Reciprocal regulation of HFE and Nramp2 gene expression by iron in human intestinal cells

Journal of Nutrition

Volumn 129, Issue 1, 1999, Pages 98-104

  Han, Okhee ^a   Fleet, James C ^a,b   Wood, Richard J ^a  

^a TUFTS UNIVERSITY   (United States)

^b UNIVERSITY OF NORTH CAROLINA AT GREENSBORO   (United States)

Author keywords

Gene expression; HFE; Human intestinal cell line; Iron; Nramp2

Indexed keywords

CARRIER PROTEIN; CYCLOHEXIMIDE; GENE PRODUCT; IRON; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MESSENGER RNA; REPRESSOR PROTEIN;

ARTICLE; CELL DIFFERENTIATION; CELL STRAIN CACO 2; CONTROLLED STUDY; GENE EXPRESSION; HEMOCHROMATOSIS; HUMAN; HUMAN CELL; INTESTINE ABSORPTION; INTESTINE CELL; IRON ABSORPTION;

EID: 0032924878     PISSN: 00223166     EISSN: None     Source Type: Journal    
DOI: 10.1093/jn/129.1.98     Document Type: Article

References (42)

1. Alvarez-Hernandez, X., Nichols, G. M. & Glass, J. (1991) Caco-2 cell line: a system for studying intestinal iron transport across epithelial cell monolayers. Biochem. Biophys. Acta 1070: 205-208.
2. Banerjee, D., Flanagan, P. R., Cluett, J. & Valberg, L. S. (1986) Transferrin receptors in the human gastrointestinal tract. Gastroenterology 91: 861-869.
3. Bomford, A. & Williams, R. (1976) Long term results of venesection therapy in idiopathic haemochromatosis. Q. J. Med. 45: 611-623.
4. Bothwell, T. H., Chartton, R. W. & Motulski, A. G. (1995) Hemochromatosis. In: The metabolic and molecular basis of inherited disease. (Scriver, C. R., Beaudet, A. L., Sly, W. S. & Valle, D., eds.), pp. 2237-2269. McGraw-Hill, New York, NY.
5. Edwards, J. A. & Hoke, J. E. (1972) Defect of intestinal mucosal iron uptake in mice with hereditary microcytic anemia. Proc. Soc. Exp. Biol. Med. 141: 81-84.
6. Feder, J. N., Gnirke, A., Thomas, W., Tsuchihashi, Z., Ruddy, D. A., Basava, A., Dormishian, F., Domingo, R., Ellis, M. C., Fullan, A., Hinton, L. M., Jones, N. L., Kimmel, B. E., Kronmal, G. S., Lauer, P., Lee, V. K., Loeb, D. B., Mapa, F. A., McClelland, E., Meyer, N. C., Mintier, G. A., Moeller, N., Moore, T., Morikang, E., Prass, C. E., Quintana, L., Stames, S. M., Schatzman, R. C., Brunke, K. J., Drayna, D. T., Risch, N. J., Bacon, B. R. & Wolff, R. K. (1996) A novel MHC class I-like gene is mutated in patients with hereditary haemochromatosis. Nat. Genet. 13: 399-408.
7. Feder, J. N., Penny, D. M., Irrinki, A., Lee, V. K., Lebron, J. A., Watson, N., Tsuchihashi, Z., Sigal, E., Bjorkman, P. J. & Schatzman, R. C. (1998) The hemochromatosis gene product complexes with the transferrin receptor and lowers its affinity for ligand binding. Proc. Natl. Acad. Sci. USA 95: 1472-1477.
8. 2-microglobulin interaction and cell surface expression. J. Biol. Chem. 272: 14025-14028.
9. Flanagan, P. R., Haist, J. & Valberg, L. S. (1980) Comparative effects of iron deficiency induced by bleeding and low-iron diet on the intestinal absorptive interaction of iron, cobalt, manganese, zinc, lead and cadmium. J. Nutr. 110: 1754-1763.
10. Fleming, M. D., Romano, M. A., Su, M. A., Garrick, L. M., Garrick, M. D. & Andrews, N. C. (1998) Nramp2 is mutated in the anemic belgrade (b) rat: evidence of a role for Nramp2 in endosomal iron transport. Proc. Natl. Acad. Sci. USA. 95: 1148-1153.
