Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-20T04:22:36.417Z Has data issue: false hasContentIssue false
  • English
  • Français

Hymenolepis diminuta: changes in intestinal morphology and the enterochromaffin cell population associated with infection in male C57 mice

Published online by Cambridge University Press:  06 April 2009

D. M. Mckay ,
D. W. Halton ,
C. F. Johnston ,
I. Fairweather  and
C. Shaw
D. M. Mckay
Affiliation:
School of Biology and Biochemistry, The Queen's University, Belfast BT7 1NN, U.K.
D. W. Halton
Affiliation:
School of Biology and Biochemistry, The Queen's University, Belfast BT7 1NN, U.K.
C. F. Johnston
Affiliation:
Department of Medicine, The Queen's University, Belfast BT7 1NN, U.K.
I. Fairweather
Affiliation:
School of Biology and Biochemistry, The Queen's University, Belfast BT7 1NN, U.K.
C. Shaw
Affiliation:
Department of Medicine, The Queen's University, Belfast BT7 1NN, U.K.
Get access Rights & Permissions [Opens in a new window]

Summary

Mean villus height, crypt depth and the number of 5-HT-positive enterochromaffin (EC) cells have been examined in two regions of the small intestine (20–30° and 60–70° distance from the pylorus) of male, 6 to 8-week-old, C57 mice following a 5-cysticercoid infection of the rat tapeworm, Hymenolepis diminuta. Test mice and sham-infected controls were autopsied 0, 4, 8, 10, 14 and 28 days post-primary infection (p-1°-i) and 2, 4, 5, 7 and 14 days post-secondary infection (p-2°-i), administered 28 days p-1°-i. Morphometric analysis revealed a statistically significant increase in crypt depth in the 60–70°o intestine region in infected mice during both primary and secondary infections; no significant deviation from the control was observed for villus height in infected mice. Statistical analysis showed a significant increase in the number of 5-HT-positive EC cells in infected mice. This response occurred in the lower portion of the intestine on days 10-p-1°-i and 5-p-2°-i, and was not due to increased mucosal surface area in this region. Results are discussed with reference to murine cestode rejection and the possible involvement therein of the neuroendocrine system.

Keywords

Hymenolepis diminutacestodeC57 mouseintestinal morphometricsvillus height/crypt depthenterochromaffin cell5-hydroxytryptamine
Type
Research Article
Information
Parasitology , Volume 101 , Issue 1 , August 1990 , pp. 107 - 113
Copyright
Copyright © Cambridge University Press 1990

