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Lactic acid fermentation stimulated iron absorption by Caco-2 cells is associated with increased soluble iron content in carrot juice

Published online by Cambridge University Press:  08 March 2007

Sharon W. Bergqvist ,
Thomas Andlid  and
Ann-Sofie Sandberg
Sharon W. Bergqvist*
Affiliation:
Department of Chemical and Biological Engineering/Food Science, Chalmers University of Technology, Box 5401, 402 29, Gothenburg, Sweden
Thomas Andlid
Affiliation:
Department of Chemical and Biological Engineering/Food Science, Chalmers University of Technology, Box 5401, 402 29, Gothenburg, Sweden
Ann-Sofie Sandberg
Affiliation:
Department of Chemical and Biological Engineering/Food Science, Chalmers University of Technology, Box 5401, 402 29, Gothenburg, Sweden
*
*Corresponding author: Dr S. W. Bergqvist, fax +46 31 833782, email [email protected]
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Abstract

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An in vitro digestion/Caco-2 cell model was applied to explore the impact of lactic acid (LA) fermentation by Lactobacillus pentosus FSC1 and Leuconostoc mesenteroides FSC2 on the Fe bioavailability of carrot juice. The redox state of Fe in fermented carrot juice was also assessed as a crucial factor for absorption. LA fermentation was shown to improve mineral solubility to different extents at simulated physiological conditions: Mn (2-fold); Fe (1·5–1·7-fold); Zn (1·2-fold); Cu (1-fold). Soluble Fe2+ was increased about 16-fold by LA fermentation, and about one third of the Fe2+ remained soluble after in vitro digestion (about 4–5-fold higher than in fresh juice). Data on cell-line studies showed a 4-fold increase in the efficiency of Fe uptake, but not in transepithelial transfer by Caco2 cells, as a result of fermentation. The increases in Fe2+ level and the efficiency of cellular Fe uptake were strain-dependent. To sum up the effect on both Fe solubility and cellular uptake efficiency, the amount of cellularly absorbed Fe from Ln. mesenteroides FSC2-fermented juice was about 20 % higher than that from L. pentosus FSC1-fermented juice (22·7 v. 19·2 μg/l juice per mg protein). To conclude, LA fermentation enhanced Fe absorption by Caco-2 cells from carrot juice because of increases in not only Fe solubility after digestion, but also the efficiency of cellular Fe uptake. The fermentation-improved efficiency of Fe uptake was possibly due to the increased level of soluble Fe2+ rather than a being a strain-specific event.

Keywords

Iron absorptionIron redox stateCaco-2 cellsLactic acid fermentation
Type
Research Article
Information
British Journal of Nutrition , Volume 96 , Issue 4 , October 2006 , pp. 705 - 711
Copyright
Copyright © The Nutrition Society 2006

