Zinc protects human peripheral blood lymphocytes from Cr(III)(phenanthroline)3-induced apoptosis

Toxicology and Applied Pharmacology

Volumn 243, Issue 3, 2010, Pages 405-419

  Sankaramanivel, Sundararaj ^a   Rajaram, Anantanarayanan ^a   Rajaram, Rama ^a  

^a CENTRAL LEATHER RESEARCH INSTITUTE   (India)

Author keywords

Apoptosis; Caspase 3; Chromium; Lymphocyte ultrastructure; Metallothionein isoforms; Mitochondrial membrane potential; Reactive oxygen species; Zinc

Indexed keywords

ACRIDINE ORANGE; ADENOSINE TRIPHOSPHATE; CASPASE 3; CATALASE; CHROMIUM DERIVATIVE; ETHIDIUM BROMIDE; LIPOCORTIN 5; METALLOTHIONEIN; METALLOTHIONEIN I; METALLOTHIONEIN IA; METALLOTHIONEIN IB; METALLOTHIONEIN II; METALLOTHIONEIN III; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; TRIS(1,10 PHENANTHROLINE) CHROMIUM; UNCLASSIFIED DRUG; ZINC;

APOPTOSIS; ARTICLE; CELL LEVEL; CELL PROTECTION; CELL STRESS; CELL ULTRASTRUCTURE; CHROMATIN; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DNA FRAGMENTATION; DNA SYNTHESIS INHIBITION; ENZYME ACTIVATION; FILOPODIUM; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; PERIPHERAL LYMPHOCYTE; PROTEIN SYNTHESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCANNING ELECTRON MICROSCOPY; SIGNAL TRANSDUCTION; STAINING; TRANSMISSION ELECTRON MICROSCOPY;

ADENOSINE TRIPHOSPHATE; APOPTOSIS; CASPASE 3; CATALASE; CELL SEPARATION; CELL SURVIVAL; CHROMIUM; CYSTEINE; DNA; DNA FRAGMENTATION; ELECTROPHORESIS, AGAR GEL; HUMANS; LIGANDS; LYMPHOCYTES; METALLOTHIONEIN; MICROSCOPY, ELECTRON, TRANSMISSION; MITOCHONDRIAL MEMBRANES; ORGANOMETALLIC COMPOUNDS; PROTECTIVE AGENTS; REACTIVE OXYGEN SPECIES; SILVER STAINING; SUPEROXIDE DISMUTASE; THYMIDINE; ZINC COMPOUNDS;

EID: 77049126137     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2009.12.018     Document Type: Article

References (76)

