Influence of breast milk polyamines on suckling rat immune system maturation

Developmental and Comparative Immunology

Volumn 34, Issue 2, 2010, Pages 210-218

  Pérez Cano, Francisco J ^a,b   González Castro, Ana ^a   Castellote, Cristina ^a,b,c   Franch, Àngels ^a,b,c   Castell, Margarida ^a,b  

^a UNIVERSITY OF BARCELONA   (Spain)

^b UB   (Spain)

^c CIBER EPIDEMIOLOGÍA Y SALUD PÚBLICA CIBERESP   (Spain)

Author keywords

Immune maturation; Intraepithelial lymphocytes; Lamina propria lymphocytes; Spermidine; Spermine; Spleen lymphocytes

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; IMMUNOGLOBULIN; SPERMIDINE; SPERMINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; BREAST MILK; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; FEMALE; IMMUNOGLOBULIN PRODUCTION; LAMINA PROPRIA; MUCOSAL IMMUNITY; NATURAL KILLER CELL; NEWBORN; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RAT; SMALL INTESTINE; SPLEEN CELL; SUCKLING;

RATTUS;

EID: 70450224862     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2009.10.001     Document Type: Article

References (55)

1. Parrot D.M.V., and Mac Donald T.T. The ontogeny of the mucosal immune system in rodents. In: Mac Donald T.T. (Ed). Ontogeny of the immune system of the gut (1990), CRC Press, Florida 51-68
2. Brandtzaeg P. Mucosal immunity: integration between mother and the breast-fed infant. Vaccine 21 (2003) 3382-3388
3. Bailey M., Haverson K., Inman C., Harris C., Jones P., Corfield G., et al. The influence of environment on development of the mucosal immune system. Vet Immunol Immunopathol 108 (2005) 189-198
4. Beaulieu J., Dupont C., and Lemieux P. Whey proteins and peptides: beneficial effects on immune health. Therapy 3 (2006) 69-78
5. Hanson L.A., and Silfverdal S.A. The mother's immune system is a balanced threat to the foetus, turning to protection of the neonate. Acta Paediatr 98 (2009) 221-228
6. Thomas T., and Thomas T.J. Polyamines in cell growth and cell death: molecular mechanisms and therapeutic applications. Cell Mol Life Sci 58 (2001) 244-258
7. Pollack P.F., Koldovsky O., and Nishioka K. Polyamines in human and rat milk and in infant formulas. Am J Clin Nutr 56 (1992) 371-375
8. Romain N., Dandrifosse G., Jeusette F., and Forget P. Polyamine concentration in rat milk and food, human milk, and infant formulas. Pediatr Res 32 (1992) 58-63
9. Dorhout B., van Beusekom C.M., Huisman M., Kingma A.W., de Hoog E., Boersma E.R., et al. Estimation of 24-hour polyamine intake from mature human milk. J Pediatr Gastroenterol Nutr 23 (1996) 298-302
10. Moinard C., Cynober L., and De Bandt J.P. Polyamines: metabolism and implications in human diseases. Clin Nutr 24 (2005) 184-197
11. Larqué E., Sabater-Molina M., and Zamora S. Biological significance of dietary polyamines. Nutrition 23 (2007) 87-95
12. Seiler N., and Raul F. Polyamines and the intestinal tract. Crit Rev Clin Lab Sci 44 (2007) 365-411
13. De Bandt J.P., Moinard C., and Cynober L. Métabolisme et fonctions des polyamines. Immuno-analyse Biol Spécialisée 21 (2006) 333-341
14. Yuan Q., Ray R.M., Viar M.J., and Johnson L.R. Polyamine regulation of ornithine decarboxylase and its antizyme in intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 280 (2001) 130-138
15. Sabater-Molina M., Larqué E., Torrella F., Plaza J., Lozano T., Muñoz A., et al. Effects of dietary polyamines at physiologic doses in early-weaned piglets. Nutrition 25 (2009) 940-946
16. Matkovics B., Kecskemeti V., Varga S.I., Novak Z., and Kertesz Z. Antioxidant properties of di- and polyamines. Comp Biochem Physiol B 104 (1993) 475-479
