Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-19T04:29:32.223Z Has data issue: false hasContentIssue false

Ontogenetic changes in helminth membrane function

Published online by Cambridge University Press:  23 August 2011

C. Arme
Affiliation:
Parasitology Research Laboratory, Department of Biological Sciences, University of Keele, Keele, Staffs ST5 5BG

Summary

During their life-cycle many parasites experience a wide range of environments including free living and those provided by a variety of intermediate and final hosts. The nutritional requirements of parasites are met by physiological processes adapted to exploit the physico-chemical characteristics provided by different hosts. In helminth parasites these adaptations are frequently expressed on the tegumentary surface. As an example of adaptations within the Trematoda, the control of monosaccharide transport in Proterometra sp. is described. Environmental sodium, although not directly involved in the uptake process, nevertheless regulates the expression of transport capabilities. In the Cestoda, the uptake of monosaccharides and amino acids is described for Hymenolepis diminuta. The metacestode of this tapeworm inhabits the blood system of an arthropod, and the adult the gut of a mammal. There are quantitative and qualitative differences in the amino acids and monosaccharides in these two environments and these are reflected in the transport mechanisms exhibited by the two forms of the life-cycle. In Echinococcus granulosus the transfer of amino acids, sugars and macromolecules across the membranes of hydatid cysts and protoscoleces is described. The major difference between these two stages in the life-cycle relates to the ability of hydatid cysts to absorb macromolecules, whereas protoscoleces are impermeable to these compounds. The potential for future work is emphasized.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1988

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Arai, H. P. (1980). Biology of the Tapeworm Hymenolepis diminuta. New York: Academic Press.Google Scholar
Arme, C. (1976). Feeding. In Ecological Aspects of Parasitology (ed. Kennedy, C. R.), pp. 7597. Amsterdam: North Holland.Google Scholar
Arme, C. (1982). Nutrition. In Modern Parasitology (ed. Cox, F. E. G.), pp. 148–72. Oxford: Blackwell Scientific Publications.Google Scholar
Arme, C. (1987). Cestoda. In In vitro Methods for Parasite Cultivation. 3rd Edn. (ed. Taylor, A. E. R. and Baker, J. R.). London: Academic Press (in the Press).Google Scholar
Arme, C., Middleton, A. & Scott, J. P. (1973). Absorption of glucose and sodium acetate by cysticercoid larvae of Hymenolepis diminuta. Journal of Parasitology 59, 214.CrossRefGoogle ScholarPubMed
Arme, C. & Pappas, P. W. (1983). Biology of the Eucestoda, Vols 1 and 2. London: Academic Press.Google Scholar
Arme, C. & Read, C. P. (1969). Fluxes of amino acids between the rat and a cestode symbiote. Comparative Physiology and Biochemistry 29, 1135–47.CrossRefGoogle Scholar
Barrett, J. (1987). Developmental aspects of metabolism in parasites. International Journal for Parasitology 17, 105–10.CrossRefGoogle ScholarPubMed
Baschong, W. (1985). Changes in the surface of Dipetalonema viteae during its development as shown by comparative peptide mapping. Parasitology 90, 351–6.CrossRefGoogle Scholar
Beach, D. H., Mueller, J. F. & Holz, G. G. (1980 a). Lipids of stages in the life cycle of the cestode Spirometra mansonoides. Molecular and Biochemical Parasitology 1, 249–68.CrossRefGoogle ScholarPubMed
Beach, D. H., Mueller, J. F. & Holz, G. G. (1980 b). Benzoquinones in stages of the life cycle of the cestode Spirometra mansonoides. Molecular and Biochemical Parasitology 1, 269–78.CrossRefGoogle ScholarPubMed
