Skip to main content
PMC home page
Biochemical Journal logoLink to Biochemical Journal
. 2000 Jan 1;345(Pt 1):69–75.

Influence of spermine on intestinal maturation of the glycoprotein glycosylation process in neonatal rats.

S Greco 1, I Hugueny 1, P George 1, P Perrin 1, P Louisot 1, M C Biol 1
PMCID: PMC1220731  PMID: 10600640

Abstract

Previous work has shown an inverse evolution of the rat intestinal glycoprotein sialylation that decreases from birth to weaning and of fucosylation that increases markedly after weaning during postnatal development. At weaning time, an increase in the intestinal level of polyamines (and especially that of spermine) was observed, owing partly to the higher level of spermine found in solid food given to rats at this period in comparison with the level found in milk. To study the role of this polyamine as a possible maturation factor of the glycoprotein glycosylation, suckling rats were treated for 4 days with spermine administered orally. This treatment allowed us to mimic the spermine increase that was observed naturally in rat small intestine after weaning because, in intestines of spermine-treated suckling rats, spermine was the only polyamine to be increased and was at a level similar to that of weaned rats. Spermine treatment did not induce appreciable changes in sialyltransferase activity or in sialylation of the brush-border-membrane glycoproteins. On the contrary, this treatment induced a rise in an alpha-1, 2-fucosyltransferase activity that was regulated at the transcriptional level, but not by its inhibitor (fuctinin), and no change in the availability of substrate (GDP-fucose). As a consequence of the increase in alpha-1,2-fucosyltransferase level and of the decrease in alpha-l-fucosidase level after treatment with spermine, several alpha-1,2-fucoproteins, naturally found in brush border membranes after weaning time, appeared precociously in these membranes after the treatment of the immature suckling rats. These results indicate that spermine is a maturation factor for the fucosylation of intestinal brush-border-membrane glycoproteins but not for their sialylation, and that this polyamine might be implicated in the increased fucosylation naturally occurring at weaning time during postnatal development.

