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A confocal scanning laser microscope study of the peptidergic and serotoninergic components of the nervous system in larval Schistosoma mansoni

Published online by Cambridge University Press:  06 April 2009

P. J. Skuce ,
C. F. Johnston ,
I. Fairweather ,
D. W. Halton  and
C. Shaw
C. F. Johnston
Affiliation:
Department of Medicine, The Queen's University, Belfast BT7 INN, Northern Ireland
I. Fairweather
Affiliation:
School of Biology and Biochemistry, The Queen's University, Belfast BT7 INN, Northern Ireland
D. W. Halton
Affiliation:
School of Biology and Biochemistry, The Queen's University, Belfast BT7 INN, Northern Ireland
C. Shaw
Affiliation:
Department of Medicine, The Queen's University, Belfast BT7 INN, Northern Ireland
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Extract

The localization and distribution of the serotoninergic and peptidergic elements of the nervous system of larval Schistosoma mansoni have been investigated using an indirect immunofluorescence technique in conjunction with confocal scanning laser microscopy (CSLM). A range of antisera was used, raised to the biogenic amine, 5-hydroxytryptamine (5-HT, or serotonin), the vertebrate peptides pancreatic polypeptide (PP), peptide YY (PYY) and neuropeptide Y (NPY) and to the native invertebrate peptide, FMRFamide; all these antisera were shown previously to be immunopositive in the adult worm. No immunoreactivity to 5-HT was detected in any of the larval stages, but both miracidia and cercariae were consistently immunoreactive to all 4 peptides. The peptidergic nervous system of the miracidium is relatively simple, taking the form of a central neural mass with associated paired anterior and posterior nerve tracts. The cercarial peptidergic nervous system comprises a central commissure joining paired anterior ganglia, from which emanate paired dorsal and ventral nerve tracts, which terminate at the body/tail junction. The excretory bladder region of the tail is also immunoreactive for the 4 peptides, and a fine pair of nerve tracts extends the length of the tail shaft. Immunoreactive nerve cell bodies are also evident in the midbody region of the intrasprocystic cercariae, these same structures being immunoreactive for the neuronal marker, neurone-specific enolase (NSE). The organization of the larval peptidergic nervous system is compared to that of the cholinergic nervous system and contrasted with the peptidergic system in the adult worm. The absence of immunoreactivity to 5-HT is discussed in relation to the proposed development of the aminergic nervous system upon establishment in the definitive host.

Keywords

Schistosoma mansoniTrematodaDigeneamiracidiumcercarialarva. s.agesneuropeptidespancreatic polypeptide (PP)peptide YY (PYY)neuropeptide Y (NPY)FMRFamide5-hydroxytryptamine (5-HTor serotonin)confocal scanning laser microscopy (CSLM).

Information

Type
Research Article
Information
Parasitology , Volume 101 , Issue 2 , October 1990 , pp. 227 - 234
Copyright
Copyright © Cambridge University Press 1990

