Novel roles for iron regulatory proteins in the adaptive response to iron deficiency

Journal of Nutrition

Volumn 133, Issue 5 SUPPL. 2, 2003, Pages

  Eisenstein, Richard S ^a   Ross, Kerry L ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Ferritin; Iron; Iron regulatory protein; Transferrin receptor

Indexed keywords

IRON; IRON REGULATORY FACTOR; MESSENGER RNA;

CITRIC ACID CYCLE; CONFERENCE PAPER; EUKARYOTE; HOMEOSTASIS; IRON ABSORPTION; IRON DEFICIENCY; IRON METABOLISM; IRON STORAGE; IRON TRANSPORT; METABOLIC BALANCE; NONHUMAN; PROKARYOTE; RESPIRATORY CHAIN;

EUKARYOTA; MAMMALIA; PROKARYOTA;

EID: 0038332156     PISSN: 00223166     EISSN: None     Source Type: Journal    
DOI: 10.1093/jn/133.5.1510s     Document Type: Conference Paper

References (65)

1. Bothwell, T. H. (1995) Overview and mechanisms of iron regulation. Nutr. Rev. 53: 237-245.
2. Kretchmer, N., Beard, J. L. & Carlson, S. (1996) The role of nutrition in the development of normal cognition. Am. J. Clin. Nutr. 63: 997S-1001S.
3. Chen, O. S., Schalinske, K. L. & Eisenstein, R. S. (1997) Dietary iron intake modulates the activity of iron regulatory proteins (IRPs) and the abundance of ferritin and mitochondrial aconitase in rat liver. J. Nutr. 127: 238-248.
4. Chen, O. S., Blemings, K. P., Schalinske, K. L. & Eisenstein, R. S. (1998) Dietary iron intake rapidly influences iron regulatory proteins, ferritin subunits and mitochondrial aconitase in rat liver. J. Nutr. 128: 525-535.
5. Dallman, P. R. (1986) Biochemical basis for the manifestations of iron deficiency. Annu. Rev. Nutr. 6: 13-40.
6. Muckenthaler, M., Gray, N. K. & Hentze, W. M. (1998) IRP-1 binding to ferritin mRNA prevents the recruitment of the small ribosomal subunit by the cap-binding complex eIF4F. Mol. Cell 2: 383-388.
7. Hentze, M. W. & Kuhn, L. C. (1996) Molecular control of vertebrate iron metabolism: mRNA-based circuits operated by iron, nitric oxide, and oxidative stress. Proc. Natl. Acad. Sci. U.S.A. 93: 8175-8182.
8. 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.
9. Casey, J. L., Koeller, D. M., Ramin, V. C., Klausner, R. D. & Harford, J. B. (1989) Iron regulation of transferrin receptor mRNA levels requires iron-responsive elements and a rapid turnover determinant in the 3′-untranslated region of the mRNA. EMBO J. 8: 3693-3699.
10. Binder, R. A., Horowitz, J. A., Basilion, J. P., Koeller, D. M., Klausner, R. D. & Harford, J. B. (1994) Evidence that the pathway of transferrin receptor mRNA degradation involves an endonucleolytic cleavage within the 3′ UTR and does not involve poly(A) tail shortening. EMBO J. 13: 1969-1980.
11. Hentze, M. W., Caughman, S. W., Casey, J. L., Koeller, D. M., Rouault, T. A., Harford, J. B. & Klausner, R. D. (1988) A model for the structure and function of iron responsive elements. Gene 72: 201-208.
12. Theil, E. C. & Eisenstein, R. S. (2000) Combinatorial mRNA regulation: iron regulatory proteins and iso-iron responsive elements (iso-IREs). J, Biol. Chem. 275: 40659-40662.
13. Theil, E. C. (2000) Targeting mRNA to regulate iron and oxygen metabolism. Biochem. Pharmacol. 59: 87-93.
14. Ke, Y. H., Sierzputowska-Gracz, H., Gdaniec, Z. & Theil, E. C. (2000) Internal loop/bulge and hairpin loop of the iron-responsive element of ferritin mRNA contribute to maximal iron regulatory protein 2 binding and translational regulation in the iso-iron-responsive element/iso-iron regulatory protein family. Biochemistry 39: 6235-6242.
