Digestive Diseases and Sciences

, Volume 49, Issue 1, pp 122–132 | Cite as

Indigestible Disaccharides Open Tight Junctions and Enhance Net Calcium, Magnesium, and Zinc Absorption in Isolated Rat Small and Large Intestinal Epithelium

  • Hitoshi Mineo
  • Midori Amano
  • Hideyuki Chiji
  • Norihiro Shigematsu
  • Fusao Tomita
  • Hiroshi Hara
Article

Abstract

The effects of three indigestible disaccharides on net calcium (Ca), magnesium (Mg), and zinc (Zn) transport in isolated rat jejunal, ileal, cecal, and colonic epithelium were determined. Permeability of fluorescein isothiocynate–dextran-4 (FD4) and transepithelial electrical resistance (TEER), which vary according to tight junction (TJ) activity in the intestinal mucosa, were also determined. The addition of 1–100 mM melibiose, difructose anhydride (DFA) III, or DFA IV to the mucosal medium increased the net absorption of the three minerals and FD4 permeability, while decreasing TEER dose dependently in the four intestinal portions. Positive linear relations were found between the net transport of the three minerals and FD4 passage in all portions of the intestine, whereas negative linear relations were observed between net absorption of the three minerals and TEER. We concluded that the three indigestible saccharides directly affect the epithelial tissue and open TJs, thereby promoting Ca, Mg, and Zn absorption in the small and large intestine in vitro.

mineral absorption indigestible saccharide Ussing chamber intestine tight junction rat 

