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Anthelmintic metabolism in parasitic helminths: proteomic insights

Published online by Cambridge University Press:  10 July 2012

PETER M. BROPHY ,
NEIL MACKINTOSH  and
RUSSELL M. MORPHEW
PETER M. BROPHY*
Affiliation:
Parasitology Group, Institute of Biological, Environmental and Rural Sciences (IBERS), Aberystwyth University, Aberystwyth, Ceredigion, Wales SY23 3FG, UK
NEIL MACKINTOSH
Affiliation:
Parasitology Group, Institute of Biological, Environmental and Rural Sciences (IBERS), Aberystwyth University, Aberystwyth, Ceredigion, Wales SY23 3FG, UK
RUSSELL M. MORPHEW
Affiliation:
Parasitology Group, Institute of Biological, Environmental and Rural Sciences (IBERS), Aberystwyth University, Aberystwyth, Ceredigion, Wales SY23 3FG, UK
*
*Corresponding author: IBERS, Aberystwyth University, Aberystwyth SY23 3FG, [email protected] Tel: +44(0)1970 622332
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Summary

Anthelmintics are the cornerstone of parasitic helminth control. Surprisingly, understanding of the biochemical pathways used by parasitic helminths to detoxify anthelmintics is fragmented, despite the increasing global threat of anthelmintic resistance within the ruminant and equine industries. Reductionist biochemistry has likely over-estimated the enzymatic role of glutathione transferases in anthelmintic metabolism and neglected the potential role of the cytochrome P-450 superfamily (CYPs). Proteomic technologies offers the opportunity to support genomics, reverse genetics and pharmacokinetics, and provide an integrated insight into both the cellular mechanisms underpinning response to anthelmintics and also the identification of biomarker panels for monitoring the development of anthelmintic resistance. To date, there have been limited attempts to include proteomics in anthelmintic metabolism studies. Optimisations of membrane, post-translational modification and interaction proteomic technologies in helminths are needed to especially study Phase I CYPs and Phase III ABC transporter pumps for anthelmintics and their metabolites.

Keywords

Proteomicshelminthanthelminticanthelmintic resistancexenobiotic
Type
Research Article
Information
Parasitology , Volume 139 , Issue 9: Symposia of the British Society for Parasitology Volume 48 Proteomic insights into parasite biology , August 2012 , pp. 1205 - 1217
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Abubucker, S., Martin, J., Taylor, C. M. and Mitreva, M. (2011). HelmCoP: An online resource for helminth functional genomics and drug and vaccine targets prioritization. Plos One 6 (7), e21832.CrossRefGoogle ScholarPubMed
Adcock, H. J., Brophy, P. M., Teesdale-Spittle, P. H. and Buckberry, L. D. (1999). Cysteine conjugate beta-lyase activity in three species of parasitic helminth. International Journal for Parasitology 29, 543–548.CrossRefGoogle ScholarPubMed
Alvarez, A. I., Merino, G., Molina, A. J., Pulido, M. M., Mckellar, Q. A. and Prieto, J. G. (2006). Role of ABC transporters in veterinary drug research and parasite resistance. Current Drug Delivery 3, 199–206.CrossRefGoogle ScholarPubMed
Alvarez, L. I., Solana, H. D., Mottier, M. L., Virkel, G. L., Fairweather, I. and Lanusse, C. E. (2005). Altered drug influx/efflux and enhanced metabolic activity in triclabendazole-resistant liver flukes. Parasitology 131, 501–510.CrossRefGoogle ScholarPubMed
Barrett, J. (1997). Helminth detoxification mechanisms. Journal of Helminthology 71, 85–89.CrossRefGoogle ScholarPubMed