15. Butt, J., Kim, H.-Y., Basilion, J. P., Cohen, S., Iwai, K., Philpott, C. C., Altschul, S., Klausner, R. D. & Rouault, T. A. (1996) Differences in the RNA binding sites of iron regulatory proteins and potential target diversity. Proc. Natl. Acad. Sci. U.S.A. 93: 4345-4349.
16. Henderson, B. R., Menotti, E. & Kuhn, L. C. (1996) Iron regulatory proteins 1 and 2 bind distinct sets of RNA target sequences. J. Biol. Chem. 271: 4900-4908.
17. Bhasker, C. R., Burgiel, G., Neupert, B., Emery-Goodman, A., Kuhn, L. C. & May, B. K. (1993) The putative iron-responsive element in the human erythroid 5-aminolevulinate synthase mRNA mediates translational control. J. Biol. Chem. 268: 12699-12705.
18. Melefors, O., Goossen, B., Johansson, H. E., Stripecke, R., Gray, N. K. & Hentze,M.W. (1993) Translational control of 5-aminolevulinate synthase mRNA by iron-responsive elements in erythroid cells. J. Biol. Chem. 268: 5974-5978.
19. Fleming, M. D., Trenor, C. C., III, Su, M. A., Foernzler, D., Bier, 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.
20. 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.
21. Gunshin, H., Allerson, C. R., Polycarpou-Schwarz, M., Rofts, A., Rogers, J. T., Kishi, F., Hentze, M. W., Rouault, T. A., Andrews, N. C. & Hediger, M. A. (2001) Iron-dependent regulation of the divalent metal ion transporter. FEBS Lett. 509: 309-316.
22. Abboud, S. & Haile, D. J. (2000) A novel mammalian iron-regulated protein involved in intracellular iron metabolism. J. Biol. Chem. 275: 19906-19912.
23. Donovan, A., Brownlie, A., Zhou, Y., Shepard, J., Pratt, S. J., Moynihan, J., Paw, B. H., Drejer, A., Barut, B., Zapata, A., Law, T. C., Brugnara, C., Lux, S. E., Pinkus, G. S., Pinkus, J. L., Kingsley, P. D., Palis, J., Fleming, M. D., Andrews, N. C. & Zon, L. I. (2000) Positional cloning of zebrafish ferroportin 1 identifies a conserved vertebrate iron transporter. Nature 403: 776-781.
24. McKie, A. T., Wehr, K., Simpson, R. J., Peters, T. J., Hentze, M. W. & Farzaneh, F. (1998) Molecular cloning and characterisation of a novel duodenal-specific gene implicated in iron absorption. Biochem. Soc. Trans. 26: S264.
25. 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. U.S.A. 95: 1148-1153.
26. Gambling, L., Danzeisen, R., Gair, S., Lea, R. G., Charania, Z., Solanky, N., Joory, K. D., Srai, S. K. S. & McCardle, H. J. (2001) Effect of iron deficiency on placental transfer of iron and expression of iron transport proteins in vivo and in vitro. Biochem, J. 356: 883-889.
27. Zoller, H., Koch, R. O., Theurl, I., Obrist, P., Pietrangelo, A., Montosi, G., Haile, D. J., Vogel, W. & Weiss, G. (2001) Expression of the duodenal iron transporters divalent-metal transporter 1 and ferroportin 1 in iron deficiency and iron overload. Gastroenterology 120: 1412-1419.
28. Fleming, R. E., Migas, M. C., Zhou, X., Jiang, J., Britton, R. S., Brunt, E. M., Tomatsu, S., Waheed, A., Bacon, B. R. & Sly, W. S. (1999) Mechanism of increased iron absorption in murine model of hereditary hemochromatosis: increased duodenal expression of the iron transporter DMT1. Proc. Natl. Acad. Sci. U.S.A. 96: 3143-3148.
29. Montosi, G., Donovan, A., Totaro, A., Garuti, C., Pignati, E., Cassanelli, S., Trenor, C. C., Gasparini, P., Andrews, N. C. & Pietrangelo, A. (2001) Autosomal-dominant hemochromatosis is associated with a mutation in the ferroportin (SLC11A3) gene. J. Clin. Invest. 108: 619-623.
