Hostname: page-component-848d4c4894-jbqgn Total loading time: 0 Render date: 2024-06-30T12:55:57.296Z Has data issue: false hasContentIssue false

Echinostoma caproni and E. trivolvis alter the binding of glycoconjugates in the intestinal mucosa of C3H mice as determined by lectin histochemistry

Published online by Cambridge University Press:  05 June 2009

T. Fujino
Affiliation:
Department of Parasitology, Faculty of Medicine, Kyushu University, Fukuoka 812, Japan
B. Fried
Affiliation:
Department of Biology, Lafayette College, Easton, Pennsylvania 18042, USA

Abstract

Mouse (C3H) mucosal glycoconjugates were examined in normal small intestines and intestines infected with Echinostoma caproni, or E. trivolvis using six different fluorescein-conjugated lectins: Triticum, vulgaris agglutinin (WGA), Ulex europaeus agglutinin I (UEA-I), Ricinus communis agglutinin I (RCA-I). Glycine max soybean agglutinin (SBA), Dolichos biflorus agglutinin (DBA), and Arachis hypogaeu peanut agglutinin (PNA). The expression of lectin-binding sites and the intensity of the binding of lectins in the mouse small intestines were changed by infection with the echinostomes. Specific differences in the reaction to glycoproteins were clearly observed between the mouse intestines infected with E. caproni and those infected with E. trivolvis. In E. caproni infection, binding of most of the lectins to the villi was remarkably reduced in accord with the villous atrophy and loss of goblet cells. In contrast, in E. trivolvis infection, the binding of WGA, RCA-I and DBA was reduced in the microvillar surfaces, but binding of UEA-I and SBA were unchanged compared to the control intestines. The lectin binding to goblet cells in E. trivolvis-infected mice mostly increased. These observations may reflect the marked increase in goblet cells and the less severe damage in the villi of E. trivolvis infection compared to E. caproni infection. Most of the glycoconjugates were slightly reduced in the hyperplastic crypts except for N-acetyl glucosamine. It is possible that glucose metabolism in the host intestines infected with E. trivolvis was activated. resulting in an increase in the rate of mucin synthesis as well as qualitative changes in mucus, thereby mediating the expulsion of the worms.

