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The tegument of Schistosoma mansoni: observations on the formation, structure and composition of cytoplasmic inclusions in relation to tegument function

Published online by Cambridge University Press:  06 April 2009

R. A. Wilson  and
P. E. Barnes
R. A. Wilson
Affiliation:
Department of Biology, University of York, Heslington, York
P. E. Barnes
Affiliation:
Department of Biology, University of York, Heslington, York
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Extract

Two major cytoplasmic inclusions, multilaminate vesicles and discoid granules, are present in the tegument of Schistosoma mansoni. These are produced at separate Golgi apparatuses in the tegument cell bodies and move up to the surface by a combination of diffusion and fluid flow. The discoid granules contain neutral mucopolysaccharide and are believed to break down to form the ground substance of the tegument. The multilaminate vesicles are rich in phospholipid and the contents, at least superficially, resemble unit membranes. The multilaminate vesicles are believed to contribute their contents to the multilaminate surface of the worm which appears to be continually replaced. These observations are related to current ideas on membrane turnover and the ability of the worm to acquire a disguise of host erythrocyte glycolipid.

Type
Research Article
Information
Parasitology , Volume 68 , Issue 2 , April 1974 , pp. 239 - 258
Copyright
Copyright © Cambridge University Press 1974

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References

REFERENCES

Amsterdam, A., Ohad, I. & Schramm, M. (1969). Dynamic changes in the ultrastructure of the acinar cell of the rat parotid gland during the secretory cycle. Journal of Cell Biology 41, 753–73.CrossRefGoogle ScholarPubMed
Bainton, D. F. & Farquahar, M. G. (1966). Origin of granules in polymorphonuclear leucocytes. Journal of Cell Biology 28, 277–301.CrossRefGoogle Scholar
Beams, H. W. & Kessel, R. G. (1969). Synthesis and deposition of oocyte envelopes (vitelline membrane, chorion) and the uptake of yolk in the dragonfly (Odonata: Aeschnidae). Journal of Cell Science 4, 241–64.CrossRefGoogle ScholarPubMed
Bonneville, M. A. & Weinstock, M. (1970). Brush border development in the intestinal absorptive cells of Xenopus during metamorphosis. Journal of Cell Biology 44, 151–71.CrossRefGoogle ScholarPubMed
Burton, P. R. (1966). The ultrastructure of the integument of the frog bladder fluke, Gorgoderina sp. Journal of Parasitology 52, 926–34.CrossRefGoogle ScholarPubMed
Caro, L. G. & Palade, G. E. (1964). Protein synthesis, storage and discharge in the pancreatic exocrine cell: an autoradiographic study. Journal of Cell Biology 20, 173–95.Google ScholarPubMed
Clegg, J. A. (1972). The schistosome surface in relation to parasitism. Functional Aspects of Parasite Surfaces: Symposium of the British Society for Parasitology, Vol. 10 (ed. Taylor, A. E. R. and Muller, R.), pp. 23–40. Oxford and London: Blackwell.Google Scholar
Clegg, J. A., Smithers, S. R. & Terry, R. J. (1971). Concomitant immunity and host antigens associated with schistosomiasis. International Journal for Parasitology 1, 43–9.CrossRefGoogle ScholarPubMed
Dauwalder, M., Whaley, W. G. & Kephart, J. E. (1972). Functional aspects of the Golgi apparatus. Sub-cellular Biochemistry 1, 225–75.Google Scholar
Dhainault, A. (1969). Origine et structure des formations mucopolysaccharidiques de la zone corticalo de l'ovocyte de Nereis diversicolor O. F. Müller (Annélide, Polychête). Journal de Microscopie 8, 69–86.Google Scholar
