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Forty years of helminth biochemistry

Published online by Cambridge University Press:  06 March 2009

J. BARRETT
J. BARRETT*
Affiliation:
IBERS, University of Aberystwyth, Aberystwyth, Ceredigion SY23 3DA, UK
*
*E-mail: [email protected]
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Summary

This review describes some of the developments in helminth biochemistry that have taken place over the last 40 years. Since the early 1970s the main anabolic and catabolic pathways in parasitic helminths have been worked out. The mode of action of the majority of anthelmintics is now known, but in many cases the mechanisms of resistance remain elusive. Developments in helminth biochemistry have depended heavily on developments in other areas. High throughput methods such as proteomics, transcriptomics and genome sequencing are now generating vast amounts of new data. The challenge for the future is to interpret and understand the biological relevance of this new information.

Keywords

helminth biochemistrymetabolic pathwaysproteomics
Type
Research Article
Information
Parasitology , Volume 136 , Special Issue 12: Special Centenary Issue – Parasitology 1908–2008 , October 2009 , pp. 1633 - 1642
Copyright
Copyright © 2009 Cambridge University Press

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References

REFERENCES

Adcock, H. J., Brophy, P. M., Teesdale-Spittle, P. H. and Buckberry, L. D. (2000). Purification and characterisation of a novel cysteine conjugate β-lyase from the tapeworm Moniezia expansa. International Journal for Parasitology 30, 567–571.CrossRefGoogle ScholarPubMed
Ash, H. L. and Read, C. P. (1975). Membrane transport in Schistosoma mansoni – transport of amino acids by adult males. Experimental Parasitology 38, 123–135.CrossRefGoogle Scholar
Barrett, J. (1968). The effect of temperature on the development and survival of the infective larvae of Strongyloides ratti Sandground, 1925. Parasitology 58, 641–651.CrossRefGoogle ScholarPubMed
Barrett, J. (1969). The effect of physical factors on the rate of respiration of the infective larvae of Strongyloides ratti Sandground, 1925. Parasitology 59, 859–875.CrossRefGoogle ScholarPubMed
Barrett, J. (1973). Nucleoside triphosphate metabolism in the muscle tissue of Ascaris lumbricoides (Nematoda). International Journal for Parasitology 3, 393–400.CrossRefGoogle ScholarPubMed
Barrett, J. (1981). Biochemistry of Parasitic Helminths. Macmillan, London and Basingstoke, UK.CrossRefGoogle Scholar
Barrett, J. (1984). The anaerobic end-products of helminths. Parasitology 88, 179–198.CrossRefGoogle ScholarPubMed
Barrett, J. (1988). The application of control analysis to helminth pathways. Parasitology 97, 355–362.CrossRefGoogle ScholarPubMed
Barrett, J. (1991). Amino acid metabolism in helminths. Advances in Parasitology 30, 39–105.CrossRefGoogle ScholarPubMed
Barrett, J. (1995). Helminth glutathione transferases. Helminthologia 32, 125–128.Google Scholar
Barrett, J. (1997). Helminth detoxification mechanisms. Journal of Helminthology 71, 85–89.CrossRefGoogle ScholarPubMed
Barrett, J. and Butterworth, P. E. (1984). Acetaldehyde formation by mitochondria from the free-living nematode Panagrellus redivivus. The Biochemical Journal 221, 535–540.CrossRefGoogle ScholarPubMed
Barrett, J. and Körting, W. (1976). Studies on beta-oxidation in the adult liver fluke Fasciola hepatica. International Journal for Parasitology 6, 155–157.CrossRefGoogle ScholarPubMed
Barrett, J. and Lloyd, G. M. (1981). A novel phosphagen phosphotransferase in the plerocercoids of Schistocephalus solidus (Cestoda: Pseudophyllidea). Parasitology 82, 11–16.CrossRefGoogle ScholarPubMed
Barrett, J. and Precious, W. Y. (1995). Application of metabolic control analysis to the pathways of carbohydrate breakdown in Hymenolepis diminuta. International Journal for Parasitology 25, 431–436.CrossRefGoogle Scholar
