group of glutathione in the enzyme-glutathione complex. Biochem. Biophys. Res. Commun. 1992; 184: 194–197
   PubMed Web of Science ®Google Scholar
• Karshikoff A., Reinemer P., Huber R., Ladenstein R. Electrostatic evidence for the activation of the glutathione thiol by Tyr7 in α-class glutathione transferases. Eur. J. Biochem. 1993; 215: 663–670
   PubMedGoogle Scholar
• Parsons J. F., Armstrong R. N. Proton configuration in the ground state and transition state of a glutathione transferase-catalyzed reaction inferred from the properties of tetradeca(3-fluorotyrosyl)glutathione transferase. J. Am. Chem. Soc. 1996; 118: 2295–2296
   Web of Science ®Google Scholar
• Nishida M., Kong K.-H., Inoue H., Takahashi K. Molecular cloning and site-directed mutagenesis of glutathione S-transferase from Escherichia coli. J. Biol. Chem. 1994; 269: 32536–32541
   PubMed Web of Science ®Google Scholar
• Wilce M. C. J., Board P. G., Feil S. C., Parker M. W. Crystal structure of a theta-class glutathione transferase. EMBO J. 1995; 14: 2133–2143
   PubMed Web of Science ®Google Scholar
• Board P. G., Coggan M., Wilce M. C. J., Parker M. W. Evidence for an essential serine residue in the active site of the theta class glutathione tranferases. Biochem. J. 1995; 311: 247–250
   PubMed Web of Science ®Google Scholar
• Chaga G., Widersten M., Andersson L., Porath J., Danielson U. H., Mannervik B. Engineering of a metal coordinating site into human glutathione transferase M1–1 based on immobilized metal ion affinity chromatography of homologous rat enzymes. Protein Eng. 1994; 7: 1115–1119
   PubMedGoogle Scholar
• Yilmaz S., Widersten M., Emahazion T., Mannervik B. Generation of a Ni(II) binding site by introduction of a histidine cluster in the structure of human glutathione transferase A1–1. Protein Eng. 1995; 8: 1163–1169
   PubMedGoogle Scholar
• Zhang P., Armstrong R. N. Construction, expression, and preliminary characterization of chimeric class glutathione S-transferases with altered catalytic properties. Biopolymers 1990; 29: 159–169
   PubMed Web of Science ®Google Scholar
• Zhang P., Liu S., Shan S., Ji X., Gilliland G. L., Armstrong R. N. Modular mutagenesis of exons 1, 2, and 8 of a glutathione S-transferase from the mu class. Mechanistic and structural consequences for chimeras of isoenzyme 3–3. Biochemistry 1992; 31: 10185–10193
   PubMed Web of Science ®Google Scholar
• Ji X., Zhang P., Armstrong R. N., Gilliland G. L. The three-dimensional structure of a glutathione S-transferase from the mu gene class. Structural analysis of the binary complex of isoenzyme 3–3 and glutathione at 2.2 Å resolution. Biochemistry 1992; 31: 10169–10184
   PubMed Web of Science ®Google Scholar
• Shan S., Armstrong R. N. Rational construction of the active site of a class mu glutathione S-transferase. J. Biol. Chem. 1994; 269: 32373–32379
   PubMed Web of Science ®Google Scholar
• Björnestedt R., Widersten M., Board P. G., Mannervik B. Design of two chimaeric human-rat class alpha glutathione transferases for probing the contribσ-complex intermediates in nucleophilic aromatic substitution reactions. Biochemistry 1989; 28: 6252–6258
   PubMedGoogle Scholar
• Lo Bello M., Parker M. W., Desideri A., Polticelli F., Falconi M., De Bocciol G., Pennelli A., Federici G., Ricci G. Peculiar spectroscopic and kinetic properties of Cys-47 in human placental glutathione transferase. Evidence for an atypical thiolate ion pair near the active site. J. Biol. Chem. 1993; 268: 19033–19038
   PubMed Web of Science ®Google Scholar
• Wang R. W., Bird A. W., Newton D. J., Lu A. Y. H., Atkins W. M. Fluorescence characterization of Trp 21 in rat glutathione S-transferase 1–1: microconformational changes induced by S-hexyl glutathione. Protein Sci. 1993; 2: 2085–2094
