High-fat diet causes iron deficiency via hepcidin-independent reduction of duodenal iron absorption

Journal of Nutritional Biochemistry

Volumn 23, Issue 12, 2012, Pages 1600-1608

  Sonnweber, Thomas ^a   Ress, Claudia ^a   Nairz, Manfred ^a   Theurl, Igor ^a   Schroll, Andrea ^a   Murphy, Anthony T ^b   Wroblewski, Victor ^b   Witcher, Derrick R ^b   Moser, Patrizia ^c   Ebenbichler, Christoph F ^a   Kaser, Susanne ^a   Weiss, Günter ^a  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b ELI LILLY AND COMPANY   (United States)

^c MEDICAL UNIVERSITY OF INNSBRUCK   (Austria)

Author keywords

Hepcidin; Iron homeostasis; Iron rich diet; Obesity; Oxidoreductases

Indexed keywords

ADIPOCYTOKINE; HEPCIDIN; HEPHAESTIN; IRON BINDING PROTEIN; OXIDOREDUCTASE;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CALORIC INTAKE; CONTROLLED STUDY; DIET SUPPLEMENTATION; DUODENUM; HOMEOSTASIS; HUMAN; INTESTINE CELL; IRON ABSORPTION; IRON DEFICIENCY; IRON INTAKE; IRON TRANSPORT; LIPID DIET; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; RETICULOENDOTHELIAL SYSTEM;

ADIPOKINES; ADIPOSE TISSUE; ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; CATION TRANSPORT PROTEINS; DIET, HIGH-FAT; DUODENUM; ERYTHROCYTES; GENE EXPRESSION REGULATION; INTESTINAL ABSORPTION; IRON; IRON, DIETARY; LIVER; MALE; MICE; MICE, INBRED C57BL; OBESITY; RECEPTORS, TRANSFERRIN;

ANIMALIA; MUS;

EID: 84869088411     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2011.10.013     Document Type: Article

References (46)