Barrett, J. and Saghir, N. (1999). Lipid binding proteins in parasitic helminths. Research and Reviews in Parasitology 59, 107–112.Google Scholar
Barrett, J., Ward, C. W. and Fairbairn, D. (1970 a). The glyoxylate cycle and the conversion of triglycerides to carbohydrates in the developing eggs of Ascaris lumbricoides. Comparative Biochemistry and Physiology 35, 577–586.CrossRefGoogle Scholar
Barrett, J., Cain, G. D. and Fairbairn, D. (1970 b). Sterols in Ascaris lumbricoides (Nematoda), Macracanthorhynchus hirudinaceus and Moniliformis dubius (Acanthocephala) and Echinostoma revolutum (Trematoda). Journal of Parasitology 56, 1004–1008.CrossRefGoogle ScholarPubMed
Barrett, J., Behm, C. A., Kolhagen, S. and Bryant, C. (1987). Propanol formation in Haemonchus contortus. Parasitology 95, 661.Google Scholar
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
Barrett, J., Brophy, P. M. and Hamilton, J. V. (2005). Analysing proteomic data. International Journal for Parasitology 35, 543–553.CrossRefGoogle ScholarPubMed
Behm, C. A. and Bryant, C. (1975). Studies of regulatory metabolism in Moniezia expansa: the role of phosphoenolpyruvate carboxykinase. International Journal for Parasitology 5, 347–354.CrossRefGoogle ScholarPubMed
Boyle, J. P., Wu, X.-J., Shoemaker, D. B. and Yoshino, T. P. (2003). Using RNA interference to manipulate endogenous gene expression in Schistosoma mansoni sporocysts. Molecular and Biochemical Parasitology 128, 205–215.CrossRefGoogle ScholarPubMed
von Brand, T. (1966). Biochemistry of Parasites. Academic Press, New York and London.Google Scholar
von Brand, T. (1972). Glimpses at the early days of parasite biochemistry. In Comparative Biochemistry of Parasites (ed. Van den Bossche, H.) pp. 1–23. Academic Press, New York and London.Google Scholar
Braschi, S., Curwen, R. S., Ashton, P. D., Verjowski-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
Britton, C. and Murray, L. (2006). Using Caenorhabditis elegans for functional analysis of genes of parasitic nematodes. International Journal for Parasitology 36, 651–659.CrossRefGoogle ScholarPubMed
Brophy, P. M. and Barrett, J. (1990 a). Glutathione transferase in helminths. Parasitology 100, 345–349.CrossRefGoogle ScholarPubMed
Brophy, P. M. and Barrett, J. (1990 b). Strategies for detoxification of aldehydic products of lipid peroxidation in helminths. Molecular and Biochemical Parasitology 42, 205–212.CrossRefGoogle ScholarPubMed
Brophy, P. M., Crowley, P. and Barrett, J. (1990). Relative distribution of glutathione transferase, Glyoxalase I and Glyoxalase II in helminths. International Journal for Parasitology 20, 259–261.CrossRefGoogle ScholarPubMed
Bryant, C. (1978). The regulation of respiratory metabolism in parasitic helminths. Advances in Parasitology 16, 311–331.CrossRefGoogle ScholarPubMed
Buckingham, S. (2004). Data's future shock. Nature, London 428, 774–777.CrossRefGoogle ScholarPubMed
Butterworth, P. E. and Barrett, J. (1985). Anaerobic metabolism in the free-living nematode Panagrellus redivivus. Physiological Zoology 58, 9–17.CrossRefGoogle Scholar
Chemale, G., Morphew, R., Moxon, V., Morrasuti, 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
Epps, W., Weiner, H. and Beuding, E. (1950). Production of steam volatile acids by bacteria- free Ascaris lumbricoides. Journal of Infectious Disease 87, 149–151.CrossRefGoogle ScholarPubMed
Esch, G. W. and Smyth, J. D. (1976). Studies on the in vitro culture of Taenia crassiceps. International Journal for Parasitology 6, 143–149.CrossRefGoogle ScholarPubMed
Grosshans, H. and Filipowicz, W. (2008). Molecular biology: the expanding world of small RNAs. Nature, London 451, 414–416.CrossRefGoogle ScholarPubMed
Heinrich, R., Rapoport, S. M. and Rapoport, T. (1977). Metabolic regulation and mathematical models. Progress in Biophysics and Molecular Biology 32, 1–82.CrossRefGoogle ScholarPubMed
Islam, M. K., Miyoshi, T., Yamada, M., Alim, M. A., Huang, X., Motobu, M. and Tsuji, N. (2006). Effect of piperazine (diethylenediamine) on the moulting, proteome expression and pyrophosphatase activity of Ascaris suum lung-stage larvae. Acta Tropica 99, 208–217.CrossRefGoogle ScholarPubMed