Type
Research Papers
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

Andresen, K., Simonsen, P. E., Andersen, B. J. & Birch-Andersen, A. (1989) Echinostoma caproni in mice: shedding of antigens from the surface of an intestinal trematode. International Journal for Parasitology, 19, 111118.CrossRefGoogle ScholarPubMed
Bindseil, E. & Christensen, N. Ø. (1984) Thymus-independent crypt hyperplasia and villous atrophy in the small intestine of mice infected with the trematode Echinostoma revolutum. Parasitology, 88, 431438.CrossRefGoogle ScholarPubMed
Boland, C. R., Montgomery, C. K. & Kim, Y. S. (1982a) Alterations in human colonic mucin occurring with cellular differentiation and malignant transformation. Proceedings of the National Academy of Sciences, USA, 79, 20512055.CrossRefGoogle ScholarPubMed
Boland, C. R., Montgomery, C. K. & Kim, Y. S. (1982b) A cancer-associated mucin alteration in benign colonic polyps. Gastroenterology, 82, 664672.CrossRefGoogle ScholarPubMed
Calderó, J., Campo, E., Calomarde, X. & Torra, M. (1988) Distribution and changes of glycoconjugates in rat colonic mucosa during development. A histochemical study using lectins. Histochemistry, 90, 261270.CrossRefGoogle ScholarPubMed
Castro, G. A., Olson, L. J. & Baker, R. D. (1967) Glucose malabsorption and intestinal histopathology in Trichinella spiralis-infected guinea pigs. Journal of Parasitology, 53, 595612.CrossRefGoogle ScholarPubMed
Colony, P. C. & Steely, J. (1987) Lectin binding patterns in developing rat colon. Gastroenterology, 92, 11161126.CrossRefGoogle ScholarPubMed
Etzler, M. E. & Branstrator, M. L. (1974) Differential localization of cell surface and secretory components in rat intestinal epithelium by use of lectins. Journal of Cell Biology, 62, 329343.CrossRefGoogle ScholarPubMed
Fischer, J., Klein, P. J., Vierbuchen, M., Skutta, B., Uhlenbruck, G. & Fischer, R. (1984) Characterization of glycoconjugates of human gastrointestinal mucosa by lectins. I. Histochemical distribution of lectin binding sites in normal alimentary tract as well as in benign and malignant gastric neoplasms. Journal of Histochemistry and Cytochemistry, 32, 681689.CrossRefGoogle ScholarPubMed
Forstner, G., Wesley, A. & Forstner, J. (1982) Clinical aspects of gastrointestinal mucus. In: Mucus in Health and Disease-II. pp. 199224. (Edited by Chantler, E. N., Elder, J. B. & Elstein, M.) Plenum Press, New York.CrossRefGoogle Scholar
Freeman, H. J., Lotan, R. & Kim, Y. S. (1980) Application of lectins for detection of goblet cell glycoconjugate differences in proximal and distal colon of the rat. Laboratory investigation, 42, 405412.Google ScholarPubMed
Hosier, D. W. & Fried, B. (1986) Infectivity, growth, and distribution of Echinostoma revolutum in Swiss Webster and ICR mice. Proceedings of the Helminthological Society of Washington, 53, 173176.Google Scholar
Huffman, J. E. & Fried, B. (1990) Echinostoma and echinostomiasis. Advances in Parasitology, 29, 215269.CrossRefGoogle ScholarPubMed
Huffman, J. E., Michos, C. & Fried, B. (1986) Clinical and pathological effects of Echinostoma revolutum (Digenea: Echinostomatidae) in the golden hamster, Mesocricetus auratus. Parasitology, 93, 505515.CrossRefGoogle ScholarPubMed
Huffman, J. E., Alcaide, A. & Fried, B. (1988a) Single and concurrent infections of the golden hamster, Mesocricetus auratus with Echinostoma revolutum and E. liei (Trematoda: Digenea). Journal of Parasitology, 74, 604608.CrossRefGoogle Scholar
Huffman, J. E., Iglesias, D. & Fried, B. (1988b) Echinostoma revolutum: Pathology of extraintestinal infection in the golden hamster. International Journal for Parasitology, 18, 873874.CrossRefGoogle ScholarPubMed
Jacobs, L. R. & Huber, P. W. (1985) Regional distribution and alterations of lectin binding to colorectal mucin in mucosal biopsies from controls and subjects with inflammatory bowel disease. Journal of Clinical Investigation, 75, 112118.CrossRefGoogle Scholar
Kim, Y. S. & Isaacs, R. (1975) Glycoprotein metabolism in inflammatory and neoplastic diseases of the human colon. Cancer Research, 35, 20922097.Google ScholarPubMed
Kim, Y. S., Isaacs, R. & Perdomo, J. M. (1974) Alterations of membrane glycopeptides in human colonic adenocarcinoma. Proceedings of the National Academy of Sciences, USA, 71, 48694873.CrossRefGoogle ScholarPubMed
Koninkx, J. F. J. G., Mirck, M. H., Hendriks, H. G. C. J. M., Mouwen, J. M. V. M. & Van Dijk, J. E. (1988) Nippostrongylus brasiliensis: histochemical changes in the composition of mucins in goblet cells during infection in rats. Experimental Parasitology, 65, 8490.CrossRefGoogle ScholarPubMed
Miller, H. R. P. & Jarrett, W. F. H. (1971) Immune reactions in mucous membranes: I. Intestinal mast cell response during helminth expulsion in the rat. Immunology, 20, 277288.Google ScholarPubMed
Miller, H. R. P. & Nawa, Y. (1979) Nippostrongylus brasiliensis: intestinal goblet-cell response in adoptively immunized rats. Experimental Parasitology, 47, 8190.CrossRefGoogle ScholarPubMed
Mohandas, A. & Nadakal, A. M. (1978) In vivo development of Echinostoma malayanum Leiper, 1911, with notes on effects of population density, chemical composition and pathogenicity and in vitro excystment of the metacercaria (Trematoda: Echinostomatidae). Zeitschrift für Parasitenkunde, 55, 139151.CrossRefGoogle ScholarPubMed
Odaibo, A. B., Christensen, N. Ø. & Ukoli, F. M. A. (1988) Establishment, survival, and fecundity in Echinostoma caproni (Trematoda) infections in NMRI mice. Proceedings of the Helminthological Society of Washington, 55, 265269.Google Scholar
Odaibo, A. B., Christensen, N. Ø. & Ukoli, F. M. A. (1989) Further studies on the population regulation in Echinostoma caproni infections in NMRI mice. Proceedings of the Helminthological Society of Washington, 56, 192198.Google Scholar
Scofield, A. M. (1974) Intestinal absorption of D-glucose and D-galactose in rats infected with Nematospiroides dubius. Comparative Biochemistry and Physiology, 47A, 219231.CrossRefGoogle Scholar
Scofield, A. M. (1977) Intestinal absorption of hexoses in rats infected with Nippostrongylus brasiliensis. International Journal for Parasitology, 7, 159165.CrossRefGoogle ScholarPubMed
Scofield, A. M. (1980) Effect of level of infection with Nippostrongylus brasiliensis on intestinal absorption of hexoses in rats. International Journal for Parasitology, 10, 375380.CrossRefGoogle ScholarPubMed
Selzman, H. M. & Liebelt, R. A. (1962) Paneth cell granule of mouse intestine. Journal of Cell Biology, 15, 136139.CrossRefGoogle ScholarPubMed
Simonsen, P. E. & Andersen, B. J. (1986) Echinostoma revolutum, in mice; dynamics of the antibody attack to the surface of an intestinal trematode. International Journal for Parasitology, 16, 475482.CrossRefGoogle Scholar
Simonsen, P. E., Bindseil, E. & Køie., M. (1989) Echinostoma caproni in mice: studies on the attachment site of an intestinal trematode. International Journal for Parasitology, 19, 561566.CrossRefGoogle ScholarPubMed
Simonsen, P. E., Vennervald, B. J. & Birch-Andersen, A. (1990) Echinostoma caproni in mice: ultrastructural studies on the formation of immune complexes on the surface of an intestinal trematode. International Journal for Parasitology, 20, 935941.CrossRefGoogle ScholarPubMed
Thorndyke, M. & Whitfield, P. J. (1987) Vasoactive intestinal polypeptide immunoreactive tegumental cells in the digenean Echinostoma liei: possible role in host-parasite interactions. General Comparative Endocrinology, 68, 202207.CrossRefGoogle ScholarPubMed
Uber, C. L., Roth, R. L. & Levy, D. A. (1980) Expulsion of Nippostrongylus brasiliensis by mice deficient in mast cells. Nature, 287, 226228.CrossRefGoogle ScholarPubMed
Weinstein, M. S. & Fried, B. (1991) The expulsion of Echinostoma trivolvis and retention of Echinostoma caproni in the ICR mouse: pathological effects. International Journal for Parasitology, 21, 255257.CrossRefGoogle ScholarPubMed