Probing the Mechanism of GSH Activation in Schistosoma haematobium Glutathione-S-transferase by Site-directed Mutagenesis and X-ray Crystallography

Journal of Molecular Biology

Volumn 360, Issue 3, 2006, Pages 678-689

  Baiocco, Paola ^a   Gourlay, Louise J ^a   Angelucci, Francesco ^a   Fontaine, Josette ^b   Hervé, Maxime ^b   Miele, Adriana E ^a   Trottein, François ^b   Brunori, Maurizio ^a   Bellelli, Andrea ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b INSERM   (France)

Author keywords

glutathione S transferase; GSH activation; mutagenesis; schistosomiasis; cation interaction

Indexed keywords

ARGININE; CATION; DIMER; GLUTATHIONE; GLUTATHIONE TRANSFERASE; GUANIDINE; MUTANT PROTEIN; TYROSINE;

ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; ENZYME ACTIVATION; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE; SCHISTOSOMA HEMATOBIUM; SCHISTOSOMIASIS; SITE DIRECTED MUTAGENESIS; X RAY CRYSTALLOGRAPHY;

SCHISTOSOMA HAEMATOBIUM;

EID: 33745637441     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.05.040     Document Type: Article

References (34)

1. WHO Expert Committee on the Control of Schistosomiasis. (1993). The Control of Schistosomiasis, WHO Technical Report Series no. 830, WHO, Geneva.
2. Armstrong R.N. Structure, catalytic mechanism, and evolution of the glutathione S-transferase. Chem. Res. Toxicol. 10 (1997) 2-18
3. Sheehan D., Meade G., Foley V.M., and Dowd C.A. Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily. Biochem. J. 360 (2001) 1-16
4. Kanaoka Y., Ago H., Inagaki E., Nanayama T., Miyano M., Kikuno R., et al. Cloning and crystal structure of hematopoietic prostaglandin D synthase. Cell 90 (1997) 1085-1095
5. Angelucci F., Baiocco P., Brunori M., Gourlay L., Morea V., and Bellelli A. Insights into the catalytic mechanism of glutathione S-transferase: the lesson from Schistosoma Haematobium. Structure 13 (2005) 1241-1246
6. Johnson K.A., Angelucci F., Bellelli A., Hervé M., Fontaine J., Tsernoglou D., et al. Crystal structure of the 28(kDa glutathione S-transferase from Schistosoma haematobium. Biochemistry 42 (2003) 10084-10094
7. Xiao G., Liu S., Ji X., Johnson W.W., Chen J., Parsone J.F., et al. First-sphere and second-sphere electrostatic effects in the active site of a class mu gluthathione transferase. Biochemistry 35 (1996) 4753-4765
8. Stenberg G., Board P.G., Carlberg I., and Mannervik B. Effects of directed mutagenesis on conserved arginine residues in a human class alpha glutathione transferase. Biochem. J. 274 (1991) 549-555
9. a of Tyr-9 in glutathione S-transferase A1-1 catalyzes product release. J. Biol. Chem. 278 (2003) 19257-19265
10. Ibarra C., Nieslanik B.S., and Atkins W.M. Contribution of aromatic-aromatic interactions to the anomalous pK(a) of tyrosine-9 and the C-terminal dynamics of glutathione S-transferase A1-1. Biochemistry 40 (2001) 10614-10624
11. Bjornestedt R., Stenberg G., Widersten M., Board P.G., Sinning I., Jones T.A., and Mannervik B. Functional significance of arginine 15 in the active site of human class alpha glutathione transferase A1-1. J. Mol. Biol. 247 (1995) 765-773
12. Stevens J.M., Armstrong R.N., and Dirr H.W. Electrostatic interactions affecting the active site of class sigma glutathione S-transferase. Biochem. J. 347 (2000) 193-197
13. Dietze E.C., Wang R.W., Lu A.Y., and Atkins W.M. Ligand effects on the fluorescence properties of tyrosine-9 in alpha 1-1 glutathione S-transferase. Biochemistry 35 (1996) 6745-6753
14. a of the thiol group of glutathione in the enzyme-glutathione complex. Biochem. Biophys. Res. Commun. 184 (1992) 194-197