11. Fleming, M. D., Trenor C. C., III, Su, M. A., Foernzler, D., Beier, D. R., Dietrich, W. F. & Andrews, N. C. (1997) Microcytic anaemia mice have a mutation in Nramp2, a candidate iron transporter gene. Nat. Genet. 16: 383-386.
12. Gross, C. N., Irrinki, A., Feder, J. N. & Enns, C. A. (1998) Co-trafficking of HFE, a nonclassical major histocompatibility complex class I protein, with the transferrin receptor implies a role in intracellular iron regulation. J. Biol. Chem. 273: 22068-22074.
13. Gunshin, H., Mackenzie, B., Berger, U. V., Gunshin, Y., Romero, M. F., Boron, W. F., Nussberger, S., Gollan, J. L. & Hediger, M. A. (1997) Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 388: 482-488.
14. Gunshin, H., Rouault, T., Rogers, J., Allerson, C., Gollan, J. L. & Hediger, M. A. (1998) Regulation of the divalent cation transporter DCT1 at the mRNA level. FASEB J. 12: A820. (abs.)
15. Han, O., Failla, M. L. & Smith, J. C. (1997) Transferrin-iron and proinflammatory cytokines influence iron status and apical iron transport efficiency of Caco-2 intestinal cell line. J. Nutr. Biochem. 8: 585-591.
16. Han, O., Failla, M. L., Hill, A. D., Morris, E. R. & Smith, J. C. (1995) Reduction of Fe (III) is required for uptake of nonheme iron by Caco-2 cells. J. Nutr. 125: 1291-1299.
17. Jumarie, C. & Malo, C. (1992) Caco-2 cells cultured in a serum free medium as a model for the study of enterocytic differentiation in vitro. J. Cell. Physiol. 149: 24-33.
18. Klausner, R. D., Van Renswoude, J., Ashwell, G., Kemf, C., Schechter, A. N., Dean, A. & Bridges, K. R. (1983) Receptor-mediated endocytosis of transferrin in K562 cells. J. Biol. Chem. 258: 4715-4724.
19. Klausner, R. D. Rouault, T. A. & Harford, J. B. (1993) Regulating the fate of mRNA: the control of cellular iron metabolism. Cell 72: 19-28.
20. Lebron, J. A., Bennett, M. J., Vaughn, D. E., Chirino, A. J., Snow, P. M., Mintier, G. A., Feder, J. N. & Bjorkman, P. J. (1998) Crystal structure of the hemochromatosis protein HFE and characterization of its interaction with transferrin receptor. Cell 93: 111-123.
21. Lee, P. L., Gelbart, T., West, C., Halloran, C. & Beutler, E. (1998) The human Nramp2 gene: characterization of the gene structure, alternative splicing, promoter region and polymorphism. Blood Cells Mol. Dis. 24: 199-215.
22. Louvard, D., Kedinger, M. & Hauri, H. P. (1992) The differentiating intestinal epithelial cell: Establishment and maintenance of functions through interactions between cellular structures. Ann. Rev. Cell Biol. 8: 157-195.
23. Nelson, R. L., Davis, F. G., Persky, V. & Becker, E. (1995) Risk of neoplastic and other diseases among people with heterozygosity for hereditary hemochromatosis. Cancer 76: 875-879.
24. Parkkila, S., Waheed, A., Britton, R. S., Bacon, B. R., Zhou, X. Y., Tomatsu, S., Fleming, E. & Sly, W. S. (1997a) Association of the transferrin receptor in human placenta with HFE, the protein defective in hereditary hemochromatosis. Proc. Natl. Acad. Sci. USA 94: 13198-13202.
25. Parkkila, S., Waheed, A., Britton, R. S., Feder, J. N., Tsuchihashi, Z., Schatzman, R. C., Bacon, B. R. & Sly, W. S. (1997b) Immunohistochemistry of HLA-H, the protein defective in patients with hereditary hemochromatosis, reveals unique pattern of expression in gastrointestinal tract. Proc. Natl. Acad. Sci. USA 94: 2534-2539.
