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Reflections on the biochemistry of Echinococcus: past, present and future

  • D. P. McMANUS (a1)


This review discusses 5 of my earliest papers on the biochemistry of larval Echinococcus published in Parasitology in the 1970s and 1980s. Two of the publications consider aspects of the basic biochemistry, intermediary metabolism and the regulation of respiratory pathways in E. granulosus and E. multilocularis, and emphasize the existence of inter- and intra-species variation in their general metabolism. The third reports on the detailed biochemical analysis of the tegumental surface of the protoscolex of E. granulosus, and the final 2 papers describe the genomic cloning of Echinococcus DNA fragments and their use, along with other DNA markers, in molecular identification of E. granulosus isolates collected worldwide from areas endemic for hydatid disease. A number of years have elapsed since these publications in Parasitology and, in this Centenary Issue article, I reflect briefly on some of the subsequent studies undertaken in these research areas that have advanced the field. As well, I provide brief insight on new research directions, emphasizing the impact of molecular biology and associated techniques on future studies of Echinococcus and hydatid disease.


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Abbasi, I., Branzburg, A., Campos-Ponce, M., Abdel Hafez, S. K., Raoul, F., Craig, P. S. and Hamburger, J. (2003). Copro-diagnosis of Echinococcus granulosus infection in dogs by amplification of a newly identified repeated DNA sequence. American Journal of Tropical Medicine and Hygiene 69, 324330.
Agosin, M. (1968). Biochemistry and physiology of echinococcus. Bulletin of the World Health Organization 39, 115120.
Agosin, M. and Repetto, Y. (1965). Studies on the metabolism of Echinococcus granulosus. 8. The pathway to succinate in E. granulosus scolices. Comparative Biochemistry and Physiology 14, 299309.
Baz, A., Carol, H., Marco, M., Casabó, L., Jones, F., Dunne, D. and Nieto, A. (1998). Fc-binding molecules specific for human IgG1 and IgG3 are present in Echinococcus granulosus protoscoleces. Parasite Immunology 20, 399404.
Bonilla, M., Denicola, A., Novoselov, S. V., Turanov, A. A., Protasio, A., Izmendi, D., Gladyshev, V. N. and Salinas, G. (2008). Platyhelminth mitochondrial and cytosolic redox homeostasis is controlled by a single thioredoxin glutathione reductase and dependent on selenium and glutathione. Journal of Biological Chemistry 283, 1789817907.
Boufana, B. S., Campos-Ponce, M., Naidich, A., Buishi, I., Lahmar, S., Zeyhle, E., Jenkins, D. J., Combes, B., Wen, H., Xiao, N., Nakao, M., Ito, A., Qiu, J. and Craig, P. S. (2008). Evaluation of three PCR assays for the identification of the sheep strain (genotype 1) of Echinococcus granulosus in canid feces and parasite tissues. American Journal of Tropical Medicine and Hygiene 78, 777783.
Bowles, J., Blair, D. and McManus, D. P. (1992). Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Molecular and Biochemical Parasitology 54, 165174.
Bowles, J. and McManus, D. P. (1993). NADH dehydrogenase 1 gene sequences compared for species and strains of the genus Echinococcus. International Journal for Parasitology 23, 969972.
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, 14711482.
Braschi, S. and Wilson, R. A. (2006). Proteins exposed at the adult schistosome surface revealed by biotinylation. Molecular and Cellular Proteomics 5, 347356.
Bryant, C. (1975) Carbon dioxide utilisation, and the regulation of respiratory metabolic pathways in parasitic helminths. Advances in Parasitology 13, 3569.
Bryant, C. (1983). Intraspecies variation of energy metabolism in parasitic helminths. International Journal for Parasitology 13, 327332.
Camicia, F., Paredes, R., Chalar, C., Galanti, N., Kamenetzky, L., Gutierrez, A. and Rosenzvit, M. C. (2008). Sequencing, bioinformatic characterization and expression pattern of a putative amino acid transporter from the parasitic cestode Echinococcus granulosus. Gene 411, 19.
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, 16331636.
Craig, P. S., McManus, D. P., Lightowlers, M. W., Chabalogoity, J. A., Garcia, H. H., Gavidia, C. M., Gilman, R. H., Gonzalez, A. E., Lorca, M., Naquira, C., Nieto, A. and Schantz, P. M. (2007). Prevention and control of cystic echinococcosis. Lancet Infectious Diseases 7, 385394.
Deplazes, P., Dinkel, A. and Mathis, A. (2003). Molecular tools for studies on the transmission biology of Echinococcus multilocularis. Parasitology 127, S53S61.
