Glutathione transferases from parasites: A biochemical view

Acta Tropica

Volumn 105, Issue 2, 2008, Pages 99-112

  Torres Rivera, Anayetzin ^a   Landa, Abraham ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Crystals; Drug design; GST; Kinetics; Parasites; Substrate specificity

Indexed keywords

GLUTATHIONE TRANSFERASE;

BIOCHEMISTRY; CATALYSIS; CRYSTAL; DETOXIFICATION; DRUG; ENZYME ACTIVITY; INHIBITOR; MAMMAL; PARASITE; REACTION KINETICS;

BIOCHEMISTRY; CATALYSIS; CESTODE; CLONORCHIS SINENSIS; CYTOSOL; ECHINOCOCCUS MULTILOCULARIS; ENZYME ACTIVITY; ENZYME SPECIFICITY; FASCIOLA HEPATICA; HAEMONCHUS CONTORTUS; HELMINTH; ISOELECTRIC POINT; MAMMAL; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; ONCHOCERCA VOLVULUS; PARAGONIMUS WESTERMANI; PARASITE; PLASMODIUM FALCIPARUM; PLASMODIUM VIVAX; PLASMODIUM YOELII; PROTOZOON; REVIEW; SCHISTOCEPHALUS SOLIDUS; SCHISTOSOMA JAPONICUM; SCHISTOSOMA MANSONI; TAENIA SOLIUM; TREMATODE; TRYPANOSOMA CRUZI;

AMINO ACID SEQUENCE; ANIMALS; CATALYSIS; DRUG DESIGN; ENZYME INHIBITORS; GLUTATHIONE TRANSFERASE; KINETICS; MOLECULAR SEQUENCE DATA; PARASITES; SUBSTRATE SPECIFICITY;

MAMMALIA;

EID: 38349159585     PISSN: 0001706X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.actatropica.2007.08.005     Document Type: Review

References (89)

