Superoxide and hydrogen peroxide-dependent inhibition of iron regulatory protein activity: A protective stratagem against oxidative injury

FASEB Journal

Volumn 10, Issue 11, 1996, Pages 1326-1335

  Cairo, Gaetano ^a   Castrusini, Elisa ^a   Minotti, Giorgio ^b   Bernelli Zazzera, Aldo ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b CATHOLIC UNIVERSITY   (Italy)

Author keywords

intracellular stores; iron responsive element; IRP; superoxide anion; superoxide dismutase

Indexed keywords

CATALASE; HYDROGEN PEROXIDE; IRON; IRON REGULATORY FACTOR; SUPEROXIDE; XANTHINE OXIDASE;

ARTICLE; CELL LYSATE; DOWN REGULATION; ENZYME ACTIVITY; IRON METABOLISM; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN ANALYSIS; RNA ANALYSIS; RNA TRANSCRIPTION;

LETHRINIDAE;

EID: 0029815291     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fasebj.10.11.8836047     Document Type: Article

References (53)

1. Aisen, P., and Listowsky, I. (1980) Iron transport and storage proteins. Annu. Rev. Biochem. 49, 357-393
2. Gordeuk, V. R., Bacon, B. R., and Brittenham, G. M. (1987) Iron overload: causes and consequences. Annu. Rev. Nutr. 7, 485-508
3. Worwood, M. (1989) An overview of iron metabolism at a molecular level. I. Int. Med. 381-391
4. Theil, E. C. (1990) Regulation of ferritin and transferrin receptor mRNAs. J. Biol. Chem. 265, 4771-4774
5. Lin, J. J., Walden, W. E., and Thach, R. E. (1990/1991) Induction of ferritin synthesis in vitro: problems of specificity inherent in the use of iron compounds. Enzyme 44, 59-67
6. Kuhn, L. C., and Hentze, M. W. (1992) Coordination of cellular iron metabolism by post-transcriptional gene regulation. J. Inorg. Biochem. 47, 183-195
7. Leibold, E. A., and Guo, B. (1992) Iron-dependent regulation of ferritin and transferrin receptor expression by the iron-responsive element binding proteins. Annu. Rev. Nutr. 12, 345-368
8. Klausner, R. D., Rouault, T. A., and Harford, J. B. (1993) Regulating the fate of mRNA: the control of cellular iron. Cell 72, 19-28
9. Theil, E. C. (1994) Iron regulatory elements (IREs): a family of mRNA non-coding sequences. Biochem. J. 304, 1-11
10. Beinert, H., and Kennedy, M. C. (1993) Aconitase, a two-faced protein: enzyme and iron regulatory factor. FASEB J. 7, 1442-1449
11. O'Halloran, T. V. (1993) Transition metals in the control of gene expression. Science 261, 715-725
12. Hentze, M. W., Rouault, T. A., Harford, J. B., and Klausner, R. D. (1989) Oxidation-reduction and the molecular mechanism of a regulatory RNA-protein interaction. Science 244, 357-359
13. Neupert, B., Thompson, N. A., Meyer, C., and Kuhn, L. C. (1990) A high yield affinity purification method for specific RNA-binding proteins: isolation of the iron regulatory factor from human placenta. Nucleic Acids Res. 18, 51-55
14. Mullner, E. W., Rothenberger, S., Muller, A. M., and Kuhn, L. C. (1992) In vivo and in vitro modulation of the mRNA-binding activity of iron-regulatory factor. Eur. J. Biochem. 208, 597-605
15. Philpott, C. C., Haile, D., Rouault, T. A., and Klausner, R. D. (1993) Modification of free Fe-S cluster cysteine residue in the active iron-responsive element-binding protein prevents RNA binding. J. Biol. Chem. 268, 17655-17658
16. Hirling, H., Henderson, B. R., and Kuhn, L. C. (1994) Mutational analysis of the [4Fe-4S] cluster converting iron regulatory factor from its RNA-binding form to cytoplasmic aconitase. EMBO J. 13, 453-461