26. Pietrangelo, A., Casalgrandi, G., Quaglino, D., Gualdi, R., Conte, D., Milani, S., Montosi, G., Cesarini, L., Ventura, E. & Cairo, G. (1995) Duodenal ferritin synthesis in genetic hemochromatosis. Gastroenterology 108: 208-217.
27. 2 knockout mice develop parenchymal iron overload: a putative role for class I genes of the major histocompatibility complex in iron metabolism. Proc. Natl. Acad. Sci. USA 93: 1529-1534.
28. Salonen, J. T., Nyyssonen, K., Korpela, H., Tuomilehto, J., Seppanen, R. & Salonen, R. (1992) High stored iron levels are associated with excess risk of myocardial infarction in eastern Finnish men. Circulation 86: 803-811.
29. 2-microglobulin knockout mice recapitulates hereditary hemochromatosis in man. J. Exp. Med 184: 1975-1985.
30. Skikne, B. & Baynes, R. D. (1994) Iron absorption. In: Iron Metabolism in Health and Disease. (Brock, J. H., Halliday, J. W., Pippard, M. J. & Powell, L. W., eds.) pp. 151-187. W. B. Saunders, London.
31. Skikne, B. S., Whittker, P., Cooke, A. & Cook, J. D. (1995) Ferritin excretion and iron balance in humans. Br. J. Hematol. 90: 681-687.
32. Smith, C., Mitchinson, M. J., Aruoma, O. I. & Halliwell, B. (1992) Stimulation of lipid peroxidation and hydroxyl-radical generation by the contents of human atherosclerotic lesions. Biochem. J. 286: 901-905.
33. Su, M. A., Trenor , C. C., III, Fleming, J. C., Fleming, M. D. & Andrews, N. C. (1998) The G185R mutation disrupts function of the iron transporter Nramp2. Blood 92: 2157-2163.
34. Tapia, V., Arredondo, M. & Nunez, M. T. (1996) Regulation of Fe absorption by cultured epithelial (Caco-2) cell monolayers with varied Fe status. Am. J. Physiol. 271: G443-G447.
35. Vidal, S. M., Malo, D., Vogan, K., Skamene, E. & Gros, P. (1993) Natural resistance to infection with intracellular parasites: isolation of a candidate for Bcg. Cell 73: 469-485.
36. Wang, X., Manganaro, F. & Schipper, H. M. (1995) A cellular stress model for the sequestration of redox-active glial iron in the aging and degenerating nervous system. J. Neurochem. 64: 1868-1877.
37. Weinberg, E. D. (1985) Roles of iron in infection and neoplasia. J. Pharmacol. 16: 358-364.
38. Weissman, J.D. & Singer, D.S. (1991) A complex regulatory DNA element associated with a major histocompatibility complex class I gene consists of both a silencer and an enhancer. Mol. Cell. Biol. 11: 4217-4227.
39. White, K. & Munro, H. N. (1988) Induction of ferritin subunit synthesis by iron is regulated at both the transcriptional and translational levels. J. Biol. Chem. 263: 8938-8942.
40. Whittaker, P., Skikne, B. S., Covell, A. M., Flowers, C., Cooke, A., Lynch, S. R. & Cook, J. D. (1989) Duodenal iron proteins in idiopathic hemochromatosis. J. Clin. Invest. 83: 261-267.
41. Wood, R. J. & Han, O. (1998) Recently identified molecular aspects of intestinal iron absorption. J. Nutr. 128: 1841-1844.
42. Zhou, X. Y., Tomatsu, S., Fleming, R. E., Parkkila, S., Waheed, A., Jiang, J., Fei, Y., Brunt, E. M., Ruddy, D. A., Prass, C. E., Schatzman, R. C., O'neill, R., Britton, R. S., Bacon, B. R. & Sly, W. S. (1998) HFE gene knockout produces mouse model of hereditary hemochromatosis. Proc. Natl. Acad. Sci. USA 95: 2492-2497.