Site-directed mutagenesis of mouse glutathione transferase P1-1 unlocks masked cooperativity, introduces a novel mechanism for 'ping pong' kinetic behaviour, and provides further structural evidence for participation of a water molecule in proton abstraction from glutathione

FEBS Journal

Volumn 278, Issue 2, 2011, Pages 273-281

  McManus, Gavin ^a   Costa, Marta ^b   Canals, Albert ^b,c   Coll, Miquel ^b,c   Mantle, Timothy J ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b INSTITUT DE BIOLOGIA MOLECULAR DE BARCELONA   (Spain)

^c INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

Author keywords

cooperativity; enzyme mechanism; GST; kinetics; thiol reactivity

Indexed keywords

GLUTATHIONE TRANSFERASE P1; GLUTATHIONE TRANSFERASE P1 1; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME KINETICS; GENETIC HETEROGENEITY; HYDROGEN BOND; MICHAELIS MENTEN KINETICS; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; SITE DIRECTED MUTAGENESIS; X RAY CRYSTALLOGRAPHY;

AMINO ACID SUBSTITUTION; ANIMALS; BIOCATALYSIS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; CYSTEINE; DINITROCHLOROBENZENE; DITHIONITROBENZOIC ACID; GLUTATHIONE; GLUTATHIONE S-TRANSFERASE PI; HYDROGEN-ION CONCENTRATION; KINETICS; MICE; MODELS, CHEMICAL; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PROTEIN BINDING; PROTEIN CONFORMATION; PROTONS; RECOMBINANT PROTEINS; WATER;

EID: 78651071342     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2010.07944.x     Document Type: Article

References (51)

