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Developmental changes of Echinococcus multilocularis metacestodes revealed by tegumental ultrastructure and lectin-binding sites

Published online by Cambridge University Press:  06 April 2009

R. Leducq  and
C. Gabrion
R. Leducq
Affiliation:
Laboratoire de Parasitologie Comparée, Place Eugène Bataillon, U.S.T.L. Montpellier II, 34095 Montpellier cedex 5, France
C. Gabrion
Affiliation:
Laboratoire de Parasitologie Comparée, Place Eugène Bataillon, U.S.T.L. Montpellier II, 34095 Montpellier cedex 5, France
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Summary

Ultrastructural investigations (SEM, TEM) combined with lectin-binding analysis, have revealed concurrent modifications in tegumentary structure and surface glycoconjugates during the establishment and differentiation of Echinococcus multilocularis metacestodes in jirds. The laminated layer, which is amorphous and rich in polysaccharides when initially secreted by the young cyst, takes on a different appearance and has a different glycoconjugate composition according to whether the cyst becomes fertile or sterile. The laminated layer of fertile cysts transforms into a microfibrillar matrix, the protein content of which may increase while sugar content decreases during protoscolex differentiation. Independently of this structure, brood capsules, from which arise protoscoleces, are formed by invagination of the cyst tegument. The intense secretion of glycoconjugates from the brood capsule wall during invagination may serve to interact with host factors passing through the laminated layer. The combined use of ultrastructural study and lectin labelling has allowed the demonstration of an ultrastructural and biochemical gradient of differentiation of the protoscolex. Seven stages of differentiation have been described. The possibility that the excreted–secreted tegumentary glycoconjugates, revealed by lectin labelling during protoscolex differentiation, might be the gradual biochemical expression of one or several stimuli implicated in the phenomenon of protoscolex maturation, is discussed.

Keywords

Echinococcus multilocularismetacestodetegumentary structurescarbohydrate moitiesdifferentiationhost–parasite relationships
Type
Research Article
Information
Parasitology , Volume 104 , Issue 1 , February 1992 , pp. 129 - 141
Copyright
Copyright © Cambridge University Press 1992