1. Agosin M., Naquira C., Capdevila J., and Pulin J. Hemoproteins in Trypanosoma cruzi with emphasis on microsomal pigments. Int. J. Biochem. 7 (1976) 585-593
2. Ahmad R., and Srivastava A.K. Purification and biochemical characterization of cytosolic glutathione-S-transferase from malarial parasites Plasmodium yoelii. Parasitol. Res. 100 (2007) 581-588
3. Alin P., Danielson U.H., and Mannervik B. 4-Hydroxyalk-2-enals are substrates for glutathione transferase. FEBS Lett. 179 (1985) 267-270
4. Andersson C., Piemonte F., Mosialou E., Weinander R., Sun T., Lundqvist G., Adang A., and Morgenstern R. Kinetic studies on rat liver microsomal glutathione transferase: consequences of activation. Biochem. Biophys. Acta 1247 (1995) 277-283
5. Armstrong R.N. Glutathione S-transferases: structure and mechanism of an archetypical detoxification enzyme. Adv. Enzymol. 69 (1994) 1-44
6. Armstrong R.N. Structure, catalytic mechanism, and evolution of the glutathione S-transferases. Chem. Res. Toxicol. 10 (1997) 2-18
7. Baiocco P., Gourlay L.J., Angelucci F., Fontaine J., Hervé M., Miele A.E., Trottein F., Brunori M., and Bellelli A. Probing the mechanism of GSH activation in Schistosoma haematobium glutathione-S-transferase by site-directed mutagenesis and X-ray crystallography. J. Mol. Biol. 360 (2006) 678-689
8. Barnes M.M., James S.P., and Wood P.B. Formation of mercapturic acid and the levels of glutathione in tissues. Biochem J. 71 (1959) 680-690
9. Barrett J. Cytochrome P450 in parasitic protozoa and helminths. Comp. Biochem. Physiol. Part C 121 (1998) 181-183
10. Bennett J.L., Day T., Feng-Tao L., Ismail M., and Farghaly A. The Development of resistance to anthelmintics: a perspective with an emphasis on the antischistosomal drug praziquantel. Exp. Parasitol. 87 (1997) 260-267
11. 2+ release channels. Int. J. Biochem. Cell Biol. 36 (2004) 1599-1612
12. Booth J., Boyland E., and Sims P. An enzyme from rat liver catalysing conjugations with glutathione. Biochem. J. 79 (1961) 516-524
13. Brophy P.M., and Barrett J. Glutathione transferases in helminths. Parasitology 100 (1990) 345-349
14. Brophy P.M., Ben-Smith A., Brown A., Behnke J.M., and Pritchard D.I. Glutathione S-transferase from the gastrointestinal nematode Heligmosomoides polygyrus and mammalian liver compared. Comp. Biochem. Physiol. 109 (1994) 585-592
15. Brophy P.M., Crowley P., and Barrett J. Detoxification reactions of Fasciola hepatica cytosolic glutathione transferases. Mol. Biochem. Parasitol. 39 (1990) 155-162
16. Brophy P.M., Papadopoulos A., Touraki M., Coles B., Körting W., and Barrett J. Purification of cytosolic glutathione transferases from Schistocephalus solidus (plerocercoid): interaction with anthelmintics and products of lipid peroxidation. Mol. Biochem. Parasitol. 36 (1989) 187-196
17. Brophy P.M., and Pritchard D.I. Parasitic helminth glutathione S-transferase: an update on their potential as targets for immuno and chemotherapy. Exp. Parasitol. 79 (1994) 89-99
18. Brophy P.M., Southan C., and Barrett J. Glutathione transferases in the tapeworm Moniezia expansa. Biochem. J. 262 (1989) 939-946
19. Burmeister C., Perbandt M., Betzel C., Walter R.D., and Liebau E. Crystallization and preliminary X-ray diffraction studies of the glutathione S-transferase from Plasmodium falciparum. Acta Crystallogr. D Biol. Crystallogr. 59 (2003) 1469-1471
20. Byoung-Kuk N., Jung-Mi K., Tong-Sook K., and Woon-Mok S. Plasmodium vivax: molecular cloning, expression and characterization of glutathione S-transferase. Exp. Parasitol. 116 (2007) 414-418
21. Capron A., Riveau G., Capron M., and Trottein F. Schistosomes: the road from host-parasite interactions to vaccines in clinical trials. Trends Parasitol. 21 (2005) 143-149
22. Chemale G., Morphew R., Moxon J.V., Morassuti A.L., LaCourse E.J., Barrett J., Johnston D.A., and Brophy P.M. Proteomic analysis of glutathione transferases from the liver fluke parasite Fasciola hepatica. Proteomics 6 (2006) 6263-6273
23. 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
24. Clark A. The comparative enzymology of the glutathione S-transferase from non-vertebrate organism. Comp. Biochem. Physiol. 92 (1989) 419-446