References

Alasalvar, C, Grigor, JM, Zhang, D, Quantick, PC & Shahidi, F (2001) Comparison of volatiles, phenolics, sugars, antioxidant vitamins, and sensory quality of different colored carrot varieties. J Agric Food Chem 49, 1410–1416.CrossRefGoogle ScholarPubMed
Alvarez-Hernandez, X, Nichols, GM & Glass, J (1991) Caco-2 cell line: a system for studying intestinal iron transport across epithelial cell monolayers. Biochim Biophys Acta 18, 205–208.CrossRefGoogle Scholar
Archibald, F (1986) Manganese: its acquisition by and function in the lactic acid bacteria. Crit Rev Microbiol 13, 63–109.Google Scholar
Arredondo, M, Orellana, A, Garate, MA & Nunez, MT (1997) Intracellular iron regulates iron absorption and IRP activity in intestinal epithelial (Caco-2) cells. Am J Physiol 273, G275–G280.Google ScholarPubMed
Au, AP & Reddy, MB (2000) Caco-2 cells can be used to assess human iron bioavailability from a semipurified meal. J Nutr 130, 1329–1334.Google Scholar
Avron, M (1963) A sensitive and simple method for determination of ferrocyanide. Anal Biochem 6, 549–554.CrossRefGoogle ScholarPubMed
Beard, JL, Dawson, H & Pinero, DJ (1996) Iron metabolism: a comprehensive review. Nutr Rev 54, 295–317.CrossRefGoogle ScholarPubMed
Bergqvist, SW, Sandberg, AS, Andlid, T, Wessling-Resnick, M (2005 a) Lactic acid decreases Fe(II) and Fe(III) retention but increases Fe(III) transepithelial transfer by Caco-2 cells. J Agric Food Chem 53, 6919–6923.CrossRefGoogle ScholarPubMed
Bergqvist, SW, Sandberg, A-S, Carlsson, N-G & Andlid, T (2005 b) Improved iron solubility in carrot juice fermented by homo- and hetero-fermentative lactic acid bacteria. Food Microbiology 22, 53–61.CrossRefGoogle Scholar
Brune, M, Hallberg, L & Skånberg, A-B (1991) Determination of iron-binding phenolic groups in foods. J Food Sci 56, 128–131 167Google Scholar
Cowart, RE, Singleton, FL & Hind, JS (1993) A comparison of bathophenanthrolinedisulfonic acid and ferrozine as chelators of iron(II) in reduction reactions. Anal Biochem 211, 151–155.CrossRefGoogle ScholarPubMed
Fernandez, M, Sun, D, Tosca, M & Mc-Namara, D (1995) Guar gum effects on plasma low-density lipoprotein and hepatic cholesterol metabolism in guinea pigs fed low- and high-cholesterol diets: a dose-response study. Am J Clin Nutr 61, 127–134.CrossRefGoogle Scholar
Fredrikson, M, Carlsson, NG, Almgren, A & Sandberg, AS (2002) Simultaneous and sensitive analysis of Cu, Ni, Zn, Co, Mn, and Fe in food and biological samples by ion chromatography. J Agric Food Chem 50, 59–65.Google Scholar
Gangloff, MB, Lai, C, Van Campen, DR, Miller, DD, Norvell, WA & Glahn, RP (1996) Ferrous iron uptake but not transfer is down-regulated in Caco-2 cells grown in high iron serum-free medium. J Nutr 126, 3118–3127.Google Scholar
Garcia-Casal, MN, Leets, I & Layrisse, M (2000) Beta-carotene and inhibitors of iron absorption modify iron uptake by Caco-2 cells. J Nutr 130, 5–9.Google Scholar
Garrick, MD, Dolan, KG & Horbinski, C (2003) DMT1: a mammalian transporter for multiple metals. Biometals 16, 41–54.Google Scholar
Gillooly, M, Bothwell, TH, Torrance, JD, MacPhail, AP, Derman, DP, Bezwoda, WR, Mills, W, Charlton, RW & Mayet, F (1983) The effects of organic acids, phytates and polyphenols on the absorption of iron from vegetables. Br J Nutr 49, 331–342.CrossRefGoogle ScholarPubMed
Glahn, RP, Lai, C, Hsu, J, Thompson, JF, Guo, M, Van Campen, DR (1998) Decreased citrate improves iron availability from infant formula: application of an in vitro digestion/Caco-2 cell culture model. J Nutr 128, 257–264.CrossRefGoogle ScholarPubMed
Gunshin, H, Mackenzie, B, Berger, UV, Gunshin, Y, Romero, MF, Boron, WF, Nussberger, S, Gollan, JL & Hediger, MA (1997) Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 388, 482–488.Google Scholar
Hallberg, L, Brune, M & Rossander, L (1989) The role of vitamin C in iron absorption. Int J Vitam Nutr Res Suppl 30, 103–108.Google Scholar