   PubMed Web of Science ®Google Scholar
• Schramm V. L., Mc Cluskey R., Emig F. A., Litwack G. Kinetic studies and active site-binding properties of glutathione S-transferase using spin-labeled glutathione, a product analogue. J. Biol. Chem. 1984; 259: 714–722
   PubMed Web of Science ®Google Scholar
• Caccuri A. M., Polizio F., Piemonte F., Tagliatesta P., Federici G., Desideri A. Investigation of the active site of human placenta glutathione transferase by means of a spin-labelled glutathione analogue. Biochim. Biophys. Acta 1992; 1122: 265–268
   PubMed Web of Science ®Google Scholar
• Desideri A., Caccuri A. M., Polizio F., Bastoni R., Federici G. Electron paramagnetic resonance identification of a highly reactive thiol group in the proximity of the catalytic site of human placenta glutathione transferase. J. Biol. Chem. 1991; 266: 2063–2066
   PubMed Web of Science ®Google Scholar
• Penington C. J., Rule G. S. Application of site-directed mutagenesis in nuclear magnetic resonance spectroscopy. Biophys. J. 1992; 62: 116–118
   PubMed Web of Science ®Google Scholar
• Sesay M. A., Ammon H. L., Armstrong R. N. Crystallization and a preliminary X-ray diffraction study of isozyme 3–3 of glutathione S-transferase from rat liver. J. Mol. Biol. 1987; 197: 377–378
   PubMed Web of Science ®Google Scholar
• Cowan S. W., Bergfors T., Jones T. A., Tibbeling G., Olin B., Board P. G., Mannervik B. Crystallization of GST2, a human class alpha glutathione transferase. J. Molec. Biol. 1989; 208: 369–370
   PubMed Web of Science ®Google Scholar
• Fu J.-H., Rose J., Chung Y.-J., Tam M. F., Wang B. C. Crystals of isoenzyme 3–3 of rat liver glutathione S-transferase with and without inhibitor. Acta Crystallogr. 1991; B47: 813–814
   Google Scholar
• Schaeffer J., Gallay O., Ladenstein R. Glutathione transferase from bovine placenta. Preparation, biochemical characterization, crystallization and preliminary crystallographic analysis of a neutral class enzyme. J. Biol. Chem. 1988; 263: 17405–17411
   PubMed Web of Science ®Google Scholar
• Parker M. W., Lo Bello M., Federici G. Crystallization of glutathione S-transferase from human placenta. J. Molec. Biol. 1990; 213: 221–222
   PubMed Web of Science ®Google Scholar
• Ji X., Von Rosenvinge E. C., Johnson W. W., Tomarev S. I., Piatigorsky J., Armstrong R. N., Gilliland G. L. 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 1995; 34: 5317–5328
   PubMed Web of Science ®Google Scholar
• Din H., Reinemer P., Huber R. X-ray crystal structures of cytosolic glutathione S-transferases. Implications for protein architecture, substrate recognition and catalytic function. Eur. J. Biochem. 1994; 220: 645–661
   PubMedGoogle Scholar
• De Groot M. J., Vermeulen N. P. E. Modeling the active sites of cytochrome P450s and glutathione S-transferases, two of the most important biotransformation enzymes. Drug Met. Rev. 1997; 29(3)747–799
   PubMed Web of Science ®Google Scholar
• Cameron A. D., Sinning I., L'Hermite G., Olin B., Board P. G., Mannervik B., Jones T. A. Structural analysis of human alpha-class glutathione transferase A1–1 in the apo-form and in complex with ethacrynic acid and its glutathione conjugate. Structure 1995; 3: 717–727
   PubMed Web of Science ®Google Scholar
• Zeng K., Rose J. P., Chen H.-C., Strickland C. L., Tu C.-P. D., Wang B.-C. A surface mutant (G82R) of a human α-glutathione S-transferase shows decreased thermal stability and a new mode of molecular association in the crystal. Protein-Struct. Funct. Genet. 1994; 20: 259–263
   PubMed Web of Science ®Google Scholar
