BIgG bovine IgG; FD fluorescein isothiocyanate-dextran; HSA human serum albumin; Lac:Man lactulose:mannitol ratio; PAR-2 protease-activated receptor-2; PHA phytohaemagglutinin; SI small intestine; b.wt body weight; Gut; Permeability; Precocious maturation; Small intestine
Abstract :
[en] Gut maturation naturally accelerates at weaning in altricial mammalian species, such as the rat. Mimicking this, gut development can also be induced precociously, 3-4 d earlier than it would occur naturally, by enteral exposure to phytohaemagglutinin (PHA), or various proteases. We investigated the early effects of gut provocation on intestinal barrier and pancreatic functions, to get a better understanding of the mechanisms that initiate gut maturation. The effects of oral administration of protease (trypsin) or PHA to 14-d-old suckling rats were studied during 24 h in comparison with water-fed controls. Intestinal in vivo permeability was assessed by oral administration of different-sized marker molecules and measuring their passage into the blood or urine 3 h later. A period of 24 h following oral administration, both PHA and protease provocation stimulated small intestinal (SI) growth and pancreatic secretion, as indicated by decreased pancreatic trypsin and increased luminal enzyme content. Within 1 h of oral administration, both treatments prevented the absorption of macromolecules to blood that was observed in controls. PHA treatment hindered the passage of fluorescein isothiocyanate-dextran (FD) 4 to blood, whereas protease treatment temporarily increased plasma levels of FD4, and the urine lactulose:mannitol ratio, indicating increased intestinal leakiness. Following protease treatment, fluorescence microscopy showed decreased vesicular uptake of FD70 in the proximal SI and increased epithelial fluorescence in the distal SI. In conclusion, PHA and protease differed in their early effects on the intestinal barrier; both exerted a blocking effect on epithelial endocytosis, whereas protease treatment alone temporarily increased epithelial leakiness, which seemed to be confined to the distal SI.
Disciplines :
Gastroenterology & hepatology
Author, co-author :
Arevalo Sureda, Ester ; Université de Liège - ULiège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Ingénierie des productions animales et nutrition
Prykhodko, Olena
Westrom, Bjorn
Language :
English
Title :
Early effects on the intestinal barrier and pancreatic function after enteral stimulation with protease or kidney bean lectin in neonatal rats.
Cummins AG, Steele TW, Labrooy JT, et al. (1988) Maturation of the rat small-intestine at weaning-changes in epithelialcell kinetics, bacterial-flora, and mucosal immune activity. Gut 29, 1672-1679.
Walthall K, Cappon GD, Hurtt ME, et al. (2005) Postnatal development of the gastrointestinal system: A species comparison. Birth Def Res 74, 132-156.
Rakhimov KR, Karimov OR, Kurbanov AS, et al. (2002) Rearrangement of spectrum of digestive proteases in postnatal ontogenesis of rats. J Evol Biochem Physiol 38, 184-188.
Pacha J (2000) Development of intestinal transport function in mammals. Physiol Rev 80, 1633-1667.
Arevalo Sureda E, Westrom B, Pierzynowski SG, et al. (2016) Maturation of the intestinal epithelial barrier in neonatal rats coincides with decreased FcRn expression, replacement of vacuolated enterocytes and changed blimp-1 expression. PLOS ONE 11, e0164775.
Menard S, Cerf-Bensussan N&Heyman M (2010) Multiple facets of intestinal permeability and epithelial handling of dietary antigens. Mucosal Immunol 3, 247-259.
Lee PC&Lebenthal E (1983) Early weanling and precocious development of small intestine in rats: genetic, dietary or hormonal control. Pediatr Res 17, 645-650.
Martin MG, Wu SV&Walsh JH (1993) Hormonal control of intestinal Fc receptor gene expression and immunoglobulin transport in suckling rats. J Clin Invest 91, 2844-2849.
Dufour C, Dandrifosse G, Forget P, et al. (1988) Spermine and spermidine induce intestinal maturation in the rat. Gastroenterology 95, 112-116.
Linderoth A, Biernat M, Prykhodko O, et al. (2005) Induced growth and maturation of the gastrointestinal tract after Phaseolus vulgaris lectin exposure in suckling rats. J Pediatr Gastroenterol Nutr 41, 195-203.
Prykhodko O, Pierzynowski SG, Nikpey E, et al. (2015) Pancreatic and pancreatic-like microbial proteases accelerate gut maturation in neonatal rats. PLOS ONE 10, e0116947.
Linderoth A, Prykhod'ko O, Ahren B, et al. (2006) Binding and the effect of the red kidney bean lectin, phytohaemagglutinin, in the gastrointestinal tract of suckling rats. Br J Nutr 95, 105-115.
Prykhod'ko O, Fed'kiv O, Linderoth A, et al. (2009) Precocious gut maturation and immune cell expansion by single dose feeding the lectin phytohaemagglutinin to suckling rats. Br J Nutr 101, 735-742.
Pusztai A&Watt WB (1974) Isolectins of Phaseolus vulgaris. A comprehensive study of fractionation. Biochim Biophys Acta 365, 57-71.
Sureda EA, Gidlund C, Weström B, et al. (2017) Induction of precocious intestinal maturation in T-cell deficient athymic neonatal rats. World J Gastroentero 23, 7531-7540.
Mancini G, Carbonara AO&Heremans JF (1965) Immunochemical quantitation of antigens by single radial immunodiffusion. Immunochemistry 2, 235-254.
Thymann T, Burrin DG, Tappenden KA, et al. (2006) Formulafeeding reduces lactose digestive capacity in neonatal pigs. Br J Nutr 95, 1075-1081.
