Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-04T19:26:42.511Z Has data issue: false hasContentIssue false

Circadian variation in the distribution of Hymenolepis diminuta (Cestoda) and 5-hydroxytryptamine levels in the gastro-intestinal tract of the laboratory rat

Published online by Cambridge University Press:  06 April 2009

C. H Cho
Affiliation:
Department of Zoology, University of Toronto, Toronto, Ontario, CanadaM5S 1A1
D. F. Mettrick
Affiliation:
Department of Zoology, University of Toronto, Toronto, Ontario, CanadaM5S 1A1

Summary

The circadian migration of Hymenolepis diminuta in the small intestine of the rat may be correlated with a circadian variation in 5-hydroxytryptamine levels present in worm tissue, in the intestinal lumen, in the intestinal mucosa, with the amount of food present in the small intestine and in arterial blood. The 5-HT and food levels in uninfected animals were also determined. The 16.00 h stage in the circadian cycle marks both the commencement of host feeding, followed by rising 5-HT levels in both worm and host tissues, and initiation of an anteriad migration of worm biomass. It was found that 5-HT levels in the intestine of parasitized animals were significantly higher than in the intestine of uninfected controls. This is the first report of circadian variation in mucosal and luminal 5-HT levels. The similarity in the circadian patterns of worm migration and worm luminal, mucosal and blood 5-HT levels were striking. Fasting eliminated the circadian rise in intestinal 5-HT levels and the worms did not migrate. Luminal 5-HT levels were significantly lower in fasted animals than in the comparable rats fed ad libitum. When the intestine was ligatured at the pyloric sphincter, worm anteriad migration still occurred after feeding, indicating that the presence of exogenous food in the intestine is not a factor in the initial migration of the worms.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1982

