The intersubunit lock-and-key motif in human glutathione transferase A1-1: Role of the key residues Met51 and Phe52 in function and dimer stability

Biochemical Journal

Volumn 393, Issue 2, 2006, Pages 523-528

  Alves, Carla S ^a   Kuhnert, Diane C ^a   Sayed, Yasien ^a   Dirr, Heini W ^a  

^a UNIVERSITY OF THE WITWATERSRAND   (South Africa)

Author keywords

8 anilinonaphthalene 1 sulphonic acid (ANS) binding; Conformational stability; Glutathione S transferases (GST); Human class Alpha GST with two type 1 subunits (hGSTA1 1); Lock and key motif

Indexed keywords

DIMERS; HYDROPHOBICITY; MONOMERS; SIZE EXCLUSION CHROMATOGRAPHY; ULTRAVIOLET RADIATION;

CONFORMATIONAL STABILITY; LOCK-AND-KEY MOTIF; SUBUNIT INTERFACE;

BIOCHEMISTRY;

8 ANILINO 1 NAPHTHALENESULFONIC ACID; DIMER; GLUTATHIONE TRANSFERASE; GLUTATHIONE TRANSFERASE A1; METHIONINE; PHENYLALANINE; TRYPTOPHAN; UNCLASSIFIED DRUG; UREA;

ARTICLE; CIRCULAR DICHROISM; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME CONFORMATION; ENZYME STABILITY; ENZYME STRUCTURE; FLUORESCENCE; GEL PERMEATION CHROMATOGRAPHY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDROPHOBICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN MOTIF;

AMINO ACID MOTIFS; DIMERIZATION; ENZYME STABILITY; GLUTATHIONE TRANSFERASE; HUMANS; ISOENZYMES; METHIONINE; MODELS, MOLECULAR; MUTATION; PHENYLALANINE; PROTEIN CONFORMATION;

EID: 30744449004     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20051066     Document Type: Article

References (49)