Barrett, J. (1998). Cytochrome P450 in parasitic protozoa and helminths. Comparative Biochemistry and Physiology C-Pharmacology Toxicology & Endocrinology 121, 181–183.CrossRefGoogle ScholarPubMed
Barrett, J., Jefferies, J. R. and Brophy, P. M. (2000). Parasite proteomics. Parasitology Today 16, 400–403.CrossRefGoogle ScholarPubMed
Barrett, J., Saghir, N., Timanova, A., Clarke, K. and Brophy, P. M. (1997). Characterisation and properties of an intracellular lipid-binding protein from the tapeworm Moniezia expansa. European Journal of Biochemistry 250, 269–275.CrossRefGoogle ScholarPubMed
Bennuru, S., Semnani, R., Meng, Z., Ribeiro, J. M. C., Veenstra, T. D. and Nutman, T. B. (2009). Brugia malayi excreted/secreted proteins at the host/parasite interface: stage- and gender-specific proteomic profiling. PLoS Neglected Tropical Diseases 3 (4), e410.CrossRefGoogle ScholarPubMed
Bernal, D., Carpena, I., Espert, A. M., De La Rubia, J. E., Esteban, J. G., Toledo, R. and Marcilla, A. (2006). Identification of proteins in excretory/secretory extracts of Echinostoma friedi (Trematoda) from chronic and acute infections. Proteomics 6, 2835–2843.CrossRefGoogle ScholarPubMed
Bird, D. M., Williamson, V. M., Abad, P., Mccarter, J., Danchin, E. G. J., Castagnone-Sereno, P. and Opperman, C. H. (2009). The genomes of root-knot nematodes. Annual Review of Phytopathology 47, 333–351.CrossRefGoogle ScholarPubMed
Braschi, S., Curwen, R. S., Ashton, P. D., Verjovski-Almeida, S. and Wilson, A. (2006). The tegument surface membranes of the human blood parasite Schistosoma mansoni: A proteomic analysis after differential extraction. Proteomics 6, 1471–1482.CrossRefGoogle ScholarPubMed
Brennan, G. P., Fairweather, I., Trudgett, A., Hoey, E., Mccoy Mcconville, M., Meaney, M., Robinson, M., Mcferran, N., Ryan, L., Lanusse, C., Mottier, L., Alvarez, L., Solana, H., Virkel, G. and Brophy, P. M. (2007). Understanding triclabendazole resistance. Experimental and Molecular Pathology 82, 104–109.CrossRefGoogle ScholarPubMed
Brophy, P. M. and Barrett, J. (1990). Glutathione transferase in helminths. Parasitology 100, 345–349.CrossRefGoogle ScholarPubMed
Brophy, P. M., Crowley, P. and Barrett, J. (1990 a). Detoxification reactions of Fasciola hepatica cytosolic glutathione transferases. Molecular and Biochemical Parasitology 39, 155–162.CrossRefGoogle ScholarPubMed
Brophy, P. M., Crowley, P. and Barrett, J. (1990 b). Relative distribution of glutathione transferase, glyoxalase-I and glyoxalase-Ii in helminths. International Journal for Parasitology 20, 259–261.CrossRefGoogle ScholarPubMed
Castro-Borges, W., Simpson, D. M., Dowle, A., Curwen, R. S., Thomas-Oates, J., Beynon, R. J. and Wilson, R. A. (2011). Abundance of tegument surface proteins in the human blood fluke Schistosoma mansoni determined by QconCAT proteomics. Journal of Proteomics 74, 1519–1533.CrossRefGoogle ScholarPubMed
Chambers, E., Ryan, L. A., Hoey, E. M., Trudgett, A., Mcferran, N. V., Fairweather, I. and Timson, D. J. (2010). Liver fluke beta-tubulin isotype 2 binds albendazole and is thus a probable target of this drug. Parasitology Research 107, 1257–1264.CrossRefGoogle ScholarPubMed
Chemale, G., Morphew, R., Moxon, J. V., Morassuti, A. L., Lacourse, E. J., Barrett, J., Johnston, D. A. and Brophy, P. M. (2006). Proteomic analysis of glutathione transferases from the liver fluke parasite, Fasciola hepatica. Proteomics 6, 6263–6273.CrossRefGoogle ScholarPubMed
