Structural Insights into Omega-Class Glutathione Transferases: A Snapshot of Enzyme Reduction and Identification of a Non-Catalytic Ligandin Site

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Brock, Joseph ^a   Board, Philip G ^b   Oakley, Aaron J ^c  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b Biology and Environment   (Australia)

^c UNIVERSITY OF WOLLONGONG   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTATHIONE; GLUTATHIONE DISULFIDE; GLUTATHIONE TRANSFERASE; GLUTATHIONE TRANSFERASE OMEGA 1-1; GLUTATHIONE TRANSFERASE OMEGA 1-2; LIGANDIN; OMEGA CLASS GLUTATHIONE TRANSFERASE; S (4 NITROPHENACYL)GLUTATHIONE; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; COMPLEX FORMATION; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME MECHANISM; ENZYME METABOLISM; ENZYME REGENERATION; ENZYME STRUCTURE; ENZYME SUBSTRATE; GLUTATHIONE METABOLISM; HUMAN; HYDROPHOBICITY; LIGAND BINDING; NONHUMAN; PROTEIN BINDING; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; BINDING SITES; CATALYSIS; ELECTRONS; GLUTATHIONE TRANSFERASE; HUMANS; LIGANDS; MODELS, MOLECULAR; MOLECULAR DOCKING SIMULATION; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; SEQUENCE ALIGNMENT;

EID: 84876047892     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0060324     Document Type: Article

References (35)