1. Aebi H., Suter H., and Feinstein R.N. Activity and stability of catalase in blood and tissues of normal and acatalasemic mice. Biochem. Genet. 2 (1968) 245-251
2. Balamurugan K., Rajaram R., Ramasami T., and Narayanan S. Chromium (III)-induced apoptosis of lymphocytes: death decision by ROS and Src-family tyrosine kinases. Free Radic. Biol. Med. 33 (2002) 1622-1640
3. Balamurugam K., Rajaram R., and Ramasami T. Caspase-3: its potential involvement in Cr(III)-induced apoptosis of lymphocytes. Mol.Cell. Biochem. 259 (2004) 43-51
4. Barnhart J. Occurrences, uses and properties of chromium. Regul. Toxicol. Pharmacol. 26 (1997) S3-S7
5. Baskic D., Popovic S., Ristic P., and Arsenijevic N.N. Analysis of cyclo-heximide induced apoptosis in human leukocytes: fluorescence microscopy using annexin V/propidium iodide versus acridine orange/ethidium bromide. Cell Biol. Int. 30 (2006) 924-932
6. Boyum A. Isolation of leucocytes from blood and bone marrow. J.Clin. Lab. Invest. 21 (1968) 77-79
7. Bradford M.M. A rapid and sensitive method for the quantiation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
8. Cai L., and Cherian M.G. Zinc-metallothionein protects from DNA damage induced by radiation better than glutathione and copper- or cadmium-metallothioneins. Toxic. Lett. 136 (2003) 193-198
9. Cai L., Satoh M., Tohyama C., and Cherian M.G. Metallothionein in radiation exposure: its induction and protective role. Toxicology 132 (1999) 85-98
10. Cavigelli M., Kagi J.H.R., and Hunziker P.E. Cell and inducer specific accretion of human isometallothioneins. Biochem. J. 292 (1993) 551-554
11. Chang K.L., Hung T.C., Hsieh B.S., Chen Y.H., Chen T.F., and Cheng H.L. Zinc at pharmacologic concentrations affects cytokine expression and induces apoptosis of human peripheral blood mononuclear cells. Nutrition 22 (2006) 465-474
12. Coyle P., Philcox J.C., Carey L.C., and Rofe A.M. Metallothionein: the multipurpose protein. Cell. Mol. Life Sci. 59 (2002) 627-647
13. Davis S.R., and Cousins R.J. Metallothionein expression in animals: a physiological perspective on function. J. Nutr. 130 (2000) 1085-1088
14. Ewing J.F., and Janero D.R. Microplate superoxide dismutase assay employing a nonenzymatic superoxide generator. Anal. Biochem. 232 (1995) 243-248
15. Feng W., Benz F.W., Cai J., Pierce W.M., and Kang Y.J. Metallothionein disulfides are present in metallothionein-overexpressing transgenic mouse heart and increase under conditions of oxidative stress. J. Biol. Chem. 281 (2006) 681-687
16. Fleet J.C., Golemboski K.A., Dietert R.R., Andrews G.K., and McCormick C.C. Induction of hepatic metallothionein by intraperitoneal metal injection: an associated inflammatory response. Am. J. Phsyiol. 258 (1990) G926-933
17. Friedman R.L., Manly S.P., McMahon M., Kerr I.M., and Stark G.R. Transcriptional and posttranscriptional regulation of interferon-induced gene expression in human cells. Cell 38 (1984) 745-755
18. Garrett S.H., Sens M.A., Shukla D., Nestor S., Somji S., Todd J.H., and Sens D.A. Metallothionein isoform-3 expression in the human prostate and cancer-derived cell lines. The Prostate 41 (1999) 196-202
19. Garrett S.H., Sens M.R., Todd J.H., Somji S., and Sens D.A. Expression of MT-3 protein in the human kidney. Toxicol. Lett. 105 (1999) 207-214
20. Hamer D.H. Metallothionein. Ann. Rev. Biochem. 55 (1986) 913-951
21. Herrmann M., Lorenz H.M., Voll R., Grunke M., Woith W., and Kalden J.R. A rapid and simple method for the isolation of apoptotic DNA fragments. Nucleic Acids Res. 22 (1994) 5506-5507
22. Heuchel R., Radtke F., Georgiev O., Stark G., Aguet M., and Schaffner W. The transcription factor MTF-1 is essential for basal and heavy metal-induced metallothionein gene expression. EMBO J. 13 (1994) 2870-2875
23. Hoey J.G., Garrett S.H., Sens M.A., Todd J.H., and Sens D.A. Expression of MT-3 mRNA in human kidney, proximal tubule cell cultures, and renal cell carcinoma. Toxicol. Lett. 92 (1997) 149-160
24. Hunziker P.E., and Kagi J.H. Isolation and characterization of six human hepatic iso-metallothioneins. Biochem. J. 231 (1985) 375-382
25. IARC. World Health Organization IARC monographs on the evaluation of the carcinogenic risk of chemicals to humans: chromium, nickel and welding. International Agency for Research on Cancer 49 (1990), Lyon, France 49-256
26. Jana M., Rajaram A., and Rajaram R. Chromium picolinate induced apoptosis of human lymphocytes and signaling mechanisms thereof. Toxic. Appl. Pharm. 237 (2009) 331-344