REFERENCES

  1. 1.
    Goda T, Yamada M, Takase S, Hosoya N: Effect of maltitol intake on intestinal calcium absorption in the rat. J Nutr SciVitaminol (Tokyo) 38:277–286, 1992Google Scholar
  2. 2.
    Brommage R, Binacua C, Antille S, Carrie AL: Intestinal calcium absorption in rats is stimulated by dietary lactulose and other resistant sugars. J Nutr 123:2186–2194, 1993Google Scholar
  3. 3.
    Chonan O, Matsumoto K, Watanuki M: Effect of galactooligosaccharides on calcium absorption and preventing bone loss in ovariectomized rats. Biosci Biotechnol Biochem 59:236–239, 1995Google Scholar
  4. 4.
    Ohta A, Ohtsuki M, Baba S, Adachi T, Sakata T, Sakaguchi E: Calcium and magnesium absorption from the colon and rectum are increased in rats fed fructooligosaccharides. J Nutr 125:2417–2424, 1995Google Scholar
  5. 5.
    Hara H, Suzuki T, Kasai T, Aoyama Y, Ohta A: Ingestion of guargum hydrolysate partially restores calcium absorption in the large intestine lowered by suppression of gastric acid secretion in rats. Br J Nutr 81:315–321, 1999Google Scholar
  6. 6.
    Watanabe O, Hara H, Aoyama Y, Kasai T: Increased intestinal calcium absorption from the ingestion of a phosphorylated guar gum hydrolysate independent of cecal fermentation in rats. Biosci Biotechnol Biochem 64:613–616, 2000Google Scholar
  7. 7.
    Dupuis Y, Digaud A, Fournier P: The relations between intestinal alkaline phosphatase and carbohydrates with regard to calcium absorption. Arch Int Physiol Biochim 86:543–556, 1978Google Scholar
  8. 8.
    Fukahori M, Sakurai H, Akatsu S, Negishi M, Sato H, Goda T, Takase S: Enhanced absorption of calcium after oral administration of maltitol in the rat intestine. J Pharm Pharmacol 50:1227–1232, 1998Google Scholar
  9. 9.
    Goda T, Takase S, Hosoya N: Maltitol-induced increase of transepithelial transport of calcium in rat small intestine. J Nutr Sci Vitaminol (Tokyo) 39:589–595, 1993Google Scholar
  10. 10.
    Suzuki T, Hara H, Kasai T, Tomita F: Effects of difructose anhydride III on calcium absorption in small and large intestines of rats. Biosci Biotechnol Biochem 62:837–841, 1998Google Scholar
  11. 11.
    Saito K, Hira T, Suzuki T, Hara H, Yokota A, Tomita F: Effects of DFA IV in rats: Calcium absorption and metabolism of DFA IV by intestinal microorganisms. Biosci Biotechnol Biochem 63:655–661, 1999Google Scholar
  12. 12.
    Hara H, Suzuki T, Aoyama Y: Ingestion of the soluble fiber, polydextrose, increases calcium absorption and bone mineralization in normal and total-gastrectomized rats. Br J Nutr 84:1–8, 2000Google Scholar
  13. 13.
    Bronner F: Calcium absorption-A paradigm for mineral absorption. J Nutr 128:917–920, 1998Google Scholar
  14. 14.
    Ballard ST, Hunter JH, Taylor AE: Regulation of tight-junction permeability during nutrient absorption across the intestinal epithelium. Annu Rev Nutr 15:35–55, 1995Google Scholar
  15. 15.
    Mineo H, Hara H, Kikuchi H, Sakurai H, Tomita F: Various indigestible saccharides enhance net calcium transport from the epithelium of the small and large intestine of rats in vitro. J Nutr 131:3243–3246, 2001Google Scholar
  16. 16.
    Mineo H, Hara H, Shigematsu N, Okuhara Y, Tomita F: Melibiose, difructose anhydride III and difructose anhydride IV enhance net calcium absorption in rat small and large intestinal epithelium by increasing the passage of tight junctions in vitro. J Nutr 132:3394–3349, 2002Google Scholar
  17. 17.
    Behling AR, Greger JL: Importance for lacutulosein yogurt for mineral utilization. J Agr Food Chem 38:200–204, 1990Google Scholar
  18. 18.
    Delzenne N, Aertssens J, Verplaetse H, Roccaro M, Roberfroid M: Effect of fermentable fructo-oligosaccharides on mineral, nitrogen and energy digestive balance in the rat. Life Sci 57:1579–1587, 1995Google Scholar
  19. 19.
    Kashimura J, Kimura M, Itokawa Y: The effects of isomaltulose, isomalt, and isomaltulose-based oligomers on mineral absorption and retention. Biol Trace Elem Res 54:239–250, 1996Google Scholar
  20. 20.
    Hidalgo IJ, Hillgren KM, Grass GM, Borchardt RT: Characterization of the unstirred water layer in Caco-2 cell monolayers using a novel diffusion apparatus. Pharm Res 8:222–227, 1991Google Scholar
  21. 21.
    Rada V, Petr JJ: A new selective medium for the isolation of glucose non-fermenting bifidobacteria from hen caeca. J Microbiol Methods 43:127–132, 2000Google Scholar
  22. 22.
    Hashimoto K, Matsunaga N, Shimizu M.: Effect of vegetable extracts on the transepithelial permeability of the human intestinal caco-2 cell monolayer. Biosci Biotechnol Biochem 58:1345–1346, 1994Google Scholar
  23. 23.
    Shimazaki T, Tomita M, Sadahiro S, Hayashi M, Awazu S: Absorption-enhancing effects of sodium caprate and palmitoyl carnitine in rat and human colons. Dig Dig Sci 43:641–645, 1998Google Scholar
  24. 24.
    Schweigel M, Martens H: Magnesium transport in the gastrointestinal tract. Front Biosci 5:D666–D677, 2000Google Scholar
  25. 25.