• Lin S.-C., Yu H.-H., Liu L.-F., Lee J.-Y., Huang A., Tam M. F., Liaw Y.-C. Crystallization and preliminary X-ray analysis of chicken-liver glutathione S-transferase CL 3–3. Acta Crystallogr. 1996; D52: 601–603
   Google Scholar
• Ji X., Johnson W. W., Sesay M. A., Dickert L., Prasad S. M., Ammon H. L., Armstrong R. N., Gilliland G. L. 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 1994; 33: 1043–1052
   PubMed Web of Science ®Google Scholar
• Fu J.-H., Rose J. New crystal forms of a α-class glutathione S-transferase from rat liver. Acta Crystallogr. 1994; D50: 219–224
   Google Scholar
• Raghunathan S., Chandross R. J., Kretsinger R. H., Allison T. J., Penington C. J., Rule G. S. Crystal structure of human class mu glutathione transferase GSTM2–2, Effects of lattice packing on conformational heterogeneity. J. Molec. Biol. 1994; 238: 815–832
   PubMed Web of Science ®Google Scholar
• Lim K., Ho J. X., Keeling K., Gilliland G. L., Ji X., Rüker F., Carter D. C. Three-dimensional structure of Schistoma japonicum glutathione S-transferase fused with a six-amino acid conserved neutralizing epitope of gp41 from HIV. Protein Sci. 1994; 3: 2233–2244
   PubMed Web of Science ®Google Scholar
• Mc Tigue M. A., Williams D. R., Tainer J. A. Crystal structures of a Schistosomal drug and vaccine target: glutathione S-transferase from Schistosoma japonica and its complex with the leading antischistosomal drug praziquantel. J. Molec. Biol. 1995; 246: 21–27
   PubMed Web of Science ®Google Scholar
• Mc Tigue M. A., Bernstein S. L., Williams D. R., Tainer J. A. Purification and crystallization of a Schistosomal glutathione S-transferase. Protein-Struct. Funct. Genet. 1995; 22: 55–57
   PubMed Web of Science ®Google Scholar
• Wilce M. C. J., Feil S. C., Board P. G., Parker M. W. Crystallization and preliminary X-ray diffraction studies of a glutathione S-transferase from the Australian sheep blowfly. Lucilia cuprina, J. Molec. Biol. 1994; 236: 1407–1409
   PubMed Web of Science ®Google Scholar
• Reinemer P., Prade L., Hof P., Neuefeind T., Huber R., Zettl R., Palme K., Schell J., Koelln I., Bartunik H. D., Bieseler B. Three-dimensional structure of glutathione S-transferase from Arabidopsis thaliana at 2.2 A resolution: structural characterization of herbicide-conjugating plant glutathione S-transferases and a novel active site architecture. J. Molec. Biol. 1996; 255: 289–309
   PubMed Web of Science ®Google Scholar
• Feil S. C., Wilce M. W., Rossjohn J., Allocati N., Aceto A., Di Ilio C., Parker M. W. Crystallization and preliminary X-ray analysis of a bacterial glutathione transferase. Acta Crystallogr. 1996; D52: 189–191
   Google Scholar
• 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., Pickett C. B., Sam K., Widersten M., Wolf C. R. Nomenclature for human glutathione transferases. Biochem. J. 1992; 282: 305–306
   PubMed Web of Science ®Google Scholar
• Ploemen J. H. T. M., Wormhoudt L. W., Haenen G. R. M. M., Oudshoorn M. J., Commandeur J. N. M., Vermeulen N. P. E., de Waziers I., Beaune P. H., Watabe T., Van Bladeren P. J. The use of human in vitro metabolic parameters to explore the risk assessment of hazardous compounds: the case of ethylenedibromide. Toxicol. Appl. Pharmacol. 1997; 143: 56–69
   PubMed Web of Science ®Google Scholar
• Cobb D., Boehlert C., Lewis D., Armstrong R. N. Stereoselectivity of isoenzyme C of glutathione S-transferase toward arene and azaarene oxides. Biochemistry 1983; 22: 805–812
   PubMed Web of Science ®Google Scholar
• Dostal L. A., Aitio A., Harris C., Bhatia A. V., Hernandez O., Bend J. R. Cytosolic glutathione S-transferases in various rat tissues differ in stereoselectivity with polycyclic arene and alkene oxide substrates. Drug Metab. Disp. 1986; 14: 303–309
   PubMed Web of Science ®Google Scholar
