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Binding and the effect of the red kidney bean lectin, phytohaemagglutinin, in the gastrointestinal tract of suckling rats

Published online by Cambridge University Press:  08 March 2007

Ann Linderoth*
Affiliation:
Department of Cell and Organism Biology, Lund University, Helgonavägen 3B, SE-223 62 Lund, Sweden
Olena Prykhod'ko
Affiliation:
Department of Cell and Organism Biology, Lund University, Helgonavägen 3B, SE-223 62 Lund, Sweden
Bo Ahrén
Affiliation:
Department of MedicineUniversity Hospital, Lund University, Lund, Sweden
Frida Fåk
Affiliation:
Department of Cell and Organism Biology, Lund University, Helgonavägen 3B, SE-223 62 Lund, Sweden
Stefan G. Pierzynowski
Affiliation:
Department of Cell and Organism Biology, Lund University, Helgonavägen 3B, SE-223 62 Lund, Sweden
Björn R. Weström
Affiliation:
Department of Cell and Organism Biology, Lund University, Helgonavägen 3B, SE-223 62 Lund, Sweden
*
*Corresponding author: Dr Ann Linderoth, fax +46 46 222 45 39, email Ann.Linderoth@cob.lu.se
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Abstract

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Enteral exposure of suckling rats to phytohaemagglutinin (PHA) has been shown to induce growth and precocious functional maturation of the gastrointestinal tract. The aim of the present study was to explore the mechanism of this action. Suckling rats, 14d old, were fed a single dose of PHA (0·05mg/g body weight) or saline. The binding of PHA to the gut epithelium and its effect on the morphology and functional properties of the gut and pancreas were studied up to 3d after treatment. Initially, at 1–24h, the PHA bound along the gut mucosal lining, resulting in disturbed gut morphology with villi shortening and rapid decreases in disaccharidase activities and macromolecular absorption capacity. During a later phase, between 1 and 3d, the PHA binding had declined, and an uptake by enterocytes was observed. An increase in crypt cell proliferation and gut growth became evident during this period, together with a functional maturation, as indicated by increases in disaccharidase (maltase and sucrase) activities and the low macromolecular absorption capacity. Pancreas growth also increased, as did its content of digestive enzymes. We conclude that enteral exposure to PHA in suckling rats temporarily causes mucosal disarrangement and functional impediment of the gut, which may be explained by binding to and disruption of the gut mucosa and a two-fold increase in the plasma corticosterone concentration. These findings may lead to a better understanding of the role of diet in gastrointestinal maturation and may constitute a basis for the treatment of mammals having an immature gut.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2006

