Zinc, antioxidant systems and metallothionein in metal mediated-apoptosis: Biochemical and cytochemical aspects

Comparative Biochemistry and Physiology - C Toxicology and Pharmacology

Volumn 146, Issue 4, 2007, Pages 443-459

  Formigari, Alessia ^a   Irato, Paola ^a   Santon, Alessandro ^a  

^a UNIVERSITY OF PADOVA   (Italy)

Author keywords

Antioxidant systems; Apoptosis; Metal toxicity; Metallothionein; Zinc

Indexed keywords

ANTIOXIDANT; CATALASE; COPPER; FLUORESCENT DYE; GLUTATHIONE; GLUTATHIONE PEROXIDASE; IRON; LIPOCORTIN 5; METALLOTHIONEIN; SUPEROXIDE DISMUTASE; THIOREDOXIN; ZINC;

ANTIOXIDANT ACTIVITY; APOPTOSIS; BIOLOGICAL ACTIVITY; CELL DEATH; CELL PROTECTION; HOMEOSTASIS; HUMAN; IMMUNOLOCALIZATION; NICK END LABELING; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; REVIEW;

EID: 34848877207     PISSN: 15320456     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpc.2007.07.010     Document Type: Review

References (153)

1. Abdel-Mageed A.B., and Agrawal K.C. Activation of nuclear factor kappaB: potential role in metallothionein-mediated mitogenic response. Cancer Res. 58 (1998) 2335-2338
2. Aiuchi T., Mihara S., Nakaya M., Masuda Y., Nakajo S., and Nakaya K. Zinc ions prevent processing of caspase-3 during apoptosis induced by geranylgeraniol in HL-60 cells. J. Biochem. 124 (1998) 300-303
3. Allan S.M., and Rothwell N.J. Inflammation in central nervous system injury. Philos. Trans. R. Soc. Lond., B Biol. Sci. 358 (2003) 1669-1677
4. Allen R.T., Hunter W.J., and Agrawal D.K. Morphological and biochemical characterization and analysis of apoptosis. J. Pharmacol. Toxicol. Methods 37 (1997) 215-228
5. Andrews G.K., and Geiser J. Expression of the mouse metallothionein-I and -II genes provides a reproductive advantage during maternal dietary Zn deficiency. J. Nutr. 129 (1999) 1643-1648
6. Bagchi D., Carryl O.R., Tran M.X., Bagchi M., Vuchetich P.J., Krohn R.L., Ray S.D., Mitra S., and Stohs S.J. Protection against chemically-induced oxidative gastrointestinal tissue injury in rats by bismuth salts. Dig. Dis. Sci. 42 (1997) 1890-1900
7. Beyersmann D., and Haase H. Functions of zinc in signalling, proliferation and differentiation of mammalian cells. BioMetals 14 (2001) 331-341
8. Bornman L., Baladi S., Richard M.J., Tyrrell R.M., and Polla B.S. Differential regulation and expression of stress proteins and ferritin in human monocytes. J. Cell. Physiol. 178 (1999) 1-8
9. Bracken W.M., and Klaassen C.D. Induction of metallothionein by steroids in rat primary hepatocyte cultures. Toxicol. Appl. Pharmacol. 87 (1987) 381-388
10. Bray T.M., and Bettger W.J. The physiological role of zinc as an antioxidant. Free Radic. Biol. Med. 8 (1990) 281-291
11. Breuer W., Greenberg E., and Cabantchik Z.I. Newly delivered transferrin iron and oxidative cell injury. FEBS Lett. 403 (1997) 213-219
12. Buttke T.M., and Sandstrom P.A. Oxidative stress as a mediator of apoptosis. Immunol. Today 15 (1994) 7-10
13. Cano-Gauci D.F., and Sarkar B. Reversible Zn exchange between metallothionein and the estrogen receptor Zn finger. FEBS Lett. 386 (1996) 1-4
14. Casciola-Rosen L.A., Anhalt G.J., and Rosen A. DNA-dependent protein kinase is one of a subset of autoantigens specifically cleaved early during apoptosis. J. Exp. Med. 182 (1995) 1625-1634
15. Chai F., Truong-Tran A.Q., Ho L.H., and Zalewski P.D. Regulation of caspase activation and apoptosis by cellular zinc fluxes and zinc deprivation: a review. Immunol. Cell Biol. 77 (1999) 272-278
