Abstract
To evaluate the role of dietary polyamines in maturation of the rat small intestine, spermine was given orally twice daily to suckling pups from day 10 to day 14 postpartum at different doses: 0, 0.2, 0.5, 1, 2.5, and 5 μmol/dose. Compared, to saline treated controls, spermine (5 μmol) produced significant increases in mucosal mass parameters (+12 to +57%,P<0.05), induced prematurely, an adult pattern of microvillous enzymes, and enhanced respectively, by 19- and 3.5-fikd (P<0.01 vs controls) the concentration of the secretory component ofp-immunoglobulins in villous and crypt cells. The response of microvillous enzymes (lactase, sucrase, maltase, and aminopeptidase) to spermine was dose-dependent and-specific since oral administration of arginine (5 μmol) or ornithine (5 μmol) was without effect. Intestinal changes were found to be significant (P<0.05) for doses of spermine exceeding 1 μmol/day, which is in the range of the amount of polyamines provided by solid pellets at weaning (0.4 μmol/g). However, intestinal changes were undetectable at the physiological amounts of polyamines consumed by pups from rat milk during the suckling period (less than 0.3 μmol/day). Consistent with a direct effect of spermine on the intestinal cell, the cytosolic activity of ornithine decarboxylase was depressed by 27-fold (P<0.005 vs controls) in the jejunum, while inhibition of ornithine decarboxylase by α-difluoromethylornithine did markedly decrease but did not suppress the cell response to spermine. Alternately, plasma corticosteronemia, which was virtually, absent by day 14 in controls, ranged between 1.4 and 4.6 μg/dl in 60% (N=9) of the spermine-treated rats. These novel findings indicate that dietary polyamines exert direct and indirect trophic effects on the rat immature intestine and can trigger at a critical level of intake the adult expression of villus and crypt cell functions.
References
Henning SJ, Guerin DM: Role of diet in determination of jejunal sucrase activity in the weanling rat. Pediatr Res 15:1068–1072, 1981
Buts JP, De Meyer R: Intestinal development in the suckling rat: Effects of weaning, diet composition and glucocorticoids on thymidine kinase activity and DNA synthesis. Pediatr Res 18:145–150, 1984
Buts JP, Nyakabasa M: Role of dietary protein adaptation at weaning in the development of the rat gastrointestinal tract. Pediatr Res 19:857–862, 1985
Buts JP, Delacroix DL, De Keyser N, Paquet S, Horsmans Y, Boelens M, Van Craynest MP, De Meyer R: Role of dietary iron in maturation of rat small intestine at weaning. Am J Physiol 246(Gastrointest Liver Physiol 9):G725-G731, 1984
Luk GD, Marton LJ, Baylin SB: Ornithine decarboxylase is important in intestinal mucosal maturation and recovery from injury in rats. Science 210:195–198, 1980
Dufour C, Dandrifosse G, Forget P, Vermesse F, Romain N, Lepoint P: Spermine and spermidine induce intestinal maturation in the rat. Gastroenterology 95:112–116, 1988
Georges P, Dandrifosse G, Vermesse P, Forget P, De Loyer P, Romain N: Reversibility of spermine-induced intestinal maturation in the rat. Dig Dis Sci 35:1528–1536, 1990
Russel DH, McVicker TA: Polyamine biogenesis in the rat mammary gland during pregnancy and lactation. Biochem J 130:71–76, 1972
Brosman ME, Yu-Wan HU: Synthesis and function of polyamines in mammary gland during lactation.In Recent Progress in Polyamine Research. L Selmeci, ME Brosman, (eds). 1985, pp 169–179
Kelly D, King TP, Brown DS, McFadyen: Polyamine profiles of porcine milk and of intestinal tissue of pigs during suckling. Reprod Nutr Dev 31:73–80, 1991
Weiser MM: Intestinal epithelial cell surface membrane glycoprotein synthesis I. An indicator of cellular differentiation. J Biol Chem 248:2536–2541, 1973
