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Immunocytochemical localization of serotonin (5-HT) in the nervous system of the hydatid organism, Echinococcus granulosus (Cestoda, Cyclophyllidea)

Published online by Cambridge University Press:  06 April 2009

D. J. A. Brownlee
Affiliation:
School of Biology and Biochemistry, The Queen's University of Belfast, Belfast BT7 INN, Northern Ireland
I. Fairweather
Affiliation:
School of Biology and Biochemistry, The Queen's University of Belfast, Belfast BT7 INN, Northern Ireland
C. F. Johnston
Affiliation:
School of Clinical Medicine, The Queen's University of Belfast, Belfast BT7 INN, Northern Ireland
M. T. Rogan
Affiliation:
Department of Biological Sciences, University of Salford, Salford M5 4WT, England

Summary

The localization and distribution of the serotoninergic components of the nervous system in the hydatid organism, Echinococcus granulosus, were determined by immunocytochemical techniques in conjunction with confocal scanning laser microscopy (CSLM). The distribution of serotonin immunoreactivity (IR) paralleled that previously described for cholinesterase activity, although it was more widespread. Nerve cell bodies and nerve fibres immunoreactive for 5-HT were present throughout the central nervous system (CNS), occurring in the paired lateral, posterior lateral and rostellar ganglia, their connecting commissures and nerve rings in the scolex and in the ten longitudinal nerve cords that run posteriorly throughout the body of the worm. A large population of nerve cell bodies was associated with the lateral nerve cords. In the peripheral nervous system (PNS), immunoreactive nerve fibres occurred in well-developed nerve plexuses innervating the somatic musculature and the musculature of the rostellum and suckers. The genital atrium and associated reproductive ducts were richly innervated with serotoninergic nerve cell bodies and nerve fibres.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1994