16. Chang A.B., Torzillo P.J., Boyce N.C., White A.V., Stewart P.M., Wheaton G.R., Purdie D.M., Wakerman J., and Valery P.C. Zinc and vitamin A supplementation in Indigenous Australian children hospitalised with lower respiratory tract infection: a randomised controlled trial. Med. J. Aust. 184 (2006) 107-112
17. Chen Y., and Maret W. Catalytic selenols couple the redox cycles of metallothionein and glutathione. Eur. J. Biochem. 268 (2001) 3346-3353
18. Cherian M.G., and Apostolova M.D. Nuclear localization of metallothionein during cell proliferation and differentiation. Cell. Mol. Biol. 46 (2000) 347-356
19. Cherian M.G., Jayasurya A., and Bay B.H. Metallothioneins in human tumors and potential roles in carcinogenesis. Mutat. Res. 533 (2003) 201-209
20. Chung R.S., and West A.K. A role for extracellular metallothioneins in CNS injury and repair. Neuroscience 123 (2004) 595-599
21. Collins J.A., Schandi C.A., Young K.K., Vesely J., and Willingham M.C. Major DNA fragmentation is a late event in apoptosis. J. Histochem. Cytochem. 45 (1997) 923-934
22. Conrad C.C., Walter C.A., Richardson A., Hanes M.A., and Grabowski D.T. Cadmium toxicity and distribution in metallothionein-I and -II deficient transgenic mice. J. Toxicol. Environ. Health 52 (1997) 527-543
23. Cozzi A., Levi S., Corsi B., Santambrogio P., Campanella A., Gerardi G., and Arosio P. Role of iron and ferritin in TNF alpha-induced apoptosis in HeLa cells. FEBS Lett. 537 (2003) 87-192
24. Culotta V.C., Lin S.J., Schmidt P., Klomp L.W., Casareno R.L., and Gitlin J. Intracellular pathways of copper trafficking in yeast and humans. Adv. Exp. Med. Biol. 448 (1999) 247-254
25. Dalton T., Fu K., Enders G.C., Palmiter R.D., and Andrews G.K. Analysis of the effects of overexpression of metallothionein-I in transgenic mice on the reproductive toxicology of cadmium. Environ. Health Perspect. 104 (1996) 68-76
26. Davis S.R., and Cousins R.J. Metallothionein expression in animals: a physiological perspective on function. J. Nutr. 130 (2000) 1085-1088
27. de Bie P., van de Sluis B., Klomp L., and Wijmenga C. The many faces of the copper metabolism protein MURR1/COMMD1. J. Heredity 96 (2005) 803-811
28. Dock, L., Vahter, M., 1999. Metal toxicology. ed 2th vol 3 In Ballantyne B, Marrs T, Syversen T (eds) General and Applied Toxicology,. London, Macmillan Reference Ltd, pp 2049-2078.
29. Donfrancesco A., Deb G., De Sio L., Cozza R., and Castellano A. Role of deferoxamine in tumor therapy. Acta Haematol. 95 (1996) 66-69
30. Fabisiak J.P., Tyurin V.A., Tyurina Y.Y., Borisenko G.G., Korotaeva A., Pitt B.R., Lazo J.S., and Kagan V.E. Redox regulation of copper-metallothionein. Arch. Biochem. Biophys. 363 (1999) 171-181
31. Feng W., Cai J., Pierce W.M., Franklin R.B., Maret W., Benz F.W., and Kang Y.J. Metallothionein transfers Zn to mitochondrial aconitase through a direct interaction in mouse hearts. Biochem. Biophys. Res. Commun. 332 (2005) 853-858
32. Fleming R.E., and Sly W.S. Ferroportin mutation in autosomal dominant hemochromatosis: loss of function, gain in understanding. J. Clin. Invest. 108 (2001) 521-522
33. Formigari A., Santon A., and Irato P. Efficacy of zinc treatment against iron-induced toxicity in rat hepatoma cell line H4-II-E-C3. Liver Int. 27 (2007) 120-127
34. Frankfurt O.S., and Krishan A. Identification of apoptotic cells by formamide-induced DNA denaturation in condensed chromatin. J. Histochem. Cytochem. 49 (2001) 369-378
35. Frazer D.M., and Anderson G.J. The orchestration of body iron intake: how and where do enterocytes receive their cues?. Blood Cells, Mol. Dis. 30 (2003) 288-297
36. Futakawa N., Kimura W., Wada Y., and Muto T. Clinicopathological characteristics and surgical procedures for carcinoma of the papilla of Vater. Hepatogastroenterology 43 (1996) 260-267
