Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-28T14:56:05.907Z Has data issue: false hasContentIssue false
  • English
  • Français

The cholinergic, serotoninergic and peptidergic components of the nervous system of Moniezia expansa (Cestoda, Cyclophyllidea)

Published online by Cambridge University Press:  06 April 2009

A. G. Maule ,
D. W. Halton ,
C. Shaw  and
C. F. Johnston
A. G. Maule
Affiliation:
Comparative Neuroendocrinology Research Group, Schools of Clinical Medicine and Biology and Biochemistry, The Queen's University of Belfast, Belfast BT7 1NN, Northern Ireland, UK
D. W. Halton
Affiliation:
Comparative Neuroendocrinology Research Group, Biology and Biochemistry, The Queen's University of Belfast, Belfast BT7 1NN, Northern Ireland, UK
C. Shaw
Affiliation:
Comparative Neuroendocrinology Research Group, Schools of Clinical Medicine and Biology and Biochemistry, The Queen's University of Belfast, Belfast BT7 1NN, Northern Ireland, UK
C. F. Johnston
Affiliation:
Comparative Neuroendocrinology Research Group, Schools of Clinical Medicine and Biology and Biochemistry, The Queen's University of Belfast, Belfast BT7 1NN, Northern Ireland, UK
Get access Rights & Permissions [Opens in a new window]

Summary

The central (CNS) and peripheral (PNS) nervous systems of the cyclophyllidean tapeworm, Moniezia expansa, were examined for the presence of cholinergic, serotoninergic and peptidergic elements using enzyme cytochemical and immunocytochemical techniques in conjunction with light and confocal scanning laser microscopy. Cholinesterase activity and 5-hydroxytryptamine- and regulatory peptide-immunoreactivities (IRs) were localized to the nerve fibres and cell bodies of all of the major neuronal components in the CNS of the worm, including the cerebral ganglia and connecting commissure, the 10 longitudinal nerve cords and associated transverse ring commissures. Although each of the 3 systems appeared well developed and comprised a significant portion of the nervous system, the serotoninergic constituent was the most highly developed, consisting of a vast array of nerve fibres and cell bodies distributed throughout the strobila of the worm. A close association of cholinesterase reactivity and peptide-IRs was evident throughout the CNS, indicating the possible co-localization of acetylcholine and neuropeptides. Within the PNS, cholinergic activity and serotoninergic- and peptidergic-IRs occurred in the subtegumental network of nerve fibres and somatic musculature. Although all 3 neuro-chemical elements were present in the acetabula, they were found in different nerve fibres; only cholinergic and peptidergic cell bodies were found. The common genital opening, vagina and ootype regions of the reproductive system displayed a rich innervation of all 3 types of neuronal populations. Within the peptidergic system, immunostaining with antiseraraised to the C-terminus of the neuropeptide Y superfamily of peptides and the invertebrate peptides, neuropeptide F (M. expansa) and FMRFamide was the most prevalent. Limited positive-IR for substance P and neurokinin A were also recorded in the CNS of the worm.

Keywords

Moniezia expansaCestodaneuropeptidesneuropeptide Y-superfamilyneuropeptide FFMRFamidesubstance Pneurokinin A5-hydroxytryptaminecholinesteraseimmunocytochemistryconfocal scanning laser microscopy.
Type
Research Article
Information
Parasitology , Volume 106 , Issue 4 , May 1993 , pp. 429 - 440
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

