Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-23T16:52:47.851Z Has data issue: false hasContentIssue false
  • English
  • Français

Fasciola hepatica: the effect of the microtubule inhibitors colchicine and tubulozole-C on the ultrastructure of the adult fluke

Published online by Cambridge University Press:  06 April 2009

A. W. Stitt  and
I. Fairweather
A. W. Stitt
Affiliation:
School of Biology and Biochemistry, The Queen's University of Belfast, Belfast B T7 INN
I. Fairweather
Affiliation:
School of Biology and Biochemistry, The Queen's University of Belfast, Belfast B T7 INN
Get access Rights & Permissions [Opens in a new window]

Summary

The effect of the microtubule inhibitors coichicine (1×10−3 M) and tubulozole-C(1×10−6 M) on the ultrastructure of adult Fasciola hepatica has been determined in vitro by transmission electron microscopy (TEM), using both intact flukes and tissue-slice material. With colchicine treatment, the apical membrane of the tegument became increasingly convoluted and blebbed, while accumulations of T1 secretory bodies occurred in the basal region of the syncytium, leading to progressively fewer secretory bodies in the syncytium. In the tegumental cells there were distinct accumulations of T1 secretory bodies around the Golgi complexes, which remained active for up to 12 h incubation. Tubulozole-treated flukes showed more severe effects, with initial accumulations of secretory bodies, both at the tegumental apex and base. This was followed in the later time-periods by the sloughing of the tegumental syncytium. In the underlying tegumental cells, the granular endoplasmic reticulum (GER) cisternae were swollen and disrupted, becoming concentrated around the nucleus. The Golgi complexes were dispersed to the periphery of the cells and gradually disappeared from the cytoplasm. After treatment with both drugs, the cell population in the vitelline follicles was altered, with an abnormally large proportion of stem cells and relatively few intermediate type I cells. The nurse cell cytoplasm became fragmented and was no longer in contact with the vitelline cells, while the shell globule clusters within the intermediate type 2 and mature cells were loosely packed. In the mature vitelline cells, ‘yolk’ globules and glycogen deposits became fewer than normal and lipid droplets were observed. The results are discussed in relation to the different modes of action of the two drugs and potential significance of this to anthelmintic (benzimidazole) therapy.

Keywords

Fasciola hepaticaliver flukemicrotubule inhibitorscolchicinetubulozoletransmission electron microscopy (TEM)
Type
Research Article
Information
Parasitology , Volume 107 , Issue 3 , September 1993 , pp. 297 - 309
Copyright
Copyright © Cambridge University Press 1993