37. Gaither L.A., and Eide D.J. The human ZIP1 transporter mediates zinc uptake in human K562 erythroleukemia cells. J. Biol. Chem. 276 (2001) 22258-22264
38. Ghoshal K., and Jacob S.T. Regulation of metallothionein gene expression. Prog. Nucleic Acid Res. Mol. Biol. 66 (2001) 357-384
39. Ghoshal K., Majumder S., Li Z., Bray T.M., and Jacob S.T. Transcriptional induction of metallothionein-I and -II genes in the livers of Cu,Zn-superoxide dismutase knockout mice. Biochem. Biophys. Res. Commun. 264 (1999) 735-742
40. Giles G.I. The redox regulation of thiol dependent signaling pathways in cancer. Curr. Pharm. Des. 12 (2006) 4427-4443
41. Hahn M.A., and Mayne G.C. Phorbol ester-induced cell death in PC-12 cells overexpressing Bcl-2 is dependent on the time at which cells are treated. Cell Biol. Int. 28 (2004) 345-359
42. Halliwell B., and Gutteridge J.M. Reoxygenation injury and antioxidant protection: a tale of two paradoxes. Arch. Biochem. Biophys. 283 (1990) 223-226
43. Hamza I., Schaefer M., Klomp L.W., and Gitlin J.D. Interaction of the copper chaperone HAH1 with the Wilson disease protein is essential for copper homeostasis. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 13363-13368
44. Hansen J.M., Zhang H., and Jones D.P. Differential oxidation of thioredoxin-1, thioredoxin-2, and glutathione by metal ions. Free Radic. Biol. Med. 40 (2006) 138-145
45. Haq F., Mahoney M., and Koropatnick A. Signaling events for metallothionein induction. Mutat. Res. 533 (2003) 211-226
46. Harris E.D. Copper transport: an overview. Proc. Soc. Exp. Biol. Med. 196 (1991) 130-140
47. Hentze M.W., and Kuhn L.C. Molecular control of vertebrate iron metabolism: mRNA-based regulatory circuits operated by iron, nitric oxide, and oxidative stress. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 8175-81782
48. Hidalgo J., Aschner M., Zatta P., and Vasak M. Roles of the metallothionein family of proteins in the central nervous system. Brain Res. Bull. 55 (2001) 133-145
49. Jacob A.K., Hotchkiss R.S., DeMeester S.L., Hiramatsu M., Kar I.E., Swanson P.E., Cobb J.P., and Buchman T.G. Endothelial cell apoptosis is accelerated by inorganic iron and heat via an oxygen radical dependent mechanism. Surgery 122 (1997) 243-253
50. Jacob S.T., Ghoshal K., and Sheridan J.F. Induction of metallothionein by stress and its molecular mechanisms. Gene Expr. 7 (1999) 301-310
51. Jiang L.J., Maret W., and Vallee B.L. The glutathione redox couple modulates zinc transfer from metallothionein to zinc-depleted sorbitol dehydrogenase. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 3483-3488
52. Jiang J., St Croix C.M., Sussman N., Zhao Q., Pitt B.R., and Kagan V.E. Contribution of glutathione and metallothioneins to protection against copper toxicity and redox cycling: quantitative analysis using MT+/+ and MT-/- mouse lung fibroblast cells. Chem. Res. Toxicol. 15 (2002) 1080-1087
53. Jimenez I., and Speisky H. Effects of copper ions on the free radical-scavenging properties of reduced glutathione: implications of a complex formation. J. Trace Elem. Med. Biol. 14 (2000) 161-167
54. Johnson T.M., Yu Z.X., Ferrans V.J., Lowenstein R.A., and Finkel T. Reactive oxygen species are downstream mediators of p53-dependent apoptosis. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 11848-11852
55. Kang Y.J. Metallothionein redox cycle and function. Exp. Biol. Med. 231 (2006) 1459-1467
56. Kerr J.F., Wyllie A.H., and Currie A.R. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26 (1972) 239-257
