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Original

The role of reactive oxygen and nitrogen species in cellular iron metabolism

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Pages 263-272 | Received 23 Sep 2005, Published online: 07 Jul 2009

References

  • Halliwell B, Gutteridge JM. Free radicals in biology and medicine3rd ed. Oxford University Press, New York 1999
  • Andrews NC. Disorders of iron metabolism. N Engl J Med 1999; 341: 1986–1995
  • Hentze MW, Muckenthaler MU, Andrews NC. Balancing acts: Molecular control of mammalian iron metabolism. Cell 2004; 117: 285–297
  • Mladenka P, Hrdina R, Hubl M, Simunek T. The fate of iron in the organism and its regulatory pathways. Acta Medica (Hradec Kralove) 2005
  • Aziz N, Munro HN. Iron regulates ferritin mRNA translation through a segment of its 5′ untranslated region. Proc Natl Acad Sci USA 1987; 84: 8478–8482
  • Hentze MW, Kuhn LC. Molecular control of vertebrate iron metabolism: mRNA-Based regulatory circuits operated by iron, nitric oxide, and oxidative stress. Proc Natl Acad Sci USA 1996; 93: 8175–8182
  • Beinert H, Kennedy MC. 19th Sir Hans Krebs lecture. Engineering of protein bound iron–sulfur clusters. A tool for the study of protein and cluster chemistry and mechanism of iron–sulfur enzymes. Eur J Biochem 1989; 186: 5–15
  • Klausner RD, Rouault TA. A double life: Cytosolic aconitase as a regulatory RNA binding protein. Mol Biol Cell 1993; 4: 1–5
  • Brown NM, Kennedy MC, Antholine WE, Eisenstein RS, Walden WE. Detection of a [3Fe–4S] cluster intermediate of cytosolic aconitase in yeast expressing iron regulatory protein 1. Insights into the mechanism of Fe–S cluster cycling. J Biol Chem 2002; 277: 7246–7254
  • Haile DJ, Rouault TA, Harford JB, Kennedy MC, Blondin GA, Beinert H, Klausner RD. Cellular regulation of the iron-responsive element binding protein: Disassembly of the cubane iron–sulfur cluster results in high-affinity RNA binding. Proc Natl Acad Sci USA 1992; 89: 11735–11739
  • Guo B, Yu Y, Leibold EA. Iron regulates cytoplasmic levels of a novel iron-responsive element-binding protein without aconitase activity. J Biol Chem 1994; 269: 24252–24260
  • Ke Y, Wu J, Leibold EA, Walden WE, Theil EC. Loops and bulge/loops in iron-responsive element isoforms influence iron regulatory protein binding. Fine-tuning of mRNA regulation?. J Biol Chem 1998; 273: 23637–23640
  • McCord JM. Iron, free radicals, and oxidative injury. Semin Hematol 1998; 35: 5–12
  • Berry CE, Hare JM. Xanthine oxidoreductase and cardiovascular disease: Molecular mechanisms and pathophysiological implications. J Physiol 2004; 555: 589–606
  • Gardner PR, Raineri I, Epstein LB, White CW. Superoxide radical and iron modulate aconitase activity in mammalian cells. J Biol Chem 1995; 270: 13399–13405
  • Missirlis F, Hu J, Kirby K, Hilliker AJ, Rouault TA, Phillips JP. Compartment-specific protection of iron–sulfur proteins by superoxide dismutase. J Biol Chem 2003; 278: 47365–47369
  • Han D, Antunes F, Canali R, Rettori D, Cadenas E. Voltage-dependent anion channels control the release of the superoxide anion from mitochondria to cytosol. J Biol Chem 2003; 278: 5557–5563
  • Liochev SI, Fridovich I. Superoxide and iron: Partners in crime. IUBMB Life 1999; 48: 157–161
