Iron-induced tissue damage and cancer: The role of reactive oxygen species-free radicals

Pathology International

Volumn 46, Issue 5, 1996, Pages 311-332

  Okada, Shigeru ^a  

^a OKAYAMA UNIVERSITY MEDICAL SCHOOL   (Japan)

Author keywords

acute tubular necrosis; animal models; free radicals; iron; nitrilotriacetate; reactive oxygen species; renal cell carcinoma

Indexed keywords

FREE RADICAL; IRON; OXYGEN RADICAL; REACTIVE OXYGEN METABOLITE;

ARTICLE; CARCINOGENESIS; HISTOPATHOLOGY; HUMAN; LIPID PEROXIDATION; MALIGNANT NEOPLASTIC DISEASE; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; TISSUE INJURY;

EID: 0029999597     PISSN: 13205463     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1440-1827.1996.tb03617.x     Document Type: Article

References (109)

1. Dargel R. Lipid peroxidation: A common pathogenetic mechanism (Review). Exp. Toxicol. Pathol. 1992; 44: 169-181.
2. MacSween RNM, Whaley K. Muir's Textbook of Pathology. Edward Arnold, Kent, 1992.
3. Contran RS, Kumar V, Robbins SL. Robbins Pathologic Basis of Disease, 5th edn. WB Saunders, Philadelphia, 1994.
4. Bolli R. Oxygen-derived free radicals and myocardial reperfusion injury: An overview. Cafdiovasc. Drug Therapy 1991; 5: 249-268.
5. McCord JM, Omar BA. Sources of free radicals. Toxicol. Ind. Health 1993; 9: 23-37.
6. Ingram LL, Meyer DL. Biochemistry of dioxygen. In: Frieden E, ed. Biochemistry of the Elements. Plenum Press, New York, 1985.
7. Halliwell B. The chemistry of free radicals. Toxicol. Ind. Health 1993; 9: 1-21.
8. Pryor WA. Free radicals and lipid peroxidation. What they are and how they got that way. In: Frei B, ed. Natural Antioxidants in Human Health and Disease. Academic Press, San Diego, 1994; 1-24.
9. Thurman RG, Connor HD, Knecht KT et al. Spin trapping in the perfused liver: carbon tetrachloride as a model system. In: Ballet F, Thurman RG, eds. Research in Perfused Liver. INSERM/ John Libbey, 1991; 69-82.
10. Lee CK, Brown BG, Rice WYJ, Doolittle DJ. Role of oxygen free radicals in the induction of sister chromatid exchanges by cigarette smoke. Environ. Mol. Mutagen. 1989; 13: 54-59.
11. Pryor W. Biological effects of cigarette smoke, wood smoke, and the smoke from plastics: The use of electron spin resonance. Free Rad. Biol. Med. 1992; 13: 659-676.
12. Loft S, Fischernielsen A, Jeding IB, Vistisen K, Poulsen HE. 8-Hydroxydeoxyguanosine as a urinary biomarker of oxidative DNA damage. J. Toxicol. Environ. Health 1993; 40: 391-404.
13. Halliwell B, Gutteridge JMC. Free Radicals in Biology and Medicine, 2nd edn. Oxford University Press, Oxford, 1989.
14. Smith JK, Carden DL, Grisham MB, Granger DN, Korthuis RJ. Role of iron in postischemic microvascular injury. Am. J. Physiol. 1989; 26: H1472-1477.
15. Das DK. Cellular, biochemical, and molecular aspects of reperfusion injury. Ann. N.Y. Acad. Sci. 1994; 723
16. Smith JA. Neutrophils, host defense, and inflammation: A double-edged sword. J. Leukocyte Biol. 1994; 56: 672-686.
17. Halliwell B. Free radicals, antioxidants, and human disease: Curiosity, cause or consequence? Lancet 1994; 344: 721-724.