References

Banwell, JG, Howard, R, Kabir, I, Adrian, TE, Diamond, RH & Abramowsky, CSmall intestinal growth caused by feeding red kidney bean phytohemagglutinin lectin to rats. Gastroenterology (1993), 104, 16691677.CrossRefGoogle ScholarPubMed
Bardocz, S, Grant, G & Pusztai, AThe effect of phytohaemagglutinin at different dietary concentrations on the growth, body composition and plasma insulin of the rat. Br J Nutr (1996) 76 613626CrossRefGoogle ScholarPubMed
Biol-N'garagba, MC, Niepceron, E, Mathian, B & Louisot, PGlucocorticoid-induced maturation of glycoprotein galactosylation and fucosylation processes in the rat small intestine. J Steroid Biochem Mol Biol (2003) 84 411422.CrossRefGoogle ScholarPubMed
Bravo, R& Macdonald-Bravo, HExistence of two populations of cyclin/proliferating cell nuclear antigen during the cell cycle:association with DNA replication sites. J Cell Biol (1987) 105, 15491554.CrossRefGoogle ScholarPubMed
Cummings, RD& Kornfeld, SCharacterization of the structural determinants required for the high affinity interaction of asparagine- linked oligosaccharides with immobilized Phaseolus vulgaris leukoagglutinating and erythroagglutinating lectins. J Biol Chem (1982) 257, 1123011234.CrossRefGoogle ScholarPubMed
Dahlqvist, AAssay of intestinal disaccharidases. Scand J Clin Lab Invest (1984). 44, 169172.CrossRefGoogle ScholarPubMed
Fritz, H, Hartwich, G& Werle, EOn protease inhibitors.I. Isolation and characterization of trypsin inhibitors from dog pancreas tissue and pancreas secretion. Hoppe Seylers Z Physiol Chem (1966) 345, 150167.CrossRefGoogle Scholar
Grant, G, Alonso, R, Edwards, JE & Murray, SDietary soya beans and kidney beans stimulate secretion of cholecystokinin and pancreatic digestive enzymes in 400-day-old Hooded-Listerrats but only soya beans induce growth of the pancreas. Pancreas. (2000) 20, 305312.CrossRefGoogle ScholarPubMed
Grant, G, Edwards, JE, Ewan, EC,Murray, S, Atkinson, T,Farningham, DA & Pusztai, ASecretion of pancreatic digestive enzymes induced in rats by first-time oral exposure to kidney bean E2L2 lectin is mediated only in part by cholecystokinin (CCK). Pancreas (1999) 19, 382389.CrossRefGoogle ScholarPubMed
Grant, G, Henderson, LT, Edwards, JE,Ewan, EC, Bardocz, S & Pusztai, AKidney bean and soybean lectins cause enzyme secretion by pancreatic acini in vitro. Life Sci (1997) 60, 15891595.CrossRefGoogle ScholarPubMed
Green, ED & Baenziger, JUOligosaccharide specificities of Phaseolus vulgaris leukoagglutinating and erythroagglutinating phytohemagglutinins. Interactions with N-glycanase-released oligosaccharides J Biol Chem (1987), 262. 1201812029.CrossRefGoogle ScholarPubMed
Hagen, SJ, Trier, JS & Dambrauskas, RExposure of the rat small intestine to raw kidney beans results in reorganization of absorptive cell microvilli. Gastroenterology (1994) 106 7384.CrossRefGoogle ScholarPubMed
Henning, SJFunctional development of the gastrointestinal tract. In Physiology of the Gastrointestinal Tract, 2nd ed., 285300 [LR, Johnson, editor]. New York: Raven Press. (1987)Google Scholar
Henning, SJ, Rubin, DC & Shulman, RJOntogeny of the intestinal mucosa. In Physiology of the Gastrointestinal Tract, 3rd ed., 571610 [LR, Johnson, editor]. New York: Raven Press. (1994)Google Scholar
Herzig, KH, Bardocz, S, Grant, G,Nustede, R,Folsch, UR & Pusztai, ARed kidney bean lectin is a potent cholecystokinin releasing stimulus in the rat inducing pancreatic growth. Gut (1997) 41, 333338.CrossRefGoogle ScholarPubMed
King, TP, Pusztai, A & Clarke, EMWImmunocystochemical localization of ingested kidney bean (Phaseolus vulgaris) lectins in rat gut. Histochem J (1980) 12, 201208.CrossRefGoogle Scholar
Kinouchi, T, Koizumi, K, Kuwata, T & Yajima, TCrucial role of milk-borne insulin in the development of pancreatic amylase at the onset of weaning in rats.. Am J Physiol (1998) 275, R1958R1967.Google ScholarPubMed
Kinouchi, T, Koizumi, K, Kuwata, T & Yajima, TMilk-borne insulin with trypsin inhibitor in milk induces pancreatic amylase development at the onset of weaning in rats. J Pediatr Gastroenterol Nutr (2000) 30, 515521.Google ScholarPubMed
Laurell, CBElectroimmunoassay.. Scand J Clin Lab Invest Suppl (1972) 124, 2137.CrossRefGoogle Scholar
Lee, PC & Lebenthal, EEarly weanling and precocious development of small intestine in rats:genetic, dietary or hormonal control. Pediatr Res (1983) 17, 645650.CrossRefGoogle ScholarPubMed