• De Groot M. J., Van der Aar E. M., Nieuwenhuizen P. J., Van der Plas R. M., Donné-Op den Kelder G. M., Commandeur J. N. M., Vermeulen N. P. E. A predictive substrate model for rat glutathione S-transferase 4–4. Chem. Res. Toxicol. 1995; 8: 649–658
   PubMed Web of Science ®Google Scholar
• Robertson I. G. C., Jensson H., Mannervik B., Jernström B. Glutathione transferases in rat lung: the presence of transferase 7–7, highly efficient in the conjugation of glutathione with the carcinogenic (+)-7β,8α-dihydroxy-9α,10α-oxy-7,8,9,10-tetrahydrobenzo[a]pyrene. Carcinogenesis 1986; 7: 295–299
   PubMed Web of Science ®Google Scholar
• Robertson I. G. C., Jernström B. The enzymatic conjugation of glutathione with bay-region diol-epoxides of benzo[a]pyrene, benzo[a]anthracene and chrysene. Carcinogenesis 1986; 7: 1633–1636
   PubMed Web of Science ®Google Scholar
• De Groot M. J., Vermeulen N. P. E., Mullenders D. L. J., Donné-Op den Kelder G. M. A homology model for rat mu class glutathione S-transferase 4–4. Chem. Res. Toxicol 1996; 9: 28–40
   PubMed Web of Science ®Google Scholar
• Kauvar L. M. GST-targeted drug candidates. Glutathione S-transferases. Structure, Function and Clinical Applications, N. P. E. Vermeulen, G. J. Mulder, H. Nieuwenhuyse, W. H. M. Peters, P. J. van Bladeren. Taylor & Francis, London 1996; 187–197
   Google Scholar
• Caccuri A. M., Ascenzi P., Antonini G., Parker M. W., Oakley A. J., Chiessi E., Nuccetelli M., Battistoni A., Bellizia A., Ricci G. Structural flexibility modulates the activity of human glutathione transferase P1–1. Influence of a poor cosubstrate on dynamics and kinetics of human glutathione transferase. J. Biol. Chem. 1996; 271: 16193–16198
   PubMed Web of Science ®Google Scholar
• Cachau R. E., Erickson J. W., Villar H. O. Novel procedure for structure refinement in homology modeling and its application to the human class mu glutathione S-transferases. Protein Eng. 1994; 7: 831–839
   PubMedGoogle Scholar
• Hsiao C.-D., Martsen E. O., Lee J.-Y., Tam M. F. Amino acid sequencing, molecular cloning and modelling of the chick liver class-Theta glutathione S-transferase CLI. Biochem. J. 1995; 312: 91–98
   PubMed Web of Science ®Google Scholar
• Barry T. R., Waters P., Doonan S., Sheehan D. Structural investigation of a glutathione binding site using computational analysis. Biochem. Soc. Trans. 1995; 23: 382S
   PubMed Web of Science ®Google Scholar
• Aceto A., Sacchetta P., Bucciarelli T., Dragani B., Angelucci S., Radatti G. L., Di Ilio C. Structural and functional properties of the 34-kDa fragment produced by the N-terminal chymotryptic cleavage of glutathione transferase P1–1. Arch. Biochem. Biophys. 1995; 316: 873–878
   PubMed Web of Science ®Google Scholar
• Askelöf P., Guthenberg C., Jakobson I., Mannervik B. Purification and characterization of two glutathione S-aryltransferase activities from rat liver. Biochem. J. 1975; 147: 513
   PubMed Web of Science ®Google Scholar
• Danielson U. H., Esterbauer H., Mannervik B. Structure-activity relationships of 4-hydroxyalkenals in the conjugation catalysed by mammalian glutathione transferases. Biochem. J. 1987; 247: 707–713
   PubMed Web of Science ®Google Scholar
• Kolm R. H., Danielson U. H., Zhang Y., Talalay P., Mannervik B. Isothiocyanates as substrates for human glutathione transferases: structure-activity studies. Biochem. J. 1995; 311: 453–459
   PubMed Web of Science ®Google Scholar
• Polhuijs M., Mulder G. J., Meyer D. J., Ketterer B. Stereoselective conjugation of 2-bromocarboxylic acids and their urea derivatives by rat liver glutathione transferase 12–12 and some other isoforms. Biochem. Pharmacol. 1992; 44: 1249–1253
   PubMed Web of Science ®Google Scholar
