Labile iron pool: The main determinant of cellular response to oxidative stress

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 531, Issue 1-2, 2003, Pages 81-92

  Kruszewski, Marcin ^a,b  

^a INSTITUTE OF NUCLEAR CHEMISTRY AND TECHNOLOGY   (Poland)

^b INSTITUTE OF ONCOLOGY   (Poland)

Author keywords

Hydrogen peroxide; Iron homeostasis; Oxidative cellular damage

Indexed keywords

HYDROXYL RADICAL; IRON; PROTEIN;

APOPTOSIS; CATALYSIS; CELL DAMAGE; CONFERENCE PAPER; HOMEOSTASIS; IRON METABOLISM; IRON STORAGE; IRON TRANSPORT; NONHUMAN; OXIDATION; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSCRIPTION REGULATION;

EID: 0344154421     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2003.08.004     Document Type: Conference Paper

References (94)

1. Greenberg G.R., Wintrobe M.M. A labile iron pool. J. Biol. Chem. 165:1946;397-398.
2. Jacobs A. An intracellular transit iron pool. Ciba Found. Symp. 51:1977;91-106.
3. Kakhlon O., Cabantchik Z.I. The labile iron pool: characterization, measurement, and participation in cellular processes. Free Radic. Biol. Med. 33:2002;1037-1046.
4. Petrat F., De Groot H., Sustmann R., Rauen U. The chelatable iron pool in living cells: a methodically defined quantity. Biol. Chem. 383:2002;489-502.
5. Andrews N.C. Iron homeostasis: insights from genetics and animal models. Nat. Rev. Genet. 1:2000;208-217.
6. McKie A.T., Barrow D., Latunde-Dada G.O., Rolfs A., Sager G., Mudaly E., Mudaly M., Richardson C., Barlow D., Bomford A., Peters T.J., Raja K.B., Shirali S., Hediger M.A., Farzaneh F., Simpson R.J. An iron-regulated ferric reductase associated with the absorption of dietary iron. Science. 291:2001;1755-1759.
7. Levy J.E., Jin O., Fujiwara Y., Kuo F., Andrews N.C. Transferrin receptor is necessary for development of erythrocytes and the nervous system. Nat. Genet. 21:1999;396-399.
8. Breuer W., Epsztejn S., Cabantchik Z.I. Iron acquired from transferrin by K562 cells is delivered into a cytoplasmic pool of chelatable iron(II). J. Biol. Chem. 270:1995;24209-24215.
9. McKie A.T., Latunde-Dada G.O., Miret S., McGregor J.A., Anderson G.J., Vulpe C.D., Wrigglesworth J.M., Simpson R.J. Molecular evidence for the role of a ferric reductase in iron transport. Biochem. Soc. Trans. 30:2002;722-724.
10. Gunshin H., Mackenzie B., Berger U.V., Gunshin Y., Romero M.F., Boron W.F., Nussberger S., Gollan J.L., Hediger M.A. Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature. 388:1997;482-488.
11. Canonne-Hergaux F., Gruenheid S., Ponka P., Gros P. Cellular and subcellular localization of the Nramp2 iron transporter in the intestinal brush border and regulation by dietary iron. Blood. 93:1999;4406-4417.
12. Latunde-Dada G.O., Van der W.J., Vulpe C.D., Anderson G.J., Simpson R.J., McKie A.T. Molecular and functional roles of duodenal cytochrome B (dcytb) in iron metabolism. Blood Cells Mol. Dis. 29:2002;356-360.
13. Fleming M.D., Trenor C.C., Su M.A., Foernzler D., Beier D.R., Dietrich W.F., Andrews N.C. Microcytic anaemia mice have a mutation in Nramp2, a candidate iron transporter gene. Nat. Genet. 16:1997;383-386.
14. Fleming M.D., Romano M.A., Su M.A., Garrick L.M., Garrick M.D., Andrews N.C. 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. 95:1998;1148-1153.
15. Edwards J.A., Garrick L.M., Hoke J.E. Defective iron uptake and globin synthesis by erythroid cells in the anemia of the Belgrade laboratory rat. Blood. 51:1978;347-357.
16. Breuer W., Epsztejn S., Millgram P., Cabantchik I.Z. Transport of iron and other transition metals into cells as revealed by a fluorescent probe. Am. J. Physiol. 268:1995;C1354-C1361.