25. Coles B., and Kadlubar F. Human alpha class glutathione S-transferases: genetic polymorphism, expression, and susceptibility to disease. Met. Enzymol. 401 (2005) 9-42
26. Danielson H.U., and Mannervik B. Kinetic independence of the subunits of cytosolic glutathione transferase from the rat. Biochem. J. 231 (1985) 263-267
27. de Groot M., Vermeulen N., Mullenders D., and Donné-Op den Kelder G. A homology model for rat mu class glutathione S-transferase 4-4. Chem. Res. Toxicol. 9 (1996) 28-40
28. Deponte M., and Becker K. Glutathione S-transferase from malarial parasites: structural and functional aspects. Met. Enzymol. 401 (2005) 241-253
29. Dierickx P.J. Anionic and neutral glutathione S-transferase isoenzymes in the freshwater worm Tubifex tubifex (O.F.M.). Arch. Int. Physiol. Biochim. 93 (1985) 193-198
30. Docampo R. Antioxidant mechanisms. In: Marr J., and Muller M. (Eds). Biochemistry and Molecular Biology of Parasites (1995), Academic Press, San Diego 147-157
31. Eaton D.L., and Bammler T.K. Concise review of the glutathione S-transferases and their significance to toxicology. Toxicol. Sci. 49 (1999) 156-164
32. Ferreira I.D., Nogueira F., Borges S.T., do Rosário V.E., and Cravo P. Is the expression of genes encoding enzymes of glutathione (GSH) metabolism involved in chloroquine resistance in Plasmodium chabaudi parasites?. Mol. Biochem. Parasitol. 136 (2004) 43-50
33. Frova C. Glutathione transferases in the genomics era: new insights and perspectives. Biomol. Eng. 23 (2006) 149-169
34. Geerts S., and Gryseels B. Drug resistance in human helminths: current situation and lessons from livestock. Clin. Microbiol. Rev. 13 (2000) 207-222
35. Girardini J., Amirante A., Zemzoumi K., and Serra E. Characterization of an omega-class glutathione S-transferase from Schistosoma mansoni with glutaredoxin-like dehydroascorbate reductase and thiol transferase activities. Eur. J. Biochem. 269 (2002) 5512-5521
36. Gupta S., Singh A., Yadav M., Singh K., and Rathaur S. MALDI mass sequencing and characterization of filarial glutathione-S-transferase. Biochem. Biophys. Res. Commun. 356 (2007) 381-385
37. Habig W.H., and Jacoby W.B. Assays for differentiation of glutathione S-transferases. Met. Enzymol. 77 (1981) 398-405
38. Hagan P., Appleton C.C., Coles G.C., Kusel J., and Tchuem-Tchuente L.A. Schistosomiasis control: keep taking the tablets. Trends Parasitol. 20 (2004) 92-97
39. Hayes J.D., Flanagan J.U., and Jowsey I.R. Glutathione transferases. Annu. Rev. Pharmacol. Toxicol. 45 (2005) 51-88
40. Herve M. Pivotal roles of the parasite PGD2 synthase and of the host D prostanoid receptor 1 in schistosome immune evasion. Eur. J. Immunol. 33 (2003) 2764-2772
41. Hong S., Kang S., Chung Y., Chung M., Oh Y., Kang I., Bahk Y.Y., Kong Y., and Cho S. Paragonimus westermani: a cytosolic glutathione S-transferase of a σ-class in adult stage. Exp. Parasitol. 94 (2000) 180-189
42. Hong S., Lee J., Lee D., Sohn W., and Cho S. Molecular cloning and characterization of a mu-class glutathione S-transferase from Clonorchis sinensis. Mol. Biochem. Parasitol. 115 (2001) 69-75
43. Ishikawa T. The ATP-dependent glutathione S-conjugate export pump. Trends Biochem. Sci. 17 (1992) 463-468
44. Ishikawa T., Li Z.S., Lu P.Y., and Rea P.A. The GS-X pump in plant, yeast, and animal cells: structure, function, and gene expression. Biosci. Rep. 17 (1997) 189-207
45. Ismail M., Botros S., Metwally A., William S., Farghally A., Feng-Tao L., Day T.A., and Bennett J.L. Resistance to praziquantel: direct evidence from Schistosoma mansoni isolated from Egyptian villagers. Am. J. Trop. Med. Hyg. 60 (1999) 932-935
46. Jaffe J., and Lambert R.A. Glutathione S-transferase in adult Dirofilaria immitis and Brugia pahangi. Mol. Biochem. Parasitol. 20 (1986) 199-206
47. Jakobson I., Askelof P., Warholm M., and Mannervik B. A steady-state-kinetic random mechanism for glutathione S-transferase A from rat liver. A model involving kinetically significant enzyme-product complexes in the forward reaction. Eur. J. Biochem. 77 (1977) 253-262
48. 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
49. Jao S.C., Chen J., Yang K., and Li W.S. Design of potent inhibitors for Schistosoma japonica glutathione S-transferase. Bioorg. Med. Chem. 14 (2006) 304-318