• Mulders T. M. T., Van Ommen B., Van Bladeren P. J., Breimer D. D., Mulder G. I. Stereoselectivity of human liver and intestinal cytosolic fractions as well as purified human glutathione S-transferase isoenzymes towards 2-bromoisovalerylurea enantiomers. Biochem. Pharmacol. 1993; 46: 1775–1780
   PubMed Web of Science ®Google Scholar
• Vos R. M. E., Van Ommen B., Hoekstein M. S. J., De Goede J. H. M., Van Bladeren P. J. Irreversible inhibition of rat hepatic glutathione S-transferase isoenzymes by a series of structurally related quinones. Chem.-Biol. Interact. 1989; 71: 381–392
   PubMed Web of Science ®Google Scholar
• Van B., Ommen J., Ploemen H. T. M., Bogaards J. J. P., Monks T. J., Lau S. S., Van Bladeren P. J. Irreversible inhibition of rat glutathione S-transferase 1–1 by quinones and their glutathione conjugates. Biochem. J. 1991; 276: 661–666
   PubMed Web of Science ®Google Scholar
• Chen W.-J., Boehlert C. C., Rider K., Armstrong R. N. Synthesis and characterization of the oxygen and desthio analogues of glutathione as dead-end inhibitors of glutathione S-transferase. Biochem. Biophys. Res. Commun. 1985; 128: 233–240
   PubMed Web of Science ®Google Scholar
• Adang A. E. P., Brussee J., Meyer D. J., Coles B., Ketterer B., Van der Gen A., Mulder G. J. Substrate specificity of rat liver glutathione S-transferase isoenzymes for a series of glutathione analogues, modified at the γ-glutamyl moiety. Biochem. J. 1988; 255: 721–724
   PubMed Web of Science ®Google Scholar
• Adang A. E. P., Brussee J., Van der Gen A., Mulder G. J. The glutathione binding site in glutathione S-transferases: investigation of the cysteinyl, glycyl and γ-glutamyl domains. Biochem. J. 1990; 269: 47–54
   PubMed Web of Science ®Google Scholar
• Keen J. H., Habig W. H., Jakoby W. B. Mechanism for the several activities of the glutathione S-transferases. J. Biol. Chem. 1976; 251: 6183–6188
   PubMed Web of Science ®Google Scholar
• Miller J. Reaction Mechanisms in Organic Chemistry, C. Eaborn, N. B. Chapman. Elsevier, New York 1968; Vol. 8: 137–179
   Google Scholar
• Rietjens I. M. C. M., Soffers A. E. M. F., Hooiveld G. J. E. J., Veeger C., Vervoort J. Quantitative structure-activity relationships based on computer calculated parameters for the overall rate of glutathione S-transferase catalyzed conjugation of a series of fluoronitrobenzenes. Chem. Res. Toxicol. 1995; 8: 481–488
   PubMed Web of Science ®Google Scholar
• Soffers A. E. M. F., Ploemen J. H. T. M., Moonen M. J. H., Wobbes T., Van Ommen B., Vervoort J., Van Bladeren P. J., Rietjens I. M. C. M. Regioselectivity and quantitative structure-activity relationships for the conjugation of a series of fluoronitrobenzenes by purified glutathione S-transferase enzymes from rat and man. Chem. Res. Toxicol. 1996; 9: 638–646
   PubMed Web of Science ®Google Scholar
• Van der Aar E. M., De Groot M. J., Bijloo G. J., Van der Goot H., Vermeulen N. P. E. Structure-activity relationships for the glutathione conjugation of 2-substituted 1-chloro-4-nitrobenzenes by rat glutathione S-transferase 4–4. Chem. Res. Toxicol. 1996; 9: 527–534
   PubMed Web of Science ®Google Scholar
• Van der Aar E. M., Bouwman T., Commandeur J. N. M., Vermeulen N. P. E. Structure-activity relationships for chemical and glutathione S-transferase-catalyzed glutathione conjugation reactions of a series of 2-substituted 1-chloro-4-nitrobenzenes. Biochem. J. 1996; 320: 531–540
   PubMed Web of Science ®Google Scholar
• Kubo Y., Armstrong R. N. Observation of a substituent effect on the stereoselectivity of glutathione S-transferases toward para-substituted 4-phenyl-3-buten-2-ones. Chem. Res. Toxicol. 1989; 2: 144–145
   PubMed Web of Science ®Google Scholar