Linderoth, A, Biernat, M, Prykhodko, O,Kornilovska, I,Pusztai, A,Pierzynowski, SG & Weström, BInduced growth and maturation of the gastrointestinal tract after Phaseolus vulgaris lectin exposure in suckling rats. J Pediatr Gastroenterol Nutr (2005) 41, 195203.CrossRefGoogle ScholarPubMed
Lowry, OH, Rosebrough, NJ, Farr, AL & Randall, RJProtein measurements with folin phenol reagent J Biol Chem (1951) 193 265275.CrossRefGoogle ScholarPubMed
Martin, MG, Wu, SV & Walsh, JHHormonal control of intestinal Fc receptor gene expression and immunoglobulin transport in suckling rats. J Clin Invest (1993) 91 28442849.CrossRefGoogle ScholarPubMed
Nanthakumar, NN & Henning, SJDistinguishing normal and glucocorticoid-induced maturation of intestine using bromodeoxyuridine. Am J Physiol (1995) 268, G139G145.Google ScholarPubMed
Otte, JM, Chen, C, Brunke, G,Kiehne, K, Schmitz, F, Folsch, UR & Herzig, KHMechanisms of lectin (phytohemagglutinin)- induced growth in small intestinal epithelial cells Digestion (2001) 64, 169178.CrossRefGoogle ScholarPubMed
Pacha, JDevelopment of intestinal transport function in mammals. Physiol Rev (2000) 80, 16331667.CrossRefGoogle ScholarPubMed
Pierzynowski, SG, Weström, BR, Svendsen, J & Karlsson, BWDevelopment of exocrine pancreas function in chronically cannulated pigs during 1—13 weeks of postnatal life. J Pediatr Gastroenterol Nutr (1990) 10 206212.Google ScholarPubMed
Polk, BD & Barnard, JA, Hormones and growth factors in intestinal development. In Development of the Gastrointestinal Tract, 3756IA, Sanderson and WA, Walker, editors. Hanilton, Ontano, Canada: B.C. Decker Inc. (2000)Google Scholar
Puccio, F, Chariot, J & Lehy, TInfluence of hydrocortisone on the development of pancreas in suckling rats.Ultrastructural morphometric and biochemical studies. Biol Neonate (1988) 54 3544.CrossRefGoogle ScholarPubMed
Pusztai, ATransport of proteins through the membranes of the adult gastrointestinal tract — a potential for drug delivery?" Adv Drug Deliv Rev (1989) 3. 215228.CrossRefGoogle Scholar
Pusztai, ADietary lectins are metabolic signals for the gut and modulate immune and hormone functions. Eur J Clin Nutr (1993) 47, 691699.Google ScholarPubMed
Pusztai, APhytohaemagglutinin stimulates pancreatic enzyme secretion in rats by a combination of cholecystokinin- and noncholecystokinin- linked pathways.InBiology of the Pancreas in Growing Animals, 273286 [SG, Pierzynowski and R, Zabielski, editors]. Amsterdam: Elsevier Science BV. (1999)Google Scholar
Pusztai, A & Watt, WBIsolectins ofPhaseolus vulgaris. A comprehensive study of fractionation. Biochim Biophys Acta (1974) 365 5771.CrossRefGoogle Scholar
Pusztai, A, Ewen, SW, Grant, G, Peumans, WJ, vanDamme, EJ,Rubio, L & Bardocz, SRelationship between survival and bindingof plant lectins during small intestinal passage and their effectiveness as growth factors. Digestion (1990) 46, 308316.CrossRefGoogle Scholar
Pusztai, A,Ewen, SWB, Carvalho, FFU, G., G, Baintner, K & Bardocz, SDietary lectins affect the hormone balance of the body and modulate its general metoblosim. In Gastrointestinal Tract and Endocrine system, 457463 [MV, Singer, Z, Riegler and G, Rohr editors] Dordrecht, The Netterlands: Kluwer Acodemic Publishers. (1995)Google Scholar
Sheen-Chen, SM, Ho, HT, Chen, WJ & Eng, HLObstructive jaundice alters proliferating cell nuclear antigen expression in rat small intestine. World J Surg (2003) 27, 11611164.CrossRefGoogle ScholarPubMed
Telemo, E, Westrom, BR, Ekstrom, G & Karlsson, BWIntestinal macromolecular transmission in the young rat: influence of protease inhibitors during development. Biol Neonate (1987) 52 141148.CrossRefGoogle Scholar
Weinman, MD, Allan, CH, Trier, JS & Hagen, SJRepair of microvilli in the rat small intestine after damage with lectins contained in the red kidney bean. Gastroenterology (1989) 97, 11931204.CrossRefGoogle ScholarPubMed
Yeh, KY, Yeh, M & Holt, PRDifferential effects of thyroxine and cortisone on jejunal sucrase expression in suckling rats. Am J Physiol. (1989) 256, G604G612.Google ScholarPubMed
Young, GPTaranto, TMJonas, HACox, AJHogg, A & Werther, GAnsulin-like growth factors and the developing and mature rat small intestine:I receptors and biological actions Digestion (1990) 46. 240252.CrossRefGoogle Scholar