Epigallocatechin-3-gallate (EGCG) protects against chromate-induced toxicity in vitro

Toxicology and Applied Pharmacology

Volumn 258, Issue 2, 2012, Pages 166-175

  Wu, Fen ^a   Sun, Hong ^a   Kluz, Thomas ^a   Clancy, Hailey A ^a   Kiok, Kathrin ^a   Costa, Max ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; BEAS 2B cells; Cell death; Chromate; DNA protein cross links; EGCG; Gene expression; Reactive oxygen species

Indexed keywords

CASPASE 3; CHROMIC ACID; DNA; DNA GLYCOSYLTRANSFERASE; EARLY GROWTH RESPONSE FACTOR 1; EPIGALLOCATECHIN GALLATE; EXCISION REPAIR CROSS COMPLEMENTING PROTEIN 4; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45A; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN; PROTEIN PHOSPHATASE 1 REGULATORY SUBUNIT 15; REACTIVE OXYGEN METABOLITE; SINGLE STRAND SELECTIVE MONOFUNCTIONAL URACIL DNA GLYCOSYLASE 1; UNCLASSIFIED DRUG; XRCC4 PROTEIN;

ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CANCER PREVENTION; CELL DEATH; CELL PROTECTION; CHEMICAL CARCINOGENESIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; CROSS LINKING; CYTOTOXICITY; DNA CONTENT; EPITHELIUM CELL; GENE EXPRESSION; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; IN VITRO STUDY; MICROARRAY ANALYSIS; OXIDATIVE STRESS; PROTEIN DNA BINDING; REAL TIME POLYMERASE CHAIN REACTION;

ANTIOXIDANTS; APOPTOSIS; BRONCHI; CARCINOGENS, ENVIRONMENTAL; CATECHIN; CHROMIUM; DOSE-RESPONSE RELATIONSHIP, DRUG; EPITHELIAL CELLS; FREE RADICAL SCAVENGERS; GENE EXPRESSION REGULATION; HUMANS; MICROSCOPY, FLUORESCENCE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYMERASE CHAIN REACTION; REACTIVE OXYGEN SPECIES;

EID: 84855764247     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2011.10.018     Document Type: Article

References (86)