Raul F, Simon P, Kedinger M, Haffen K: Intestinal enzyme activities in isolated villus and crypt cells during postnatal development on the rat. Cell Tissue Res 176:167–178, 1977
Schmitz J, Preiser H, Maestracci D, Ghosh K, Cerda JJ, Crane RK: Purification of human intestinal brush border membrane. Biochim Biophys Acta 323:98–112, 1973
Messer M, Dahlqvist: A one step ultramicromethod for the assay of intestinal disaccharidases. Anal Biochem 14:376–392, 1966
Maroux S, Louvard D, Baratti J: The aminopeptidase from the hog intestinal brush border. Biochim Biophys Acta 321:282–295, 1973
Okuyama T, Kobayashi: Determination of diamine oxidase activity by liquid scintillation counting. Arch Biochem Biophys 95:242–250, 1961
Fogel WA, Bieganski T, Wozniac J: Interference of aldehyde metabolizing enzymes with diamine oxidase/histaminase activity as determined by,14C-putrescine method. Biochem Pharmacol 27:1159–1162, 1978
Pegg AE, Williams-Ashman HG: Biosynthesis of putrescine in the prostate gland of the rat. Biochem J 108:533–539, 1968
Burton K: A study of the condition and mechanisms of the diphenylamine reaction for the colorimetric estimation of deoxyribonucleic acid. Biochemistry 62:315–323, 1956
Giles KW, Myers M: An improved diphenylamine method for the estimation of DNA. Nature 206:93–94, 1965
Kolanowski J: Simultaneous determination of cortisol, deoxycortisol and corticosterone in plasma and urine by competitive protein binding assay. Response of normal subjects to ACTH and metapyrone. J Steroid Biochem 5:55–64, 1974
Henquin JC, Lambert AE: Bicarbonate modulation of glucose-induced biphasic insulin release by rat islets. Am J Physiol 231(3):713–721, 1976
Buts JP, Delacroix D: Ontogenic changes in secretory component expression by villous and crypt cells of rat small intestine. Immunology 54:181–187, 1985
Henning SJ, Sims JM: Delineation of the glucocorticoidsensitive period of intestinal development in the rat. Endocrinology 104:1158–1163, 1979
Buts JP, De Keyser N, Kolanowski J, Van Hoof F: Hormonal regulation of the rat small intestine: Responsiveness of villus and crypt cells to insulin during the suckling period and unresponsiveness after weaning. Pediatr Res 27:161–164, 1990
Wild GE, Daly AS, Sauriol N, Bennett G: Effects of exogenously administered spermidine on enterocyte membrane function and composition in the neonatal rat intestine. Gastroenterology 98:A435, 1990
Heby O, Persson L: Molecular genetic of polyamine synthesis in eukaryotic cells. Trends Biochem Sciences 15:153–158, 1990
Bardocz S, Brown DS, Grant G, Pusztai A: Luminal and basolateral polyamine uptake by rat small intestine stimulated to grow byPhaseolus vulgaris lectin phytohaemagglutinin in vivo. Biochim Biophys Acta 1034:46–52, 1990
Stein J, Lembck B, Caspary WF; Characteristics of putrescine uptake by human brush border membrane vesicles.In Falk Symposium. Polyamines in the, Gastrointestinal Tract. RH Dowling, UR Fölsch (eds). Kiel, Germany, 1991
Iseki K, Kobayashi M, Miyazaki K: Spermine uptake by rat brush border membrane vesicles. Biochim Biophys Acta 1068:105–110, 1991
Pegg A, McCann P: Polyamine metabolism and function. Am J Physiol 243(Cell Physiol, 12):C212-C221, 1982
Alarcon P, Lebenthal E, Lee PC: effect of difluoromethyl ornithine (DFMO) on small intestine of adult and weanling rats. Dig Dis Sci 32:883–898, 1987
Tabata K, Johnson LR: Mechanism of induction of mucosal ornithine decarboxylase by food. Am J Physiol 251(Gastrointest Liver Physiol 14):G370-G374, 1986
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Buts, JP., De Keyser, N., Kolanowski, J. et al. Maturation of villus and crypt cell functions in rat small intestine. Digest Dis Sci 38, 1091–1098 (1993). https://doi.org/10.1007/BF01295726
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DOI: https://doi.org/10.1007/BF01295726