Digestive Diseases and Sciences

, Volume 35, Issue 2, pp 251–256

Stimulation of secretory IgA and secretory component of immunoglobulins in small intestine of rats treated withSaccharomyces boulardii

  • Jean-Paul Buts
  • Paul Bernasconi
  • Jean-Pierre Vaerman
  • Charles Dive
Original Articles

Abstract

Saccharomyces boulardii (S.b.) is largely used in Western European countries for the treatment of acute infectious enteritis and antibiotic-induced gastrointestinal disorders. To study the mechanisms of the protective effect of S.b. against enteral pathogen infection, we assessed the response of the intestinal secretion of secretory IgA (s-IgA) and of the secretory component of immunoglobulins (SC) to oral administration of high doses (0.5 mg/g body weight, three times per day) of S.b. cells in growing rats. S.b. cells (biological activity: 2.8× 109 viable cells/100 mg) were administered daily by gastric intubation to weanling rats from day 14 until day 22 postpartum. Control groups received either 0.9% saline or ovalbumin following the same schedule. Expressed per milligram of cell protein, SC content was significantly increased in crypt cells isolated from the jejunum (48.5% vs saline controls, P< 0.05) as it was in the duodenal fluid (62.8% vs saline controls, P<0.01) of rats treated with S.b. Oral treatment with S.b. had no effect on the secretion of SC by the liver. In the duodenal fluid of rats treated with S.b. cells, the mean concentration of s-IgA was increased by 56.9% (P<0.01) over the concentration of s-IgA measured in saline controls. Compared to control rats treated from day 14 until day 22 postpartum with an antigenic load of ovalbumin equivalent to the total protein load provided by Sb cells (0.05 mg protein/g body weight, three times per day), S.b.-treated rats also exhibited a significantly higher intestinal concentration of SC (69% in villus cells, P<0.025 and 80% in crypt cells, P<0.01 These changes in intestinal SC and s-IgA concentration appeared not to be due to an increase in enterocyte turnover rate, since the mucosal mass parameters and the incorporation rate of [3H]thymidine into DNA measured in the jejunum, ileum, and colon remained unchanged in S.b.- treated rats. Our findings suggest that one of the mechanisms by which S.b. exerts its immunoprotective effect in the gastrointestinal tract is a stimulation of the intestinal secretion of s-IgA and of the secretory component of immunoglobulins.

Key words

Saccharomyces boulardii secretory component secretory IgA intestinal mucosal mass growing rat 