Chemale, G., Perally, S., Lacourse, E. J., Prescott, M. C., Jones, L. M., Ward, D., Meaney, M., Hoey, E., Brennan, G. P., Fairweather, I., Trudgett, A. and Brophy, P. M. (2010). Comparative proteomic analysis of triclabendazole response in the liver fluke Fasciola hepatica. Journal of Proteome Research 9, 4940–4951.CrossRefGoogle ScholarPubMed
Chemale, G., Van Rossum, A. J., Jefferies, J. R., Barrett, J., Brophy, P. M., Ferreira, H. B. and Zaha, A. (2003). Proteomic analysis of the larval stage of the parasite Echinococcus granulosus: Causative agent of cystic hydatid disease. Proteomics 3, 1633–1636.CrossRefGoogle ScholarPubMed
Chen, C.-K., Leung, S. S. F., Guilbert, C., Jacobson, M. P., Mckerrow, J. H. and Podust, L. M. (2010). Structural characterization of CYP51 from Trypanosoma cruzi and Trypanosoma brucei bound to the antifungal drugs posaconazole and fluconazole. PLoS Neglected Tropical Diseases 4 (4), e651.CrossRefGoogle Scholar
Cheng, G. F., Lin, J. J., Feng, X. G., Fu, Z. Q., Jin, Y. M., Yuan, C. X., Zhou, Y. C. and Cai, Y. M. (2005). Proteomic analysis of differentially expressed proteins between the male and female worm of Schistosoma japonicum after pairing. Proteomics 5, 511–521.CrossRefGoogle ScholarPubMed
Craig, H., Wastling, J. M. and Knox, D. P. (2006). A preliminary proteomic survey of the in vitro excretory/secretory products of fourth-stage larval and adult Teladorsagia circumcincta. Parasitology 132, 535–543.CrossRefGoogle ScholarPubMed
Cuervo, P., De Jesus, J. B., Junqueira, M., Mendonca-Lima, L., Gonzalez, L. J., Betancourt, L., Grimaldi, G. Jr., Domont, G. B., Fernandes, O. and Cupolillo, E. (2007). Proteome analysis of Leishmania (Viannia) braziliensis by two-dimensional gel electrophoresis and mass spectrometry. Molecular and Biochemical Parasitology 154, 6–21.CrossRefGoogle ScholarPubMed
Curwen, R. S., Ashton, P. D., Johnston, D. A. and Wilson, R. A. (2004). The Schistosoma mansoni soluble proteome: a comparison across four life-cycle stages. Molecular and Biochemical Parasitology 138, 57–66.CrossRefGoogle ScholarPubMed
Cvilink, V., Lamka, J. and Skalova, L. (2009). Xenobiotic metabolizing enzymes and metabolism of anthelminthics in helminths. Drug Metabolism Reviews 41, 8–26.CrossRefGoogle ScholarPubMed
Cvilink, V., Skalova, L., Szotakova, B., Lamka, J., Kostiainen, R. and Ketola, R. A. (2008). LC-MS-MS identification of albendazole and flubendazole metabolites formed ex vivo by Haemonchus contortus. Analytical and Bioanalytical Chemistry 391, 337–343.CrossRefGoogle ScholarPubMed
Daborn, P. J., Yen, J. L., Bogwitz, M. R., Le Goff, G., Feil, E., Jeffers, S., Tijet, N., Perry, T., Heckel, D., Batterham, P., Feyereisen, R., Wilson, T. G. and French-Constant, R. H. (2002). A single P450 allele associated with insecticide resistance in Drosophila. Science 297, 2253–2256.CrossRefGoogle ScholarPubMed
Devine, C., Brennan, G. P., Lanusse, C. E., Alvarez, L. I., Trudgett, A., Hoey, E. and Fairweather, I. (2010). Inhibition of cytochrome P450-mediated metabolism enhances ex vivo susceptibility of Fasciola hepatica to triclabendazole. Parasitology 137, 871–880.CrossRefGoogle ScholarPubMed
Dieterich, C., Clifton, S. W., Schuster, L. N., Chinwalla, A., Delehaunty, K., Dinkelacker, I., Fulton, L., Fulton, R., Godfrey, J., Minx, P., Mitreva, M., Roeseler, W., Tian, H., Witte, H., Yang, S.-P., Wilson, R. K. and Sommer, R. J. (2008). The Pristionchus pacificus genome provides a unique perspective on nematode lifestyle and parasitism. Nature Genetics 40, 1193–1198.CrossRefGoogle ScholarPubMed
