The effects of hexavalent chromium on thioredoxin reductase and peroxiredoxins in human bronchial epithelial cells

Free Radical Biology and Medicine

Volumn 47, Issue 10, 2009, Pages 1477-1485

  Myers, Judith M ^a   Myers, Charles R ^a,b  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b FREE RADICAL RESEARCH CENTER   (United States)

Author keywords

BEAS 2B cells; Chromate; Chromium; Free radicals; Peroxiredoxin; Thioredoxin reductase

Indexed keywords

APOPTOSIS SIGNAL REGULATING KINASE 1; CELL PROTEIN; CHROMIUM; DISULFIDE; PEROXIREDOXIN; PEROXIREDOXIN 1; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; THIOREDOXIN 1; THIOREDOXIN 2; THIOREDOXIN REDUCTASE;

AMINO TERMINAL SEQUENCE; ARTICLE; BRONCHUS MUCOSA; CONTROLLED STUDY; ELECTRON; EPITHELIUM CELL; EXPOSURE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOPRECIPITATION; OXIDATION REDUCTION REACTION; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN DOMAIN; SIGNAL TRANSDUCTION;

BRONCHI; CELLS, CULTURED; CHROMIUM; DOSE-RESPONSE RELATIONSHIP, DRUG; EPITHELIAL CELLS; HUMANS; OXIDATION-REDUCTION; PEROXIREDOXINS; THIOREDOXIN-DISULFIDE REDUCTASE;

EID: 70350034011     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2009.08.015     Document Type: Article

References (72)