Benito, A. A. (1984). Hydatidosis of sheep. II. Levels of glucose, lipids and proteins in the hydatid liquid. Archivos de Zootecnia 33, 163–9.Google Scholar
Benjamin, L. R. & James, B. L. (1987). The development of the metacercaria of Maritrema linguilla Jag. 1908 (Digenea: Microphallidae) in the intermediate host, Ligia oceanica (L). Parasitology 94, 221–31.CrossRefGoogle Scholar
Bortoletti, G. & Ferretti, G. (1985). Morphological studies on the early development of Taenia taeniaeformis larvae in susceptible hosts. International Journal for Parasitology 15, 365–75.CrossRefGoogle Scholar
Bråaten, T. (1986 a). An electron microscope study of the tegument and associated structures of the procercoid of Diphyllobothrium latum (L.) Zeitschrift für Parasitenkunde 30, 95103.CrossRefGoogle Scholar
Bråten, T. (1986 b). The fine structure of the tegument of Diphyllobothrium latum (L.). A comparison of the plerocercoid and adult stages. Zeitschrift für Parasitenkunde 30, 104–12.CrossRefGoogle Scholar
Brown, D. D. (1981). Gene expression in eukaryotes. Science 211, 667–74.CrossRefGoogle ScholarPubMed
Carter, C. E. & Fairbairn, D. (1975). Multienzymic nature of pyruvate kinase during development of Hymenolepis diminuta (Cestoda). Journal of Experimental Zoology 194, 439–48.CrossRefGoogle ScholarPubMed
Chappell, L. H. (1974). Methionine uptake by larval and adult Schistosoma mansoni. International Journal for Parasitology 4, 361–9.CrossRefGoogle ScholarPubMed
Chen, S. N. & Howells, R. E. (1979). The uptake of dyes, monosaccharides and amino acids by the filarial worm Brugia pahangi. Parasitology 78, 343–54.CrossRefGoogle ScholarPubMed
Chen, S. N. & Howells, R. E. (1981 a). Brugia pahangi: uptake and incorporation of nucleic acid precursors by microfilariae and macrofilariae in vitro. Experimental Parasitology 51, 296306.CrossRefGoogle Scholar
Chen, S. N. & Howells, R. E. (1981 b). The uptake in vitro of monosaccharides, disaccharide and nucleic acid precursors by adult Dirofilaria immitis. Annals of Tropical Medicine and Parasitology 75, 329–37.CrossRefGoogle ScholarPubMed
Christensen, J. P. B., BøGh, H. O. & Andreassen, J. (1986). Hymenolepis diminuta: the effect of serum on different ages of worms in vitro. International Journal for Parasitology 16, 447–53.CrossRefGoogle ScholarPubMed
Coggins, J. R. (1980). Tegumental and apical end organ fine structure in the metacestode and adult Proteocephalus ambloplitus. International Journal for Parasitology 10, 409–18.CrossRefGoogle Scholar
Coil, W. H. (1986). The early embryology of Hymenolepis diminuta (Cestoda). Proceedings of the Helminthological Society of Washington 53, 3847.Google Scholar
Coles, G. C. (1984). Recent advances in schistosome biochemistry. Parasitology 89, 603–37.CrossRefGoogle ScholarPubMed
Crabtree, J. E. & Wilson, R. A. (1986). Schistosoma mansoni: an ultrastructural examination of pulmonary migration. Parasitology 92, 343–54.CrossRefGoogle ScholarPubMed
Crane, R. K. (1974). Intestinal absorption of glucose. In Intestinal Absorption (ed. Smyth, D. H.), chapter 10. New York: Plenum.Google ScholarPubMed
Daugherty, J. W. (1957). Intermediary protein metabolism in helminths. IV. The active absorption of methionine by the cestode H. diminuta. Experimental Parasitology 6, 60–7.CrossRefGoogle ScholarPubMed
Dunn, J. & Threadgold, L. T. (1984). Taenia crassiceps: temperature, polycations, polyanions and cysticercal endocytosis. Experimental Parasitology 58, 110–24.CrossRefGoogle ScholarPubMed
Edwards, G. T. (1982). Host IgG in equine hydatid cyst fluid. Annals of Tropical Medicine and Parasitology 76, 485–7.CrossRefGoogle ScholarPubMed
Engelkirk, P. G. & Williams, J. F. (1982). Taenia taeniaeformis (Cestoda) in the rat: ultrastructure of the host – parasite interface on days 1–7 post-infection. Journal of Parasitology 68, 620–33.CrossRefGoogle Scholar
