Xenobiotic metabolizing enzymes and metabolism of anthelminthics in helminths

References

• Abo-Dalo, B., Ndjonka, D., Pinnen, F., Liebau, E., Luersen, K. (2004). A novel member of the GCN5-related N-acetyltransferase superfamily from Caenorhabditis elegans preferentially catalyses the N-acetylation of thialysine [S-(2-aminoethyl)-L-cysteine]. Biochem J 384:129–137.
   PubMed Web of Science ®Google Scholar
• Adcock, H. J., Brophy, P. M., Teesdale-Spittle, P. H., Buckberry, L. D. (1999). Cysteine conjugate beta-lyase activity in three species of parasitic helminth. Int J Parasitol 29:543–548.
   PubMed Web of Science ®Google Scholar
• Aisien, S. O., Walter, R. D. (1992). Polyamine N-acetyltransferase from Fasciola hepatica. Mol Biochem Parasitol 51:65–72.
   PubMed Web of Science ®Google Scholar
• Aisien, S. O., Walter, R. D. (1993). Biogenic-amine acetylation: an additional function of the N-acetyltransferase from Fasciola hepatica. Biochem J 291(Pt 3):733–737.
   PubMed Web of Science ®Google Scholar
• Alvarez, A. I., Merino, G., Molina, A. J., Pulido, M. M., McKellar, Q. A., Prieto, J. G. (2006). Role of ABC transporters in veterinary drug research and parasite resistance. Curr Drug Deliv 3:199–206.
   PubMedGoogle Scholar
• Alvarez, L. I., Imperiale, F. A., Sanchez, S. F., Murno, G. A., Lanusse, C. E. (2000). Uptake of albendazole and albendazole sulphoxide by Haemonchus contortus and Fasciola hepatica in sheep. Vet Parasitol 94:75–89.
   PubMed Web of Science ®Google Scholar
• Alvarez, L. I., Mottier, M. L., Lanusse, C. E. (2007). Drug transfer into target helminth parasites. Trends Parasitol 23:97–104.
   PubMed Web of Science ®Google Scholar
• Alvarez, L. I., Solana, H. D., Mottier, M. L., Virkel, G. L., Fairweather, I., Lanusse, C. E. (2005). Altered drug influx/efflux and enhanced metabolic activity in triclabendazole-resistant liver flukes. Parasitology 131:501–510.
   PubMed Web of Science ®Google Scholar
• Alvinerie, M., Dupuy, J., Eeckhoutte, C., Sutra, J. F., Kerboeuf, D. (2001). In vitro metabolism of moxidectin in Haemonchus contortus adult stages. Parasitol Res 87:702–704.
   PubMed Web of Science ®Google Scholar
• Asojo, O. A., Homma, K., Sedlacek, M., Ngamelue, M., Goud, G. N., Zhan, B. et al. (2007). X-ray structures of Na-GST-1 and Na-GST-2 two glutathione S-transferase from the human hookworm Necator americanus. BMC Struct Biol 7:42.
   PubMed Web of Science ®Google Scholar
• Azevedo, J. L., Hyman, B. C. (1993). Molecular characterization of lengthy mitochondrial DNA duplications from the parasitic nematode Romanomermis culicivorax. Genetics 133:933–942.
   PubMed Web of Science ®Google Scholar
• Bagnall, N. H., Kotze, A. C. (2004). cDNA cloning and expression patterns of a peroxiredoxin, a catalase, and a glutathione peroxidase from Haemonchus contortus. Parasitol 0Res 94:283–289.
   PubMed Web of Science ®Google Scholar
• Barrett, J. (1997). Helminth detoxification mechanisms. J Helminthol 71:85–89.
   PubMed Web of Science ®Google Scholar
• Blackhall, W. J., Liu, H. Y., Xu, M., Pritchard, R. K., Beech, R. N. (1998). Selection at a P-glycoprotein gene in ivermectin- and moxidectin-selected strains of Haemonchus contortus. Mol Biochem Parasitol 95:193–201.
   PubMed Web of Science ®Google Scholar
• Board, P. G., Baker, R. T., Chelvanayagam, G., Jermiin, L. S. (1997). Zeta, a novel class of glutathione transferases in a range of species from plants to humans. Biochem J 328(Pt 3):929–935.
   PubMed Web of Science ®Google Scholar
• Board, P. G., Coggan, M., Chelvanayagam, G., Easteal, S., Jermiin, L. S., Schulte, G. K. et al. (2000). Identification, characterization, and crystal structure of the Omega-class glutathione transferases. J Biol Chem 275:24798–24806.
   PubMed Web of Science ®Google Scholar
• Brennan, G. P., Fairweather, I., Trudgett, A., Hoey, E., McCoy, M., McConville, M. et al. (2007). Understanding triclabendazole resistance. Exp Mol Pathol 82:104–109.
   PubMed Web of Science ®Google Scholar
• Brophy, P. M., Barrett, J. (1990a). Blocking factors and the isolation of glutathione transferases from Hymenolepis diminuta (Cestoda: Cyclophyllidea). Parasitology 100(Pt 1):137–141.
   PubMed Web of Science ®Google Scholar
• Brophy, P. M., Barrett, J. (1990b). Glutathione transferase in helminths. Parasitology 100(Pt 2):345–349.
   PubMed Web of Science ®Google Scholar
• Brophy, P. M., Bensmith, A., Brown, A., Behnke, J. M., Pritchard, D. I. (1994a). Glutathione S-transferases from the gastrointestinal nematode Heligmosomoides-Polygyrus and mammalian liver compared. Compar Biochem Physiol B Biochem Mol Biol 109:585–592.
   PubMed Web of Science ®Google Scholar
• Brophy, P. M., Campbell, A. M., van Eldik, A. J., Teesdale-Spittle, P. H., Liebau, E., Wang, M. F. (2000). Beta-carbonyl substituted glutathione conjugates as inhibitors of O. volvulus GST2. Bioorg Med Chem Lett 10:979–981.
   PubMed Web of Science ®Google Scholar
• Brophy, P. M., Crowley, P., Barrett, J. (1990c). Detoxification reactions of Fasciola hepatica cytosolic glutathione transferases. Mol Biochem Parasitol 39:155–161.
