Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-25T14:27:14.042Z Has data issue: false hasContentIssue false
  • English
  • Français

Mode of action of a potentially important excretory–secretory product from Giardia lamblia in mice enterocytes

Published online by Cambridge University Press:  03 March 2005

J. SHANT ,
S. GHOSH ,
S. BHATTACHARYYA ,
N. K. GANGULY  and
S. MAJUMDAR
J. SHANT
Affiliation:
Department of Experimental Medicine and Biotechnology, Post-graduate Institute of Medical Education and Research, Chandigarh 160012, India Present address: Department of Neurosurgery, University of Mississippi Medical Center, Jackson, MS 39216, USA.
S. GHOSH
Affiliation:
Department of Experimental Medicine and Biotechnology, Post-graduate Institute of Medical Education and Research, Chandigarh 160012, India
S. BHATTACHARYYA
Affiliation:
Department of Experimental Medicine and Biotechnology, Post-graduate Institute of Medical Education and Research, Chandigarh 160012, India
N. K. GANGULY
Affiliation:
Department of Experimental Medicine and Biotechnology, Post-graduate Institute of Medical Education and Research, Chandigarh 160012, India
S. MAJUMDAR
Affiliation:
Department of Experimental Medicine and Biotechnology, Post-graduate Institute of Medical Education and Research, Chandigarh 160012, India
Get access Rights & Permissions [Opens in a new window]

Abstract

Giardia, a common enteric protozoan parasite is a well-recognized cause of diarrhoeal illness. The detailed mechanism of diarrhoea due to this infection is not well understood. A 58 kDa enterotoxin (ESP) was purified from the excretory–secretory product of the parasite. The present study was designed to investigate the mode of action of this enterotoxin of G. lamblia in mice enterocytes. An increase in cyclic adenosine monophosphate level, as well as intracellular Ca2+ concentration, was observed in the ESP-triggered enterocytes. The levels of phospholipase Cγ1 and inositol triphosphate were found to be upregulated. The activity of protein kinase C (PKC) in the enterocytes was also enhanced following stimulation with the ESP. An increase in the level of reactive oxygen species in ESP-stimulated cells correlated well with the decline in the activity of antioxidant enzymes (superoxide dismutase and catalase). The significantly high levels of nitrite and citrulline indicated the generation of reactive nitrogen intermediates in the ESP-triggered enterocytes. Thus, ESP could induce cross-talk among the different signal transduction pathways in the enterocytes, which could together bring about a common secretory response.

Keywords

Giardia lambliaexcretory-secretory product (ESP)phospholipase Cγ1protein kinase Creactive oxygen specieselectrolyte imbalance
Type
Research Article
Information
Parasitology , Volume 131 , Issue 1 , July 2005 , pp. 57 - 69
Copyright
© 2005 Cambridge University Press