Greetham, D., Morgan, C., Campbell, A. M., Van Rossum, A. J., Barrett, J. and Brophy, P. M. (2004). Evidence of glutathione transferase complexing and signaling in the model nematode Caenorhabdtis elegans using a pull-down proteomic assay. Proteomics 4, 1989–1995.CrossRefGoogle Scholar
Hart, E. H., Morphew, R. M., Millares, P., Wolf, B. T., Brophy, P. M. and Hamilton, J. V. (2012). The soluble proteome phenotype of ivermectin resistant and ivermectin susceptible female Haemonchus contortus compared. Veterinary Parasitology (In press).CrossRefGoogle ScholarPubMed
Hernandez-Gonzalez, A., Valero, M. L., Sanchez Del Pinto, M., Oleaga, A. and Siles-Lucas, M. (2010). Proteomic analysis of in vitro newly excysted juveniles from Fasciola hepatica. Molecular and Biochemical Parasitology 172, 121–128.CrossRefGoogle ScholarPubMed
Hewitson, J. P., Harcus, Y., Murray, J., Van Agtmaal, M., Filbey, K. J., Grainger, J. R., Bridgett, S., Blaxter, M. L., Ashton, P. D., Ashford, D. A., Curwen, R. S., Wilson, R. A., Dowle, A. A. and Maizels, R. M. (2011). Proteomic analysis of secretory products from the model gastrointestinal nematode Heligmosomoides polygyrus reveals dominance of Venom Allergen-Like (VAL) proteins. Journal of Proteomics 74, 1573–1594.CrossRefGoogle ScholarPubMed
Hoeckner, M., Dallinger, R. and Stuerzenbaum, S. R. (2011). Nematode and snail metallothioneins. Journal of Biological Inorganic Chemistry 16, 1057–1065.CrossRefGoogle Scholar
Jefferies, J. R., Campbell, A. M., Van Rossum, A. J., Barrett, J. and Brophy, P. M. (2001). Proteomic analysis of Fasciola hepatica excretory-secretory products. Proteomics 1, 1128–1132.3.0.CO;2-0>CrossRefGoogle ScholarPubMed
Jones, L. M., Staffa, K., Perally, S., Lacourse, E. J., Brophy, P. M. and Hamilton, J. V. (2010). Proteomic analyses of Caenorhabditis elegans dauer larvae and long-lived daf-2 mutants implicates a shared detoxification system in longevity assurance. Journal of Proteome Research 9, 2871–2881.CrossRefGoogle ScholarPubMed
Ju, J.-W., Joo, H.-N., Lee, M.-R., Cho, S.-H., Cheun, H.-I., Kim, J.-Y., Lee, Y.-H., Lee, K.-J., Sohn, W.-M., Kim, D.-M., Kim, I.-C., Park, B. C. and Kim, T.-S. (2009). Identification of a serodiagnostic antigen, legumain, by immunoproteomic analysis of excretory-secretory products of Clonorchis sinensis adult worms. Proteomics 9, 3066–3078.CrossRefGoogle ScholarPubMed
Kaminsky, R., Ducray, P., Jung, M., Clover, R., Rufener, L., Bouvier, J., Weber, S. S., Wenger, A., Wieland-Berghausen, S., Goebel, T., Gauvry, N., Pautrat, F., Skripsky, T., Froelich, O., Komoin-Oka, C., Westlund, B., Sluder, A. and Maeser, P. (2008). A new class of anthelmintics effective against drug-resistant nematodes. Nature 452, 176–180.CrossRefGoogle ScholarPubMed
Keiser, J. and Utzinger, J. (2010). The drugs we have and the drugs we need against major helminth infections. In Advances in Parasitology, Vol 73: Important Helminth Infections in Southeast Asia: Diversity and Potential for Control and Elimination, Pt B, Vol. 73 pp. 197–230.Google ScholarPubMed
Kerboeuf, D., Soubieux, D., Guilluy, R., Brazier, J. L. and Riviere, J. L. (1995). In vivo metabolism of aminopyrine by the larvae of the helminth Heligmosomoides polygyrus. Parasitology Research 81, 302–304.CrossRefGoogle ScholarPubMed
Knudsen, G. M., Medzihradszky, K. F., Lim, K. C., Hansell, E. and Mckerrow, J. H. (2005). Proteomic analysis of Schistosoma mansoni cercarial secretions. Molecular & Cellular Proteomics 4, 1862–1875.CrossRefGoogle ScholarPubMed