    Chutkow JG: Sites of magnesium absorption and excretion in the intestinal tract of the rat. J Lab Clin Med 63:71–79, 1964Google Scholar
  26. 26.
    Ross DB: In vitro studies on the transport of magnesium across the intestinal wall of the rat. J Physiol (London) 160:417–428, 1962Google Scholar
  27. 27.
    Sharrer E, Lutz T: Effects of short chain fatty acids and K on absorption of Mg and other cations by the colon and ceacum. Z Ernaehrungswiss 29:162–168, 1990Google Scholar
  28. 28.
    Simon DB, Lu Y, Choate KA, Velazquez H, Al-Sabban E, Praga M, Casari G, Bettinelli A, Colussi G, Rodriguez-Soriano J, McCredie D, Milford D, Sanjad S, Lifton RP: Paracellin-1, a renal tight junction protein required for paracellular Mg2+ resorption science 285:103–106, 1999Google Scholar
  29. 29.
    Hempe JM, Cousins RJ: Cystein-rich intestinal portion and intestinal metallothionein: an inverse relationships as a conceptual model for zinc absorption in rats. J Nutr 122:89–95, 1992Google Scholar
  30. 30.
    Antonson DL, Barak AJ, Vanderhoof JA: Determination of the site of zinc absorption in rat small intestine. J Nutr 109:142–147, 1979Google Scholar
  31. 31.
    Seal CJ, Mathers JC: Intestinal zinc transfer by everted gut sacs from rats given diets containing different amounts and types of dietary fiber. Br J Nutr 62:153–163, 1989Google Scholar
  32. 32.
    Hara H, Konishi A, Kasai T: Contribution of the cecum and colon to zinc absorption in rats. J Nutr 130:83–89, 2000Google Scholar
  33. 33.
    McMahon RJ, Cousins RJ: Regulation of zinc transporter ZnT-1 by dietary zinc. Proc Natl Acad Sci USA 95:4841–4846, 1998Google Scholar
  34. 34.
    Duflos C, Bellaton C, Pansu D, Bronner F: Calcium solubility, intestinal sojourn time and paracellular permeability codetermine passive calcium absorption in rats. J Nutr 125:2348–2355, 1995Google Scholar
  35. 35.
    Younes H, Demigne C, Remesy C: Acidic fermentation in the caecum increases absorption of calcium and magnesium in the large intestine of the rat. Br J Nutr 75:301–314, 1996Google Scholar
  36. 36.
    Levrat MA, Remesy C, Demigne C: High propionic acid fermentation and mineral accumulation in the cecum of rats adapted to different levels of inulin. J Nutr 121:1730–1737, 1991Google Scholar
  37. 37.
    Karbach U, Feldmeier H: The cecum is the site with the highest calcium absorption in rat intestine. Dig Dis Sci 38:1815–1824, 1993Google Scholar
  38. 38.
    Hara H, Haga S, Kasai T, Kiriyama S: Fermentation products of sugar-beet fiber by cecal bacteria lower plasma cholesterol concentration in rats. J Nutr 128:688–693, 1998Google Scholar
  39. 39.
    Fowler N, Gonzalez E, Rawlins FA, Giebisch GH, Whittembury G: Effect of hypertonic urea and mannitol on distal nephron permeability. Pflugers Arch 368:3–11, 1977Google Scholar
  40. 40.
    DiBona DR.: Functional analysis of tight junction organization. Pflugers Arch 405 (Suppl 1):S59–S66, 1985Google Scholar
  41. 41.
    Terada Y, Inoshita S, Hanada S, Shimamura H, Kuwahara M, Ogawa W, Kasuga M, Sasaki S, Marumo F: Hyperosmolality activates Akt and regulates apoptosis in renal tubular cells. Kidney Int 60:553–567, 2001Google Scholar
  42. 42.
    Mineo H, Hara H, Tomita F: Short-chain fatty acids enhance diffusional Ca transport in the epithelium of the rat cecum and colon. Life Sci 69:517–526, 2001Google Scholar
  43. 43.
    Ferraris RP, Yasharpour S, Lloyd KC, Mirzayan R Diamond JM: Luminal glucose concentrations in the gut under normal conditions. Am J Physiol 259:G822–G837, 1990Google Scholar
  44. 44.
    Hashimoto K, Matsunaga N, Shimizu M: Effects of ß-lactogloblin on the tihgt-junctional stability of Caco-2-SF monolayer. Biosci Biotechnol Biochem 62:1819–1821, 1998Google Scholar
  45. 45.
    Jensen-Jarolim E, Gajdzik L, Haber I, Kraft D, Scheiner O, Graf J: Hot spices influence permeability of human intestinal epithelial monolayers. J Nutr 128:577–581, 1998Google Scholar
  46. 46.
    Karczewski H, Groot J: Molecular physiology and pathophysiology of tight junctions. III. Tight junction regulation by intracellular messengers: differences in response within and between epithelia. Am J Physiol 297:G660–G665, 2000Google Scholar
  47. 47.
    Kishi K, Goda T, Takase S: Maltitol increases transepithelial diffusional transfer of calcium in rat ileum. Life Sci 59:1133–1140, 1996Google Scholar

Copyright information

© Plenum Publishing Corporation 2004

Authors and Affiliations

  • Hitoshi Mineo
    • 1
    • 2
  • Midori Amano
    • 1
    • 3
  • Hideyuki Chiji
    • 3
  • Norihiro Shigematsu
    • 4
  • Fusao Tomita
    • 2
  • Hiroshi Hara
    • 2
  1. 1.Northern Advancement Center for Science and TechnologyColabo-Hokkaido, Sapporo
  2. 2.Division of Applied Bioscience, Graduate School of AgricultureHokkaido UniversitySapporoJapan
  3. 3.Department of Food Science and Human Nutrition, Faculty of Human Life ScienceFuji Women's UniversityIshikari
  4. 4.Central Research CenterFancl CorporationYokohama

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