   PubMed Web of Science ®Google Scholar
• Brophy, P. M., Papadopoulos, A., Touraki, M., Coles, B., Korting, W., Barrett, J. (1989a). Purification of cytosolic glutathione transferases from Schistocephalus-Solidus (Plerocercoid)—interaction with anthelmintics and products of lipid-peroxidation. Mol Biochem Parasitol 36:187–196.
   PubMed Web of Science ®Google Scholar
• Brophy, P. M., Patterson, L. H., Brown, A., Pritchard, D. I. (1995). Glutathione S-transferase (GST) expression in the human hookworm Necator americanus: potential roles for excretory-secretory forms of GST. Acta Trop 59:259–263.
   PubMed Web of Science ®Google Scholar
• Brophy, P. M., Pritchard, D. I. (1994b). Parasitic helminth glutathione S-transferases: an update on their potential as targets for immuno- and chemotherapy. Exp Parasitol 79:89–96.
   PubMed Web of Science ®Google Scholar
• Brophy, P. M., Southan, C., Barrett, J. (1989b). Glutathione transferases in the tapeworm Moniezia expansa. Biochem J 262:939–946.
   PubMed Web of Science ®Google Scholar
• Campbell, A. M., Teesdale-Spittle, P. H., Barrett, J., Liebau, E., Jefferies, J. R., Brophy, P. M. (2001). A common class of nematode glutathione S-transferase (GST) revealed by the theoretical proteome of the model organism Caenorhabditis elegans. Comp Biochem Physiol B Biochem Mol Biol 128:701–708.
   PubMed Web of Science ®Google Scholar
• Creaney, J., Wijffels, G. L., Sexton, J. L., Sandeman, R. M., Spithill, T. W., Parsons, J. C. (1995). Fasciola hepatica: localisation of glutathione S-transferase isoenzymes in adult and juvenile liver fluke. Exp Parasitol 81:106–116.
   PubMed Web of Science ®Google Scholar
• Cvilink, V., Kubicek, V., Nobilis, M., Krizova, V., Szotakova, B., Lamka, J., et al. (2008a). Biotransformation of flubendazole and selected model xenobiotics in Haemonchus contortus. Vet Parasitol 151:242–248.
   PubMed Web of Science ®Google Scholar
• Cvilink, V., Skalova, L., Szotakova, B., Lamka, J., Kostiainen, R., Ketola, R. A. (2008b). LC-MS-MS identification of albendazole and flubendazole metabolites formed ex vivo by Haemonchus contortus. Anal Bioanal Chem 391:337–343.
   PubMed Web of Science ®Google Scholar
• Cvilink, V., Szotakova, B., Krizova, V., Lamka, J., Skalova, L. (2008c). Phase I biotransformation of albendazole in lancet fluke (Dicrocoeliumdendriticum). Res Vet Sci.
   PubMed Web of Science ®Google Scholar
• Delatour, P., Benoit, E., Besse, S., Boukraa, A. (1991a). Comparative enantioselectivity in the sulphoxidation of albendazole in man, dogs, and rats. Xenobiotica 21:217–221.
   PubMed Web of Science ®Google Scholar
• Delatour, P., Benoit, E., Caude, M., Tambute, A. (1990). Species differences in the generation of the chiral sulfoxide metabolite of albendazole in sheep and rats. Chirality 2:156–160.
   PubMed Web of Science ®Google Scholar
• Delatour, P., Garnier, F., Benoit, E., Caude, I. (1991b). Chiral behaviour of the metabolite albendazole sulphoxide in sheep, goats, and cattle. Res Vet Sci 50:134–138.
   PubMed Web of Science ®Google Scholar
• Douch, P. G., Buchanan, L. L. (1978). Glutathione conjugation of some xenobiotics by Ascaris suum and Moniezia expansa. Xenobiotica 8:171–176.
   PubMed Web of Science ®Google Scholar
• Dowd, C. A., Buckley, C. M., Sheehan, D. (1997). Glutathione S-transferases from the white-rot fungus, Phanerochaete chrysosporium. Biochem J 324(Pt 1):243–248.
   PubMed Web of Science ®Google Scholar
• Dzik, J. M. (2006). Molecules released by helminth parasites involved in host colonization. Acta Biochim Pol 53:33–64.
   PubMed Web of Science ®Google Scholar
• Edwards, R., Dixon, D. P., Walbot, V. (2000). Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health. Trends Plant Sci 5:193–198.
   PubMed Web of Science ®Google Scholar
• Esterbauer, H., Cheeseman, K. H., Dianzani, M. U., Poli, G., Slater, T. F. (1982). Separation and characterization of the aldehydic products of lipid peroxidation stimulated by ADP-Fe2+ in rat liver microsomes. Biochem J 208:129–140.
   PubMed Web of Science ®Google Scholar
• Fakae, B. B., Campbell, A. M., Barrett, J., Scott, I. M., Teesdale-Spittle, P. H., Liebau, E., et al. (2000). Inhibition of glutathione S-transferases (GSTs) from parasitic nematodes by extracts from traditional Nigerian medicinal plants. Phytother Res 14:630–634.
   PubMed Web of Science ®Google Scholar
• Feng, J. J., Guo, H. F., Yao, M. Y., Xiao, S. H. (1995). Effects of mebendazole, albendazole, and praziquantel on glutathione S-transferase and superoxide dismutase of Echinococcus granulosus cyst wall harbored in mice. Zhongguo Yao Li Xue Bao 16:297–300.
   PubMed Web of Science ®Google Scholar
• Fernandez, C., Hormaeche, C. E. (1994). Isolation and biochemical characterisation of a glutathione S-transferase from Echinococcus granulosus protoscoleces. Int J Parasitol 24:1063–1066.
   PubMed Web of Science ®Google Scholar
• Fernandez, V., Chalar, C., Martinez, C., Musto, H., Zaha, A., Fernandez, C. (2000). Echinococcus granulosus: molecular cloning and phylogenetic analysis of an inducible glutathione S-transferase. Exp Parasitol 96:190–194.