Kohler, P. and Bachmann, R. (1981). Intestinal tubulin as possible target for the chemotherapeutic action of mebendazole in parasitic nematodes. Molecular and Biochemical Parasitology 4, 325–336.CrossRefGoogle ScholarPubMed
Kotze, A. C., Dobson, R. J. and 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. Veterinary Parasitology 136, 275–282.CrossRefGoogle ScholarPubMed
Kulas, J., Schmidt, C., Rothe, M., Schunck, W.-H. and Menzel, R. (2008). Cytochrome P450-dependent metabolism of eicosapentaenoic acid in the nematode Caenorhabditis elegans. Archives of Biochemistry and Biophysics 472, 65–75.CrossRefGoogle ScholarPubMed
Kwa, M. S. G., Veenstra, J. G., Vandijk, M. and Roos, M. H. (1995). Beta-tubulin genes from the parasitic nematode Haemonchus contortus modulate drug-resistance in Caenorhabditis elegans. Journal of Molecular Biology 246, 500–510.CrossRefGoogle ScholarPubMed
Lacourse, E. J., Perally, S., Hernandez-Viadel, M., Wright, H. A. and Brophy, P. M. (2008). A proteomics approach to quantify protein levels following RNA interference: Case study with glutathione transferase superfamily from the model metazoan Caenorhabditis elegans. Journal of Proteome Research 7, 3314–3318.CrossRefGoogle ScholarPubMed
Lacourse, J. E., Perally, S., Morphew, R. M., Moxon, J. V., Prescott, M. C., Dowling, D., O'neill, S. M., Williams, D. J. L., Kipar, A., Hetzel, U., Hoey, E., Zafra, R., Buffoni, L., Arevalo, J. P. and Brophy, P. M. (2012). Sigma class glutathione transferase of the liver fluke Fasciola hepatica. PLoS Neglected Tropical Diseases 6 (5), e1666.CrossRefGoogle ScholarPubMed
Laing, S. T., Ivens, A., Laing, R., Ravikumar, S., Butler, V., Woods, D. J. and Gilleard, J. S. (2010). Characterization of the xenobiotic response of Caenorhabditis elegans to the anthelmintic drug albendazole and the identification of novel drug glucoside metabolites. Biochemical Journal 432, 505–514.CrossRefGoogle Scholar
Laschuk, A., Monteiro, K. M., Vidal, N. M., Pinto, P. M., Duran, R., Cervenanski, C., Zaha, A. and Ferreira, H. B. (2011). Proteomic survey of the cestode Mesocestoides corti during the first 24 hours of strobilar development. Parasitology Research 108, 645–656.CrossRefGoogle ScholarPubMed
Lee, W. C. and Lee, K. H. (2004). Applications of affinity chromatography in proteomics. Analytical Biochemistry 324, 1–10.CrossRefGoogle ScholarPubMed
Lindblom, T. H. and Dodd, A. K. (2009). Xenobiotic detoxification in the nematode Caenorhabditis elegans Journal of Experimental Zoology Part a-Ecological Genetics and Physiology 311A, 312–312.CrossRefGoogle Scholar
Mathieson, W. and Wilson, R. A. (2010). A comparative proteomic study of the undeveloped and developed Schistosoma mansoni egg and its contents: The miracidium, hatch fluid and secretions. International Journal for Parasitology 40, 617–628.CrossRefGoogle ScholarPubMed
McKellar, Q. A. and Jackson, F. (2004). Veterinary anthelmintics: old and new. Trends in Parasitology 20, 456–461.CrossRefGoogle ScholarPubMed
Millares, P., Lacourse, E. J., Perally, S., Ward, D., Prescott, M. C., Hodgkinson, J., Brophy, P. M. and Rees, H. H. (2012). Proteomic profiling and protein Identification by MALDI-TOF mass spectrometry in unsequenced parasitic nematodes. Plos One 7, (3). e33590.CrossRefGoogle ScholarPubMed
Morgan, C., Lacourse, E. J., Rushbrook, B. J., Greetham, D., Hamilton, J. V., Barrett, J., Bailey, K. and Brophy, P. M. (2006). Plasticity demonstrated in the proteome of a parasitic nematode within the intestine of different host strains. Proteomics 6, 4633–4645.CrossRefGoogle ScholarPubMed