17. Peulen O., Gharbi M., Powroznik B., and Dandrifosse G. Differential effect of dietary spermine on alkaline phosphatase activity in jejunum and ileum of unweaned rats. Biochimie 86 (2004) 487-493
18. Deloyer P., Peulen O., and Dandrifosse G. Intestinal effects of long-lasting spermine ingestion by suckling rats. Exp Physiol 90 (2005) 901-908
19. Wang J.Y. Polyamines regulate expression of E-cadherin and play an important role in control of intestinal epithelial barrier function. Inflammopharmacology 13 (2005) 91-101
20. Kraehenbuhl J.P., and Neutra M.R. Molecular and cellular basis of immune protection of mucosal surfaces. Physiol Rev 72 (1992) 853-879
21. Robijn R.J., Logtenberg T., Wiegman L.J., van Berge Henegouwen G.P., Houwen R.W., and Koningsberger J.C. Intestinal T lymphocytes. Scand J Gastroenterol 212 (1995) 23-33
22. Ter Steege J.C., Buurman W.A., and Forget P.P. The neonatal development of intraepithelial and lamina propria lymphocytes in the murine small intestine. Dev Immunol 5 (1997) 121-128
23. Mowat A. Anatomical basis of tolerance and immunity to intestinal antigens. Nat Rev Immunol 3 (2003) 331-341
24. Beagley K.W., Fujihashi K., Lagoo A.S., Lagoo-Deenadaylan S., Black C.A., Murray A.M., et al. Differences in intraepithelial lymphocyte T cell subsets isolated from murine small versus large intestine. J Immunol 154 (1995) 5611-5619
25. Lundquist C., Baranov V., Hammarström S., Athlin L., and Hammarström M.L. Intra-epithelial lymphocytes. Evidence for regional specialization and extrathymic T cell maturation in the human gut epithelium. Int Immunol 7 (1995) 1473-1487
26. Pérez-Cano F.J., Castellote C., González-Castro A., Pelegrí C., Castell M., and Franch A. Developmental changes in intraepithelial T lymphocytes and NK cells in the small intestine of neonatal rats. Pediatr Res 58 (2005) 885-891
27. Pérez-Cano F.J., Castellote C., Marín-Gallén S., Franch A., and Castell M. Neonatal immunoglobulin secretion and lymphocyte phenotype in rat small intestine lamina propria. Pediatr Res 58 (2005) 164-169
28. Ter Steege J.C., Buurman W.A., and Forget P.P. Spermine induces maturation of the immature intestinal immune system in neonatal mice. J Pediatr Gastroenterol Nutr 25 (1997) 332-340
29. Jolois O., Peulen O., Collin S., Simons M., Dandrifosse G., and Heinen E. Spermine induces precocious development of the spleen in mice. Exp Physiol 87 (2002) 69-75
30. Reeves P.G., Nielsen F.H., and Fahey Jr. G.C. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 123 (1993) 1939-1951
31. Pérez-Cano F.J., Marín-Gallén S., Castell M., Rodríguez-Palmero M., Rivero M., Franch A., et al. Bovine whey protein concentrate supplementation modulates maturation of immune system in suckling rats. Br J Nutr 98 (2007) S80-S84
32. Pérez-Cano F.J., Castellote C., Marín-Gallén S., González-Castro A., Franch A., and Castell M. Phenotypic and functional characteristics of rat spleen lymphocytes during suckling. Dev Comp Immunol 31 (2007) 1264-1277
33. Peulen O., and Dandrifosse G. Spermine-induced maturation in Wistar rat intestine: a cytokine-dependent mechanism. J Pediatr Gastroenterol Nutr 38 (2004) 524-532
34. Gharbi M., Powroznik B., Mazzucchelli G., Deville C., Nollevaux G., Rusu D., et al. Modulation of intestinal urea cycle by dietary spermine in suckling rat. Biochem Biophys Res Commun 336 (2005) 1119-1124
35. Til H.P., Falke H.E., Prinsen M.K., and Willems M.I. Acute and subacute toxicity of tyramine, spermidine, spermine, putrescine and cadaverine in rats. Food Chem Toxicol 35 (1997) 337-348
36. Buts J.P., De Keyser N., Kolanowski J., Sokal E., and Van Hoof F. Maturation of villus and crypt cell functions in rat small intestine. Role of dietary polyamines. Dig Dis Sci 38 (1993) 1091-1098