   PubMed Web of Science ®Google Scholar
• Geerts, S., Gryseels, B. (2000). Drug resistance in human helminths: current situation and lessons from livestock. Clin Microbiol Rev 13:207–222.
   PubMed Web of Science ®Google Scholar
• Gilleard, J. S. (2006). Understanding anthelmintic resistance: the need for genomics and genetics. Int J Parasitol 36:1227–1239.
   PubMed Web of Science ®Google Scholar
• Girardini, J., Amirante, A., Zemzoumi, K., Serra, E. (2002a). Characterization of an Omega-class glutathione S-transferase from Schistosoma mansoni with glutaredoxin-like dehydroascorbate reductase and thiol transferase activities. Eur J Biochem 269:5512–5521.
   PubMedGoogle Scholar
• Girardini, J. E., Dissous, C., Serra, E. (2002b). Schistosoma mansoni ferredoxin NADP(H) oxidoreductase and its role in detoxification. Mol Biochem Parasitol 124:37–45.
   PubMed Web of Science ®Google Scholar
• Gupta, S., Rathaur, S. (2005). Filarial glutathione S-transferase: its induction by xenobiotics and potential as drug target. Acta Biochim Pol 52:493–500.
   PubMed Web of Science ®Google Scholar
• Hahn, M. E. (2002). Aryl hydrocarbon receptors: diversity and evolution. Chem Biol Interact 141:131–160.
   PubMed Web of Science ®Google Scholar
• Hayes, J. D., Pulford, D. J. (1995). The glutathione S-transferase supergene family: regulation of GST and the contribution of the isoenzymes to cancer chemoprotection and drug resistance. Crit Rev Biochem Mol Biol 30:445–600.
   PubMed Web of Science ®Google Scholar
• Hayes, J. D., Strange, R. C. (1995). Potential contribution of the glutathione S-transferase supergene family to resistance to oxidative stress. Free Radic Res 22:193–207.
   PubMed Web of Science ®Google Scholar
• Hendrix, C. M., Robinson, E. (2006). Diagnostic Parasitology for Veterinary Technicians. St. Louise: Mosby Elsevier.
   Google Scholar
• Higgins, C. F., Linton, K. J. (2003). ABC transporters, an introduction and overview. In: I. B. Holland ( ed.), ABC Proteins ( pp. 317–335). London: Academic Press.
   Google Scholar
• Holy, J. M., O’Leary, K. A., Oaks, J. A., Tracy, J. W. (1989). Immunocytochemical localization of the major glutathione S-transferases in adult Schistosoma mansoni. J Parasitol 75:181–190.
   PubMed Web of Science ®Google Scholar
• Hong, S. J., Kang, S. Y., Chung, Y. B., Chung, M. H., Oh, Y. J., Kang, I., et al. (2000). Paragonimus westermani: a cytosolic glutathione S-transferase of a sigma-class in adult stage. Exp Parasitol 94:180–189.
   PubMed Web of Science ®Google Scholar
• Hong, S. J., Lee, J. Y., Lee, D. H., Sohn, W. M., Cho, S. Y. (2001). Molecular cloning and characterization of a Mu-class glutathione S-transferase from Clonorchis sinensis. Mol Biochem Parasitol 115:69–75.
   PubMed Web of Science ®Google Scholar
• Hong, S. J., Yu, J. R., Kang, S. Y. (2002). Ultrastructural localization of 28-kDa glutathione S-transferase in adult Clonorchis sinensis. Korean J Parasitol 40:173–176.
   PubMedGoogle Scholar
• Hoppner, J., Perbandt, M., Betzel, C., Walter, R. D., Liebau, E. (2004). Crystallization of the major cytosolic glutathione S-transferase from Onchocerca volvulus. Acta Crystallogr D Biol Crystallogr 60:1496–1497.
   PubMed Web of Science ®Google Scholar
• Hoque, E., Pflugmacher, S., Fritscher, J., Wolf, M. (2007). Induction of glutathione S-transferase in biofilms and germinating spores of Mucor hiemalis strain EH5 from cold sulfidic spring waters. Appl Environ Microbiol 73:2697–2707.
   PubMed Web of Science ®Google Scholar
• Hotez, P., Raff, S., Fenwick, A., Richards, F., Jr., Molyneux, D. H. (2007). Recent progress in integrated neglected tropical disease control. Trends Parasitol 23:511–514.
   PubMed Web of Science ®Google Scholar
• Isaac, R. E., Eaves, L., Muimo, R., Lamango, N. (1991). N-acetylation of biogenic amines in Ascaridia galli. Parasitology 102(Pt 3):445–450.
   PubMed Web of Science ®Google Scholar
• Isaac, R. E., Muimo, R., Macgregor, A. N. (1990). N-Acetylation of serotonin, octopamine, and dopamine by adult Brugia-Pahangi. Mol Biochem Parasitol 43:193–198.
   PubMed Web of Science ®Google Scholar
• Jakobsson, P. J., Morgenstern, R., Mancini, J., Ford-Hutchinson, A., Persson, B. (1999). Common structural features of MAPEG—a widespread superfamily of membrane-associated proteins with highly divergent functions in eicosanoid and glutathione metabolism. Prot Sci 8:689–692.
   PubMed Web of Science ®Google Scholar
• Jakobsson, P. J., Morgenstern, R., Mancini, J., Ford-Hutchinson, A., Persson, B. (2000). Membrane-associated proteins in eicosanoid and glutathione metabolism (MAPEG). A widespread protein superfamily. Am J Respir Crit Care Med 161:S20–S24.
   PubMed Web of Science ®Google Scholar
• Jefferies, J. R., Campbell, A. M., van Rossum, A. J., Barrett, J., Brophy, P. M. (2001). Proteomic analysis of Fasciola hepatica excretory-secretory products. Proteomics 1:1128–1132.
   PubMed Web of Science ®Google Scholar
• Jez, J. M., Penning, T. M. (2001). The aldo-keto reductase (AKR) superfamily: an update. Chem Biol Interact 130–132:499–525.
