Sugars increase non-heme iron bioavailability in human epithelial intestinal and liver cells

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Christides, Tatiana ^a   Sharp, Paul ^b  

^a UNIVERSITY OF GREENWICH   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FERRITIN; FRUCTOSE; GLUCOSE; NONHEME IRON PROTEIN; PHYTIC ACID; SUCROSE; TANNIN;

ARTICLE; BIOAVAILABILITY; CELL LEVEL; CELL MIGRATION; CELL STRAIN CACO 2; CELL STRAIN HEPG2; CONTROLLED STUDY; DIET; EPITHELIUM CELL; HOMEOSTASIS; HUMAN; HUMAN CELL; IN VITRO STUDY; IRON METABOLISM; IRON TRANSPORT; LIVER CELL; OXIDATION; PROTEIN ANALYSIS;

BIOLOGICAL AVAILABILITY; CACO-2 CELLS; DIETARY SUCROSE; EPITHELIUM; FERRITINS; FERROZINE; FRUCTOSE; GLUCOSE; HEP G2 CELLS; HUMANS; INTESTINES; IRON; LIVER; NUTRITIVE SWEETENERS; PHYTIC ACID; SUCROSE; TANNINS; ZEA MAYS;

EID: 84892401421     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0083031     Document Type: Article

References (73)