1. Taioli E., Zhitkovich A., Kinney P., Udasin I., Toniolo P., and Costa M. Increased DNA-protein crosslinks in lymphocytes of residents living in chromium-contaminated areas. Biol. Trace Elem. Res. 50 (1995) 175-180
2. Costa M., Zhitkovich A., Toniolo P., Taioli E., Popov T., and Lukanova A. Monitoring human lymphocytic DNA-protein cross-links as biomarkers of biologically active doses of chromate. Environ. Health Perspect. 104 (1996) 917-919
3. Ishikawa Y., Nakagawa K., Satoh Y., Kitagawa T., Sugano H., Hirano T., and Tsuchiya E. Characteristics of chromate workers' cancers, chromium lung deposition and precancerous bronchial lesions: an autopsy study. Br. J. Cancer 70 (1994) 160-166
4. Ishikawa Y., Nakagawa K., Satoh Y., Kitagawa T., Sugano H., Hirano T., and Tsuchiya E. "Hot spots" of chromium accumulation at bifurcations of chromate workers' bronchi. Cancer Res. 54 (1994) 2343-2346
5. Raithel H.-J., Schaller K.-H., Kraus T., and Lehnert G. Biomonitoring of nickel and chromium in human pulmonary tissue. Int. Arch. Occup. Environ. Health 65 (1993) S197-S200
6. Hayes R.B. Carcinogenic effects of chromium. In: Langard S. (Ed). Biological and Environmental Aspects of Chromium Vol. 5 (1982), Elsevier, Amsterdam 221-239
7. Deschamps F., Moulin J.J., Wild P., Labriffe H., and Haguenoer J.M. Mortality study among workers producing chromate pigments in France. Int. Arch. Occup. Environ. Health 67 (1995) 147-152
8. Langard S. Role of chemical species and exposure characteristics in cancer among persons occupationally exposed to chromium compounds. Scand. J. Work Environ. Health 19 Suppl. 1 (1993) 81-89
9. Cantoni O., and Costa M. Analysis of the induction of alkali sensitive sites in the DNA by chromate and other agents that induce single strand breaks. Carcinogenesis 5 (1984) 1207-1209
10. Christie N.T., Cantoni O., Evans R.M., Meyn R.E., and Costa M. Use of mammalian DNA repair-deficient mutants to assess the effects of toxic metal compounds on DNA. Biochem. Pharmacol. 33 (1984) 1661-1670
11. Levy L.S., and Venitt S. Carcinogenicity and mutagenicity of chromium compounds: the association between bronchial metaplasia and neoplasia. Carcinogenesis 7 (1986) 831-835
12. Tsapakos M.J., Hampton T.H., and Wetterhahn K.E. Chromium(VI)-induced DNA lesions and chromium distribution on rat kidney, liver and lung. Cancer Res. 43 (1983) 5662-5667
13. Whiting R.F., Stich H.F., and Koropatnick D.J. DNA damage and DNA repair in cultured human cells exposed to chromate. Chem.-Biol. Interact. 26 (1979) 267-280
14. Becker N., Chang-Claude J., and Frentzel-Beyme R. Risk of cancer for arc welders in the Federal Republic of Germany: results of a second follow up (1983-8). Br. J. Ind. Med. 48 (1991) 675-683
15. Nakagawa K., Matsubara T., Kinoshita I., Tsuchiya E., Sugano H., and Hirano T. Surveillance study of a group of chromate workers-early detection and high incidence of lung cancer [in Japanese]. Lung Cancer 24 (1984) 301-310
16. Franchini I., Magnani F., and Mutti A. Mortality experience among chromplating workers. Scand. J. Work Environ. Health 9 (1983) 247-252
17. Stern R.M. Assessment of risk of lung cancer for welders. Arch. Environ. Health 38 (1983) 148-155
18. Environmental Protection Agency. Chromium. Washington, DC: Office of Health and Environmental Assessment, U.S. EPA.
19. Gadd G.M., and White C. Microbial treatment of metal pollution-a working biotechnology?. TIBTECH (1993) 11
20. Zhitkovich A., Voitkun V., Kluz T., and Costa M. Utilization of DNA-protein cross-links as a biomarker of chromium exposure. Environ. Health Perspect. 106 Suppl. 4 (1998) 969-974
21. Buttner B., and Beyersmann D. Modification of the erythrocyte anion carrier by chromate. Xenobiotica 15 (1985) 735-741
22. Standeven A.M., and Wetterhahn K.E. Ascorbate is the principal reductant of chromium(VI) in rat lung ultrafiltrates and cytosols, and mediates chromium-DNA binding in vitro. Carcinogenesis 13 (1992) 1319-1324
23. Mikalsen A., Alexander J., and Ryberg D. Microsomal metabolism of hexavalent chromium: inhibitory effect of oxygen and involvement of cytochrome P-450. Chem.-Biol. Interact. 69 (1989) 175-192
24. Jennette K.W. Microsomal reduction of the carcinogen chromate produces chromium(V). J. Am. Chem. Soc. 104 (1982) 874-875
25. Shi X., Dong Z., Dalal N.S., and Gannett P.M. Chromate-mediated free radical generation from cysteine, penicillamine, hydrogen peroxide, and lipid hydroperoxides. Biochim. Biophys. Acta 1226 (1994) 65-72