1. Vuilleumier S, &, Pagni M, (2002) The elusive roles of bacterial glutathione S-transferases: new lessons from genomes. Appl Microbiol Biotechnol 58, 138-146.
2. Soranzo N, Sari Gorla M, Mizzi L, De Toma G, &, Frova C, (2004) Organisation and structural evolution of the rice glutathione S-transferase gene family. Mol Genet Genomics 271, 511-521.
3. Sappl PG, Onate-Sanchez L, Singh KB, &, Millar AH, (2004) Proteomic analysis of glutathione S-transferases of Arabidopsis thaliana reveals differential salicylic acid-induced expression of the plant-specific phi and tau classes. Plant Mol Biol 54, 205-219.
4. Hayes JD, Flanagan JU, &, Jowsey IR, (2005) Glutathione transferases. Annu Rev Pharmacol Toxicol 45, 51-88.
5. Bammler TK, Smith CA, &, Wolf CR, (1994) Isolation and characterization of two mouse Pi-class glutathione S-transferase genes. Biochem J 298, 385-390.
6. Suzuki T, Takagi Y, Osanai H, Li L, Takeuchi M, Katoh Y, Kobayashi M, &, Yamamoto M, (2005) Pi-class glutathione S-transferase genes are regulated by Nrf2 through an evolutionarily conserved regulatory element in zebrafish. Biochem J 388, 65-73.
7. Okuda A, Imagawa M, Maeda Y, Sakai M, &, Muramatsu M, (1989) Structural and functional analysis of an enhancer GPEI having a phorbol 12-O-tetradecanoate 13-acetate responsive element-like sequence found in the rat glutathione transferase P gene. J Biol Chem 264, 16919-16926.
8. Suzuki T, Morimura S, Diccianni MB, Yamada R, Hochi S, Hirabayashi M, Yuki A, Nomura K, Kitagawa T, Imagawa M, et al. (1996) Activation of glutathione transferase P gene by lead requires glutathione transferase P enhancer I. J Biol Chem 271, 1626-1632.
9. Ikeda H, Serria MS, Kakizaki I, Hatayama I, Satoh K, Tsuchida S, Muramatsu M, Nishi S, &, Sakai M, (2002) Activation of mouse Pi-class glutathione S-transferase gene by Nrf2 (NF-E2-related factor 2) and androgen. Biochem J 364, 563-570.
10. Lo HW, &, Ali-Osman F, (1998) Structure of the human allelic glutathione S-transferase-pi gene variant, hGSTP1 C, cloned from a glioblastoma multiforme cell line. Chem Biol Interact 111-112, 91-102.
11. Henderson CJ, Smith AG, Ure J, Brown K, Bacon EJ, &, Wolf CR, (1998) Increased skin tumorigenesis in mice lacking pi class glutathione S-transferases. Proc Natl Acad Sci USA 95, 5275-5280.
12. Sundberg K, Johansson AS, Stenberg G, Widersten M, Seidel A, Mannervik B, &, Jernstrom B, (1998) Differences in the catalytic efficiencies of allelic variants of glutathione transferase P1-1 towards carcinogenic diol epoxides of polycyclic aromatic hydrocarbons. Carcinogenesis 19, 433-436. (Pubitemid 28375445)
13. Ritchie KJ, Walsh S, Sansom OJ, Henderson CJ, &, Wolf CR, (2009) Markedly enhanced colon tumorigenesis in ApcMin mice lacking glutathione S-transferase Pi. Proc Natl Acad Sci USA 106, 20859-20864.
14. Lenney W, &, Fryer AA, (2007) The genetics of asthma: are the glutathione S-transferases serious players? Clin Exp Allergy 37, 1124-1126.
15. Islam T, Berhane K, McConnell R, Gauderman WJ, Avol E, Peters JM, &, Gilliland FD, (2009) Glutathione-S-transferase (GST) P1, GSTM1, exercise, ozone and asthma incidence in school children. Thorax 64, 197-202.
16. Adler V, Yin Z, Fuchs SY, Benezra M, Rosario L, Tew KD, Pincus MR, Sardana M, Henderson CJ, Wolf CR, et al. (1999) Regulation of JNK signaling by GSTp. EMBO J 18, 1321-1334.
17. Mileo AM, Abbruzzese C, Mattarocci S, Bellacchio E, Pisano P, Federico A, Maresca V, Picardo M, Giorgi A, Maras B, et al. (2009) Human papillomavirus-16 E7 interacts with glutathione S-transferase P1 and enhances its role in cell survival. PLoS ONE 4, e7254.
18. Manevich Y, Feinstein SI, &, Fisher AB, (2004) Activation of the antioxidant enzyme 1-CYS peroxiredoxin requires glutathionylation mediated by heterodimerization with pi GST. Proc Natl Acad Sci USA 101, 3780-3785.
19. Ricci G, Lo Bello M, Caccurri AM, Pastore A, Nuccetelli M, Parker MW, &, Federici G, (1995) 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 270, 1243-1248.
20. Caccuri AM, Antonini G, Ascenzi P, Nicotra M, Nuccetelli M, Mazzetti AP, Federici G, Lo Bello M, &, Ricci G, (1999) Temperature adaptation of glutathione S-transferase P1-1. A case for homotropic regulation of substrate binding. J Biol Chem 274, 19276-19280.
21. Vega MC, Walsh SB, Mantle TJ, &, Coll M, (1998) The three-dimensional structure of Cys-47-modified mouse liver glutathione S-transferase P1-1. Carboxymethylation dramatically decreases the affinity for glutathione and is associated with a loss of electron density in the αB-310B region. J Biol Chem 273, 2844-2850.
22. Abdalla AM, Bruns CM, Tainer JA, Mannervik B, &, Stenberg G, (2002) Design of a monomeric human glutathione transferase GSTP1, a structurally stable but catalytically inactive protein. Protein Eng 15, 827-834.
23. Henderson CJ, Wolf CR, Kitteringham N, Powell H, Otto D, &, Park BK, (2000) Increased resistance to acetaminophen hepatotoxicity in mice lacking glutathione S-transferase Pi. Proc Natl Acad Sci USA 97, 12741-12745.
24. Phillips MF, &, Mantle TJ, (1993) Inactivation of mouse liver glutathione S-transferase YfYf (Pi class) by ethacrynic acid and 5,5′-dithiobis-(2-nitrobenzoic acid). Biochem J 294, 57-62.