Morphew, R. M., Wright, H. A., Lacourse, E. J., Woods, D. J. and Brophy, P. M. (2007). Comparative proteomics of excretory-secretory proteins released by the liver fuke Fasciola hepatica in sheep host bile and during in vitro culture ex-host. Molecular and Cellular Proteomics 6, 963–972.CrossRefGoogle Scholar
Moxon, J. V., Lacourse, E. J., Wright, H. A., Perally, S., Prescott, M. C., Gillard, J. L., Barrett, J., Hamilton, J. V. and Brophy, P. M. (2010). Proteomic analysis of embryonic Fasciola hepatica: Characterization and antigenic potential of a developmentally regulated heat shock protein. Veterinary Parasitology 169, 62–75.CrossRefGoogle ScholarPubMed
Mueller, P., Warr, E., Stevenson, B. J., Pignatelli, P. M., Morgan, J. C., Steven, A., Yawson, A. E., Mitchell, S. N., Ranson, H., Hemingway, J., Paine, M. J. I. and Donnelly, M. J. (2008). Field-caught permethrin-resistant Anopheles gambiae overexpress CYP6P3, a P450 that metabolises pyrethroids. Plos Genetics 4 (11), e1000286.CrossRefGoogle Scholar
Mulvenna, J., Hamilton, B., Nagaraj, S. H., Smyth, D., Loukas, A. and Gorman, J. J. (2009 a). Proteomics analysis of the excretory/secretory component of the blood-feeding stage of the hookworm, Ancylostoma caninum. Molecular & Cellular Proteomics 8, 109–121.CrossRefGoogle ScholarPubMed
Mulvenna, J., Moertel, L., Jones, M. K., Nawaratna, S., Lovas, E. M., Gobert, G. N., Colgrave, M., Jones, A., Loukas, A. and Mcmanus, D. P. (2009 b). Exposed proteins of the Schistosoma japonicum tegument. International Journal for Parasitology 40, 543–554.CrossRefGoogle ScholarPubMed
Mulvenna, J., Sripa, B., Brindley, P. J., Gorman, J., Jones, M. K., Colgrave, M. L., Jones, A., Nawaratna, S., Laha, T., Suttiprapa, S., Smout, M. J. and Loukas, A. (2010). The secreted and surface proteomes of the adult stage of the carcinogenic human liver fluke Opisthorchis viverrini. Proteomics 10, 1063–1078.CrossRefGoogle ScholarPubMed
O'leary, K. A. and Tracy, J. W. (1991). Schistosoma mansoni - glutathione S-transferase-catalyzed detoxication of dichlorvos. Experimental Parasitology 72, 355–361.CrossRefGoogle ScholarPubMed
Pérez-Sánchez, R., Ramajo-Hernández, A., Ramajo-Martín, V. and Oleaga, A. (2006). Proteomic analysis of the tegument and excretory-secretory products of adult Schistosoma bovis worms. Proteomics 6, S226–S236.CrossRefGoogle ScholarPubMed
Precious, W. Y. and Barrett, J. (1989). The possible absence of cytochrome P-450 linked xenobiotic metabolism in helminths. Biochimica et Biophysica Acta 992, 215–222.CrossRefGoogle ScholarPubMed
Prichard, R. K., Von Samson-Himmelstjerna, G., Blackhall, W. J. and Geary, T. G. (2007). Foreword: Towards markers for anthelmintic resistance in helminths of importance in animal and human health. Parasitology 134, 1073–1076.CrossRefGoogle ScholarPubMed
Prieto, J. H., Koncarevic, S., Park, S. K., Yates, J., Iii and Becker, K. (2008). Large-scale differential proteome analysis in Plasmodium falciparum under drug treatment. Plos One 3 (12), e4098.CrossRefGoogle ScholarPubMed
Rebello, K. M., Barros, J. S. L., Mota, E. M., Carvalho, P. C., Perales, J., Lenzi, H. L. and Neves-Ferreira, A. G. C. (2011). Comprehensive proteomic profiling of adult Angiostrongylus costaricensis, a human parasitic nematode. Journal of Proteomics 74, 1545–1559.CrossRefGoogle ScholarPubMed
Reichert, K. and Menzel, R. (2005). Expression profiling of five different xenobiotics using a Caenorhabditis elegans whole genome microarray. Chemosphere 61, 229–237.CrossRefGoogle ScholarPubMed