17. Picard V., Epsztejn S., Santambrogio P., Cabantchik Z.I., Beaumont C. Role of ferritin in the control of the labile iron pool in murine erythroleukemia cells. J. Biol. Chem. 273:1998;15382-15386.
18. Cozzi A., Corsi B., Levi S., Santambrogio P., Albertini A., Arosio P. Overexpression of wild type and mutated human ferritin H-chain in HeLa cells: in vivo role of ferritin ferroxidase activity. J. Biol. Chem. 275:2000;25122-25129.
19. Chasteen N.D. Ferritin. Uptake, storage, and release of iron. Met. Ions Biol. Syst. 35:1998;479-514.
20. Meyron-Holtz E.G., Vaisman B., Cabantchik Z.I., Fibach E., Rouault T.A., Hershko C., Konijn A.M. Regulation of intracellular iron metabolism in human erythroid precursors by internalized extracellular ferritin. Blood. 94:1999;3205-3211.
21. Konijn A.M., Glickstein H., Vaisman B., Meyron-Holtz E.G., Slotki I.N., Cabantchik Z.I. The cellular labile iron pool and intracellular ferritin in K562 cells. Blood. 94:1999;2128-2134.
22. Roberts S., Bomford A. Ferritin iron kinetics and protein turnover in K562 cells. J. Biol. Chem. 263:1988;19181-19187.
23. Rothman R.J., Serroni A., Farber J.L. Cellular pool of transient ferric iron, chelatable by deferoxamine and distinct from ferritin, that is involved in oxidative cell injury. Mol. Pharmacol. 42:1992;703-710.
24. Delanghe J.R., Langlois M.R. Hemopexin: a review of biological aspects and the role in laboratory medicine. Clin. Chim. Acta. 312:2001;13-23.
25. Alayash A.I., Patel R.P., Cashon R.E. Redox reactions of hemoglobin and myoglobin: biological and toxicological implications. Antioxid. Redox. Signal. 3:2001;313-327.
26. Applegate L.A., Luscher P., Tyrrell R.M. Induction of heme oxygenase: a general response to oxidant stress in cultured mammalian cells. Cancer Res. 51:1991;974-978.
27. Dennery P.A., McDonagh A.F., Spitz D.R., Rodgers P.A., Stevenson D.K. Hyperbilirubinemia results in reduced oxidative injury in neonatal Gunn rats exposed to hyperoxia. Free Radic. Biol. Med. 19:1995;395-404.
28. Suttner D.M., Dennery P.A. Reversal of HO-1 related cytoprotection with increased expression is due to reactive iron. FASEB J. 13:1999;1800-1809.
29. Kvam E., Hejmadi V., Ryter S., Pourzand C., Tyrrell R.M. Heme oxygenase activity causes transient hypersensitivity to oxidative ultraviolet A radiation that depends on release of iron from heme. Free Radic. Biol. Med. 28:2000;1191-1196.
30. Gonzales S., Erario M.A., Tomaro M.L. Heme oxygenase-1 induction and dependent increase in ferritin. A protective antioxidant stratagem in hemin-treated rat brain. Dev. Neurosci. 24:2002;161-168.
31. Beinert H. Iron-sulfur proteins: ancient structures, still full of surprises. J. Biol. Inorg. Chem. 5:2000;2-15.
32. Brazzolotto X., Gaillard J., Pantopoulos K., Hentze M.W., Moulis J.M. 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. 274:1999;21625-21630.
33. Kennedy M.C., Antholine W.E., Beinert H. An EPR investigation of the products of the reaction of cytosolic and mitochondrial aconitases with nitric oxide. J. Biol. Chem. 272:1997;20340-20347.
34. Soum E., Drapier J.C. Nitric oxide and peroxynitrite promote complete disruption of the [4Fe-4S] cluster of recombinant human iron regulatory protein 1. J. Biol. Inorg. Chem. 8:2003;226-232.
35. Castro L.A., Robalinho R.L., 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. 359:1998;215-224.
36. 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. 41:2002;7435-7442.
37. Kruszewski M., Starzyński R., Drapier J.C., Smuda E., Lipinski P. Modulation of IRP1 by NO: an unexpected correlation between RNA-binding activity of IRP1 and labile iron pool. Free Radic. Biol. Med. 33(Suppl. 2):2002;S378.