   PubMed Web of Science ®Google Scholar
• Kampkotter, A., Volkmann, T. E., de Castro, S. H., Leiers, B., Klotz, L. O., Johnson, T. E., et al. (2003). Functional analysis of the glutathione S-transferase 3 from Onchocerca volvulus (Ov-GST-3): a parasite GST confers increased resistance to oxidative stress in Caenorhabditis elegans. J Mol Biol 325:25–37.
   PubMed Web of Science ®Google Scholar
• Kang, S. Y., Ahn, I. Y., Park, C. Y., Chung, Y. B., Hong, S. T., Kong, Y., et al. (2001). Clonorchis sinensis: molecular cloning and characterization of 28-kDa glutathione S-transferase. Exp Parasitol 97:186–195.
   PubMed Web of Science ®Google Scholar
• Kerboeuf, D., Blackhall, W., Kaminsky, R., von Samson-Himmelstjerna G., (2003). P-glycoprotein in helminths: function and perspectives for anthelmintic treatment and reversal of resistance. Int J Antimicrob Agents 22:332–346.
   PubMed Web of Science ®Google Scholar
• Kerboeuf, D., Soubieux, D., Guilluy, R., Brazier, J. L., Riviere, J. L. (1995). In vivo metabolism of aminopyrine by the larvae of the helminth Heligmosomoides polygyrus. Parasitol Res 81:302–304.
   PubMed Web of Science ®Google Scholar
• Kim, T. H., Hwang, S. B., Jeong, P. Y., Lee, J., Cho, J. W. (2005). Requirement of tyrosylprotein sulfotransferase-A for proper cuticle formation in the nematode C. elegans. FEBS Lett 579:53–58.
   PubMed Web of Science ®Google Scholar
• Kim, T. Y., Lee, J. Y., Kim, T. I., Moon, K. H., Kang, S. Y., Hong, S. J. (2007). Molecular cloning and enzymatic characterization of a class Mu glutathione S-transferase of Paragonimus westermani. Parasitol Res 101:1225–1231.
   Web of Science ®Google Scholar
• Kodym, R., Calkins, P., Story, M. (1999). The cloning and characterization of a new stress response protein. A mammalian member of a family of Theta-class glutathione S-transferase-like proteins. J Biol Chem 274:5131–5137.
   PubMed Web of Science ®Google Scholar
• Kohler, P., Bachmann, R. (1981). Intestinal tubulin as possible target for the chemotherapeutic action of mebendazole in parasitic nematodes. Mol Biochem Parasitol 4:325–336.
   PubMed Web of Science ®Google Scholar
• Kotze, A. C. (1997). Cytochrome P450 monooxygenase activity in Haemonchus contortus (Nematoda). Int J Parasitol 27:33–40.
   PubMed Web of Science ®Google Scholar
• Kotze, A. C. (1999). Peroxide-supported in-vitro cytochrome P450 activities in Haemonchus contortus. Int J Parasitol 29:389–396.
   PubMed Web of Science ®Google Scholar
• Kotze, A. C. (2000). Oxidase activities in macrocyclic-resistant and -susceptible Haemonchus contortus. J Parasitol 86:873–876.
   PubMed Web of Science ®Google Scholar
• Kotze, A. C., Dobson, R. J., Chandler, D. (2006). Synergism of rotenone by piperonyl butoxide in Haemonchus contortus and Trichostrongylus colubriformis in vitro: potential for drug-synergism through inhibition of nematode oxidative detoxification pathways. Vet Parasitol 136:275–282.
   PubMed Web of Science ®Google Scholar
• Kotze, A. C., McClure, S. J. (2001). Haemonchus contortus utilises catalase in defence against exogenous hydrogen peroxide in vitro. Int J Parasitol 31:1563–1571.
   PubMed Web of Science ®Google Scholar
• Krause, S., Sommer, A., Fischer, P., Brophy, P. M., Walter, R. D., Liebau, E. (2001). Gene structure of the extracellular glutathione S-transferase from Onchocerca volvulus and its overexpression and promoter analysis in transgenic Caenorhabditis elegans. Mol Biochem Parasitol 117:145–154.
   PubMed Web of Science ®Google Scholar
• Krueger, S. K., Williams, D. E. (2005). Mammalian flavin-containing monooxygenases: structure/function, genetic polymorphisms, and role in drug metabolism. Pharmacol Ther 106:357–387.
   PubMed Web of Science ®Google Scholar
• Liebau, E., Eckelt, V. H., Wildenburg, G., Teesdale-Spittle, P., Brophy, P. M., Walter, R. D., et al. (1997). Structural and functional analysis of a glutathione S-transferase from Ascaris suum. Biochem J 324(Pt 2):659–666.
   PubMed Web of Science ®Google Scholar
• Liebau, E., Eschbach, M. L., Tawe, W., Sommer, A., Fischer, P., Walter, R. D., et al. (2000). Identification of a stress-responsive Onchocerca volvulus glutathione S-transferase (Ov-GST-3) by RT-PCR differential display. Mol Biochem Parasitol 109:101–110.
   PubMed Web of Science ®Google Scholar
• Liebau, E., Walter, R. D., Henkle-Duhrsen, K. (1994a). Isolation, sequence, and expression of an Onchocerca volvulus glutathione S-transferase cDNA. Mol Biochem Parasitol 63:305–309.
   PubMed Web of Science ®Google Scholar
• Liebau, E., Walter, R. D., Henkle-Duhrsen, K. (1994b). Onchocerca volvulus: isolation and sequence of a second glutathione S-transferase cDNA. Exp Parasitol 79:68–71.
   PubMed Web of Science ®Google Scholar
• Liebau, E., Wildenburg, G., Brophy, P. M., Walter, R. D., Henkle-Duhrsen, K. (1996). Biochemical analysis, gene structure, and localization of the 24-kDa glutathione S-transferase from Onchocerca volvulus. Mol Biochem Parasitol 80:27–39.
   PubMed Web of Science ®Google Scholar
• Liebau, E., Wildenburg, G., Walter, R. D., Henkle-Duhrsen, K. (1994c). A novel type of glutathione S-transferase in Onchocerca volvulus. Infect Immun 62:4762–4767.