57. Kim H.Y., and Gladyshev V.N. Role of structural and functional elements of mouse methionine-S-sulfoxide reductase in its subcellular distribution. Biochemistry 44 (2005) 8059-8067
58. Kimura T., Oguro I., Kohroki J., Takehara M., Itoh N., Nakanishi T., and Tanaka K. Metallothionein-null mice express altered genes during development. Biochem. Biophys. Res. Commun. 270 (2000) 458-461
59. Klassen A.C., Klassen D.K., Aronoff R., Hal A.G., and Braslow J. Organizational characteristics of solid-organ donor hospitals and nondonor hospitals. J. Transpl. Coord. 9 (1999) 87-94
60. Klassen R.B., Crenshaw K., Kozyraki R., Verroust P.J., Tio L., Atrian S., Allen P.L., and Hammond T.G. Megalin mediates renal uptake of heavy metal metallothionein complexes. Am. J. Physiol. Renal. Physiol. 287 (2004) F393-F403
61. Klomp L.W., Lin S.J., Yuan D.S., Klausner R.D., Culotta V.C., and Gitlin J.D. Identification and functional expression of HAH1, a novel human gene involved in copper homeostasis. J. Biol. Chem. 272 (1997) 9221-9226
62. Koc M., Nad'ova Z., and Kovar J. Sensitivity of cells to apoptosis induced by iron deprivation can be reversibly changed by iron availability. Cell Prolif. 39 (2006) 551-561
63. Koizumi T., and Li Z.G. Role of oxidative stress in single-dose, cadmium-induced testicular cancer. J. Toxicol. Environ. Health 37 (1992) 25-36
64. Kondo Y., Rusnak J.M., Hoyt D.G., Settineri C.E., Pitt B.R., and Lazo J.S. Enhanced apoptosis in metallothionein null cells. Mol. Pharmacol. 52 (1997) 195-201
65. Koopman G., Reutelingsperger C., Kuijten G.A., Keehnen R.M., Pals S.T., and Van Oers M.H. Annexin V for flow cytometric of phophatidylserine expression on B cells undergoing apoptosis. Blood 84 (1994) 1415-1420
66. Kordas K., and Stoltzfus R.J. New evidence of iron and zinc interplay at the enterocyte and neural tissues. J. Nutr. 134 (2004) 1295-1298
67. Kourie J.I. Interaction of reactive oxygen species with ion transport mechanisms. Am. J. Physiol. 275 (1998) C1-C24
68. Kovar J., Valenta T., and Stybrova H. Differing sensitivity of tumor cells to apoptosis induced by iron deprivation in vitro. In Vitro Cell. Dev. Biol., Anim. 37 (2001) 450-458
69. Kroncke K.D., Fehsel K., Schmidt T., Zenke F.T., Dasting I., Wesener J.R., Bettermann H., Breunig K.D., and Kolb-Bachofen V. Nitric oxide destroys zinc-sulfur clusters inducing zinc release from metallothionein and inhibition of the Zn finger-type yeast transcription activator LAC9. Biochem. Biophys. Res. Commun. 200 (1994) 1105-1110
70. Kuo Y.M., Zhou B., Cosco D., and Gitschier J. The copper transporter CTR1 provides an essential function in mammalian embryonic development. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 6836-6841
71. Lazo J.S., and Pitt B.R. Metallothioneins and cell death by anticancer drugs. Annu. Rev. Pharmacol. Toxicol. 35 (1995) 635-653
72. Lazo J.S., Kondo Y., Dellapiazza D., Michalska A.E., Choo K.H., and Pitt B.R. Enhanced sensitivity to oxidative stress in cultured embryonic cells from transgenic mice deficient in metallothionein I and II genes. J. Biol. Chem. 270 (1995) 5506-5510
73. Le N.T., and Richardson D.R. The role of iron in cell cycle progression and the proliferation of neoplastic cells. Biochim. Biophys. Acta 1603 (2002) 31-46
74. Lee J., Prohaska J.R., Dagenais S.L., Glover T.W., and Thiele D.J. Isolation of a murine copper transporter gene, tissue specific expression and functional complementation of a yeast copper transport mutant. Gene 254 (2000) 87-96