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

Abbas, M. K. & Cain, G. D. (1987). Actin and intermediate-sized filaments of the spines and cytoskeleton of Schistosoma mansoni. Parasitology Research 73, 66–74.CrossRefGoogle ScholarPubMed
Bennett, C. E., Hughes, D. L. & Harness, E. (1980). Fasciola hepatica: changes in tegument during killing of adult flukes surgically transferred to sensitized rats. Parasite immunology 2, 39–55.CrossRefGoogle Scholar
Boisvieux-Ulrich, C., Lainé, M.-C. & Sandoz, D. (1989). In vitro effects of colchicine and nocodazole on ciliogenesis in quail oviduct. Biology of the Cell 67, 67–79.CrossRefGoogle ScholarPubMed
Borgers, M. & De Nollin, S. (1975). Ultrastructural changes in Ascaris suum intestine after mebendazole treatment in vivo. Journal of Parasitology 61, 110–22.CrossRefGoogle ScholarPubMed
Borgers, M., De Nollin, S., De Brabander, M. & Thienpont, D. (1975 a). Influence of the anthelmintic mebendazole on microtubules and intracellular organelle movement in nematode intestinal cells. American Journal of Veterinary Research 36, 1153–66.Google Scholar
Borgers, M., De Nollin, S., Verheyen, A., Vanparijs, O. & Thienpont, D. (1975 b). Morphological changes in cysticerci of Taenia taeniaeformis after mebendazole treatment. Journal of Parasitology 61, 830–43.CrossRefGoogle ScholarPubMed
Burton, P. R. (1968). Effects of various treatments on microtubules and axial units of lung-fluke spermatozoa. Zeitschrift für Zellforschung 87, 226–48.CrossRefGoogle ScholarPubMed
Campbell, W. C. (1990). Benzimidazoles: veterinary uses. Parasitology Today 6, 130–3.CrossRefGoogle ScholarPubMed
Coffe, G. & Raymond, M.-N. (1990). Association between microtubules and Golgi vesicles isolated from rat parotid glands. Biologie Cellulaire 70, 143–52.CrossRefGoogle ScholarPubMed
Coles, G. C. (1986). Anthelmintic activity of triclabendazole. Journal of Helminthology 60, 210–12.CrossRefGoogle ScholarPubMed
De Brabander, M., Geuens, G., Nuydens, R., Willebrords, R., Moeremans, M., Van Ginckel, R., Distelmans, W., Dragonetti, C. & Mareel, M. (1986). Tubulozole: a new stereoselective microtubule inhibitor. Annals of the New York Academy of Sciences 466, 757–66.Google Scholar
Dabora, S. L. & Sheetz, M. P. (1988). The microtubuledependent formation of a tubulovesicular network with characteristics of the ER from cultured cell extracts. Cell 54, 27–35.CrossRefGoogle ScholarPubMed
Dustin, P. (1984). Microtubules, 2nd, Edn.Berlin, Heidelberg, New York: Springer.Google Scholar
Fairweather, I., Anderson, H. R. & Threadgold, L. T. (1986). Fasciola hepatica: tegumental changes induced in vitro by the deacetylated (amine) metabolite of diamphenethide. Experimental Parasitology 62, 336–48.Google Scholar
Fairweather, I., Anderson, H. R. & Threadgold, L. T. (1988). Fasciola hepatica: morphological changes in vitelline cells following treatment in vitro with the deacetylated (amine) metabolite of diamphenethide (DAMD). International Journal for Parasitology 18, 1061–9.CrossRefGoogle ScholarPubMed
Fetterer, R. H. (1986). The effect of albendazole and triclabendazole on colchicine binding in the liver fluke Fasciola hepatica. Journal of Veterinary Pharmacology and Therapeutics 9, 49–54.CrossRefGoogle ScholarPubMed
Geuens, G. M. A., Nuydens, R. M., Willebrords, R. E., Van De Veire, R. M. L., Goosens, F., Dragonetti, C. H., Mareel, M. M. K. & De Brabander, M. J. (1985). Effects of tubulozole on the microtubule system of cells in culture and in vivo. Cancer Research 45, 733–42.Google ScholarPubMed
Goldman, R. D., Hill, B. F., Steinert, P., Whitman, M. A. & Zackroff, R. V. (1980). Intermediate filament–microtubule interactions: evidence in support of a common organisation centre. In Microtubules and Microtubule Inhibitors (ed. De Brabander, M. & De Mey, J.), pp. 91–102. Amsterdam: Elsevier/NorthHolland Biomedical Press.Google Scholar
Hanna, R. E. B. (1976). Fasciola hepatica: a light and electron microscope autoradiographic study of incorporation of monosaccharides into glycogen and glycoprotein. Experimental Parasitology 39, 204–13.CrossRefGoogle ScholarPubMed
Hanna, R. E. B. (1980 a). Fasciola hepatica: glycocalyx replacement in the juvenile as a possible mechanism for protection against host immunity. Experimental Parasitology 50, 103–14.Google Scholar
Hanna, R. E. B. (1980 b). Fasciola hepatica: an immunofluorescent study of antigenic changes in the tegument during development in the rat and the sheep. Experimental Parasitology 50, 155–70.CrossRefGoogle ScholarPubMed
