Glutathione transferases in the genomics era: New insights and perspectives

Biomolecular Engineering

Volumn 23, Issue 4, 2006, Pages 149-169

  Frova, Carla ^a  

^a UNIVERSITY OF MILAN   (Italy)

Author keywords

Evolution; Forced evolution; Omics; Protein families; Thioredoxin fold; Transgenics

Indexed keywords

ENZYME KINETICS; GENETIC ENGINEERING; KNOWLEDGE ACQUISITION; MICROORGANISMS; MOLECULAR DYNAMICS; PROTEINS;

EVOLUTION; FORCED EVOLUTION; GLUTATHIONE TRANSFERASES (GST); OMICS; PROTEIN FAMILIES; THIOREDOXIN FOLD; TRANSGENICS;

BIOMEDICAL ENGINEERING;

GLUTATHIONE TRANSFERASE;

BIOLOGY; BIOTECHNOLOGY; EUKARYOTE; EVOLUTION; GENETIC ENGINEERING AND GENE TECHNOLOGY; GENOMICS; MEMBRANE STRUCTURE; MICROSOME; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEOMICS; REVIEW; STRUCTURE ANALYSIS; TRANSGENIC ORGANISM; TRANSGENICS;

ANIMALS; BIOTECHNOLOGY; EUKARYOTIC CELLS; EVOLUTION, MOLECULAR; GENOMICS; GLUTATHIONE TRANSFERASE; HUMANS; STRUCTURE-ACTIVITY RELATIONSHIP;

EUKARYOTA;

EID: 33746474688     PISSN: 13890344     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bioeng.2006.05.020     Document Type: Review

References (135)