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

ADAM, R. D. ( 2001). Biology of Giardia lamblia. Clinical Microbiology Reviews 14, 447–475.CrossRefGoogle Scholar
BECKMAN, J. S., BECKMAN, T. W., CHEN, 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, 1620–1624.CrossRefGoogle Scholar
BEERS, R. F. & SIZER, J. W. ( 1984). A spectophotometric method for measuring the breakdown of hydrogen peroxide by catalase. Journal of Biological Chemistry 195, 133–140.Google Scholar
BHATNAGAR, R., AHUJA, N., GOILA, R., BATRA, S., WAHEED, S. M. & GUPTA, P. ( 1999). Activation of phospholipase C and protein kinase C is required for expression of anthrax lethal toxin cytotoxicity in J774A.1 cells. Cell Signal 11, 111–116.CrossRefGoogle Scholar
BOYDE, T. R. & RAHMATULLAH, M. ( 1980). Optimization of conditions for the colorimetric determination of citrulline, using diacetyl monoxime. Analytical Biochemistry 107, 424–431.CrossRefGoogle Scholar
BURET, A., GALL, D. G. & OLSON, M. E. ( 1990). Effects of murine giardiasis on growth, intestinal morphology, and disaccharidase activity. Journal of Parasitology 76, 403–409.CrossRefGoogle Scholar
BURET, A., HARDIN, J. A., OLSON, M. E. & GALL, D. G. ( 1992). Pathophysiology of small intestinal malabsorption in gerbils infected with Giardia lamblia. Gastroenterology 103, 506–513.CrossRefGoogle Scholar
CARTWRIGHT, C. A., McROBERTS, J. A., MANDEL, K. G. & DHARMSATHAPHORN, K. ( 1985). Synergistic action of cyclic adenosine monophosphate- and calcium-mediated chloride secretion in a colonic epithelial cell line. Journal of Clinical Investigation 76, 1837–1842.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 Science 62, 403–419.CrossRefGoogle Scholar
DIAMOND, L. S., HARLOW, D. R. & 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
DONOWITZ, M., COHEN, M. E., GOULD, M. & SHARP, G. W. ( 1989). Elevated intracellular Ca2+ acts through protein kinase C to regulate rabbit ileal NaCl absorption. Evidence for sequential control by Ca2+/calmodulin and protein kinase C. Journal of Clinical Investigation 83, 1953–1962.Google Scholar
DONOWITZ, M. & WELSH, M. J. ( 1987). Regulation of Mammalian Small Intestinal Electrolyte Secretion. Raven Press, New York.
ECKMANN, L. & GILLIN, F. D. ( 2001). Microbes and microbial toxins: paradigms for microbial-mucosal interactions I. Pathophysiological aspects of enteric infections with the lumen-dwelling protozoan pathogen Giardia lamblia. American Journal of Physiology, Gastrointestinal and Liver Physiology 280, G1–G6.Google Scholar
FARTHING, M. J. ( 1997). The molecular pathogenesis of giardiasis. Journal of Pediatric Gastroenterology and Nutrition 24, 79–88.CrossRefGoogle Scholar
FORSYTHE, R. M., XU, D. Z., LU, Q. & DEITCH, E. A. ( 2002). Lipopolysaccharide-induced enterocyte-derived nitric oxide induces intestinal monolayer permeability in an autocrine fashion. Shock 17, 180–184.CrossRefGoogle Scholar
GANGULY, U., CHAUDHURY, A. G., BASU, A. & SEN, P. C. ( 2001). STa-induced translocation of protein kinase C from cytosol to membrane in rat enterocytes. FEMS Microbiology Letters 204, 65–69.CrossRefGoogle Scholar
GOROWARA, S., SAPRU, S. & GANGULY, N. K. ( 1998). Role of intracellular second messengers and reactive oxygen species in the pathophysiology of V. cholera O139 treated rabbit ileum. Biochimica et Biophysica Acta 1407, 21–30.CrossRefGoogle Scholar
GOROWARA, S., GANGULY, N. K., MAHAJAN, R. C. & WALIA, B. N. ( 1992). Study on the mechanism of Giardia lamblia induced diarrhoea in mice. Biochimica et Biophysica Acta 1138, 122–126.CrossRefGoogle Scholar
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