Han, O, Failla, ML, Hill, AD, Morris, ER, Smith, JC Jr (1994) Inositol phosphates inhibit uptake and transport of iron and zinc by a human intestinal cell line. J Nutr 124, 580–587.CrossRefGoogle ScholarPubMed
Han, O, Failla, ML, Hill, AD, Morris, ER, Smith, JC Jr (1995) Reduction of Fe(III) is required for uptake of nonheme iron by Caco-2 cells. J Nutr 125, 1291–1299.Google Scholar
Hurrell, RF, Reddy, M & Cook, JD (1999) Inhibition of non-haem iron absorption in man by polyphenolic-containing beverages. Br J Nutr 81, 289–295.Google Scholar
Ito, M, Ohishi, K, Yoshida, Y, Yokoi, W & Sawada, H (2003) Antioxidative effects of lactic acid bacteria on the colonic mucosa of iron-overloaded mice. J Agric Food Chem 51, 4456–4460.Google Scholar
Lee, J, Hwang, KT, Heo, MS, Lee, JH & Park, KY (2005) Resistance of Lactobacillus plantarum KCTC 3099 from kimchi to oxidative stress. J Med Food 8, 299–304.Google Scholar
Lin, M-Y, Yen, C-L (1999) Antioxidative ability of lactic acid bacteria. J Agric Food Chem 47, 1460–1466.Google Scholar
Mazur, A, Remesy, C, Gueux, E, Levrat, MA & Demigne, C (1990) Effects of diets rich in fermentable carbohydrates on plasma lipoprotein levels and on lipoprotein catabolism in rats. J Nutr 120, 1037–1045.Google Scholar
Miller, NJ, Sampson, J, Candeias, LP, Bramley, PM, Rice-Evans, CA (1996) Antioxidant activities of carotenes and xanthophylls. FEBS Lett 384, 240–242.CrossRefGoogle ScholarPubMed
Narasinga Rao, BS & Subba, Rao, K (1992) Studies on the role of iron binding ligands and the intestinal brush border receptors in iron absorption. Indian J Biochem 29, 214–218.Google Scholar
National Food Administration (2002) The NORBAGREEN 2002 study: Consumption of vegetables, potatoes, fruit, bread and fish in the Nordic and Baltic countries. TemaNord 2003, 556Google Scholar
Nunez, MT, Alvarez, X, Smith, M, Tapia, V & Glass, J (1994) Role of redox systems on Fe3+ uptake by transformed human intestinal epithelial (Caco-2) cells. Am J Physiol 267, C1582–C1588.Google Scholar
Pandey, A, Bringel, F & Meyer, J (1994) Iron requirement and search for siderophores in lactic acid bacteria. Appl Microbiol Biotechnol 40, 735–739.CrossRefGoogle Scholar
Rice-Evans, CA, Miller, NJ & Paganga, G (1996) Structure-antioxidant activity relationships of flavonoids and phenolic acids. Free Radic Biol Med 20, 933–956.Google Scholar
Stiles, ME (1996) Biopreservation by lactic acid bacteria. Antonie Van Leeuwenhoek 70, 331–345.Google Scholar
Svanberg, U, Lorri, W, Sandberg, A-S (1993) Lactic fermentation of non-tannin and high-tannin cereals: effects on in vitro estimation of iron availability and phytate hydrolysis. J Food Sci 58, 408–412.Google Scholar
Teucher, B, Olivares, M & Cori, H (2004) Enhancers of iron absorption: ascorbic acid and other organic acids. Int J Vitam Nutr Res 74, 403–419.CrossRefGoogle ScholarPubMed
Torsdottir, I, Alpsten, M, Holm, G, Sandberg, A-S, Tölli, J (1991) A small dose of soluble alginate-fiber affects postprandial glycemia and gastric emptying in humans with diabetes. J Nutr 121, 795–799.Google Scholar
Torsdottir, I, Blomqvist, R, Ekman, R, Hagander, B, Sandberg, A-S (1992) Fermented or fresh vegetables decrease the postprandial blood glucose and insulin levels in health persons. Scand J Nutr 36, 4–7.Google Scholar
Umbreit, J (2005) Iron deficiency: a concise review. Am J Hematol 78, 225–231.Google Scholar
Wollenberg, P & Rummel, W (1987) Dependence of intestinal iron absorption on the valency state of iron. Naunyn Schmiedebergs Arch Pharmacol 336, 578–582.Google Scholar
Wood, RJ & Han, O (1998) Recently identified molecular aspects of intestinal iron absorption. J Nutr 128, 1841–1844.Google Scholar
Yeung, CK, Glahn, RP & Miller, DD (2005) Inhibition of iron uptake from iron salts and chelates by divalent metal cations in intestinal epithelial cells. J Agric Food Chem 53, 132–136.Google Scholar