1. Adler V., Yin Z., Fuchs S.Y., Benezra M., Rosario L., Tew K.D., Pinkus M.R., Sardana M., Henderson C.J., Wolf C.R., and Ronai Z. Regulation of JNK signaling by GSTp. EMBO J. 18 (1999) 1321-1334
2. Allocati N., Casalone E., Masulli M., Ceccarelli I., Carletti E., Parker M.W., and Di Ilio C. Functional analysis of the evolutionarily conserved proline 53 residue in Proteus mirabilis glutathione S-transferase B1-1. FEBS Lett. 445 (1999) 347-350
3. Allocati N., Favaloro B., Masulli M., Alexeyev M.F., and Di Ilio C. Proteus mirabilis glutathione S-transferase B1-1 is involved in protective mechanisms against oxidative and chemical stress. Biochem. J. 373 (2003) 305-311
4. Andersson C.E., Mosialou E., Weinander R., and Morgenstern R. Enzymology of microsomal glutathione S-transferase. Adv. Pharmacol. 27 (1994) 19-35
5. Armstrong R.N. Structure, catalytic mechanism, and evolution of the glutathione transferases. Chem. Res. Toxicol. 10 (1997) 2-18
6. Armstrong R.N. Mechanistic imperatives for the evolution of glutathione transferases. Curr. Opin. Chem. Biol. 2 (1998) 618-623
7. Axarli I.A., Ridgen D.J., and Labrou N.E. Characterization of the ligandin site of maize glutathione S-transferase I. Biochem. J. 382 (2004) 885-893
8. Bartling D., Radzio R., Steiner U., and Weiler E.W. A glutathione S-transferase with glutathione-peroxidase activity from Arabidopsis thaliana. Eur. J. Biochem. 216 (1993) 579-586
9. Bijörnestedt R., Tardioli S., and Mannervik B. The high activity of rat glutathione transferase 8-8 with alkene substrates is dependent on a glycine residue in the active site. J. Biol. Chem. 270 (1995) 29705-29709
10. Board P.G., Baker R.T., Chelvanayagam G., and Jermiin L.S. Zeta, a novel class of glutathione transferases in a large range of species from plants to humans. Biochem. J. 328 (1997) 929-935
11. Board P.G., Coggan M., Chelvanayagam G., Easteal S., Jermiin L.S., Schulte G.K., Danley D.E., Hoth L.R., Griffor M.C., Kamath A.V., Rosner M.H., Chrunyk B.A., Perregaux D.E., Gabel C.A., Geoghegan K.F., and Pandit J. Identification, characterization, and crystal structure of the Omega class glutathione transferases. J. Biol. Chem. 275 (2000) 24798-24806
12. Bresell A., Weinander R., Lundqvist G., Raza H., Shimoji M., Sun T.-H., Balk L., Wiklund R., Eriksson J., Jansson C., Persson B., Jakobsson P.-J., and Morgenstern R. Bioinformatic and enzymatic characterization of the MAPEG superfamily. FEBS J. 272 (2005) 1688-1703
13. Broo K., Larsson A.-K., Jemth P., and Mannervik P. An ensemble of Theta class glutathione transferases with novel catalytic properties generated by stochastic recombination of fragments of two mammalian enzymes. J. Mol. Biol. 318 (2002) 59-70
14. Burns C.M., Hubatsch I., Ridderström M., Mannervik B., and Tainer J.A. Human glutathione transferase A4-4 crystal structures and mutagenesis reveal the basis of high catalytic efficiency with toxic lipid peroxidation products. J. Mol. Biol. 288 (1999) 427-439
15. Busenlehner L.S., Codreanu S.G., Holm P.J., Bhakat P., Hebert H., Morgenstern R., and Armstrong R.N. Stress sensor triggers conformational response of the integral membrane protein microsomal glutathione transferase 1. Biochemistry 43 (2004) 11145-11152
16. Byrum R.S., Goulet J.L., Griffith R.J., and Koller B.H. Role of the 5-lipoxygenase-activating protein (FLAP) in murine acute inflammatory responses. J. Exp. Med. 185 (1997) 1065-1075
17. Caccuri A.M., Antonini G., Allocati N., Di Ilio C., De Maria F., Innocenti F., Parker M.W., Fasulli M., Lo Bello M., Tirella P., Federici G., and Ricci G. GSTB1-1 from Proteus mirabilis. A snapshot of an enzyme in the evolutionary pathway from a redox enzyme to a conjugating enzyme. J. Biol. Chem. 277 (2002) 16777-16784
18. Caccuri A.M., Antonini G., Ascenzi P., Nicotra M., Nuccetelli M., Mazzetti A.P., Federici G., Lo Bello M., and Ricci G. Temperature adaptation of glutathione S-transferase P1-1. A case of homotropic regulation of substrate binding. J. Biol. Chem. 274 (1999) 19276-19280