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References

REFERENCES

Alkarmi, T. & Behbehani, K. (1989). Echinococcus multilocularis: inhibition of murine neutrophil and macrophage chemotaxis. Experimental Parasitology 69, 16–22.CrossRefGoogle ScholarPubMed
Arme, C. (1988). Ontogenic changes in helminth membrane function. Parasitology 96, S83–S104.CrossRefGoogle Scholar
Bennett, H. S. (1963). Morphological aspects of extracellular polysaccharides. Journal of Histochemistry and Cytochemistry 11, 14–23.CrossRefGoogle Scholar
BERRADA-Rkhami, O., Leducq, R., Gabrion, J. & Gabrion, C. (1990). Selective distribution of sugars on the tegumental surface of adult Bothriocephalus gregarius (Cestoda: Pseudophyllidea). International Journal for Parasitology 20, 285–97.CrossRefGoogle ScholarPubMed
Bortoletti, G. & Ferretti, G. (1973). Investigation on larval forms of Echinococcus granulosus with electron microscope. Rivista di Parassitologia 34, 89–110.Google Scholar
Coltorti, E. A. & Varela-Diaz, V. M. (1974). Echinococcus granulosus: penetration of macromolecules and their localization on the parasite membranes cysts. Experimental Parasitology 35, 225–31.CrossRefGoogle Scholar
Contat, F., Petavy, A. F., Deblock, S. & Euzeby, J. (1983). Contribution à l'étude épidémiologique de l'échinoccocose alvéolaire en Haute-Savoie. Bulletin de la Société Française de Parasitologie 1, 55–8.Google Scholar
Davies, C., Rickard, M. D., Bout, D. T. & Smyth, J. D. (1978). Ultrastructural immunocytochemical localization of two hydatid fluid antigens (antigen 5 and antigen B) in the brood capsules and protoscoleces of ovine and equine Echinococcus granulosus and E. multilocularis. Parasitology 77, 143–52.CrossRefGoogle ScholarPubMed
Dunne, D. W. (1990). Schistosome carbohydrates. Parasitology Today 6, 45–8.CrossRefGoogle ScholarPubMed
Goldstein, I. J. & Poretz, R. D. (1986). Isolation, physiochemical characterization and carbohydrate-binding specificity of lectins. In The Lectins. Properties, Functions, and Applications in Biology and Medicine (ed. Liener, I. E., Sharon, N. & Goldstein, I. J.), pp. 33–248. London: Academic Press.Google Scholar
Ham, P. J., Smail, A. J. & Groeger, B. K. (1988). Surface carbohydrate changes on Onchocerca lienalis larvae as they develop from microfilariae to the infective third-stage in Simulium ornatum. Journal of Helminthology 62, 195–205.CrossRefGoogle Scholar
Harris, A., Heath, D. D., Lawrence, S. B. & Saw, R. J. (1989). Echinococcus granulosus: ultrastructure of epithelial changes during the first 8 days of metacestode development in vitro. International Journal for Parasitology 19, 621–9.CrossRefGoogle ScholarPubMed
Joshua, G. W. P., Harrison, L. J. S. & Sewell, M. M. H. (1988). Excreted/secreted products of developing Taenia saginata metacestodes. Parasitology 97, 477–89.CrossRefGoogle ScholarPubMed
Joshua, G. W. P., Harrison, L. J. S. & Sewell, M. M. H. (1989). Development changes in proteins and glycoproteins revealed by direct radio-iodination of viable Taenia saginata larvae. Parasitology 99, 265–74.CrossRefGoogle ScholarPubMed
Kaushal, N. A., Simpson, A. J. G., Haussain, R. & Ottesen, E. A. (1984). Brugia malayi: stage-specific expression of carbohydrates containing N-acetyl-D-glucosamine on the sheathed surfaces of microfilariae. Experimental Parasitology 58, 182–7.CrossRefGoogle ScholarPubMed
Kilejian, A. & Schwabe, C. W. (1971). Studies on the polysaccharides of the Echinococcus granulosus cyst, with observations on a possible mechanism for laminated membrane formation. Comparative Biochemistry and Physiology 40B, 25–36.Google ScholarPubMed
Kore, I., Hierro, J., Lasalvia, E., Falco, M. & Calcagno, M. (1967). Chemical characterization of the polysaccharide of the hydatid membrane of Echinococcus granulosus. Experimental Parasitology 20, 219–24.Google Scholar
Lamsam, S. & Mcmanus, D. P. (1990). Molecular characterization of the surface and cyst fluid components of Taenia crassiceps. Parasitology 101, 115–25.CrossRefGoogle ScholarPubMed
Lascano, E. F., Coltorti, E. A. & Varela-Diaz, V. M. (1975). Fine structure of the germinal membrane of Echinococcus granulosus cysts. Journal of Parasitology 61, 853–60.CrossRefGoogle ScholarPubMed
Leducq, R., Gabrion, J. & Gabrion, C. (1988). Caractérisation des glycoconjugués de surface et intracellulaires dans les formes larvaires d'Echinococcus multilocularis à l'aide de lectines. Comptes Rendus de la Société de Biologie 182, 501–8.Google Scholar
Leducq, R., Berrada-Rkhami, O., Gabrion, J. & Gabrion, C. (1990). Lectin analysis of glycoconjugate distribution during differentiation and strobilization of Bothriocephalus gregarius metacestode in a paratenic host. International Journal for Parasitology 20, 645–54.CrossRefGoogle Scholar
