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A freeze fracture study of the developing tegumental outer membrane of Schistosoma mansoni

Published online by Cambridge University Press:  06 April 2009

Diane J. McLaren ,
D. J. Hockley ,
O. L. Goldring  and
B. J. Hammond
Diane J. McLaren
Affiliation:
Division of Parasitology, National Institute for Medical Research, Mill Hill, London NW7 1AA
D. J. Hockley
Affiliation:
Division of Viral Products, National Institute for Biological Standards and Control, Hampstead, London NW3 6RB
O. L. Goldring
Affiliation:
WHO, JUIS International Training and Research Centre, ITR Central Laboratory of the Netherlands, Plesmanlaan 125, Amsterdam
B. J. Hammond
Affiliation:
Computer Laboratory, National Institute for Medical Research, Mill Hill, London NW7 1AA
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Summary

The freeze fracture technique has been used to quantify changes in the integral components of the double outer membrane of Schistosoma mansoni during the 6-week period of development within the mouse. The intramembraneous particle (IMP) density on the P1 face begins to rise Within 6 h of host penetration, reaches a maximum at day 4 and then falls rapidly after day 9, so that it is at a low level between 3 and 6 weeks. The E1 face IMP density follows the same course as that of the P1 face except that maximum particle density is recorded on day 1 and the counts begin to fall on day 5. The IMP density on the P1 face remains at a consistently low level throughout development. The E2 face IMP density rises gradually to a peak at day 4, when the parasites have migrated to the lungs, and remains thereafter at a similar level, so that by 6 weeks the E2 face has a higher IMP density than the other three fracture faces. The E2 face IMP show a marked increase in size on day 4. Morphological studies indicate that a different type of inclusion body makes a transient appearance in the tegument of the lung worms, and immunocytochemical techniques show the lung worms to be nonimmunogenic. It is suggested, therefore, that the E2 face IMP may represent complexes of parasite antigens and acquired host antigens. The tegumental membranes of cultured specimens have also been examined by freeze fracturing and the IMP densities compared with those obtained from in vivo parasites; the cultured schistosomula have a lower E2 face particle density than the in vivo specimens.

Type
Research Article
Information
Parasitology , Volume 76 , Issue 3 , June 1978 , pp. 327 - 348
Copyright
Copyright © Cambridge University Press 1978

