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The serotoninergic, cholinergic and peptidergic components of the nervous system in the monogenean parasite,Diclidophora merlangi: a cytochemical study

  • A. G. Maule (a1), D. W. Halton (a1), C. F. Johnston (a2), C. Shaw (a2) and I. Fairweather (a1)...


Confocal scanning laser microscopy has been employed with immunocytochemical techniques to map the distribution of serotoninergic and peptidergic components in the nervous system of the monogenean gill-parasite, Diclidophora merlangi; results are compared with the distribution of cholinergic components, following histochemical staining for cholinesterase activity. While all three neurochemical elements are present in the central and peripheral nervous systems, the cholinergic and peptidergic systems dominate the CNS, whereas the PNS has a majority of serotoninergic nerve fibres. The cholinergic and peptidergic neuronal pathways overlap extensively in staining patterns, suggesting possible co-localization of acetylcholine and neuropeptides. Within the peptidergic nervous system, immunoreactivity to the pancreatic polypeptide family of peptides and FMRFamide were the most prevalent.



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Abrahams, S. L., Northup, J. K. & Mansour, T. E. (1976). Adenosine cyclic 3′,5′-monophosphate in the liver fluke, Fasciola hepatica. I. Activation of adenylate cyclase by 5-hydroxytryptamine. Molecular Pharmacology 12, 4958.
Andreini, C. C., Beretta, C., Faustini, B. & Galliana, G. (1970). Spectrofluorimetric and chromatographic characterization of a butanol extract from Fasciola hepatica. Experientia 26, 166–7.
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.
Beauvillain, J. C., Tramu, G. & Garaud, J. (1984). Coexistence of substances related to enkephalin and somatostatin in granules of the guinea-pig median eminence: demonstration by use of colloidal gold immunocytochemical methods. Brain Research 301, 389–93.
Bennett, J. L. & Gianutsos, G. (1977). Distribution of catecholamines in immature Fasciola hepatica: a histochemical and biochemical study. International Journal for Parasitology 7, 221–5.
Boer, H. H., Schot, L. P. C., Veenstra, J. A. & Reichelt, D. (1980). Immunocytochemical identification of neural elements in the central nervous system of the snail, some insects, a fish, and a mammal with an antiserum to the molluscan cardio-excitatory tetrapeptide FMRF-amide. Cell and Tissue Research 213, 21–7.
Brand, T. Von (1966). Biochemistry of Parasites. New York and London: Academic Press.
Bueding, E. (1952). Acetylcholinesterase activity of S. mansoni. British Journal of Pharmacology 7, 563–6.
Chance, M. R. A. & Mansour, T. E. (1953). A contribution to the pharmacology of movement in the liver fluke. British Journal of Pharmacology 8, 1098–102.
Chen, S.-T., Tsai, M. S. & Shen, C. L. (1989). Distribution of FMRFamide-like immunoreactivity in the central nervous system of the Formosan monkey (Macaca cyclopsis). Peptides 10, 825–34.
Chou, T.-C. T., Bennett, J. & Bueding, E. (1972). Occurrence and concentrations of biogenic amines in trematodes. Journal of Parasitology 58, 1098–102.
Coons, A. H., Leduc, E. H. & Connolly, J. M. (1955). Studies on antibody production. I. A method for the histochemical demonstrations of specific antibody and its application to a study of the hyper-immune rabbit. Journal of Experimental Medicine 102, 4960.
Cottrell, G. A. (1989). The biology of the FMRFamide series of peptides in molluscs with special reference to Helix. Comparative Biochemistry and Physiology 993A, 41–5.
Cottrell, G. A., Schot, L. P. C. & Dockray, G. J. (1983). Identification and probable role of a single neuron containing the neuropeptide Helix FMRFamide. Nature, London 304, 638–40.
Dockray, G. J. (1977). Progress in gastroenterology. Molecular evolution of gut hormones: application of comparative studies on the regulation of digestion. Gastroenterology 72, 344–58.