1. Charley PJ, Sarkar B, Stitt CF, Saltman P (1963) Chelation of Iron by Sugars. Biochim Biophys Acta 69: 313-321.
2. Charley PJ, Stitt C, Shore E, Saltman P (1963) Studies in the Regulation of Intestinal Iron Absoprtion. J Lab Clin Med 61: 397-410.
3. Pollack S, Kaufman RM, Crosby WH (1964) Iron Absorption: Effects of Sugars and Reducing Agents. Blood 24: 577-581.
4. McLean E, Cogswell M, Egli I, Wojdyla D, de Benoist B (2009) Worldwide prevalence of anaemia, WHO Vitamin and Mineral Nutrition Information System, 1993-2005. Public Health Nutr 12: 444-454.
5. Wood MJ, Skoien R, Powell LW (2009) The global burden of iron overload. Hepatol Int 3: 434-444.
6. Fleming RE, Ponka P (2012) Iron overload in human disease. N Engl J Med 366: 348-359.
7. Brissot P, Ropert M, Le Lan C, Loreal O (2012) Non-transferrin bound iron: A key role in iron overload and iron toxicity. Biochim Biophys Acta 1820: 403-410.
8. O'Brien J, Powell LW (2012) Non-alcoholic fatty liver disease: is iron relevant? Hepatol Int 6: 332-341.
9. Fujita N, Takei Y (2011) Iron overload in nonalcoholic steatohepatitis. Adv Clin Chem 55: 105-132.
10. Gunshin H, Mackenzie B, Berger UV, Gunshin Y, Romero MF, et al. (1997) Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 388: 482-488.
11. Tandy S, Williams M, Leggett A, Lopez-Jimenez M, Dedes M, et al. (2000) Nramp2 expression is associated with pH-dependent iron uptake across the apical membrane of human intestinal Caco-2 cells. J Biol Chem 275: 1023-1029.
12. Montalbetti N, Simonin A, Kovacs G, Hediger MA (2013) Mammalian iron transporters: families SLC11 and SLC40. Mol Aspects Med 34: 270-287.
13. McKie AT, Barrow D, Latunde-Dada GO, Rolfs A, Sager G, et al. (2001) An iron-regulated ferric reductase associated with the absorption of dietary iron. Science 291: 1755-1759.
14. Carpenter CE, Mahoney AW (1992) Contributions of heme and nonheme iron to human nutrition. Crit Rev Food Sci Nutr 31: 333-367.
15. Davis PS, Deller DJ (1967) Effect of Orally Administered Chelating Agents EDTA, DTPA and Fructose on Radioiron Absorption in Man. Australas Ann Med 16: 70-74.
16. Roza MPd, VanCampen D, Miller D (1986) Effects of some carbohydrates on iron absorption. Arch Latinoam Nutr 36: 688-700.
17. Holbrook JT, Smith JC Jr, Reiser S (1989) Dietary fructose or starch: effects on copper, zinc, iron, manganese, calcium, and magnesium balances in humans. Am J Clin Nutr 49: 1290-1294.
18. Pollack S, Kaufman RM, Crosby WH (1964) Iron Absorption: Effects of Sugars and Reducing Agents. Blood 24: 577-581.
19. Bates GW, Boyer J, Hegenauer JC, Saltman P (1972) Facilitation of iron absorption by ferric fructose. Am J Clin Nutr 25: 983-986.
20. Brodan V, Brodanova M, Kuhn E, Kordac V, Valek J (1967) [Effect on the absorption of iron from the digestive system of simultaneous absorption of nutrients. 3. Effect of fructose]. Cesk Gastroenterol Vyz 21: 521-525.
21. Beynen AC, Brouwer IA, Lemmens AG (1992) Dietary Fructose vs Glucose Does Not Influence Iron Status in Rats. Biological Trace Element Research 35: 89-92.
22. Heinrich HC, Gabbe EE, Bruggemann J, Oppitz KH (1974) Effects of fructose on ferric and ferrous iron absorption in man. Nutr Metab 17: 236-248.
23. Ivaturi R, Kies C (1992) Mineral balances in humans as affected by fructose, high fructose corn syrup and sucrose. Plant Food Hum Nutr 42: 143-151.
24. Brouwer IA, Lemmens AG, Beynen AC (1993) Dietary fructose v. glucose lowers ferrous-iron absorption in rats. British Journal of Nutrition 70: 171-178.
25. O'Dell BL (1993) Fructose and mineral metabolism. Am J Clin Nutr 58(S): 771S-778S.
26. Ogden CL, Kit BK, Carroll MD, Park S (2011) Consumption of Sugar Drinks in the United States, 2005-2008. National Center for Health Statistics data brief 71: 1-8.
27. Whitton C, Nicholson SK, Roberts C, Prynne CJ, Pot GK, et al. (2011) National Diet and Nutrition Survey: UK food consumption and nutrient intakes from the first year of the rolling programme and comparisons with previous surveys. Br J Nutr 106: 1899-1914.