19. Caccuri A.M., Antonini G., Nicotra M., Battistoni A., Lo Bello M., Board P.G., Parker M.W., and Ricci G. Catalytic mechanism and role of hydroxyl residues in the active site of theta class glutathione S-transferases. Investigation of Ser-9 and Tyr-113 in a glutathione S-transferase from the Australian sheep bowfly, Lucilia cuprina. J. Biol. Chem. 272 (1997) 29681-29686
20. Chelvanayagam G., Parker M.W., and Board P.G. Fly fishing for GSTs: a unified nomenclature for mammalian and insect glutathione transferases. Chem. Biol. Interact. 133 (2001) 256-260
21. Cho S.G., Lee Y.H., Park H.S., Ryoo K., Kank K.W., Park J., Eom S.J., Kim M.J., Chang T.S., Choi S.Y., Shim J., Kim Y., Dong M.J., Kim S.G., Ichijo H., and Choi F.J. Glutathione S-transferase mu modulates the stress-activated signals by suppressing apoptosis signal-regulating kinase 1. J. Biol. Chem. 276 (2001) 12749-12755
22. Coleman J.O.D., Blake-Kalff M.M.A., and Davies T.G.E. Detoxification of xenobiotics by plants: chemical modification and vacuolar compartmentation. Trends Plant Sci. 2 (1997) 144-151
23. Collison E.J., and Grant C.M. Role of yeast glutaredoxins as glutathione S-transferases. J. Biol. Chem. 278 (2003) 22492-22497
24. Copley S.D., Novak W.R.P., and Babbitt P.C. Divergence of function in the thioredoxin fold superfamily: evidence for evolution of peroxiredoxins from a thioredoxin-like ancestor. Biochemistry 43 (2004) 13981-13995
25. Cromer B.A., Morton C.J., Board P.G., and Parker M.W. From glutathione transferase to pore in a CLIC. Eur. Biophys. J. 31 (2002) 356-364
26. Dirr H., Reinemer P., and 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
27. Dirr H., Reinemer P., and Huber R. Refined crystal structure of porcine class Pi glutathione S-transferase (pGST P1-1) at 2.1 Å resolution. J. Mol. Biol. 243 (1994) 72-92
28. Dixon D.P., Cummins I., Cole D.J., and Edwards R. Glutathione mediated detoxification systems in plants. Curr. Opin. Plant Biol. 1 (1998) 258-266
29. Dixon D.P., Davies B.G., and Edwards E. Functional divergence in the glutathione transferase superfamily in plants. J. Biol. Chem. 277 (2002) 30859-30869
30. Dixon D.P., Lapthorn A., and Edwards R. Plant glutathione transferases. Genome Biol. 3 (2002) 3004.1-3004.10
31. Dixon D.P., McEwen A.G., Lapthorn A.J., and Edwards R. Forced evolution of a herbicide detoxifying glutathione trasnsferase. J. Biol. Chem. 278 (2003) 23930-23935
32. Dulhunty A., Gage P., Curtis S., Chelvanayagam G., and Board P. The glutathione transferase structural family includes a nuclear chloride channel and a ryanodine receptor calcium release channel modulator. J. Biol. Chem. 276 (2001) 3319-3323
33. Edwards R., Dixon D.P., and Walbot V. Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health. Trends Plant Sci. 5 (2000) 193-198
34. Engle M.R., Singh S.P., Czernik P.J., Gaddy D., Montagne D.C., Ceci J.D., Yang Y., Awasthi Y.C., and Zimniak P. Physiological role of mGSTA4-4, a glutahione S-transferase metabolizing 4-hydroxynonenal: generation and analysid of mGSTA4 null mouse. Toxicol. Appl. Pharmacol. 194 (2004) 296-308
35. Epp O., Ladenstein R., and Wendel A. The refined structure of the selenoenzyme glutathione peroxidase at 0.2 nm resolution. Eur. J. Biochem. 133 (1983) 51-69
36. Erhardt J., and Dirr H.W. Native dimer stabilizes the subunit tertiary structure of porcine class Pi glutathione S-transferase. Eur. J. Biochem. 230 (1995) 614-620
37. Fernandez-Cañon J.M., and Peñalva M.A. Characterisation of a fungal maleylacetoacetate isomerase genes and identification of its human homologue. J. Biol. Chem. 273 (1998) 328-337
38. Fernandez-Cañon J.M., Baetscher M.W., Finegold M., Burlingame T., Gibson K.M., and Grompe M. Maleylacetoacetate isomerase (MAAI/GSTZ)-deficient mice reveal a glutathione-dependent nonenzymatic bypass in tyrosine catabolism. Mol. Cell. Biol. 22 (2002) 4943-4951
39. Frova C. The plant glutathione transferase gene family: genomic structure, functions, expression and evolution. Physiol. Plant. 119 (2003) 469-479
40. Frova C., De Toma G., Mizzi L., and Sari Gorla M. Plant GSTs: diversification and evolution. In: Schnarrenberger C., and Wittmann-Liebhold B. (Eds). Genes, Gene Families and Isozymes: Medimond International Proceedings. Italy (2004) 199-205