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References

REFERENCES

Apel, K., Miller, K. R., Bogorad, L. & Miller, G. J. (1976). Chloroplast membranes of the green alga Acetabularia mediterranea. II. Topography of the chloroplast membrane. Journal of Cell Biology 71, 876–93.Google Scholar
Armond, P. A., Staehelin, L. A. & Arntzen, C. J. (1977). Spatial relationship of photosystem I, photosystem II, and the light-harvesting complex in chloroplast membranes. Journal of Cell Biology 73, 400–18.Google Scholar
Branton, D. & Deamer, D. (1972). Membrane structure. Protoplasmatologia II/E/I: 1–70.Google Scholar
Branton, D., Bullivant, S., Gilula, N. B., Karnovksy, M. J., Moor, H., Mühlethaler, K, Northcote, D. H., Packer, L., Satir, B., Satir, P., Speth, V., Staehelin, L. A., Steere, R. L. & Weinstein, R. S. (1975). Freeze etching nomenclature. Science 190, 54–6.Google Scholar
Breathnach, A. S., Gross, M., Martin, B. & Stolinski, C. (1976). A comparison of membrane fracture faces of fixed and unfixed glycerinated tissue. Journal of Cell Science 21, 437–48.Google Scholar
Clegg, J. A. (1965). In vitro cultivation of Schistosoma mansoni. Experimental Parasitology 16, 133–47.Google Scholar
Clegg, J. A. & Smithers, S. R. (1972). The effects of immune rhesus monkey serum on schistosomula of Schistosoma mansoni during cultivation in vitro. International Journal for Parasitology 2, 79–98.CrossRefGoogle ScholarPubMed
Clegg, J. A., Smithers, S. R. & Terry, R. J. (1971). Acquisition of ‘human’ antigens by Schistosoma mansoni during cultivation in vitro. Nature, London 232, 653–4.CrossRefGoogle ScholarPubMed
Cullen, S. E., David, C. S., Shreffler, D. C. & Nathenson, S. G. (1974). Membrane molecules determined by the H–2 associated immune response region: isolation and some properties. Proceedings of the National Academy of Sciences, USA 71, 648–54.CrossRefGoogle ScholarPubMed
Dempsey, G. P., Bullivant, S. & Watkins, W. B. (1973). Endothelial cell membranes: polarity as seen by freeze-fracturing. Science 179, 190–2.Google Scholar
Goldring, O. L., Clegg, J. A., Smithers, S. R. & Terry, R. J. (1976). Acquisition of human blood group antigens by Schistosoma mansoni. Clinical and Experimental Immunology 26, 181–7.Google ScholarPubMed
Goldring, O. L., Kusel, J. R. & Smithers, S. R. (1977). Schistosoma mansoni: origin in vitro of host-like surface antigens. Experimental Parasitology 43, 82–93.CrossRefGoogle ScholarPubMed
Goldring, O. L., Seer, A., Smithers, S. R. & McLaren, D. J. (1977). Host antigens and parasite antigens of murine Schistosoma mansoni. Transactions of the Royal Society of Tropical Medicine and Hygiene 71, 144–8.Google Scholar
Hasty, D. L. & Hay, E. D. (1977). Freeze-fracture studies of the developing cell surface. I. The plasmalemma of the corneal fibroblast. Journal of Cell Biology 72, 667–86.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.Google Scholar
Hockley, D. J., McLaren, D. J., Ward, B. J. & Nermut, M. V. (1975). A freeze fracture study of the tegumental membrane of Schistosoma mansoni (Platyhehninthes: Trematoda). Tissue and Cell 7, 485–96.CrossRefGoogle ScholarPubMed
Hong, K. & Hubbell, W. L. (1972). Preparation and properties of phospholipid bilayers containing rhodopsin. Proceedings of the National Academy of Sciences, USA 69, 2617–21.CrossRefGoogle ScholarPubMed
Kusel, J. R. (1972). Protein composition and protein synthesis in the surface membranes of Schistosoma mansoni. Parasitology 65, 55–69.Google Scholar
Marchesi, V. T., Tillack, T. W., Jackson, R. L., Segrest, J. P. & Scott, R. E. (1972). Chemical characterization and surface orientation of the major glycoprotein of the human erythrocyte membrane. Proceedings of the National Academy of Sciences, USA 69, 1445–9.Google Scholar
Mason, T. E., Phifer, R. F., Spicer, S. S., Swallow, R. A. & Dreskin, R. B. (1969). An immunological-enzyme bridge method for localizing tissue antigens. Journal of Histochemistry and Cytochemistry 17, 563–9.CrossRefGoogle ScholarPubMed
McLaren, D. J., Clegg, J. A. & Smithers, S. R. (1975). Acquisition of host antigens by young Schistosoma mansoni in mice: correlation with failure to bind antibody in vitro. Parasitology 70, 67–75.CrossRefGoogle ScholarPubMed
McLaren, D. J. & Hockley, D. J. (1976). Schistosoma mansoni: the occurrence of microvilli on the surface of the tegument during transformation from cercaria to schistosomulum. Parasitology 73, 169–87.Google Scholar
McLaren, D. J. & Hockley, D. J. (1977). Blood flukes have a double outer membrane. Nature, London 269, 147–9.CrossRefGoogle ScholarPubMed
Misra, D. N. & Gupta, Das N. N. (1966). Distortion in dimensions produced by shadowing for electron microscopy. Journal of the Royal Microscopical Society 84, 373–84.Google Scholar
Mühlethaler, K., Wehrli, E. & Moor, H. (1970). Double fracture methods for freeze etching. In Proceedings of the 7th International Congress of Electron Microscopy, Grenoble, vol. 1 (ed. Favard, P.), pp. 449–50. Socié Française de Microscopic Électronique, Paris.Google Scholar
Parish, G. R. (1975). Changes of particle frequency in freeze-etched erythrocyte membranes after fixation. Journal of Microscopy 104, 245–56.CrossRefGoogle ScholarPubMed
Pfenninger, K. H. & Bunge, R. P. (1974). Freeze-fracturing of nerve growth cones and young fibres. A study of developing plasma membrane. Journal of Cell Biology 63, 180–96.CrossRefGoogle Scholar
Da Silva, Pinto P. & Branton, D. (1970). Membrane splitting in freeze etching: covalently bound ferritin as a membrane marker. Journal of Cell Biology 45, 598–605.CrossRefGoogle Scholar
Ruben, G. C., Telford, J. N. & Carroll, R. C. (1976). Identification and trans-membranous localization of active cytochrome oxidase in reconstituted membranes of purified phospholipids by electron microscopy. Journal of Cell Biology 68, 724–39.Google Scholar
Sanders, E. J. & Dicaprio, R. A. (1976). A freeze-fracture and concanavalin A-binding study of the membrane of cleaving Xenopus embryos. Differentiation 7, 13–21.CrossRefGoogle ScholarPubMed
Schwartz, B. D., Kato, K., Culien, S. E. & Nathenson, S. G. (1973). H–2 histocompatibility alloantigens. Some biochemical properties of the molecules solubilized by NP-40 detergent. Biochemistry 12, 2157–64.Google Scholar
Sher, A. (1977). Immunity and immune evasion in schistosomiasis. In Proceedings of the Brook Lodge Symposium. Escape from Immune Surveillance, an Interpretative Survey of the Interface between Immune Mechanisms and Disease.(N.I.A.I.D. Sponsored Symposium)(in the Press).Google Scholar
Seer, A., Kusel, J. R., Perez, H. & Clegg, J. A. (1974). Partial isolation of a membrane antigen which induces the formation of antibodies lethal to schistosornes cultured in vitro. Clinical and Experimental Immunology 18, 357–69.Google Scholar
Smithers, S. R. & Terry, R. J. (1965). The infection of laboratory hosts with cercariae of Schistosoma mansoni and the recovery of adult worms. Parasitology 55, 695–700.Google Scholar
Smithers, S. R., Terry, R. J. & Hockley, D. J. (1969). Host antigens in schistosomiasis. Proceedings of the Royal Society, London, B 171, 483–94.Google Scholar
Springer, T. A. & Strominger, J. L. (1976). Detergent-soluble HLA antigens contain a hydrophilic region at the COOH-terminus and a penultimate hydrophobic region. Proceedings of the National Academy of Sciences, USA 73, 2481–5.CrossRefGoogle Scholar
Stirewalt, M. A. (1974). Schistosoima mansoni: cercaria to schistosomule. In Advances in Parasitology, vol. 12 (ed. Dawes, B.), pp. 115–82. New York and London: Academic Press.Google Scholar
Tillack, T. W. & Marchesi, V. T. (1970). Demonstration of the outer surface of freeze etched red blood cell membranes. Journal of Cell Biology 45, 469–73.Google ScholarPubMed
Wilson, R. A. & Barnes, P. B. (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
Yu, J. & Branton, D. (1976). Reconstitution of intramermbrane particles in recombinants of erythrocyte protein Band 3 and lipid: effects of spectrin-actin association. Proceedings of the National Academy of Sciences, USA 73, 3891–5.Google Scholar