Liance, M., Bresson-Hadni, S., Vuitton, D., Bretagne, S. & Houin, R. (1990). Comparison of the viabilty and developmental characteristics of Echinococcus multilocularis isolates from human patients in France. International Journal for Parasitology 20, 83–6.CrossRefGoogle Scholar
Mankau, S. K. (1957). Studies on Echinococcus alveolaris (Klemm, 1883), from St. Lawrence Island, Alaska. I. Histogenesis of the alveolar cyst in white mice. Journal of Parasitology 43, 153–9.CrossRefGoogle Scholar
Marchiondo, A. A. & Anderson, F. L. (1983). Fine structure and freeze-etch study of the protoscolex tegument of Echinococcus multilocularis (Cestoda). Journal of Parasitology 69, 709–18.CrossRefGoogle ScholarPubMed
Muramatsu, T. (1989). Les sucres de la membrane cellulaire. La Recherche 20, 624–34.Google Scholar
Norman, L. & Kagan, J. G. (1961). The maintenance of Echinococcus multilocularis in gerbils (Meriones unguiculatus) by intraperitoneal inoculation. Journal of Parasitology 47, 870–4.CrossRefGoogle ScholarPubMed
Ohbayashi, M. (1960). Studies on Echinococcosis X. Histological observations on experimental cases of multilocular echinococcosis. Japanese Journal of Veterinary Research 8, 134–45.Google Scholar
Olivo, A., Plancarte, A. & Flisser, A. (1988). Presence of antigen B from Taenia solium cysticercus in other Playthelminthes. International Journal for Parasitology 18, 543–5.CrossRefGoogle Scholar
Richards, K. S. (1984). Echinococcus granulosus equinus: the histochemistry of the laminated layer of the hydatid cyst. Folia Histochemica et Cytobiologica 22, 21–32.Google ScholarPubMed
Rogan, M. T. & Richards, K. S. (1987). Echinococcus granulosus: changes in the surface ultrastructure during protoscolex formation. Parasitology 94, 359–67.CrossRefGoogle ScholarPubMed
Roth, J. & Binder, M. (1978). Colloidal gold, ferritin and peroxidase as markers for electron microscopic double labeling lectin techniques. Journal of Histochemistry and Cytochemistry 26, 163–9.CrossRefGoogle ScholarPubMed
Roth, J. (1983). Application of lectin-gold complexes for electron microscopic localization of glycoconjugates on thin sections. Journal of Histochemistry and Cytochemistry 31, 987–99.CrossRefGoogle ScholarPubMed
Sakamoto, T. & Sugimura, M. (1969). Studies on echinococcosis XXI. Electron microscopical observations on general structure of larval tissue of multilocular Echinococcus. Japanese Journal of Veterinary Research 17, 67–80.Google ScholarPubMed
Sakamoto, T. & Sugimura, M. (1970). Studies on echinococcosis XXIII. Electron microscopical observations on histogenesis of larval Echinococcus multilocularis. Japanese Journal of Veterinary Research 18, 131–44.Google Scholar
Sandeman, R. M. & Williams, J. F. (1984). Lectin binding to cystic stages of Taenia taeniaeformis. Journal of Parasitology 70, 661–7.CrossRefGoogle ScholarPubMed
Sharon, N. (1975). Les sucres dans la vie sociale des cellules. La Recherche 6, 16–24.Google Scholar
Siddiqui, A. A., Karcz, S. R. & Podesta, R. B. (1987). Developmental and immune regulation of gene expression in Hymenolepis diminuta. Molecular and Biochemical Parasitology 25, 19–28.CrossRefGoogle ScholarPubMed
Simpson, A. J. G., Correa-Oliveria, R., Smithers, S. R. & Sher, A. (1983). The exposed carbohydrates of schistosomula of Schistosoma mansoni and their modification during maturation in vivo. Molecular and Biochemical Parasitology 8, 191–205.CrossRefGoogle ScholarPubMed
Slais, J. (1966). The importance of the bladder for the development of the cysticercus. Parasitology 56, 707–13.CrossRefGoogle ScholarPubMed
Suzuki, S., Tsuyama, S., Suganuma, T., Yamamoto, N. & Murata, F. (1981). Postembedding staining of Brunner's gland with lectin-ferritin conjugates. Journal of Histochemistry and Cytochemistry 29, 946–52.CrossRefGoogle ScholarPubMed
Thompson, R. C. A. (1976). The development of brood capsules and protoscoleces in secondary hydatid cysts of Echinococcus granulosus. A histological study. Zeitschrift für Parasitenkunde 51, 31–6.CrossRefGoogle Scholar
Yamashita, J. (1960). On susceptibility and histogenesis of E. multilocularis in the experimental mouse with the stade of echinococcosis in Japan. Parasitologia 2, 399–406.Google Scholar
Yarzabal, L. A., Dupas, H., Bout, D., Naquira, F. & Capron, A. (1977). Echinococcus granulosus: the distribution of hydatid fluid antigens in the tissues of the larval stage. II. Localisation of the thermostable lipoprotein of parasitic origin (Antigen B). Experimental Parasitology 42, 115–20.CrossRefGoogle ScholarPubMed