1. Oakley AJ, (2005) Glutathione transferases: new functions. Current Opinion in Structural Biology 15: 716-723.
2. Board PG, Coggan M, Chelvanayagam G, Easteal S, Jermiin LS, et al. (2000) Identification, Characterization and Crystal structure of the Omega Class Glutathione Transferases. J Biol Chem 275: 24798-24806.
3. Whitbread AK, Tetlow N, Eyre HJ, Sutherland GR, Board PG, (2003) Characterization of the human Omega class glutathione transferase genes and associated polymorphisms. Pharmacogenetics 13: 131-144.
4. Dulhunty AF, Pouliquin P, Coggan M, Gage PW, Board PG, (2005) A recently identified member of the glutathione transferase structural family modifies cardiac RyR2 substate activity, coupled gating and activation by Ca2+ and ATP. Biochem J 390: 333-343.
5. Laliberte RE, Perregaux DG, Hoth LR, Rosner PJ, Jordan CK, et al. (2003) Glutathione s-transferase omega 1-1 is a target of cytokine release inhibitory drugs and may be responsible for their effect on interleukin-1beta posttranslational processing. J Biol Chem 278: 16567-16578.
6. Li YJ, Scott WK, Hedges DJ, Zhang F, Gaskell PC, et al. (2002) Age at onset in two common neurodegenerative diseases is genetically controlled. Am J Hum Genet 70: 985-993.
7. van de Giessen E, Fogh I, Gopinath S, Smith B, Hu X, et al. (2008) Association study on glutathione S-transferase omega 1 and 2 and familial ALS. Amyotroph Lateral Scler 9: 81-84.
8. Pongstaporn W, Pakakasama S, Sanguansin S, Hongeng S, Petmitr S, (2009) Polymorphism of glutathione S-transferase Omega gene: association with risk of childhood acute lymphoblastic leukemia. J Cancer Res Clin Oncol 135: 673-678.
9. Oakley A, (2011) Glutathione transferases: a structural perspective. Drug Metab Rev 43: 138-151.
10. Zhou H, Brock J, Liu D, Board PG, Oakley AJ, (2012) Structural insights into the dehydroascorbate reductase activity of human omega-class glutathione transferases. J Mol Biol 420: 190-203.
11. Schmuck EM, Board PG, Whitbread AK, Tetlow N, Cavanaugh JA, et al. (2005) Characterization of the monomethylarsonate reductase and dehydroascorbate reductase activities of Omega class glutathione transferase variants: implications for arsenic metabolism and the age-at-onset of Alzheimer's and Parkinson's diseases. Pharmacogenet Genomics 15: 493-501.
12. Whitbread AK, Masoumi A, Tetlow N, Schmuck E, Coggan M, et al. (2005) Characterization of the omega class of glutathione transferases. Methods Enzymol 401: 78-99.
13. Crawford MJ, Hutson DH, King PA, (1976) Metabolic demethylation of the insecticide dimethylvinphos in rats, in dogs, and in vitro. Xenobiotica 6: 745-762.
14. Board PG, Anders MW, (2007) Glutathione transferase omega 1 catalyzes the reduction of S-(phenacyl)glutathiones to acetophenones. Chem Res Toxicol 20: 149-154.
15. Board PG, Coggan M, Cappello J, Zhou H, Oakley AJ, et al. (2008) S-(4-Nitrophenacyl)glutathione is a specific substrate for glutathione transferase omega 1-1. Anal Biochem 374: 25-30.
16. McTigue MA, Williams DR, Tainer JA, (1995) 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: 21-27.
17. Ji X, von Rosenvinge EC, Johnson WW, Armstrong RN, Gilliland GL, (1996) Location of a potential transport binding site in a sigma class glutathione transferase by x-ray crystallography. Proc Natl Acad Sci U S A 93: 8208-8213.
18. Oakley AJ, Lo Bello M, Nuccetelli M, Mazzetti AP, Parker MW, (1999) 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 291: 913-926.
19. Catanzariti AM, Soboleva TA, Jans DA, Board PG, Baker RT, (2004) An efficient system for high-level expression and easy purification of authentic recombinant proteins. Protein Sci 13: 1331-1339.
20. Baker RT, Catanzariti AM, Karunasekara Y, Soboleva TA, Sharwood R, et al. (2005) Using deubiquitylating enzymes as research tools. Methods Enzymol 398: 540-554.
21. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, et al. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr 67: 235-242.
22. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
23. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66: 213-221.
24. Litwack G, Ketterer B, Arias IM, (1971) Ligandin: a hepatic protein which binds steroids, bilirubin, carcinogens and a number of exogenous organic anions. Nature 234: 466-467.
25. Reinemer P, Prade L, Hof P, Neuefeind T, Huber R, et al. (1996) 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 Mol Biol 255: 289-309.
26. Sampayo-Reyes A, Zakharyan RA, (2006) Inhibition of human glutathione S-transferase omega by tocopherol succinate. Biomed Pharmacother 60: 238-244.
27. Chen BY, Ma XX, Guo PC, Tan X, Li WF, et al. (2011) Structure-guided activity restoration of the silkworm glutathione transferase Omega GSTO3-3. J Mol Biol 412: 204-211.
28. Meux E, Prosper P, Masai E, Mulliert G, Dumarcay S, et al. (2012) Sphingobium sp. SYK-6 LigG involved in lignin degradation is structurally and biochemically related to the glutathione transferase omega class. FEBS Lett 586: 3944-3950.
29. Meux E, Prosper P, Ngadin A, Didierjean C, Morel M, et al. (2011) Glutathione transferases of Phanerochaete chrysosporium: S-glutathionyl-p-hydroquinone reductase belongs to a new structural class. J Biol Chem 286: 9162-9173.
30. Mathieu Y, Prosper P, Buee M, Dumarcay S, Favier F, et al. (2012) Characterization of a Phanerochaete chrysosporium glutathione transferase reveals a novel structural and functional class with ligandin properties. J Biol Chem 287: 39001-39011.
31. Rossjohn J, Polekhina G, Feil SC, Allocati N, Masulli M, et al. (1998) A mixed disulfide bond in bacterial glutathione transferase: functional and evolutionary implications. Structure 6: 721-734.
32. Allocati N, Federici L, Masulli M, Favaloro B, Di Ilio C, (2008) Cysteine 10 is critical for the activity of Ochrobactrum anthropi glutathione transferase and its mutation to alanine causes the preferential binding of glutathione to the H-site. Proteins 71: 16-23.
33. Federici L, Masulli M, Bonivento D, Di Matteo A, Gianni S, et al. (2007) Role of Ser11 in the stabilization of the structure of Ochrobactrum anthropi glutathione transferase. Biochem J 403: 267-274.
34. Katti SK, Robbins AH, Yang Y, Wells WW, (1995) Crystal structure of thioltransferase at 2.2 A resolution. Protein Sci 4: 1998-2005.
35. Washburn MP, Wells WW, (1999) Identification of the dehydroascorbic acid reductase and thioltransferase (Glutaredoxin) activities of bovine erythrocyte glutathione peroxidase. Biochem Biophys Res Commun 257: 567-571.