15. Liu S., Zhang P., Ji X., Johnson W.W., Gilliland G.L., and Armstrong R.N. Contribution of tyrosine 6 to the catalytic mechanism of isoenzyme 3-3 of glutathione S-transferase. J. Biol. Chem. 267 (1992) 4296-4299
16. Pettersson P.L., and Mannervik B. The role of glutathione in the isomerization of delta 5-androstene-3,17-dione catalyzed by human glutathione transferase A1-1. J. Biol. Chem. 276 (2001) 11698-11704
17. Johansson A.S., and Mannervik B. Active-site residues governing high steroid isomerase activity in human glutathione transferase A3-3. J. Biol. Chem. 277 (2002) 16648-16654
18. Nyquist R.M., Heitbrink D., Bolwien C., Gennis R.B., and Heberle J. Direct observation of protonation reactions during the catalytic cycle of cytochrome c oxidase. Proc. Natl Acad. Sci. USA 22 (2003) 8715-8720
19. Frank R.A., Titman C.M., Pratap J.V., Luisi B.F., and Perham R.N. A molecular switch and proton wire synchronize the active sites in thiamine enzymes. Science 306 (2004) 872-876
20. Ortiz-Salmerón E., Nuccetelli M., Oakley A.J., Parker M.W., Lo Bello M., and García-Fuentes L. Thermodynamic description of the effect of the mutation Y49F on human glutathione transferase P1-1 in binding with glutathione and the inhibitor S-hexylglutathione. J. Biol. Chem. 278 (2003) 46938-46948
21. Stevens J.M., Armstrong R.N., Hornby J.A., and Dirr H.W. Class sigma glutathione transferase unfolds via a dimeric and a monomeric intermediate: impact of subunit interface on conformational stability in the superfamily. Biochemistry 37 (1998) 15534-15541
22. Ricci G., Caccuri A.M., Lo Bello M., Rosato N., Mei G., Nicotra M., et al. Structural flexibility modulates the activity of human glutathione transferase P1-1. Role of helix 2 flexibility in the catalytic mechanism. J. Biol. Chem. 271 (1996) 16187-16192
23. Chern M.K., Wu T.C., Hsieh C.H., Chou C.C., Liu L.F., Kuan I.C., et al. Tyr115, Gln165 and Trp209 contribute to the 1 (2000)2-epoxy-3-(p-nitrophenoxy)propane-conjugating activity of glutathione S-transferase cGSTM1-1. J. Mol. Biol. 300 (2000) 1257-1269
24. Nilsson L.O., Edalat M., Pettersson P.L., and Mannervik B. Aromatic residues in the C-terminal region of glutathione transferase A1-1 influence the rate-determining steps in the catalytic mechanism. Biochim. Biophys. Acta 1598 (2002) 199-205
25. Wongsantichon J., and Ketterman A.J. An intersubunit lock-and-key 'clasp' motif in the interface of Delta class glutathione transferase. Biochem. J. 394 (2005) 135-144
26. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
27. Navaza J. AMoRe: An automated package for molecular replacement. Acta Crystallog. sect. A 50 (1994) 157-163
28. Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallog. sect. D 50 (1994) 760-763
29. Murshudov G., Vagin A., and Dodson E. Refinement of macromolecular structures by the maximum likelihood method. Acta Crystallog. sect. D 53 (1997) 240-255
30. McRee D.E. XtalView/Xfit- a versatile program for manipulating atomic coordinates and electron density. J. Struct. Biol. 125 (1999) 156-165
31. Laskowski R.A., MacArthur M.W., Moss D.S., and Thornton J. M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallog. 26 (1993) 283-291
32. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallog. sect. D 60 (2004) 2126-2132
33. Liang J., Edelsbrunner H., and Woodward C. Anatomy of protein pockets and cavities: measurement of binding site geometry and implications for ligand design. Protein Sci. 7 (1998) 1884-1897
34. Kolm R.H., Sroga G.E., and Mannervik B. Participation of the phenolic hydroxyl group of Tyr-8 in the catalytic mechanism of human glutathione transferase P1-1. Biochem. J. 285 (1992) 537-540