  • Graf E, Mahoney JR, Bryant RG, Eaton JW. Iron-catalyzed hydroxyl radical formation. Stringent requirement for free iron coordination site. J Biol Chem 1984; 259: 3620–3624
  • Hrdina R, Gersl V, Klimtova I, Simunek T, Mazurova Y, Machackova J, Adamcova M. Effect of sodium 2,3-dimercaptopropane-1-sulphonate (DMPS) on chronic daunorubicin toxicity in rabbits: Comparison with dexrazoxane. Acta Medica (Hradec Kralove) 2002; 45: 99–105
  • Omar R, Nomikos I, Piccorelli G, Savino J, Agarwal N. Prevention of postischaemic lipid peroxidation and liver cell injury by iron chelation. Gut 1989; 30: 510–514
  • Simunek T, Boer C, Bouwman RA, Vlasblom R, Versteilen AMG, Sterba M, Gersl V, Hrdina R, Ponka P, de Lange JJ, Paulus WJ, Musters RJP. SIH—a novel lipophilic iron chelator—protects H9c2 cardiomyoblasts from oxidative stress-induced mitochondrial injury and cell death. J Mol Cell Cardiol 2005; 39: 345–354
  • Simunek T, Klimtova I, Kaplanova J, Sterba M, Mazurova Y, Adamcova M, Hrdina R, Gersl V, Ponka P. Study of daunorubicin cardiotoxicity prevention with pyridoxal isonicotinoyl hydrazone in rabbits. Pharmacol Res 2005; 51: 223–231
  • Castro LA, Robalinho RL, Cayota A, Meneghini R, Radi R. Nitric oxide and peroxynitrite-dependent aconitase inactivation and iron-regulatory protein-1 activation in mammalian fibroblasts. Arch Biochem Biophys 1998; 359: 215–224
  • Martins EA, Robalinho RL, Meneghini R. Oxidative stress induces activation of a cytosolic protein responsible for control of iron uptake. Arch Biochem Biophys 1995; 316: 128–134
  • Pantopoulos K, Mueller S, Atzberger A, Ansorge W, Stremmel W, Hentze MW. Differences in the regulation of iron regulatory protein-1 (IRP-1) by extra- and intracellular oxidative stress. J Biol Chem 1997; 272: 9802–9808
  • Pantopoulos K, Weiss G, Hentze MW. Nitric oxide and oxidative stress (H2O2) control mammalian iron metabolism by different pathways. Mol Cell Biol 1996; 16: 3781–3788
  • Bouton C, Raveau M, Drapier JC. Modulation of iron regulatory protein functions. Further insights into the role of nitrogen- and oxygen-derived reactive species. J Biol Chem 1996; 271: 2300–2306
  • Pantopoulos K, Hentze MW. Activation of iron regulatory protein-1 by oxidative stress in vitro. Proc Natl Acad Sci USA 1998; 95: 10559–10563
  • Brazzolotto X, Gaillard J, Pantopoulos K, Hentze MW, Moulis JM. Human cytoplasmic aconitase (iron regulatory protein 1) is converted into its [3Fe–4S] form by hydrogen peroxide in vitro but is not activated for iron-responsive element binding. J Biol Chem 1999; 274: 21625–21630
  • Mueller S, Pantopoulos K, Hubner CA, Stremmel W, Hentze MW. IRP1 activation by extracellular oxidative stress in the perfused rat liver. J Biol Chem 2001; 276: 23192–23196
  • Keyer K, Imlay JA. Superoxide accelerates DNA damage by elevating free-iron levels. Proc Natl Acad Sci USA 1996; 93: 13635–13640
  • Gardner PR, Fridovich I. Inactivation-reactivation of aconitase in Escherichia coli. A sensitive measure of superoxide radical. J Biol Chem 1992; 267: 8757–8763
  • Starzynski RR, Lipinski P, Drapier JC, Diet A, Smuda E, Bartlomiejczyk T, Gralak MA, Kruszewski M. Down-regulation of iron regulatory protein 1 activities and expression in superoxide dismutase 1 knockout mice is not associated with alterations in iron metabolism. J Biol Chem 2005; 280: 4207–4212