17. Martins, E. A., Robalinho, R. L., and Meneghini, R. (1995) Oxidative stress induces activation of a cytosolic protein responsible for control of iron uptake. Arch. Biochem. Biophys. 316, 128-134
18. Pantopoulos, K., and Hentze, M. W. (1995) Rapid responses to oxidative stress mediated by iron regulatory protein. EMBO J. 14, 2917-2924
19. Cairo, C., Tacchini, L., Pogliaghi, C., Anzon, E., Tomasi, A., and Bernelli- Zazzera A. (1995) Induction of ferritin synthesis by oxidative stress: transcriptional and post-transcriptional regulation by expansion of the free iron pool. J. Biol. Chem. 270, 700-703
20. Romaniuk, P. J., and Uhlenbeck, O. C. (1985) Nucleoside and nucleotide inactivalion of R17 coat protein: evidence for a transient covalent RNA-protein bond. Biochemistry 24, 4239-4244
21. Malter, J. S., and Hong, Y. (1991) A redox switch and phosphorylation are involved in the post-translational up-regulation of the adenosine-uridine binding factor by phorbol ester and ionophore. J. Biol. Chem. 266, 3167-3171
22. Clerch, L. B., and Massaro, D. (1992) Oxidation-reduction-sensitive binding of lung protein to rat catalase mRNA. J. Biol. Chem. 267, 2853-2855
23. Chu, E., Voeller, D. M., Morrison, P. F., Jones, K. L., Takechi, T., Maley, G. F., Maley, F., and Allegra, C. J. (1994) The effect of reducing reagents on binding of thymidilate synthase protein to thymidilate synthase messenger RNA. J. Biol. Chem. 269, 20289-20293
24. Levi, S., Yewdall, S. J., Harrison, P. M., Santambrogio, P., Cozzi, A., Rovida, E., Albertini, A., and Arosio, P. (1992) Evidence that H- and L-chain have cooperative roles in the iron uptake mechanism of human ferritin. Biochem. J. 288, 591-596
25. Minotti, G., Cavaliere, A. F., Mordente, A., Rossi, M., Schiavello, R., Zamparelli, R., and Possati, G. F. (1995) Secondary alcohol metabolites mediate iron delocalization in cytosolic fractions of myocardial biopsies exposed to anticancer anthracyclines. J. Clin. Invest. 95, 1595-1605
26. Leibold E. A., and Munro H. N. (1988) Cytoplasmic protein binds in vitro to a highly conserved sequence in the 5′ untranslated region of ferritin heavy and light subunit mRNA. Proc. Natl. Acad. Sci. USA 85, 2171-2175
27. Gonzalez Flecha, B., Llesuy, S., and Boveris, A. (1991) Hydroperoxide-initiated chemiluminescence: an assay for oxidative stress in biopsies of heart, liver and muscle. Free Rad. Biol. Med. 10, 93-100
28. Stralin, P., and Marklund, S. L. (1994) Effects of oxidative stress on expression of extracellular superoxide dismutase, CuZn-superoxide dismutase and Mn-superoxide dismutase in human dermal fibroblasts. Biochem J. 298, 347-352
29. Mullner, E. W., Neupert, B., and Kuhn, L. C. (1989) A specific mRNA binding factor regulates the iron-dependent stability of cytoplasmic transferrin receptor mRNA. Cell 58, 373-382
30. Cairo, G., and Pietrangelo, A. (1994) Transferrin receptor gene expression during rat liver regeneration. Evidence for post-transcriptional regulation by iron regulatory factors, a second iron-responsive element binding protein. J. Biol. Chem. 269, 6405-6409
31. 3+: evidence for superoxide dismutaselike activity. Arch. Biochem. Biophys. 253, 257-267
32. Drapier, J. C., and Hibbs, J. B., Jr. (1986) Murine cytotoxic activated macrophages inhibit aconitase in tumor cells. J. Clin. Invest. 78, 790-797