Full Text

The Full Text of this article is available as a PDF (149.5 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. BURTON K. A study of the conditions and mechanism of the diphenylamine reaction for the colorimetric estimation of deoxyribonucleic acid. Biochem J. 1956 Feb;62(2):315–323. doi: 10.1042/bj0620315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bardocz S. The role of dietary polyamines. Eur J Clin Nutr. 1993 Oct;47(10):683–690. [PubMed] [Google Scholar]
  3. Bardócz S., Duguid T. J., Brown D. S., Grant G., Pusztai A., White A., Ralph A. The importance of dietary polyamines in cell regeneration and growth. Br J Nutr. 1995 Jun;73(6):819–828. doi: 10.1079/bjn19950087. [DOI] [PubMed] [Google Scholar]
  4. Biol M. C., Lenoir D., Greco S., Galvain D., Hugueny I., Louisot P. Role of insulin and nutritional factors in intestinal glycoprotein fucosylation during postnatal development. Am J Physiol. 1998 Nov;275(5 Pt 1):G936–G942. doi: 10.1152/ajpgi.1998.275.5.G936. [DOI] [PubMed] [Google Scholar]
  5. Biol M. C., Martin A., Richard M., Louisot P. Developmental changes in intestinal glycosyl-transferase activities. Pediatr Res. 1987 Sep;22(3):250–256. doi: 10.1203/00006450-198709000-00003. [DOI] [PubMed] [Google Scholar]
  6. Biol M. C., Pintori S., Mathian B., Louisot P. Dietary regulation of intestinal glycosyl-transferase activities: relation between developmental changes and weaning in rats. J Nutr. 1991 Jan;121(1):114–125. doi: 10.1093/jn/121.1.114. [DOI] [PubMed] [Google Scholar]
  7. Bry L., Falk P. G., Midtvedt T., Gordon J. I. A model of host-microbial interactions in an open mammalian ecosystem. Science. 1996 Sep 6;273(5280):1380–1383. doi: 10.1126/science.273.5280.1380. [DOI] [PubMed] [Google Scholar]
  8. Buts J. P., De Keyser N., Dive C. Intestinal development in the suckling rat: effect of insulin on the maturation of villus and crypt cell functions. Eur J Clin Invest. 1988 Aug;18(4):391–398. doi: 10.1111/j.1365-2362.1988.tb01029.x. [DOI] [PubMed] [Google Scholar]
  9. Buts J. P., De Keyser N., Kolanowski J., Sokal E., Van Hoof F. Maturation of villus and crypt cell functions in rat small intestine. Role of dietary polyamines. Dig Dis Sci. 1993 Jun;38(6):1091–1098. doi: 10.1007/BF01295726. [DOI] [PubMed] [Google Scholar]
  10. Büller H. A., Rings E. H., Pajkrt D., Montgomery R. K., Grand R. J. Glycosylation of lactase-phlorizin hydrolase in rat small intestine during development. Gastroenterology. 1990 Mar;98(3):667–675. doi: 10.1016/0016-5085(90)90287-b. [DOI] [PubMed] [Google Scholar]
  11. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  12. Chu S. H., Walker W. A. Developmental changes in the activities of sialyl- and fucosyltransferases in rat small intestine. Biochim Biophys Acta. 1986 Oct 1;883(3):496–500. doi: 10.1016/0304-4165(86)90289-8. [DOI] [PubMed] [Google Scholar]
  13. Dufour C., Dandrifosse G., Forget P., Vermesse F., Romain N., Lepoint P. Spermine and spermidine induce intestinal maturation in the rat. Gastroenterology. 1988 Jul;95(1):112–116. doi: 10.1016/0016-5085(88)90298-3. [DOI] [PubMed] [Google Scholar]
  14. Galand G. Effect of an antiglucocorticoid (RU-38486) on hydrocortisone induction of maltase-glucosamylase, sucrase-isomaltase and trehalase in brush border membranes of suckling rats. Experientia. 1988 Jun 15;44(6):516–518. doi: 10.1007/BF01958934. [DOI] [PubMed] [Google Scholar]
  15. Hamr A., Delannoy P., Verbert A., Kolínská J. The hydrocortisone-induced transcriptional down-regulation of beta-galactoside alpha2,6-sialyltransferase in the small intestine of suckling rats is suppressed by mifepristone (RU-38.486). J Steroid Biochem Mol Biol. 1997 Jan;60(1-2):59–66. doi: 10.1016/s0960-0760(96)00170-7. [DOI] [PubMed] [Google Scholar]
  16. Henning S. J. Postnatal development: coordination of feeding, digestion, and metabolism. Am J Physiol. 1981 Sep;241(3):G199–G214. doi: 10.1152/ajpgi.1981.241.3.G199. [DOI] [PubMed] [Google Scholar]
  17. Kaouass M., Deloyer P., Dandrifosse G. Intestinal development in suckling rats: direct or indirect spermine action? Digestion. 1994;55(3):160–167. doi: 10.1159/000201142. [DOI] [PubMed] [Google Scholar]
  18. Kaouass M., Deloyer P., Gouders I., Peulen O., Dandrifosse G. Role of interleukin-1 beta, interleukin-6, and TNF-alpha in intestinal maturation induced by dietary spermine in rats. Endocrine. 1997 Apr;6(2):187–194. doi: 10.1007/BF02738963. [DOI] [PubMed] [Google Scholar]
  19. Kaouass M., Sulon J., Deloyer P., Dandrifosse G. Spermine-induced precocious intestinal maturation in suckling rats: possible involvement of glucocorticoids. J Endocrinol. 1994 May;141(2):279–283. doi: 10.1677/joe.0.1410279. [DOI] [PubMed] [Google Scholar]
  20. Kessler M., Acuto O., Storelli C., Murer H., Müller M., Semenza G. A modified procedure for the rapid preparation of efficiently transporting vesicles from small intestinal brush border membranes. Their use in investigating some properties of D-glucose and choline transport systems. Biochim Biophys Acta. 1978 Jan 4;506(1):136–154. doi: 10.1016/0005-2736(78)90440-6. [DOI] [PubMed] [Google Scholar]