38. Abboud S., Haile D.J. A novel mammalian iron-regulated protein involved in intracellular iron metabolism. J. Biol. Chem. 275:2000;19906-19912.
39. 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. Positional cloning of zebrafish ferroportin1 identifies a conserved vertebrate iron exporter. Nature. 403:2000;776-781.
40. McKie A.T., Marciani P., Rolfs A., Brennan K., Wehr K., Barrow D., Miret S., Bomford A., Peters T.J., Farzaneh F., Hediger M.A., Hentze M.W., Simpson R.J. A novel duodenal iron-regulated transporter, IREG1, implicated in the basolateral transfer of iron to the circulation. Mol. Cell. 5:2000;299-309.
41. Vulpe C.D., Kuo Y.M., Murphy T.L., Cowley L., Askwith C., Libina N., Gitschier J., Anderson G.J. Hephaestin, a ceruloplasmin homologue implicated in intestinal iron transport, is defective in the sla mouse. Nat. Genet. 21:1999;195-199.
42. Wardrop S.L., Watts R.N., Richardson D.R. Nitrogen monoxide activates iron regulatory protein 1 RNA-binding activity by two possible mechanisms: effect on the [4Fe-4S] cluster and iron mobilization from cells. Biochemistry. 39:2000;2748-2758.
43. Watts R.N., Richardson D.R. Nitrogen monoxide (no) and glucose: unexpected links between energy metabolism and no-mediated iron mobilization from cells. J. Biol. Chem. 276:2001;4724-4732.
44. Epsztejn S., Kakhlon O., Glickstein H., Breuer W., Cabantchik I. Fluorescence analysis of the labile iron pool of mammalian cells. Anal. Biochem. 248:1997;31-40.
45. Gackowski D., Kruszewski M., Bartlomiejczyk T., Jawien A., Ciecierski M., Olinski R. The level of 8-oxo-7,8-dihydro-2′-deoxyguanosine is positively correlated with the size of the labile iron pool in human lymphocytes. J. Biol. Inorg. Chem. 7:2002;548-550.
46. Lipinski P., Drapier J.C., Oliveira L., Retmanska H., Sochanowicz B., Kruszewski M. Intracellular iron status as a hallmark of mammalian cell susceptibility to oxidative stress: a study of L5178Y mouse lymphoma cell lines differentially sensitive to H(2)O(2). Blood. 95:2000;2960-2966.
47. Petrat F., De Groot H., Rauen U. Subcellular distribution of chelatable iron: a laser scanning microscopic study in isolated hepatocytes and liver endothelial cells. Biochem. J. 356:2001;61-69.
48. Lai C.C., Huang W.H., Klevay L.M., Gunning W.T. III, Chiu T.H. Antioxidant enzyme gene transcription in copper-deficient rat liver. Free Radic. Biol. Med. 21:1996;233-240.
49. Breuer W., Greenberg E., Cabantchik Z.I. Newly delivered transferrin iron and oxidative cell injury. FEBS Lett. 403:1997;213-219.
50. Henle E.S., Luo Y., Gassmann W., Linn S. Oxidative damage to DNA constituents by iron-mediated fenton reactions. The deoxyguanosine family. J. Biol. Chem. 271:1996;21177-21186.
51. Meneghini R. Iron homeostasis, oxidative stress, and DNA damage. Free Radic. Biol. Med. 23:1997;783-792.
52. McCord J.M. Iron, free radicals, and oxidative injury. Semin. Hematol. 35:1998;5-12.
53. Touati D. Iron and oxidative stress in bacteria. Arch. Biochem. Biophys. 373:2000;1-6.
54. Emerit J., Beaumont C., Trivin F. Iron metabolism, free radicals, and oxidative injury. Biomed. Pharmacother. 55:2001;333-339.
55. Ballmaier D., Pflaum M., Kielbassa C., Epe B. Oxidative DNA damage profiles in mammalian cells. Recent Results Cancer Res. 143:1997;35-47.
56. Wallace S.S. Enzymatic processing of radiation-induced free radical damage in DNA. Radiat. Res. 150:1998;S60-S79.
57. Lloyd D.R., Phillips D.H. Oxidative DNA damage mediated by copper(II), iron(II) and nickel(II) fenton reactions: evidence for site-specific mechanisms in the formation of double-strand breaks, 8-hydroxydeoxyguanosine and putative intrastrand cross-links. Mutat. Res. 424:1999;23-36.