75. Lee J., Prohaska J.R., and Thiele D.J. Essential role for mammalian copper transporter Ctr1 in copper homeostasis and embryonic development. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 6842-6847
76. Levadoux-Martin M., Hesketh J.E., Beattie J.H., and Wallace H.M. Influence of metallothionein-1 localization on its function. Biochem. J. 355 (2001) 473-479
77. Lill R., Diekert K., Kaut A., Lange H., Pelzer W., Prohl C., and Kispal G. The essential role of mitochondria in the biogenesis of cellular iron-sulfur proteins. Biol. Chem. 380 (1999) 1157-1166
78. Liu Y., Liu J., Iszard M.B., Andrews G.K., Palmiter R.D., and Klaassen C.D. Transgenic mice that overexpress metallothionein-I are protected from cadmium lethality and hepatotoxicity. Toxicol. Appl. Pharmacol. 135 (1995) 222-228
79. Liu J., Liu Y., Habeebu S.S., and Klaassen C.D. Susceptibility of MT-null mice to chronic CdCl2-induced nephrotoxicity indicates that renal injury is not mediated by the CdMT complex. Toxicol. Sci. 46 (1998) 197-203
80. Malorni W., Rivabene R., Santini M.T., Paradisi S., Iosi F., and Donelli G. Down-modulation of CD4 antigen during programmed cell death in U937 cells. FEBS Lett. 336 (1993) 335-339
81. Maret W. Oxidative metal release from metallothionein via zinc-thiol/disulfide interchange. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 237-241
82. Maret W. Metallothionein/disulfide interactions, oxidative stress, and the mobilization of cellular zinc. Neurochem. Int. 27 (1995) 111-117
83. Maret W., and Vallee B.L. Thiolate ligands in metallothionein confer redox activity on zinc clusters. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 3478-3482
84. Masella R., Di Benedetto R., Vari R., Filesi C., and Giovannini C. Novel mechanisms of natural antioxidant compounds in biological systems: involvement of glutathione and glutathione-related enzymes. J. Nutr. Biochem. 16 (2005) 577-586
85. Mason A.Z., Perico N., Moeller R., Thrippleton K., Potter T., and Lloyd D. Metal donation and apo-metalloenzyme activation by stable isotopically labeled metallothionein. Mar. Environ. Res. 58 (2004) 371-375
86. Masters B.A., Kelly E.J., Quaife C.J., Brinster R.L., and Palmiter R.D. Targeted disruption of metallothionein I and II genes increases sensitivity to cadmium. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 584-588
87. Mates J.M., Perez-Gomez C., and Nunez de Castro I. Antioxidant enzymes and human diseases. Clin. Biochem. 32 (1999) 595-603
88. Matsushita K., Kitagawa K., Matsuyama T., Ohtsuki T., Taguchi A., Mandai K., Mabuchi T., Yagita Y., Yanagihara T., and Matsumoto M. Effect of systemic zinc administration on delayed neuronal death in the gerbil hippocampus. Brain Res. 743 (1996) 362-365
89. 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., and 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
90. Medici V., Santon A., Sturniolo G.C., D'Inca R., Giannetto S., Albergoni V., and Irato P. Metallothionein and antioxidant enzymes in Long-Evans Cinnamon rats treated with zinc. Arch. Toxicol. 76 (2002) 509-516
91. Meplan C., Richard M.J., and Hainaut P. Metalloregulation of the tumor suppressor protein p53: zinc mediates the renaturation of p53 after exposure to metal chelators in vitro and in intact cells. Oncogene 19 (2000) 5227-5236
92. Miles A.T., Hawksworth G.M., Beattie J.H., and Rodilla V. Induction, regulation, degradation, and biological significance of mammalian metallothioneins. Crit. Rev. Biochem. Mol. Biol. 35 (2000) 35-70
93. Mori M., Hattori A., Sawaki M., Tsuzuki N., Sawada N., Oyamada M., Sugawara N., and Enomoto K. The LEC rat: a model for human hepatitis, liver cancer, and much more. Am. J. Pathol. 144 (1994) 200-204