Dockray, G. J., Vaillant, C. & Williams, R. G. (1981). New vertebrate brain—gut peptide related to a molluscan neuropeptide and an opioid peptide. Nature, London 293, 656–7.
Duve, H. & Thorpe, A. (1981). Gastrin/cholecystokinin (CCK)-like immunoreactive neurones in the brain of the blowfly, Calliphora erythrocephala (Diptera). General and Comparative Endocrinology 43, 381–91.
Duve, H. & Thorpe, A. (1982). The distribution of pancreatic polypeptide in the nervous system and gut of the blowfly, Calliphora vomitaria (Diptera). Cell and Tissue Research 227, 6777.
El-Salhy, M., Grimelius, L., Emson, P. C. & Falkmer, S. (1987). Polypeptide YY- and neuropeptide Y-immunoreactive cells and nerves in the endocrine pancreas of some vertebrates: an onto- and phylogenetic study. Histochemical Journal 19, 111–17.
Endo, Y., Iwanaga, T., Fujita, T. & Nishiitsutsuji-Uwo, J. (1982). Localization of pancreatic polypeptide (PP) like immunoreactivity in the central and visceral nervous systems of the cockroach Periplaneta. Cell and Tissue Research 227, 19.
Fairweather, I., Macartney, C. A., Johnston, C. F., Halton, D. W. & Buchanan, K. D. (1988). Immunocytochemical demonstration of 5- hydroxytryptamine (serotonin) and vertebrate neuropeptides in the nervous system of excysted cysticercoid larvae of the rat tapeworm, Hymenolepis diminuta (Cestoda, Cyclophillidea). Parasitology Research 74, 371–9.
Fairweather, I., Maule, A. C., Mitchell, S. H., Johnston, C. F. & Halton, D. W. (1987). Immunocytochemical demonstration of 5-hydroxytryptamine (serotonin) in the nervous system of the liver fluke, Fasciola hepatica (Trematoda, Digenea). Parasitology Research 73, 255–8.
Falkmer, S., El-Salhy, M. & Titlbach, M. (1984). Evolution of the neuroendocrine system in vertebrates. A review with particular reference to the phylogeny and postnatal maturation of the islet parenchyma. In Evolution and Tumor Pathology of the Neuroendocrine System (ed. Falkmer, S., Hakanson, R. & Sundler, F.), pp. 5987. Amsterdam, New York and Oxford: Elsevier.
Fetterer, R. H., Pax, R. A. & Bennett, J. L. (1977). Schistosoma mansoni: direct method for simultaneous recording of electrical and motor activity. Experimental Parasitology 43, 286–94.
Florey, E. (1967). Neurotransmitters and modulators in the animal kingdom. Federation Proceedings 26, 1164–78.
Fripp, P. J. (1967). Histochemical localization of esterase activity in schistosomes. Experimental Parasitology 21, 380– 90.
Fritsch, H. A. R., Van Noorden, S. & Pearse, A. G. E. (1982). Gastrointestinal and neurohormonal peptides in the alimentary tract and cerebral complex of Ciona intestinalis (Ascidiaceae). Cell and Tissue Research 233, 369402.
Gentleman, S., Abrahams, S. L. & Mansour, T. E. (1976). Adenosine cyclic 3′,5′-monophosphate in the liver fluke Fasciola hepatica. II. Activation of protein kinase by 5-hydroxytryptamine. Molecular Pharmacology 12, 5968.
Gianutsos, G. & Bennett, J. L. (1977). The regional distribution of dopamine and norepinephrine in Schistosoma mansoni and Fasciola hepatica. Comparative Biochemistry and Physiology 58C, 157–9.
Glattli, E., Rudin, W. & Hecker, H. (1987). Immunoelectron microscope demonstration of pancreatic polypeptide in midgut epithelium of haematophagous dipterans. Journal of Histochemistry and Cytochemistry 35, 891–6.
Gomori, G. (1952). Microscopic Histochemistry, Principles and Practice. Chicago: University of Chicago Press.
