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Neurobiology of parasitic platyhelminths: possible solutions to the problems of correlating structure with function

Published online by Cambridge University Press:  06 April 2009

R. A. Pax
Affiliation:
Departments of Pharmacology and Toxicology and Zoology, Michigan State University, East Lansing, MI 48824, USA
J. L. Bennett
Affiliation:
Departments of Pharmacology and Toxicology and Zoology, Michigan State University, East Lansing, MI 48824, USA

Extract

This paper provides an overview of research on the nervous system of parasitic platyhelminths. We have emphasized studies concerned with the physiological, pharmacological and biochemical nature of the major small molecule neurotransmitters of these parasites. We have attempted to provide a critical review of the work by focusing on important unresolved issues. Finally, we have focused on some recent work in our laboratory, using patch-clamp recording techniques and quantitative fluorescence cytometry, as an example of newer methods that will hopefully resolve some of the unanswered questions concerning the nervous system of these parasites.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1991

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References

Barker, L. R., Bueding, E. & Timms, A. R. (1966). The possible role of acetylcholine in Schistosoma mansoni. British Journal of Pharmacology 26, 656–65.Google ScholarPubMed
Basch, P. F. & Gupta, B. C. (1988). Immunocytochemical localization of regulatory peptides in six species of trematode parasites. Comparative Biochemistry and Physiology 91C, 565–70.Google ScholarPubMed
Benham, C. D., Bolton, T. B., Land, R. J. & Takewake, T. (1985). The mechanism of action of barium and TEA on single calcium-activated potassium channels in arterial and intestinal smooth muscle cell membranes. Pfluger's Archives 403, 120–7.CrossRefGoogle ScholarPubMed
Bennett, J. L. & Bueding, E. (1971). Localization of biogenic amines in Schistosoma mansoni. Comparative Biochemistry and Physiology 39A, 859–67.CrossRefGoogle ScholarPubMed
Bennett, J. L. & Bueding, E. (1973). Uptake of 5-hydroxytryptamine by Schistosoma mansoni. Journal of Molecular Pharmacology 9, 311–19.Google ScholarPubMed
Bennett, J. L. & Gianutsos, G. (1977). Distribution of catecholamine in immature Fasciola hepatica: A histochemical and biochemical study. International Journal for Parasitology 7, 221–5.CrossRefGoogle ScholarPubMed
Bennett, J. L. & Gianutsos, G. (1978). Disulfiram: A compound that selectively induces abnormal egg production and norepinephrine levels in Schistosoma mansoni. Biochemical Pharmacology 27, 817–21.CrossRefGoogle ScholarPubMed
Bettendorf, H. (1987). Über Muskulatur und Sinneszellen der Trematoden. Zoologische Jahrbucher(Anatomie) 10, 307–58.Google Scholar
Blair, K. L., Bennett, J. L. & Pax, R. A. (1988). Protein kinase-C: Its physiological demonstration in the neuromusculature of Schistosoma mansoni. Experimental Parasitology 66, 243–52.CrossRefGoogle Scholar
Blair, K. L., Day, T. A., Lewis, M. C., Bennett, J. L. & Pax, R. A. (1991). Studies on muscle cells isolated from Schistosoma mansoni: a calcium-dependent potassium channel. Parasitology 102, 251258.CrossRefGoogle Scholar
Bueding, E. (1952). Acetylcholinesterase activity of Schistosoma mansoni. British Journal of Pharmacology 7, 563–6.Google ScholarPubMed
Bueding, E., Schiller, E. L. & Bourgeois, J. G. (1966). Some physiological, biochemical and morphologic effects of tris (p-aminophenyl) carbonium salts (TAC) on S. mansoni. American Journal of Tropical Medicine and Hygiene 16, 500–15.CrossRefGoogle Scholar
Castagna, M., Takai, Y., Kaibuchi, K., Sano, K., Kikkawa, U. & Nishizika, Y. (1982). Direct activation of calcium-activated, phospholipid-dependent protein kinase by tumor-promoting phorbol esters. Journal of Biological Chemistry 257, 7847–51.CrossRefGoogle ScholarPubMed
Catto, B. A. & Ottesen, E. A. (1979). Serotonin uptake in schistosomules of Schistosoma mansoni. Comparative Biochemistry and Physiology 63, 235–42.Google Scholar
