Hostname: page-component-77c89778f8-rkxrd Total loading time: 0 Render date: 2024-07-19T19:39:28.607Z Has data issue: false hasContentIssue false
  • English
  • Français

The action of serotonin and the nematode neuropeptide KSAYMRFamide on the pharyngeal muscle of the parasitic nematode, Ascaris suum

Published online by Cambridge University Press:  06 April 2009

D. J. A. Brownlee ,
L. Holden-Dye ,
I. Fairweather  and
R. J. Walker
D. J. A. Brownlee
Affiliation:
Department of Physiology and Pharmacology, School of Biological Sciences, University of Southampton, Southampton SO16 7PX School of Biology and Biochemistry, Medical Biology Centre, The Queen's University of Belfast, Belfast BT7 1NN, N. Ireland
L. Holden-Dye
Affiliation:
Department of Physiology and Pharmacology, School of Biological Sciences, University of Southampton, Southampton SO16 7PX
I. Fairweather
Affiliation:
School of Biology and Biochemistry, Medical Biology Centre, The Queen's University of Belfast, Belfast BT7 1NN, N. Ireland
R. J. Walker
Affiliation:
Department of Physiology and Pharmacology, School of Biological Sciences, University of Southampton, Southampton SO16 7PX
Get access Rights & Permissions [Opens in a new window]

Summary

The pharyngeal component of the enteric nervous system of the parasitic nematode, Ascaris suum exhibits immunoreactivity for serotonin (5-hydroxytryptamine or 5-HT) and for FMRFamide-like peptides. This paper describes the application of an in vitro pharmacological approach to investigate the functional role of 5-HT and FMRFamide-like peptides. The pharyngeal pumping behaviour of Ascaris suum was monitored using a modified pressure transducer system which measures pharyngeal pressure changes and therefore pumping. The pharynx did not contract spontaneously; however, 5-HT (10-1000 μM) stimulated pumping at a frequency of 0·5 Hz. FMRFamide had no apparent effect on pharyngeal pumping. The native nematode FMRFamide-related peptide (FaRP), KSAYMRFamide inhibited the pumping elicited by 5-HT. The duration of inhibition was dose-dependent (0·1-1000 nM) with a threshold of 0·1 nM. In 4 preparations, the inhibition of the pharyngeal muscle was preceded by an initial excitation and increase in the amplitude of pharyngeal pressure changes. The pharynx is involved in various nematode processes, including feeding, regulation of hydrostatic pressure and excretion. The role of 5-HT and KSAYMRFamide in the pharyngeal function of nematodes is discussed.

Keywords

Ascaris suumnematodepharynxenteric nervous system (ENS)serotonin5-HTneuropeptideFMRFamideKSAYMRFamideFaRP
Type
Research Article
Information
Parasitology , Volume 111 , Issue 3 , September 1995 , pp. 379 - 384
Copyright
Copyright © Cambridge University Press 1995

