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Entamoeba histolytica Gal/GalNAc lectin depletes antioxidant defences of target epithelial cells

Published online by Cambridge University Press:  13 May 2004

S. RAWAL ,
S. MAJUMDAR ,
V. DHAWAN  and
H. VOHRA
S. RAWAL
Affiliation:
Department of Experimental Medicine and Biotechnology, Post-graduate Institute of Medical Education and Research, Sector-12, Chandigarh 160 012, India
S. MAJUMDAR
Affiliation:
Department of Experimental Medicine and Biotechnology, Post-graduate Institute of Medical Education and Research, Sector-12, Chandigarh 160 012, India
V. DHAWAN
Affiliation:
Department of Experimental Medicine and Biotechnology, Post-graduate Institute of Medical Education and Research, Sector-12, Chandigarh 160 012, India
H. VOHRA
Affiliation:
Department of Experimental Medicine and Biotechnology, Post-graduate Institute of Medical Education and Research, Sector-12, Chandigarh 160 012, India
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Abstract

Among the variety of virulence factors of Entamoeba histolytica, an adherence lectin (Gal/GalNAc, 260 kDa) is known to mediate colonization and subsequent host responses. Gal/GalNAc lectin is universally recognized by the immune sera of patients with amoebic liver abscess. It plays a crucial role in cytolysis and phagocytosis of human and rat colonic mucin glycoproteins. The objective of the present study was to elucidate the role of antioxidants in E. histolytica Gal/GalNAc lectin-induced signals in the target epithelial cells. We have attempted to define a pathway in target cells, Henle-407 cells (human intestinal epithelial cell line), that could link this immunodominant antigen to a known biological pathway for target cell activation and triggering of subsequent disease pathology/parasite survival. Since several workers have demonstrated that cAMP and cGMP may act as important cellular signals for altering ion transport, so in the present study, cAMP and cGMP levels were measured in Henle-407 cells which showed significant increase at 15 min after stimulation. Elevated cAMP and cGMP levels are implicated in altered electrolyte transport and conductance. Results showed that there were increased levels of ROS and RNI which led to reduced activities of antioxidant enzymes – catalase, superoxide dismutase and glutathione peroxidase. Despite the increased glutathione (reduced) levels, the enzymes were not able to combat the damage caused by ROS and RNI. Thus, there was an increased local concentration of the free radicals and reduced activities of all the three enzymes which could damage the target cell in terms of cytoskeleton and permeability changes.

Keywords

Entamoeba hystolyticaglycoproteinsadherence lectinGal/GalNAc lectin
Type
Research Article
Information
Parasitology , Volume 128 , Issue 6 , June 2004 , pp. 617 - 624
Copyright
2004 Cambridge University Press

