Binding and the effect of the red kidney bean lectin, phytohaemagglutinin, in the gastrointestinal tract of suckling rats | British Journal of Nutrition | Cambridge Core (original) (raw)

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

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.

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, 1669–1677.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) 76 613–626CrossRefGoogle 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) 84 411– 422.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, 1549 –1554.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, 11230– 11234.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, 150– 167.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, 305–312.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, 382–389.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, 1589–1595.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. 12018–12029.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 73–84.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., 571–610 [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, 333–338.CrossRefGoogle ScholarPubMed

King, TP, Pusztai, A & Clarke, EMWImmunocystochemical localization of ingested kidney bean (Phaseolus vulgaris) lectins in rat gut. Histochem J (1980) 12, 201–208.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, R1958–R1967.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, 515–521.Google ScholarPubMed

Lee, PC & Lebenthal, EEarly weanling and precocious development of small intestine in rats:genetic, dietary or hormonal control. Pediatr Res (1983) 17, 645–650.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, 195–203.CrossRefGoogle ScholarPubMed

Lowry, OH, Rosebrough, NJ, Farr, AL & Randall, RJProtein measurements with folin phenol reagent J Biol Chem (1951) 193 265–275.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 2844–2849.CrossRefGoogle ScholarPubMed

Nanthakumar, NN & Henning, SJDistinguishing normal and glucocorticoid-induced maturation of intestine using bromodeoxyuridine. Am J Physiol (1995) 268, G139–G145.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, 169–178.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) 10 206–212.Google ScholarPubMed

Polk, BD & Barnard, JA, Hormones and growth factors in intestinal development. In Development of the Gastrointestinal Tract, 37–56IA, 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 35–44.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. 215–228.CrossRefGoogle Scholar

Pusztai, ADietary lectins are metabolic signals for the gut and modulate immune and hormone functions. Eur J Clin Nutr (1993) 47, 691–699.Google ScholarPubMed

Pusztai, APhytohaemagglutinin stimulates pancreatic enzyme secretion in rats by a combination of cholecystokinin- and noncholecystokinin- linked pathways.In_Biology of the Pancreas in Growing Animals_, 273–286 [SG, Pierzynowski and R, Zabielski, editors]. Amsterdam: Elsevier Science BV. (1999)Google Scholar

Pusztai, A & Watt, WBIsolectins of_Phaseolus vulgaris._ A comprehensive study of fractionation. Biochim Biophys Acta (1974) 365 57–71.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, 308–316.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, 457–463 [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, 1161–1164.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) 52 141–148.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, 1193–1204.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, G604–G612.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. 240–252.CrossRefGoogle Scholar