1. McClung J.P., Karl J.P. Iron deficiency and obesity: the contribution of inflammation and diminished iron absorption. Nutr Rev 2009, 67:100-104.
2. Lecube A., Carrera A., Losada E., Hernandez C., Simo R., Mesa J. Iron deficiency in obese postmenopausal women. Obesity (Silver Spring) 2006, 14:1724-1730.
3. Zafon C., Lecube A., Simo R. Iron in obesity. An ancient micronutrient for a modern disease. Obes Rev 2010, 11:322-328.
4. Weiss G. Iron metabolism in the anemia of chronic disease. Biochim Biophys Acta 2009, 1790:682-693.
5. Zimmermann M.B., Zeder C., Muthayya S., Winichagoon P., Chaouki N., Aeberli I., et al. Adiposity in women and children from transition countries predicts decreased iron absorption, iron deficiency and a reduced response to iron fortification. Int J Obes (Lond) 2008, 32:1098-1104.
6. Anderson G.J., Frazer D.M., McLaren G.D. Iron absorption and metabolism. Curr Opin Gastroenterol 2009, 25:129-135.
7. Gunshin H., Mackenzie B., Berger U.V., Gunshin Y., Romero M.F., Boron W.F., et al. Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 1997, 388:482-488.
8. McKie A.T., Barrow D., Latunde-Dada G.O., Rolfs A., Sager G., Mudaly E., et al. An iron-regulated ferric reductase associated with the absorption of dietary iron. Science 2001, 291:1755-1759.
9. Wang J., Pantopoulos K. Regulation of cellular iron metabolism. Biochem J 2011, 434:365-381.
10. Hentze M.W., Muckenthaler M.U., Andrews N.C. Balancing acts: molecular control of mammalian iron metabolism. Cell 2004, 117:285-297.
11. Vulpe C.D., Kuo Y.M., Murphy T.L., Cowley L., Askwith C., Libina N., et al. Hephaestin, a ceruloplasmin homologue implicated in intestinal iron transport, is defective in the sla mouse. Nat Genet 1999, 21:195-199.
12. Mims M.P., Prchal J.T. Divalent metal transporter 1. Hematology 2005, 10:339-345.
13. Zoller H., Theurl I., Koch R.O., McKie A.T., Vogel W., Weiss G. Duodenal cytochrome b and hephaestin expression in patients with iron deficiency and hemochromatosis. Gastroenterology 2003, 125:746-754.
14. Pietrangelo A. Physiology of iron transport and the hemochromatosis gene. Am J Physiol Gastrointest Liver Physiol 2002, 282:G403-G414.
15. Zoller H., Koch R.O., Theurl I., Obrist P., Pietrangelo A., Montosi G., et al. Expression of the duodenal iron transporters divalent-metal transporter 1 and ferroportin 1 in iron deficiency and iron overload. Gastroenterology 2001, 120:1412-1419.
16. Nemeth E., Tuttle M.S., Powelson J., Vaughn M.B., Donovan A., Ward D.M., et al. Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science. 2004, 306:2090-2093.
17. Nicolas G., Chauvet C., Viatte L., Danan J.L., Bigard X., Devaux I., et al. The gene encoding the iron regulatory peptide hepcidin is regulated by anemia, hypoxia, and inflammation. J Clin Invest 2002, 110:1037-1044.
18. Chung B., Matak P., McKie A.T., Sharp P. Leptin increases the expression of the iron regulatory hormone hepcidin in HuH7 human hepatoma cells. J Nutr 2007, 137:2366-2370.
19. Bekri S., Gual P., Anty R., Luciani N., Dahman M., Ramesh B., et al. Increased adipose tissue expression of hepcidin in severe obesity is independent from diabetes and NASH. Gastroenterology 2006, 131:788-796.
20. del Giudice E.M., Santoro N., Amato A., Brienza C., Calabro P., Wiegerinck E.T., et al. Hepcidin in obese children as a potential mediator of the association between obesity and iron deficiency. J Clin Endocrinol Metab 2009, 94:5102-5107.
21. Tussing-Humphreys L.M., Nemeth E., Fantuzzi G., Freels S., Holterman A.X., Galvani C., et al. Decreased serum hepcidin and improved functional iron status 6 months after restrictive bariatric surgery. Obesity (Silver Spring). 2010, 18:2010-2016.
22. Theurl I., Aigner E., Theurl M., Nairz M., Seifert M., Schroll A., et al. Regulation of iron homeostasis in anemia of chronic disease and iron deficiency anemia: diagnostic and therapeutic implications. Blood 2009, 113:5277-5286.
23. Theurl I., Ludwiczek S., Eller P., Seifert M., Artner E., Brunner P., et al. Pathways for the regulation of body iron homeostasis in response to experimental iron overload. J Hepatol 2005, 43:711-719.
24. Ludwiczek S., Theurl I., Muckenthaler M.U., Jakab M., Mair S.M., Theurl M., et al. Ca2+ channel blockers reverse iron overload by a new mechanism via divalent metal transporter-1. Nat Med 2007, 13:448-454.