94. Nodera M., Yanagisawa H., and Wada O. Increased apoptosis in a variety of tissues of zinc-deficient rats. Life Sci. 69 (2001) 1639-1649
95. Oancea M., Mazumder S., Crosby M.E., and Almasan A. Apoptosis assays. Methods Mol. Med. 129 (2006) 279-290
96. Okayasu T., Tochimaru H., Hyuga T., Takahashi T., Takekoshi Y., Li Y., Togashi Y., Takeichi N., Kasai N., and Arashima S. Inherited copper toxicity in Long-Evans cinnamon rats exhibiting spontaneous hepatitis: a model of Wilson's disease. Pediatr. Res. 31 (1992) 253-257
97. Park J.D., Liu Y., and Klaassen C.D. Protective effect of metallothionein against the toxicity of cadmium and other metals. Toxicology 163 (2001) 93-100
98. Parkin G. Chemistry. Zinc-zinc bonds: a new frontier. Science 305 (2004) 1117-1118
99. Penaloza C., Lin L., Lockshin R.A., and Zakeri Z. Cell death in development: shaping the embryo. Histochem. Cell Biol. 126 (2006) 149-158
100. Penkowa M., Flori S., Giralt M., Quintana A., Molinero A., Carrasco J., and Hidalgo J. Metallothionein reduces central nervous system inflammation, neurodegeneration, and cell death following kainic acid-induced epileptic seizures. J. Neurosci. Res. 79 (2005) 522-534
101. Perry D.K., Smyth M.J., and Stennicke H.R. Zinc is a potent inhibitor of the apoptotic protease, caspase-3. J. Biol. Chem. 272 (1997) 18530-18533
102. Petris M.J., and Mercer J.F. The Menkes protein (ATP7A; MNK) cycles via the plasma membrane both in basal and elevated extracellular copper using a C-terminal di-leucine endocytic signal. Hum. Mol. Genet. 8 (1999) 2107-2115
103. Powell S.R. The antioxidant properties of zinc. J. Nutr. 130 (2000) 1447S-1454S
104. Puig S., and Thiele D.J. Molecular mechanisms of copper uptake and distribution. Curr. Opin. Chem. Biol. 6 (2002) 171-180
105. 2 with sulfhydryl groups in HL-60 cells: zinc-metallothionein and other sites. Arch. Biochem. Biophys. 334 (1996) 241-250
106. Raff M. Cell suicide for beginners. Nature 396 (1998) 119-122
107. Rainwater R., Parks D., Anderson M.E., Tegtmeyer P., and Mann K. Role of cysteine residues in regulation of p53 function. Mol. Cell. Biol. 15 (1995) 3892-3903
108. Romero-Isart N., and Vasak M. Advances in the structure and chemistry of metallothioneins. J. Inorg. Biochem. 88 (2002) 388-396
109. Rouault T., and Klausner R.D. Regulation of iron metabolism in eukaryotes. Curr. Top. Cell. Regul. 35 (1997) 1-19
110. Sagher D., Brunell D., Brot N., Vallee B.L., and Weissbac H. Selenocompounds can serve as oxidoreductants with the methionine sulfoxide reductase enzymes. J. Biol. Chem. 281 (2006) 31184-31187
111. Saitoh M., Nishitoh H., Fujii M., Takeda K., Tobiume K., Sawada Y., Kawabata M., Miyazono K., and Ichijo H. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J. 17 (1998) 2596-2606
112. Santon A., Irato P., Medici V., D'Inca R., Albergoni V., and Sturniolo G.C. Effect and possible role of Zn treatment in LEC rats, an animal model of Wilson's disease. Biochim. Biophys. Acta 1637 (2003) 91-97
113. Santon A., Albergoni V., Sturniolo G.C., and Irato P. Evaluation of MT expression and detection of apoptotic cells in LEC rat kidneys. Biochim. Biophys. Acta 1688 (2004) 223-231
114. Santon A., Formigari A., Albergoni V., and Irato P. Effect of Zn treatment on wild type and MT-null cell lines in relation to apoptotic and/or necrotic processes and on MT isoform gene expression. Biochim. Biophys. Acta 1763 (2006) 305-312
115. Sato M. Dose-dependent increases in metallothionein synthesis in the lung and liver of paraquat-treated rats. Toxicol. Appl. Pharmacol. 107 (1991) 98-105