Eckert, J. and Deplazes, P. (2004). Biological, epidemiological, and clinical aspects of echinococcosis, a zoonosis of increasing concern. Clinical Microbiology Reviews 17, 107135.
Esteves, A., Dallagiovanna, B. and Ehrlich, R. (1993). A developmentally regulated gene of Echinococcus granulosus codes for a 15.5-kilodalton polypeptide related to fatty acid binding proteins. Molecular and Biochemical Parasitology 58, 215222.
González, G., Spinelli, P., Lorenzo, C., Hellman, U., Nieto, A., Willis, A. and Salinas, G. (2000). Molecular characterization of P-29, a metacestode-specific component of Echinococcus granulosus which is immunologically related to, but distinct from, antigen 5. Molecular and Biochemical Parasitology 105, 177184.
Hatch, C. (1975). Observations on the epidemiology of equine hydatidosis in Ireland. Irish Veterinary Journal 29, 155157.
Hou, Q. L., Wang, H., Zhang, Z. Z., Cao, W. Y., Zhang, F. C. and Zhang, W. B. (2007). [Immunolocalization of the antioxidant protein TPx of Echinococcus granulosus] [Article in Chinese] Xi Bao Yu Fen Zi Mian Yi Xue Za Zhi 23, 9981000.
Jakobsson, E., Alvite, G., Bergfors, T., Esteves, A. and Kleywegt, G. J. (2003). The crystal structure of Echinococcus granulosus fatty-acid-binding protein 1. Biochimica et Biophysica Acta 1649, 4050.
Le, T. H., Pearson, M. S., Blair, D., Dai, N., Zhang, L. H. and McManus, D. P. (2002). Complete mitochondrial genomes confirm the distinctiveness of the horse-dog and sheep-dog strains of Echinococcus granulosus. Parasitology 124, 97112.
Macpherson, C. N. L. and McManus, D. P. (1982). A comparative study of Echinococcus granulosus from human and animal hosts in Kenya using isoelectric focusing and isoenzyme analysis. International Journal for Parasitology 12, 515521.
Matsumoto, J., Sakamoto, K., Shinjyo, N., Kido, Y., Yamamoto, N., Yagi, K., Miyoshi, H., Nonaka, N., Katakura, K., Kita, K. and Oku, Y. (2008). Anaerobic NADH-fumarate reductase system is predominant in the respiratory chain of Echinococcus multilocularis, providing a novel target for the chemotherapy of alveolar echinococcosis. Antimicrobial Agents and Chemotherapy 52, 164170.
McManus, D. P. (1981). A biochemical study of adult and cystic stages of Echinococcus granulosus of human and animal origin from Kenya. Journal of Helminthology 55, 2127.
McManus, D. P. (2002). The molecular epidemiology of Echinococcus granulosus and cystic hydatid disease. Transactions of the Royal Society of Tropical Medicine and Hygiene 96 (Suppl. 1), S151S157.
McManus, D. P. (2006). Molecular characterization of taeniid cestodes. Parasitology International 55 (Suppl.), S31S37.
McManus, D. P. and Barrett, N. J. (1985). Isolation, fractionation and partial characterisation of the tegumental surface from protoscoleces of the hydatid organisms, Echinococcus granulosus. Parasitology 90, 111129.
McManus, D. P. and Bryant, C. A. (1995). Biochemistry, physiology and molecular biology of Echinococcus. In Echinococcus and Hydatid Disease (ed. Thompson, R. C. A. and Lymbery, A. J.),pp. 135181. CAB International, Wallingford, UK.
McManus, D. P., Knight, M. and Simpson, A. J. G. (1985). Isolation and characterisation of nucleic acids from the hydatid organisms, Echinococcus spp. (Cestoda). Molecular and Biochemical Parasitology 16, 251266.
McManus, D. P. and Rishi, A. K. (1989). Genetic heterogeneity within Echinococcus granulosus: isolates from different hosts and geographical areas characterized with DNA probes. Parasitology 99, 1729.
McManus, D. P. and Simpson, A. J. G. (1985). Identification of the Echinococcus (hydatid disease) organisms using cloned DNA markers. Molecular and Biochemical Parasitology 17, 171178.
McManus, D. P. and Smyth, J. D. (1978). Differences in the chemical composition and carbohydrate metabolism of Echinococcus granulosus (horse and sheep strains) and E. multilocularis. Parasitology 77, 103109.
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, 351366.
McManus, D. P. and Thompson, R. C. A. (2003). Molecular epidemiology and taxononomy of cystic echinococcosis. Parasitology 127, S37S51.
McManus, D. P., Zhang, W., Li, J. and Bartley, P. B. (2003). Echinococcosis. Lancet 362, 12951304.
Mühlschlegel, F., Sygulla, L., Frosch, P., Massetti, P. and Frosch, M. (1993). Paramyosin of Echinococcus granulosus: cDNA sequence and characterization of a tegumental antigen. Parasitology Research 79, 660666.