Hanna, R. E. B. (1980 c). Fasciola hepatica: autoradiography of protein synthesis, transport, and secretion by the tegument. Experimental Parasitology 50, 297–304.CrossRefGoogle ScholarPubMed
Hanna, R. E. B. & Threadgold, L. T. (1975). Development of an in vitro technique for cytological investigations of slices of Fasciola hepatica: evaluation by morphological criteria. International Journal for Parasitology 5, 321–31.CrossRefGoogle Scholar
Ho, W. C., Allan, V. J., Meer, G., Van Berger, E. G. & Kreis, T. E. (1989). Reclustering of scattered Golgi elements occurs along microtubules. European Journal of Cell Biology 48, 250–63.Google ScholarPubMed
Iida, H. & Shibata, Y. (1991). Functional Golgi units in microtubule-disrupted cultured atrial monocytes. Journal of Histochemistry and Cytochemistry 39, 1349–55.CrossRefGoogle Scholar
Ireland, C. M., Gull, K., Gutteridge, W. E. & Pogson, C. I. (1979). The interaction of benzimidazole carbamates with mammalian microtubule protein. Biochemical Pharmacology 28, 2680–2.CrossRefGoogle Scholar
Irwin, S. W. B. & Threadgold, L. T. (1970). Electron-microscope studies on Fasciola hepatica. VIII. The development of the vitelline cells. Experimental Parasitology 28, 399–411.CrossRefGoogle ScholarPubMed
Isseroff, H. & Read, C. P. (1969). Studies on membrane transport-VI. Absorption of amino acids by fascioliid trematodes. Comparative Biochemistry and Physiology 30, 1153–60.CrossRefGoogle ScholarPubMed
Isseroff, H. & Read, C. P (1974). Studies on membrane transport-VIlI. Absorption of monosaccharides by Fasciola hepatica. Comparative Biochemistry and Physiology [A] 47, 141–52.CrossRefGoogle Scholar
Kelly, R. B. (1990). Microtubules, membrane traffic, and cell organization. Cell 61, 5–7.Google Scholar
Köhler, P. & Bachmann, R. (1981). Intestinal tubulin as a possible target for the chemotherapeutic action of mebendazole in parasitic nematodes. Molecular and Biochemical Parasitology 4, 325–36.CrossRefGoogle ScholarPubMed
Kreis, T. E. (1990). Role of microtubules in the organisation of the Golgi apparatus. Cell Motility and the Cytoskeleton 15, 67–70.Google Scholar
Lacey, E. (1988). The role of the cytoskeletal protein, tubulin, in the mode of action and mechanism of drug resistance to benzimidazoles. International Journal for Parasitology 18, 885–936.Google Scholar
Lackie, J. M. (1986). Cell Movement and Cell Behaviour. London: Allen and Unwin.Google Scholar
Laclette, J. P., Merchant, M. T., Willms, K. & Canñedo, L. (1981). Paracrystalline bundles of large tubules, induced in vitro by mebendazole in Cysticercus cellulosae. Parasitology 83, 513–18.CrossRefGoogle Scholar
Lazarides, E (1980). Intermediate filaments as mechanical integrators of cellular space. Nature, London 283, 246–56.CrossRefGoogle ScholarPubMed
Lee, C. & Chen, L. B. (1988). Dynamic behavior of endoplasmic reticulum in living cells. Cell 54, 37–46.CrossRefGoogle ScholarPubMed
Lee, C., Ferguson, M. & Chen, L. B. (1989). Construction of the endoplasmic reticulum. Journal of Cell Biology 109, 2045–55.Google Scholar
McCracken, R. O. & Stillwell, W. H. (1991). A possible biochemical mode of action for benzimidazole anthelmintics. International Journal for Parasitology 21, 99–104.CrossRefGoogle ScholarPubMed
McIntosh, J. R. & Pfarr, C. M. (1991). Mitotic motors. Journal of Cell Biology 115, 577–85.CrossRefGoogle ScholarPubMed
Mareel, M. M. & De Mets, M. (1984). Effect of microtubule inhibitors on invasion and on related activities of tumor cells. International Review of Cytology 90, 125–68.CrossRefGoogle ScholarPubMed
Ornelles, D. A., Fey, E. G. & Penman, S. (1986). Cytochalasin releases mRNA from the cytoskeletal framework and inhibits protein synthesis. Molecular and Cellular Biology 6, 1650–62.Google ScholarPubMed
Pavelka, M. & Ellinger, A. (1983). Effect of colchicine on the Golgi complex of rat pancreatic acinar cells. Journal of Cell Biology 97, 737–48.CrossRefGoogle ScholarPubMed
Rogalski, A. A. & Singer, S. J. (1984). Associations of elements of the Golgi apparatus with microtubules. Journal of Cell Biology 99, 1092–100.Google Scholar
Rogan, M. T. & Threadgold, L. T. (1984). Fasciola hepatica: tegumental alterations as a consequence of lectin binding. Experimental Parasitology 57, 248–60.CrossRefGoogle ScholarPubMed
Sandoval, I. V., Bonifacino, J. S., Klausner, R. D., Henkart, M. & Wehland, J. (1984). Role of microtubules in the organization and localization of the Golgi apparatus. Journal of Cell Biology 99, 113s–18s.CrossRefGoogle ScholarPubMed
