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Dietary lipids containing gangliosides reduce Giardia muris infection in vivo and survival of Giardia lamblia trophozoites in vitro

Published online by Cambridge University Press:  13 May 2004

M. SUH ,
M. BELOSEVIC  and
M. T. CLANDININ
M. SUH
Affiliation:
Nutrition and Metabolism Research Group, Departments of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, Alberta T6G 2E9, Canada
M. BELOSEVIC
Affiliation:
Department of Biological Sciences, University of Alberta, Edmonton, AB T6G 2E9, Canada. Department of Medical Microbiology and Immunology, University of Alberta, Edmonton, AB T6G 2E9, Canada.
M. T. CLANDININ
Affiliation:
Nutrition and Metabolism Research Group, Departments of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, Alberta T6G 2E9, Canada Department of Medicine, University of Alberta, Edmonton, Alberta T6G 2E9, Canada
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Abstract

We examined whether a ganglioside supplemented diet affected the course of Giardia muris infection in mice and survival of Giardia lamblia trophozoites in vitro. Female CD-1 mice were fed 1 of 5 experimental diets: standard lab chow as a control diet; semi-synthetic diets containing 20% (w/w) triglyceride based on the fat composition of a conventional infant formula; triglyceride diet; triglyceride diet containing a low level of ganglioside (0·1% w/w); and triglyceride diet containing a high level of ganglioside (1·0% w/w of diet). After 2 weeks of feeding, mice were inoculated with G. muris by gastric intubation and fed the experimental diets during the course of the infection. Cysts released in the faeces and trophozoites present in the small intestine were enumerated at various times post-infection. The average cyst output and the number of trophozoites during the course of the infection in mice fed ganglioside-containing diet were found to be significantly lower (3-log10 reduction) compared to animals fed control diets. The results of in vitro growth studies indicated that gangliosides may be directly toxic to the parasites. Thus, gangliosides have a protective effect against G. muris infection in vivo and affect the survival of G. lamblia trophozoites in vitro.

Keywords

dietgangliosideGiardiaprotozoaintestineinfection
Type
Research Article
Information
Parasitology , Volume 128 , Issue 6 , June 2004 , pp. 595 - 602
Copyright
2004 Cambridge University Press