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References

REFERENCES

ASAOKA, Y., NAKAMURA, S., YOSHIDA, K. & NISHIZUKA, Y. (1992). Protein kinase C, calcium and phospholipid degradation. Trends in Biochemical Sciences 17, 414–417.CrossRefGoogle Scholar
BAKER, S. S. & CAMPBELL, C. I. (1991). Rat enterocyte injury by oxygen dependent process. Gastroenterology 101, 716–720.CrossRefGoogle Scholar
BECKMAN, J. S., BECKMAN, T. W., CHE, J., MARSHALL, P. A. & FREEMAN, B. A. (1990). Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proceedings of the National Academy of Sciences, USA 87, 1620–1625.CrossRefGoogle Scholar
BEERS, R. F. & SIZER, I. W. (1952). A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. Journal of Biological Chemistry 195, 133–140.Google Scholar
BRAGA, L. L., NINOMIYA, H. & McCOY, J. J. (1992). Inhibition of the complement membrane attack complex by the galactose-specific adhesion of Entamoeba histolytica. Journal of Clinical Investigation 90, 1131–1137.CrossRefGoogle Scholar
BROWN, C. G. (1995). Nitric oxide regulates mitochondrial respiration and cell function by inhibiting cytochrome oxidase. FEBS Letters 369, 136–139.CrossRefGoogle Scholar
BURCHARD, G. D., PRANGE, G. & MIRELMAN, D. ( 1992). Inteaction between trophozoites of Entamoeba histolytica and human intestinal cell line HT-29 in the presence or absence of leukocytes. Parasitology Research 78, 140–145.Google Scholar
CARRERAS, M. C., PERGAMENT, G. A., GATZ, S. D., PODEROSO, J. J. & BOVERIS, A. (1994). Kinetics of nitric oxide and H2O2 production and formation of peroxynitrite during the repiratory burst of human neutrophils. FEBS Letters 341, 65–68.CrossRefGoogle Scholar
CARRERO, J. C. & LACLETTE, J. P. (1996). Molecular biology of Entamoeba histolytica: a review. Archives of Medical Research 27, 403–412.Google Scholar
CHADEE, K., PETRI, W. A., INNES, D. J. & RAVDIN, J. I. (1987). Rat and human colonic mucins bind to and inhibit adherence lectin of Entamoeba histolytica. Journal of Clinical Investigation 80, 1245–1257.CrossRefGoogle Scholar
CHEUNG, K., ARCHIBALD, A. C. & ROBINSON, M. F. (1984). Luminol-dependent chemiluminescence produced by neutrophils stimulated by immune complexes. Australian Journal of Experimental Biology and Medical Sciences 62, 403–419.CrossRefGoogle Scholar
DAVIES, B. J. (1964). Disc electrophoresis II. Methods and application to human serum proteins. Annuals of the New York Academy of Sciences, USA 121, 4042–427.Google Scholar
FIELD, M. (1981). Secretion of electrolytes and water by mammalian small intestine. In Physiology of the Gastrointestinal Tract (ed. Johnson, L. R. ), pp. 963–982. Raven Press, New York.
FONDACARO, J. D. (1986). Intestinal ion transport and diarrhoeal disease. American Journal of Physiology 250, G1–G8.Google Scholar
FRESHNEY, R. I. (1987). Culture of Animal Cells. A Manual of Basic Techniques, 2nd Edn. John Wiley and Sons Inc, London.
GREEN, L. C., WAGNER, D. A., GLOGOWSKI, J., SKIPPER, P. L., WISHNOK, J. S. & TANNENBAUM, S. R. (1982). Analysis of nitrate, nitrite and [15N] nitrate in biological fluids. Analytical Biochemistry 126, 131–138.CrossRefGoogle Scholar
GRISHAM, M. B., RYAN, E. & VON RITLER, C. (1987). 5-Aminosalicylic acid scavenges hydroxyl radical and inhibits myeloperoxidase activity. Gastroenterology 92, 1416.Google Scholar
HUGHES, M. A., LEE, C. W., HOLM, C. F., GHOSH, S., MILLS, A., LOCKHART, L. A., REED, S. L. & MANN, B. J. (2003). Identification of Entamoeba histolytica thiol-specific antioxidant as a GalNAc lectin-associated protein. Molecular and Biochemical Parasitology 127, 113–120.CrossRefGoogle Scholar
IANTOMASI, T., FAVILLI, F., MARRACCINI, P., MAGALDI, T., BRUNI, P. & VINCENZINI, M. T. (1997). Glutathione transport system in human small intestine epithelial cells. Biochimica et Biophysica Acta 1330, 274–283.CrossRefGoogle Scholar
KITAHORA, T., SUZUKI, K., ASAKURA, H., YOSHIDA, T., SUEMATSU, M., WATANABE, M., AISO, S. & TSUCHIYA, M. (1988). Active oxygen species generated by monocytes and polymorphonuclear cells in Crohn's disease. Digestive Diseases and Sciences 33, 951–955.CrossRefGoogle Scholar
KLEBANOFF, S. J. (1993). Reactive nitrogen intermediates and antimicrobial activity: role of nitrite. Free Radical Biology and Medicine 14, 351–360.CrossRefGoogle Scholar
KONO, Y. ( 1978). Generation of superoxide radical during auto-oxidation of hydroxylamine and an assay for superoxide dismutase. Archives of Biochemistry and Biophysics 186, 189–195.CrossRefGoogle Scholar
LAWRENCE, R. A. & BURKE, R. F. (1976). Glutathione peroxidase activity in selenium deficient rat liver. Biochemical and Biophysical Research Communications 71, 957–958.CrossRefGoogle Scholar
LEIPPE, M. (1997). Amoebapores. Parasitology Today 13, 178–183.CrossRefGoogle Scholar