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. Wallace, L. A. and Dirr, H. W. (1999) Folding and assembly of dimeric human glutathione transferase A1-A1. Biochemistry 38, 16686-16694
3. Dirr, H. (2001) Folding and assembly of glutathione transferases. Chem. Bio. Int. 133, 19-23
4. 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
5. Armstrong, R. N. (1997) Structure, catalytic mechanism, and evolution of the glutathione transferases. Chem. Res. Toxicol. 10, 2-18
6. Wilce, M. C. and Parker, M. W. (1994) Structure and function of glutathione S-transferases. Biochim. Biophys. Acta 1205, 1-18
7. Ji, X., von Rosenvinge, E. C., Johnson, W. W., Tomarev, S. I., Piatigorsky, 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
8. Bousset, L., Belrhali, H., Janin, J., Melki, R. and Morera, S. (2001) Structure of the globular region of the prion protein Ure2 from the yeast Saccharomyces cerevisiae. Structure 9, 39-46
9. Stevens, J. M., Armstrong, R. N. and Dirr, H. W. (2000) Electrostatic interactions affecting the active site of class Sigma glutathione S-transferase. Biochem. J. 347, 193-197
10. Kanaoka, Y., Ago, H., Inagaki, E., Nanayama, T., Miyano, M., Kikuno, R., Fujii, Y., Eguchi, N., Toh, H., Urade, Y. and Hayaishi, O. (1997) Cloning and crystal structure of hematopoietic prostaglandin D synthase. Cell 90, 1085-1095
11. Agianian, B., Tucker, P. A., Schouten, A., Leonard, K., Bullard, B. and Gros, P. (2003) Structure of a Drosophila Sigma class glutathione S-transferase reveals a novel active site topography suited for lipid peroxidation products. J. Mol. Biol. 326, 151-165
12. Sayed, Y, Wallace, L. A. and Dirr, H. W. (2000) The hydrophobic lock-and-key intersubunit motif of glutathione transferase A1-A1: implications for catalysis, ligandin function and stability. FEBS Lett. 465, 169-172
13. Hornby, J. A., Codreanu, S. G., Armstrong, R. N. and Dirr, H. W. (2002) Molecular recognition at the dimer interface of a class Mu glutathione transferase: role of a hydrophobic interaction motif in dimer stability and protein function. Biochemistry 41, 14238-14247
14. Stenberg, G., Abdalla, A. M. and Mannervik, B. (2000) Tyrosine 50 at the subunit interface of dimeric human glutathione transferase P1-P1 is a structural key residue for modulating protein stability and catalytic function. Biochem. Biophys. Res. Commun. 271, 59-63
15. Vargo, M. A., Nguyen, L. and Colman, R. F. (2004) Subunit interface residues of glutathione S-transferase A1-A1 that are important in the monomer-dimer equilibrium. Biochemistry 43, 3327-3335
16. Abdalla, A. M., Bruns, C. M., Tainer, J. A., Mannervik, B. and Stenberg, G. (2002) Design of a monomeric human glutathione transferase GSTP1, a structurally stable but catalytically inactive protein. Protein Eng. 15, 827-834
17. Hegazy, U. M., Mannervik, B. and Stenberg, G. (2004) Functional role of the lock and key motif at the subunit interface of glutathione transferase P1-P1. J. Biol. Chem. 279, 9586-9596
18. Wallace, L. A., Blatch, G. L. and Dirr, H. W. (1998) A topologically conserved aliphatic residue in α-helix 6 stabilizes the hydrophobic core in domain II of glutathione transferases and is a structural determinant for the unfolding pathway. Biochem. J. 336, 413-418
19. Stenberg, G., Bjornestedt, R. and Mannervik, B. (1992) Heterologous expression of recombinant human glutathione transferase A1-A1 from a hepatoma cell line. Protein Expression Purif. 3, 80-84
20. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 227, 680-685
21. Perkins, S. J. (1986) Protein volumes and hydration effects: the calculations of partial specific volumes, neutron scattering matchpoints and 280-nm absorption coefficients for proteins and glycoproteins from amino acid sequences. Eur. J. Biochem. 157, 169-180
22. Habig, W. H. and Jakoby, W. B. (1981) Assays for differentiation of glutathione S-transferases. Methods Enzymol. 77, 398-405
23. Woody, R. W. (1995) Circular dichroism. Methods Enzymol. 246, 34-71
24. Pace, C. N. (1986) Determination and analysis of urea and guanidine hydrochloride denaturation curves. Methods Enzymol. 131, 266-280
25. Kirk, W. R., Kurian, E. and Prendergast, F. G. (1996) Characterization of the sources of protein-ligand affinity: 1-sulfonato-8-(1′) anilinonaphthalene binding to intestinal fatty acid binding protein. Biophys. J. 70, 69-83
26. Mosebi, S., Sayed, Y., Burke, J. and Dirr, H. W. (2003) Residue 219 impacts on the dynamics of the C-terminal region in glutathione transferase A1-A1: implications for stability and catalytic and ligandin functions. Biochemistry 42, 15326-15332
27. Wallace, L. A., Sluis-Cremer, N. and Dirr, H. W. (1998) Equilibrium and kinetic unfolding properties of dimeric human glutathione transferase A1-A1. Biochemistry 37, 5320-5328
28. Semisotnov, G. V., Rodionova, N. A., Kutyshenko, V. P., Ebert, B., Blanck, J. and Ptitsyn, O. B. (1987) Sequential mechanism of refolding of carbonic anhydrase B. FEBS Lett. 224, 9-13