  • Fillebeen C, Chahine D, Caltagirone A, Segal P, Pantopoulos K. A phosphomimetic mutation at Ser-138 renders iron regulatory protein 1 sensitive to iron-dependent degradation. Mol Cell Biol 2003; 23: 6973–6981
  • McCord JM, Fridovich I. The reduction of cytochrome c by milk xanthine oxidase. J Biol Chem 1968; 243: 5753–5760
  • Cairo G, Castrusini E, Minotti G, Bernelli-Zazzera A. Superoxide and hydrogen peroxide-dependent inhibition of iron regulatory protein activity: A protective stratagem against oxidative injury. FASEB J 1996; 10: 1326–1335
  • Flint DH, Tuminello JF, Emptage MH. The inactivation of Fe–S cluster containing hydro-lyases by superoxide. J Biol Chem 1993; 268: 22369–22376
  • Richardson DR, Ponka P. Identification of a mechanism of iron uptake by cells which is stimulated by hydroxyl radicals generated via the iron-catalysed Haber–Weiss reaction. Biochim Biophys Acta 1995; 1269: 105–114
  • Biemond P, Swaak AJ, van Eijk HG, Koster JF. Superoxide dependent iron release from ferritin in inflammatory diseases. Free Radic Biol Med 1988; 4: 185–198
  • Reif DW, Simmons RD. Nitric oxide mediates iron release from ferritin. Arch Biochem Biophys 1990; 283: 537–541
  • Thomas CE, Aust SD. Reductive release of iron from ferritin by cation free radicals of paraquat and other bipyridyls. J Biol Chem 1986; 261: 13064–13070
  • Ignarro LJ. Biosynthesis and metabolism of endothelium-derived nitric oxide. Annu Rev Pharmacol Toxicol 1990; 30: 535–560
  • Soum E, Drapier JC. Nitric oxide and peroxynitrite promote complete disruption of the [4Fe–4S] cluster of recombinant human iron regulatory protein 1. J Biol Inorg Chem 2003; 8: 226–232
  • Cairo G, Ronchi R, Recalcati S, Campanella A, Minotti G. Nitric oxide and peroxynitrite activate the iron regulatory protein-1 of J774A.1 macrophages by direct disassembly of the Fe–S cluster of cytoplasmic aconitase. Biochemistry 2002; 41: 7435–7442
  • Drapier JC, Hirling H, Wietzerbin J, Kaldy P, Kuhn LC. Biosynthesis of nitric oxide activates iron regulatory factor in macrophages. EMBO J 1993; 12: 3643–3649
  • Gonzalez D, Drapier JC, Bouton C. Endogenous nitration of iron regulatory protein-1 (IRP-1) in nitric oxide-producing murine macrophages: Further insight into the mechanism of nitration in vivo and its impact on IRP-1 functions. J Biol Chem 2004; 279: 43345–43351
  • Pantopoulos K, Hentze MW. Nitric oxide signaling to iron-regulatory protein: Direct control of ferritin mRNA translation and transferrin receptor mRNA stability in transfected fibroblasts. Proc Natl Acad Sci USA 1995; 92: 1267–1271
  • Weiss G, Goossen B, Doppler W, Fuchs D, Pantopoulos K, Werner-Felmayer G, Wachter H, Hentze MW. Translational regulation via iron-responsive elements by the nitric oxide/NO-synthase pathway. EMBO J 1993; 12: 3651–3657
  • Kim S, Ponka P. Control of transferrin receptor expression via nitric oxide-mediated modulation of iron-regulatory protein 2. J Biol Chem 1999; 274: 33035–33042
  • Henry Y, Lepoivre M, Drapier JC, Ducrocq C, Boucher JL, Guissani A. EPR characterization of molecular targets for NO in mammalian cells and organelles. FASEB J 1993; 7: 1124–1134
  • Recalcati S, Taramelli D, Conte D, Cairo G. Nitric oxide-mediated induction of ferritin synthesis in J774 macrophages by inflammatory cytokines: Role of selective iron regulatory protein-2 downregulation. Blood 1998; 91: 1059–1066