   PubMed Web of Science ®Google Scholar
• Lim, K., Ho, J. X., Keeling, K., Gilliland, G. L., Ji, X., Ruker, F., et al. (1994). Three-dimensional structure of Schistosoma japonicum glutathione S-transferase fused with a six-amino-acid conserved neutralizing epitope of gp41 from HIV. Prot Sci 3:2233–2244.
   PubMed Web of Science ®Google Scholar
• Lincke, C. R., The, I., van Groenigen M., Borst, P., (1992). The P-glycoprotein gene family of Caenorhabditis elegans. Cloning and characterization of genomic and complementary DNA sequences. J Mol Biol 228:701–711.
   PubMed Web of Science ®Google Scholar
• Lindblom, T. H., Dodd, A. K. (2006). Xenobiotic detoxification in the nematode Caenorhabditis elegans. J Exp Zoolog A Comp Exp Biol 305:720–730.
   PubMedGoogle Scholar
• Lo, W. J., Chiou, Y. C., Hsu, Y. T., Lam, W. S., Chang, M. Y., Jao, S. C., et al. (2007). Enzymatic and nonenzymatic synthesis of glutathione conjugates: application to the understanding of a parasite’s defense system and alternative to the discovery of potent glutathione S-transferase inhibitors. Bioconjug Chem 18:109–120.
   PubMed Web of Science ®Google Scholar
• Lopez, M. F., Patton, W. F., Sawlivich, W. B., Erdjument-Bromage, H., Barry, P., Gmyrek, K., et al. (1994). A glutathione S-transferase (GST) isozyme from broccoli with significant sequence homology to the mammalian theta-class of GSTs. Biochim Biophys Acta 1205:29–38.
   PubMed Web of Science ®Google Scholar
• Mannervik, B., Alin, P., Guthenberg, C., Jensson, H., Tahir, M. K., Warholm, M., et al. (1985). Identification of three classes of cytosolic glutathione transferase common to several mammalian species: correlation between structural data and enzymatic properties. Proc Natl Acad Sci U S A 82:7202–7206.
   PubMed Web of Science ®Google Scholar
• Mannervik, B., Danielson, U. H. (1988). Glutathione transferases—structure and catalytic activity. CRC Crit Rev Biochem 23:283–337.
   PubMed Web of Science ®Google Scholar
• McTigue, M. A., Williams, D. R., Tainer, J. A. (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.
   PubMed Web of Science ®Google Scholar
• Mehlhorn, H. (2001). Encyclopedic Reference of Parasitology. Berlin: Springer.
   Google Scholar
• Menzel, R., Bogaert, T., Achazi, R. (2001). A systematic gene expression screen of Caenorhabditis elegans cytochrome P450 genes reveals CYP35 as strongly xenobiotic inducible. Arch Biochem Biophys 395:158–168.
   PubMed Web of Science ®Google Scholar
• Menzel, R., Rodel, M., Kulas, J., Steinberg, C. E. (2005). CYP35: xenobiotically induced gene expression in the nematode Caenorhabditis elegans. Arch Biochem Biophys 438:93–102.
   PubMed Web of Science ®Google Scholar
• Menzel, R., Yeo, H. L., Rienau, S., Li, S., Steinberg, C. E., Sturzenbaum, S. R. (2007). Cytochrome P450s and short-chain dehydrogenases mediate the toxicogenomic response of PCB52 in the nematode Caenorhabditis elegans. J Mol Biol 370:1–13.
   PubMed Web of Science ®Google Scholar
• Meyer, D. J., Muimo, R., Thomas, M., Coates, D., Isaac, R. E. (1996). Purification and characterization of prostaglandin-H E-isomerase, a Sigma-class glutathione S-transferase, from Ascaridia galli. Biochem J 313(Pt 1):223–227.
   PubMed Web of Science ®Google Scholar
• Milhon, J. L., Thiboldeaux, R. L., Glowac, K., Tracy, J. W. (1997). Schistosoma japonicum GSH S-transferase Sj26 is not the molecular target of praziquantel action. Exp Parasitol 87:268–274.
   PubMed Web of Science ®Google Scholar
• Miller, C. M., Howell, M. J., Boray, J. C. (1994). Glutathione S-transferases as markers of salicylanilide resistance in isolates of Fasciola hepatica. Int J Parasitol 24:533–542.
   PubMed Web of Science ®Google Scholar
• Molyneux, D. H. (2006). Control of human parasitic diseases: context and overview. Adv Parasitol 61:1–45.
   PubMed Web of Science ®Google Scholar
• Morello, A., Repetto, Y., Atias, A. (1982). Characterization of glutathione S-transferase activity in Echinococcus granulosus. Comp Biochem Physiol B 72:449–452.
   PubMed Web of Science ®Google Scholar
• Moreno, L., Alvarez, L., Mottier, L., Virkel, G., Bruni, S. S., Lanusse, C. (2004). Integrated pharmacological assessment of flubendazole potential for use in sheep: disposition kinetics, liver metabolism, and parasite diffusion ability. J Vet Pharmacol Ther 27:299–308.
   PubMed Web of Science ®Google Scholar
• Moroni, P., Buronfosse, T., Longin-Sauvageon, C., Delatour, P., Benoit, E. (1995). Chiral sulfoxidation of albendazole by the flavin adenine dinucleotide-containing and cytochrome P450-dependent monooxygenases from rat liver microsomes. Drug Metab Dispos 23:160–165.
   PubMed Web of Science ®Google Scholar
• Mottier, L., Alvarez, L., Ceballos, L., Lanusse, C. (2006a). Drug transport mechanisms in helminth parasites: passive diffusion of benzimidazole anthelmintics. Exp Parasitol 113:49–57.
   PubMed Web of Science ®Google Scholar
• Mottier, L., Alvarez, L., Fairweather, I., Lanusse, C. (2006b). Resistance-induced changes in triclabendazole transport in Fasciola hepatica: ivermectin reversal effect. J Parasitol 92:1355–1360.