41. Gerlt J.A., and Babbitt P.C. Mechanistically diverse enzyme superfamilies: the importance of chemistry in the evolution of catalysis. Curr. Opin. Chem. Biol. 2 (1998) 607-612
42. 8-barrel enzymes. Curr. Opin. Chem. Biol. 7 (2003) 252-264
43. Hansson L.O., Bolton-Grob R., Massoud T., and Mannervik B. Evolution of different substrate specificities in Mu class glutathione transferase probed by DNA shuffling. J. Mol. Biol. 287 (1999) 265-276
44. Harris J.M., Meyer D.J., Coles B., and Ketterer B. A novel glutathione transferase (13-13) isolated from the matrix of rat liver mitochondria having structural similarity to class theta enzymes. Biochem. J. 278 (1991) 137-141
45. Harrop S.J., DeMaere M.Z., Fairlie W.D., Reztova T., Valenzuela S.M., Mazzanti M., Tonini R., Qiu M.R., Jankova L., Warton K., Bauskin A.R., Wu W.M., Pankhurst S., Campbell T.J., Breit S.N., and Curmi P.M.G. Crystal sructure of a soluble form of the intracellular chloride ion channel CLIC1 (NCC27) at 1.4-Å resolution. J. Biol. Chem. 276 (2001) 44993-45000
46. Hayes J.D., Flanagan J.U., and Jowsey I.R. Glutathione transferases. Annu. Rev. Pharmacol. Toxicol. 45 (2005) 51-88
47. Hayes J.D., and Pulford D.J. The glutathione S-transferase supergene family. Regulation of GST and the contribution of the isoenzymes to cancer chemoprotection and drug resistance. CRC Crit. Rev. Biochem. Mol. Biol. 30 (1995) 445-600
48. Hederos S., Broo K.S., Jakobsson E., Kleywegt G., Mannervik B., and Baltzer L. Incorporation of a single His residue by rational design enables thiol-ester hydrolysis by human glutathione transferase A1-1. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 13163-13167
49. Hegazy U.M., Mannervik B., and Stenberg G. Functional role of the lock and key motif at the subunit interface of glutathione transferase P1-1. J. Biol. Chem. 279 (2004) 9586-9596
50. Henderson C.J., Smith A.G., Ure J., Brown K., Bacon E.J., and Wolf C.R. Increased skin tumorigenesis in mice lacking pi class glutathione S-transferases. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 5275-5280
51. Hornby J.A., Codreanu S.G., Armstrong R.N., and Dirr H.W. 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 (2002) 14238-14247
52. Hu X., Benson P.J., Srivastava S.K., Xia H., Bleicher R.J., Zaren H.A., Awasthi S., Awasthi Y.C., and Singh S.V. Induction of glutathione S-transferase π as a bioassay for the evaluation of potency inhibitors of benzo(a)pyrene-induced cancer in a murine model. Int. J. Cancer 73 (1997) 897-902
53. Ivarsson Y., Mackey A.J., Edalat M., Pearson W.R., and Mannervik B. Identification of residues in glutathione transferase capable of driving functional diversification in evolution. J. Biol. Chem. 278 (2003) 8733-8738
54. Jakobsson P.-J., Mancini J.A., and Ford-Hutchinson A.W. Identification and characterization of a novel human microsomal glutathione S-transferase with leukotriene C4 synthase activity and significant sequence identity to 5-lipoxygenase-activating protein and leukotriene C4 synthase. J. Biol. Chem. 271 (1996) 22203-22210
55. Jakobsson P.-J., Mancini J.A., Riendeau D., and Ford-Hutchinson A.W. Identification and characterization of a novel microsomal enzyme with glutathione-dependent transferase and peroxidase activity. J. Biol. Chem. 272 (1997) 22934-22939
56. Jakobsson P.-J., Morgenstern R., Mancini J., Ford-Hutchinson A., and Persson B. Common structural features of MAPEG-a widespread superfamily of membrane associated proteins with highly divergent functions in eicosanoid and glutathione metabolism. Protein Sci. 8 (1999) 689-692
57. Jakobsson P.-J., Morgenstern R., Mancini J., Ford-Hutchinson A., and Persson B. Membrane-associated proteins in eicosanoid and glutathione metabolism (MAPEG). A widespread protein superfamily. Am. J. Respir. Crit. Care Med. 161 (2000) S20-S24
58. Jensson H., Guthenberg C., Alin P., and Mannervik B. Rat glutathione transferase 8-8, an enzyme efficiently detoxifying 4-hydroxyalk-2-enals. FEBS Lett. 203 (1986) 207-209
59. Jeppesen M.G., Ortiz P., Shepard W., Kinzy T.G., Nyborg J., and Andersen G.R. The crystal structure of the glutathione S-transferase-like domain of elongation factor 1Bγ from Saccharomyces cerevisiae. J. Biol. Chem. 278 (2003) 47190-47198
