The ligandin (non-substrate) binding site of human pi class glutathione transferase is located in the electrophile binding site (H-site)

Journal of Molecular Biology

Volumn 291, Issue 4, 1999, Pages 913-926

  Oakley, Aaron J ^a   Lo Bello, Mario ^b   Nuccetelli, Marzia ^b   Mazzetti, Anna P ^b   Parker, Michael W ^a  

^a ST VINCENT'S INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

Detoxification; Glutathione transferases; Inhibitor complexes; Ligandin binding site; X ray crystallography

Indexed keywords

GLUTATHIONE TRANSFERASE; LIGANDIN;

ARTICLE; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME BINDING; PRIORITY JOURNAL; X RAY CRYSTALLOGRAPHY;

MAMMALIA;

EID: 0033609951     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1999.3029     Document Type: Article

References (61)

1. Ahmad H., Singhal S. S., Awasthi S. The inhibition of the α, μ, and π class isozymes of glutathione S-transferases by sulfasalazine, 5-aminosalicylic acid and sulfapyridine. Biochem. Arch. 8:1992;335-361.
2. Armstrong R. N. Structure, catalytic mechanism, and evolution of the glutathione transferases. Chem. Res. Toxicol. 10:1997;2-18.
3. Awasthi S., Sharma R., Singhal S. S., Herzog N. K., Chaubey M., Awasthi Y. C. Modulation of cisplatin cytotoxicity by sulphasalazine. Brit. J. Cancer. 70:1994;190-194.
4. Bico P., Erhardt J., Kaplan W., Dirr H. Porcine class pi glutathione S-transferase: anionic ligand binding and conformational analysis. Biochim. Biophys. Acta. 1247:1995;225-230.
5. Board P. G., Baker R. T., Chelvanayagam G., Jermiin L. S. Zeta, a novel class of glutathione transferases in a range of species from plants to humans. Biochem. J. 328:1997;929-935.
6. Brünger A. T. X-PLOR, Version 3.1: A system for X-ray Crystallography and NMR. 1992;Yale University Press, New Haven.
7. Buetler T. M., Eaton D. L. Glutathione S-transferases: amino acid sequence comparison, classification and phylogenetic relationship. Environ. Carcinogen. Ecotoxicol. Rev. C10:1992;181-203.
8. Caccuri A. M., Aceto A., Piemonte F., Di Ilio C., Rosato N., Federici G. Interaction of hemin with placental glutathione transferase. Eur. J. Biochem. 189:1990;493-497.
9. CCP4. The CCP4 Suite: programs for protein crystallography. Acta Crystallog. sect. D. 50:1994;750-763.
10. Coles B., Ketterer B. The role of glutathione and glutathione transferases in chemical carcinogenesis. CRC Crit. Rev. Biochem. Mol. Biol. 25:1990;47-70.
11. Das K. M., Rubin R. Clinical pharmacokinetics of sulphasalazine. Clin. Pharmacokin. 1:1976;406-425.
12. 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. 266:1991;2063-2066.
13. Dirr 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. 220:1994;645-661.
14. Engh R. A., Huber R. Accurate bond and angle parameters for X-ray structure refinement. Acta Crystallog. sect. D. 47:1991;392-400.
15. García-Sáez I., 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 withS -(p -nitrobenzyl)glutathione and other inhibitors. J. Mol. Biol. 237:1994;298-314.
16. Gupta V., Jani J. P., Jacobs S., Levitt M., Fields L., Awasthi S., Xu B. H., Sreevardhan M., Awasthi Y. C., Singh S. V. Activity of melphalan in combination with the glutathione transferase inhibitor sulfasalazine. Cancer Chemother. Pharmacol. 36:1995;13-19.
17. Habig W. H., Pabst M. J., Fleischner G., Gatmaitan Z., Arias I. M., Jakoby W. B. The identity of glutathione S-transferase B with ligandin, a major binding protein of liver. Proc. Natl Acad. Sci. USA. 71:1974a;3879-3882.
18. Habig W. H., Pabst M. J., Jakoby W. B. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J. Biol. Chem. 249:1974b;7130-7139.
19. 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. Mol. Biol. 30:1995;445-600.