18. Halliwell B, Gutteridge JMC, Cross CE. Free radicals, antioxidants, and human disease: Where are we now? J. Lab. Clin. Med. 1992; 119: 598-620.
19. Packer L. Oxygen radicals in biological systems. In: Method in Enzymology, Vol. 244. Academic Press, San Diego, 1994; 000-000.
20. Pompella A, Maellaro E, Casini AF, Comporti M. Histochemical detection of lipid peroxidation in the liver of bromobenzene-poisoned mice. Am. J. Pathol. 1987; 129: 295-301.
21. Toyokuni S, Uchida K, Okamoto K et al. Formation of 4-hydroxy-2-nonenal-modified proteins in the renal proximal tubules of rats treated with a renal carcinogen, ferric nitrilotriacetate. Proc. Natl Acad. Sci. USA 1994; 91: 2616-2620.
22. Uchida K, Szweda LI, Chae HZ, Stadtman ER. Immunochemical detection of 4-hydroxynonenal protein adducts in oxidized hepatocytes. Proc. Natl Acad. Sci. USA 1993; 90: 8742-8746.
23. Aust SD, Morehouse LA, Thomas CE. Role of metals on oxygen radical reactions. J. Free Rad. Biol. Med. 1985; 1: 3-25.
24. Halliwell B, Gutteridge JMC. Role of free radicals and catalytic metal ions in human disease: An overview. In: Packer L, Glazer AN, eds. Oxygen Radicals in Biological Systems. Academic Press, San Diego, 1990; 1-85.
25. Hamazaki S, Okada S, Li J-L, Toyokuni S, Midorikawa O. Oxygen reduction and lipid peroxidation by iron chelates with special reference to ferric nitrilotriacetate. Arch. Biochem. Biophys. 1989; 272: 10-17.
26. Spiro T. Chemistry and biochemistry of iron. In: Brown EB, Aisen P, Fielding J, Crichton RR, eds. Proteins of Iron Metabolism. Grune & Stratton, New York, 1977; xxiii-xxxii.
27. 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.
28. Tsukihara T, Aoyama H, Yamashita E et al. Structures of metal sites of oxidized bovine heart cytochrome c oxidase at 2.8Å. Science 1995; 269: 1069-1074.
29. Spear N, Aust SD. Thiol-mediated NTA-Fe(III) reduction and lipid peroxidation. Arch. Biochem. Biophys. 1994; 312: 198-202.
30. Spiro TG, Saltman P. Inorganic chemistry. In: Jacobs A, Worwood M, eds. Iron in Biochemistry and Medicine. Academic Press, New York, 1974; 1-28.
31. Neilands JB, Konopka K, Schwyn B et al. Comparative biochemistry of microbial iron. In: Winkelmann G, van der Helm D, Neilands JB, eds. Iron Transport in Microbes, Plants and Animals. VCH Verlagsgesellschaft, Weinheim, 1987; 3-33.
32. Anderegg G. Critical survey of stability constants of NTA complexes. Pure Appl. Chem. 1982; 54: 2693-2758.
33. Goyer RA, Falk HL, Hogan M, Feldman DD, Richter W. Renal tumors in rats given trisodium nitrilotriacetic acid in drinking water for 2 years. J. Natl Cancer Inst. 1981; 66: 869-880.
34. Anderson RL, Bishop WE, Campbell RL. A review of the environmental and mammalian toxicology of nitrilotriacetic acid. CRC Critical Rev. Toxicol. 1985; 15: 1-102.
35. Nakano K, Okada S, Toyokuni S, Midorikawa O. Renal changes induced by chronic oral administration of potassium bromate or ferric nitrilotriacetate in Wistar rats. Naika Hokann (Jpn. Arch. Intern. Med. 1989; 36: 1989 (In Japanese with English abstract).
36. Nishida Y, Yoshizawa K, Akamatsu T. Preparation of iron (III) complex with nitrilotriacetic acid and origin of its unique reactivity. Chem. Lett. 1991; 1521-1524.
37. Awai M, Narasaki M, Yamanoi Y, Seno S. Induction of diabetes in animals by parenteral administration of ferric nitrilotriacetate. Am. J. Pathol. 1979; 95: 663-674.
38. Okada S, Midorikawa O. Induction of the rat renal adenocarcinoma by Fe-nitrilotriacetate (Fe-NTA) Naika Hokan (Jpn. Arch. Intern. Med.) 1982; 29: 485-491. (in Japanese with English abstract).
39. Hamazaki S, Okada S, Ebina Y, Fujioka M, Midorikawa O. Nephrotoxicity of ferric nitrilotriacetate: An electron microscopical and metabolic study. Am. J. Pathol. 1986; 123: 343-350.
40. Ebina Y, Okada S, Hamazaki S et al. Nephrotoxicity and renal cell carcinoma after use of iron- and aluminum-nitrilotriacetate complexes in rats. J. Natl Cancer Inst. 1986; 76: 107-113.
41. Li J-L, OkadaS, Hamazaki S, Ebina Y, Midorikawa O. Subacute nephrotoxicity and induction of renal cell carcinoma in mice treated with ferric nitrilotriacetate. Cancer Res. 1987; 47: 1867-1869.
42. Inoue S, Kawanishi S. Hydroxyl radical production and human DNA damage induced by ferric nitrilotriacetate and hydrogen peroxide. Cancer Res. 1987; 47: 6522-6527.
43. Aruoma OI, Halliwell B, Gajewski E, Dizdaroglu M. Damage to the bases in DNA induced by hydrogen peroxide and ferric ion chelates. J. Biol. Chem. 1989; 264: 20509-20512.
44. Fukuzawa K, Fujii T. Peroxide dependent and independent lipid peroxidation: Site-specific mechanisms of initiation by chelated iron and inhibition by α-tocopherol. Lipids 1992; 27: 227-233.
45. Fukuzawa K, Fujii T, Ikebata W. Lipid peroxidation by iron chelated with nitrilotriacetate. (1) Induction dependent on hydrogen peroxide and lipid hydroperoxide. In: Yagi K, Kondo M, Niki E, Yoshikawa T, eds. Oxygen Radicals. Elsevier Science Publishers, Amsterdam, 1992; 237-240.
46. Fukuzawa K, Fujii T, Mukai K. Lipid peroxidation by iron chelated with nitrilotriacetate. (2) Induction without the requirement for hydrogen peroxide and lipid hydroperoxides. In: Yagi K, Kondo M, Niki E, Yoshikawa T, eds. Oxygen Radicals. Elsevier Science Publishers, Amsterdam, 1992; 241-244.
47. Toyokuni S, Okada S, Hamazaki S et al. Combined histochemical and biochemical analysis of sex hormone dependence of ferric nitrilotriacetate-induced renal lipid peroxidation in ddY mice. Cancer Res. 1990; 50: 5574-5580.
48. Okada S, Fukunaga Y, Hamazaki S, Yamada Y, Toyokuni S. Sex differences in the localization and severity of ferric nitrilotriacetate-induced lipid peroxidation in the mouse kidney. Acta Pathol. Jpn. 1991; 41: 221-226.
49. Li J-L, Okada S, Hamazaki S, Denk I-L, Midorikawa O. Sex differences in ferric nitrilotriacetate-induced lipid peroxidation and nephrotoxicity in mice. Biochim. Biophys. Acta 1988; 963: 82-87.
50. Deguchi J, Miyamoto M, Okada S. Sex hormone dependent renal cell carcinogenesis induced by ferric nitrilotriacetate in Wistar rats. Jpn. J. Cancer Res. 1995; 86: 1068-1071.
51. Okada S, Hamazaki S, Ebina Y, Li J-L, Midorikawa O. Nephrotoxicity and its prevention by vitamin E in ferric nitrilotriacetate-promoted lipid peroxidation. Biochim. Biophys. Acta 1987; 922: 28-33.
52. Toyokuni S, Okada S, Hamazaki S et al. Cirrhosis of the liver induced by cupric nitrilotriacetate in Wistar rats: An experimental model of copper toxicosis. Am. J. Pathol. 1989; 134: 1263-1274.
53. Liu M, Okada S. Induction of free radicals and tumors in the kidneys of Wistar rats by ferric ethylenediamine-N, N′-diacetate. Carcinogenesis 1994; 15: 2817-2821.
54. Hamazaki S, Okada S, Ebina Y, Li J-L, Midorikawa O. Effect of dietary vitamin E on ferric nitrilotriacetate-induced nephrotoxicity in rats. Toxicol. Appl. Pharmacol. 1988; 92: 500-506.
55. Gutteridge JMC, Halliwell B. Radical-promoting loosely-bound iron in biological fluids and the bleomycin assay. Life Chem. Rep. 1987; 4: 113-142.
56. Liu M, Okada S, Kawabata T. Radical-promoting 'free' iron level in the serum of rats treated with ferric nitrilotriacetate: Comparison with other iron chelate complexes. Acta Med. Okayama 1991; 45: 401-408.
57. Zhang D, Okada S, Kawabata T, Yasuda T. An improved simple colorimetric method for quantitation of non-transferrin-bound iron in serum. Biochem. Mol. Biol. Int. 1995; 35: 635-641.
58. Kasai H, Nishimura S. Hydroxylation of deoxyguanosine at the C-8 position by ascorbic acid and other reducing agents. Nucleic Acids Res. 1984; 12: 2137-2145.
59. Floyd RA. The role of 8-hydroxyguanosine in carcinogenesis. Carcinogenesis 1990; 11: 1447-1450.
60. Adachi S, Zeisig M, Moller L. Improvements in the analytical method for 8-hydroxydeoxyguanosine in nuclear DNA. Carcinogenesis 1995; 16: 253-258.
61. Umemura T, Sai K, Takagi A, Hasegawa R, Kurokawa Y. Formation of 8-hydroxydeoxyguanosine (8-OH-dG) in rat kidney DNA after intraperitoneal administration of ferric nitrilotriacetate (Fe-NTA). Carcinogenesis 1990; 11: 345-347.
62. Toyokuni S, Mori T, Dizdaroglu M. DNA base modifications in renal chromatin of Wistar rats treated with a renal carcinogen, ferric nitrilotriacetate. Int. J. Cancer 1994; 57: 123-128.
63. Yamaguchi R, Hirano T, Asami S, Sugita A, Kasai H. Induction of 8-hydroxyguanine repair enzymes in the rat kidney after administration of ferric nitrilotriacetate, a renal carcinogen (abstract in Japanese). Proc. Jpn. Cancer Assoc. 1995 (54th Annual Meeting); A49.
64. Sarker AH, Watanabe S, Seki S, Akiyama T, Okada S. Oxygen radical-induced single-strand DNA breaks and repair of the damage in a cell-free system. Mutation Res. 1995; 337: 85-95.
65. Uchida K, Fukuda A, Kawakishi S, Hiai H, Toyokuni S. A renal carcinogen ferric nitrilotriacetate mediates a temporary accumulation of aldehyde-modified proteins within cytosolic compartment of rat kidney. Arch. Biochem. Biophys. 1995; 317: 405-411.
66. Okada S, Minamiyama Y, Hamazaki S, Toyokuni S, Sotomatsu A. Glutathione cycle dependency of ferric nitrilotriacetate-induced lipid peroxidation in mouse proximal renal tubules. Arch. Biochem. Biophys. 1993; 301: 138-142.
67. Halliwell B, Aruoma OI. DNA and Free Radicals. Ellis Norwood, West Sussex, 1993.
68. Toyokuni S, Sagripanti S, Hitchins VM. Cytotoxic and mutagenic effects of ferric nitrilotriacetate on L5178Y mouse lymphoma cells. Cancer Lett. 1995; 88: 157-162.