HARDCASTLE, J., HARDCASTLE, P. T. & NOBLE, J. M. ( 1984). The involvement of calcium in the intestinal response to secretagogues in the rat. Journal of Physiology 355, 465–478.CrossRefGoogle Scholar
HOQUE, K. M., PAL, A., NAIR, G. B., CHATTOPADHYAY, S. & CHAKRABARTI, M. K. ( 2001). Evidence of calcium influx across the plasma membrane depends upon the initial rise of cytosolic calcium with activation of IP(3) in rat enterocytes by heat-stable enterotoxin of Vibrio cholerae non-O1. FEMS Microbiology Letters 196, 45–50.CrossRefGoogle Scholar
JIMENEZ, J. C., FONTAINE, J., GRZYCH, J. M., DEI-CAS, E. & CAPRON, M. ( 2004). Systemic and mucosal responses to oral administration of excretory and secretory antigens from Giardia intestinalis. Clinical and Diagnostic Laboratory Immunology 11, 152–160.CrossRefGoogle Scholar
KATELARIS, P. H., SIDHU, G. S., OAKENFULL, D. G. & NGU, M. C. ( 1988). Pathogenesis of diarrhoea caused by Giardia lamblia: evidence for an exotoxin. Journal of Gastroenterology and Hepatology 3 (Suppl. I), A4(abstract).Google Scholar
KAUR, T., SINGH, S., VERMA, M. & GANGULY, N. K. ( 1997). Calcium and protein kinase C play a significant role in response to Shigella toxin in rabbit ileum both in vivo and in vitro. Biochimica et Biophysica Acta 1361, 75–91.CrossRefGoogle Scholar
KAWAMOTO, S. & HIDAKA, H. ( 1984). 1-(5-Isoquinolinesulfonyl)-2-methylpiperazine (H-7) is a selective inhibitor of protein kinase C in rabbit platelets. Biochemical and Biophysical Research Communications 125, 258–264.CrossRefGoogle Scholar
KHURANA, S., GANGULY, N. K., KHULLAR, M., PANIGRAHI, D. & WALIA, B. N. ( 1991). Studies on the mechanism of Salmonella typhimurium enterotoxin-induced diarrhoea. Biochimica et Biophysica Acta 1097, 171–176.CrossRefGoogle Scholar
KONO, Y. ( 1978). Generation of superoxide radical during autoxidation of hydroxylamine and an assay for superoxide dismutase. Archives of Biochemistry and Biophysics 186, 189–195.CrossRefGoogle Scholar
McNEIL, K. S., KNOX, D. P. & PROUDFOOT, L. ( 2002). Anti-inflammatory responses and oxidative stress in Nippostrongylus brasiliensis-induced pulmonary inflammation. Parasite Immunology 24, 15–22.CrossRefGoogle Scholar
MEHTA, A., SINGH, S. & GANGULY, N. K. ( 1999). Effect of Salmonella typhimurium enterotoxin (S-LT) on lipid peroxidation and cell viability levels of isolated rat enterocytes. Molecular and Cellular Biochemistry 196, 175–181.CrossRefGoogle Scholar
MINKE, W. E., ROACH, C., HOL, W. G. & VERLINDE, C. L. ( 1999). Structure-based exploration of the ganglioside GM1 binding sites of Escherichia coli heat-labile enterotoxin and cholera toxin for the discovery of receptor antagonists. Biochemistry 38, 5684–5692.CrossRefGoogle Scholar
NASH, T. E., GILLIN, F. D. & SMITH, P. D. ( 1983). Excretory-secretory products of Giardia lamblia. Journal of Immunology 131, 2004–2010.Google Scholar
NAYA, M. J., PEREBOOM, D., ORTEGO, J., ALDA, J. O. & LANAS, A. ( 1997). Superoxide anions produced by inflammatory cells play an important part in the pathogenesis of acid and pepsin induced oesophagitis in rabbits. Gut 40, 175–181.CrossRefGoogle Scholar
OLDHAM, K. G. ( 1990). Polyphosphoinositide turnover. In Receptor Effector Coupling: A Practical Approach (ed. Hulme, E. C.), pp. 99–102. Oxford University Press, Oxford.
OLSON, M. E., MORCK, D. W. & CERI, H. ( 1996). The efficacy of a Giardia lamblia vaccine in kittens. Canadian Journal of Veterinary Research 60, 249–256.Google Scholar
PACE, J. L. & GALAN, J. E. ( 1994). Measurement of free intracellular calcium levels in epithelial cells as consequence of bacterial invasion. Methods in Enzymology 236, 482–490.CrossRefGoogle Scholar