50. Kawalek J.C., Rew R.S., and Haevner J. Glutathione S-transferase, a possible drug metabolism enzyme in Haemonchus contortus: comparative activity of a cambendazole resistant and a susceptible strain. Int. J. Parasitol. 14 (1984) 173-177
51. Kang S., Ahn I., Park C., Chung Y., Hong S., Kong Y., Cho S., and Hong S. Clonorchis sinensis: molecular cloning and characterization of 28-kDa glutathione S-transferase. Exp. Parasitol. 97 (2001) 186-195
52. Ketterer B. Detoxication reactions of glutathione and glutathione transferases. Xenobiotica 16 (1986) 957-973
53. Lawrence R.A., and Burk R.F. Glutathione peroxidase activity in selenium-deficient rat liver. Biochem. Biophys. Res. Commun. 71 (1976) 952-958
54. Liebau E., Bergmann B., Campbell A.M., Teesdale-Spittle P., Brophy P.M., Lüersen K., and Walter R.D. The glutathione S-transferase from Plasmodium falciparum. Mol. Biochem. Parasitol. 124 (2002) 85-90
55. Liebau E., De Maria F., Burmeister C., Perbandt M., Turella P., Antonini G., Federici G., Giansanti F., Stella L., Lo Bello M., Caccuri A.M., and Ricci G. Cooperativity and pseudo-cooperativity in the glutathione S-transferase from Plasmodium falciparum. J. Biol. Chem. 280 (2005) 26121-26128
56. Liebau E., Eckelt V.H.O., Wildenburg, Teesdale-Spittle P., Brophy P.M., Walter R.D., and Henkle-Dürsen K. Structural and funtional analysis of a glutathione S-transferase form Ascaris suum. Biochem. J. 324 (1997) 659-666
57. Liebau E., Müller V., Lucius R., Walter R.D., and Henkle-Dürsen K. Molecular cloning, expression and characterization of a recombinant glutathione S-transferase from Echinococcus multilocularis. Mol. Biochem. Parasitol. 77 (1996) 49-56
58. Liebau E., Wildenburg G., Brophy P.M., Walter R.D., and Henkle-Dürsen K. Biochemical analysis, gene structure and localization of the 24 kDa glutathione S-transferase from Onchocerca volvulus. Mol. Biochem. Parasitol. 80 (1996) 27-39
59. Mannervik B. The isoenzymes of glutathione transferase. Adv. Enzymol. 57 (1985) 357-417
60. McTigue M., Williams D.R., and Tainer J.A. Crystal structures of a schistosomal drug and vaccine target: glutathione S-transferase from Schistosoma japonicum and its complex with the leading antischistosomal drug praziquantel. J. Mol. Biol. 246 (1995) 21-27
61. Moutiez M., Aumercier M., Schöneck R., Meziane-Cherif D., Lucas V., Aumercier P., Ouaissi A., Sergheraert C., and Tartar A. Purification and characterization of a trypanothione-glutathione thioltransferase from Trypanosoma cruzi. Biochem. J. 310 (1995) 433-437
62. Nare B., Smith J.M., and Prichard R.K. Differential effects of oltipraz and its oxy-analogue on the viability of Schistosoma mansoni and the activity of glutathione S-transferase. Biochem. Pharmacol. 42 (1991) 1287-1292
63. Nathan S.T., Mathew N., Kalyanasundaram M., and Balaraman K. Structure of glutathione S-transferase of the filarial parasite Wuchereria bancrofti: a target for drug development against adult worm. J. Mol. Model. 11 (2005) 194-199
64. Oakley A.J. Glutathione transferases: new functions. Curr. Opin. Struct. Biol. 15 (2005) 1-8
65. O'Leary K., Hathaway K.M., and Tracy J.W. Schistosoma mansoni: single-step purification and characterization of glutathione S-transferase isoenzyme 4. Exp. Parasitol. 75 (1992) 47-55
66. Plancarte A., Rendon J.L., and Landa A. Purification, characterization and kinetic properties of the Taenia solium glutathione S -transferase isoform 26.5 kDa. Parasitol. Res. 93 (2004) 137-144
67. Pemberton K.D., and Barrett J. The detoxification of xenobiotic compounds by Onchocerca gutturosa (Nematoda: Filarioidea). Int. J. Parasitol. 19 (1989) 875-878
68. Perbandt M., Höppner J., Betzel C., Walter R.D., and Liebau E. Structure of the major cytosolic glutathione S-transferase from the parasitic nematode Onchocerca volvulus. J. Biol. Chem. 280 (2005) 12630-12636
69. Precious W., and Barret J. The possible absence of cytochrome P-450 linked xenobiotic metabolism in helminths. Biochem. Biophys. Acta 992 (1989) 215-222
70. Raffalli-Mathieu F., and Mannervik B. Human glutathione transferase A3-3 active as steroid double-bond isomerase. Met. Enzymol. 401 (2005) 265-278