33. Ulvik, R., and Romslo, I. (1979) Studies on the mobilization of iron from ferritin by isolated rat liver mitochondria. Biochim. Biophys. Acta 588, 256-271
34. Henderson, B. C., Seiser, C., and Kuhn, L. C. (1993) Characterization of a second RNA-binding protein in rodents with specificity for iron-responsive elements. J. Biol. Chem. 269, 27327-27334
35. Guo, B., Yu, Y., and Leibold, E. A. (1994) Iron regulates cytoplasmic levels of a novel iron-responsive element-binding protein without aconitase activity. J. Biol. Chem. 269, 24252-24260
36. Biemond, P., Swaak, A. G. J., Beidorff, C. M., and Koster, J. F. (1986) Superoxide-dependent and -independent mechanisms of iron mobilization from ferritin by xanthine oxidase. Biochem. J. 239, 169-173
37. Minotti, G. (1993) Sources and role of iron in lipid peroxidation. Chem. Res. Toxicol. 6, 134-146
38. Rubin, E., and Farber, J.L. (1994) Reversible cell injury. In Pathology, 2nd Ed (Rubin, E., and Farber, J. L., eds) pp. 11-31, J. B. Lippincott Co., Philadelphia
39. Ryan, T.P and Aust, S.D. (1992) The role of iron in oxygen radical-mediated toxicities. Crit. Rev. Toxicol. 22, 119-141
40. Minotti, G. (1992) The role of an endogenous nonheme iron in microsomal redox reactions. Arch. Biochem. Biophys. 297, 189-198
41. Powis, G. (1989) Free radical formation by antitumor quinones. Free Rad. Biol. Med. 6, 63-101
42. Yamazaki, I., and Piette, L. (1991) EPR spin-trapping studies on the oxidizing species formed in the reaction of the ferrous ion with hydrogen peroxide. J. Am. Chem. Soc. 113, 7588-7593
43. 2-reactive species in oxygen toxicity in biology. J. Biol. Chem. 265, 13589-13594
44. Kadir, F. H., al-Massad, F. K., Fatemi, S. J., Singh, H. K., Wilson, M. T., and Moore, G. R. (1991) Electron transfer between horse ferritin and ferrihaemoproteins. Biochem. J. 278, 817-820
45. Watt, R. K., Frankel, R. B., and Watt, G. D. (1992) Redox reactions of apo mammalian ferritin. Biochemistry 31, 9673-9679
46. Flint, D. H., Tuminello, J. F., and Emptage, M. H. (1993) The inactivation of Fe-S containing hydro-lyases by superoxide. J. Biol. Chem. 268, 22369-22376
47. Torchinsky, Y. M. (1981) Sulfur in Proteins, pp. 48-56, Pergamon Press, New York
48. Rady, R., Bush, K. M., Cosgrove, T. P., and Freeman, B. A. (1991) Reactions of xanthine oxidase-derived oxidants with lipids and proteins of human plasma. Arch. Biochem. Biophys. 286, 117-125
49. Thomas, J. P., Bachowski, G. J., and Girotti, A. W. (1986) Inhibition of cell membrane lipid peroxidation by cadmium and zinc metallothioneins. Biochim. Biophys. Acta 884, 448-461
50. Fliss, H. F., and Menard, M. (1991) Oxidant induced mobilization of zinc from metallothionein. Arch. Biochem. Biophys. 293, 195-199
51. Vile, G. F., and Tyrrel, R. M. (1993) Oxidative stress resulting from ultraviolet A irradiation of human skin fibroblasts leads to a heme oxygenase-dependent increase in ferritin. J. Biol. Chem. 268, 14678-14681
52. Balla, G., Jacob, H. S., Balla, J., Rosenberg, M., Nath, K., Apple, F., Eaton, J. W., and Vercellolti, G. M. (1992) Ferritin: a cytoprotective antioxidant stratagem of endothelium. J. Biol. Chem. 267, 18148-18153
53. Kehrer, J. P. (1989) Concepts related to the study of reactive oxygen and cardiac reperfusion injury. Free Rad. Res. Commun. 5, 305-312