60. Jepson I., Holt D.C., Roussel V., Wright S.Y., and Greenland A.J. Transgenic plant analysis as a tool for the study of maize glutathione S-transferases. In: Hatzios K. (Ed). Regulation of Enzymatic Systems Detoxifying Xenobiotics in Plants (1997), Kluwer Academic Publishers, The Netherlands 313-323
61. Jowsey R.I., Thomson R.E., Orton T.C., Elcombe C.R., and Hayes J.D. Biochemical and genetic characterization of a murine class Kappa glutathione S-transferase. Biochem. J. 373 (2003) 559-569
62. Kanaoka Y., Ago H., Inagaki E., Nanayama T., Miyano M., Kikuno R., Fujii Y., Eguchi N., Toh H., Urade Y., and Hayaishi O. Cloning and crystal structure of hematopoietic prostglandin D synthase. Cell 90 (1997) 1085-1095
63. Kanaoka Y., Maekawa A., Penrose J.F., Austen K.F., and Lam B.K. Attenuated zymosan-induced peritoneal vascular permeability and IgE-dependent passive cutaneous anaphylaxis in mice lacking leukotriene C4 synthase. J. Biol. Chem. 276 (2001) 22608-22613
64. Karavangeli M., Labrou N.E., Clonis Y.D., and Tsaftaris A. Development of transgenic tobacco plants overexpressing maize glutathione S-transferase I for chloroacetanilide herbicides phytoremediation. Biomol. Eng. 22 (2005) 121-128
65. Labrou N.E., Ridgen D.J., and Clonis Y.D. Engineering the pH-dependence of kinetic parameters of maize glutathione S-transferase I by site-directed mutagenesis. Biomol. Eng. 21 (2004) 61-66
66. Labrou N.E., Karavangeli M., Tsaftaris A., and Clonis Y.D. Kinetic analysis of maize glutathione S-transferase I catalyzing the detoxification from chloroacetanilide herbicides. Planta 222 (2005) 91-97
67. Ladner J.E., Parson J.F., Rife C.L., Gilliland G.L., and Armstrong R.N. Parallel evolutionary pathways for glutathione transferases: structure and mechanisms of the mitochondrial class Kappa enzyme rGSTK1-1. Biochemistry 43 (2004) 352-361
68. Lam B.K., Penrose J.F., Xu K., Baldasaro M.H., and Austen K.F. Site-directed mutagenesis of human leukotriene C4 synthase. J. Biol. Chem. 272 (1997) 13923-13928
69. Larsson A.-K., Emerén L.O., Bardsley W.G., and Mannervik B. Directed enzyme evolution guided by multidimensional analysis of substrate-activity space. Protein Eng. Des. Select. 17 (2004) 49-55
70. Lengqvist J., Svensson R., Evergren E., Morgenstern R., and Griffith W. Observation of an intact noncovalent homotrimer of detergent-solubilized rat microsomal glutathione transferase-1 by electrospray mass spectrometry. J. Biol. Chem. 279 (2004) 13311-13316
71. Li J., Xia Z., and Ding J. Thioredoxin-like domain of human κ class glutathione transferase reveals sequence homology and structure similarity to the θ class enzyme. Protein Sci. 14 (2005) 2361-2369
72. Light G.G., Mahan J.R., Roxas V.P., and Allen R.D. Transgenic cotton (Gossypium hirsutum L.) seedlings expressing a tobacco glutathione S-transferase fail to provide improved stress tolerance. Planta 222 (2005) 346-354
73. Lim C.E.L., Matthaei K.I., Blackburn A.C., Davis R.P., Dahlstrom J.E., Koina M.E., Anders M.W., and Board P.G. Mice deficient in glutathione transferase Zeta/Maleylacetoacetate isomerase exhibit a range of pathological changes and elevated expression of Alpha, Mu, and Pi class glutathione transferases. Am. J. Pathol. 165 (2004) 679-693
74. Lin X., Kaul S., Rounsley S., Shea T.P., Benito M.I., Town C.D., Fujii C.Y., Mason T., Bowman C.L., Barnstead M., Feldblyum T.V., Buell C.R., Ketchum K.A., Lee J., Ronning C.M., Koo H.L., Moffat K.S., Cronin L.A., Shen M., Pai G., Van Aken S., Umayam L., Tallon L.J., Gill J.E., Adams M.D., Carrera A.J., Creasy T.H., Goodman H.M., Somerville C.R., Copenhaver G.P., Preuss D., Nierman W.C., White O., Eisen J.A., Salzberg S.L., Fraser C.M., and Venter J.C. Sequence and analysis of chromosome 2 of the plant Arabidopsis thaliana. Nature 402 (1999) 761-768
75. Listowsky I. High capacity binding by glutathione S-transferases and glucocorticoid resistance. In: Tew K.D., Pickett C.B., Mantle T.J., Mannervik B., and Hayes J.D. (Eds). Structure and Function of Glutathione Transferases (1993), CRC Press, Boca Raton, FL 199-209