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References

REFERENCES

Brizzi, G. & Blum, J. J. (1970). Effects of growth conditions on serotonin content of Tetrahymena pyriformis. Journal of Protozoology 17, 553–5.CrossRefGoogle ScholarPubMed
Carlberg, M. & Anctil, M. (1993). Biogenic amines in coelenterates. Comparative Biochemistry and Physiology 106C, 19.Google ScholarPubMed
Chou, T.-C. T., Bennett, J. & Bueding, E. (1972). Occurrence and concentrations of biogenic amines in trematodes. Journal of Parasitology 58, 1098–102.CrossRefGoogle ScholarPubMed
Coons, A. H., Leduc, E. H. & Connolly, J. M. (1955). Studies on antibody production. I. A method for the histochemical demonstration of specific antibody and its application to a study of the hyperimmune rabbit. Journal of Experimental Medicine 102, 4960.CrossRefGoogle Scholar
Fairweather, I. & Halton, D. W. (1991). Neuropeptides in platyhelminths. Parasitology 102, S77–S92.CrossRefGoogle ScholarPubMed
Fairweather, I., Macartney, G. 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, Cyclophyllidea). Parasitology Research 74, 371–9.CrossRefGoogle ScholarPubMed
Fairweather, I., Mahendrasingam, S., Johnston, C. F., Halton, D. W., Mccullough, J. S. & Shaw, C. (1990). An ontogenetic study of the cholinergic and serotoninergic nervous systems in Trilocularia acanthiaevulgaris (Cestoda, Tetraphyllidea). Parasitology Research 76, 487–96.CrossRefGoogle ScholarPubMed
Fairweather, I., Maule, A. G., 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.CrossRefGoogle ScholarPubMed
Gianutsos, C. & Bennett, J. L. (1977). The regional distribution of dopamine and norepinephrine in Schistosoma mansoni and Fasciola hepatica. Comparative Biochemistry and Physiology 58C, 157–9.Google ScholarPubMed
Gordon, B. & Webb, R. A. (1989). Release of exogenously-supplied and endogenous serotonin from tissue slices of Hymenolepis diminuta. Brain Research 486, 376–80.CrossRefGoogle ScholarPubMed
Gustafsson, M. K. S. (1992). The neuroanatomy of parasitic flatworms. Advances in Neuroimmunology 2, 267–86.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Halton, D. W., Shaw, C., Maule, A. C., Johnston, C. F. & Fairweather, I. (1992). Peptidergic messengers: a new perspective of the nervous system of parasitic platyhelminths. Journal of Parasitology 78, 179–93.CrossRefGoogle ScholarPubMed
Hariri, M. (1974). Occurrence and concentration of biogenic amines in Mesocestoides corti (Cestoda). Journal of Parasitology 60, 737–43.CrossRefGoogle ScholarPubMed
Janakidevi, K., Dewey, V. C. & Kidder, G. W. (1966). Serotonin in Protozoa. Archives of Biochemistry and Biophysics 113, 758–9.CrossRefGoogle ScholarPubMed
Johnston, C. F., Shaw, C., Halton, D. W. & Fairweather, I. (1990). Confocal scanning laser microscopy and helminth neuroanatomy. Parasitology Today 6, 305–8.CrossRefGoogle ScholarPubMed
Mckay, D. M., Fairweather, I., Johnston, C. F., Shaw, C. & Halton, D. W. (1991). Immunocytochemical and radioimmunometrical demonstration of serotonin- and neuropeptide-immunoreactivities in the adult rat tapeworm, Hymenolepis diminuta (Cestoda, Cyclophyllidea). Parasitology 103, 275–89.CrossRefGoogle ScholarPubMed
Mansour, T. E. (1981). Biochemical and molecular strategies in chemotherapy of parasitic worm infections. In Molecular Basis of Drug Action (ed. Singer, T. P. & Ondarza, R. N.), pp. 5369. New York: Elsevier/North Holland.Google Scholar
Mansour, T. E. (1984). Serotonin receptors in parasitic worms. In Advances in Parasitology 23, (ed. Baker, J. R. & Muller, R.), pp. 136. London: Academic Press.Google Scholar
Martelly, I. & Franquinet, R. (1984). Planarian regeneration as a model for cellular activation studies. Trends in Biochemical Sciences 9, 468–71.CrossRefGoogle Scholar
Maule, A. C., Halton, D. W., Shaw, C. & Johnston, C. F. (1993). The cholinergic, serotoninergic and peptidergic components of the nervous system of Moniezia expansa (Cestoda, Cyclophyllidea). Parasitology 106, 429–40.CrossRefGoogle ScholarPubMed
Morseth, D. J. (1967). Observations on the fine structure of the nervous system of Echinococcus granulosus. Journal of Parasitology 53, 492500.CrossRefGoogle ScholarPubMed
Pax, R. A. & Bennett, J. L. (1992). Neurobiology of parasitic flatworms: how much ‘neuro’ in the biology? Journal of Parasitology 78, 194205.CrossRefGoogle ScholarPubMed
Ribeiro, P. & Webb, R. A. (1983 a). The synthesis of 5- hydroxytryptamine from tryptophan and 5-hydroxy- tryptophan in the cestode Hymenolepis diminuta. International Journal for Parasitology 13, 101–6.CrossRefGoogle ScholarPubMed
Ribeiro, P. & Webb, R. A. (1983 b). The occurrence and synthesis of octopamine and catecholamines in the cestode Hymenolepis diminuta. Molecular and Biochemical Parasitology 7, 5362.CrossRefGoogle ScholarPubMed
Ribeiro, P. & Webb, R. A. (1984). The occurrence, synthesis and metabolism of 5-hydroxytryptamine and 5-hydroxytryptophan in the cestode Hymenolepis diminuta: a high performance liquid chromatographic study. Comparative Biochemistry and Physiology 79C, 159–64.Google ScholarPubMed
Ribeiro, P. & Webb, R. A. (1986). Demonstration of specific high-affinity binding sites for [3H]5- hydroxytryptamine in the cestode Hymenolepis diminuta. Comparative Biochemistry and Physiology 84C, 353–8.Google ScholarPubMed
Ribeiro, P. & Webb, R. A. (1987). Characterization of a serotonin transporter and an adenylate cyclase-linked serotonin receptor in the cestode Hymenolepis diminuta. Life Science 40, 755–68.CrossRefGoogle Scholar
Sakamoto, T. & Sugimura, M. (1969). Studies on echinococcosis. XXI. Electron microscopical observations on general structure of larval tissue of multilocular echinococcus. Japanese Journal of Veterinary Research 17, 6781.Google ScholarPubMed
Shield, J. M. (1969). Dipylidium caninum, Echinococcus granulosus and Hydatigera taeniaeformis: histochemical identification of cholinesterases. Experimental Parasitology 25, 217–31.CrossRefGoogle ScholarPubMed
Sukhdeo, M. V. K., Hsu, S. C., Thompson, C. S. & Mettrick, D. F. (1984). Hymenolepis diminuta: behavioral effects of 5-hydroxytryptamine, acetylcholine, histamine and somatostatin. Journal of Parasitology 70, 682–8.CrossRefGoogle ScholarPubMed
Thompson, C. S. & Mettrick, D. F. (1989). The effects of 5-hydroxytryptamine and glutamate on muscle contraction in Hymenolepis diminuta (Cestoda). Canadian Journal of Zoology 67, 1257–62.CrossRefGoogle Scholar
Thompson, R. C. A. & Allsopp, C. E. (1988). Hydatidosis: Veterinary Perspectives and Annotated Bibliography. Wallingford: C.A.B. International.Google Scholar
Thompson, R. C. A. & Lymbery, A. J. (1990). Echinococcus: biology and strain variation. International Journal for Parasitology 20, 457–70.CrossRefGoogle ScholarPubMed
Ward, S. M., Allen, J. M. & Mckerr, C. (1986). Neuromuscular physiology of Grillotia erinaceus metacestodes (Cestoda: Trypanorhyncha) in vitro. Parasitology 93, 121–32.CrossRefGoogle Scholar
Webb, R. A. (1985). The uptake and metabolism of 5- hydroxytryptamine by tissue slices of the cestode Hymenolepis diminuta. Comparative Biochemistry and Physiology 80C, 305–12.Google ScholarPubMed
Webb, R. A. (1988). Endocrinology of Acoelomates. In Invertebrate Endocrinology, vol. 2, Endocrinology of Selected Invertebrate Types (ed. Downer, R. G. H. & Laufer, H.), pp. 3162. New York: Alan R. Liss.Google Scholar
Webb, R. A. (1991). Serotonin—a ubiquitous neuroactive agent in platyhelminths. In Neurobiology and Endocrinology of Selected Invertebrates (ed. Loughton, B. G. & Saleuddin, A. S. M.), pp. 145–62. Captus University Press.Google Scholar
Webb, R. A. & Eklove, H. (1989). Demonstration of intense glutamate-like immunoreactivity in the longitudinal nerve cords of the cestode Hymenolepis diminuta. Parasitology Research 75, 545–8.CrossRefGoogle ScholarPubMed
Webb, R. A. & Mizukawa, K. (1985). Serotonin-like immunoreactivity in the cestode Hymenolepis diminuta. Journal of Comparative Neurology 234, 431–40.CrossRefGoogle Scholar
Wikgren, M., Reuter, M., Gustafsson, M. K. S. & Lindroos, P. (1990). Immunocytochemical localization of histamine in flatworms. Cell and Tissue Research 260, 479–84.CrossRefGoogle ScholarPubMed