71. Rao K.V.N., He Y., and Kalyanasundaram R. Expression of a 28-kilodalton glutathione S-transferase antigen of Schistosoma mansoni on the surface of filamentous phages and evaluation of its vaccine potential. Clin. Diagn. Lab. Immunol. 10 (2003) 536-541
72. Rathaur S., Fisher P., Domagalski M., Walter R.D., and Liebau E. Brugia malayi and Wucheria bancrofti: gene comparison and recombinant expression of π-class related glutathione S-transferase. Exp. Parasitol. 103 (2003) 177-181
73. Ricci G., Turella P., De Maria F., Antonini G., Nardocci L., Board P.G., Parker M.W., Carbonelli M.G., Federici G., and Caccuria A.M. Binding and kinetic mechanisms of the zeta class glutathione transferase. J. Biol. Chem. 279 (2004) 33336-33342
74. Rossjohn J., Feil S.C., Wilce M.C.J., Sexton J.L., Spithill T.W., and Parker M.W. Crystallization, structural determination and analysis of a novel parasite vaccine candidate: Fasciola hepatica glutathione S-transferase. J. Mol. Biol. 273 (1997) 857-872
75. Salinas G., Braun G., and Taylor D.W. Molecular characterisation and localisation of an Onchocerca volvulus π-class glutathione S-transferase. Mol. Biochem. Parasitol. 66 (1994) 1-9
76. Salvatore L., Wijffels G., Sexton J., Panaccio M., Mailer S., McCauley I., and Spithill T. Biochemical analysis of recombinant glutathione S-transferase of Fasciola hepatica. Mol. Biochem. Parasitol. 69 (1995) 281-288
77. Sheehan D., Meade G., Foley V.M., and Dowd C.A. Structure, function and evolution of glutathione transferases: implications for classifications of non-mammalians members of an ancient enzyme superfamily. Biochem J. 360 (2001) 1-16
78. Tracy J.W., and Vande Waa E.A. Xenobiotic metabolism. In: Marr J., and Muller M. (Eds). Biochemistry and Molecular Biology of Parasites (1995), Academic Press, San Diego 161-173
79. Trottein F., Vaney M.C., Bachet B., Pierce R.J., Colloch N., Lecocq J.P., Capron A., and Mornon J.P. Crystallization and preliminary X-ray diffraction studies of a protective cloned 28 kDa glutathione S-transferase from Schistosoma mansoni. J. Mol. Biol. 224 (1992) 515-518
80. Tsuchida S., Izumi T., Shimizu T., Ishikawa T., Hatayama I., Satoh K., and Sato K. Purification of a new acidic glutathione S-transferase, GSTYn1Yn1, with a high leukotriene-C4 synthase activity from the rat brain. Eur. J. Biochem. 170 (1987) 159-164
81. van Bladeren P.J. Glutathione conjugation as a bioactivation reaction. Chem. Biol. Interact. 129 (2000) 61-76
82. van Rossum A.J., Brophy P.M., Tait A., Barrett J., and Jefferies J.R. Proteomic identification of glutathione S-transferases from the model nematode Caenorhabditis elegans. Proteomics 1 (2001) 1463-1468
83. van Rossum A.J., Jefferies J.R., Rijsewijk A.M., LaCourse E.J., Teesdale-Spittle P., Barret J., Tait A., and Brophy P.M. Binding of hematin by a new class of glutathione transferase from the blood-feeding parasitic nematode Haemonchus contortus. Infect. Immun. 72 (2004) 2780-2790
84. Vibanco-Pérez N., Jiménez L., Mendoza-Hernández G., and Landa A. Characterization of a recombinant mu-class glutathione S-transferase from Taenia solium. Parasitol. Res. 88 (2002) 398-404
85. Vibanco-Pérez N., and Landa A. Glutathione S-transferase in helminth parasites. Rev. Lat. Microbiol. 40 (1998) 73-85
86. Walker J., Crowley P., Moreman A., and Barret J. Biochemical properties of cloned glutathione S-transferase from Schistosoma mansoni and Schistosoma japonicum. Mol. Biochem. Parasitol. 61 (1993) 255-264
87. Wilce M., and Parker M. Structure and function of glutathione S-transferases. Biochem. Biophys. Acta 1205 (1994) 1-18
88. Wu Z., Hu X., Wu D., Xu J., Chen S., Wu Z., and Yu X. Clonorchis sinensis: molecular cloning and functional expression of a novel cytosolic glutathione transferase. Parasitol. Res. 100 (2007) 227-232
89. Zhan B., Liu S., Perally S., Xue J., Fujiwara R., Brophy P.M., Xiao S., Liu Y., Feng J., Williamson A., Wang Y., Bueno L.L., Mendez S., Goud G., Bethony J.M., Hawdon J.M., Loukas A., Jones K., and Hotez P.J. Biochemical characterization and vaccine potential of a heme-binding glutathione transferase from the adult hookworm Ancylostoma caninum. Infect. Immun. 73 (2005) 6903-6911