Engelkirk, P. G. & Williams, J. F. (1983). Taenia taeniaeformis (Cestoda) in the rat: ultrastructure of the host – parasite interface on days 8 to 22 post-infection. Journal of Parasitology 69, 828–37.CrossRefGoogle Scholar
Epel, D. (1972). Activation of a Na+-dependent amino acid transport system upon fertilization of sea urchin eggs. Cell Research 72, 7489.CrossRefGoogle ScholarPubMed
Etges, D. J. & Bogtish, B. J. (1985). The effect of colchicine on translocation of incorporated [3H]proline in Hymenolepis diminuta. Journal of Parasitology 71, 290–6.CrossRefGoogle ScholarPubMed
Foley, M., Kusel, J. R. & Garland, P. B. (1988). Changes in the organization of the surface membrane upon transformation of cercariae to schistosomula of the helminth parasite Schistosoma mansoni. Parasitology 96, (in the Press).CrossRefGoogle Scholar
Font, W. F. & Wittrock, D. D. (1980). Scanning electron microscopy of Leucochloridiomorpha constantiae during development from metacercaria to adult. Journal of Parasitology 66, 955–64.CrossRefGoogle ScholarPubMed
Fraya, G. J. & Hadda, R. (1980). Comparative chemical composition of protoscoleces and hydatid cyst fluid of Echinococcus granulosus (Cestoda). International Journal for Parasitology 10, 359–64.CrossRefGoogle Scholar
Fried, B. & Fujino, T. (1984). Scanning electron microscopy of Echinostoma revolutum (Trematoda) during development in the chick embryo and the domestic chick. International Journal for Parasitology 14, 7581.CrossRefGoogle ScholarPubMed
Fukuda, K. (1986). Differentiation and degeneration of tegumental cells in adult lung flukes, Paragonimus species (Trematoda: Troglotrematidae). International Journal for Parasitology 16, 147–56.Google ScholarPubMed
Gitler, C. (1984). Host – parasite interface: membranes. In Tropical and Geographical Medicine (ed. Warren, K. S. and Mahmoud, A. A. F.), pp. 106118. New York: McGraw Hill.Google Scholar
Gomme, J. (1982). Epidermal nutrient absorption in marine invertebrates: a comparative analysis. American Zoologist 22, 691708.CrossRefGoogle Scholar
Grammeltvedt, A. -F. (1973). Differentiation of the tegument and associated structures in Diphyllobothrium dentriticum Nitsch (1824) (Cestoda; Pseudophyllidea). An electron microscope study. International Journal for Parasitology 3, 321–7.CrossRefGoogle Scholar
Halton, D. W. & McCrae, J. M. (1985). Development of the tegument and alimentary tract in a digenetic trematode, Fellodistomum fellis. Parasitology 90, 193204.CrossRefGoogle Scholar
Harris, A., Heath, D. D., Lawrence, S. B. & Shaw, R. J. (1987). Ultrastructure of changes at the surface during the early development phrases of Taenia ovis cysticerci in vitro. International Journal for Parasitology 17, 903–10.CrossRefGoogle Scholar
Harris, B. G. & Read, C. P. (1968). Studies on membrane transport. III. Further characterisation of amino acid systems in Hymenolepis diminuta (Cestoda). Comparative Biochemistry and Physiology 26, 545–52.CrossRefGoogle Scholar
Harris, B. G. & Read, C. P. (1969). Factors affecting protein synthesis in Hymenolepis diminuta (Cestoda). Comparative Biochemistry and Physiology 28, 645–54.CrossRefGoogle ScholarPubMed
Hayunga, E. G. & Sumner, M. P. (1986). Expression of lectin-binding surface glycoproteins during the development of Schistosoma mansoni schistosomula. Journal of Parasitology 72, 913–20.CrossRefGoogle ScholarPubMed
Henderson, D. (1977). The effect of worm age weight and number in the infection on the absorption of glucose by Hymenolepis diminuta. Parasitology 75, 277–84.CrossRefGoogle ScholarPubMed
Holy, J. M. & Oaks, J. A. (1986). Ultrastructure of the tegumental microvilli (microtriches) of Hymenolepis diminuta. Cell and Tissue Research 244, 457–66.CrossRefGoogle Scholar