Erasmus, D. A. (1967). The host-parasite interface of Cyathocotyle bushiensis Khan, 1962 (Trematoda: Stringeoidea), II. Electron microscope studies of the tegument. Journal of Parasitology 53, 703–14.CrossRefGoogle ScholarPubMed
Favard-Séréno, C. (1971). Cycles sécrétoires successifs au cours do l'élaboration des enveloppes de l'ovocyte chez le Grillon (Insecte, Orthoptère). Rôle do l'appareil de Golgi. Journal de Microscopie 11, 401–24.Google Scholar
Fleischer, B., Fleischer, S. & Ozawa, H. (1969). Isolation and characterization of Golgi membranes from bovine liver. Journal of Cell Biology 43, 59–79.CrossRefGoogle ScholarPubMed
Glauert, A. M. & Lucy, J. A. (1968). Globular micelles and organisation of membrane lipids. In Ultrastructure in Biological Systems. Vol. 4. The Membranes (ed. Dalton, A. J. and Haguenau, F.), pp. 1–32. New York and London: Academic Press.Google Scholar
Glick, D. & Scott, J. E. (1970). Phosphotungstic acid not a stain for polysaccharide. Journal of Histochemistry and Cytochemistry 18, 455.CrossRefGoogle Scholar
Hicks, R. M. (1966). The function of the Golgi complex in transitional epithelium. Synthesis of the thick cell membrane. Journal of Cell Biology 30, 623–43.CrossRefGoogle ScholarPubMed
Hockley, D. J. & McLaren, D. J. (1973). Schistosoma mansoni: changes in the outer membrane of the tegument during development from cercaria to adult worm. International Journal for Parasitology 3, 13–25.CrossRefGoogle ScholarPubMed
Jamieson, J. D. (1972). Transport and discharge of exportable proteins in pancreatic exocrine cells: in vitro studies. In Current Topics in Membranes and Transport, vol. 3 (ed. Bronner, F. and Kleinzeller, A.), pp. 273–338. New York and London: Academic Press.Google Scholar
Jamieson, J. D. & Palade, G. E. (1971). Condensing vacuole conversion and zymogen granule discharge in pancreatic exocrine cells: metabolic studies. Journal of Cell Biology 48, 503–22.CrossRefGoogle ScholarPubMed
Kay, D. (1965). Techniques for Electron Microscopy. Oxford and Edinburgh: Blackwell.Google Scholar
Koss, L. G. (1969). The asymmetric unit membranes of the epithelium of the urinary bladder of the rat. Laboratory Investigation 21, 154–68.Google ScholarPubMed
Kurigama, Y., Omura, T., Siekevitz, P. & Palade, G. E. (1969). Effects of phenobarbital on the synthesis and degradation of the protein components of rat liver microsomal membranes. Journal of Biological Chemistry 244, 2017–26.CrossRefGoogle Scholar
Morré, D. J. & Mollenhauer, H. H. (1974). The endomembrane concept. In Dynamic aspects of plant ultrastructure (ed. Robards, A. W.,) pp. 84–137. London: McGraw Hill.Google Scholar
Morris, G. P. & Threadgold, L. T. (1968). Ultrastructure of the tegument of adult Schistosoma mansoni. Journal of Parasitology 54, 15–27.CrossRefGoogle ScholarPubMed
Niebauer, G., Krawczyk, W. S., Kidd, R. L. & Wilgram, G. F. (1969). Osmium-zinc iodide reactive sites in the epidermal Langerhans cell. Journal of Cell Biology 43, 80–9.CrossRefGoogle ScholarPubMed
Novikoff, B. A., Essner, E. & Quintana, N. (1964). Golgi apparatus and lysosomes. Federation Proceedings 23, 1010–22.Google ScholarPubMed
Oaks, J. A. & Lumsden, R. D. (1971). Cytological studies on the absorptive surface of cestodes. V. Incorporation of carbohydrate-containing macromolecules into tegument membranes. Journal of Parasitology 57, 1256–68.CrossRefGoogle ScholarPubMed
Omura, T., Siekevitz, P. & Palade, G. E. (1967). Turnover of constituents of the endoplasmic reticulum membranes of rat hepatocytes. Journal of Biological Chemistry 242, 2389–96.CrossRefGoogle ScholarPubMed