29. Sinning, L, Kleywegt, G. J., Cowan, S. W., Reinemer, R, Dirr, H. W., Huber, R., Gilliland, G. L, Armstrong, R. N., Ji, X., Board, P G. et al. (1993) Structure determination and refinement of human Alpha class glutathione transferase A1-A1, and a comparison with the Mu and Pi class enzymes. J. Mol. Biol. 232, 192-212
30. Codreanu, S. G., Thompson, L. C., Hachey, D. L., Dirr, H. W. and Armstrong, R. N. (2005) Influence of the dimer interface on glutathione transferase structure and dynamics revealed by amide H/D exchange mass spectrometry. Biochemistry 44, 10605-10612
31. Cameron, A. D., Sinning, I, L'Hermite, G., Olin, B., Board, P. G., Mannervik, B. and Jones, T. A. (1995) Structural analysis of human Alpha-class glutathione transferase A1-A1 in the apo-form and in complexes with ethacrynic acid and its glutathione conjugate. Structures 3, 717-727
32. Bruns, C. M., Hubatsch, I., Ridderstrom, M., Mannervik, B. and Tainer, J. A. (1999) Human glutathione transferase A4-A4 crystal structures and mutagenesis reveal the basis of high catalytic efficiency with toxic lipid peroxidation products. J. Mol. Biol. 288, 427-439
33. Allardyce, C. S., McDonagh, P. D., Lian, L. Y., Wolf, C. R. and Roberts, G. C. (1999) The role of tyrosine-9 and the C-terminal helix in the catalytic mechanism of Alpha-class glutathione S-translerases. Biochem. J. 343, 525-531
34. Nilsson, L. O., Gustafsson, A. and Mannervik, B. (2000) Redesign of substrate-selectivity determining modules of glutathione transferase A1-A1 installs high catalytic efficiency with toxic alkenal products of lipid peroxidation. Proc. Natl. Acad. Sci. U.S.A. 97, 9408-9412
35. Pal, A., Gu, Y, Pan, S. S., Ji, X. and Singh, S. V. (2001) C-terminal region amino acid substitutions contribute to catalytic differences between murine class Alpha glutathione transferases mGSTA1-mGSTA1 and mGSTA2-mGSTA2 toward anti-diol epoxide isomers of benzo[c]phenanthrene. Biochemistry 40, 7047-7053
36. Gustafsson, A., Etahadieh, M., Jemth, P and Mannervik, B. (1999) The C-terminal region of human glutathione transferase A1-A1 affects the rate of glutathione binding and the ionization of the active-site Tyr9. Biochemistry 38, 16268-16275
37. Nilsson, L. O., Edalat, M., Pettersson, P. L. and Mannervik, B. (2002) Aromatic residues in the C-terminal region of glutathione transferase A1-A1 influence rate-determining steps in the catalytic mechanism. Biochim. Bioptiys. Acta 1597, 157-163
38. Nieslanik, B. S., Ibarra, C. and Atkins, W. M. (2001) The C-terminus of glutathione S-transferase A1-A1 is required for entropically-driven ligand binding. Biochemistry 40, 3536-3543
39. Bjornestedt, R., Stenberg, G., Widersten, M., Board, P. G., Sinning, I., Jones, T. A. and Mannervik, B. (1995) Functional significance of arginine 15 in the active site of human class Alpha glutathione transferase A1-A1. J. Mol. Biol. 247, 765-773
40. Dirr, H. W. and Wallace, L. A. (1999) Role of the C-terminal helix 9 in the stability and ligandin function of class Alpha glutathione transferase A1-A1. Biochemistry 38, 15631-15640
41. Sayed, Y., Hornby, J. A., Lopez, M. and Dirr, H. (2002) Thermodynamics of the ligandin function of human class Alpha glutathione transferase A1-A1: energetics of organic anion ligand binding. Biochem. J. 363, 341-346
42. Kuhnert, D. C., Sayed, Y., Mosebi, S., Sayed, M., Sewell, T. and Dirr, H. W. (2005) Tertiary interactions stabilise the C-terminal region of human glutathione transferase A1-A1 : a crystallographic and calorimetric study. J. Mol. Biol. 349, 825-838
43. 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 S-transferases. J. Biol. Chem. 280, 19480-19487
44. Meet, K. E. and Timm, D. E. (1994) Conformational stability of dimeric proteins: quantitative studies by equilibrium denaturation. Protein Sci. 3, 2167-2174
45. Hornby, J. A., Luo, J. K., Stevens, J. M., Wallace, L. A., Kaplan, W., Armstrong, R. N. and Dirr, H. W. (2000) Equilibrium folding of dimeric class Mu glutathione transferases involves a stable monomeric intermediate. Biochemistry 39, 12336-12344
46. Stevens, J. M., Hornby, J. A., Armstrong, R. N. and Dirr, H. W. (1998) Class Sigma glutathione transferase unfolds via a dimeric and a monomeric intermediate: impact of subunit interface on conformational stability in the superfamily. Biochemistry 37, 15534-15541
47. Myers, J. K., Pace, C. N. and Scholtz, J. M. (1995) Denaturant m values and heat capacity changes: relation to changes in accessible surface areas of protein unfolding. Protein Sci. 4, 2138-2148
48. Soulages, J. L. (1998) Chemical denaturation: potential impact of undetected intermediates in the free energy of unfolding and m-values obtained from a two-state assumption. Biophys. J. 75, 484-492
49. DeLano, W. L. (2002) The PyMOL Molecular Graphics System, DeLano Scientific, San Carlos, U.S.A.