Kacser, H. and Burns, J. A. (1979). Molecular democracy: who shares the controls? Biochemical Society Transactions 7, 1149–1160.CrossRefGoogle ScholarPubMed
Kennedy, M. W. (2000). The nematode polyprotein allergens/antigens. Parasitology Today 16, 373–380.CrossRefGoogle ScholarPubMed
Köhler, P., Bryant, C. and Behm, C. A. (1978). ATP synthesis in a succinate decarboxylase system from Fasciola hepatica mitochondria. International Journal for Parasitology 8, 399–404.CrossRefGoogle Scholar
Komuniecki, R., Komuniecki, P. R. and Saz, H. J. (1981). Pathway of formation of branched-chain volatile fatty acids in Ascaris mitochondria. Journal of Parasitology 67, 841–846.CrossRefGoogle ScholarPubMed
Körting, W. and Fairbairn, D. (1972). Anaerobic energy metabolism in Moniliformis dubius (Acanthocephala). Journal of Parasitology 58, 45–50.CrossRefGoogle ScholarPubMed
Lender, M., Doligalska, M., Lucius, R. and Hartmann, S. (2008). Attempts to establish RNA interference in the parasitic nematode Heligmosomoides polygyrus. Molecular and Biochemical Parasitology 161, 21.CrossRefGoogle Scholar
Lloyd, G. M. and Barrett, J. (1983). Fasciola hepatica: effect of quinolinic acid and 3-mercaptopicolonic acid on phosphoenolpyruvate carboxykinase and end-product formation. Experimental Parasitology 56, 259–265.CrossRefGoogle ScholarPubMed
Mansour, T. E. (1962). Effect of serotonin on glycolysis in homogenates of liver fluke Fasciola hepatica. Journal of Pharmacology and Experimental Therapeutics 135, 94–101.Google ScholarPubMed
McGonigle, L., Mousley, A., Marks, N. J., Brennan, G. P., Dalton, J. P., Spithill, T. W., Day, T. A. and Maule, A. G. (2008). The silencing of cysteine proteases in Fasciola hepatica newly excysted juveniles using RNA interference reduces gut penetration. International Journal for Parasitology 38, 149–155.CrossRefGoogle ScholarPubMed
McManus, D. P. and Smyth, J. D. (1982). Intermediary carbohydrate metabolism in protoscoleces of Echinococcus granulosus (horse and sheep strains) and E. multilocularis. Parasitology 84, 351–366.CrossRefGoogle ScholarPubMed
Meyer, F., Meyer, H. and Bueding, E. (1970). Lipid metabolism in parasitic and free-living flatworms, Schistsoma mansoni and Dugesia dorotocephala. Biochimica et Biophysica Acta 210, 257–266.CrossRefGoogle Scholar
Mied, P. A. and Bueding, E. (1979). Glycogen synthase of Hymenolepis diminuta. 1. Allosteric activation and inhibition. Journal of Parasitology 65, 14–24.CrossRefGoogle ScholarPubMed
Morgan, C., La Course, J. E., 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
Munir, W. A. and Barrett, J. (1985). The metabolism of xenobiotic compounds by Hymenolepis diminuta (Cestoda: Cyclophyllidea). Parasitology 91, 145–156.CrossRefGoogle Scholar
Nicholson, J. K., Holmes, E., Lindon, J. C. and Wilson, I. D. (2004). The challenges of modeling mammalian biocomplexity. Nature Biotechnology 22, 1268–1274.CrossRefGoogle ScholarPubMed
Pappas, P. W., Uglem, G. L. and Read, C. P. (1973). Influx of purines and pyrimidines across brush border of Hymenolepis diminuta. Parasitology 66, 525–538.CrossRefGoogle ScholarPubMed
Passey, R. F. and Fairbairn, D. (1957). The conversion of fat to carbohydrate during embryonation of Ascaris eggs. Canadian Journal of Biochemistry and Physiology 35, 511–525.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
Precious, W. Y. and Barrett, J. (1993). Quantification of the control of carbohydrate catabolism in the tapeworm Hymenolepis diminuta. Biochemistry and Cell Biology 71, 315–323.CrossRefGoogle ScholarPubMed
Pietrazack, S. M. and Saz, H. J. (1981). Succinate decarboxylation to propionate and the associated phosphorylation in Fasciola hepatica and Spirometra mansonoides. Molecular Biochemistry and Parasitology 3, 61–70.CrossRefGoogle Scholar