37. Wery I., Kaouass M., Deloyer P., Buts J.P., Barbason H., and Dandrifosse G. Exogenous spermine induces maturation of the liver in suckling rats. Hepatology 24 (1996) 1206-1210
38. Peulen O., Dewe W., Dandrifosse G., Henrotay I., and Romain N. The relationship between spermine content of human milk during the first postnatal month and allergy in children. Public Health Nutr 1 (1998) 181-184
39. Helgeland L., Brandtzaeg P., Rolstad B., and Vaage J.T. Sequential development of intraepithelial γδ and αβ T lymphocytes expressing CD8αα in neonatal rat intestine: requirement for the thymus. Immunology 92 (1997) 447-456
40. Camerini V., Panwala C., and Kronenberg M. Regional specialization of the mucosal immune system. Intraepithelial lymphocytes of the large intestine have a different phenotype and function than those of the small intestine. J Immunol 151 (1993) 1765-1776
41. Boll G., Rudolphi A., Spiess S., and Reimann J. Regional specialization of intraepithelial T cells in the murine small and large intestine. Scand J Immunol 41 (1995) 103-113
42. Lefrancois L. Phenotypic complexity of intraepithelial lymphocytes of the small intestine. J Immunol 147 (1991) 1746-1751
43. Cheroutre H. IELs: enforcing law and order in the court of the intestinal epithelium. Immunol Rev 206 (2005) 114-131
44. Hayday A., Theodoridis E., Ramsburg E., and Shires J. Intraepithelial lymphocytes: exploring third way in immunology. Nat Immunol 2 (2001) 997-1003
45. Marín-Gallén S., Pérez-Cano F.J., Castell M., Castellote C., and Franch A. Intestinal intraepithelial NK and NKT cell ontogeny in Lewis rats. Dev Comp Immunol 32 (2008) 1405-1408
46. Pérez-Cano F.J., Franch A., Castellote C., and Castell M. Immunomodulatory action of spermine and spermidine on NR8383 macrophage line in various culture conditions. Cell Immunol 226 (2003) 86-94
47. Benamouzig R., Mahe S., Luengo C., Rautureau J., and Tome D. Fasting and postprandial polyamine concentrations in the human digestive lumen. Am J Clin Nutr 65 (1997) 766-770
48. Milovic V. Polyamines in the gut lumen: bioavailability and biodistribution. Eur J Gastroenterol Hepatol 13 (2001) 1021-1025
49. Holtta E., Janne J., and Hovi T. Suppression of the formation of polyamines and macromolecules by DL-alpha-difluoromethylornithine and methylglyoxal bis(guanylhydrazone) in phytohaemagglutinin-activated human lymphocytes. Biochem J 178 (1979) 109-117
50. Elitsur Y., Strom J., and Luk G.D. Inhibition of ornithine decarboxylase activity decreases polyamines and suppresses DNA synthesis in human colonic lamina propria lymphocytes. Immunopharmacology 25 (1993) 253-260
51. Shanahan F. The intestinal immune system. In: Johnson L.R. (Ed). Physiology of the Gastrointestinal Tract (1994), Raven Press, New York p. 643-84
52. Bruder M.C., Spanhaak S., Bruijntjes J.P., Michielsen C.P.P.C., Vos J.G., and Kuper C.F. Intestinal T lymphocytes of different rat strains in immunotoxicity. Toxicol Pathol 27 (1999) 171-179
53. James S.P., and Kiyono H. Gastrointestinal lamina propria T cells. In: Ogra P.L., Mestecky J., Lamm M.E., Strober W., Bienenstock J., and McGhee J.R. (Eds). Mucosal immunology (1999), Academic Press, San Diego, CA 381-396
54. Kroese F.G.M. Immunology of the rat. In: Pastoret P.P., Griebel P., Bazin H., and Govaerts A. (Eds). Handbook of vertebrate immunology (1998), Academic Press, San Diego, CA 137-198
55. Ackerman K.D., Felten S.Y., Dijkstra C.D., Livnat S., and Felten D.L. Parallel development of noradrenergic innervation and cellular compartmentation in the rat spleen. Exp Neurol 103 (1989) 239-255