76. Loyall L., Uchida K., Brown S., Furuya M., and Frohnmeyer H. Glutathione and a UV-light induced glutathione S-transferase are involved in signalling to chalcone synthase in cell cultures. Plant Cell 12 (2000) 1939-1950
77. Mandal A.K., Skoch J., Bacskai B.J., Hyman B.T., Christmas P., Miller D., Yamin T.-D., Xu S., Wisniewski D., Evans J.F., and Soberman R.J. The membrane organization of leukotriene synthesis. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 6587-6592
78. Marrs K.A. The functions and regulation of plant glutathione S-transferases. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47 (1996) 127-158
79. Martin J.L. Thioredoxin-a fold for all reasons. Structure 3 (1995) 245-250
80. Martin J.L., Bardwell J.C.A., and Kuriyan J. Crystal structure of the DsbA protein required for disulfide bond formation in vivo. Nature 365 (1993) 464-468
81. McGonigle B., Keeler S.J., Lau S.-M.C., Koeppe M.K., and O'Keefe D.P. A genomics approach to the comprehensive analysis of the glutathione S-transferase gene family in soybean and maize. Plant Physiol. 124 (2000) 1105-1120
82. Milligan A.S., Daly A., Parry M.A.J., Lazzeri P.A., and Jepson I. The expression of a maize glutathione S-transferase gene in transgenic wheat confers tolerance, both in planta and in vitro. Mol. Breed. 7 (2001) 301-315
83. Morel F., Rauch C., Coles B., Le Ferrac E., and Guillouzo A. The human glutathione transferase alpha locus: genomic organisation of gene cluster and functional characterisation of the genetic polymorphysm in the hGSTA1 promoter. Pharmacogenetics 12 (2002) 277-286
84. Morel F., Rauch C., Petit E., Piton A., Theret N., Coles B., and Guillouzo A. Gene and protein characterization of the human glutathione S-transferase Kappa and evidence for peroxisomal localization. J. Biol. Chem. 279 (2004) 16246-16253
85. Morgenstern R., and DePierre J. Microsomal glutathione transferase: purification in unactivated form and further characterization of the activation process, substrate specificity and aminoacid composition. Eur. J. Biochem. 134 (1983) 591-597
86. Morgenstern R., Guthenberg C., and DePierre J.W. Microsomal S-transferase purification, initial characterization and demonstration that it is not identical to the cytosolic glutathione S-transferases A, B and C. Eur. J Biochem. 128 (1982) 243-248
87. Mosialou E., Piemonte F., Andersson C., Vos R.I., van Bladeren P.J., and Morgenstern R. Microsomal glutathione transferase: lipid-derived substrates and lipid dependence. Arch. Biochem. Biophys. 320 (1995) 210-216
88. Mueller L.A., Godman C.D., Silady R.A., and Walbot V. AN9, a petunia glutathione S-transferase required for anthocyanin sequestration, is a flavonoid binding protein. Plant Physiol. 123 (2000) 1561-1570
89. Nagano N., Orengo C.A., and Thornton J.M. One fold with many functions: the evolutionary relationships between TIM barrel families based on their sequences, structures and functions. J. Mol. Biol. 321 (2002) 741-765
90. Nilsson L.O., Gustafsson A., and Mannervik B. Redesign of substrate-selectivity determining modules of glutathione transferase A1-1 installs high catalytic efficiency with toxic alkenal products of lipid peroxidation. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 9408-9412
91. Pemble S.E., and Taylor J.B. An evolutionary perspective on glutathione transferases inferred from class-Theta glutathione transferase cDNA sequences. Biochem. J. 287 (1992) 957-963
92. Pemble S.E., Wardle A.F., and Taylor J.B. Glutathione S-transferase class Kappa characterization by the cloning of rat mitochondrial GST and identification of a human homologue. Biochem. J. 319 (1996) 749-754
93. Pettersson P.L., Johansson A.-S., and Mannervik B. Transmutation of human glutathione transferase A2-2 with peroxidase activity into an efficient steroid isomerase. J. Biol. Chem. 277 (2002) 30019-30022
94. Pflugmacher S., Sandermann Jr. H., and Schroeder P. Taxonomic distribution of plant glutathione S-transferases acting on xenobiotics. Phytochemistry 54 (2000) 267-273
95. Polyak K., Xia Y., Zweier J.L., Kinzler K.W., and Vogelstein B. A model for p53-induced apoptosis. Nature 389 (1997) 300-305