Greenberg, M. J., Price, D. A. & Lehman, H. K. (1985). FMRFamide-like peptides of molluscs and vertebrates: distribution and evidence of function. In Neurosecretion and the Biology of Neuropeptides (ed. Kobayashi, H., Bern, H. A. & Urano, A.), pp. 370–6. Berlin, Heidelberg and New York: Japan Scientific Society Press/Springer.
Grimmelikhuijzen, C. J. P. (1983). FMRFamide immunoreactivity is generally occurring in the nervous systems of coelenterates. Histochemistry 78, 361–81.
Grimmelikhuijzen, C. J. P. (1986). FMRFamide-like peptides in the primitive nervous systems of higher animals. In Handbook of Comparative Opioid and Related Neuropeptide Mechanisms, Vol. 1 (ed. Stefano, G. B.), pp. 103–15. Boca Raton, Florida: CRC Press.
Grimmelikhuijzen, C. J. P., Balfe, A., Carraway, R., Emson, P. C., Powell, D., Rehfeld, J. F., Rokaeus, A. & Sundler, F. (1981). The presence of brain–gut peptides in the nervous system of coelenterates. Abstracts of International Symposium on Brain—Gut Axis: The New Frontier.
Gustafsson, M. K. S. (1985). Cestode neurotransmitters. Parasitology Today 1, 72–5.
Gustafsson, M. K. S. (1987). Immunocytochemical demonstration of neuropeptides and serotonin in the nervous system of adult Schistosoma mansoni. Parasitology Research 74, 168–74.
Gustafsson, M. K. S., Lehtonen, M. A. I. & Sundler, F. (1986). Immunocytochemical evidence for the presence of ‘mammalian’ neurohormonal peptides in neurones of the tapeworm Diphyllobothrium dendriticum. Cell and Tissue Research 243, 41–9.
Gustafsson, M. K. S. & Wikgren, W. C. (1989). Development of immunoreactivity to the invertebrate neuropeptide small cardiac peptide B in the tapeworm Diphyllobothrium dendriticum. Parasitology Research 75, 396400.
Gustafsson, M. K. S., Wikgren, M. C., Karhi, T. J. & Schot, L. P. C. (1985). Immunocytochemical demonstration of neuropeptides and serotonin in the tapeworm Diphyllobothrium dendriticum. Cell and Tissue Research 240, 255–60.
Halton, D. W. (1979). The surface topography of a monogenean, Diclidophora merlangi, revealed by scanning electron microscopy. Zeitschrift für Parasitenkunde 61, 112.
Halton, D. W. & Arme, C. (1971). An in vitro technique for detecting tissue damage in Diclidophora merlangi: possible screening method for selection of undamaged tissues or organisms prior to physiological investigation. Experimental Parasitology 30, 54–7.
Halton, D. W., Maule, A. G., Johnston, C. F. & Fairweather, I. (1987). Occurrence of 5-hydroxytryptamine (serotonin) in the nervous system of a monogenean, Diclidophora merlangi. Parasitology Research 74, 151–4.
Halton, D. W. & Morris, G. P. (1969). Occurrence of cholinesterase and ciliated sensory structures in a fish gill fluke, Diclidophora merlangi (Trematoda: Monogenea). Zeitschrift für Parasitenkunde 33, 2130.
Hanley, M. R. & Iversen, L. L. (1980). Substance P receptors. In Neurotransmitter Receptors. Part I, Amino Acids, Peptides and Benzodiazepines (ed. Enna, S. J. & Yamamura, H. I.) pp. 71103. London: Chapman and Hall.
Hariri, M. J. (1974). Occurrence and concentration of biogenic amines in Mesocestoides corti (Cestoda). Journal of Parasitology 60, 737–43.
Hillman, G. R. & Senft, A. W. (1973). Schistosome motility measurements: response to drugs. Journal of Pharmacology and Experimental Therapeutics 185, 177–84.
Hökfelt, T., Johansson, O., Ljungdahl, A., Lundberg, J. M. & Schultzberg, M. (1980). Peptidergic neurones. Nature, London 284, 515–21.