Hoole, D. & Mitchell, J. B. (1983). Gorgoderina vitelliloba: an ultrastructural study on the development of the tegument from the metacercaria to the adult fluke. Parasitology 86, 323–33.CrossRefGoogle Scholar
Howells, R. E. (1980). Filariae: dynamics of the surface. In Host Invader Interplay (ed. Bossche, H. van den), pp. 6984. Amsterdam: Elsevier/North Holland.Google Scholar
Howells, R. E. & Chen, S. N. (1981). Brugia pahangi: feeding and nutrient uptake in vitro and in vivo. Experimental Parasitology 51, 4258.CrossRefGoogle ScholarPubMed
Howells, R. E., Mendis, A. M. & Bray, P. G. (1983). The mechanisms of amino acid uptake by Brugia pahangi in vitro. Zeitschrift für Parasitenkunde 69, 247–53.CrossRefGoogle ScholarPubMed
Hulinska, D. H. (1980). The morphogenesis of microtriches in the tegument of Taenia hydatigena during its larval development. Folia Parasitologia 27, 329–36.Google ScholarPubMed
Hulinska, D. H. (1981). Scanning electron microscopy of the surface of the adult Multiceps endothoracius and a comparison of its larval and adult scoleces. Folia Parasitologia 28, 249–52.Google Scholar
Hurd, H. & Arme, C. (1984). Tenebrio molitor (Coleoptera): effect of metacestodes of Hymenolepis diminuta (Cestoda) on haemolymph amino acids. Parasitology 89, 253–62.CrossRefGoogle Scholar
Hued, H. & Arme, C. (1987 a). Hymenolepis diminuta (Cestoda): the role of intermediate host sex in the establishment, growth and development of metacestodes in Tenebrio molitor (Coleoptera). Helminthologia 24, 2332.Google Scholar
Hurd, H. & Arme, C. (1987 b). Hymenolepis diminuta: effect of infection upon the patency of the follicular epithelium in the intermediate host Tenebrio molitor. Journal of Invertebrate Pathology 49, 227–34.CrossRefGoogle ScholarPubMed
Insler, G. D. (1981). Population and developmental changes in thymidine uptake kinetics of Hymenolepis diminuta (Cestoda: Cyclophyllidea) Comparative Biochemistry and Physiology 70B, 697702.Google Scholar
Isseroff, H., Bock, K., Owczarek, A. & Smith, K. R. (1983). Schistosomiasis: proline production and release by ova. Journal of Parasitology 69, 285–9.CrossRefGoogle ScholarPubMed
Isseroff, H. & Read, C. P. (1974). Studies on membrane transport. VIII. Absorption of monosaccharides by Fasdola hepatica. Comparative Biochemistry and Physiology 47A, 141–52.CrossRefGoogle Scholar
Jeffs, S. A. & Arme, C. (1984). Hymenolepis diminuta: protein synthesis in cysticercoids. Parasitology 88, 351–7.CrossRefGoogle Scholar
Jeffs, S. A. & Arme, C. (1985 a). Hymenolepis diminuta (Cestoda): uptake of cycloleucine by metacestodes. Comparative Physiology and Biochemistry 81A, 495–9.CrossRefGoogle Scholar
Jeffs, S. A.Arme, C. (1985 b). Hymenolepis diminuta: characterization of the neutral amino acid transport loci of the metacestode. Comparative Biochemistry and Physiology 81A, 387–90.CrossRefGoogle Scholar
Jeffs, S. A. & Arme, C. (1986). Echinococcus granulosus: absorption of cycloleucine and α-amino-isobutyric acid by protoscoleces. Parasitology 92, 153–63.CrossRefGoogle Scholar
Jeffs, S. A. & Arme, C. (1987). Echinococcus granulosus: specificity of amino acid transport systems in protoscoleces. Parasitology 95, 71–8.CrossRefGoogle ScholarPubMed
Jeffs, S. A. & Arme, C. (1988). Echinococcus granulosus (Cestoda): uptake of L-amino acids by secondary hydatid cysts. Parasitology (in the Press).CrossRefGoogle Scholar
Jeffs, S. A., Hurd, H., Allen, J. T. & Arme, C. (1987). Kinetics of molecular transfer across the tegument of protoscoleces and hydatid cysts of Echinococcus granulosus and the relevance of these studies to drug targeting. In Helminth Zoonoses (ed. Geerts, S., Kumar, V. and Brandt, J.), pp. 3743. Dordrecht: Martinus Nijhoff.CrossRefGoogle Scholar