25. Florini JR, &, Vestling CS, (1957) Graphical determination of the dissociation constants for two-substrate enzyme systems. Biochim Biophys Acta 25, 575-578.
26. Phillips MF, &, Mantle TJ, (1991) The initial-rate kinetics of mouse glutathione S-transferase YfYf. Evidence for an allosteric site for ethacrynic acid. Biochem J 275, 703-709.
27. Pabst MJ, Habig WH, &, Jakoby WB, (1974) Glutathione S-transferase A. A novel kinetic mechanism in which the major reaction pathway depends on substrate concentration. J Biol Chem 249, 7140-7147.
28. Mannervik B, &, Askelöf P, (1975) Absence of a ping-pong pathway in the kinetic mechanism of glutathione S-transferase A from rat liver. Evidence based on quantitative comparison of the asymptotic properties of experimental data and alternative rat equations. FEBS Lett 56, 218-221.
29. McManus G, (2005) Studies on the three cysteines of mouse glutathione S-transferase P1. PhD Thesis, University of Dublin, Ireland.
30. Segel IH, (1975) In Enzyme Kinetics: Behaviour and Analysis of Rapid Equilibrium and Steady State Enzyme Systems, chapter 9, pp. 623-625. John Wiley & Sons Inc., New York.
31. Zhang ZR, Bai M, Wang XY, Zhou JM, &, Perrett S, (2008) Restoration of glutathione transferase activity by single-site mutation of the yeast prion protein Ure2p. J Mol Biol 384, 641-651.
32. Garcia-Saez I, Parraga A, Phillips MF, Mantle TJ, &, Coll M, (1994) Molecular structure at 1.8 Ã of mouse liver class pi glutathione S-transferase complexed with S-(p-nitrobenzyl)glutathione and other inhibitors. J Mol Biol 237, 298-314.
33. Caccuri AM, Lo Bello M, Nuccetelli M, Nicotra M, Rossi P, Antonini G, Federici G, &, Ricci G, (1998) Proton release upon glutathione binding to glutathione transferase P1-1: kinetic analysis of a multistep glutathione binding process. Biochemistry 37, 3028-3034.
34. Caccuri AM, Antonini G, Board PG, Parker MW, Nicotra M, Lo Bello M, Federici G, &, Ricci G, (1999) Proton release on binding of glutathione to Alpha, Mu and Delta class glutathione transferases. Biochem J 344, 419-425.
35. Tang SS, &, Chang GG, (1995) Steady-state kinetics and chemical mechanism of octopus hepatopancreatic glutathione transferase. Biochem J 309, 347-353.
36. Micaloni C, Kong GK, Mazzetti AP, Nuccetelli M, Antonini G, Stella L, McKinstry WJ, Polekhina G, Rossjohn J, Federici G, et al. (2003) Engineering a new C-terminal tail in the H-site of human glutathione transferase P1-1: structural and functional consequences. J Mol Biol 325, 111-122.
37. Xun L, Belchik SM, Xun R, Huang Y, Zhou H, Sanchez E, Kang C, &, Board PG, (2010) S-glutathionyl-(chloro)hydroquinone reductases: a novel class of glutathione transferases. Biochem J 428, 419-427.
38. Parraga A, Garcia-Saez I, Walsh SB, Mantle TJ, &, Coll M, (1998) The three-dimensional structure of a class-Pi glutathione S-transferase complexed with glutathione: the active-site hydration provides insights into the reaction mechanism. Biochem J 333, 811-816.
39. Orozco M, Vega C, Parraga A, Garcia-Saez I, Coll M, Walsh S, Mantle TJ, &, Javier Luque F, (1997) On the reaction mechanism of class Pi glutathione S-transferase. Proteins 28, 530-542.
40. Oakley AJ, Lo Bello M, Battistoni A, Ricci G, Rossjohn J, Villar HO, &, Parker MW, (1997) The structures of human glutathione transferase P1-1 in complex with glutathione and various inhibitors at high resolution. J Mol Biol 274, 84-100.
41. Hegazy UM, Mannervik B, &, Stenberg G, (2004) Functional role of the lock and key motif at the subunit interface of glutathione transferase p1-1. J Biol Chem 279, 9586-9596.
42. Misquitta SA, &, Colman RF, (2005) Communication between the two active sites of glutathione S-transferase A1-1, probed using wild-type-mutant heterodimers. Biochemistry 44, 8608-8619.
43. Widersten M, Björnestedt R, &, Mannervik B, (1996) Involvement of the carboxyl groups of glutathione in the catalytic mechanism of human glutathione transferase A1-1. Biochemistry 35, 7731-7742.
44. Walsh SB, (1997) Structural and kinetic studies on native and modified forms of glutathione S-transferase P1-1. PhD thesis, University of Dublin, Ireland.
45. Fisher CL, &, Pei GK, (1997) Modification of a PCR-based site-directed mutagenesis method. BioTechniques 23, 570-571.
46. Leslie AGW, (1992) Recent changes to the MOSFLM package for processing film and image plate data. Joint CCP4a+ ESF-EAMCB Newsletter on Protein Crystallography No. 26.
47. Evans P, (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr 50, 760-763.
48. Navaza J, (1994) AMoRe: an automated package for molecular replacement. Acta Crystallogr 50, 157-163.
49. Brunger AT, Adams PD, &, Rice LM, (1997) New applications of simulated annealing in X-ray crystallography and solution NMR. Structure 5, 325-336.
50. Winn MD, Isupov MN, &, Murshudov GN, (2001) Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr 57, 122-133.
51. Roussel A, &, Cambillau C, (1989) TURBO-FRODO. In Silicon Graphics Geometry Partners Directory, pp. 77-78. Silicon Graphics, Mountain View, CA.