Pierzynowski SG, Westrom BR, Svendsen J, et al. (1990) Development of exocrine pancreas function in chronically cannulated pigs during 1-13 weeks of postnatal life. J Pediatr Gastroenterol Nutr 10, 206-212.
Fritz H, Hartwich G&Werle E (1966) [On protease inhibitors. I. Isolation and characterization of trypsin inhibitors from dog pancreas tissue and pancreas scretion]. Hoppe Seylers Z Physiol Chem 345, 150-167.
Lowry OH, Rosebrough NJ, Farr AL, et al. (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193, 265-275.
Pusztai A, Ewen SW, Grant G, et al. (1990) Relationship between survival and binding of plant lectins during small intestinal passage and their effectiveness as growth factors. Digestion 46, Suppl. 2, 308-316.
Zoppi G, Andreotti G, Pajno-Ferrara F, et al. (1972) Exocrine pancreas function in premature and full term neonates. Pediatr Res 6, 880-886.
Kisfalvi K, Hajnal F, Varga G, et al. (1993) Influence of gastrointestinal (GI) hormones on suckling, gastric emptying and pancreatic trypsin content in the developing rat. J Dev Physiol 19, 149-155.
Herzig KH, Bardocz S, Grant G, et al. (1997) Red kidney bean lectin is a potent cholecystokinin releasing stimulus in the rat inducing pancreatic growth. Gut 41, 333-338.
Grant G, Edwards JE, Ewan EC, et al. (1999) Secretion 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 19, 382-389.
Kordas K, Burghardt B, Kisfalvi K, et al. (2000) Diverse effects of phytohaemagglutinin on gastrointestinal secretions in rats. J Physiol Paris 94, 31-36.
Washington MC, Murry CR, Raboin SJ, et al. (2011) Cholecystokinin-8 activates myenteric neurons in 21-and 35-day old but not 4-and 14-day old rats. Peptides 32, 272-280.
Telemo E, Westrom BR&Karlsson BW (1982) Proteolytic activity as a regulator of the transmission of orally fed proteins from the gut to the blood serum in the suckling rat. Biol Neonate 41, 85-93.
Martin MG, Wu SV&Walsh JH (1997) Ontogenetic development and distribution of antibody transport and Fc receptor mRNA expression in rat intestine. Dig Dis Sci 42, 1062-1069.
Kelly D, Begbie R&King TP (1992) Postnatal intestinal development. In Occasional Publication no. 15, pp. 63-79 [MA Varley, PEV Williams and TL Lawrence, editors]. Edinburgh: British Society of Animal Production.
Brittan M&Wright NA (2004) Stem cell in gastrointestinal structure and neoplastic development. Gut 53, 899-910.
Baba R, Fujita M, Tein CE, et al. (2002) Endocytosis by absorptive cells in the middle segment of the suckling rat small intestine. Anat Sci Int 77, 117-123.
Kumagai N, Baba R, Sakuma Y, et al. (2011) Origin of the apical transcytic membrane system in jejunal absorptive cells of neonates. Med Mol Morphol 44, 71-78.
Cummings RD&Kornfeld S (1982) Characterization 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 257, 11230-11234.
Green ED&Baenziger JU (1987) Oligosaccharide specificities of Phaseolus vulgaris leukoagglutinating and erythroagglutinating phytohemagglutinins. Interactions with N-glycanase-released oligosaccharides. J Biol Chem 262, 12018-12029.
Arévalo Sureda E, Westrom B, Pierzynowski S, et al. (2015) Increased pancreatic protease activity in relation to PAR-2 receptor expression during intestinal postnatal development in rats. 48th Annual meeting of the European Society for Pediatric Gastroenterology, Hepatology and Nutrition (ESPGHAN). Amsterdam, The Netherlands.
Volynets V, Reichold A, Bardos G, et al. (2016) Assessment of the Intestinal Barrier with Five Different Permeability Tests in Healthy C57BL/6J and BALB/cJ Mice. Dig Dis Sci 61, 737-746.
Prykhod'ko O, Pierzynowski SG&Westrom BR (2010) Immune suppression by cyclosporin A inhibits phytohemagglutinin-induced precocious gut maturation in suckling rats. J Pediatr Gastroenterol Nutr 50, 473-480.
Jacob C, Yang PC, Darmoul D, et al. (2005) Mast cell tryptase controls paracellular permeability of the intestine. Role of protease-activated receptor 2 and beta-arrestins. J Biol Chem 280, 31936-31948.
Groschwitz KR, Wu D, Osterfeld H, et al. (2013) Chymasemediated intestinal epithelial permeability is regulated by a protease-activating receptor/matrix metalloproteinase-2-dependent mechanism. Am J Physiol-Gastr L 304, G479-G489.
Vanuytsel T, Vermeire S&Cleynen I (2013) The role of Haptoglobin and its related protein, Zonulin, in inflammatory bowel disease. Tissue Barriers 1, e27321.
Fasano A (2011) Zonulin and its regulation of intestinal barrier function: The biological door to inflammation, autoimmunity, and cancer. Physiol Rev 91, 151-175.
Vergnolle N (2016) Protease inhibition as new therapeutic strategy for GI diseases. Gut 65, 1215-1224.
Linderoth A, Prykhod'ko O, Pierzynowski SG, et al. (2006) Enterally but not parenterally administered Phaseolus vulgaris lectin induces growth and precocious maturation of the gut in suckling rats. Biol Neonate 89, 60-68.
Fiocchi C (2008) What is 'physiological' intestinal inflammation and how does it differ from 'pathological' inflammation Inflamm Bowel Dis 14, Suppl. 2, S77-S78.