Kennedy, M. W., Foley, M., Knox, K., Harnett, W., Worms, M. J., Kusel, J. R., Birmingham, J. & Garland, P. B. (1987). Are the biophysical properties of the surface lipid of filariae different from other parasitic nematodes ? In Molecular Paradigms for Eradicating Helminthic Parasites. UCLA Symposia on Molecular and Cellular Biology, New Series, vol. 59 (ed. MacInnes, A. J.). New York: Alan R. Liss (in the Press).Google Scholar
Kilejian, A. A. (1966). Permeation of L-proline in the cestode Hymenolepis diminuta. Journal of Parasitology 52, 1108–15.CrossRefGoogle ScholarPubMed
Køie, M. (1987). Scanning electron microscopy of rediae, cercariae, metacercariae and adults of Mesorchis denticulatus (Rudolphi 1802) (Trematoda, Echinostomatidae). Parasitology Research 73, 50–6.CrossRefGoogle ScholarPubMed
Lackie, A. M. (1981). Humoral mechanisms in the immune response of insects to the larvae of Hymenolepis diminuta (Cestoda). Parasite Immunology 3, 201–8.CrossRefGoogle Scholar
Luckins, A. G., Frame, I. A., Gray, M. A., Crowe, J. S. & Ross, C. A. (1986). Analysis of trypanosome variable antigen types in cultures of metacyclic and mammalian forms of Trypanosoma congolense. Parasitology 93, 99109.CrossRefGoogle ScholarPubMed
Lumsden, R. D., Oaks, J. A. & Mueller, J. F. (1974). Brush border development in the tegument of the tapeworm, Spirometra manonsoides. Journal of Parasitology 60, 209–26.CrossRefGoogle Scholar
Mackinnon, B. M. & Burt, M. D. B. (1984). The development of the tegument and cercomer of the polycephalic larvae (cercoscolices) of Paricterotaenia paradoxa (Rudolphi, 1802) (Cestoda: Dilepididae) at the ultrastructural level. Parasitology 88, 117–30.CrossRefGoogle Scholar
Mackinnon, B. M. & Burt, M. D. B. (1985 a). The comparative ultrastructure of the plerocercoid and adult primary scolex of Haplobothrium globuliforme Cooper, 1914 (Cestoda: Haplobothrioidea). Canadian Journal of Zoology 63, 1488–96.CrossRefGoogle Scholar
Mackinnon, B. M. & Burt, M. D. B. (1985 b). Histological and ultrastructural observations on the secondary scolex and strobila of Haplobothrium globuliforme (Cestoda: Haplobothrioidea). Canadian Journal of Zoology 63, 19952000.CrossRefGoogle Scholar
Mackinnon, B. M., Jarecka, L. & Burt, M. D. B. (1985). Ultrastructure of the tegument and penetration glands of developing procercoids of Haplobothrium globuliforme Cooper, 1914 (Cestoda: Haplobothrioidea). Canadian Journal of Zoology 63, 1470–7.CrossRefGoogle Scholar
Malmberg, M., Andreassen, J. & Malmberg, G. (1985). Hymenolepis diminuta: a comparison between young developing, and small, destrobilated worms in the small intestine. Zeitschrift für Parasitenkunde 71, 747–57.CrossRefGoogle Scholar
Marshall, E. & Howells, R. E. (1986). Turnover of the surface proteins of adult and third and fourth stage larval Brugia pahangi. Molecular and Biochemical Parasitology 18, 1724.CrossRefGoogle ScholarPubMed
McManus, D. P. & Smyth, J. D. (1978). Differences in the chemical composition and carbohydrate metabolism of Echinococcus granulosus (horse and sheep strains) and E. multilocularis. Parasitology 77, 103–9.CrossRefGoogle ScholarPubMed
Mills, G. L., Taylor, D. C. & Williams, J. F. (1981). Lipid composition of metacestodes of Taenia taeniaeformis and lipid changes during growth. Molecular and Biochemical Parasitology 3, 301–18.CrossRefGoogle ScholarPubMed
Ogbe, M. G. (1982). Scanning electron microscopy of tegumental surfaces of adult and developing Schistosoma margrebowiei Le Roux, 1933. International Journal for Parasitology 12, 191–8.CrossRefGoogle Scholar
Pappas, P. W. (1983). Host – parasite interface. In Biology of the Eucestoda, vol. 2, (ed. Arme, C. and Pappas, P. W.), pp. 297334. London: Academic Press.Google Scholar
Pappas, P. W. (1984). Kinetic analysis of the membrane-bound alkaline phosphatase activity of Hymenolepis diminuta (Cestoda: Cyclophyllidea) in relation to development of the tapeworm in the definitive host. Journal of Cellular Biochemistry 25, 131–7.CrossRefGoogle Scholar