25. Grundy M.A., Gorman N., Sinclair P.R., Chorney M.J., Gerhard G.S. High-throughput non-heme iron assay for animal tissues. J Biochem Biophys Methods 2004, 59:195-200.
26. Torrance J.D., Bothwell T.H. A simple technique for measuring storage iron concentrations in formalinised liver samples. S Afr J Med Sci 1968, 33:9-11.
27. Dixon J.B., Bhathal P.S., Hughes N.R., O'Brien P.E. Nonalcoholic fatty liver disease: improvement in liver histological analysis with weight loss. Hepatology 2004, 39:1647-1654.
28. Kaser S., Moschen A., Cayon A., Kaser A., Crespo J., Pons-Romero F., et al. Adiponectin and its receptors in non-alcoholic steatohepatitis. Gut 2005, 54:117-121.
29. Arndt S., Maegdefrau U., Dorn C., Schardt K., Hellerbrand C., Bosserhoff A.K. Iron-induced expression of bone morphogenic protein 6 in intestinal cells is the main regulator of hepatic hepcidin expression in vivo. Gastroenterology 2010, 138:372-382.
30. Pinhas-Hamiel O., Newfield R.S., Koren I., Agmon A., Lilos P., Phillip M. Greater prevalence of iron deficiency in overweight and obese children and adolescents. Int J Obes Relat Metab Disord 2003, 27:416-418.
31. Yanoff L.B., Menzie C.M., Denkinger B., Sebring N.G., McHugh T., Remaley A.T., et al. Inflammation and iron deficiency in the hypoferremia of obesity. Int J Obes (Lond) 2007, 31:1412-1419.
32. Zimmermann M.B., Zeder C., Chaouki N., Saad A., Torresani T., Hurrell R.F. Dual fortification of salt with iodine and microencapsulated iron: a randomized, double-blind, controlled trial in Moroccan schoolchildren. Am J Clin Nutr 2003, 77:425-432.
33. Moretti D., Zimmermann M.B., Wegmuller R., Walczyk T., Zeder C., Hurrell R.F. Iron status and food matrix strongly affect the relative bioavailability of ferric pyrophosphate in humans. Am J Clin Nutr 2006, 83:632-638.
34. Schweiger C., Weiss R., Berry E., Keidar A. Nutritional deficiencies in bariatric surgery candidates. Obes Surg 2010, 20:193-197.
35. Tussing-Humphreys L.M., Nemeth E., Fantuzzi G., Freels S., Guzman G., Holterman A.X., et al. Elevated systemic hepcidin and iron depletion in obese premenopausal females. Obesity (Silver Spring) 2010, 18:1449-1456.
36. Aeberli I., Hurrell R.F., Zimmermann M.B. Overweight children have higher circulating hepcidin concentrations and lower iron status but have dietary iron intakes and bioavailability comparable with normal weight children. Int J Obes (Lond) 2009, 33:1111-1117.
37. Frazer D.M., Wilkins S.J., Becker E.M., Murphy T.L., Vulpe C.D., McKie A.T., et al. A rapid decrease in the expression of DMT1 and Dcytb but not Ireg1 or hephaestin explains the mucosal block phenomenon of iron absorption. Gut 2003, 52:340-346.
38. Gunshin H., Starr C.N., Direnzo C., Fleming M.D., Jin J., Greer E.L., et al. Cybrd1 (duodenal cytochrome b) is not necessary for dietary iron absorption in mice. Blood 2005, 106:2879-2883.
39. Garrick M.D., Dolan K.G., Horbinski C., Ghio A.J., Higgins D., Porubcin M., et al. DMT1: a mammalian transporter for multiple metals. Biometals 2003, 16:41-54.
40. Conrad M.E., Umbreit J.N., Moore E.G. Iron absorption and transport. Am J Med Sci 1999, 318:213-229.
41. Nunez M.T., Tapia V. Transferrin stimulates iron absorption, exocytosis, and secretion in cultured intestinal cells. Am J Physiol 1999, 276:C1085-C1090.
42. Cherukuri S., Potla R., Sarkar J., Nurko S., Harris Z.L., Fox P.L. Unexpected role of ceruloplasmin in intestinal iron absorption. Cell Metab 2005, 2:309-319.
43. Kemna E.H., Kartikasari A.E., van Tits L.J., Pickkers P., Tjalsma H., Swinkels D.W. Regulation of hepcidin: insights from biochemical analyses on human serum samples. Blood Cells Mol Dis 2008, 40:339-346.
44. Shayeghi M., Latunde-Dada G.O., Oakhill J.S., Laftah A.H., Takeuchi K., Halliday N., et al. Identification of an intestinal heme transporter. Cell 2005, 122:789-801.
45. Fleming R.E., Sly W.S. Hepcidin: a putative iron-regulatory hormone relevant to hereditary hemochromatosis and the anemia of chronic disease. Proc Natl Acad Sci U S A 2001, 98:8160-8162.
46. Vanoaica L., Darshan D., Richman L., Schumann K., Kuhn L.C., Intestinal ferritin H. is required for an accurate control of iron absorption. Cell Metab 2010, 12:273-282.