26. Shi X.L., and Dalal N.S. One-electron reduction of chromate by NADPH-dependent glutathione reductase. J. Inorg. Biochem. 40 (1990) 1-12
27. Suzuki Y., and Fukuda K. Reduction of hexavalent chromium by ascorbic acid and glutathione with special reference to the rat lung. Arch. Toxicol. 64 (1990) 169-176
28. 5: generation of hydroxyl radical and superoxide. Free Radic. Biol. Med. 42 (2007) 738-755
29. Myers C.R., Myers J.M., Carstens B.P., and Antholine W.E. Reduction of chromium(VI) to chromium(V) by human microsomal enzymes: effects of iron and quinones. Toxic Subst. Mech. 19 (2000) 25-51
30. Sugden K.D., Campo C.K., and Martin B.D. Direct oxidation of guanine and 7,8-dihydro-8-oxoguanine in DNA by a high-valent chromium complex: a possible mechanism for chromate genotoxicity. Chem. Res. Toxicol. 14 (2001) 1315-1322
31. Sugden K.D. Formation of modified cleavage termini from the reaction of chromium(V) with DNA. J. Inorg. Biochem. 77 (1999) 177-183
32. Standeven A.M., and Wetterhahn K.E. Is there a role for reactive oxygen species in the mechanism of chromium(VI) carcinogenesis?. Chem. Res. Toxicol. 4 (1991) 616-625
33. Dillon C.T., Lay P.A., Bonin A.M., Cholewa M., Legge G.J.F., Collins T.J., and Kostka K.L. Permeability, cytotoxicity, and genotoxicity of chromium(V) and chromium(VI) complexes in V79 Chinese hamster lung cells. Chem. Res. Toxicol. 11 (1998) 119-129
34. Shi X., Chiu A., Chen C.T., Halliwell B., Castranova V., and Vallyathan V. Reduction of chromium(VI) and its relationship to carcinogenesis. J. Toxicol. Environ. Health B 2 (1999) 87-104
35. Shi X., and Dalal N.S. The role of superoxide radical in chromium(VI)-generated hydroxyl radical: the Cr(VI) Haber-Weiss cycle. Arch. Biochem. Biophys. 292 (1992) 323-327
36. Shi X., Ding M., Ye J., Wang S., Leonard S.S., Zang L., Castranova V., Vallyathan V., Chiu A., Dalal N., and Liu K. Cr(IV) causes activation of nuclear transcription factor-κB, DNA strand breaks and dG hydroxylation via free radical reactions. J. Inorg. Biochem. 75 (1999) 37-44
37. Nkabyo Y.S., Ziegler T.R., Gu L.H., Watson W.H., and Jones D.P. Glutathione and thioredoxin redox during differentiation in human colon epithelial (Caco-2) cells. Am. J. Physiol. Gastrointest. Liver Physiol. 283 (2002) G1352-G1359
38. Hansen J.M., Go Y.M., and Jones D.P. Nuclear and mitochondrial compartmentation of oxidative stress and redox signaling. Annu. Rev. Pharmacol. Toxicol. 46 (2006) 215-234
39. Powis G., and Montfort W.R. Properties and biological activities of thioredoxins. Annu. Rev. Biophys. Biomol. Struct. 30 (2001) 421-455
40. Watson W.H., Pohl J., Montfort W.R., Stuchlik O., Reed M.S., Powis G., and Jones D.P. Redox potential of human thioredoxin 1 and identification of a second dithiol/disulfide motif. J. Biol. Chem. 278 (2003) 33408-33415
41. Szadkowski A., and Myers C.R. Acrolein oxidizes the cytosolic and mitochondrial thioredoxins in human endothelial cells. Toxicology 243 (2008) 164-176
42. Myers J.M., Antholine W.E., and Myers C.R. Hexavalent chromium causes the oxidation of thioredoxin in human bronchial epithelial cells. Toxicology 246 (2008) 222-233
43. Nordberg J., and Arnér E.S. Reactive oxygen species, antioxidants, and the mammalian thioredoxin system. Free Radic. Biol. Med. 31 (2001) 1287-1312
44. Arnér E.S.J., and Holmgren A. Physiological functions of thioredoxin and thioredoxin reductase. Eur. J. Biochem. 267 (2000) 6102-6109
45. Nonn L., Williams R.R., Erickson R.P., and Powis G. The absence of mitochondrial thioredoxin 2 causes massive apoptosis, exencephaly, and early embryonic lethality in homozygous mice. Mol. Cell. Biol. 23 (2003) 916-922
46. 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
47. Chen Y., Cai J., and Jones D.P. Mitochondrial thioredoxin in regulation of oxidant-induced cell death. FEBS Lett. 580 (2006) 6596-6602
48. Kim J.A., Park S., Kim K., Rhee S.G., and Kang S.W. Activity assay of mammalian 2-Cys peroxiredoxins using yeast thioredoxin reductase system. Anal. Biochem. 338 (2005) 216-223
49. Chang T.S., Cho C.S., Park S., Yu S., Kang S.W., and Rhee S.G. Peroxiredoxin III, a mitochondrion-specific peroxidase, regulates apoptotic signaling by mitochondria. J. Biol. Chem. 279 (2004) 41975-41984
50. Ichijo H., Nishida E., Irie K., ten Dijke P., Saitoh M., Moriguchi T., Takagi M., Matsumoto K., Miyazono K., and Gotoh Y. Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways. Science 275 (1997) 90-94