58. Mello-Filho A.C., Meneghini R. Iron is the intracellular metal involved in the production of DNA damage by oxygen radicals. Mutat. Res. 251:1991;109-113.
59. 2. Mutat. Res. 326:1995;155-163.
60. Barbouti A., Doulias P.T., Zhu B.Z., Frei B., Galaris D. Intracellular iron, but not copper, plays a critical role in hydrogen peroxide-induced DNA damage. Free Radic. Biol. Med. 31:2001;490-498.
61. Itoh H., Shioda T., Matsura T., Koyama S., Nakanishi T., Kajiyama G. Iron ion induces mitochondrial DNA damage in HTC rat hepatoma cell culture - role of antioxidants in mitochondrial DNA protection from oxidative stresses. Arch. Biochem. Biophys. 313:1994;120-125.
62. Epsztejn S., Glickstein H., Picard V., Slotki I.N., Breuer W., Beaumont C., Cabantchik Z.I. H-ferritin subunit overexpression in erythroid cells reduces the oxidative stress response and induces multidrug resistance properties. Blood. 94:1999;3593-3603.
63. Kakhlon O., Gruenbaum Y., Cabantchik Z.I. Repression of ferritin expression increases the labile iron pool, oxidative stress, and short-term growth of human erythroleukemia cells. Blood. 97:2001;2863-2871.
64. Lin F., Girotti A.W. Hemin-enhanced resistance of human leukemia cells to oxidative killing: antisense determination of ferritin involvement. Arch. Biochem. Biophys. 352:1998;51-58.
65. Girotti A.W. Lipid hydroperoxide generation, turnover, and effector action in biological systems - review. J. Lipid Res. 39:1998;1529-1542.
66. Tang L., Zhang Y., Qian Z., Shen X. The mechanism of Fe(2+)-initiated lipid peroxidation in liposomes: the dual function of ferrous ions. Biochem. J. 352(Pt 1):2000;27-36.
67. Sochaski M.A., Bartfay W.J., Thorpe S.R., Baynes J.W., Bartfay E., Lehotay D.C., Liu P.P. Lipid peroxidation and protein modification in a mouse model of chronic iron overload. Metabolism. 51:2002;645-651.
68. Santos N.C., Castilho R.F., Meinicke A.R., Hermes-Lima M. The iron chelator pyridoxal isonicotinoyl hydrazone inhibits mitochondrial lipid peroxidation induced by Fe(II)-citrate. Eur. J. Pharmacol. 428:2001;37-44.
69. Traverso N. Oxidative elements in the pathogenesis of atherosclerosis. Ital. Heart J. 2(Suppl. 3):2001;37S-39S.
70. Steinbrecher U.P., Parthasarathy S., Leake D.S., Witztum J.L., Steinberg D. Modification of low density lipoprotein by endothelial cells involves lipid peroxidation and degradation of low density lipoprotein phospholipids. Proc. Natl. Acad. Sci. U.S.A. 81:1984;3883-3887.
71. Gackowski D., Kruszewski M., Jawien A., Ciecierski M., Olinski R. Further evidence that oxidative stress may be a risk factor responsible for the development of atherosclerosis. Free Radic. Biol. Med. 31:2001;542-547.
72. Gieseg S., Duggan S., Gebicki J.M. Peroxidation of proteins before lipids in U937 cells exposed to peroxyl radicals. Biochem. J. 350(Pt 1):2000;215-218.
73. Gebicki S., Gebicki J.M. Formation of peroxides in amino acids and proteins exposed to oxygen free radicals. Biochem. J. 289(Pt 3):1993;743-749.
74. Gebicki S., Gebicki J.M. Crosslinking of DNA and proteins induced by protein hydroperoxides. Biochem. J. 338(Pt 3):1999;629-636.
75. Headlam H.A., Davies M.J. Cell-mediated reduction of protein and peptide hydroperoxides to reactive free radicals. Free Radic. Biol. Med. 34:2003;44-55.
76. Koppenol W.H. The basic chemistry of nitrogen monoxide and peroxynitrite. Free Radic. Biol. Med. 25:1998;385-391.
77. Fridovich I. Oxygen toxicity: a radical explanation. J. Exp. Biol. 201(Pt 8):1998;1203-1209.
78. -. Free Radic. Biol. Med. 26:1999;777-778.
79. Kuhn L.C. Iron and gene expression: molecular mechanisms regulating cellular iron homeostasis. Nutr. Rev. 56:1998;s11-s19.