  • Phillips JD, Kinikini DV, Yu Y, Guo B, Leibold EA. Differential regulation of IRP1 and IRP2 by nitric oxide in rat hepatoma cells. Blood 1996; 87: 2983–2992
  • Oria R, Sanchez L, Houston T, Hentze MW, Liew FY, Brock JH. Effect of nitric oxide on expression of transferrin receptor and ferritin and on cellular iron metabolism in K562 human erythroleukemia cells. Blood 1995; 85: 2962–2966
  • Richardson DR, Neumannova V, Ponka P. Nitrogen monoxide decreases iron uptake from transferrin but does not mobilise iron from prelabelled neoplastic cells. Biochim Biophys Acta 1995; 1266: 250–260
  • Stamler JS, Singel DJ, Loscalzo J. Biochemistry of nitric oxide and its redox-activated forms. Science 1992; 258: 1898–1902
  • Richardson DR, Neumannova V, Nagy E, Ponka P. The effect of redox-related species of nitrogen monoxide on transferrin and iron uptake and cellular proliferation of erythroleukemia (K562) cells. Blood 1995; 86: 3211–3219
  • Hanson ES, Foot LM, Leibold EA. Hypoxia post-translationally activates iron-regulatory protein 2. J Biol Chem 1999; 274(8)5047–5052, Feb 19
  • Wang J, Chen G, Pantopoulos K. Nitric oxide inhibits the degradation of IRP2. Mol Cell Biol 2005; 25: 1347–1353
  • Bouton C, Oliveira L, Drapier JC. Converse modulation of IRP1 and IRP2 by immunological stimuli in murine RAW 264.7 macrophages. J Biol Chem 1998; 273: 9403–9408
  • Kim S, Ponka P. Effects of interferon-gamma and lipopolysaccharide on macrophage iron metabolism are mediated by nitric oxide-induced degradation of iron regulatory protein 2. J Biol Chem 2000; 275: 6220–6226
  • Watts RN, Richardson DR. The mechanism of nitrogen monoxide (NO)-mediated iron mobilization from cells. NO intercepts iron before incorporation into ferritin and indirectly mobilizes iron from ferritin in a glutathione-dependent manner. Eur J Biochem 2002; 269: 3383–3392
  • Watts RN, Richardson DR. Differential effects on cellular iron metabolism of the physiologically relevant diatomic effector molecules, NO and CO, that bind iron. Biochim Biophys Acta 2004; 1692: 1–15
  • Mulero V, Brock JH. Regulation of iron metabolism in murine J774 macrophages: Role of nitric oxide-dependent and -independent pathways following activation with gamma interferon and lipopolysaccharide. Blood 1999; 94: 2383–2389
  • Konijn AM, Hershko C. Ferritin synthesis in inflammation. I. Pathogenesis of impaired iron release. Br J Haematol 1977; 37: 7–16
  • Kwok JC, Richardson DR. The iron metabolism of neoplastic cells: Alterations that facilitate proliferation?. Crit Rev Oncol Hematol 2002; 42: 65–78
  • Weiss G, Werner-Felmayer G, Werner ER, Grunewald K, Wachter H, Hentze MW. Iron regulates nitric oxide synthase activity by controlling nuclear transcription. J Exp Med 1994; 180: 969–976
  • Harhaji L, Vuckovic O, Miljkovic D, Stosic-Grujicic S, Trajkovic V. Iron down-regulates macrophage anti-tumour activity by blocking nitric oxide production. Clin Exp Immunol 2004; 137: 109–116
  • Huie RE, Padmaja S. The reaction of no with superoxide. Free Radic Res Commun 1993; 18: 195–199
  • Ischiropoulos H, Zhu L, Chen J, Tsai M, Martin JC, Smith CD, Beckman JS. Peroxynitrite-mediated tyrosine nitration catalyzed by superoxide dismutase. Arch Biochem Biophys 1992; 298: 431–437

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