PAPANASTASIOU, P., BRUDERER, T., LI, Y., BOMMELI, C. & KOHLER, P. ( 1997). Primary structure and biochemical properties of a variant-specific surface protein of Giardia. Molecular and Biochemical Parasitology 86, 13–27.CrossRefGoogle Scholar
PETERSON, J. W., MOLINA, N. C., HOUSTON, C. W. & FADER, R. C. ( 1983). Elevated cAMP in intestinal epithelial cells during experimental cholera and salmonellosis. Toxicon 21, 761–775.CrossRefGoogle Scholar
PINKUS, L. M. ( 1981). Separation and use of enterocytes. Methods in Enzymology 77, 154–162.CrossRefGoogle Scholar
ROUT, W. R., FORMAL, S. B., DAMMIN, G. J. & GIANNELLA, R. A. ( 1974). Pathophysiology of Salmonella diarrhea in the Rhesus monkey: intestinal transport, morphological and bacteriological studies. Gastroenterology 67, 59–70.Google Scholar
RUSCHKOWSKI, S., ROSENSHINE, I. & FINLAY, B. B. ( 1992). Salmonella typhimurium induces an inositol phosphate flux in infected epithelial cells. FEMS Microbiology Letters 74, 121–126.CrossRefGoogle Scholar
SACHINIDIS, A., SEUL, C., GOUNI-BERTHOLD, I., SEEWALD, S., KO, Y., VETTER, H., FINGERLE, J. & HOPPE, J. ( 2000). Cholera toxin treatment of vascular smooth muscle cells decreases smooth muscle alpha-actin content and abolishes the platelet-derived growth factor-BB-stimulated DNA synthesis. British Journal of Pharmacology 130, 1561–1570.CrossRefGoogle Scholar
SEARS, C. L. & KAPER, J. B. ( 1996). Enteric bacterial toxins: mechanisms of action and linkage to intestinal secretion. Microbiological Reviews 60, 167–215.Google Scholar
SHANT, J., GHOSH, S., BHATTACHARYYA, S., GANGULY, N. K. & MAJUMDAR, S. ( 2004). The alteration in signal transduction parameters induced by excretory-secretory product from G. lamblia. Parasitology 129, 421–430.CrossRefGoogle Scholar
SHANT, J., BHATTACHARYYA, S., GHOSH, S., GANGULY, N. K. & MAJUMDAR, S. ( 2002). A potentially important excretory-secretory product of Giardia lamblia. Experimental Parasitology 102, 178–186.CrossRefGoogle Scholar
STUEHR, D. J. & MARLETTA, M. A. ( 1985). Mammalian nitrate 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
SUGDEN, D., VANECEK, J., KLEIN, D. C., THOMAS, T. P. & ANDERSON, W. B. ( 1985). Activation of protein kinase C potentiates isoprenaline-induced cyclic AMP accumulation in rat pinealocytes. Nature, London 314, 359–361.CrossRefGoogle Scholar
SVOBODA, P. & NOVOTNY, J. ( 2002). Hormone-induced subcellular redistribution of trimeric G proteins. Cellular and Molecular Life Sciences 59, 501–512.CrossRefGoogle Scholar
TABOURET, G., VOULDOUKIS, I., DURANTON, C., PREVOT, F., BERGEAUD, J. P., DORCHIES, P., MAZIER, D. & JACQUIET, P. ( 2001). Oestrus ovis (Diptera: Oestridae): effects of larval excretory/secretory products on nitric oxide production by murine RAW 264·7 macrophages. Parasite Immunology 23, 111–119.CrossRefGoogle Scholar
THOMPSON, R. C., HOPKINS, R. M. & HOMAN, W. L. ( 2000). Nomenclature and genetic groupings of Giardia infecting mammals. Parasitology Today 16, 210–213.CrossRefGoogle Scholar
TOYODA, S., LEE, P. C. & LEBENTHAL, E. ( 1985). Physiological factors controlling release of enterokinase from rat enterocytes. Digestive Disease Science 30, 1174–1180.CrossRefGoogle Scholar
TURVILL, J. L., MOURAD, F. H. & FARTHING, M. J. ( 1999). Proabsorptive and prosecretory roles for nitric oxide in cholera toxin induced secretion. Gut 44, 33–39.CrossRefGoogle Scholar
VIGNOLI, A. L., SRIVASTAVA, R. C., STAMMATI, A., TURCO, L., TANORI, M. & ZUCCO, F. ( 2001). Nitric oxide production in Caco-2 cells exposed to different inducers, inhibitors and natural toxins. Toxicology In Vitro 15, 289–295.CrossRefGoogle Scholar