   PubMed Web of Science ®Google Scholar
• Mottier, L., Virkel, G., Solana, H., Alvarez, L., Salles, J., Lanusse, C. (2004). Triclabendazole biotransformation and comparative diffusion of the parent drug and its oxidized metabolites into Fasciola hepatica. Xenobiotica 34:1043–1057.
   PubMed Web of Science ®Google Scholar
• Muimo, R., Isaac, R. E. (1993). Properties of an arylalkylamine N-acetyltransferase from the Nematode, Ascaridia-Galli. Compar Biochem Physiol B Biochem Mol Biol 106:969–976.
   Web of Science ®Google Scholar
• Munir, W. A., Barrett, J. (1985). The metabolism of xenobiotic compounds by Hymenolepis diminuta (Cestoda: Cyclophyllidea). Parasitology 91(Pt 1):145–156.
   PubMed Web of Science ®Google Scholar
• Nava, G., Robert, L., Plancarte, A. (2007). Characterization of Taenia solium cysticerci microsomal glutathione S-transferase activity. Parasitol Res 101:1373–1381.
   PubMed Web of Science ®Google Scholar
• Nebbia, C. (2001). Biotransformation enzymes as determinants of xenobiotic toxicity in domestic animals. Vet J 161:238–252.
   PubMed Web of Science ®Google Scholar
• O’Hanlon, G. M., Cleator, M., Mercer, J. G., Howells, R. E., Rees, H. H. (1991a). Metabolism and fate of ecdysteroids in the nematodes Ascaris suum and Parascaris equorum. Mol Biochem Parasitol 47:179–187.
   PubMed Web of Science ®Google Scholar
• O’Hanlon, G. M., Howarth, O. W., Rees, H. H. (1987). Identification of ecdysone 25-O-beta-D-glucopyranoside as a new metabolite of ecdysone in the nematode Parascaris equorum. Biochem J 248:305–307.
   PubMed Web of Science ®Google Scholar
• O’Hanlon, G. M., Mercer, J. G., Rees, H. H. (1991b). Evidence for the release of 20-hydroxyecdysone 25-glucoside by adult female Parascaris equorum (Nematoda) in vitro. Parasitol Res 77:271–272.
   PubMed Web of Science ®Google Scholar
• O’Leary, K. A., Hathaway, K. M., Tracy, J. W. (1992). Schistosoma mansoni: single-step purification and characterization of glutathione S-transferase isoenzyme 4. Exp Parasitol 75:47–55.
   PubMed Web of Science ®Google Scholar
• O’Leary, K. A., Tracy, J. W. (1988). Purification of three cytosolic glutathione S-transferases from adult Schistosoma mansoni. Arch Biochem Biophys 264:1–12.
   PubMed Web of Science ®Google Scholar
• O’Leary, K. A., Tracy, J. W. (1991). Schistosoma mansoni: glutathione S-transferase-catalyzed detoxication of dichlorvos. Exp Parasitol 72:355–361.
   PubMed Web of Science ®Google Scholar
• Ouellette, M., Legare, D. (2003). Drug resistance mediated by ABC transporters in parasites of human. In: Holland I. B. ( ed.), ABC Proteins ( pp. 317–335). London: Academic Press.
   Google Scholar
• Panaccio, M., Wilson, L. R., Crameri, S. L., Wijffels, G. L., Spithill, T. W. (1992). Molecular characterization of cDNA sequences encoding glutathione S-transferases of Fasciola hepatica. Exp Parasitol 74:232–237.
   PubMed Web of Science ®Google Scholar
• Paul, J. M., Barrett, J. (1980). Peroxide metabolism in the cestodes Hymenolepis-Diminuta and Moniezia-Expansa. Int J Parasitol 10:121–124.
   Web of Science ®Google Scholar
• Pemble, S. E., Wardle, A. F., Taylor, J. B. (1996). Glutathione S-transferase class Kappa: characterization by the cloning of rat mitochondrial GST and identification of a human homologue. Biochem J 319(Pt 3):749–754.
   PubMed Web of Science ®Google Scholar
• Perbandt, M., Hoppner, J., Betzel, C., Walter, R. D., Liebau, E. (2005). Structure of the major cytosolic glutathione S-transferase from the parasitic nematode Onchocerca volvulus. J Biol Chem 280:12630–12636.
   PubMed Web of Science ®Google Scholar
• Petalcorin, M. I., Joshua, G. W., Agapow, P. M., Dolphin, C. T. (2005). The FMO genes of Caenorhabditis elegans and C. briggsae: characterisation, gene expression, and comparative genomic analysis. Gene 346:83–96.
   PubMed Web of Science ®Google Scholar
• Pica-Mattoccia, L., Carlini, D., Guidi, A., Cimica, V., Vigorosi, F., Cioli, D. (2006). The schistosome enzyme that activates oxamniquine has the characteristics of a sulfotransferase. Mem Inst Oswaldo Cruz 101(Suppl 1):307–312.
   PubMed Web of Science ®Google Scholar
• Plancarte, A., Rendon, J. L., Landa, A. (2004). Purification, characterization, and kinetic properties of the Taenia solium glutathione S-transferase isoform 26.5 kDa. Parasitol Res 93:137–144.
   PubMed Web of Science ®Google Scholar
• Porchet, E., McNair, A., Caron, A., Kusnierz, J. P., Zemzoumi, K., Capron, A. (1994). Tissue expression of the Schistosoma mansoni 28-kDa glutathione S-transferase. Parasitology 109(Pt 5):565–572.
   PubMed Web of Science ®Google Scholar
• Precious, W. Y., Barrett, J. (1989a). The possible absence of cytochrome P-450–linked xenobiotic metabolism in helminths. Biochim Biophys Acta 992:215–222.
   PubMed Web of Science ®Google Scholar
• Precious, W. Y., Barrett, J. (1989b). Xenobiotic metabolism in helminths. Parasitol Today 5:156–160.
   PubMedGoogle Scholar
• Raines, P. S., Barrett, J. (1988). Hymenolepis-Diminuta—lack of sulfate activation and sulfotransferase activity. Exp Parasitol 65:209–213.
   PubMed Web of Science ®Google Scholar
• Rao, U. R., Salinas, G., Mehta, K., Klei, T. R. (2000). Identification and localization of glutathione S-transferase as a potential target enzyme in Brugia species. Parasitol Res 86:908–915.