69. Akiyama T, Hamazaki S, Okada S. Absence of ras mutations and low incidence of p53 mutations in renal cell carcinomas induced by ferric nitrilotriacetate. Jpn. J. Cancer Res. 1995; 86: 1143-1149.
70. Kikuchi Y, Kobayashi E, Nishizawa M et al. Cloning of the rat homologue of the von Hippel-Lindau tumor suppressor gene and its non-somatic mutation in rat renal cell carcinomas. Jpn. J. Cancer Res. 1995; 86: 905-909.
71. Deguchi J, Kawabata T, Kondo A, Okada S. Transforming growth factor-α expression of renal proximal tubules in Wistar rats treated with ferric and aluminum nitrilotriacetate. Jpn. J. Cancer Res. 1993; 84: 649-655.
72. Kondo A, Deguchi J, Okada S. Renal cysts and associated renal tumours in male ddY mice injected with ferric nitrilotriacetate. Virchows Arch. 1995; 427: 91-99.
73. Bradbear RA, Bain C, Siskind V et al. Cohort study of internal malignancy in genetic hemochromatosis and other chronic nonalcoholic liver diseases. J. Natl Cancer Inst. 1985; 75: 81-84.
74. Niederau C, Fischer R, Sonnenberg A et al. Survival and causes of death in cirrhotic and non-cirrhotic patients with primary hemochromatosis. N. Engl. J. Med. 1985; 313: 1256-1262.
75. Fargion S, Mandelli C, Piperno A et al. Survival and prognostic factors in 212 Italian patients with genetic hemochromatosis. Hepatology 1992; 15: 655-659.
76. Richmond HG. Induction of sarcoma in the rat by iron-dextran complex. Br. Med. J. 1959; 1: 947-949.
77. Haddow A, Horning ES. On the carcinogenicity of an iron-dextran complex. J. Natl Cancer Inst. 1960; 24: 109-147.
78. Okada S, Hamazaki S, Toyokuni S, Midorikawa O. Induction of mesothelioma by intraperitoneal injection of ferric saccharate in male Wistar rats. Br. J. Cancer 1989; 60: 708-711.
79. Basset P, Quesneau Y, Zwiller J. Iron-induced L1210 cell growth: Evidence of a transferrin-independent iron transport. Cancer Res. 1986; 46: 1644-1647.
80. Sturrock A, Alexander J, Lamb J, Craven CM, Kaplan J. Characterization of a transferrin-independent uptake system for iron in HeLa cells. J. Biol. Chem. 1990; 265: 3139-3145.
81. Stevens RG, Jones DY, Micozzi MS, Taylor PR. Body iron stores and the risk of cancer. N. Engl. J. Med. 1988; 319: 1047-1052.
82. Stevens RG, Graubard BI, Micozzi MS, Neriishi K, Blumberg BS. Moderate elevation of body iron level and increased risk of cancer occurrence and death. Int. J. Cancer 1994; 56: 364-369.
83. van Aspeen IA, Feskens EJM, Bowles CH, Kromhout D. Body iron stores and mortality due to cancer and ischaemic heart disease: A 17-year follow-up study of elderly men and women. Int. J. Epidemiol. 1995; 24: 665-670.
84. Knekt P, Reunanen A, Takkunen H et al. Body iron stores and risk of cancer. Int. J. Cancer 1994; 56: 379-382.
85. Nelson RL, Davis FG, Sutter E et al. Body iron stores and risk of colonic neoplasia. J. Natl Cancer Inst. 1994; 86: 455-460.
86. Weinberg ED. Association of iron with colorectal cancer. Biometals 1994; 7: 211-216.
87. Icso J, Szollosova M, Sorahan T. Lung cancer among iron ore miners in east Slovakia: A case-control study. Occup. Environ. Med. 1994; 51: 642-643.
88. Mandel JS, McLaughlin JK, Schlehofer B et al. International renal-cell cancer study. 4. Occupation. Int. J. Cancer 1995; 61: 601-605.