Hökfelt, T., Lundberg, J. M., Skirboll, L., Johansson, O., Schultzberg, M. & Vincent, S. R. (1982). Coexistence of classical transmitters and peptides in neurons. In Co-transmission (ed. Cuello, A. C.), pp. 77–125. London: Macmillan.
Hökfelt, T., Millhorn, D., Seroogy, K., Tsuruo, Y., Ceccatelli, S., Lindh, B., Meister, B., Melander, T., Schalling, M., Bartfai, T. & Terenius, L. (1987). Coexistence of peptides with classical neurotransmitters. Experientia 43, 768–80.
Holmes, S. D. & Fairweather, I. (1984). Fasciola hepatica: the effects of neuropharmacological agents upon in vitro motility. Experimental Parasitology 58, 194208.
Kaloustian, K. V. & Edmands, J. A. (1986). Immunochemical evidence for substance P-like peptide in tissues of the earthworm Lumbricus terrestris: action on intestinal contraction. Comparative Biochemistry and Physiology 83C, 329–33.
Kasschau, M. R. & Mansour, T. E. (1982 a). Adenylate cyclase in adults and cercariae of Schistosoma mansoni. Molecular and Biochemical Parasitology 5, 107–16.
Kasschau, M. R. & Mansour, T. E. (1982 b). Serotonin-activated adenylate cyclase during early development of Schistosoma mansoni. Nature, London 296, 66–8.
Koelle, I. E. (1951). Elimination of enzymatic diffusion artifacts in histochemical localization of cholinesterase and survey of their cellular distribution. Journal of Pharmacology and Experimental Therapeutics 114, 167–84.
Kralj, N. (1967). Morphologic and histochemical studies on the nervous system of tapeworms revealed by the cholinesterase method (Taenia hydatigena, Dipylidium caninum and Moniezia expansa). Veterinarski Arhiv 37, 277–86.
Li, C. & Calabrese, R. L. (1983). Evidence for proctolin like substances in the central nervous system of the leech. Society of Neuroscience 9, 76.
Lundberg, J. M. & Hökfelt, T. (1983). Coexistence of peptides and classical neurotransmitters. Trends in Neuropharmacological Sciences 6, 325–33.
Magee, R. M., Fairweather, I., Johnston, C. F., Halton, D. W. & Shaw, C. (1989). Immunocytochemical demonstration of neuropeptides in the nervous System of the liver fluke, Fasciola hepatica (Trematoda, Digenea). Parasitology 98, 227–38.
Magee, R. M., Foy, W. L., Fairweather, I., Johnston, C. F., Halton, D. W. & Buchanan, K. D. (1987). Substance P immunoreactivity in the liver fluke, Fasciola hepatica. Regulatory Peptides 18, 363.
Maggio, J. E. (1988). Tachykinins. Annual Reviews in Neuroscience 11, 1328.
Mansour, T. E. (1979). Chemotherapy of parasitic worms: new biological strategies. Science 205, 462–9.
Mansour, T. E. (1984). Serotonin receptors in parasitic worms. Advances in Parasitology 23, 136.
Mansour, T. E. & Stone, D. B. (1970). Biochemical effects of lysergic acid diethylamide on the liver fluke, Fasciola hepatica. Biochemical Pharmacology 19, 1137–45.
Maule, A. G., Halton, D. W., Johnston, C. F., Fairweather, I. & Shaw, C. (1989 a). Immunocytochemical demonstration of neuropeptides in the fish-gill parasite, Diclidophora merlangi (Monogenoidea). International Journal for Parasitology 19, 307–16.
Maule, A. G., Halton, D. W., Allen, J. M. & Fairweather, I. (1989 b). Studies on motility in vitro of an ectoparasitic monogenean, Diclidophora merlangi. Parasitology 98, 8593.