Pappas, P. W. & Gamble, H. R. (1980). Membrane transport of aromatic amino acids by Hymenolepis diminuta (Cestoda). Parasitology 81, 395403.CrossRefGoogle ScholarPubMed
Pappas, P. W., Narcisi, E. M. & Rentko, V. (1983). Alterations in brush border membrane proteins and membrane-bound enzymes of the tapeworm, Hymenolepis diminuta, during development in the definitive host. Molecular and Biochemical Parasitology 8, 317–23.CrossRefGoogle ScholarPubMed
Payares, G., McLaren, D. J., Evans, W. H. & Smithers, S. R. (1985). Changes in the surface antigen profile of Schistosoma mansoni during maturation from cercaria to adult worm. Parasitology 91, 83100.CrossRefGoogle ScholarPubMed
Perry, R. N. (1977). The water dynamics of stages of Ditylenchus dipsaci and D. myceliophagus during desiccation and rehydration. Parasitology 75, 4570.CrossRefGoogle Scholar
Philipp, M. & Rumjaneck, F. D. (1984). Antigenic and dynamic properties of helminth surface structures. Molecular and Biochemical Parasitology 10, 245–68.CrossRefGoogle ScholarPubMed
Phillips, A. A. (1985). Hymenolepis diminuta: monosaccharide absorption by the cysticercoid. Ph.D. thesis, University of Keele.Google Scholar
Poljakova-Krusteva, O., Stoitsova, S. & Mizinsra-Boevska, Y. (1984). Pinocytosis in the tegument of Hymenolepis fraterna. Helminthology 17, 52–7.Google Scholar
Read, C. P. (1961). Competition between sugars in their absorption by tapeworms. Journal of Parasitology 47, 1015–16.CrossRefGoogle ScholarPubMed
Read, C. P., Rothman, A. H. & Simmons, J. E. Jr. (1963). Studies on membrane transport with special reference to parasite – host integration. Annals of the New York Academy of Sciences 113, 154205.CrossRefGoogle ScholarPubMed
Richards, K. S. & Arme, C. (1984). An ultrastructural analysis of cyst wall development in the metacestode of Hymenolepis diminuta (Cestoda). Parasitology 89, 537–66.CrossRefGoogle ScholarPubMed
Richards, K. S. & Arme, C. (1985). Phagocytosis of microvilli of the metacestode of Hymenolepis diminuta by Tenebrio molitor haemocytes. Parasitology 90, 365–74.CrossRefGoogle Scholar
Richter, H. P., Jung, D. & Passow, H. (1984). Regulatory changes of membrane transport and ouabain binding during progesterone-induced maturation of X enopus oocytes. Journal of Membrane Biology 72, 203–10.CrossRefGoogle Scholar
Roberts, L. S. (1980). Development of Hymenolepis diminuta in its definitive host. In Biology of the Tapeworm Hymenolepis diminuta, (ed. Arai, H. P.), pp. 352424. New York: Academic Press.Google Scholar
Robinson, R. D., Andreassen, J. & Arme, C. (1987). Hymenolepis diminuta: ultrastructural observations on complement-mediated tegumental lysis and destrobilation of 4-day-old worms in vitro. International Journal for Parasitology 17, 1225–32.CrossRefGoogle ScholarPubMed
Rogan, M. T. & Richards, K. S. (1987). Echinococcus granulosus: changes in the surface ultrastructure during protoscolex formation. Parasitology 94, 359–68.CrossRefGoogle ScholarPubMed
Rutherford, T. A., Webster, J. M. & Barlow, J. S. (1977). Physiology of nutrient uptake by the entomophilic nematode, Mermis nigrescens (Mermithidae). Canadian Journal of Zoology 55, 1773–81.CrossRefGoogle Scholar
Schramlova, J. & Blazek, K. (1981). Ultrastructure of the bladder tegument of Cysticercus bovis in various stages of its development. Folia Parasitologia 28, 61–9.Google ScholarPubMed
Siddiqui, A. A. & Podesta, R. B. (1985 a). Developmental regulation of protein synthesis in Hymenolepis diminuta: two dimensional electrophoretic and fluorographic analysis of protein synthesis in oncospheres. Journal of Parasitology 71, 119–22.CrossRefGoogle Scholar