20. 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. 31:1992;10169-10184.
21. NAr reaction catalysed by glutathione transferase. Biochemistry. 32:1993;12949-12954.
22. 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. 34:1995;5317-5328.
23. Ji X., von Rosenvinge E. C., Johnson W. W., Armstrong R. N., Gilliland G. L. Location of a potential transport binding site in a sigma class glutathione transferase by X-ray crystallography. Proc. Natl Acad. Sci. USA. 93:1996;8208-8213.
24. Ji X., Tordova M., O'Donnell R., Parsons J. F., Hayden J. B., Gilliland G. L., Zimniak P. Structure and function of the xenobiotic substrate-binding site and the location of a potential non-substrate-binding site in a class π glutathione S-transferase. Biochemistry. 36:1997;9690-9702.
25. Ketley J. N., Habig W. H., Jakoby W. B. Binding of nonsubstrate ligands to the glutathione S-transferases. J. Biol. Chem. 250:1975;8670-8673.
26. Ketterer B., Carne T., Tipping E. Ligandin and Protein A: intracellular binding proteins. Blauer G., Sund H. Transport by Proteins. 1978;79-92 FEBS Symposium no. 58, Walter de Gruyter, Berlin.
27. Kleywegt G., Jones T. A. Halloween ... MAsks and Bones. Bailey S., Hubbard R., Waller D. From First Map to Final Model. 1994;59-66 EPSRC, Daresbury Laboratory, Warrington.
28. Kraulis P. MOLSCRIPT: a program to produce both detailed and schematic plots of proteins. J. Appl. Crystallog. 24:1991;946-950.
29. Laskowski R. A., McArthur M. W., Moss D. S., Thorton J. M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallog. 26:1993;282-291.
30. Litwack G., Ketterer B., Arias I. M. Ligandin: a hepatic protein which binds steroids, bilirubin, carcinogens and a number of exogenous organic anions. Nature. 234:1971;466-467.
31. Lo Bello M., Pastore A., Petruzzelli R., Parker M. W., Wilce M. C. J., Federici G., Ricci G. Conformational stability of human placental glutathione transferase as probed by limited proteolysis. Biochem. Biophys. Res. Commun. 194:1993;804-810.
32. 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. 270:1995;1249-1253.
33. Lo Bello M., Oakley A. J., Battistoni A., Mazzetti A. P., Nuccetelli M., Mazzarese G., Rossjohn J., Parker M. W., Ricci G. Multifunctional role of Tyr108 in the catalytic mechanism of human glutathione transferase P1-1. Crystallographic and kinetic studies of the Y108F mutant enzyme. Biochemistry. 36:1997;6207-6217.
34. Lo Bello M., Nuccetelli M., Chiessi E., Lahm A., Mazzetti A. P., Battistoni A., Caccuri A. M., Oakley A. J., Parker M. W., Tramontano A., Federici G., Ricci G. 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. 284:1998;1717-1725.
35. Mannervik B., Danielson U. H. Glutathione transferases - structure and catalytic activity. CRC Crit. Rev. Biochem. 23:1988;283-337.
36. Mannervik B., Ålin 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 propoerties. Proc. Natl Acad. Sci. USA. 82:1985;7202-7206.
37. McTigue 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. Mol. Biol. 246:1995;21-27.
38. Meyer D. J., Coles B., Pemble S. E., Gilmore K. S., Fraser G. M., Ketterer B. Theta, a new class of glutathione transferases from rat and man. Biochem. J. 274:1991;409-414.
39. Nishihira J., Ishibashi T., Sakai M., Tsuda S., Hikichi K. Identification of the hydrophobic ligand-binding region in recombinant glutathione S-transferase P and its binding effect on the conformational state of the enzyme. Arch. Biochem. Biophys. 302:1993;128-133.
40. Nuccetelli M., Mazzetti A. P., Rossjohn J., Parker M. W., Board P. G., Caccuri A. M., Federici G., Ricci G., Lo Bello M. Shifting substrate specificity of human glutathione transferase (from class Pi to class Alpha) by a single point mutation. Biochem. Biophys. Res. Commun. 252:1998;184-189.