  21. Kobata A. alpha-L-fucosidases from almond emulsin. Methods Enzymol. 1982;83:625–631. doi: 10.1016/0076-6879(82)83061-9. [DOI] [PubMed] [Google Scholar]
  22. Köttgen E., Reutter W., Gerok W. Two different gamma-glutamyltransferases during development of liver and small intestine: a fetal (sialo-) and an adult (asialo-) glycoprotein. Biochem Biophys Res Commun. 1976 Sep 7;72(1):61–66. doi: 10.1016/0006-291x(76)90960-8. [DOI] [PubMed] [Google Scholar]
  23. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  24. Lenoir D., Ruggiero-Lopez D., Louisot P., Biol M. C. Developmental changes in intestinal glycosylation: nutrition-dependent multi-factor regulation of the fucosylation pathway at weaning time. Biochim Biophys Acta. 1995 Mar 8;1234(1):29–36. doi: 10.1016/0005-2736(94)00254-m. [DOI] [PubMed] [Google Scholar]
  25. Lux G. D., Marton L. J., Baylin S. B. Ornithine decarboxylase is important in intestinal mucosal maturation and recovery from injury in rats. Science. 1980 Oct 10;210(4466):195–198. doi: 10.1126/science.6774420. [DOI] [PubMed] [Google Scholar]
  26. Malo C., Qureshi I. A., Letarte J. Postnatal maturation of enterocytes in sparse-fur mutant mice. Am J Physiol. 1986 Feb;250(2 Pt 1):G177–G184. doi: 10.1152/ajpgi.1986.250.2.G177. [DOI] [PubMed] [Google Scholar]
  27. Noack J., Kleessen B., Proll J., Dongowski G., Blaut M. Dietary guar gum and pectin stimulate intestinal microbial polyamine synthesis in rats. J Nutr. 1998 Aug;128(8):1385–1391. doi: 10.1093/jn/128.8.1385. [DOI] [PubMed] [Google Scholar]
  28. Olaya J., Neopikhanov V., Uribe A. Lipopolysaccharide of Escherichia coli, polyamines, and acetic acid stimulate cell proliferation in intestinal epithelial cells. In Vitro Cell Dev Biol Anim. 1999 Jan;35(1):43–48. doi: 10.1007/s11626-999-0042-4. [DOI] [PubMed] [Google Scholar]
  29. Pegg A. E., McCann P. P. Polyamine metabolism and function. Am J Physiol. 1982 Nov;243(5):C212–C221. doi: 10.1152/ajpcell.1982.243.5.C212. [DOI] [PubMed] [Google Scholar]
  30. Piau J. P., Labarriere N., Dabouis G., Denis M. G. Evidence for two distinct alpha(1,2)-fucosyltransferase genes differentially expressed throughout the rat colon. Biochem J. 1994 Jun 15;300(Pt 3):623–626. doi: 10.1042/bj3000623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Pollack P. F., Koldovskỳ O., Nishioka K. Polyamines in human and rat milk and in infant formulas. Am J Clin Nutr. 1992 Aug;56(2):371–375. doi: 10.1093/ajcn/56.2.371. [DOI] [PubMed] [Google Scholar]
  32. Romain N., Dandrifosse G., Jeusette F., Forget P. Polyamine concentration in rat milk and food, human milk, and infant formulas. Pediatr Res. 1992 Jul;32(1):58–63. doi: 10.1203/00006450-199207000-00011. [DOI] [PubMed] [Google Scholar]
  33. Ruggiero-Lopez D., Biol M. C., Louisot P., Martin A. Participation of an endogenous inhibitor of fucosyltransferase activities in the developmental regulation of intestinal fucosylation processes. Biochem J. 1991 Nov 1;279(Pt 3):801–806. doi: 10.1042/bj2790801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Schaffner W., Weissmann C. A rapid, sensitive, and specific method for the determination of protein in dilute solution. Anal Biochem. 1973 Dec;56(2):502–514. doi: 10.1016/0003-2697(73)90217-0. [DOI] [PubMed] [Google Scholar]
  35. Shub M. D., Pang K. Y., Swann D. A., Walker W. A. Age-related changes in chemical composition and physical properties of mucus glycoproteins from rat small intestine. Biochem J. 1983 Nov 1;215(2):405–411. doi: 10.1042/bj2150405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Taatjes D. J., Roth J. Selective loss of sialic acid from rat small intestinal epithelial cells during postnatal development: demonstration with lectin-gold techniques. Eur J Cell Biol. 1990 Dec;53(2):255–266. [PubMed] [Google Scholar]
  37. Torres-Pinedo R., Mahmood A. Postnatal changes in biosynthesis of microvillus membrane glycans of rat small intestine: I. Evidence of a developmental shift from terminal sialylation to fucosylation. Biochem Biophys Res Commun. 1984 Dec 14;125(2):546–553. doi: 10.1016/0006-291x(84)90574-6. [DOI] [PubMed] [Google Scholar]
  38. Vertino-Bell A., Ren J., Black J. D., Lau J. T. Developmental regulation of beta-galactoside alpha 2,6-sialyltransferase in small intestine epithelium. Dev Biol. 1994 Sep;165(1):126–136. doi: 10.1006/dbio.1994.1240. [DOI] [PubMed] [Google Scholar]
  39. Wild G. E., Daly A. S., Sauriol N., Bennett G. Effect of exogenously administered polyamine on the structural maturation and enzyme ontogeny of the postnatal rat intestine. Biol Neonate. 1993;63(4):246–257. doi: 10.1159/000243938. [DOI] [PubMed] [Google Scholar]
  40. Wéry I., Dandrifosse G. Evolution of biochemical parameters characterizing the proximal small intestine after orally administered spermine in unweaned rats. Endocr Regul. 1993 Dec;27(4):201–207. [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES