Iron homeostasis, oxidative stress, and DNA damage

Free Radical Biology and Medicine

Volumn 23, Issue 5, 1997, Pages 783-792

  Meneghini, Rogerio ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Calcium; DNA strand break; Fenton chemistry; Ferritin; Heme oxygenase; Hydroxyl radical; Iron regulatory protein; Iron responsive element; Metallothionein; Nuclease; Phospho glycolate; Transferrin receptor

Indexed keywords

HEME OXYGENASE; HYDROGEN PEROXIDE; IRON; METALLOTHIONEIN; NUCLEIC ACID BASE; TRANSFERRIN RECEPTOR;

DNA DAMAGE; DNA STRAND BREAKAGE; HOMEOSTASIS; IRON METABOLISM; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; REACTION ANALYSIS; REVIEW;

ANIMALS; CALCIUM; CELL NUCLEUS; DNA DAMAGE; HOMEOSTASIS; HUMANS; HYDROXYL RADICAL; IRON; METALLOTHIONEIN; OXIDATIVE STRESS;

EID: 0030857377     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0891-5849(97)00016-6     Document Type: Review

References (74)

1. Halliwell B., Gutteridge J. M. C. Free radicals in biology and medicine. 1989;Clarendon Press, Oxford.
2. Sandstrom B. E., Granstrom M., Marklund S. L. New roles for quin2: Powerful transition-metal ion chelator that inhibits copper-, but potentiates iron-driven, Fenton-type reactions. Free Radic. Biol. Med. 16:1994;177-185.
3. 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.
4. Halliwell B., Aruoma O. I. DNA damage by oxygen-derived species: Its mechanism and measurement in mammalian systems. FEBS Lett. 281:1991;9-19.
5. Dizdaroglu M. Measurements of radiation-induced damage to DNA at the molecular level. Int. J. Radiat. Biol. 61:1992;175-183.
6. Moriya M. Single-stranded shuttle phagemid for mutagenesis studies in mammalian cells: 8-Oxoguanine in DNA induces targeted G×C → T×A transversions in simian kidney cells. Proc. Natl. Acad. Sci. USA. 90:1993;1122-1126.
7. Cheng K. C., Cahill D. S., Kasai H., Nishimura S., Loeb L. A. 8-Hydroxyguanine, an abundant form of oxidative DNA damage, causes G→T and A→C substitutions. J. Biol. Chem. 267:1992;166-172.
8. Demple B., Harrison L. Repair of oxidative damage to DNA: Enzymology and biology. Annu. Rev. Biochem. 63:1994;915-948.
9. Boiteux S., Gajewiski E., Laval J., Dizdaroglu M. Substrate specificity of the Escherichia coli Fpg protein (formamidopyrimidine-DNA glycosylase): Excision of purine lesions in DNA produced by ionizing radiation or photosensitization. Biochemistry. 31:1992;106-110.
10. Michaels M. L., Cruz C., Grollman A. P., Miller J. H. Evidence that MutY and MutM combine to prevent mutations by an oxidatively damaged form of guanine in DNA. Proc. Natl. Acad. Sci. USA. 89:1992;7022-7025.
11. Breen A. P., Murphy J. A. Reactions of oxyl radicals with DNA. Free Radic. Biol. Med. 18:1995;1033-1077.
12. von Sontag C. Carbohydrate radicals: From ethylene glycol to DNA strand breakage. Int. J. Radiat. Biol. 46:1984;507-519.
13. Mello-Filho A. C., Meneghini R. In vivo formation of single-strand breaks in DNA by hydrogen peroxide is mediated by the Haber-Weiss reaction. Biochim. Biophys. Acta. 781:1984;56-63.
14. Meneghini R. Genotoxicity of active oxygen species in mammalian cells. Mutat. Res. 195:1988;215-230.
15. Stevens R. G., Jones D. Y., Micozzi M. S., Taylor P. R. Body iron stores and risk of cancer. N. Engl. J. Med. 319:1988;1047-1056.
16. Ames B. N., Shigenaga M. K., Hagen T. M. Oxidants, antioxidants, and the degenerative diseases of aging. Proc. Natl. Acad. Sci. USA. 90:1993;7915-7922.
17. Nassi-Calo L., Mello-Filho A.C., Meneghini R. o-Phenanthroline protects mammalian cells from hydrogen peroxide-induced gene mutation and morphological transformation. Carcinogenesis. 10:1989;1055-1057.
18. Bali P. K., Zak O., Aisen P. A new role for the transferrin receptor in the release of iron from transferrin. Biochemistry. 30:1991;324-328.
19. Guerinot M. L. Microbial iron transport. Annu. Rev. Microbiol. 48:1994;743-772.
20. 2. Eur. J. Biochem. 209:1992;621-627.
21. Eide D., Davis-Kaplan S., Jordan I., Sipe D., Kaplan J. Regulation of iron uptake in Saccharomyces cerevisiae. The ferrireductase and Fe(II) transporter are regulated independently. J. Biol. Chem. 267:1992;20774-20781.
22. Askwith C., Eide D., Van Ho A., Bernard P. S., Li L., Davis-Kaplan S., Sipe D. M., Kaplan J. The FET3 gene of S. cerevisiae encodes a multicopper oxidase required for ferrous iron uptake. Cell. 76:1994;403-410.
23. Dancis A., Yuan D. S., Haile D., Askwith C., Eide D., Moehle C., Kaplan J., Klausner R. D. Molecular characterization of a copper transport protein in S. cerevisiae: An unexpected role for copper in iron transport. Cell. 76:1994;393-402.
24. Watkins J. A., Altazan J. D., Elder P., Li C.-Y., Nuñez M.-T., Cui X.-X., Glass J. Kinetic characterization of reductant dependent processes of iron mobilization from endocytic vesicles. Biochemistry. 31:1992;5820-5830.
25. Aisen P. The transferrin receptor and the release of iron from transferrin. Adv. Exp. Med. Biol. 356:1994;31-40.
26. Klausner R. D., Rouault T. A., Harford J. B. Regulating the fate of mRNA: The control of cellular iron metabolism. Cell. 72:1993;19-28.
27. Kuhn L. C. Molecular regulation of iron proteins. Hershko C. Baillière's clinical haematology. 7:1994;763-785 Baillière Tindall, London.
28. Leibold E. A., Munro H. N. Cytoplasmic protein binds in vitro to a high conserved sequence in the 5′-untranslated region of ferritin heavy and light subunit mRNAs. Proc. Natl. Acad. Sci. USA. 85:1988;2171-2175.
29. Crichton R. R., Ward R. J. Iron metabolism-New perspectives in view. Biochemistry. 31:1992;11255-11264.
30. Reif D. W. Ferritin as a source of iron for oxidative stress. Free Radic. Biol. Med. 12:1992;417-427.
31. Oteiza P. I., Kleinman C. G., Demasi M., Bechara E. J. H. 5-Aminolevulinic acid induces iron release from ferritin. Arch. Biochem. Biophys. 316:1995;607-611.
32. Rouault T. A., Stout C. D., Kaptain S., Harford J. B., Klausner R. D. Structural relationship between an iron-regulated RNA-binding protein (IRE-BP) and aconitase: Functional implications. Cell. 64:1991;881-883.
33. Haile D. J., Rouault T. A., Harford J. B., Kennedy M. C., Blondin G. A., Beinert H., Klausner R. D. 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. 89:1992;11735-11739.
34. Henderson B. R., Menotti E., Kuhn L. C. Iron regulatory proteins 1 and 2 bind distinct sets of RNA target sequences. J. Biol. Chem. 271:1996;4900-4908.
35. Haile D. J., Rouault T. A., Tang C.K., Chin J., Harford J. B., Klausner R. D. Reciprocal control of RNA-binding and aconitase activity in the regulation of the iron-responsive element binding protein: Role of the iron-sulfur cluster. Proc. Natl. Acad. Sci. USA. 89:1992;7536-7540.
36. Hartwig A., Klyszcz-Nasko H., Schlepegrell R., Beyersmann D. Cellular damage by ferric nitrilotriacetate and ferric citrate in V79 cells: Interralationship between lipid peroxidation, DNA strand breaks and sister chromatid exchanges. Carcinogenesis. 14:1993;107-112.
37. Umemura T., Sai K., Takagi A., Hasegawa R., Yuji K. Formation of 8-hydroxydeoxyguanosine (8-OH-dG) in rat kidney DNA after intraperitoneal adminstration of ferric nitrilotriacetate (Fe-NTA). Carcinogenesis. 11:1990;345-347.
38. Hartwig A., Schlepegrell R. Induction of oxidative DNA damage by ferric iron in mammalian cells. Carcinogenesis. 16:1995;3009-3013.
39. Nascimento A. L. T. O., Meneghini R. Cells transfected with transferrin receptor cDNA lacking the iron regulatory domain become more sensitive to the DNA damaging action of oxidative stress. Carcinogenesis. 16:1995;1335-1338.
40. Meneghini R., Benfato M. S., Bertoncini C. R. A., Carvalho H., Gurgueira S., Robalinho R. L., Teixeira H. D., Wendel C. M. A., Nascimento A. L. T. O. Iron homeostasis and oxidative DNA damage. Cancer J. 8:1995;109-113.
41. Girelli D., Corrocher R., Bisceglia L., Olivieri O., De Franceschi L., Zelante L., Gasparini P. Molecular basis for the recently described hereditary hyperferritinemia cataract syndrome: A mutation in the iron-responsive element of ferritin L-subunit gene (the "Verona mutation"). Blood. 86:1995;4050-4053.
42. Beaumont C., Leneuve P., Devaux I., Scoazec J. Y., Berthier M., Loiseau M. N., Grandchamp B., Bonneau D. Mutation in the iron responsive element of the L ferritin mRNA in a family with dominant hyperferritinaemia and cataract. Nat. Genet. 11:1995;444-446.
43. 2 and chelated iron. Free Radic. Biol. Med. 7:1989;499-505.
44. McGahan M. C., Harned J., Grimes A. M., Fleisher L. N. Regulation of ferritin levels in cultured lens epithelial cells. Exp. Eye Res. 59:1994;551-556.
45. Li Z., Demple B. SoxS, an activator of superoxide stress genes in Escherichia coli. Purification and interaction with DNA. J. Biol. Chem. 269:1994;18371-18377.
46. Rao G. N., Berk B. C. Active oxygen species stimulate vascular smooth muscle cell growth and proto-oncogene expression. Circ. Res. 70:1992;593-599.
47. Burdon R. H. Superoxide and hydrogen peroxide in relation to mammalian cell proliferation. Free Radic. Biol. Med. 18:1995;775-794.
48. Chen Q. L., Olashaw N., Wu J. Participation of reactive oxygen species in the lysophosphatidic acid-stimulated mitogen-activated protein kinase kinase activation pathway. J. Biol. Chem. 270:1995;28499-28502.
49. Keyse S. M., Tyrrell R. M. Both near UV radiation and the oxidizing agent hydrogen peroxide induce a 32 KDa stress protein in normal skin fibroblasts. J. Biol. Chem. 262:1987;14821-14825.
50. 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.
51. Vile G. F., Tyrrell R. M. Oxidative stress resulting from ultraviolet A irradiation of human skin fibroblasts leads to a heme oxygenase-dependent increase in ferritin. J. Biol. Chem. 268:1993;14678-14681.
52. Cairo G., Tacchini L., Pogliaghi G., Anzon E., Tomasi A., Bernelli-Zazzera A. Induction of ferritin synthesis by oxidative stress. Transcriptional and posttranscriptional regulation by expansion of the "free" iron pool. J. Biol. Chem. 270:1995;700-703.
53. Vile G. F., Basu-Modak S., Waltner C., Tyrrell R. M. Heme oxygenase 1 mediates an adaptive response to oxidative stress in human skin fibroblasts. Proc. Natl. Acad. Sci. USA. 91:1994;2607-2610.
54. Martins E. A. L., Robalinho R. L., Meneghini R. Oxidative stress induces activation of a cytosolic protein responsible for control of iron uptake. Arch. Biochem. Biophys. 316:1995;128-134.
55. Pantopoulos K., Hentze M. W. Rapid responses to oxidative stress mediated by iron regulatory protein. EMBO J. 14:1995;2917-2924.
56. Drapier J. C., Hirling H., Wietzerbin J., Kaldy P., Kuhn L. C. Biosynthesis of nitric oxide activates iron regulatory factor in macrophages. EMBO J. 12:1993;3643-3649.
57. 2+ concentration and citotoxicity in hepatocytes exposed to oxidative stress. Toxicology. 52:1988;55-63.
58. Cantoni O., Sestili P., Cattabeni F., Bellomo G., Pou S., Cohen M., Cerutti P. Calcium chelator quin 2 prevents hydrogen peroxide-induced DNA breakage and cytotoxicity. Eur. J. Biochem. 182:1989;209-212.
59. Burkitt M. J., Milne L., Tsang S. Y., Tam S. C. Calcium indicator dye Quin2 inhibits hydrogen peroxide-induced DNA strand break formation via chelation of iron. Arch. Biochem. Biophys. 311:1994;321-328.
60. Bertoncini C. R. A., Meneghini R. DNA strand breaks produced by oxidative stress in mammalian cells exhibit 3′-phosphoglycolate termini. Nucleic Acids Res. 23:1995;2995-3002.
61. Csermely P., Fodor P., Somogyi J. The tumor promoter tetradecanoylphobol-13-acetate elicits the redistribution of heavy metals in subcellular fractions of rabbit thymocytes as measured by plasma emission spectroscopy. Carcinogenesis. 8:1987;1663-1666.
62. Smith A. G., Carthew P., Francis J. E., Edwards R. E., Dinsdale D. Characterization and accumulation of ferritin in hepatocyte nuclei of mice with iron overload. Hepatology. 12:1990;1399-1405.
63. Kukielka E., Cederbaum A. I. Ferritin stimulation of hydroxyl radical production by rat liver nuclei. Arch. Biochem. Biophys. 308:1994;70-77.
64. Prince R. C., Grossman M. J. Novel iron-sulfur clusters. Trends Biochem. Sci. 18:1993;153-154.
65. Hidalgo E., Demple B. An iron-sulfur center essential for transcriptional activation by the redox-sensing SoxR protein. EMBO J. 13:1994;138-146.
66. Zitomer R. S., Lowry C. V. Regulation of gene expression by oxygen in Saccharomyces cerevisiae. Microbiol. Rev. 56:1992;1-11.
67. Marsden M. P. F., Laemmli U. K. Metaphase chromosome structure: evidence for a radical loop model. Cell. 17:1979;849-858.
68. 2+ concentration in isolated rat liver nuclei. Proc. Natl. Acad. Sci. USA. 86:1989;453-457.
69. Gurgueira S. A., Meneghini R. An ATP-dependent iron transport system in isolated rat liver nuclei. J. Biol. Chem. 271:1996;13616-13620.
70. Thornalley P. J., Vasak M. Possible role for metallothionein in protection against radiation-induced oxidative stress. Kinetics and mechanism of its reaction with superoxide and hydroxyl radicals. Biochim. Biophys. Acta. 827:1985;36-44.
71. Tsujikawa K., Imai T., Kakutani M., Kayamori Y., Mimura T., Otaki N., Kimura M., Fukuyama R., Shimizu N. Localization of metallothionein in nuclei of growing primary cultured adult rat hepatocytes. FEBS Lett. 283:1991;239-242.
72. Chubatsu L. S., Meneghini R. Metallothionein protects DNA from oxidative damage. Biochem. J. 291:1993;193-198.
73. Goncharova E. I., Rossman T. G. A role for metallothionein and zinc in spontaneous mutagenesis. Cancer Res. 54:1994;5318-5323.
74. Reznikoff C. A., Bertram J. S., Brankow D. W., Heidelberger C. Quantitative and qualitative studies of chemical transformation of cloned C3H mouse embryo cells sensitive to postconfluent inhibition of cell division. Cancer J. 33:1973;3239-3249.