LEROY, A., BRUYNE, G. D., MAREEL, M., NOKKAEW, C., BAILEY, G. & NELIS, H. (1995). Contact-dependent transfer of the galactose-specific lectin of Entamoeba histolytica to the lateral surface of enterocytes in culture. Infection and Immunity 63, 4253–4260.Google Scholar
MORON, M. S., DEPIERRE, J. W. & MAWNERVIK, B. (1979). Levels of glutathione, glutathione reductase and glutathione-S-transferase activities in rat liver and lung. Biochimica et Biophysica Acta 582, 67–78.CrossRefGoogle Scholar
MULDER, T. P. J., VERSPAGET, H. W., JANSSENS, A. R., DEBRUIN, P. A. F., PENA, A. S. & LAURE, C. B. H. W. (1991). Decrease in two intestinal copper/zinc containing proteins with antioxidant function in inflammatory bowel disease. Gut 32, 1146–1150.CrossRefGoogle Scholar
NAYA, M. J., PEREBOOM, D., ORTEGO, J., ALDO, J. O. & LANES, A. (1997). Superoxide anions produced by inflammatory cells play an important role in the pathogenesis of acid and pepsin induced oesophagitis in rabbits. Gut 40, 175–181.CrossRefGoogle Scholar
NGUYEN, T., BRUNSON, D., CRESPI, C. L., PENMAN, B. W., WISHNOK, J. S. & TANNENBAUM, S. R. (1992). DNA damage and mutation in human cells exposed to nitric oxide in vitro. Proceedings of the National Academy of Sciences, USA 89, 3030–3034.CrossRefGoogle Scholar
PAGLIA, D. E. & VALENTINE, W. N. (1967). Studies on the quantitative and qualitative characterization of red blood cell's glutathione peroxidase. Journal of Laboratory and Clinical Medicine 70, 158–169.Google Scholar
PARKS, D. A. (1989). Oxygen radicals: mediators of gastrointestinal pathophysiology. Gut 30, 293–298.CrossRefGoogle Scholar
PETRI, W. A. Jr., CHAPMAN, M. D., SONDGRASS, T., MANN, B. J., BROMAN, J. & RAVDIN, J. I. (1989). Subunit structure of the galactose and N-acetyl-D-galactosamine inhibitable adherence lectin of E. histolytica. Journal of Biological Chemistry 264, 3007–3012.Google Scholar
PETRI, W. A. & SCHNAAR, R. L. (1995). Identification of adhesins and receptors. Methods in Enzymology 253, 98–104.CrossRefGoogle Scholar
PRAKASH, A., CHAKRABORTI, A., MAHAJAN, R. C. & GANGULY, N. K. (2002). DNA polymorphism in north Indian isolates of Entamoeba histolytica detected by PCR fingerprinting. Parasitology Research 2, 126–129.CrossRefGoogle Scholar
RADOMSKI, M. W., REES, D. D., DUTRA, A. & MONCADA, S. (1992). S-nitroglutathione inhibits platelet activation in vitro and in vivo. British Journal of Pharmacology 107, 745–749.CrossRefGoogle Scholar
RAO, M. C. (1985). Toxins which activate guanylate cyclase: Heat stable enterotoxins. CIBA Foundation Symposium 112, 74–87.CrossRefGoogle Scholar
RASMUSSEN, H., ISALES, C., GANESAN, S., CALLE, R. & ZAWALICH, W. (1992). Ca2+ cyclic AMP interactions in sustained cellular responses. In Interactions among Cell Signaling Systems. Ciba Foundation Symposium164, pp. 98–112. Wiley, Chichester.
RAVDIN, J. I. (1986). Pathogenesis of disease caused by Entamoeba histolytica: studies of adherence, secreted toxins and contact dependent cytolysis. Review of Infectious Diseases 8, 247–258.CrossRefGoogle Scholar
RAVDIN, J. I. (1995). Amebiasis. Clinical Infectious Diseases 20, 1453–1466.CrossRefGoogle Scholar
RIGOTHIER, M. C., COCONNIER, W. H., SERVIN, A. L. & GAYRAL, P. ( 1991). A new in vitro model of Entamoeba histolytica adhesion, using the human colon carcinoma cell line CaCO-2: scanning electron microscopic study. Infection and Immunity 59, 4142–4146.Google Scholar
SEGUIN, R., MANN, B. J., KELLER, K. & CHADEE, K. (1995). Identification of the galactose-adherence lectin epitopes of Entamoeba histolytica that stimulate tumor necrosis factor–production by macrophages. Proceedings of the National Academy of Sciences, USA 92, 12175–12179.CrossRefGoogle Scholar
STADMAN, T. C. (1980). Selenium dependent enzymes. Annual Review of Biochemistry 49, 93–110.CrossRefGoogle Scholar
STUEHR, D. J. & MARLETTA, M. A. (1985). Mammalian nitrite biosynthesis: Mouse macrophages produce nitrite and nitrate in response to Escherichia coli lipopolysaccharide. Proceedings of the National Academy of Sciences, USA 82, 7738–7742.CrossRefGoogle Scholar
VINES, R. R., RAMAKRISHNAN, G., ROGERS, J. B., LOCKHART, L. A., MANN, B. J. & PETRI Jr., W. A. (1998). Regulation of adherence and virulence by the Entamoeba histolytica lectin cytoplasmic domain which contains a β2-integrin motif. Molecular Biology of the Cell 9, 2069–2079.CrossRefGoogle Scholar
YAMAMOTO, N. & DROFFNER, M. L. (1985). Mechanism determining aerobic or anaerobic growth in the facultative anaerobe Salmonella typhimurium. Proceedings of the National Academy of Sciences, USA 82, 2077–2081.CrossRefGoogle Scholar
WALSH, J. A. (1986). Problems in recognition and diagnosis of amoebiasis. Estimates of the global magnitude of morbidity and mortality. Review of Infectious Diseases 8, 228–238.Google Scholar