30. Devalia, V., Carter, K., Walker, A. P., Perkins, S. J., Worwood, M., May, A. & Dooley, J. S. (2002) Autosomal dominant reticuloendothelial iron overload associated with a 3-base pair deletion in the ferroportin 1 gene (SLC11A3). Blood 100: 695-697.
31. Goossen, B. & Hentze, M. W. (1992) Position is the critical determinant for function of iron-responsive elements as translational regulators. Mol. Cell. Biol. 12: 1959-1966.
32. Alen, C. & Sonenshein, A. L. (1999) Bacillus subtilis aconitase is an RNA binding protein. Proc. Natl. Acad. Sci. U.S.A. 96: 10412-10417.
33. Gray, N. K., Pantopoulos, K., Dandekar, T., Ackrell, B. & Hentze, M. W. (1996) Translational regulation of mammalian and drosophila citric acid cycle enzymes via iron-responsive elements. Proc. Natl. Acad. Sci. U.S.A. 93: 4925-4930.
34. Kim, H.-Y., LaVaute, T., Iwai, K., Klausner, R. D. & Rouault, T. A. (1996) Identification of a conserved and functional iron-responsive element in the 5′-untranslated region of mammalian mitochondrial aconitase. J. Biol. Chem. 271: 24226-24230.
35. Kohler, S. A., Henderson, B. R. & Kuhn, L. C. (1995) Succinate dehydrogenase B mRNA of Drosophila melanogaster has a functional iron-responsive element in its 5′-untranslated region. J. Biol. Chem. 270: 30781-30786.
36. Oexle, H., Gnaiger, E. & Weiss, G. (1999) Iron-dependent changes in cellular energy metabolism: influence on citric acid cycle and oxidative phosphorylation. Biochim. Biophys. Acta 1413: 99-107.
37. Ross, K. L. & Eisenstein, R. S. (2002) Iron deficiency decreases mitochondrial aconitase abundance and citrate concentration without affecting tricarboxylic acid cycle capacity in rat liver. J. Nutr. 132: 643-651.
38. Schalinske, K. L., Chen, O. S. & Eisenstein, R. S. (1998) Iron differentially stimulates translation of mitochondrial aconitase and ferritin mRNAs in mammalian cells. J. Biol. Chem. 273: 3740-3746.
39. Tang, Y. & Guest, J. R. (1999) Direct evidence for mRNA binding and post-transcriptional regulation by Escherichia coli aconitases. Microbiology 145: 3069-3079.
40. Hentze, M. W. & Argos, P. (1991) Homology between IRE-BP, a regulatory RNA-binding protein, aconitase, and isopropylmalate isomerase. Nucleic Acids Res. 19: 1739-1740.
41. Rouault, T. A., Stout, C. D., Kaptain, S., Harford, J. B. & Klausner, R. D. (1991) Structural relationship between an iron-regulated RNA-binding protein (IRE-BP) and aconitase: functional implications. Cell 64: 881-883.
42. Dandekar, T., Stripecke, R., Gray, N. K., Goossen, R., Constable, A., Johansson, H. E. & Hentze, W. (1991) Identification of a novel IRE in murine and human eALAS mRNA. EMBO J. 10: 1903-1909.
43. Gardner, P. R. (1997) Superoxide-driven aconitase Fe-S center cycling. Biosci. Rep. 17: 33-42.
44. Beutler, E. (1959) Iron enzymes in iron deficiency. VI. Aconitase activity and citrate metabolism. J. Clin. Invest. 38: 1605-1616.
45. Ohira, Y., Cartier, L.-J., Chen, M. & Holloszy, J. O. (1987) Induction of an increase in mitochondrial matrix enzymes in muscle of iron-deficient rats. Am. J. Physiol. 253: C639-C644.
46. Williamson, J. R. & Cooper, R. H. (1980) Regulation of the citric acid cycle in mammalian systems. FEBS Lett. 117: K73-K85.
47. Guthrie, H. A., Froozani, M., Sherman, A. R. & Barron, G. P. (1974) Hyperlipidemia in offspring of iron-deficient rats. J. Nutr. 104: 1273-1278.