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References

REFERENCES

BELOSEVIC, M. & FAUBERT, G. M. ( 1983). Giardia muris: Correlation between oral dosage, course of infection, and trophozoite distribution in the mouse small intestine. Experimental Parasitollogy 56, 93–100.CrossRefGoogle Scholar
BELOSEVIC, M., FAUBERT, G. M. & MacLEAN, J. D. ( 1989). Disaccharidase activity in the small intestine of gerbils (Meriones unguiculatus) during primary and challenge infections with Giardia lamblia. Gut 30, 1213–1219.CrossRefGoogle Scholar
BOUHOURS, D. & BOUHOURS, J. F. ( 1983). Developmental changes of hematoside of rat small intestine: Postnatal hydration of fatty acids and sialic acid. Journal of Biological Chemistry 258, 299–304.Google Scholar
BROWN, D. A. & ROSE, J. K. ( 1992). Sorting of GPI-anchored proteins to glycolipid-enriched membrane sub-domains during transport to the apical cell surface. Cell 68, 533–544.CrossRefGoogle Scholar
BURET, A., GALL, D. G. & OLSON, M. E. ( 1991). Growth, activities of enzymes in the small intestine, and ultrastructure of microvillus border in gerbils infected with Giardia duodenalis. Parasitology Research 77, 109–114.CrossRefGoogle Scholar
CLANDININ, M. T. & YAMASHIRO, S. ( 1982). Dietary factors affecting the incidence of dietary fat-induced myocardial lesions. Journal of Nutrition 112, 825–828.CrossRefGoogle Scholar
DANIELS, C. W. & BELOSEVIC, M. ( 1995). Disaccharidase activity in male and female C57BL/6 mice infected with Giardia muris. Parasitology Research 81, 143–147.CrossRefGoogle Scholar
DIAMOND, L. S., HARLOW, S. D. & CUNNICK, C. C. ( 1978). A new medium for the axenic cultivation of Entamoeba histolytica and other Entamoeba. Transactions of the Royal Society of Tropical Medicine and Hygiene 72, 431–432.CrossRefGoogle Scholar
FARTHING, M. J. G. ( 1996). Giardiasis. Gastroenerology Clinics of North America 25, 493–515.CrossRefGoogle Scholar
FOLCH, J. & SLOANE-STANLEY, G. H. ( 1957). A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry 226, 497–509.Google Scholar
FORSTNER, G. G. & WHERRETT, J. R. ( 1973). Plasma membrane and mucosal glycosphingolipids in the rat intestine. Biochimica et Biophysica Acta 306, 446–459.CrossRefGoogle Scholar
GIBSON, G. R., RAMIREZ, D., MAIER, J., CASTILLO, C. & DAS, S. ( 1999). Giardia lamblia: Incorporation of free and conjugated fatty acids into glycerol-based phospholipids. Experimental Parasitology 92, 1–11.Google Scholar
GILLIN, F. D. ( 1987). Giardia lamblia: The role of conjugated and unconjugated bile salts in killing by human milk. Experimental Parasitology 63, 74–83.CrossRefGoogle Scholar
GILLIN, F. D., REINER, D. S. & GAULT, M. J. ( 1985). Cholate-dependent killing of Giardia lamblia by human milk. Infection and Immunity 47, 619–622.Google Scholar
GILLON, J., THAMERY, D. A. & FERGUSON, A. ( 1982). Features of small intestinal pathology (epithelial cell kinetics, intraepithelial lymphocytes, disaccharidase) in a primary Giardia muris infection. Gut 23, 498–506.CrossRefGoogle Scholar
HOLMGREN, J., LINDBLAD, M., FREDMAN, P., SVENNERHOLM, L. & MYRVOLD, H. ( 1985). Comparision of receptors for cholera and Escherichia coli enterotoxins in human intestine. Gasteroenterology 89, 27–35.CrossRefGoogle Scholar
IWAMORI, M., SHIMOMURA, J., TSUYUHARA, S. & NAGAI, Y. ( 1984). Gangliosides of various rat tissues: distribution of ganglio-N-tetraose-containing gangliosides and tissue-characteristic composition of gangliosides. Journal of Biochemistry 95, 761–770.CrossRefGoogle Scholar
JARROL, E. L., MULLER, P. J., MEYER, E. A. & MORSE, S. A. ( 1981). Lipid and carbohydrate metabolism of Giardia lamblia. Molecular and Biochemical Parasitology 2, 187–196.CrossRefGoogle Scholar
JENNNINGS, W., ROWL, R., HECKER, R., GIBSON, G. E., FITCH, R. J. & REID, D. P. ( 1976). The significance of lowered jejunal disaccharidase levels. Australian and New Zealand Journal of Medicine 6, 556–560.CrossRefGoogle Scholar