Robinson, M. W., Lawson, J., Trudgett, A., Hoey, E. M. and Fairweather, I. (2004). The comparative metabolism of triclabendazole sulphoxide by triclabendazole-susceptible and triclabendazole-resistant Fasciola hepatica. Parasitology Research 92, 205–210.CrossRefGoogle ScholarPubMed
Saeed, H. M., Mostafa, M. H., O'connor, P. J., Rafferty, J. A. and Doenhoff, M. J. (2002). Evidence for the presence of active cytochrome P450 systems in Schistosoma mansoni and Schistosoma haematobium adult worms. FEBS Letters 519, 205–209.CrossRefGoogle ScholarPubMed
Simmer, F., Moorman, C., Van Der Linden, A. M., Kuijk, E., Van Den Berghe, P. V. E., Kamath, R. S., Fraser, A. G., Ahringer, J. and Plasterk, R. H. A. (2003). Genome-wide RNAi of C. elegans using the hypersensitive rrf-3 strain reveals novel gene functions. Plos Biology 1, 77–84.CrossRefGoogle ScholarPubMed
Soblik, H., Younis, A. E., Mitreva, M., Renard, B. Y., Kirchner, M., Geisinger, F., Steen, H. and Brattig, N. W. (2011). Life cycle stage-resolved proteomic analysis of the excretome/secretome from Strongyloides ratti-identification of stage-specific proteases. Molecular & Cellular Proteomics 10, (12): M111.010157.CrossRefGoogle ScholarPubMed
Sotillo, J., Luz Valero, M., Sanchez Del Pino, M. M., Fried, B., Guillermo Esteban, J., Marcilla, A. and Toledo, R. (2010). Excretory/secretory proteome of the adult stage of Echinostoma caproni. Parasitology Research 107, 691–697.CrossRefGoogle ScholarPubMed
Sutherland, I. A. and Leathwick, D. M. (2011). Anthelmintic resistance in nematode parasites of cattle: a global issue/ Trends in Parasitology 27, 176–181.CrossRefGoogle ScholarPubMed
Van Rossum, A. J., Brophy, P. M., Tait, A., Barrett, J. and Jefferies, J. R. (2001). Proteomic identification of glutathione S-transferases from the model nematode Caenorhabditis elegans. Proteomics 1, 1463–1468.3.0.CO;2-H>CrossRefGoogle ScholarPubMed
Van Rossum, A. J., Jefferies, J. R., Rijsewijk, F. A. M., Lacourse, E. J., Teesdale-Spittle, P., Barrett, J., Tait, A. and Brophy, P. M. (2004). Binding of hematin by a new class of glutathione transferase from the blood-feeding parasitic nematode Haemonchus contortus. Infection and Immunity 72, 2780–2790.CrossRefGoogle ScholarPubMed
Wang, Y., Cheng, Z., Lu, X. and Tang, C. (2009). Echinococcus multilocularis: Proteomic analysis of the protoscoleces by two-dimensional electrophoresis and mass spectrometry. Experimental Parasitology 123, 162–167.CrossRefGoogle ScholarPubMed
Wilson, R. A., Wright, J. M., De Castro-Borges, W., Parker-Manuel, S. J., Dowle, A. A., Ashton, P. D., Young, N. D., Gasser, R. B. and Spithill, T. W. (2011). Exploring the Fasciola hepatica tegument proteome. International Journal for Parasitology 41, 1347–1359.CrossRefGoogle ScholarPubMed
Wolstenholme, A. J., Fairweather, I., Prichard, R., Von Samson-Himmelstjerna, G. and Sangster, N. C. (2004). Drug resistance in veterinary helminths. Trends in Parasitology 20, 469–476.CrossRefGoogle ScholarPubMed
Yan, F., Xu, L., Liu, L., Yan, R., Song, X. and Li, X. (2010). Immunoproteomic analysis of whole proteins from male and female adult Haemonchus contortus. Veterinary Journal 185, 174–179.CrossRefGoogle ScholarPubMed
Yatsuda, A. P., Krijgsveld, J., Cornelissen, A., Heck, A. J. R. and De Vries, E. (2003). Comprehensive analysis of the secreted proteins of the parasite Haemonchus contortus reveals extensive sequence variation and differential immune recognition. Journal of Biological Chemistry 278, 16941–16951.CrossRefGoogle ScholarPubMed