51. 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
52. Tobiume K., Saitoh M., and Ichijo H. Activation of apoptosis signal-regulating kinase 1 by the stress-induced activating phosphorylation of pre-formed oligomer. J. Cell. Physiol. 191 (2002) 95-104
53. Halvey P.J., Watson W.H., Hansen J.M., Go Y.M., Samali A., and Jones D.P. Compartmental oxidation of thiol-disulphide redox couples during epidermal growth factor signalling. Biochem. J. 386 (2005) 215-219
54. Sun Y., and Rigas B. The thioredoxin system mediates redox-induced cell death in human colon cancer cells: implications for the mechanism of action of anticancer agents. Cancer Res. 68 (2008) 8269-8277
55. Cox A.G., Pullar J.M., Hughes G., Ledgerwood E.C., and Hampton M.B. Oxidation of mitochondrial peroxiredoxin 3 during the initiation of receptor-mediated apoptosis. Free Radic. Biol. Med. 44 (2008) 1001-1009
56. Arnér E.S., Bjornstedt M., and Holmgren A. 1-Chloro-2,4-dinitrobenzene is an irreversible inhibitor of human thioredoxin reductase: loss of thioredoxin disulfide reductase activity is accompanied by a large increase in NADPH oxidase activity. J. Biol. Chem. 270 (1995) 3479-3482
57. Holmgren A. Bovine thioredoxin system: purification of thioredoxin reductase from calf liver and thymus and studies of its function in disulfide reduction. J. Biol. Chem. 252 (1977) 4600-4606
58. Gromer S., Arscott L.D., Williams Jr. C.H., Schirmer R.H., and Becker K. Human placenta thioredoxin reductase: isolation of the selenoenzyme, steady state kinetics, and inhibition by therapeutic gold compounds. J. Biol. Chem. 273 (1998) 20096-20101
59. Wise J.P., Leonard J.C., and Patierno S.R. Clastogenicity of lead chromate particles in hamster and human cells. Mutat. Res 278 (1992) 69-79
60. Myers C.R., and Myers J.M. Cloning and sequence of cymA, a gene encoding a tetraheme cytochrome c required for reduction of iron(III), fumarate, and nitrate by Shewanella putrefaciens MR-1. J. Bacteriol. 179 (1997) 1143-1152
61. Getz E.B., Xiao M., Chakrabarty T., Cooke R., and Selvin P.R. A comparison between the sulfhydryl reductants tris(2-carboxyethyl)phosphine and dithiothreitol for use in protein biochemistry. Anal. Biochem. 273 (1999) 73-80
62. Sandalova T., Zhong L., Lindqvist Y., Holmgren A., and Schneider G. Three-dimensional structure of a mammalian thioredoxin reductase: implications for mechanism and evolution of a selenocysteine-dependent enzyme. Proc. Natl. Acad. Sci. USA 98 (2001) 9533-9538
63. Jacob C., Giles G.I., Giles N.M., and Sies H. Sulfur and selenium: the role of oxidation state in protein structure and function. Angew. Chem. Int. Ed. Engl. 42 (2003) 4742-4758
64. Nordberg J., Zhong L., Holmgren A., and Arnér E.S. Mammalian thioredoxin reductase is irreversibly inhibited by dinitrohalobenzenes by alkylation of both the redox active selenocysteine and its neighboring cysteine residue. J. Biol. Chem. 273 (1998) 10835-10842
65. Borthiry G.R., Antholine W.E., Myers J.M., and Myers C.R. Reductive activation of hexavalent chromium by human lung epithelial cells: generation of Cr(V) and Cr(V)-thiol species. J. Inorg. Biochem. 102 (2008) 1449-1462
66. 2-catalzyed by recyclable chromic potassium sulphate at room temperature. React. Kinet. Catal. Lett. 93 (2008) 141-148
67. Watson W.H., Heilman J.M., Hughes L.L., and Spielberger J.C. Thioredoxin reductase-1 knockdown does not result in thioredoxin-1 oxidation. Biochem. Biophys. Res. Commun. 368 (2008) 832-836
68. 2 is not reflected in its reaction with other oxidants and thiol reagents. J. Biol. Chem. 282 (2007) 11885-11892
69. Cox A.G., Brown K.K., Arnér E.S., and Hampton M.B. The thioredoxin reductase inhibitor auranofin triggers apoptosis through a Bax/Bak-dependent process that involves peroxiredoxin 3 oxidation. Biochem. Pharmacol. 76 (2008) 1097-1109
70. Lee Y.M., Park S.H., Shin D.I., Hwang J.Y., Park B., Park Y.J., Lee T.H., Chae H.Z., Jin B.K., Oh T.H., and Oh Y.J. Oxidative modification of peroxiredoxin is associated with drug-induced apoptotic signaling in experimental models of Parkinson disease. J. Biol. Chem. 283 (2008) 9986-9998
71. Holmgren A. Thioredoxin. Annu. Rev. Biochem 54 (1985) 237-271
72. Anestål K., Prast-Nielsen S., Cenas N., and Arnér E.S.J. Cell death by SecTRAPs: thioredoxin reductase as a prooxidant killer of cells. PLoS ONE e1846 (2008) 3