27. Kagi J.H.R., and Valee B.L. Metallothionein: a cadmium and zinc containing protein from equine renal cortex II: Physiochemical properties. J. Biol. Chem. 236 (1961) 2435-2442
28. Kang Y.J. Antioxidant defense against anthracycline cardiotoxicity by metallothionein. Cardiovas. Toxicol. 7 (2007) 95-100
29. Kang Y.J., Chen Y., Yu A., Voss-McCowman M., and Epstein P.N. Over expression of metallothionein in the heart of transgenic mice suppresses doxorubicin cardiotoxicity. J. Clin. Invest. 100 (1997) 1501-1506
30. Kimura T., Fujita I., Itoh N., Muto N., Nakanishi T., Takahashi K., Azuma J., and Tanaka K. Metallothionain acts a cytoprotectant against doxorubicin toxicity. J. Pharm. Exp. Ther. 292 (2000) 292-302
31. Kondoh M., Inoue Y., Atagi S., Futakawa N., Higashimoto M., and Sato M. Specific induction of metallothionein synthesis by mitochondrial oxidative stress. Life Sci. 69 (2001) 2137-2146
32. Krezel A., and Maret W. Different redox states of metallothionein/thionein in biological tissue. Biochem. J. 402 (2007) 551-558
33. Lambert J.C., Zhou Z., Wang L., Song Z., McClain C.J., and Kang Y.J. Preservation of structural integrity by zinc is independent of metallothionein in alcohol intoxicated mice. Am. J. Pathol. 164 (2004) 1959-1966
34. Maguire K.N.A.P., and Hallock J.S. Preparation and resolution of tris(2,2′-bipyridine) and tris(1,10-phenanthroline) complexes of Cr(III). Inorg. Chim. Acta 35 (1979) L309-L311
35. Majumder S., Ghoshal K., Summers D., Bai S., Datta J., and Jacob T. Chromium(VI) down-regulated heavy metal-induced metallothionein gene transcription by modifying transactivation potential of the key transcription factor, metal-responsive transcription factor 1. J. Biol. Chem. 278 (2003) 26216-26226
36. Manygoats K.R., Yazzie M., and Strearns D.M. Ultrastructural damage in chromium picolinate-treated cells: a TEM study. J. Biol. Inorg. Chem. 7 (2002) 791-798
37. Masaki H., Ochiai Y., Okano Y., Yagami A., Akamatsu H., Matsunaga K., Sakurai H., and Suzuki K. A zinc(II)-glycine complex is an effective inducer of metallothionein and removes oxidative stress. J. Derm. Sci. 45 (2007) 73-75
38. Merten K.E., Feng W., Zhang L., Pierce W., Cai J., Klein J.B., and Kang Y.J. Modulation of cytochrome c oxidase-va is possibly involve in metallothionein production from doxorubicin cardiotoxicity. J. Pharmcol. Exp. Ther. 315 (2005) 1314-1319
39. Messer J., Reynolds M., Stoddard L., and Zhitkovich A. Causes of DNA single strand breaks during reduction of chromate by glutathione in vitro and in cells. Free Rad. Biol. Med. 40 (2006) 1981-1992
40. Mididoddi S., McGuirt J.P., Sens M.A., Todd J.H., and Sens D.A. Isoform-specific expression of metallothionein m RNA in the developing and adult human kidney. Toxicol. Lett. 85 (1996) 17-27
41. 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
42. Minami T., Miyata E., Sakamoto Y., Kohama A., Yamazaki H., and Ichida S. Expression of metallothionein mRNAs on mouse cerebellum microglia cells by thimerosal and its metabolites. Toxicology 261 (2009) 25-32
43. Min K.S., Nishida K., and Onosaka S. Protective effect of metallothionein to ras DNA damage induced by hydrogen peroxide and ferric ion-nitrilotriacetic acid. Chemico-Biol. Inter. 122 (1999) 137-152
44. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Meth. 65 (1983) 55-63
45. Nam D.H., Kim E.Y., and Iwata h. Functional analysis of avian metallothionein isoforms: an ecotoxicological approach for assessing potential tolerability to element exposure. Environ. Sci. Technol. 42 (2009) 9391-9396
46. Nudler S.I., Quinteros F.A., Miler E.A., Cabilla J.P., Ronchetti S.A., and Duvilanski B.H. Chromium VI administration induces oxidative stress in hypothalamus and anterior pituitary gland from male rats. Toxicol. Lett. 185 (2009) 187-192
47. Ostrakhovitch E.A., Olsson P.E., Jiang S., and Cherian M.G. Interaction of metallothionein with tumor suppressor p53 protein. FEBS Lett. 580 (2006) 1235-1238
48. Palmiter R.D. Regulation of metallothionein genes by heavy metals appears to be mediated by a zinc-sensitive inhibitor that interacts with a constitutively active transcription factor, MTF-1. Proc. Nat. Acad. Sci. 91 (1994) 1219-1223
49. 2 cells against CYP2E1-dependent toxicity. Free Rad. Biol. Med. 34 (2003) 443-455