116. Sato M., and Bremner I. Oxygen free radicals and metallothionein. Free Radic. Biol. Med. 14 (1993) 325-337
117. Schaeffer C., Thomassin L., Rochette L., and Connat J.L. Apoptosis induced in vascular smooth muscle cells by oxidative stress is partly prevented by pretreatment with CGRP. Ann. N. Y. Acad. Sci. 1010 (2003) 733-737
118. Schwarz M.A., Lazo J.S., Yalowich J.C., Reynolds I., Kagan V.E., Tyurin V., Kim Y.M., Watkins S.C., and Pitt B.R. Cytoplasmic metallothionein overexpression protects NIH 3T3 cells from tert-butyl hydroperoxide toxicity. J. Biol. Chem. 269 (1994) 15238-15243
119. Schwarz M.A., Lazo J.S., Yalowich J.C., Allen W.P., Whitmore M., Bergonia H.A., Tzeng E., Billiar T.R., Robbins P.D., and Lancaster Jr. J.R. Metallothionein protects against the cytotoxic and DNA-damaging effects of nitric oxide. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 4452-4456
120. Shimoda R., Achanzar W.E., Qu W., Nagamine T., Takagi H., Mori M., and Waalkes M.P. Metallothionein is a potential negative regulator of apoptosis. Toxicol. Sci. 73 (2003) 294-300
121. Siah C.W., Ombiga J., Adams L.A., Trinder D., and Olynyk J.K. Normal iron metabolism and the pathophysiology of iron overload disorders. Clin. Biochem. Rev. 27 (2006) 5-16
122. Sies H. Chapter 1: oxidative stress: introductory remarks. In: Sies H. (Ed). Oxidative Stress (1985), Academic Press, London
123. Sies H. Strategies of antioxidant defense. Eur. J. Biochem. 215 (1993) 213-219
124. Simonart T., Degraef C., Andrei G., Mosselmans R., Hermans P., Van Vooren J.P., Noel J.C., Boelaert J.R., Snoeck R., and Heenen M. Iron chelators inhibit the growth and induce the apoptosis of Kaposi's sarcoma cells and of their putative endothelial precursors. J. Invest. Dermatol. 115 (2000) 893-900
125. Simonart T., Boelaert J.R., and Van Vooren J.P. Enhancement of classic Kaposi's sarcoma growth after intralesional injections of desferrioxamine. Dermatology 204 (2002) 290-292
126. Singhal R.K., Anderson M.E., and Meister A. Glutathione, a first line of defense against cadmium toxicity. FASEB J. 1 (1987) 220-223
127. Somani S.M., Husain K., and Schlorff E.C. Response of antioxidant system to physical and chemical stress. In: Baskin S.I., and Salem H. (Eds). Oxidants, Antioxidants and Free Radicals (1997), Taylor & Francis, Bristol 125-141
128. Sreedhar B., Subramaniyan R., and Nair K.M. A protective role for zinc on intestinal peroxidative damage during oral iron repletion. Biochem. Biophys. Res. Commun. 318 (2004) 992-997
129. Steinebach O.M., and Wolterbeek B.T. Metallothionein biodegradation in rat hepatoma cells: a compartmental analysis aided 35S-radiotracer study. Biochim. Biophys. Acta 1116 (1992) 155-165
130. Sturniolo G.C., Mestriner C., Irato P., Albergoni V., Longo G., and D'Inca R. Zinc therapy increases duodenal concentrations of metallothionein and iron in Wilson's disease patients. Am. J. Gastroenterol. 94 (1999) 334-338
131. Suzuki K.T., Kanno S., Misawa S., and Sumi Y. Changes in copper distribution in the plasma and kidneys of LEC rats following acute hepatitis. Res. Commun. Chem. Pathol. Pharmacol. 82 (1993) 225-232
132. Suzuki K.T., Nakamura M., Hatanaka Y., Kayanoki Y., Tatsumi H., and Taniguchi N. Induction of apoptotic cell death in human endothelial cells treated with snake venom: implication of intracellular reactive oxygen species and protective effects of glutathione and superoxide dismutases. J. Biochem. 122 (1997) 1260-1264
133. Takahashi Y., Kako K., Kashiwabara S., Takehara A., Inada Y., Arai H., Nakada K., Kodama H., Hayashi J., Baba T., and Munekata E. Mammalian copper chaperone Cox17p has an essential role in activation of cytochrome C oxidase and embryonic development. Mol. Cell. Biol. 22 (2002) 7614-7621