   PubMed Web of Science ®Google Scholar
• Rathaur, S., Fischer, P., Domagalski, M., Walter, R. D., Liebau, E. (2003). Brugia malayi and Wuchereria bancrofti: gene comparison and recombinant expression of Pi-class– related glutathione S-transferases. Exp Parasitol 103:177–181.
   PubMed Web of Science ®Google Scholar
• Reichert, K., Menzel, R. (2005). Expression profiling of five different xenobiotics using a Caenorhabditis elegans whole-genome microarray. Chemosphere 61:229–237.
   PubMed Web of Science ®Google Scholar
• Robinson, M. W., Lawson, J., Trudgett, A., Hoey, E. M., Fairweather, I. (2004). The comparative metabolism of triclabendazole sulphoxide by triclabendazole-susceptible and triclabendazole-resistant Fasciola hepatica. Parasitol Res 92:205–210.
   PubMed Web of Science ®Google Scholar
• Roh, J. Y., Jung, I. H., Lee, J. Y., Choi, J. (2007). Toxic effects of di(2-ethylhexyl)phthalate on mortality, growth, reproduction, and stress-related gene expression in the soil nematode Caenorhabditis elegans. Toxicology 237:126–133.
   PubMed Web of Science ®Google Scholar
• Roh, J. Y., Lee, J., Choi, J. (2006). Assessment of stress-related gene expression in the heavy metal-exposed nematode Caenorhabditis elegans: a potential biomarker for metal-induced toxicity monitoring and environmental risk assessment. Environ Toxicol Chem 25:2946–2956.
   PubMed Web of Science ®Google Scholar
• Rossjohn, J., Feil, S. C., Wilce, M. C., Sexton, J. L., Spithill, T. W., Parker, M. W. (1997). Crystallization, structural determination, and analysis of a novel parasite vaccine candidate: Fasciola hepatica glutathione S-transferase. J Mol Biol 273:857–872.
   PubMed Web of Science ®Google Scholar
• Rothwell, J., Sangster, N. (1997). Haemonchus contortus: the uptake and metabolism of closantel. Int J Parasitol 27:313–319.
   PubMed Web of Science ®Google Scholar
• Saeed, H. M., Mostafa, M. H., O’Connor, P. J., Rafferty, J. A., Doenhoff, M. J. (2002). Evidence for the presence of active cytochrome P450 systems in Schistosoma mansoni and Schistosoma haematobium adult worms. FEBS Lett 519:205–209.
   PubMed Web of Science ®Google Scholar
• Salinas, A. E., Wong, M. G. (1999). Glutathione S-transferases—a review. Curr Med Chem 6:279–309.
   PubMed Web of Science ®Google Scholar
• Salinas, G., Braun, G., Taylor, D. W. (1994). Molecular characterisation and localisation of an Onchocerca volvulus Pi-class glutathione S-transferase. Mol Biochem Parasitol 66:1–9.
   PubMed Web of Science ®Google Scholar
• Sangster, N. C., Prichard, R. K. (1986). Thiabendazole uptake, metabolism, and excretion in thiabendazole resistant and susceptible Trichostrongylus colubriformis. J Parasitol 72:798–800.
   PubMed Web of Science ®Google Scholar
• Sheehan, D., Meade, G., Foley, V. M., Dowd, C. A. (2001). Structure, function, and evolution of glutathione transferases: implications for classification of nonmammalian members of an ancient enzyme superfamily. Biochem J 360:1–16.
   PubMed Web of Science ®Google Scholar
• Smith, J. M., Prichard, R. K. (2002). Localization of P-glycoprotein mRNA in the tissues of Haemonchus contortus adult worms and its relative abundance in drug-selected and susceptible strains. J Parasitol 88:612–620.
   PubMed Web of Science ®Google Scholar
• Solana, H. D., Rodriguez, J. A., Lanusse, C. E. (2001). Comparative metabolism of albendazole and albendazole sulphoxide by different helminth parasites. Parasitol Res 87:275–280.
   PubMed Web of Science ®Google Scholar
• Solana, H. D., Sallovitz, J. M., Lanusse, C. E., Rodriguez, J. A. (2002). Enantioselective binding of albendazole sulphoxide to cytosolic proteins from helminth parasites. Meth Find Exp Clin Pharmacol 24:7–13.
   PubMed Web of Science ®Google Scholar
• Sommer, A., Nimtz, M., Conradt, H. S., Brattig, N., Boettcher, K., Fischer, P., et al. (2001). Structural analysis and antibody response to the extracellular glutathione S-transferases from Onchocerca volvulus. Infect Immun 69:7718–7728.
   PubMed Web of Science ®Google Scholar
• Sommer, A., Rickert, R., Fischer, P., Steinhart, H., Walter, R. D., Liebau, E. (2003). A dominant role for extracellular glutathione S-transferase from Onchocerca volvulus is the production of prostaglandin D2. Infect Immun 71:3603–3606.
   PubMed Web of Science ®Google Scholar
• Szotakova, B., Baliharova, V., Lamka, J., Nozinova, E., Wsol, V., Velik, J., et al. (2004). Comparison of in vitro activities of biotransformation enzymes in pig, cattle, goat, and sheep. Res Vet Sci 76:43–51.
   PubMed Web of Science ®Google Scholar
• Taylor, J. B., Vidal, A., Torpier, G., Meyer, D. J., Roitsch, C., Balloul, J. M., et al. (1988). The glutathione transferase activity and tissue distribution of a cloned Mr28K protective antigen of Schistosoma mansoni. EMBO J 7:465–472.
   PubMed Web of Science ®Google Scholar
• Testa, B. (1995). The Metabolism of Drugs and other Xenobiotics: Biochemistry of Redox Reactions. London: Academic Press.
   Google Scholar
• Testa, B., Mayer, J. A. (2003). Hydrolysis in Drug and Prodrug Metabolism. Weinheim, Zürich: VHCA & WILEY-VCH.