Maule, A. G., Shaw, C., Halton, D. W., Johnston, C. F. & Fairweather, I. (1989 c). Localization, quantification and characterization of pancreatic polypeptide immunoreactivity in the parasitic flatworm Diclidophora merlangi and its fish host (Merlangius merlangus). General and Comparative Endocrinology 74, 50–6.
Maule, A. G., Shaw, C., Halton, D. W., Johnston, C. F., Fairweather, I. & Buchanan, K. O. (1989 d). Tachykinin immunoreactivity in the parasitic flatworm Diclidophora merlangi and its fish host the whiting (Merlangius merlangus): radioimmunoassay and chromatographic characterisation using region-specific substance P and neurokinin A antisera. Comparative Biochemistry and Physiology (in the Press).
Nawa, H., Hirose, T., Takashima, H., Inayama, S. & Nakanishi, S. (1983). Nucleotide sequence of cloned cDNA's for two types of bovine brain substance P precursor. Nature, London 306, 32–6.
Nawa, H., Kotani, H. & Nakanishi, S. (1984). Tissue- specific generation of two preprotachykinin mRNAs from one gene by alternative RNA splicing. Nature, London 312, 729–34.
O'shea, M. & Schaffer, M. (1985). Neuropeptide function: the invertebrate contribution. Annual Reviews in Neuroscience 8, 171–98.
Painter, S. D. (1982). FMRFamide catch contractures of a molluscan smooth muscle: pharmacology, ionic dependence and cyclic nucleotides. Journal of Comparative Physiology 148, 491501.
Pierobon, P., Kemali, M. & Milici, N. (1969). Substance P and Hydra: an immunohistochemical and physiology study. Comparative Biochemistry and Physiology 92C, 217–21.
Price, D. A. & Greenberg, M. J. (1977). Structure of a molluscan cardioexcitatory neuropeptide. Science 197, 670–1.
Rahman, M. S. & Mettrick, D. F. (1985). Schistosoma mansoni: effects of in vitro serotonin (5-HT) on aerobic and anaerobic carbohydrate metabolism. Experimental Parasitology 60, 1017.
Ramisz, A. (1965). Studies on the nervous system of nematodes and cestodes by means of histochemical method for active acetylcholinesterase – Trichinella spiralis and Syphacia obvelata. Acta Parasitologica Polonica 13, 205–14.
Ramisz, A. (1967). Studies on the nervous system of nematodes and cestodes by means of histochemical method for active acetyicholinesterase. III. Nematodes of the genus Capillaria and cestodes of the genera Dilepis and Choanotaenia. Acta Parasitologica Polonica 14, 365–79.
Ramisz, A. & Swankowska, Z. (1970). Studies on the nervous system of Fasciola hepatica and Dicrocoelium dendriticum by means of histochemical method for active acetylcholinesterase. Acta Parasitologica Polonica 17, 217–23.
Reuter, M. (1987). Immunocytochemical demonstration of serotonin and neuropeptides in the nervous system of Gyrodactylus salaris (Monogenea). Acta Zoologica 68, 187–93.
Reuter, M., Lehtonen, M. & Wikgren, M. (1988). Immunocytochemical evidence of neuroactive substances in flatworms of different taxa – a comparison. Acta Zoologica 69, 2937.
Reuter, M. & Palmberg, I. (1989). Development and differentiation of neuronal subsets in asexually reproducing Microstomum lineare. Histochemistry 91, 123–31.
Richard, J., Klein, M. J. & Stoeckel, M. E. (1989). Neural and glandular localisation of substance P in Echinostoma caproni (Trematoda–Digenea). Parasitology Research 75, 641–8.
Scharrer, B. (1982). Peptidergic neurons. Acta Morphologica Neerlande Scandinavica 20, 219–23.
Schot, L. P. C., Boer, H. H., Swaab, D. F. & Van Noorden, S. (1981). Immunocytochemical demonstration of peptidergic neurones in the CNS of the pond snail Lymnaea stagnalis with antisera raised to biologically active peptides of vertebrates. Cell and Tissue Research 216, 273–91.