Chance, M. R. A. & Mansour, T. (1953). A contribution of the pharmacology of movement in the liver fluke. British Journal of Pharmacology 4, 713.Google Scholar
Changeux, J. P. (1981). The acetylcholine receptors: An allosteric membrane protein. Harvey Lectures, 75, 85254.Google Scholar
Dwyer, T. M. & Cuchens, J. (1987). Membrane potential measurement by flow cytometry. Journal of Electrophysiological Methods 14, 4350.Google Scholar
Estey, S. J. & Mansour, T. E. (1987). Nature of serotonin-activated cyclase during development of Schistosoma mansoni. Molecular and Biochemical Parasitology 26, 4760.CrossRefGoogle ScholarPubMed
Fetterer, R. H., Pax, R. A. & Bennett, J. L. (1977). Schistosoma mansoni: direct methods for simultaneous recording of electrical and motor activity. Experimental Parasitology 43, 286–94.CrossRefGoogle ScholarPubMed
Gianutsos, G. & Bennett, J. L. (1977). The regional distribution of dopamine and norepinephrine in Schistosoma mansoni and Fasciola hepatica. Comparative Biochemistry and Physiology 58, 157–9.Google ScholarPubMed
Gustafsson, M. K. S. (1985). Cestode neurotransmitters. Parasitology Today 1, 72–5.CrossRefGoogle ScholarPubMed
Halton, D. W., Fairweather, I., Shaw, C. & Johnston, C. F. (1990). Regulatory peptides in parasitic platyhelminths. Parasitology Today 6, 284–90.CrossRefGoogle ScholarPubMed
Hamill, O. P., Marty, A., Neher, E., Sakmann, B. & Sigworth, F. J. (1981). Improved patch-clamp techniques for high-resolution current recording from cells an cell-free membrane patch. Pfluger's Archives 391, 85100.CrossRefGoogle Scholar
Hille, B. (1984). Ionic channels of Excitable membranes. Sunderland, MA, USA: Sinauer Associates, Inc.Google Scholar
Hillman, G. R. (1983). The neuropharmacology of schistosomes. Pharmacological Therapy 22, 103–15.CrossRefGoogle ScholarPubMed
Hillman, G. R. & Senft, A. W. (1973). Schistosome motility measurements: response to drugs. Journal of Pharmacology and Experimental Therapy 185, 177–84.Google ScholarPubMed
Holmes, S. C. & Fairweather, I. (1984). Fasciola hepatica: the effects of neuropharmacological agents upon in vitro motility. Experimental Parasitology 58, 194208.CrossRefGoogle ScholarPubMed
Julius, D.MacDermott, A. B., Axel, R. & Jessel, T. M. (1988). Molecular characterization of a functional cDNA encoding the serotonin 1c receptor. Science 241, 558–64.CrossRefGoogle ScholarPubMed
Kandell, E. R. & Schwartz, J. H. (1985). Principles of Neural Science. New York: Elsevier Press.Google Scholar
Koopowitz, H., Bernado, K. & Keenan, L. (1979). Primitive nervous systems: electrical activity in the ventral nerve cords of the flatworm, Notoplana acticola. Journal of Neurobiology 10, 367–81.CrossRefGoogle ScholarPubMed
Latorre, R., Oberhauser, A., Labarca, P. & Alvarex, O. (1989). Varieties of calcium-activated potassium channels. Annual Review of Physiology 51, 385–99.CrossRefGoogle ScholarPubMed
Lee, M. B., Bueding, E. & Schiller, E. L. (1977). The occurrence and distribution of 5-hydroxytryptamine in Hymenolepis diminuta and H. nana. Journal of Parasitology 64, 257–64.CrossRefGoogle Scholar
Mansour, T. E. (1984). Serotonin receptors in parasitic worms. Advances in Parasitology 23, 136.Google ScholarPubMed
Mansour, J. M. & Mansour, T. E. (1986). GTP-binding proteins associated with serotonin-activated adenylate cyclase in Fasciola hepatica. Molecular and Biochemical Parasitology 21, 139–49.CrossRefGoogle ScholarPubMed
Maule, A. G., Halton, D. W., Johnston, C. F., Shaw, C. & Fairweather, I. (1990). The serotoninergic, cholinergic and peptidergic components of the nervous system in the monogenean parasite, Diclidophora merlangi: a cytochemical study. Parasitology 100, 255–73.CrossRefGoogle ScholarPubMed
McNall, S. J. & Mansour, T. E. (1984). Novel serotonin receptors in Fasciola; Characterization by studies on adenylate cyclase activation and LSD binding. Biochemical Pharmacology 33, 2789–97.CrossRefGoogle ScholarPubMed