28. White JS (2008) Straight talk about high-fructose corn syrup: what it is and what it ain't. Am J Clin Nutr 88: 1716S-1721S.
29. Yun S, Habicht JP, Miller DD, Glahn RP (2004) An in vitro digestion/Caco-2 cell culture system accurately predicts the effects of ascorbic acid and polyphenolic compounds on iron bioavailability in humans. J Nutr 134: 2717-2721.
30. Scheiber-Mojdehkar B, Sturm B, Plank L, Kryzer I, Goldenberg H (2003) Influence of parenteral iron preparations on non-transferrin bound iron uptake, the iron regulatory protein and the expression of ferritin and the divalent metal transporter DMT-1 in HepG2 human hepatoma cells. Biochem Pharmacol 65: 1973-1978.
31. Hubert N, Lescoat G, Sciot R, Moirand R, Jego P, et al. (1993) Regulation of ferritin and transferrin receptor expression by iron in human hepatocyte cultures. J Hepatol 18: 301-312.
32. Gangloff MB, Lai C, Van Campen DR, Miller DD, Norvell WA, et al. (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.
33. Sturm B, Goldenberg H, Scheiber-Mojdehkar B (2003) Transient increase of the labile iron pool in HepG2 cells by intravenous iron preparations. Eur J Biochem 270: 3731-3738.
34. Glahn RP, Lee OA, Yeung A, Goldman MI, Miller DD (1998) Caco-2 cell ferritin formation predicts nonradiolabeled food iron availability in an in vitro digestion/Caco-2 cell culture model. J Nutr 128: 1555-1561.
35. Lung'aho MG, Mwaniki AM, Szalma SJ, Hart JJ, Rutzke MA, et al. (2011) Genetic and physiological analysis of iron biofortification in maize kernels. PLoS One 6: e20429.
36. Wawer AA, Sharp PA, Perez-Moral N, Fairweather-Tait SJ (2012) Evidence for an enhancing effect of alginate on iron availability in Caco-2 cells. J Agric Food Chem 60: 11318-11322.
37. Pullakhandam R, Nair KM, Pamini H, Punjal R (2011) Bioavailability of iron and zinc from multiple micronutrient fortified beverage premixes in Caco-2 cell model. J Food Sci 76: H38-42.
38. Beiseigel JM, Hunt JR, Glahn RP, Welch RM, Menkir A, et al. (2007) Iron bioavailability from maize and beans: a comparison of human measurements with Caco-2 cell and algorithm predictions. Am J Clin Nutr 86: 388-396.
39. Caro I BX, Rousset M, Meunier V, Bourrie M, Julian B, Joyeux H, Roques C, Berger Y, Zweibaum A, Fabre G (1995) Characterisation of a newly isolated Caco-2 clone (TC-7), as a model of transport processes and biotransformation of drugs. Int J Pharm 116: 147-158.
40. Chantret I, Rodolosse A, Barbat A, Dussaulx E, Brot-Laroche E, et al. (1994) Differential expression of sucrase-isomaltase in clones isolated from early and late passages of the cell line Caco-2: evidence for glucose-dependent negative regulation. J Cell Sci 107: 213-225.
41. Sharp P, Tandy S, Yamaji S, Tennant J, Williams M, et al. (2002) Rapid regulation of divalent metal transporter (DMT1) protein but not mRNA expression by non-haem iron in human intestinal Caco-2 cells. FEBS Lett 510: 71-76.
42. Jumarie C, Malo C (1991) Caco-2 cells cultured in serum-free medium as a model for the study of enterocytic differentiation in vitro. J Cell Physiol 149: 24-33.
43. Boato F, Wortley GM, Liu RH, Glahn RP (2002) Red Grape Juice Inhibits Iron Availability: Application of an in Vitro Digestion/Caco-2 Cell Model. J Agric Food Chem 50: 6935-6938.
44. Riemer J, Hoepken HH, Czerwinska H, Robinson SR, Dringen R (2004) Colorimetric ferrozine-based assay for the quantitation of iron in cultured cells. Anal Biochem 331: 370-375.
45. Sturm B, Laggner H, Ternes N, Goldenberg H, Scheiber-Mojdehkar B (2005) Intravenous iron preparations and ascorbic acid: effects on chelatable and bioavailable iron. Kidney Int 67: 1161-1170.
46. Motulsky H (2010) Intuitive Biostatistics. Oxford, UK: Oxford University Press.
47. Stitt C, Charley PJ, Butt EM, Saltman P (1962) Rapid induction of iron deposition in spleen and liver with an iron-fructose chelate. Proc Soc Exp Biol Med 110: 70-71.
48. Milward EA, Baines SK, Knuiman MW, Bartholomew HC, Divitini ML, et al. (2008) Noncitrus fruits as novel dietary environmental modifiers of iron stores in people with or without HFE gene mutations. Mayo Clin Proc 83: 543-549.