Siddiqui, A. A. & Podesta, R. B. (1985 b). Developmental regulation of protein synthesis in Hymenolepis diminuta: 2-dimensional electrophoretic and fluorographic analysis of polypeptide synthesis in formation of brush border membranes. Cellular and Molecular Biology 31, 209–16.Google ScholarPubMed
Sinden, R. E. (1985). A cell biologist's view of host cell recognition and invasion by malarial parasites. Transactions of the Royal Society of Tropical Medicine and Hygiene 79, 598605.CrossRefGoogle ScholarPubMed
Stephens, G. C. (1964). Uptake of organic material by aquatic invertebrates. III. Uptake of glycine by brackish-water annelids. Biological Bulletin 126, 150–62.CrossRefGoogle Scholar
Stewart, G. L., Raines, K. M. & Kilgore, M. W. (1986). Glucose absorption in vitro by the enteric stages of Trichinella spiralis. Parasitology 93, 581–6.CrossRefGoogle ScholarPubMed
Taylor, A. E. R. & Baker, J. R. (1987). In Vitro Methods for Parasite Cultivation. 3rd edn. London: Academic Press.Google Scholar
Taylor, A. E. R. & Muller, R. (1972). Functional aspects of parasite surface. Symposia of the British Society for Parasitology, vol. 10. Oxford: Blackwell Scientific Publications.Google Scholar
Threadgold, L. T. & Dunn, J. (1983). Taenia crassiceps: regional variations in ultrastructure and evidence of endocytosis in the cysticercus' tegument. Experimental Parasitology 55, 121–31.CrossRefGoogle ScholarPubMed
Threadgold, L. T. & Dunn, J. (1984). Taenia crassiceps: basic mechanisms of endocytosis in the cystercercus. Experimental Parasitology 58, 263–9.CrossRefGoogle Scholar
Threadgold, L. T. & Robinson, A. (1984). Amplification of the cestode surface: a stereological analysis. Parasitology 89, 523–35.CrossRefGoogle Scholar
Turner, C. M. R., Barry, J. D. & Vickerman, K. (1986). Independent expression of the metacyclic and bloodstream variable antigen repertoires of Trypanosoma brucei rhodesiense. Parasitology 92, 6773.CrossRefGoogle ScholarPubMed
Ubelaker, J. E. (1983). The morphology development and evolution of tapeworm larvae. In Biology of the Eucestoda (ed. Arme, C. and Pappas, P. W.), pp. 235–96. London: Academic Press.Google Scholar
Uglem, G. L. (1980). Sugar transport by larval and adult Proterometra macrostoma (Digenea) in relation to environmental factors. Journal of Parasitology 66, 748–58.CrossRefGoogle ScholarPubMed
Uglem, G. L. (1987). Environmental sodium regulates cutaneous sugar transport in a digenean fluke. Parasitology 94, 16.CrossRefGoogle Scholar
Uglem, G. L. & Larson, O. R. (1987). Facilitated diffusion and active transport systems in metacercariae of Clinostomum marginatum (Digenea) International Journal for Parasitology 17, 847–50.CrossRefGoogle Scholar
Uglem, G. L., Lewis, M. C. & Larson, O. R. (1985). Niche segregation and sugar transport capacity of the tegument in digenean flukes. Parasitology 91, 121–7.CrossRefGoogle Scholar
Uglem, G. L. & Read, C. P. (1975). Sugar transport and metabolism in Schistosoma mansoni. Journal of Parasitology 61, 390–7.CrossRefGoogle ScholarPubMed
Vidor, E., Piens, M.-A., Abbas, M. & Petavy, A.-F. (1987). Biochimie du liquide hydatique (Echinococcus granulosus). Influence de la localisation sur la permeabilite des kystes. Annales de Parasitologie Humaine et Comparée 61, 333–40.CrossRefGoogle Scholar
Voge, M. & Heyneman, D. (1957). Development of Hymenolepis diminuta (Cestoda: Hymenolepidae) in the intermediate host, Tribolium confusum. University of California Publications in Zoology 59, 549–79.Google Scholar
Walkey, M. & Fairbairn, D. (1973). L( + )-Lactate dehydrogenases from Hymenolepis diminuta (Cestoda). Journal of Experimental Zoology 183, 365–74.CrossRefGoogle ScholarPubMed
Yoneda, K., Walzer, P. D., Richey, C. S. & Birk, M. G. (1982). Pneumocystis carinii: Freeze-fracture study of stages of the organism. Experimental Parasitology 53, 6876.CrossRefGoogle ScholarPubMed