96. Prabhu K.S., Reddy P.V., Gumpricht E., Hildenbrandt G.R., Scholz R.W., Sordillo L.M., and Reddy C.C. Microsomal glutathione S-transferase A1-1 with glutathione peroxidase activity from sheep liver: molecular cloning, expression and characterization. Biochem. J. 360 (2001) 345-354
97. Prabhu K.S., Reddy P.V., Jones E.C., Liken A.D., and Reddy C.C. Characterization of a class alpha glutathione-S-transferase with glutathione peroxidase activity in human liver microsomes. Arch. Biochem. Biophys. 424 (2004) 72-80
98. Ranson H., Collin F., and Hemingway J. The role of alternative mRNA splicing in generating heterogeneity within the Anopheles gambiae class I glutathione S-transferase family. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 14284-14289
99. Raza H., Robin M.A., Fang J.K., and Avadhani N.G. Multiple isoforms of mitochondrial glutathione S-transferases and their differential induction under oxidative stress. Biochem. J. 366 (2002) 45-55
100. Robinson A., Huttley G.A., Booth H.S., and Board P.G. Modelling and bioinformatics studies of the human Kappa-class glutathione transferase predict a novel third glutathione transferase family with similarità to prokaryotic 2-hydroxychromene-2-carboxylate isomerases. Biochem. J. 379 (2004) 541-552
101. Roxas V.P., Smith Jr. R.K., Allen E.R., and Allen R.D. Overexpression of glutathione S-transferase/glutathione peroxidase enhances the growth of transgenic tobacco seedlings during stress. Nat. Biotechnol. 15 (1997) 988-991
102. Roxas V.P., Lodhi S.A., Garrett D.K., Mahan J.R., and Allen R.D. Stress tolerance in transgenic tobacco seedlings that overexpress glutathione S-transferase/glutathione peroxidase. Plant Cell Physiol. 41 (2000) 1229-1234
103. Rugh C.L., Senecoff J.F., Meagher R.B., and Merkle S.A. Development of transgenic yellow poplar for mercury phytoremediation. Nat. Biotechnol. 16 (1998) 925-928
104. Rui L., Kwon Y.M., Reardon K.F., and Wood T.K. Metabolic pathway engineering to enhance aerobic degradation of chlorinated ethenes and to reduce their toxicity by cloning a novel glutathione S-transferase, an evolved toluene o-monooxigenase, and γ-glutamylcysteine synthetase. Environ. Microbiol. 6 (2004) 491-500
105. Sappl P.G., Onate-Sanchez L., Singh K.B., and Millar A.H. Proteomic analysis of glutathione S-transferases of Arabidopsis thaliana reveals differential salicilic acid-induced expression of the plant-specific phi and tau classes. Plant Mol. Biol. 54 (2004) 205-219
106. Satoh K., Nagano Y., Shimomura C., Suzuki N., Saeki Y., and Yokota H. Expression of prostglandin E synthase mRNA is induced in β-amyloid treated rat astrocytes. Neurosci. Lett. 283 (2000) 221-223
107. Sayed Y., Wallace L.A., and Dirr H.W. The hydrophobic lock-and-key intersubunit motif of glutathione transferase A1-1: implications for catalysis, ligandin function and stability. FEBS Lett. 465 (2000) 169-172
108. Schmidt-Krey I., Mitsuoka K., Hirai T., Murata K., Cheng Y., Fujiyoshi Y., Morgenstern R., and Hebert H. The three-dimensional map of microsomal glutathione transferase 1 at 6 Å resolution. EMBO J. 19 (2000) 6311-6316
109. Schmidt-Krey I., Kanaoka Y., Mills D.J., Irikura D., Haase W., Lam B.K., Austen K.F., and Kuhlbrandt W. Human leukotriene C4 synthase at 4.5 Å resolution in projection. Structure 12 (2004) 2009-2014
110. 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
111. Smith A.P., DeRidder B.P., Guo W.-J., Seeley E.H., Regnier F.E., and Goldsbrough P.B. Proteomic analysis of Arabidopsis glutathione S-transferases from benoxacor- and copper-treated seedlings. J. Biol. Chem. 279 (2004) 26098-26104
112. Smith A.P., Nourizadeh S.D., Peer W.A., Xu J., Bandyopadhyay A., Murphy A.S., and Goldsbrough P.B. Arabidopsis AtGSTF2 is regulated by ethylene and auxin, and encodes a glutathione S-transferase that interacts with flavonoids. Plant J. 36 (2003) 433-442
113. Smith W.L., DeWitt D.L., and Garavito R.M. Cyclooxygenases: structural, cellular and molecular biology. Annu. Rev. Biochem. 69 (2000) 145-182
114. Soranzo N., Sari Gorla M., Mizzi L., De Toma G., and Frova C. Organisation and structural evolution of the rice glutathione S-transferase gene family. Mol. Gen. Genomics 271 (2004) 511-521