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References

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 Scholar
Bennett, J. & 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. Molecular Pharmacology 9, 311–19.Google Scholar
Bennett, J., Bueding, E., Timms, A. R. & Engstrom, R. G. (1969). Occurrence and levels of 5-hydroxytryptamine in Schistosoma mansoni. Molecular Pharmacology 5, 542–5.Google ScholarPubMed
Bruckner, D. A. & Voge, M. (1974). The nervous system of larval Schistosoma mansoni as revealed by acetylcholinesterase staining. Journal of Parasitology 60, 437–46.Google Scholar
Bueding, E., Schiller, E. L. & Bourgeois, J. G. (1967). Some physiological, biochemical and morphologic effects of Tris(μ-aminophenyl) carbonium salts (TAC) on Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 16, 500–15.Google Scholar
Bueding, E., Bennett, J. L., Chou, T., Pert, C. & Tomosky, T. (1974). Effect of antischistosomal drugs on the uptake of 5-hydroxytryptamine by Schistosoma mansoni. Proceedings of the Third International Congress on Parasitology 3, 1443–4.Google Scholar
Catto, B. A. & Ottesen, E. A. (1979). Serotonin uptake in schistosomules of Schistosoma mansoni. Comparative Biochemistry and Physiology 63C, 235–42.Google Scholar
Chiang, P. K., Bourgeois, J. G. & Bueding, E. (1974). 5-hydroxytryptamine and dopamine in Biomphalaria glabrata. Journal of Parasitology 60, 264–71.CrossRefGoogle 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
Clark-Rosenberg, R. L. & Marangos, P. J. (1980). Phylogenetic distribution of neurone-specific enolase. Journal of Neurochemistry 35, 756–9.Google Scholar
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, 49–60.Google Scholar
Dei-Cas, E., Dhainaut-Courtois, N., Dhainaut, A. & Vernes, A. (1979). Ultrastructural localization of tritiated 5-HT in adult Schistosoma mansoni. A preliminary report. Biologie Cellulaire 35, 321–4.Google Scholar
Dei-Cas, E., Dhainaut-Courtois, N. & Biguet, J. (1981). Contribution à l'étude du système nerveux des formes adultes et larvaires de Schistosoma mansoni Sambon, 1907. (Trematoda Digenea). II. Rôle de la sérotonine et de la dopamine. Annales de Parasitologie Humaine et Comparee 56, 271–84.CrossRefGoogle Scholar
Di Conza, J. J. & Basch, P. F. (1975). Histochemical demonstration of acetylcholinesterase in sporocysts of Schistosoma mansoni (Trematoda). Parasitology 71, 305–10.Google Scholar
Etges, F. J., Carter, O. S. & Webbe, G. (1975). Behavioural and developmental physiology of schistosome larvae as related to their molluscan hosts. Annals of the New York Academy of Sciences 266, 480–96.CrossRefGoogle ScholarPubMed
Estey, S. J. & Mansour, T. E. (1987). Nature of serotonin-activated adenylate cyclase during development of Schistosoma mansoni. Molecular and Biochemical Parasitology 26, 47–60.Google Scholar
Fripp, P. J. (1967). Histochemical localization of esterase activity in schistosomes. Experimental Parasitology 21, 380–90.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 58C, 157–9.Google Scholar
Grabda-Kazubska, B. & Moczoń, T. (1981). Nervous system and chaetotaxy in the cercaria of Haplometra cylindracea (Zeder, 1800) (Digenea, Plagiorchiidae). Zeitschrift für Parasitenkunde 65, 53–61.CrossRefGoogle Scholar
Gupta, B. C. & Basch, P. F. (1989). Human chorionic gonadotrophin-like immunoreactivity in schistosomes and Fasciola. Parasitology Research 76, 86–9.CrossRefGoogle Scholar
Gustafsson, M. K. S. (1987). Immunocytochemical demonstration of neuropeptides and serotonin in the nervous system of adult Schistosoma mansoni. Parasitology Research 74, 168–74.Google Scholar
Halton, D. W., Magee, R. M., Johnston, C. F., Fairweather, I. & Shaw, C. (1989). Immunocytochemical mapping of 5-hydroxytryptamine (5-HT) and regulatory peptides in certain marine trematode larvae. In Proceedings of the Joint British, Netherlands and Belgian Societies for Parasitology with the Belgian Society for Protozoology, The University of Southampton, March 1989, p. 40.Google Scholar