Naidich, A., McManus, D. P., Canova, S. G., Gutierrez, A. M., Zhang, W., Guarnera, E. A. and Rosenzvit, M. C. (2006). Patent and pre-patent detection of Echinococcus granulosus genotypes in the definitive host. Molecular and Cellular Probes 20, 510.
Nakao, M., McManus, D. P., Schantz, P. M., Craig, P. S. and Ito, A. (2007). A molecular phylogeny of the genus Echinococcus inferred from complete mitochondrial genomes. Parasitology 134, 713722.
Oaks, J. A., Knowles, W. J. and Cain, G. D. (1977). A simple method of obtaining an enriched fraction of tegumental brush border from Hymenolepis diminuta. Journal of Parasitology 63, 476485.
Pappas, P. W. and Narcisi, E. M. (1982). A comparison of membrane-bound enzymes of the isolated brush border plasma membranes of the cestodes of Hymenolepis diminuta and H. microstoma. Parasitology 84, 391396.
Reiterova, K., Miterpakova, M., Turcekova, L., Antolova, D. and Dubinsky, P. (2005). Field evaluation of an intravital diagnostic test of Echinococcus multilocularis infection in red foxes. Veterinary Parasitology 128, 6571.
Rishi, A. K. and McManus, D. P. (1987). Genomic cloning of human Echinococcus granulosus DNA: isolation of recombinant plasmids and their use as genetic markers in strain characterization. Parasitology 94, 369383.
Rishi, A. K. and McManus, D. P. (1988). Molecular cloning of Taenia solium DNA and characterisation of taeniid cestodes by DNA analysis. Parasitology 97, 161176.
Rosenzvit, M. C., Camicia, F., Kamenetzky, L., Muzulin, P. M. and Gutierrez, A. M. (2006 a). Identification and intra-specific variability analysis of secreted and membrane-bound proteins from Echinococcus granulosus. Parasitology International 55 (Suppl.), S63S67.
Rosenzvit, M. C., Zhang, W., Motazedian, H., Smyth, D., Pearson, M., Loukas, A., Jones, M. K. and McManus, D. P. (2006 b). Identification of membrane-bound and secreted proteins from Echinococcus granulosus by signal sequence trap. International Journal for Parasitology 36, 123130.
Shaikenov, B. S., Rysmukhambetova, A. T., Massenov, B., Deplazes, P., Mathis, A. and Torgerson, P. R. (2004). Short report: the use of a polymerase chain reaction to detect Echinococcus granulosus (G1 strain) eggs in soil samples. American Journal of Tropical Medicine and Hygiene 71, 441443.
Smyth, D., McManus, D. P., Smout, M. J., Laha, T., Zhang, W. and Loukas, A. (2003). Isolation of cDNAs encoding secreted and transmembrane proteins from Schistosoma mansoni by a signal sequence trap method. Infection and Immunity 71, 25482554.
Smyth, J. D. and Davies, Z. (1974). Occurrence of physiological strains of Echinococcus granulosus demonstrated by in vitro culture of protoscoleces from sheep and horse hydatid cysts. International Journal for Parasitology 4, 443445.
Smyth, J. D. and McManus, D. P. (1989). The Physiology and Biochemistry of Cestodes. Cambridge University Press, Cambridge, UK.
Smyth, J. D. and Smyth, M. M. (1964). Natural and experimental hosts of Echinococcus granulosus and E. multilocularis, with comments on the genetics of speciation in the genus Echinococcus. Parasitology 54, 493514.
Stefanic, S., Shaikenov, B. S., Deplazes, P., Dinkel, A., Torgerson, P. R. and Mathis, A. (2004). Polymerase chain reaction for detection of patent infections of Echinococcus granulosus (“sheep strain”) in naturally infected dogs. Parasitology Research 92, 347351.
Thompson, R. C. A. and McManus, D. P. (2002). Towards a taxonomic revision of Echinococcus. Trends in Parasitology 18, 452457.
Wachira, T. M., Bowles, J., Zehyle, E. and McManus, D. P. (1993). Molecular examination of the sympatric existence and distribution of sheep and camel strains of Echinococcus granulosus in Kenya. American Journal of Tropical Medicine and Hygiene 48, 473479.
Xiao, N., Qiu, J., Nakao, M., Li, T., Yang, W., Chen, X., Schantz, P. M., Craig, P. S. and Ito, A. (2005). Echinococcus shiquicus n. sp., a taeniid cestode from Tibetan fox and plateau pika in China. International Journal for Parasitology 35, 693701.
Xiao, S. H., Feng, J. J., Guo, H. F., Jiao, P. Y., Yao, M. Y. and Jiao, W. (1994). Effects of mebendazole, albendazole, and praziquantel on fumarate hydratase, pyruvate kinase, and phosphoenolpyruvate carboxykinase of Echinococcus granulosus cyst wall harbored in mice. Zhongguo Yao Li Xue Bao 15, 6972.
Xiao, S. H., Feng, J. and Yao, M. (1995). Effect of antihydatid drugs on carbohydrate metabolism of metacestode of Echinococcus granulosus. Chinese Medical Journal 108, 682688.


Reflections on the biochemistry of Echinococcus: past, present and future

  • D. P. McMANUS (a1)


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