89. Selby JV, Friedman GD. Epidemiologic evidence of an association between body iron stores and risk of cancer. Int. J. Cancer 1988; 41: 677-682.
90. Yoshiji H, Nakae D, Mizumoto Y et al. Inhibitory effect of dietary iron deficiency on inductions of putative preneoplastic lesions as well as 8-hydroxydeoxyguanosine in DNA and lipid peroxidation in the livers of rats caused by exposure to a choline-deficient L-amino acid defined diet. Carcinogenesis 1992; 13: 1227-1233.
91. United States Surgeon General. The health consequences of smoking: Cancer and chronic lung disease in the workplace (Report). Washington DC, Department of Health, Education and Welfare, Department of Health and Human Services, 1985.
92. Church DF, Pryor WA. Free-radical chemistry of cigarette smoke and its toxicological implications. Environ. Health Perspect. 1985; 64: 111-126.
93. Pryor WA. Cigarette smoke and the involvement of free radical reactions in chemical carcinogenesis. Br. J. Cancer 1987; 55 (Suppl. VIII): 19-23.
94. Qian MW, Eaton JW. Iron translocation by free fatty acids. Am. J. Pathol. 1991; 139: 1425-1434.
95. Isogai Y, Iizuka T, Shiro Y. The mechanism of electron donation to molecular oxygen by phagocytic cytochrome b(558). J. Biol. Chem. 1995; 270: 7853-7857.
96. --radical-anion generating activity. J. Biol. Chem. 1955; 270: 12685-12689.
97. Letendre ED. The importance of iron in the pathogenesis of infection and neoplasia. Trends Biochem. Sci. 1985; 166-168.
98. Barclay R. The role of iron in infection. Med. Lab. Sci. 1985; 42: 166-177.
99. Ward CG. Influence of iron on infection. Am. J. Surg. 1986; 151: 291-295.
100. Morris CJ, Earl JR, Trenam CW, Blake DR. Reactive oxygen species and iron: A dangerous partnership in inflammation. Int. J. Biochem. Cell Biol. 1995; 27: 109-122.
101. Weitzman SA, Gordon LI. Inflammation and cancer: Role of phagocyte-generated oxidants in carcinogenesis. Blood 1990; 76: 655-663.
102. Manson JE, Willett WC, Stampfer MJ et al. Body weight and mortality among women. N. Engl. J. Med. 1995; 677-685.
103. Turner-Warwick M, Lebowitz M, Burrows B, Johnson A. Cryptogenic fibrosing alveolitis and lung cancer. Thorax 1980; 35: 496-499.
104. Weitzman SA, Gordon LI. Inflammation and cancer: Role of phagocyte-generated oxidants in carcinogenesis. Blood 1990; 76: 655-663.
105. Sternberg SS, Antonioli DA, Carter D, Mills SE, Oberman HA. Diagnostic Surgical Pathology, 2nd edn. Raven Press, New York, 1994.
106. Saffiotti U, Daniel LN, Mao Y et al. Mechanisms of carcinogenesis by crystalline silica in relation to oxygen radicals. Environ. Health Perspect. 1994; 102: 159-163.
107. Ishii A, Matsuoka H, Aji T et al. Parasite infection and cancer: with special emphasis on Schistosoma japonicum infections (Trematoda): A review. Mut. Res. 1994; 305: 273-281.
108. Blaser MJ, Chyou PH, Nomura A. Age at establishment of Helicobacter pylori infection and gastric carcinoma, gastric ulcer, and duodenal ulcer risk. Cancer Res. 1995; 55: 562-565.
109. Nyren O, McLaughlin JK, Gridley G et al. Cancer risk after hip replacement with metal implants: A population-based cohort study in Sweden. J. Natl Cancer Inst. 1995; 87: 28-33.