48. Sherman, A. R., Bartholmey, S. J. & Perkins, E. G. (1982) Fatty acid patterns in iron-deficiency maternal and neonatal rats. Lipids 17: 639-643.
49. Liu, Y., Costello, L. C. & Franklin, R. B. (1996) Prolactin specifically regulates citrate oxidation and m-aconitase of rat prostate epithelial cells. Metabolism 45: 442-449.
50. Babcock, M., de Silva, D., Oaks, R., Davis-Kaplan, S., Jiralerspong, S., Montermini, L., Pandolfo, M. & Kaplan, J. (1997) Regulation of mitochondrial iron accumulation by Yfhlp, a putative homolog of frataxin. Science 276: 1709-1712.
51. Deeney, J. T., Prentki, M. & Corkey, B. E. (2000) Metabolic control of beta-cell function. Semin. Cell Dev. Biol. 11: 267-275.
52. Ruderman, N. B., Saha, A. K., Vavvas, D. & Witters, L. A. (1999) Malonyl CoA, fuel sensing, and insulin resistance. Am. J. Physiol. 276: E1-E18.
53. Craig, E. A., Voisine, C. & Schilke, B. (1999) Mitochondrial iron metabolism in the yeast Saccharomyces cerevisiae. Biol. Chem. 380: 1167-1173.
54. Henderson, S. A., Dallman, P. R. & Brooks, G. A. (1986) Glucose turnover and oxidation are increased in the iron-deficient anemic rat. Am. J. Physiol. 250: E414-E421.
55. Des-Rosiers, C., Donato, L. D., Comte, B., Laplante, A., Marcoux, C., David, F., Fernandez, C. A. & Brunengraber, H. (1995) Isotopomer analysis of citric acid cycle and gluconeogenesis in rat liver. Reversibility of isocitrate dehydrogenase and involvement of ATP-citrate lyase. J. Biol. Chem. 270: 10027-10036.
56. Cartier, L.-J., Ohira, Y., Chen, M., Cuddihee, R. W. & Holloszy, J. O. (1986) Perturbation of mitochondrial composition in muscle by iron deficiency. J. Biol. Chem. 261: 13827-13832.
57. Maguire, J. J., Davies, K. J. A., Dallman, P. R. & Packer, L. J. (1982) Effects of dietary iron deficiency on iron-sulfur proteins and bioenergetic functions of skeletal muscle mitochondria. Biochim. Biophys. Acta 679: 210-220.
58. Masini, A., Salvioli, G., Cremonesi, P., Botti, B., Gallesi, D. & Ceccarelli, D. (1994) Dietary iron deficiency in the rat. I. Abnormalities in energy metabolism of the hepatic tissue. Biochim. Biophys. Acta 1188: 46-52.
59. Willis, W. T. & Dallman, P. R. (1989) Impaired control of respiration in iron-deficient muscle mitochondria. Am. J. Physiol. 257: C1080-C1085.
60. Knutson, M. D., Walter, P. B., Ames, B. N. & Viteri, F. E. (2000) Both iron deficiency and daily iron supplements increase lipid peroxidation in rats. J. Nutr. 130: 621-628.
61. Walter, W. B., Knutson, M. D., Paler-Martinez, A., Lee, S., Xu, Y., Viteri, F. E. & Ames, B. N. (2002) Iron deficiency and iron excess damage mitochondria and mitochondrial DNA in rats. Proc. Natl. Acad. Sci. U.S.A. 99: 2264-2269.
62. Tang, Y., Quail, M. A., Artymuik, P. J., Guest, J. R. & Green, J. (2002) Escherichia coli aconitases and oxidative stress: post-transcriptional regulation of sodA expression. Microbiology 148: 1027-1037.
63. Ke, Y., Wu, J., Leibold, E. A., Walden, W. E. & Theil, E. C. (1998) Loops and bulge/loops in iron-responsive element isoforms influence iron regulatory protein binding. J. Biol. Chem. 273: 23637-23640.
64. Gray, N. K. & Wickens, M. (1998) Control of translation initiation in animals. Annu. Rev. Cell Dev. Biol. 14: 399-458.
65. Hubert, N. and Hentze, M. W. (2002) Previously uncharacterized isoforms of divalent metal transporter (DMT)-1: implications for regulation and cellular function. Proc. Natl. Acad. Sci. U.S.A. 99: 12345-12350.