Smyth, J. D. & Halton, D. W. (1983). The Physiology of Trematodes, 2nd edn.Cambridge: Cambridge University Press.
Smyth, J. D. & Mcmanus, D. P. (1989). The Physiology and Biochemistry of Cestodes. Cambridge: Cambridge University Press.
Sukhdeo, M. V. K. & Mettrick, D. F. (1987). Parasite behaviour: understanding platyhelminth responses. Advances in Parasitology 26, 73144.
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, 858–64.
Sukhdeo, S. C., Sukhdeo, M. V. K. & Mettrick, D. F. (1988). Histochemical localization of acetylcholinesterase in the cerebral ganglia of Fasciola hepatica, a parasitic flatworm. Journal of Parasitology 74, 1023–32.
Sundler, F., Hakanson, R., Alumets, J. & Walles, B. (1977). Neuronal localization of pancreatic polypeptide (PP) and vasoactive intestinal peptide (VIP) immunoreactivity in the earthworm (Lumbricus terrestris). Brain Research Bulletin 2, 61–5.
Terada, M., Ishii, A. I., Kino, H. & Sano, M. (1982). Studies on chemotherapy of parasitic helminths. VI. Effects of various neuropharmacological agents on the motility of Diphylidium canium. Japanese Journal of Pharmacology 32, 479–88.
Thorndyke, M. C. (1982). Cholecystokinin (CCK)/gastrin-like immunoreactive neurones in the cerebral ganglion of the protochordate ascidians Styela clava and Ascidiella aspersa. Regulatory Peptides 3, 281–8.
Thorndyke, M. C. & Whitfield, P. J. (1987). Vasoactive intestinal polypeptide-like immunoreactive tegumental cells in the digenean helminth Echinostoma liei: possible role in host–parasite interactions. General and Comparative Endocrinology 68, 202–7.
Tomosky-Sykes, T. K., Jardine, I., Mueller, J. F. & Bueding, E. (1977). Sources of error in neurotransmitter analysis. Analytical Biochemistry 83, 99108.
Tramu, G., Leonardelli, J. & Dubois, M. P. (1977). Immunohistochemical evidence for an ACTH-like substance in hypothalamic LH–RH neurons. Neuroscience Letters 6, 305–9.
Vanderhaeghen, J. J., Lotstra, F., Liston, D. R. & Rossier, J. (1983). Proenkephalin, [met]enkephalin and oxytocin immunoreactivities are localized in bovine hypothalamic magnocellular neurons. Proceedings of the National Academy of Sciences, USA 80, 5139–43.
Walker, R. J. & Holden-Dye, L. (1989). Commentary on the evolution of transmitters, receptors and ion channels in invertebrates. Comparative Biochemistry and Physiology 93A, 2539.
Webb, R. A. & Mizukawa, K. (1985). Serotonin-like immunoreactivity in the cestode Hymenolepis diminuta. Journal of Comparative Neurology 234, 431–40.
Weber, E., Evans, C. J., Samuelsson, S. J. & Barchas, J. D. (1981). Novel peptide neuronal system in the rat brain and pituitary. Science 214, 1248–51.
Welsh, J. H. & Moorhead, M. (1960). The quantitative distribution of 5-hydroxytryptamine in the invertebrates, especially in their nervous systems. Journal of Neurochemistry 6, 146–69.
White, J. G., Amos, W. B. & Fordham, M. (1987). An evaluation of confocal versus conventional imaging of biological structures by fluorescence light microscopy. Journal of Cell Biology 105, 41–8.
Wikgren, M., Reuter, M. & Gustafsson, M. (1986). Neuropeptides in free-living and parasitic flatworms (Platyhelminthes). An immunocytochemical study. Hydrobiologia 132, 93–9.

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The serotoninergic, cholinergic and peptidergic components of the nervous system in the monogenean parasite,Diclidophora merlangi: a cytochemical study

  • A. G. Maule (a1), D. W. Halton (a1), C. F. Johnston (a2), C. Shaw (a2) and I. Fairweather (a1)...


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