KARLSSON, K. A. ( 1995). Microbial recognition of target-cell glycoconjugates. Current Opinions in Structural Biology 5, 622–635.CrossRefGoogle Scholar
KYOGASHIMA, M., GINSBURG, V. & KRIVAN, H. C. ( 1989). Escherichia coli K99 binds to N-glycolylsialoparagloboside and N-glycolyl-GM3 found in piglet small intestine. Archives of Biochemistry and Biophysics 270, 391–397.CrossRefGoogle Scholar
LAEGREID, A. & OTNAESS, A. B. K. ( 1987). Trace amouns of ganglioside GM1 in human milk inhibit enterotoxin from Vibrio cholerae and Escherichia coli. Life Sciences 40, 55–62.CrossRefGoogle Scholar
ORTEGA-BARRIA, E., WARD, H. D., KEUTSCH, G. T. & PEREIRA, M. E. ( 1994). Growth inhibition of the intestinal parasite Giardia lamblia by a dietary lectin is associated with arrest of the cell cycle. Journal of Experimental Medicine 94, 2283–2288.CrossRefGoogle Scholar
REINER, D. S., WANG, C. S. & GILLIN, F. D. ( 1986). Human milk kills Giardia lamblia by generating toxic lipolytic products. Journal of Infectious Diseases 154, 825–832.CrossRefGoogle Scholar
ROBERTS-THOMSON, I. C., STEVENS, D. P., MAHMOUD, A. F. & WARREN, K. S. ( 1976). Giardiasis in the mouse: an animal model. Gastroenterology 71, 57–61.Google Scholar
ROHRER, L., WINTERHALTER, K. H., ECKERT, J. & KOHLER, P. ( 1986). Killing of Giardia lamblia by human milk is mediated by unsaturated fatty acids. Antimicrobial Agents and Chemotherapy 30, 254–257.CrossRefGoogle Scholar
ROLSMA, M. D., KUHLENSCHMIDT, T. B., GELBERG, H. B. & KUHLENSCHMIDT, M. ( 1998). Structure and function of a ganglioside receptor for porcine rotavirus. Journal of Virology 72, 9079–9091.Google Scholar
RUEDA, R. J., GARCIA-SALMERON, L., MALDONADO, J. & GIL, A. ( 1996). Changes during lactation in ganglioside distribution in human milk from mothers delivering preterm and term infants. Journal of Biological Chemistry 377, 599–601.Google Scholar
RUEDA, R. J., SABATELL, L., MALDINADO, J., MOLINA-FONT, J. A. & GIL, A. ( 1998). Addition of gangliosides to an adapted milk formula modifies levels of fecal Escherichia coli in preterm newborn infants. Journal of Pediatrics 133, 90–94.CrossRefGoogle Scholar
SORICE, M., GRIGGI, T., NICODEMO, G., GAROFALO, T., MARANGI, M., SANGUIGNI, S., BECKER, S. I. & MIRELMAN, D. ( 1996). Evidence for the existence of ganglioside molecules in the antigen of Entamoeba histolytica. Parasite Immunology 18, 133–137.CrossRefGoogle Scholar
STEEL, R. G. D. & TORRIE, J. H. ( 1990). Principles and Procedures of Statistics, 2nd Edn. McGraw-Hill Inc., New York.
STEVENS, T. L., GIBSON, G. R., ADAM, R., MAIER, J., ALLISON-ENNIS, M. & DAS, S. ( 1997). Uptake and cellular localization of exogenous lipids by Giardia lamblia, a primitive eukaryote. Experimental Parasitology 86, 133–143.CrossRefGoogle Scholar
SUZUKI, K. ( 1964). A simple and accurate micro-method for quantitative determination of ganglioside patterns. Life Sciences 3, 1227–1233.CrossRefGoogle Scholar
UNDERDOWN, B. J., ROBERTS-THOMSON, I. C., ANDERS, R. F. & MITCHELL, G. F. ( 1981). Giardiasis in mice: studies on the characteristics of chronic infection in C3H/He mice. Journal of Immunology 126, 669–672.Google Scholar
VAZQUEZ, E., GIL, A. & RUEDA, R. ( 2001). Dietary gangliosides positively modulate the percentage of Th1 and Th2 lymphocyte subsets in small intestine of mice at weaning. BioFactors 15, 1–9.CrossRefGoogle Scholar
WALTERSPIEL, J. N., MORROW, A. L., GUERRERO, M. L., RUIZ-PALACIOS, G. M. & PICKERING, L. K. ( 1994). Secretory anti-Giardia lamblia antibodies in human milk protective effect against diarrhea. Pediatrics 93, 28–31.Google Scholar
WATARAI, S., SUGIMOTO, C., ONOE, S., ONUMA, M. & YASUDA, T. ( 1995). Gangliosides as a possible receptor on bovine erythrocytes for Theileria sergenti. Journal of Veterinary Medical Science 57, 17–22.CrossRefGoogle Scholar
WILLIAMS, M. A. & McCLUER, R. H. ( 1980). The use of Sep-Pak C18 cartridges during the isolation of gangliosdies. Journal of Neurochemistry 35, 266–269.CrossRefGoogle Scholar
WOLFE, M. S. ( 1992). Giardiasis. Clinical Microbiology Reviews 5, 93–100.CrossRefGoogle Scholar