41. Oakley A. J., Lo Bello M., Battistoni A., Ricci G., Rossjohn J., Villar H. O., Parker M. W. The structures of human glutathione transferase P1-1 in complex with glutathione and various inhibitors at high resolution. J. Mol. Biol. 274:1997a;84-100.
42. Oakley A. J., Rossjohn J., Lo Bello M., Caccuri A. M., Federici G., Parker M. W. The three-dimensional structure for the human pi class glutathione transferase P1-1 in complex with the inhibitor ethacrynic acid and its glutathione conjugate. Biochemistry. 36:1997b;576-585.
43. Oakley A. J., Lo Bello M., Ricci G., Federici G., Parker M. W. Evidence for an induced fit mechanism operating in pi class glutathione transferases. Biochemistry. 37:1998;9912-9917.
44. Otwinowski Z. Oscillation data reduction program. Sawyer L., Isaacs N., Bailey S. Data Collection and Processing. 1993;56-62.
45. Pemble S. E., Wardle A. F., Taylor J. B. Glutathione S-transferase class Kappa: characterisation by the cloning of the rat mitochondrial GST and identification of a human homologue. Biochem. J. 319:1996;749-754.
46. Prade L., Huber R., Manoharan T. H., Fahl W. E., Reuter W. Structures of class pi glutathione S-transferase from human placenta in complex with substrate, transition-state analogue and inhibitor. Structure. 5:1997;1287-1295.
47. Pullar T. Sulphasalazine and related drugs in rheumatoid arthritis. Pharmac. Ther. 42:1989;459-468.
48. Reinemer P., Dirr H. W., Ladenstein R., Schäffer J., Gallay O., Huber R. The three-dimensional structure of class pi glutathione S-transferase in complex with glutathione sulfonate at 2.3 Å resolution. EMBO J. 10:1991;1997-2005.
49. Reinemer P., Dirr H. W., Ladenstein R., Huber R., Lo Bello M., Federici G., Parker M. W. Three-dimensional structure of class pi glutathione S -transferase from human placenta in complex withS -hexylglutathione at 2.8 Å resolution. J. Mol. Biol. 227:1992;214-226.
50. Reinemer P., Prade L., Hof P., Neuefeind T., Hiber 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 Å resolution: structural characterisation of herbicide-conjugating plant glutathione S -transferase and a novel active site architecture. J. Mol. Biol. 255:1996;289-309.
51. 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 P 1-1. J. Biol. Chem. 270:1995;1243-1248.
52. Rossjohn J., Polekhina G., Feil S. C., Allocati N., Masulli M., Di Ilio C., Parker M. W. A mixed disulfide bond in bacterial glutathione transferase: functional and evolutionary implications. Structure. 6:1998;721-734.
53. 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. Mol. Biol. 232:1993;192-212.
54. Svartz N. Salazopyrin, a new sulfanilamide preparation. Acta Medica Scandinavica. 110:1942;577-598.
55. Tahir M. K., Guthenberg C., Mannervik B. Inhibitors for distinction of three types of human glutathione transferase. FEBS Letters. 181:1985;249-252.
56. Tipping E., Ketterer B. The influence of soluble binding proteins on lipophile transport and metabolism in hepatocytes. Biochem. J. 195:1981;441-452.
57. Tsuchida S., Sato K. Glutathione transferases and cancer. CRC Crit. Rev. Biochem. Mol. Biol. 27:1992;337-384.
58. 2O (1/0. 5/n) (n≅2.25). Acta Crystallog. sect. C. 46:1990;883-886.
59. Waxman D. J. Glutathione S-transferases: role in alkylating agent resistance and possible target for modulation chemotherapy - a review. Cancer Res. 50:1990;6449-6454.
60. Wilce M. C. J., Parker M. W. Structure and function of glutathione S-transferases. Biochim. Biophys. Acta. 1205:1994;1-18.
61. Wilce M. C. J., Board P. G., Feil S. C., Parker M. W. Crystal structure of a theta-class glutathione transferase. EMBO J. 14:1995;2133-2143.