80. Cazzola M., Skoda R.C. Translational pathophysiology: a novel molecular mechanism of human disease. Blood. 95:2000;3280-3288.
81. Iwai K., Drake S.K., Wehr N.B., Weissman A.M., LaVaute T., Minato N., Klausner R.D., Levine R.L., Rouault T.A. Iron-dependent oxidation, ubiquitination, and degradation of iron regulatory protein. 2. Implications for degradation of oxidized proteins. Proc. Natl. Acad. Sci. U.S.A. 95:1998;4924-4928.
82. Picard V., Govoni G., Jabado N., Gros P. Nramp 2 (DCT1/DMT1) expressed at the plasma membrane transports iron and other divalent cations into a calcein-accessible cytoplasmic pool. J. Biol. Chem. 275:2000;35738-35745.
83. Simonart T., Boelaert J.R., Mosselmans R., Andrei G., Noel J.C., De Clercq E., Snoeck R. Antiproliferative and apoptotic effects of iron chelators on human cervical carcinoma cells. Gynecol. Oncol. 85:2002;95-102.
84. Chaston T.B., Lovejoy D.B., Watts R.N., Richardson D.R. Examination of the antiproliferative activity of iron chelators: multiple cellular targets and the different mechanism of action of triapine compared with desferrioxamine and the potent pyridoxal isonicotinoyl hydrazone analogue 311. Clin. Cancer Res. 9:2003;402-414.
85. Jiang X.P., Wang F., Yang D.C., Elliott R.L., Head J.F. Induction of apoptosis by iron depletion in the human breast cancer MCF-7 cell line and the 13762NF rat mammary adenocarcinoma in vivo. Anticancer Res. 22:2002;2685-2692.
86. Ferry-Dumazet H., Mamani-Matsuda M., Dupouy M., Belloc F., Thiolat D., Marit G., Arock M., Reiffers J., Mossalayi M.D. Nitric oxide induces the apoptosis of human BCR-ABL-positive myeloid leukemia cells: evidence for the chelation of intracellular iron. Leukemia. 16:2002;708-715.
87. Feger F., Ferry-Dumazet H., Mamani M.M., Bordenave J., Dupouy M., Nussler A.K., Arock M., Devevey L., Nafziger J., Guillosson J.J., Reiffers J., Mossalayi M.D. Role of iron in tumor cell protection from the pro-apoptotic effect of nitric oxide. Cancer Res. 61:2001;5289-5294.
88. Kim Y.M., Chung H.T., Simmons R.L., Billiar T.R. Cellular non-heme iron content is a determinant of nitric oxide-mediated apoptosis, necrosis, and caspase inhibition. J. Biol. Chem. 275:2000;10954-10961.
89. Tampo Y., Kotamraju S., Chitambar C.R., Kalivendi S.V., Keszler A., Joseph J., Kalyanaraman B. Oxidative stress-induced iron signaling is responsible for peroxide-dependent oxidation of dichlorodihydrofluorescein in endothelial cells: role of transferrin receptor-dependent iron uptake in apoptosis. Circ. Res. 92:2003;56-63.
90. Hutchings M.I., Crack J.C., Shearer N., Thompson B.J., Thomson A.J., Spiro S. Transcription factor FnrP from Paracoccus denitrificans contains an iron-sulfur cluster and is activated by anoxia: identification of essential cysteine residues. J. Bacteriol. 184:2002;503-508.
91. Chong T.W., Horwitz L.D., Moore J.W., Sowter H.M., Harris A.L. A mycobacterial iron chelator, desferri-exochelin, induces hypoxia-inducible factors 1 and 2, NIP3, and vascular endothelial growth factor in cancer cell lines. Cancer Res. 62:2002;6924-6927.
92. Bruick R.K., McKnight S.L. A conserved family of prolyl-4-hydroxylases that modify HIF. Science. 294:2001;1337-1340.
93. Picard V., Renaudie F., Porcher C., Hentze M.W., Grandchamp B., Beaumont C. Overexpression of the ferritin H subunit in cultured erythroid cells changes the intracellular iron distribution. Blood. 87:1996;2057-2064.
94. Wojewodzka M., Kruszewski M., Iwanenko T., Collins A.R., Szumiel I. Application of the comet assay for monitoring DNA damage in workers exposed to chronic low-dose irradiation. I. Strand breakage. Mutat. Res. 416:1998;21-35.