Ongun, A., Thomson, W. W. & Mudd, J. B. (1968). Lipid fixation during preparation of chloroplasts for electron microscopy. Journal of Lipid Research 9, 416–24.CrossRefGoogle ScholarPubMed
Ovtracht, L. & Thiery, J. P. (1972). Mise en évidence par cytochemie ultrastructurale de compartiments physiologiquement différents dans un même saccule golgien. Journal de Microscopie 15, 135–70.Google Scholar
Pearse, A. G. E. (1960). Histochemistry, Theoretical and Applied. London: Churchill.Google Scholar
Pease, D. C. (1970). Phosphotungstic acid as a specific electron stain for complex carbohydrates. Journal of Histochemistry and Cytochemistry 18, 455–8.CrossRefGoogle ScholarPubMed
Rambourg, A. (1967). An improved silver-methenamine technique for the detection of periodic acid-reactive complex carbohydrates with the electron microscope. Journal of Histochemistry and Cytochemistry 15, 409–12.CrossRefGoogle ScholarPubMed
Reissig, M. (1970). Characterisation of cell types in the parenchyma of Schistosoma mansoni. Parasitology 60, 273–9.CrossRefGoogle ScholarPubMed
Remsen, C. C. & Watson, S. W. (1972). Freeze-etching of bacteria. International Review of Cytology 33, 253–96.CrossRefGoogle ScholarPubMed
Seligman, A. M., Hanker, J. S., Wasserkrug, H., Dmochowski, H. & Katzoff, L. (1965). Histochemical demonstration of some oxidised macromolecules with thiocarbohydrazide (TCH) or thiosemicarbazide (TSC) and osmium tetroxide. Journal of Histochemistry and Cytochemistry 13, 629–39.CrossRefGoogle ScholarPubMed
Silk, M. H., Spence, I. M. & Gear, J. H. S. (1969). Ultrastructural studies of the blood fluke — Schistosoma mansoni I. The integument. South African Journal of Medical Science 34, 1–10.Google ScholarPubMed
Silva, M. T., Guerra, F. C. & Magalhaes, M. M. (1968). The fixative action of uranyl acetate in electron microscopy. Experientia 24, 1074.CrossRefGoogle ScholarPubMed
Smith, J. H., Reynolds, E. S. & Von Lichtenberg, F. (1969). The integument of Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 18, 28–49.CrossRefGoogle ScholarPubMed
Smithers, S. R. & Terry, R. J. (1965). The infection of laboratory hosts with cercariae of Schistosoma mansoni and recovery of the adult worms. Parasitology 55, 695–700.CrossRefGoogle ScholarPubMed
Smithers, S. R., Terry, R. J. & Hockley, D. J. (1969). Host antigens in schistosomiasis. Proceedings of the Royal Society B 171, 483–94.Google ScholarPubMed
Stirewalt, M. A. (1963). Chemical biology of secretions of larval helminths. Annals of New York Academy of Sciences 113, 36–53.CrossRefGoogle ScholarPubMed
Terzakis, J. A. (1968). Uranyl acetate, a stain and a fixative. Journal of Ultrastructure Research 22, 168–84.CrossRefGoogle Scholar
Wessels, N. K., Spooner, B. S., Ash, J. F., Bradley, M. O., Ludiena, M. A., Taylor, E. L., Wrenn, J. T. & Yamada, K. M. (1971). Microfilaments in cellular and developmental processes. Science 171, 135–43.CrossRefGoogle Scholar
Wetzel, B. K. (1961). Sodium permanganate fixation for electron microscopy. Journal of Biophysical and Biochemical Cytology 9, 711–6.CrossRefGoogle ScholarPubMed
Wilson, R. A. & Barnes, P. E. (1974). An in vitro investigation of dynamic processes occurring in the schistosome tegument, using compounds known to disrupt secretory processes. Parasitology 68, 259–70.CrossRefGoogle Scholar
Wilson, R. A., Pullin, R. & Denison, J. (1971). An investigation of the mechanism of infection by digenetic trematodes: the penetration of the miracidium of Fasciola hepatica into its snail host Lymnaea truncatula. Parasitology 63, 491–506.CrossRefGoogle ScholarPubMed