Prichard, R. K. (1976). Regulation of pyruvate kinase and phosphoenolpyruvate carboxykinase activity in adult Fasciola hepatica (Trematoda). International Journal for Parasitology 6, 227–233.CrossRefGoogle ScholarPubMed
Prichard, R. K. (2001). Genetic variability following selection of Haemonchus contortus with anthelmintics. Trends in Parasitology 17, 445–453.CrossRefGoogle ScholarPubMed
Rogers, W. P. and Lazarus, M. (1949). Glycolysis and related phosphorus metabolism in parasitic nematodes. Parasitology 39, 302–314.CrossRefGoogle ScholarPubMed
Schuller, D. J., Liu, Q., Kriksunov, I. A., Campbell, A. M., Barrett, J., Brophy, P. M. and Hao, Q. (2005). The crystal structure of a new class of glutathione transferase from the model human hookworm nematode Heligmosomoides polygyrus. Proteins: Structure, Function and Bioinformatics 61, 1024–1031.CrossRefGoogle ScholarPubMed
Smyth, J. D. and Davies, Z. (1975). In vitro suppression of segmentation in Echinococcus multilocularis with morphological transformation of protoscoleces into monozooic adults. Parasitology 71, 125–135.CrossRefGoogle ScholarPubMed
Starling, J. A., Allen, B. L., Kaeini, M. R., Payne, D. M., Blytt, H. J., Hofer, H. W. and Harris, B. G. (1982). Phosphofructokinase from Ascaris suum. Purification and properties. Journal of Biological Chemistry 257, 3795–3800.CrossRefGoogle Scholar
Stone, D. M. and Mansour, T. E. (1967). Phosphofructokinase in liver fluke Fasciola hepatica 2. Kinetic properties of the enzyme. Molecular Pharmacology 3, 177–187.Google ScholarPubMed
Van Rossum, A. J., Jefferies, J. R., Rijsewijk, F. A. M., La Course, E. J., Teesdale-Spittle, P., Barrett, J., Tait, A. and Brophy, P. M. (2004). Binding of haematin by a new class of glutathione transferase from the blood feeding parasitic nematode Haemonchus contortus. Infection and Immunity 72, 2780–2790.CrossRefGoogle ScholarPubMed
Vermeire, J. J., Taft, A. S., Hoffmann, K. F., Fitzpatrick, J. M. and Yoshino, T. P. (2006). Schistosoma mansoni: DNA microarray gene expression profiling during the miracidium-to-mother sporocyst transformation. Molecular and Biochemical Parasitology 147, 39–47.CrossRefGoogle ScholarPubMed
Viney, M. E. and Thompson, F. J. (2008). Two hypotheses to explain why RNA interference does not work in animal parasitic nematodes. International Journal for Parasitology 38, 43–47.CrossRefGoogle Scholar
Walker, J. and Barrett, J. (1991). Cystathionine β-synthase and γ-cystathionase in helminths. Parasitology Research 77, 709–713.CrossRefGoogle ScholarPubMed
Walker, J., Barrett, J. and Thong, K-W. (1992). The identification of a variant form of cystathionine β-synthase in nematodes. Experimental Parasitology 75, 415–424.CrossRefGoogle ScholarPubMed
Walker, J., Crowley, P., Moreman, A. D. and Barrett, J. (1993). Biochemical properties of cloned glutathione S-transferases from Schistosoma mansoni and Schistosoma japonicum. Molecular and Biochemical Parasitology 61, 255–264.CrossRefGoogle ScholarPubMed
Wang, Y. L., Utzinger, J., Xiao, S. H., Xue, J., Nicholson, J. K., Tanner, M., Singer, B. H. and Holmes, E. (2006). System level metabolic effects of a Schistosoma japonicum infection in the Syrian hamster. Molecular and Biochemical Parasitology 146, 1–9.CrossRefGoogle ScholarPubMed
Ward, C. W. and Fairbairn, D. (1970). Enzymes of beta-oxidation and the tricarboxylic acid cycle in adult Hymenolepis diminua (Cestoda) and Ascaris lumbricoides (Nematoda). Journal of Parasitology 56, 1009–1012.CrossRefGoogle Scholar
Wickramasinghe, S., Uda, K., Nagataki, M., Yatawara, L., Rajapakse, R. P. V. J., Watanabe, Y., Suzuki, T. and Agatsuma, T. (2007). Toxocara canis: molecular cloning, characterization, expression and comparison of the kinetics of cDNA-derived arginine kinase. Experimental Parasitology 117, 124–132.CrossRefGoogle ScholarPubMed
Wong, P. C. L. and Yeung, S. B. (1981). Pathways of purine ribonucleotide biosynthesis in the adult worm Metastrongylus apri (Nematoda Metastrongyloidea) from the pig lung. Molecular and Biochemical Parasitology 2, 285–293.CrossRefGoogle ScholarPubMed