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, 49–60.CrossRefGoogle Scholar
Fairweather, I. & Halton, D. W. (1991). Neuropeptides in platyhelminths. Parasitology 102, (Suppl.) 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., Mahendrasingham, S., Johnston, C. F., Halton, D. W. & Shaw, C. (1990 a). Peptidergic nerve elements in three developmental stages of the tetraphyllidean tapeworm Trilocularia acanthiaevulgaris. An immunocytochemical study. Parasitology Research 76, 497–508.CrossRefGoogle ScholarPubMed
Fairweather, I., Mahendrasingham, S., Johnston, C. F., Halton, D. W. & Shaw, C. (1990 b). An ontogenic study of the cholinergic and serotoninergic nervous system in Trilocularia acanthiaevulgaris (Cestoda, Tetraphyllidea). Parasitology Research 76, 487–96.CrossRefGoogle Scholar
Fairweather, I., Maule, A. G., Mitchell, S. H., Johnston, C. F. & Halton, D. W. (1987). Immunocytochemical demonstration of 5-hydroxtryptamine (serotonin) in the nervous system of the liver fluke, Fasciola hepatica (Trematoda, Digenea). Parasitology Research 73, 255–8.CrossRefGoogle Scholar
Gomori, G. (1952). Microscopic Histochemistry, Principles and Practice. Chicago: University of Chicago Press.CrossRefGoogle Scholar
Gunn, A. & Probert, A. J. (1981). Moniezia expansa: subcellular distribution, kinetic properties of acetylcholinesterase and effects of inhibitors and anthelmintics. Experimental Parasitology 51, 373–81.CrossRefGoogle ScholarPubMed
Gustafsson, M. K. S. (1991). Skin the tapeworms before you stain their nervous system! A new method for wholemount immunocytochemistry. Parasitology Research 77, 509–16.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Gustafsson, M. K. S. & Wikgren, M. C. (1989). Development of immunoreactivity to the invertebrate neuropeptide small cardiac peptide B in the tapeworm Diphyllobothrium dendriticum. Parasitology Research 75, 396–400.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. G., 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
Howells, R. E. & Erasmus, D. A. (1969). Histochemical observations on the tegumentary epithelium and interproglottidal glands of Moniezia expansa (Rud., 1805) (Cestoda, Cyclophyllidea). Parasitology 59, 505–18.CrossRefGoogle ScholarPubMed
Koelle, L. E. (1951). Elimination of enzymatic diffusion artifacts in histochemical localisation of cholinesterase and survey of their cellular distribution. Journal of Pharmacology and Experimental Therapeutics 114, 167–84.Google Scholar
Kralj, N. (1967). Morphological and histochemical studies on the nervous system of tapeworms revealed by the cholinesterase method (Taenia hydatigena, Dipylidium caninum and Moniezia expansa). Veteraniski Archiv 37, 277–84.Google Scholar
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
Maule, A. G., Halton, D. W., Johnston, C. F., Fairweather, I. & Shaw, C. (1989). Immunocytochemical demonstration of neuropeptides in the fish-gill parasite, Diclidophora merlangi (Monogenoidea). International Journal for Parasitology 19, 307–16.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
Maule, A. G., Shaw, C., Halton, D. W., Brennan, G. P., Johnston, C. F. & Moore, S. (1992). Neuropeptide F (Moniezia expansa): localization and characterization using specific antisera. Parasitology 105, 505–12.CrossRefGoogle ScholarPubMed
Maule, A. G., Shaw, C., Halton, D. W., Thim, L., Johnston, C. F., Fairweather, I. & Buchanan, K. D. (1991). Neuropeptide F: a novel parasitic flatworm regulatory peptide from Moniezia expansa (Cestoda: Cyclophyllidea). Parasitology 102, 309–16.CrossRefGoogle Scholar
Sukhdeo, M. V. K. (1992). The behavior of parasitic flatworms in vivo: what is the role of the brain? Journal of Parasitology 78, 231–42.CrossRefGoogle ScholarPubMed
Sukhdeo, M. V. K., Hsu, S. C., Thompson, C. S. & Mettrick, D. F. (1984). Hymenolepis diminuta: behavioural effects of 5-hydroxtryptamine, acetylcholine, histamine and somatostatin. Journal of Parasitology 70, 682–8.CrossRefGoogle Scholar
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, C. S., Sangster, N. C. & Mettrick, D. F. (1986). Cholinergic inhibition of muscular contraction in Hymenolepis diminuta (Cestoda). Canadian Journal of Zoology 67, 1257–62.CrossRefGoogle Scholar
Tower, W. L. (1897). The nervous system in the cestode Moniezia expansa. Zoologische Jahrbücher, Abteilung für Morphologie 13, 359–84.Google Scholar
Ward, S. M., Allen, J. M. & McKerr, G. (1986). Neuromuscular physiology of Grillotia erinaceus metacestodes (Cestoda: Trypanorhyncha) in vitro. Parasitology 93, 121–32.CrossRefGoogle Scholar