50. Perry D.K., Smyth M.J., Stennicke H.R., Salvesen G.S., Duriez P., Poirier G.G., and Hannun Y.A. Zinc is a potent inhibitor of the apoptotic protease, caspase-3: a novel target for zinc in the inhibition of apoptosis. J. Biol.Chem. 272 (1997) 18530-18533
51. Quaife C.J., Findley S.D., Erickson J.C., Froelick G.J., Kelley E.J., Zambrowicz B.P., and Palmiter R.D. Induction of a new metallothionein isoform (MT-IV) occurs during differentiation of stratified squamous epithelia. Biochemistry 33 (1994) 7250-7259
52. Quievryn G., Peterson E., Messer J., and Zhitkovich A. Genotoxicity and mutagenicity of chromium(VI)/ascorbate-generated DNA adducts in human and bacterial cells. Biochemistry 42 (2003) 1061-1070
53. Rajaram R., Nair B.U., and Ramasami T. Chromium (III) induced abnormalities in human lymphocytes cell proliferation: evidence for apoptosis. Biochem. Biophys. Res. Commun. 210 (1995) 434-440
54. Romero-Isart N., and Vasak M. Advances in structure and chemistry of metallothioneins. J. Inorg. Biochem. 88 (2002) 388-396
55. 2 in cultured endothelial cells. Arch. Biochem. Biophys. 302 (1993) 348-355
56. Rudolf E., and Cervinka M. The role of intracellular zinc in chromium(VI)-induced oxidative stress, DNA damage and apoptosis. Chemico-Biol. Inter. 162 (2006) 212-227
57. 6(3) or rhodamine 123, is a reliable fluorescent probe to analyse ΔΨ changes in intact cells: implications for studies on mitochondrial function during apoptosis. FEBS Lett. 411 (1997) 77-82
58. 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. Biochem. Biophy. Acta 1763 (2006) 305-311
59. Sato M., and Bremner I. Oxygen free radicals and metallothionein. Free Radic. Biol. Med. 14 (1993) 325-337
60. Schagger H., and Jagow V.G. Tricine-sodium dodecyl polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Chem. 166 (1987) 368-379
61. Scheuhammer AM., and Cherian MG. Quantification of metallothionein by silver saturation. Methd. in Enzym. 121 (1991) 78-83
62. 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., Lancaster J.R., and Pitt B.R. Metallothionein protects against the cytotoxic and DNA-damaging effects of nitric oxide. Proc. Natl. Acad. Sci. 92 (1995) 4452-4456
63. Shibuya K., Suzuki J.S., Kito H., Naganuma A., Tohyama C., and Satoh M. Protective role of metallothionein in bone marrow injury caused by X-ray irradiation. J. Toxic. Sci. 33 (2008) 479-484
64. +2. Toxicol. Sci. 90 (2006) 369-376
65. Suhy D.A., Simon K.D., Linzer D.I.H., and Halloran T.V. Metallothionein is a part of a zinc-scavenging mechanism for cell survival under conditions of extreme zinc deprivation. J. Biol. Chem. 274 (1999) 9183-9192
66. Suntres Z.E., and Lui E.M.K. Antioxidant effect of zinc and zinc-metallothionein in the acute cytotoxicity of hydrogen peroxide in Ehrlich ascites tumor cells. Chemico-Biol. Inter. 162 (2006) 11-23
67. Uchida Y., Takio K., Titani K., Ihara Y., and Tomonaga M. The growth inhibitory factor that is deficient in the Alzheimer's disease brain is a 68 amino acid metallothionein-like protein. Neuron 7 (1991) 337-347
68. 2 cells after prolonged cadmium exposure. Toxic. In Vitro 21 (2007) 314-319
69. Vasanat C., Rajaram R., and Ramasami T. Apoptosis of lymphocytes induced by chromium(VI/V) is through ROS mediated activation of Src-family tyrosine kinases and caspase-3. Free Rad. Biol. Med. 35 (2003) 1082-1100
70. Wang G.W., Zhou Z., Klein J.B., and Kang Y.J. Inhibition of hypoxia/reoxygenation induced apoptosis in metallothionein over expressing cardiomyocytes. Am. J. Physiol. Heart Circ. Physiol. 280 (2001) H2292-H2299
71. Wang G.W., Klein J.B., and Kang Y.J. Metallothionein inhibits doxorubicin-induced mitochondrial cytochrome c release and caspase-3 activation in cardiomyocytes. J. Pharm. Exp. Ther. 298 (2001) 461-468
72. Wellinghausen N., Kirchner H., and Rink L. The immunobiology of zinc. Immunol. Today (1997) 519-521
73. Winge D.R., Premakumar R., and Rajagopalan K.V. Metal-induced formation of metallothionein in rat liver. Arch. Biochem. Biophys. 170 (1975) 242-252
74. Yang J.P., Merin J.P., Nakano T., Kato T., Kitade Y., and Okamoto T. Inhibition of the DNA binding activity of NF-K{green}B by gold compounds. FEBS Lett. 361 (1995) 89-96
75. Yasutake A., Sawada M., Shimada A., Satoh M., and Tohyama C. Mercury accumulation and its distribution to metallothionein in mouse brain after sub-chronic pulse exposure to mercury vapor. Arch. Toxicol. 78 (2004) 489-495
76. Zhitkovich A. Importance of chromium-DNA adducts in mutagenicity and toxicity of chromium(VI). Chem. Res. Toxicol. 18 (2005) 3-11