Sarwin, K. E. & Scholey, J. M. (1991). Motor proteins in cell division. Trends in Cell Biology 1, 122–9.Google Scholar
Skuce, P. J. & Fairweather, I. (1988). Fasciola hepatica: perturbation of secretory activity in the vitelline cells by the sodium ionophore monensin. Experimental Parasitology 65, 20–30.Google Scholar
Skuce, P. J. & Fairweather, I. (1989). Fasciola hepatica: the effect of the sodium ionophore monensin on the adult tegument. Parasitology Research 75, 223–32.Google Scholar
Skuce, P. J. & Fairweather, I. (1990). The effect of the hydrogen ionophore closantel upon the pharmacology and ultrastructure of the adult liver fluke Fasciola hepatica. Parasitology Research 76, 241–50.CrossRefGoogle ScholarPubMed
Soifer, D. (1986). Dynamic aspects of microtubule biology. Annals of the New York Academy of Sciences, 466, 1–7.Google Scholar
Spurr, A. R. (1969). A low-viscosity epoxy resin embedding medium for electron microscopy. Journal of Ultrastructure Research 26, 31–43.CrossRefGoogle ScholarPubMed
Stitt, A. W. & Fairweather, I. (1991). Fasciola hepatica: the effect of the microfilament inhibitor cytochalasin B on the ultrastructure of the adult fluke. Parasitology Research 77, 675–85.Google Scholar
Stitt, A. W. & Fairweather, I. (1932). Spermatogenesis in Fasciola hepatica: an ultrastructural comparison of the effects of the anthelmintic, triclabendazole (‘Fasinex’) and the microtubule inhibitor, tubulozole. Invertebrate Reproduction and Development 22, 139–50.Google Scholar
Stitt, A. W., Fairweather, I. & Johnston, C. F. (1991). Fasciola hepatica: disruption of spermatogenesis by the microfilament inhibitor cytochalasin B. Parasitology Research 77, 123–8.CrossRefGoogle ScholarPubMed
Stitt, A. W., Fairweather, I., Trudgett, A. G. & Johnston, C. F. (1992). Fasciola hepatica: localization and partial characterization of tubulin. Parasitology Research 78, 103–7.Google Scholar
Terasaki, M., Chen, L. B. & Fujiwara, K. (1986). Microtubules and the endoplasmic reticulum are highly interdependent structures. Journal of Cell Biology 103, 1557–68.Google Scholar
Threadgold, L. T. (1963). The tegument and associated structures of Fasciola hepatica. Quarterly Journal of the Microscopical Society 104, 505–12.Google Scholar
Threadgold, L. T. (1967). Electron microscope studies of Fasciola hepatica. III. Further observations on the tegument and associated structures. Parasitology 57, 633–7.CrossRefGoogle Scholar
Threadgold, L. T. & Brennan, G. P. (1978). Fasciola hepatica: basal infolds and associated vacuoles of the tegument. Experimental Parasitology 46, 300–16.Google Scholar
Thyberg, J. & Moskalewski, S. (1985). Microtubules and the organization of the Golgi complex. Experimental Cell Research 159, 1–16.Google Scholar
Traas, J. A., Burgain, S. & De Vaulx, R. D. (1989). The organization of the cytoskeleton during meiosis in eggplant (Solanum melongena (L)): microtubules and F-actin are both necessary for coordinated meiotic division. Journal of Cell Science 92, 541–50.CrossRefGoogle Scholar
Turner, J. R. & Tartakoff, A. M. (1989). The response of the Golgi complex to microtubule alterations: the roles of metabolic energy and membrane traffic in Golgi complex organization. Journal of Cell Biology 109, 2081–8.CrossRefGoogle ScholarPubMed
Vale, R. D (1992). Microtubule motors: many new models off the assembly line. Trends in Biochemical Sciences 17, 300–4.CrossRefGoogle ScholarPubMed
Van Den Bossche, H., Rochette, F. & Hörig, C. (1982). Mebendazole and related anthelmintics. Advances in Pharmacology and Chemotherapy 19, 67–128.Google Scholar
Van Ginckel, R., De Brabander, M., Vanherck, W. & Heeres, J. (1984). The effects of tubulazole, a new synthetic microtubule inhibitor on experimental neoplasms. European Journal of Cancer and Clinical Oncology 20, 99–105.CrossRefGoogle ScholarPubMed
Verheyen, A., Borgers, M., Vanparijs, O. & Thienpont, D. (1976). The effects of mebendazole on the ultrastructure of cestodes. In Biochemistry of Parasites and Host–Parasite Relationships (ed. Van den Bossche, H.), pp. 605–18. Amsterdam: Elsevier/North-Holland Biomedical Press.Google Scholar
Watts, S. D. M. (1981). Colchicine binding in the rat tapeworm, Hymenolepis diminuta. Biochimica et Biophysica Acta 667, 59–69.Google Scholar
Wilson, L. & Bryan, J. (1974). Biochemical and pharmacological properties of microtubules. Advances in Cell and Molecular Biology 3, 21–72.Google Scholar