   Google Scholar
• Testa, B., van de Waterbeemd H., (2007). ADME-Tox Approaches. In: Triggle, D., Taylor, J ( eds.), Comprehensive Medicinal Chemistry II, Vol. 5. Philadelphia: Elsevier.
   Google Scholar
• Tew, K. D., Ronai, Z. (1999). GST function in drug and stress response. Drug Resist Update 2:143–147.
   PubMed Web of Science ®Google Scholar
• Trottein, F., Godin, C., Pierce, R. J., Sellin, B., Taylor, M. G., Gorillot, I., et al. (1992). Interspecies variation of schistosome 28-kDa glutathione S-transferases. Mol Biochem Parasitol 54:63–72.
   PubMed Web of Science ®Google Scholar
• Uetrecht, J. P., Trager, W. (2007). Drug Metabolism: Chemical and Enzymatic Aspects. New York: Informa Healthcare.
   Google Scholar
• van Rossum, A. J., Brophy, P. M., Tait, A., Barrett, J., Jefferies, J. R. (2001a). Proteomic identification of glutathione S-transferases from the model nematode Caenorhabditis elegans. Proteomics 1:1463–1468.
   PubMed Web of Science ®Google Scholar
• van Rossum, A. J., Jefferies, J., Young, C. J., Barrett, J., Tait, A., Brophy, P. M. (2001b). Glutathione S-transferase (GST) functional genomics: role of Caenorhabditis elegans in investigating GST expression in parasitic nematodes. Chem Biolog Interact 133:274–277.
   Web of Science ®Google Scholar
• van Rossum, A. J., Jefferies, J. R., Rijsewijk, F. A., LaCourse, E. J., Teesdale-Spittle, P., Barrett, J., et al. (2004). Binding of hematin by a new class of glutathione transferase from the blood-feeding parasitic nematode Haemonchus contortus. Infect Immun 72:2780–2790.
   PubMed Web of Science ®Google Scholar
• Vande Waa, E. A., Campbell, C. K., O’Leary, K. A., Tracy, J. W. (1993). Induction of Schistosoma mansoni glutathione S-transferase by xenobiotics. Arch Biochem Biophys 303:15–21.
   PubMed Web of Science ®Google Scholar
• Velik, J., Baliharova, V., Skalova, L., Szotakova, B., Wsol, V., Lamka, J. (2005). Liver microsomal biotransformation of albendazole in deer, cattle, sheep, and pig and some related wild breeds. J Vet Pharmacol Ther 28:377–384.
   PubMed Web of Science ®Google Scholar
• Vibanco-Perez, N., Jimenez, L., Mendoza-Hernandez, G., Landa, A. (2002). Characterization of a recombinant Mu-class glutathione S-transferase from Taenia solium. Parasitol Res 88:398–404.
   PubMed Web of Science ®Google Scholar
• Vibanco-Perez, N., Jimenez, L., Merchant, M. T., Landa, A. (1999). Characterization of glutathione S-transferase of Taenia solium. J Parasitol 85:448–453.
   PubMed Web of Science ®Google Scholar
• Vuilleumier, S. (1997). Bacterial glutathione S-transferases: what are they good for? J Bacteriol 179:1431–1441.
   PubMed Web of Science ®Google Scholar
• Walker, J., Crowley, P., Moreman, A. D., Barrett, J. (1993). Biochemical properties of cloned glutathione S-transferases from Schistosoma-Mansoni and Schistosoma-Japonicum. Mol Biochem Parasitol 61:255–264.
   PubMed Web of Science ®Google Scholar
• Weston, K., Yochem, J., Greenwald, I. (1989). A Caenorhabditis elegans cDNA that encodes a product resembling the rat glutathione S-transferase P subunit. Nucleic Acids Res 17:2138.
   PubMed Web of Science ®Google Scholar
• Wijffels, G. L., Sexton, J. L., Salvatore, L., Pettitt, J. M., Humphris, D. C., Panaccio, M., et al. (1992). Primary sequence heterogeneity and tissue expression of glutathione S-transferases of Fasciola hepatica. Exp Parasitol 74:87–99.
   PubMed Web of Science ®Google Scholar
• Wilce, M. C., Parker, M. W. (1994). Structure and function of glutathione S-transferases. Biochim Biophys Acta 1205:1–18.
   PubMed Web of Science ®Google Scholar
• Wildenburg, G., Liebau, E., Henkle-Duhrsen, K. (1998). Onchocerca volvulus: ultrastructural localization of two glutathione S-transferases. Exp Parasitol 88:34–42.
   PubMed Web of Science ®Google Scholar
• Wittich, R. M., Walter, R. D. (1989). A novel type of putrescine (diamine)-acetylating enzyme from the nematode Ascaris suum. Biochem J 260:265–269.
   PubMed Web of Science ®Google Scholar
• Wittich, R. M., Walter, R. D. (1990). Putrescine N-acetyltransferase in Onchocerca volvulus and Ascaris suum, an enzyme which is involved in polyamine degradation and release of N-acetylputrescine. Mol Biochem Parasitol 38:13–17.
   PubMed Web of Science ®Google Scholar
• Wolstenholme, A. J., Fairweather, I., Prichard, R., von Samson-Himmelstjerna, G., Sangster, N. C. (2004). Drug resistance in veterinary helminths. Trends Parasitol 20:469–476.
   PubMed Web of Science ®Google Scholar
• Xu, M., Molento, M., Blackhall, W., Ribeiro, P., Beech, R., Prichard, R. (1998). Ivermectin resistance in nematodes may be caused by alteration of P-glycoprotein homolog. Mol Biochem Parasitol 91:327–335.
   PubMed Web of Science ®Google Scholar
• Yatsuda, A. P., Krijgsveld, J., Cornelissen, A. W., Heck, A. J., de Vries E., (2003). Comprehensive analysis of the secreted proteins of the parasite Haemonchus contortus reveals extensive sequence variation and differential immune recognition. J Biol Chem 278:16941–16951.
   PubMed Web of Science ®Google Scholar
• Zhou, Z. H., Syvanen, M. (1997). A complex glutathione transferase gene family in the housefly Musca domestica. Mol Gen Genet 256:187–194.
   PubMedGoogle Scholar