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References

  1. 1.
    Surawicz CM, Elmer GW, Speelman P, McFarland LV, Chinn J, Van Belle G: Prevention of antibiotic-associated diarrhea bySaccharomyces boulardii: A prospective study. Gastroenterology 96:981–988, 1989.PubMedGoogle Scholar
  2. 2.
    Chapoy P: Traitement des diarrhées aiguës infantiles. Essai contrôlé deSaccharomyces boulardii. Ann Pediatr 32:561–563, 1985.Google Scholar
  3. 3.
    Massot J, Desconclois M, Astoin J: Protection parSaccharomyces boulardii de la diarrhée àEscherichia coli du souriceau. Ann Pharm Franc 40:445–449, 1982Google Scholar
  4. 4.
    Toothaker RD, Elmer GW: Prevention of clindamycin induced mortality in hamster bySaccharomyces boulardii. Antimicrob Agents Chemother 26:552–556, 1984PubMedGoogle Scholar
  5. 5.
    Massot J, Sanchez O, Couchy R, Astoin J, Parodi L: Bacterio-pharmacological activity ofSaccharomyces Boulardii in clindamycin induced colitis in the hamster. Arzneim Forsch/Drug Res 34:794–797, 1984Google Scholar
  6. 6.
    Buts JP, Bernasconi P, Van Craynest MP, Maldague P, De Meyer R: Response of human and rat small intestinal mucosa to oral administration ofSaccharomyces boulardii. Pediatr Res 20:192–196, 1986PubMedGoogle Scholar
  7. 7.
    Buts JP, Nyakabasa M: Role of dietary protein adaptation at weaning in the development of the rat gastrointestinal tract. Pediatr Res 19:857–862, 1985PubMedGoogle Scholar
  8. 8.
    Buts JP, Delacroix DL: Ontogenic changes in secretory component expression by villous and crypt cells of rat small intestine. Immunology 54:181–187, 1985PubMedGoogle Scholar
  9. 9.
    Weiser MM: Intestinal epithelial cell surface membrane glycoprotein synthesis. J Biol Chem 248:2536–2541, 1973PubMedGoogle Scholar
  10. 10.
    Raul F, Simon P, Kedinger M, Haffen K: Intestinal enzyme activities in isolated villous and crypt cells during postnatal development of the rat. Cell Tissue Res 176:167–178, 1977PubMedGoogle Scholar
  11. 11.
    Vaerman JP, Heremans JF, Bazin H, Beckers A: Identification and some properties of rat secretory component. J Immunol 114:265–269, 1975PubMedGoogle Scholar
  12. 12.
    Delacroix DL, Vaerman JP: A solid-phase direct competition radioimmunoassay for quantitation of secretory IgA in human serum. J Immunol Methods 40:345–358, 1981PubMedGoogle Scholar
  13. 13.
    Delacroix DL, Vaerman JP: Secretory component (SC): Preferential binding to heavy (>11 s) IgA polymers and IgM in serum in contrast to predominance of 11 s and free SC forms in secretions. Clin Exp Immunol 49:717–723, 1982PubMedGoogle Scholar
  14. 14.
    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, 1984PubMedGoogle Scholar
  15. 15.
    Acosta Altamirano G, Barranco Acosta C, Van Roost E, Vaerman JP: Isolation and characterization of secretory IgA (s-IgA) and free secretory component (FSC) from rat bile. Mol Immunol 17:1525–1537, 1980PubMedGoogle Scholar
  16. 16.
    Burton K: A study of the conditions and mechanism of the diphenylamine reaction for the calorimetric estimation of deoxyribonucleic acid. Biochem J 62:315–323, 1956PubMedGoogle Scholar
  17. 17.
    Giles KW, Meyers M: An improved diphenylamine method for the estimation of DNA. Nature 206:93–94, 1965PubMedGoogle Scholar
  18. 18.
    Lowry OH, Rosebrough NJ, Farr AL, Randall RJ: Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275, 1951PubMedGoogle Scholar
  19. 19.
    Blehaut H, Massot J, Elmer GW, Levy RH: Disposition kinetics ofSaccharomyces boulardii in man and rat. Biopharm Drug Disp 1989 (in press)Google Scholar
  20. 20.
    Brugier S, Patte F: Antagonismein vitro entre l'Ultra-Levure et différents germes bactériens. Med Paris 45:3–8, 1975Google Scholar
  21. 21.
    Ducluzeau R, Bensaada M: Effect comparé de l'administration unique ou en continu deSaccharomyces boulardii sur l'établissement de diverses souches deCandida dans le tractus digestif de souris gnotoxéniques. Ann Microbiol (Inst Pasteur) 133B:491–501, 1982Google Scholar
  22. 22.
    Vidon N, Huchet B, Rambaud JC: Influence deSaccharomyces boulardii sur la sécrétion jéjunale induite chez le rat par la toxine cholérique. Gastroenterol Clin Biol 10:13–16, 1986PubMedGoogle Scholar
  23. 23.
    Corthier G, Dubos F, Ducluzeau R: Prevention ofClostridium difficile induced mortality in gnotobiotic mice bySaccharomyces boulardii. Can J Microbiol 32:894–896, 1986PubMedGoogle Scholar
  24. 24.
    Machado Gaetano JA, Parames MT, Babo MJ, Santos A, Bandeira Ferreira A, Freitas AA, Clementa Coelho MR, Matthioli Mateus A: Immunopharmacological effects ofSaccharomyces boulardii in healthy volunteers. Int J Immunopharmacol 8:245–259, 1986PubMedGoogle Scholar
  25. 25.
    Tomasi TB: The gamma-A globulins: First line of defense. Hosp Pract 2:26–35, 1967Google Scholar
  26. 26.
    Stokes GR, Soothill JF, Turner MW: Immune exclusion is a function of IgA. Nature 255:745–746, 1975PubMedGoogle Scholar
  27. 27.
    Brandtzaeg P: Mucosal and glandular distribution of immunoglobulin component. Differential localization of free and bound SC in secretory epithelial cells. J Immunol 112:1553–1557, 1974PubMedGoogle Scholar
  28. 28.
    Brandtzaeg P: Transport models for secretory IgA and secretory IgM. Clin Exp Immunol 44:221–232, 1981PubMedGoogle Scholar
  29. 29.
    Mostov KE, Kraehenbuhl JP, Blobel G: Receptor mediated transcellular transport of immunoglobulin: Synthesis of secretory component as multiple and larger transmembrane forms. Proc Natl Acad Sci USA 77:7257–7261, 1980PubMedGoogle Scholar
  30. 30.
    Mostov KE, Blobel G: A transmembrane precursor of secretory component. The receptor for transcellular transport of polymeric immunoglobulins. J Biol Chem 257:11816–11821, 1982PubMedGoogle Scholar
  31. 31.
    Kuhn LC, Kraehenbuhl JP: The sacrificial receptor translocation of polymeric IgA across epithelia. Trends Biochem Sci 7:299–302, 1982Google Scholar
  32. 32.
    Walker WA, Isselbacker KJ, Bloch KJ: Intestinal uptake of macromolecules III studies on the mechanism by which immunization interferes with antigen uptake. J Immunol 115:854–861, 1975PubMedGoogle Scholar
  33. 33.
    Svanborg Eden C, Svennerholm AM: Secretory immunoglobulin A and G antibodies prevent adhesion of Escherichia Coli to human urinary tract epithelial cells. Infect Immun 22:790–797, 1978PubMedGoogle Scholar
  34. 34.
    Manning RJ, Walker PG, Carter L, Barrington PJ, Jackson GDF: Studies on the origins of biliary immunoglobulins in rats. Gastroenterology 87:173–179, 1984PubMedGoogle Scholar
  35. 35.
    Jackson GDF, Cooper GN: Immune responses of rats to liver Vibrio cholerae: Secretions of antibodies in bile. Parasite Immunol 3:127–135, 1981PubMedGoogle Scholar
  36. 36.
    Tomasi TB, Larson DO, Challacombe S, Mc Nabb P: Mucosal immunity: The origin and migration pattern of cells in the secretory system. J Allergy Clin Immunol 65:12–19, 1980PubMedGoogle Scholar

Copyright information

© Plenum Publishing Corporation 1990

Authors and Affiliations

  • Jean-Paul Buts
    • 1
    • 2
    • 3
  • Paul Bernasconi
    • 1
    • 2
    • 3
  • Jean-Pierre Vaerman
    • 1
    • 2
    • 3
  • Charles Dive
    • 1
    • 2
    • 3
  1. 1.The Laboratory of Pediatric Gastroenterology and Nutrition, Unit of GastroenterologyUniversity of LouvainBelgium
  2. 2.The International Institute of Cellular and Molecular PathologyBrusselsBelgium
  3. 3.Biocodex LaboratoriesMontrougeFrance
  4. 4.Department of PediatricsCliniques Universitaires Saint-LucBrusselsBelgium

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