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

Alghali, S. O. (1987). Hymenolepis citelli, H. diminuta, H. microstoma: immunoglobulin-containing cells in the lamina propria of the mouse gut during primary and secondary infections. Journal of Helminthology 61, 329–40.Google Scholar
Anderson, N., Hansky, J. & Titchen, D. A. (1985). Effects of plasma pepsinogen, gastrin and pancreatic polypeptide on Ostertagia spp. transferred directly into the abomasum of sheep. International Journal for Parasitology 15, 159–65.CrossRefGoogle ScholarPubMed
Bartlet, A. L. (1968). 5-hydroxytryptamine and enterochromafnn cells in the ovine biliary mucosa during fasciohasis. British Journal of Pharmacology and Chemotherapy 33, 408–12.CrossRefGoogle Scholar
Befus, A. D. (1977). Hymenolepis diminuta and H. microstoma: mouse immunoglobulin binding to the tegumental surface. Experimental Parasitology 41, 242–51.CrossRefGoogle Scholar
Befus, A. D., Johnston, N. & Bienenstock, J. (1979). Nippostrongylus brasiliensis: mast cells and histamine levels in tissues of infected and normal rats. Experimental Parasitology 48, 1–8.CrossRefGoogle ScholarPubMed
Bindseil, E. & Christensen, O. (1984). Thymus-independent crypt hyperplasia and villus atrophy in the small intestine of mice infected with the trematode Echinostoma revolutum. Parasitology 88, 431–8.CrossRefGoogle Scholar
Blalock, J. E., Harbour-McMenamin, D. & Smith, E. M. (1985). Peptide hormones shared by the neuroendocrine and immunologic systems. Journal of Immunology 135 (Suppl.), 859s–861s.Google Scholar
Castro, G. A., Copeland, E. M., Dudrick, S. J. & Johnston, L. R. (1976). Serum and central gastrin levels in rats infected with intestinal parasites. American Journal of Tropical Medicine and Hygiene 25, 848–53.CrossRefGoogle Scholar
Coupland, R. E. & Fujita, T. (1976). Chromaffin, Enterochromaffin and Related Cells. Amsterdam, Oxford and New York: Elsevier Scientific Publishing Company.Google Scholar
Dawkins, H. J. S., Muir, G. M. & Grove, D. I. (1981). Histopathological appearances in primary and secondary infections with Strongyloides ratti in mice. International Journal for Parasitology 11, 97–103.CrossRefGoogle ScholarPubMed
Donowitz, M., Charney, A. N. & Heffernan, J. M. (1977). Effect of serotonin treatment on intestinal transport in the rabbit. American Journal of Physiology 232, E85–E94.Google ScholarPubMed
Facer, P., Bishop, A. E., Lloyd, R. V., Wilson, B. S., Hennessy, R. J. & Polak, J. M. (1985). Chromogranin A: A newly recognised marker for endocrine cells of the human gastrointestinal tract. Gastroenterology 89, 1366–73.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.Google Scholar
Ferreria, N. (1971). Argentaffin and other endocrine cells of the small intestine of the adult mouse. 1. Ultrastructure and classification. American Journal of Anatomy 131, 315–30.Google Scholar
Grube, D. (1986). The endocrine cells of the digestive system: amines, peptides and modes of action. Anatomy and Embryology 175, 151–62.CrossRefGoogle ScholarPubMed
Gruner, S. & Mettrick, D. (1984). The effects of 5-hvdroxvtrvptamine on glucose absorption by Hymenolepis diminuta (Cestoda) and by the mucosa of the rat small intestine. Canadian Journal of Zoology 62, 798–803.Google Scholar
Haverback, B. J. & Davidson, J. D. (1958). Serotonin and the gastrointestinal tract. Gastroenterology 35, 570–7.CrossRefGoogle ScholarPubMed
Hopkins, C. A. (1980). Immunity and Hymenolepis diminuta. In Biology of the Tapeworm Hymenolepis diminuta (ed. Arai, H.), pp. 551–614. London and New York: Academic Press.Google Scholar
Hutton, J. L., Peshavaria, M., Johnston, C. F., Ravazzola, M. & Orci, I. (1988). Immunolocalisation of Betagranin: a Chromogranin A-related protein of the pancreatic B-cell. Endocrinology 122, 1014–20.CrossRefGoogle Scholar
Koninkx, J. F. J. G., Mirck, M. H., Hendricks, H. C. C. M., Mouwen, J. M. V. M. & Van Dijk, J. E. (1988). Nippostrongylus brasiliensis: Histochemical changes in the composition of mucins in goblet cells during infections in rats. Experimental Parasitology 65, 84–90.Google Scholar
McCaigue, M. D. (1987). C57 mice and the tapeworm Hymenolepis diminuta: some immunological aspects of host–parasite interactions. Ph.D. thesis, The Queen's University, Belfast.Google Scholar
McCaigue, M. D. & Halton, D. W. (1987). Immunological damage to Hymenolepis diminuta following a challenge infection in C57 mice. International Journal for Parasitology 17, 795–803.Google Scholar
McCaigue, M. D., Halton, D. W. & Hopkins, C. A. (1986). Hymenolepis diminuta: Ultrastructural abnormalities in worms from C57 mice. Experimental Parasitology 62, 51–60.Google Scholar
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, 217–23.CrossRefGoogle ScholarPubMed
Miller, H. R. P. & Huntley, J. F. (1981). Protection against nematodes by intestinal mucus. In Mucus in Health and Disease-II (ed. Chantler, E. N., Elder, J. B. & Elstein, M.), pp. 243–5. London and New York: Plenum Press.Google Scholar
Miller, H. R. P. & Jarrett, W. F. H. (1971). Immune reactions in mucus membranes. 1. Intestinal mast cell response during helminth expulsion in the rat. Immunology 20, 277–88.Google Scholar
Murray, M., Miller, H. R. P., Sanford, J. & Jarrett, W. F. H. (1971). 5-hydroxytryptamine in intestinal immunological reactions. International Archives of Allergy 40, 236–47.Google Scholar
Murray, M., Smith, W. D., Waddell, A. H. & Jarrett, W. H. F. (1971). Nippostrongylus brasiliensis: Histamine and 5-hydroxytrvptamine inhibition and worm expulsion. Experimental Parasitology 30, 58–63.CrossRefGoogle ScholarPubMed
Nawa, Y. & Korenaga, M. (1983). Mast and goblet cell responses in the small intestine of rats concurrently infected with Nippostrongylus brasiliensis and Strongvloides ratti. Journal of Parasitology 69, 1168–70.Google Scholar
O'Dorisio, M. S. (1986). Neuropeptides and gastrointestinal immunity. American Journal of Medicine 81, (Suppl. B6), S74–S82.CrossRefGoogle ScholarPubMed
Ogilvie, B. M. & Jones, V. E. (1973). Immunity in the parasitic relationship between helminths and hosts. Progressive Allergy 17, 93–144.Google ScholarPubMed
Ovington, K. S., Bacarese-Hamilton, A. J. & Bloom, S. R. (1985). Nippostrongylus brasiliensis: Changes in plasma levels of gastrointestinal hormones in the infected rat. Experimental Parasitology 60, 276–84.CrossRefGoogle ScholarPubMed
Roepstroff, A. & Andreasson, J. (1982). Course of heavy primary infection and earlier immunologically mediated rejection of secondary infections of Hymenolepis diminuta in mice. International Journal for Parasitology 12, 23–8.Google Scholar
Sokal, R. R. & Rohlf, R. S. (1981). Biometry, 2nd Edn.San Francisco: Freeman.Google Scholar
Stephenson, L. S., Pond, W. G., Nesheim, M. C., Krook, L. P. & Crompton, D. W. T. (1980). Ascaris suum: Nutrient absorption, growth and intestinal pathology in young pigs experimentally infected with 15-day-old larvae. Experimental Parasitology 49, 15–25.Google Scholar
Stevens, F. M. & Shaw, C. (1982). Prolactin-like immunoreactivity in human small-intestinal mucosa. British Medical Journal 284, 1014–16.Google Scholar
Thompson, J. H. (1971). Serotonin and the alimentary tract. Research Communications in Chemical Pathology and Pharmacology 2, 687–781.Google Scholar
Titchen, D. A. & Reid, A. M. (1988). Putative roles of peptides in the genesis and control of parasitic disease. In Aspects of Digestive Physiology in Ruminants (ed. Dobson, A. & Dobson, M. J.), pp. 217–37. London: Caustock and Cornell.Google Scholar
Tutton, P. J. M. (1974). The influence of serotonin on crypt cell proliferation in the jejunum of the rat. Virchows Archives and Abstracts of B Cell Pathology 16, 79–87.CrossRefGoogle Scholar
Wingren, V., Enerbäck, L., Ahlman, H., Allenmark, S. & Dahlstrom, A. (1983). Amines of the mucosal mast cell of the gut in normal and nematode infected rats. Histochemistry 17, 145–58.Google Scholar