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

Ahlman, H., Lundberg, J., Dahlstrom, A., & Kewenter, J., (1976). A possible vagal adrenergic release of serotonin from enterochromaffin cells in the cat. Acta physiologica scandinavica 98, 336–75.CrossRefGoogle ScholarPubMed
Arai, H. S., (1980). Migratory activity and related phenomena in Hymenolepis diminuta. In Biology of the Tapeworm Hymenolepis diminuta (ed. Arai, H S.),pp. 615–37. New York: Academic Press.CrossRefGoogle Scholar
Barker, L. R., Bueding, E., & Timms, A. R., (1966). The possible role of acetylcholine in Schistosoma mansoni. British Journal of Pharmacological Chemotherapy 26, 656–65.CrossRefGoogle ScholarPubMed
Beernink, K. D., Nelson, S. D., & Mansour, T. E., (1963). Effect of lysergic acid derivatives on the liver fluke, Fasciola hepatica. International Journal of Neuropharmacology 2, 102–12.CrossRefGoogle Scholar
Biggio, G., Piccardi, M. P., Porceddu, M. L., & Gessa, G. L., (1977). Changes in gastro-intestinal serotonin content associated with fasting and satiation. Experientia 33, 745–6.CrossRefGoogle ScholarPubMed
Cho, C. H., Ogle, C. W., & Dai, S., (1976). Acute gastric ulcer formation in response to electrical vagal stimulation in rats. European Journal of Pharmacology 35, 215–19.CrossRefGoogle ScholarPubMed
Crompton, D. W. T., (1973). The sites occupied by some parasitic helminths in the alimentary tract of vertebrates. Biological Reviews 48, 2783.CrossRefGoogle ScholarPubMed
Dunkley, L. C., & Mettrick, D. F., (1977). Hymenolepis diminuta: Migration, and the rat host's intestinal and blood plasma glucose levels following dietary carbohydrate intake. Experimental Parasitology 41, 213–28.CrossRefGoogle Scholar
Hariri, M. J., (1974). Occurrence and concentration of biogenic amines in Mesocestoides corti (Cestoda). Journal of Parasitology 60, 737–43.CrossRefGoogle ScholarPubMed
Hillman, G. R., & Senft, A. W., (1973). Schistosome motility measurements: Response to drugs. Journal of Pharmacology and Experimental Therapeutics 185, 177–84.Google ScholarPubMed
Hillman, G. R., Olsen, N. J., & Senft, A. W., (1974). Effect of methysergide and dihydroergotamine on Schistosoma mansoni. Journal of Pharmacology and Experimental Therapeutics 188, 529–35.Google ScholarPubMed
Hopkins, C. A., & Allen, L. M., (1979). Hymenolepis diminuta: the role of the tail in determining the position of the worm in the intestine of the rat. Parasitology. 79, 401–10.CrossRefGoogle ScholarPubMed
Konturek, S., Radecki, T., Pawlik, W., Thor, P., & Biernat, J., (1974). Significance of vagus nerves in the regulation of pancreatic secretion. Acta physiologica polonica 25, 423–33.Google ScholarPubMed
Mansour, T. E., (1957). The effect of lysergic acid diethylamide, 5-hydroxytryptamine, and related compounds on the liver fluke, Fasciola hepatica. British Journal of Pharmacology 12, 406–10.Google ScholarPubMed
Mansour, T. E., (1959). The effect of serotonin and related compounds on the carbohydrate metabolism of the liver fluke, Fasciola hepatica. Journal of Pharmacology and Experimental Therapeutics 126, 212–16.Google ScholarPubMed
Mansour, T. E., (1962). Effect of serotonin on glycolysis in homogenates from the liver fluke, Fasciola hepatica. Journal of Pharmacology and Experimental Therapeutics 135, 94101.Google ScholarPubMed
Mansour, T. E., (1964). The pharmacology and biochemistry of parasitic helminths. Advances in Pharmacology 3, 129–62.CrossRefGoogle ScholarPubMed
Mansour, T. E., (1979). Chemotherapy of parasitic worms: new biochemical strategies. Science 205, 462–9.CrossRefGoogle ScholarPubMed
Mansour, T. E., & Mansour, J. M., (1962). Effects of serotonin (5-hydroxytryptamine) and adenosine 3',5'-phosphate on phosphofructokinase from the liver fluke, Fasciola hepatica. Journal of Biological Chemistry 237, 629–34.CrossRefGoogle Scholar
Mettrick, D. F., (1971a). Effect of host dietary constituents on intestinal pH and the migrational behavior of the rat tapeworm Hymenolepis diminuta. Canadian Journal of Zoology 49, 1513–25.CrossRefGoogle ScholarPubMed
Mettrick, D. F., (1971b). Hymenolepis diminuta: pH changes in rat intestinal contents and worm migration. Experimental Parasitology 29, 386401.CrossRefGoogle ScholarPubMed
Mettrick, D. F., (1975). Correlations between the amino acid pools of Hymenolepis diminuta and the rat intestine. Canadian Journal of Zoology 53, 320–31.CrossRefGoogle ScholarPubMed
Mettrick, D. F., & Cho, C. H., (1981a). Migration of Hymenolepis diminita (Cestoda,) and changes in 5-HT (Serotonin) levels in the rat host following parenteral and oral 5-HT administration. Canadian Journal of Physiology and Pharmacology 59, 281–6.CrossRefGoogle ScholarPubMed
Mettrick, D. F., & Cho, C. H., (1981b). Hymenolepis diminuta: Effect of electrical vagal stimulation on worm migration. Journal of Parasitology 67, 386–90.CrossRefGoogle Scholar
Mettrick, D. F., & Podesta, R. B., (1974). Ecological and physiological aspects of helminth–host interactions in the mammalian gastrointestinal canal. In Advances in Parasitology, vol. 13 (ed. Dawes, Ben), pp. 183278. London: Academic Press.Google Scholar
Mettrick, D. F., & Podesta, R. B., (1982). Effect of gastrointestinal hormones and amines on intestinal motility and the migration of Hymenolepis diminuta in the rat small intestine. International Journal for Parasitology 12, 151–4.CrossRefGoogle ScholarPubMed
Mettrick, D. F., Rahman, M. S., & Podesta, R. B., (1981). Effect of 5-hydroxytryptamine (5-HT; Serotonin) on in vitro glucose uptake and glycogen reserves in Hymenolepis diminuta. Molecular and Biochemical Parasitology 4, 217–24.CrossRefGoogle ScholarPubMed
Podesta, R. B., & Mettrick, D. F., (1981). A simple method for analyzing oral and intravenous treatment effects on biomass re-distribution of Hymenolepis diminuta in the rat intestine. Canadian Journal of Zoology 59, 861–3.CrossRefGoogle Scholar
Read, C. P., & Kilejian, A. Z., (1969). Circadian migratory behaviour of a cestode symbiote in the rat host. Journal of Parasitology 55, 584–8.CrossRefGoogle ScholarPubMed
Sauerbier, I., & von Mayersbach, H., (1976). Circadian variation of serotonin levels in human blood. Hormone Metabolic Research 8, 157–8.CrossRefGoogle ScholarPubMed
Schwartz, T. W., Holst, J. J., Fahrenkrug, J., Lindkaer-Jensen, S., Nielsen, O. V., Rehfeld, J. F., Schaffalitzky de Muckadell, O. B., & Stadil, F., (1978). Vagal, cholinergic regulation of pancreatic polypeptide secretion. Journal of Clinical Investigation 61, 781–9.CrossRefGoogle ScholarPubMed
Stone, D. B., & Mansour, T. E., (1967). Phosphofructokinase from the liver fluke, Fasciola hepatica. 1. Activation by adenosine 3',5'-phosphate and by serotonin. Molecular Pharmacology 3, 161–76.Google Scholar
Tobe, T., Izumikawa, F., Sano, M., & Tanaka, C., (1976). Release mechanisms of 5-HT in mammalian gastrointestinal tract — especially, vagal release of 5-HT. In Endocrine Out and Pancreas (ed. Fujita, T.), pp. 371–80. Amsterdam: Elsevier.Google Scholar
Weissbach, H., Waalkes, T. P., & Udenfriend, S., (1958). A simplified method for measuring serotonin in tissues; simultaneous assay of both serotonin and histamine. Journal of Biological Chemistry 230, 865–71.CrossRefGoogle Scholar