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

Albertson, D. G. & Thomson, J. N. (1976). The pharynx of Caenorhabditis elegans. Philosophical Transactions of the Royal Society of London B 275, 299–325.Google Scholar
Avery, L. & Horvitz, H. R. (1990). Effects of starvation and neuroactive drugs on feeding in Caenorhabditis elegans. Journal of Experimental Zoology 253, 263–70.Google Scholar
Browniee, D. J. A., Fairweather, I., Johnston, C. F., Smart, D., Shaw, C. & Halton, D. W. (1993). Immunocytochemical demonstration of neuropeptides in the central nervous system of the roundworm, Ascaris suum (Nematoda, Ascaroidea). Parasitology 106, 305–16.Google Scholar
Brownlee, D. J. A., Fairweather, I. & Johnston, C. F. (1993). Immunocytochemical demonstration of neuropeptides in the peripheral nervous system of the roundworm. Ascaris suum (Nematoda: Ascaroidea). Parasitology Research 79, 302–8.CrossRefGoogle ScholarPubMed
Brownlee, D. J. A., Fairweather, I., Johnston, C. F. & Shaw, C. (1994 a). Immunocytochemical demonstration of peptidergie and serotoninergie components in the enteric nervous system of the roundworm Ascaris suum (Nematoda, Ascaroidea). Parasitology 108, 89–103.Google Scholar
Brownlee, D. J. A., Thorndyke, M. C., Fairweather, I. & Johnston, C. F. (1994 b). Immunocytochemical demonstration of SALMFamide in the nervous system of a range of parasites (nematode, trematode and cestode). Regulatory Peptides 51, 277.CrossRefGoogle Scholar
Byerly, L. & Masuda, M. O. (1979). Voltage-clamp analysis of the potassium current that produces a negative-going action potential in Ascaris muscle. Journal of Physiology 288, 263–84.Google Scholar
Chaudhuri, J. & Donahue, M. J. (1989). Serotonin receptors in the tissues of adult Ascaris suum. Molecular and Biochemical Parasitology 35, 191–8.Google Scholar
Chaudhuri, J., Martin, R. E. & Donahue, M. J. (1988). Evidence for the absorption and synthesis of 5-hydroxytryptamine in perfused muscle and intestinal tissue and whole worms of adult Ascaris suum. Parasitology 96, 157–70.Google Scholar
Cowden, C., Sithigorngul, P., Brackley, P., Guastella, J. & Stretton, A. O. W. (1993). Localization and differential expression of FMRFamide-like immunoreactivity in the nematode Ascaris suum. Journal of Comparative Neurology 333, 455–68.Google Scholar
Cowden, C. & Stretton, A. O. W. (1993). AF2, an Ascaris neuropeptide: isolation, sequence, and bioactivity. Peptides 14, 423–30.Google Scholar
Cowden, C., Stretton, A. O. W. & Davis, R. E. (1989). AF1, a sequenced bioactive neuropeptide isolated from the nematode Ascaris suum. Neuron 2, 1465–73.Google Scholar
Croll, N. A. (1972). Behavioural activities of nematodes. Helminthological Abstracts 41A, 359–77.Google Scholar
Davenport, T. R. B., Lee, D. L. & Isaac, R. E. (1988). Immunocytochemical demonstration of a neuropeptide in Ascaris suum (Nematoda) using an antiserum to FMRFamide. Parasitology 97, 81–8.Google Scholar
Del Castillo, J., de Mello, W. C. & Morales, T. (1964). Hyperpolarizing action potentials recorded from the oesophagus of Ascaris lumbricoides. Nature, London 203, 530–1.CrossRefGoogle Scholar
Del Castillo, J. & Morales, T. (1967). The electrical and mechanical activity of the esophageal cell of Ascaris lumbricoides. Journal of General Physiology 50, 603–29.Google Scholar
Donahue, M. J., Yacoub, N. J., Michnoff, C. A., Masaracchia, R. A. & Harris, B. G. (1981). Serotonin (5-hydroxytryptamine): a possible regulator of glycogenolysis in perfused muscle segments of Ascaris suum. Biochemical and Biophysical Research Communications 101, 112–17.CrossRefGoogle ScholarPubMed
Geary, T. G., Price, D. A., Bowman, J. W., Winterrowd, C. A., Mackenzie, C. D., Garrison, R. D., Williams, J. F. & Friedman, A. R. (1992). Two FMRFamide-like peptides from the free-living nematode Panagrellus redivivus. Peptides 13, 209–14.Google Scholar
Horvitz, H. R., Chalfie, M., Trent, C., Sulston, J. E. & Evans, P. D. (1982). Serotonin and octopamine in the nematode Caenorhabditis elegans. Science 216, 1012–14.Google Scholar
Maule, A. G., Shaw, C., Bowman, J. W., Halton, D. W., Thompson, D. P., Geary, T. G. & Thim, L. (1994). KSAYMRFamide: A novel FMRFamide-related heptapeptide from the free-living nematode, Panagrellus redivivus, which is myoactive in the parasitic nematode, Ascaris suum. Biochemical and Biophysical Research Communications 200, 973–80.Google Scholar
Maule, A. G., Shaw, C., Bowman, J. W., Halton, D. W., Thompson, D. P., Thim, L., Kubiak, T. M., Martin, R. A. & Geary, T. G. (1995). Isolation and preliminary biological characterization of KPNFIRFamide, a novel FMRFamide-related peptide from the freeliving nematode, Panagrellus redivivus. Peptides 16, 87–93.Google Scholar
Misura, S. K., Sen, R. & Ghatak, S. (1984). Ascaris lumbricoides and Ascaridia galli: biogenic amines in adults and developmental stages. Experimental Parasitology 57, 34–9.Google Scholar
Raizen, D. M. & Avery, L. (1994). Electrical activity and behaviour in the pharynx of Caenorhabditis elegans. Neuron 12, 483–95.Google Scholar
Rosoff, M. L., Doble, K. E., Price, D. A. & Li, C. (1993). The flp-1 propeptide is processed into multiple, highly similar FMRFamide-like peptides in Caenorhabditis. Peptides 14, 331–8.Google Scholar
Sawada, M. A. & Coggeshell, R. E. (1976). Ionic mechanism of 5-hydroxytryptamine-induced hyperpolarization and inhibitory junctional potential in the bodywall muscle cells of Hirudo medicinalis. Journal of Neurobiology 7, 63–73.CrossRefGoogle Scholar
Ward, S., Thomson, N., White, J. G. & Brenner, S. (1975). Electron microscopical reconstruction of the anterior sensory anatomy of the nematode Caenorhabditis elegans. Journal of Comparative Neurology 160, 313–38.Google Scholar
Willard, A. C. (1981). Effects of serotonin on the generation of the motor programme for swimming by the medicinal leech. Journal of Neuroscience 1, 936–44.CrossRefGoogle ScholarPubMed
Willett, J. D. (1980). Control mechanisms in nematodes. In Nematodes and Biological Models, vol. 1, Behavioral and Developmental Models (ed. Zuckerman, B. M.), pp. 197–225. New York: Academic Press.Google Scholar
Williams, J. A., Shahkolahi, A. M., Abbassi, M. & Donahue, M. J. (1992). Identification of a novel 5-HTN (Nematoda) receptor from Ascaris suum muscle. Comparative Biochemistry and Physiology 101C, 469–74.Google Scholar