Jennings, J. B. & Leflore, W. B. (1972). The histochemical demonstration of certain aspects of cercarial morphology. Transactions of the American Microscopical Society 91, 52–62.CrossRefGoogle ScholarPubMed
Kasschau, M. R. & Mansour, T. E. (1982 a). Serotonin-activated adenylate cyclase during early development of Schistosoma mansoni. Nature, London 296, 66–8.CrossRefGoogle ScholarPubMed
Kasschau, M. R. & Mansour, T. E. (1982 b). Adenylate cyclase in adults and cercariae of Schistosoma mansoni. Molecular and Biochemical Parasitology 5, 107–16.CrossRefGoogle ScholarPubMed
Krvavica, S., Lui, A. & Bečejac, S. (1967). Acetylcholinesterase and butyrylcholinesterase in the liver fluke (Fasciola hepatica). Experimental Parasitology 21, 240–8.CrossRefGoogle Scholar
Leflore, W. B., Bass, H. S. & Smith, B. F. (1980). Histochemical localization of hydrolytic enzymes in cercariae of Cloacitrema michiganensis (Trematoda: Philophthalmidae). Transactions of the American Microscopical Society 99, 201–6.CrossRefGoogle Scholar
Lewert, R. M. & Hopkins, D. R. (1965). Cholinesterase activity in Schistosoma mansoni cercariae. Journal of Parasitology 51, 616.CrossRefGoogle Scholar
Machado, C. R. S., Machado, A. B. M. & Pellegrino, J. (1972). Catecholamine-containing neurons in Schistosoma mansoni. Zeitschrift für Zellforschung und mikroskopische Anatomie 124, 230–7.Google Scholar
Magee, R. M., Johnston, C. F., Fairweather, I., Halton, D. W. & Shaw, C. (1989). Serotonin(5-HT) and neuropeptides in the intramolluscan stages of Fasciola hepatica.. In Proceedings of the Joint British, Netherlands and Belgian Societies for Parasitology with the Belgian Society for Protozoology, The University of Southampton, March 1989, p. 40.Google Scholar
Mansour, T. E. (1984). Serotonin receptors in parasitic worms. Advances in Parasitology 23, 1–6.Google ScholarPubMed
Niagi, E. N. M. & Bender, D. A. (1990). Schistosoma mansoni: effects on tryptophan metabolism in mice. Experimental Parasitology 70, 43–54.Google Scholar
Niewiadomska, K. & Moczoń, T. (1982). The nervous system of Diplostomum pseudospathaceum Niewiadomska, (Digenea, Diplostomatidae) I. Nervous system and chaetotaxy in the cercaria. Zeitschrift für Parasitenkunde 68, 295–304.CrossRefGoogle Scholar
Orido, Y. (1989). Histochemical evidence of the catecholamine-associated nervous system in certain schistosome cercariae. Parasitology Research 76, 146–9.Google Scholar
Panitz, E. & Knapp, S. E. (1967). Acetylcholinesterase activity in Fasciola hepatica miracidia. Journal of Parasitology 53, 354.CrossRefGoogle ScholarPubMed
Pepler, W. J. (1958). Histochemical demonstration of an acetylcholinesterase in the ova of Schistosoma mansoni. Journal of Histochemistry and Cytochemistry 6, 139–41.CrossRefGoogle ScholarPubMed
Senft, A. W., Senft, G. R., Hillman, D. P. & Kryger, S. (1976). Influence of Hycanthone on morphology and serotonin uptake of Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 25, 832–40.Google Scholar
Skuce, P. J., Johnston, C. F., Fairweather, I., Halton, D. W., Shaw, C. & Buchanan, K. D. (1990). Immunoreactivity to the pancreatic polypeptide family in the nervous system of the adult human blood fluke, Schistosoma mansoni. Cell and Tissue Research (in Press).CrossRefGoogle Scholar
Sternberger, L. A. (1974). Immunocytochemistry. In Foundations of Immunology (ed. Oster, A. & Weiss, I.). Eaglewood Cliffs: Prentice Hall.Google Scholar
Venkatanarsaiah, J. (1981). Detection of cholinesterase in the nervous system of the oncomiracidium of a monogenean, Pricea multae Chanhan, 1945. Parasitology 82, 241–4.CrossRefGoogle Scholar
Young, L. E., Young, R. E. & Bundy, D. A. P. (1988). Ultrastructural and neuropharmacological findings in the nerve/muscle system of a digenean (Cercaria caribbea LXXI Cable). Comparative Biochemistry and Physiology 90C, 295–303.Google Scholar
Zaccone, G. (1984). Immunohistochemical demonstration of neurone-specific enolase in the nerve endings and skin receptors of marine eels. Histochemical Journal 16, 1231–6.CrossRefGoogle ScholarPubMed