Nishizuka, Y. (1988). The molecular heterogeneity of protein kinase C and its implications for cellular regulation. Nature, London 334, 661–5.CrossRefGoogle ScholarPubMed
Pax, R. A., Siefker, C. & Bennett, J. L. (1984). Schistosoma mansoni: differences in acetylcholine, dopamine and serotonin control of circular and longitudinal parasite muscle. Experimental Parasitology 58, 314–24.CrossRefGoogle Scholar
Probert, A. J. & Durrani, M. S. (1977). Fasciola hepatica and Fasciola gigantica: total cholinesterase, characteristics and effects of specific inhibitors. Experimental Parasitology 42, 203–10.CrossRefGoogle ScholarPubMed
Ramisz, A. (1967). Studies on the nervous system of nematodes and cestodes by means of a histochemical method for active acetylcholinesterase. III. Nematodes of the genus Capillaria and cestodes of the genera Dilepis and Choanotaenia. Acta Parasitologica Polonica 14, 365–85.Google Scholar
Ribeiro, P. & Webb, R. A. (1986). Demonstration of specific high-affinity binding sites for 5-hydroxytryptamine in the cestode Hymenolepis diminuta. Comparative Biochemistry and Physiology 84C, 353–8.Google ScholarPubMed
Saimi, Y. & Martinac, B. (1989). Calcium-dependent potassium channel in Paramecium studied under patch clamp. Journal of Membrane Biology 112, 7889.CrossRefGoogle ScholarPubMed
Samii, S. I. & Webb, R. A. (1990). Acetylcholine-like immunoreactivity in the cestode Hymenolepis diminuta. Brain Research 513, 161–3.CrossRefGoogle ScholarPubMed
Semeyn, D. R., Pax, R. A. & Bennett, J. L. (1982). Surface electrical activity from Schistosoma mansoni: A sensitive measure of drug action. Journal of Parasitology 68, 353–63.CrossRefGoogle ScholarPubMed
Silk, M. H. & Spence, I. M. (1969). Ultrastructural studies of the blood fluke - Schistosoma mansoni. The musculature. South African Journal of Medical Sciences 34, 1120.Google ScholarPubMed
Smyth, J. D. & Halton, D. W. (1983). The Physiology of Trematodes, 2nd End. Cambridge: Cambridge University Press.Google Scholar
Sukhdeo, M. V. K. & Mettrick, D. F. (1984). Migrational responses of Hymenolepis diminuta to surgical alterations of gastrointestinal tract. International Journal for Parasitology 13, 355–8.CrossRefGoogle Scholar
Sukhdeo, M. V. K. & Mettrick, D. F. (1987). Parasite behaviour: understanding platyhelminth responses. Advances in Parasitology 26, 73144.CrossRefGoogle ScholarPubMed
Sukhdeo, S. C., Sangster, N. C. & Mettrick, D. F. (1986). Effects of cholinergic drugs on longitudinal muscle contractions of Fasciola hepatica. Journal of Parasitology 72, 492–7.CrossRefGoogle ScholarPubMed
Thompson, C. S., Sangster, N. C. & Mettrick, D. F. (1986). Cholinergic inhibition of muscle contraction in Hymenolepis diminuta. Canadian Journal of Zoology 64, 2111–5.CrossRefGoogle Scholar
Tomosky, K. T., Bueding, E. & Bennett, J. L. (1974). Tryptaminergic and dopaminergic response of Schistosoma mansoni. Journal of Pharmacology and Experimental Therapeutics 190, 260–71.Google ScholarPubMed
Wade, M. H., Trosko, J. E. & Schindler, M. (1986). A fluorescence photobleaching assay of gap junction-mediated communication between human cells. Science 232, 525–8.CrossRefGoogle ScholarPubMed
Webb, R. A. (1986). The uptake and metabolism of L-glutamate by tissue slices of the cestode Hymenolepis diminuta. Comparative Biochemistry and Physiology 85C, 151–62.Google ScholarPubMed
Webb, R. A. & Eklove, H. (1989). Demonstration of intense glutamate-like immunoreactivity in the longitudinal nerve cords of the cestode Humenolepis diminuta. Parasitology Research 75, 545–8.CrossRefGoogle ScholarPubMed
Weller, T. H. & Wheeldon, S. K. (1982). The cultivation in vitro of cells derived from adult Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 31, 335–48.CrossRefGoogle ScholarPubMed
Wood, P. J. & Mansour, T. E. (1986). Schistosoma mansoni: serotonin uptake and it drug metabolism. Experimental Parasitology 62, 114–9.CrossRefGoogle Scholar
Zernecke, E. (1985). Untersuchungen über den feineren Ban den Cestoden. Zoologische Jahrbucher 9, 92161.Google Scholar