49. Fleming DJ, Tucker KL, Jacques PF, Dallal GE, Wilson PW, et al. (2002) Dietary factors associated with the risk of high iron stores in the elderly Framingham Heart Study cohort. Am J Clin Nutr 76: 1375-1384.
50. Marriott BP, Olsho L, Hadden L, Connor P (2010) Intake of added sugars and selected nutrients in the United States, National Health and Nutrition Examination Survey (NHANES) 2003-2006. Crit Rev Food Sci Nutr 50: 228-258.
51. Heckman MA, Sherry K, Mejia EGd (2010) Consumption of Sugar Drinks in the United States, 2005-2008. Compr Rev Food Sci F 9: 303-317.
52. Hallberg L, Rossander L (1982) Effect of different drinks on the absorption of non-heme iron from composite meals. Hum Nutr Appl Nutr 36: 116-123.
53. Collings R, Fairweather-Tait SJ, Dainty JR, Roe MA (2011) Low-pH cola beverages do not affect women's iron absorption from a vegetarian meal. J Nutr 141: 805-808.
54. Coca-Cola Great Brittain website. Available: http://www.coca-cola.co.uk/ faq/ingredients/how-much-caffeine-is-in-diet-coke-coca-cola-and-coke-zero.html. Accessed 2013 May 26.
55. Gillooly M, Bothwell TH, Torrance JD, MacPhail AP, Derman DP, et al. (1983) The effects of organic acids, phytates and polyphenols on the absorption of iron from vegetables. Br J Nutr 49: 331-342.
56. Glahn RP, Wortley GM, South PK, Miller DD (2002) Inhibition of iron uptake by phytic acid, tannic acid, and ZnCl2: studies using an in vitro digestion/Caco-2 cell model. J Agric Food Chem 50: 390-395.
57. Riby JE, Fujisawa T, Kretchmer N (1993) Fructose absorption. Am J Clin Nutr 58: 748S-753S.
58. Timson DJ (2012) Fructose Chemistry. In: Preedy VR, editor. Dietary Sugars. 1st ed. Cambridge, UK: The Royal Society of Chemistry: 115-135.
59. Verstraeten LM (1967) D-fructose and its derivatives. Adv Carbohydr Chem Biochem 22: 229-305.
60. Moreira LM LJ, Lima P, Santos V, Santos FV (2012) Sucrose chemistry. In: Preedy VR, editor. Dietary Sugars. 1st ed. Cambridge, UK: The Royal Society of Chemistry: 138-148.
61. Tsuchiya H, Ebata Y, Sakabe T, Hama S, Kogure K, et al. (2013) High-fat, high-fructose diet induces hepatic iron overload via a hepcidin-independent mechanism prior to the onset of liver steatosis and insulin resistance in mice. Metabolism 62: 62-69.
62. Hui H, Huang D, McArthur D, Nissen N, Boros LG, et al. (2009) Direct spectrophotometric determination of serum fructose in pancreatic cancer patients. Pancreas 38: 706-712.
63. Mayes PA (1993) Intermediary metabolism of fructose. Am J Clin Nutr 58: 754S-765S.
64. Dencker H, Lunderquist A, Meeuwisse G, Norryd C, Tranberg KG (1972) Absorption of fructose as measured by portal catheterization. Scand J Gastroenterol 7: 701-705.
65. Dencker H, Meeuwisse G, Norryd C, Olin T, Tranberg KG (1973) Intestinal transport of carbohydrates as measured by portal catheterization in man. Digestion 9: 514-524.
66. Niewoehner CB (1986) Metabolic effects of dietary versus parenteral fructose. J Am Coll Nutr 5: 443-450.
67. Holdsworth CD, Dawson AM (1965) Absorption of Fructose in Man. Proc Soc Exp Biol Med 118: 142-145.
68. Gkouvatsos K, Papanikolaou G, Pantopoulos K (2012) Regulation of iron transport and the role of transferrin. Biochim Biophys Acta 1820: 188-202.
69. Graham RM, Chua ACG, Trinder D (2012) Plasma Iron and Iron Delivery to the Tissues. In: Anderson GJ, McLaren GD, editors. Iron Physiology and Pathophysiology in Humans. London: Humana Press: 117-139.
70. Deugnier Y, Turlin B (2011) Pathology of hepatic iron overload. Semin Liver Dis 31: 260-271.
71. Hider RC (2002) Nature of nontransferrin-bound iron. Eur J Clin Invest 32 Suppl 1: 50-54.
72. Baker E, Baker SM, Morgan EH (1998) Characterisation of non-transferrin-bound iron (ferric citrate) uptake by rat hepatocytes in culture. Biochim Biophys Acta 1380: 21-30.
73. Wright TL, Brissot P, Ma WL, Weisiger RA (1986) Characterization of non-transferrin-bound iron clearance by rat liver. J Biol Chem 261: 10909-10914.