115. Stenberg G., Abdalla A.-M., and Mannervik B. Tyrosine 50 at the subunit interface of dimer human glutathione transferase P1-1 is a structural key residue for modulating protein stability and catalytic function. BBRC 271 (2000) 59-63
116. Summers A.O., and Lewis E. Volatilization ofmercuric chloride by mercury-resistant plasmid-bearing strains of Escherichia coli, Staphylococcus aureus, and Pseudomonas aeroginosa. J. Bacteriol. 113 (1973) 1070-1072
117. Sun T.H., and Morgenstern R. Binding of glutathione and an inhibitor to microsomal glutathione transferase. Biochem. J. 326 (1997) 193-196
118. Svartz J., Blomgran R., Hammarstrom S., and Soderstrom M. Leukotriene C4 synthase homo-oligomers detected in living cells by bioluminescence resonance energy transfer. BBA 1633 (2003) 90-95
119. Tan K.L., Chelvanayagam G., Parker M.W., and Board P.G. Mutagenesis of the active site of the human Theta-class glutathione transferase GSTT2-2: catalysis with different substrates involves different residues. Biochem. J. 319 (1996) 315-321
120. Thom R., Dixon D.P., Edwards R., Cole D.J., and Lapthorn A.J. The structure of a Zeta class glutathione S-transferase from Arabidopsis thaliana: characterisation of a GST with novel active-site architecture and a putative role in tyrosine catabolism. J. Mol. Biol. 308 (2001) 949-962
121. Thom R., Cummins I., Dixon D.P., Edwards R., Cole D.J., and Lapthorn A.J. Structure of a Tau class glutathione S-transferase from wheat active in herbicide detoxification. Biochemistry 41 (2002) 7008-7020
122. Thorén S., Weinander R., Saha S., Jegerschold C., Pettersson P.L., Samuelsson B., Hebert H., Hamberg M., Morgenstern R., and Jakobsson P.-J. Human microsomal prostglandin E synthase-1. J. Biol. Chem. 278 (2003) 22199-22209
123. Toba G., and Aigaki T. Disruption of the microsomal glutathione S-transferase-like gene reduces life span of Drosophila melanogaster. Gene 253 (2000) 179-187
124. Tobin M.B., Gustafsson C., and Huisman G.W. Directed evolution: the "rational" basis for "irrational" design. Curr. Opin. Struct. Biol. 10 (2000) 421-427
125. Tomarev S.I., Zinovieva R.D., Guo K., and Piatigorsky J. Squid glutathione S-transferase. J. Biol. Chem. 268 (1993) 4534-4542
126. Toung Y.P., Hsieh T.S., and Tu C.P. The glutathione S-transferase D genes. A divergently organized, intronless gene family in Drosophila melanogaster. J. Biol. Chem. 268 (1993) 9737-9746
127. Trebino C.E., Stock J.L., Gibbons C.P., Naiman B.M., Wachtmann T.S., Umland J.P., Pandher K., Lapointe J.-M., Saha S., Roach M.L., Carter D., Thomas N.A., Durtschi B.A., McNeish J.D., Hambor J.E., Jakobsson P.-J., Carty T.J., Perez J.R., and Audoly L.P. Impaired inflammatory and pain responses in mice lacking an inducible prostglandin E synthase. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 9044-9049
128. 4 synthase activity from the rat brain. Eur. J. Biochem. 170 (1987) 159-164
129. Urade Y., Eguchi N., Aritake K., and Hayaishi O. Functional analyses of lipocalin-type and hematopoietic prostaglandin synthases. Folia Pharmacol. Jpn. 123 (2004) 5-13
130. Urano J., Nakagawa T., Maki Y., Masumara T., Tanaka K., Murata N., and Ushimaru T. Molecular cloning and characterization of a rice dehydroascorbate reductase. FEBS Lett. 466 (2000) 107-111
131. Vuilleumier S. Bacterial glutathione S-transferases: what are they good for?. J. Bacteriol. 179 (1997) 1431-1441
132. Vuilleumier S., and Pagni M. The elusive roles of bacterial glutathione S-transferases: new lessons from genomes. Appl. Microbiol. Biotechnol. 58 (2002) 138-146
133. Wagner U., Edwards R., Dixon D.P., and Mauch F. Probing the diversity of the Arabidopsis glutathione S-transferase gene family. Plant Mol. Biol. 49 (2002) 515-532
134. Xia B., Vlamis-Gardikas A., Holmgren A., Wright P.E., and Dyson H.J. Solution structure of Escherichia coli glutaredoxin-2 shows similarity to mammalian glutathione S-transferases. J. Mol. Biol. 310 (2001) 907-918
135. Yu H.-J., Liu J.-Q., Bock A., Li J., Luo G.-M., and Shen J.-C. Engineering glutathione transferase to a novel glutathione peroxidase mimic with high catalytic efficiency. J. Biol. Chem. 280 (2005) 11930-11935