134. Takahashi Y., Ogra Y., and Suzuki K.T. Nuclear trafficking of metallothionein requires oxidation of a cytosolic partner. J. Cell. Physiol. 202 (2005) 563-569
135. Templeton D.M., and Cherian M.G. Toxicological significance of metallothionein. Methods Enzymol. 205 (1991) 11-24
136. Thomas D.J., and Caffrey T.C. Lipopolysaccharide induces double-stranded DNA fragmentation in mouse thymus: protective effect of zinc pretreatment. Toxicology 68 (1991) 327-337
137. Truong-Tran A.Q., Carter J., Ruffin R.E., and Zalewski P.D. The role of zinc in caspase activation and apoptotic cell death. BioMetals 14 (2001) 315-330
138. Turrens J.F. Mitochondrial formation of reactive oxygen species. J. Physiol. 552 (2003) 335-344
139. Valko M., Rhodes C.J., Moncol J., Izakovic M., and Mazur M. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem. Biol. Interact. 160 (2006) 1-40
140. Vasak M., and Hasler D.W. Metallothioneins: new functional and structural insights. Curr. Opin. Chem. Biol. 4 (2000) 177-183
141. Vasconcelos M.H., Tam S.C., Beattie J.H., and Hesketh J.E. Uptake and effects of antisense oligodeoxynucleotides specific for rat metallothionein-1 and -2 mRNA in H4 rat hepatoma cells in culture. Biochem. Soc. Trans. 24 (1996) 408S
142. Vasconcelos M.H., Tam S.C., Hesketh J.E., Reid M., and Beattie J.H. Metal- and tissue-dependent relationship between metallothionein mRNA and protein. Toxicol. Appl. Pharmacol. 182 (2002) 91-97
143. Viarengo A., Burlando B., Ceratto N., and Panfili I. Antioxidant role of metallothioneins: a comparative overview. Cell. Mol. Biol. 46 (2000) 407-417
144. Weissgarten J., Berman S., Modai D., Rosenberg R., Rapoport M., Cohen M., and Averbukh Z. Zn metabolism affects apoptosis rate and proliferative responsiveness of PBMC from patients on chronic hemodialysis. Metabolism 51 (2002) 1392-1396
145. Willson J.K. Biology of large bowel cancer. Hematol./Oncol. Clin. North Am. 3 (1989) 19-34
146. Wiseman D.A., Wells S.M., Hubbard M., Welker J.E., and Black S.M. Alterations in zinc homeostasis underlie endothelial cell death induced by oxidative stress from acute exposure to hydrogen peroxide. Am. J. Physiol., Lung Cell. Mol. Physiol. 292 (2007) L165-L177
147. Yanagisawa H., Sato M., Nodera M., and Wada O. Excessive zinc intake elevates systemic blood pressure levels in normotensive rats-potential role of superoxide-induced oxidative stress. J. Hypertens. 22 (2004) 543-550
148. Yao D., Shi W., Gou Y., Zhou X., Yee A.T., Zhou Y., and Liu Z. Fatty acid-mediated intracellular iron translocation: a synergistic mechanism of oxidative injury. Free Radic. Biol. Med. 39 (2005) 1385-1398
149. Yin X., Wu H., Chen Y., and Kang Y.J. Induction of antioxidants by adriamycin in mouse heart. Biochem. Pharmacol. 56 (1998) 87-93
150. Yoshida M., Saegusa Y., Fukuda A., Akama Y., and Owada S. Measurement of radical-scavenging ability in hepatic metallothionein of rat using in vivo electron spin resonance spectroscopy. Toxicology 213 (2005) 74-80
151. Zalewski P.D., Forbes I.J., and Giannakis C. Physiological role for zinc in prevention of apoptosis (gene-directed death). Biochem. Int. 24 (1991) 1093-1101
152. Zeng J., Vallee B.L., and Kagi J.H. Zn transfer from transcription factor IIIA fingers to thionein clusters. Proc. Natl. Acad. Sci. U. S. A. 88 (1991) 9984-9988
153. Zhou Z., Sun X., Lambert J.C., Saari J.T., and Kang Y.J. Metallothionein-independent Zn protection from alcoholic liver injury. Am. J. Pathol. 160 (2002) 2267-2274