1. Adler H.T., Chinery R., Wu D.Y., Kussick S.J., Payne J.M., Fornace A.J., Tkachuk D.C. Leukemic HRX fusion proteins inhibit GADD34-induced apoptosis and associate with the GADD34 and hSNF5/INI1 proteins. Mol. Cell. Biol. 1999, 19:7050-7060.
2. Ahmad N., Feyes D.K., Nieminen A.L., Agarwal R., Mukhtar H. Green tea constituent epigallocatechin-3-gallate and induction of apoptosis and cell cycle arrest in human carcinoma cells. J. Natl. Cancer Inst. 1997, 89:1881-1886.
3. Ahmed M.M. Regulation of radiation-induced apoptosis by early growth response-1 gene in solid tumors. Curr. Cancer Drug Targets 2004, 4:43-52.
4. Azad N., Iyer A.K., Manosroi A., Wang L., Rojanasakul Y. Superoxide-mediated proteasomal degradation of Bcl-2 determines cell susceptibility to Cr(VI)-induced apoptosis. Carcinogenesis 2008, 29:1538-1545.
5. Bagchi D., Joshi S.S., Bagchi M., Balmoori J., Benner E.J., Kuszynski C.A., Stohs S.J. Cadmium- and chromium-induced oxidative stress, DNA damage, and apoptotic cell death in cultured human chronic myelogenous leukemic K562 cells, promyelocytic leukemic HL-60 cells, and normal human peripheral blood mononuclear cells. J. Biochem. Mol. Toxicol. 2000, 14:33-41.
6. Bagchi D., Bagchi M., Stohs S.J. Chromium (VI)-induced oxidative stress, apoptotic cell death and modulation of p53 tumor suppressor gene. Mol. Cell. Biochem. 2001, 222:149-158.
7. Banu S.K., Stanley J.A., Lee J., Stephen S.D., Arosh J.A., Hoyer P.B., Burghardt R.C. Hexavalent chromium-induced apoptosis of granulosa cells involves selective sub-cellular translocation of Bcl-2 members, ERK1/2 and p53. Toxicol. Appl. Pharmacol. 2011, 251:253-266.
8. Bartek J., Bartkova J., Lukas J. DNA damage signalling guards against activated oncogenes and tumour progression. Oncogene 2007, 26:7773-7779.
9. Baruthio F. Toxic effects of chromium and its compounds. Biol. Trace Elem. Res. 1992, 32:145-153.
10. Carlisle D.L., Pritchard D.E., Singh J., Patierno S.R. Chromium(VI) induces p53-dependent apoptosis in diploid human lung and mouse dermal fibroblasts. Mol. Carcinog. 2000, 28:111-118.
11. Chaum E., Yin J., Yang H., Thomas F., Lang J.C. Quantitative AP-1 gene regulation by oxidative stress in the human retinal pigment epithelium. J. Cell. Biochem. 2009, 108:1280-1291.
12. Chiu A., Shi X.L., Lee W.K., Hill R., Wakeman T.P., Katz A., Xu B., Dalal N.S., Robertson J.D., Chen C., Chiu N., Donehower L. Review of chromium (VI) apoptosis, cell-cycle-arrest, and carcinogenesis. J. Environ. Sci. Health C Environ. Carcinog. Ecotoxicol. Rev. 2010, 28:188-230.
13. Choi Y.T., Jung C.H., Lee S.R., Bae J.H., Baek W.K., Suh M.H., Park J., Park C.W., Suh S.I. The green tea polyphenol (-)-epigallocatechin gallate attenuates beta-amyloid-induced neurotoxicity in cultured hippocampal neurons. Life Sci. 2001, 70:603-614.
14. Chow H.H., Cai Y., Hakim I.A., Crowell J.A., Shahi F., Brooks C.A., Dorr R.T., Hara Y., Alberts D.S. Pharmacokinetics and safety of green tea polyphenols after multiple-dose administration of epigallocatechin gallate and polyphenon E in healthy individuals. Clin. Cancer Res. 2003, 9:3312-3319.
15. Costa M., Zhitkovich A., Toniolo P. DNA-protein cross-links in welders: molecular implications. Cancer Res. 1993, 53:460-463.
16. Costa M., Zhitkovich A., Harris M., Paustenbach D., Gargas M. DNA-protein cross-links produced by various chemicals in cultured human lymphoma cells. J. Toxicol. Environ. Health 1997, 50:433-449.
17. Darwanto A., Theruvathu J.A., Sowers J.L., Rogstad D.K., Pascal T., Goddard W., Sowers L.C. Mechanisms of base selection by human single-stranded selective monofunctional uracil-DNA glycosylase. J. Biol. Chem. 2009, 284:15835-15846.
18. De Flora S., Bagnasco M., Serra D., Zanacchi P. Genotoxicity of chromium compounds. A review. Mutat. Res. 1990, 238:99-172.
19. Deschamps F., Moulin J.J., Wild P., Labriffe H., Haguenoer J.M. Mortality study among workers producing chromate pigments in France. Int. Arch. Occup. Environ. Health 1995, 67:147-152.
20. Elbekai R.H., El-Kadi A.O. The role of oxidative stress in the modulation of aryl hydrocarbon receptor-regulated genes by As3+, Cd2+, and Cr6+. Free Radic. Biol. Med. 2005, 39:1499-1511.
21. Filip A., Daicoviciu D., Clichici S., Mocan T., Muresan A., Postescu I.D. Photoprotective effects of 2 natural products on ultraviolet B-induced oxidative stress and apoptosis in SKH-1 mouse skin. J. Med. Food 2011, 14:761-766.
22. Flores A., Perez J.M. Cytotoxicity, apoptosis, and in vitro DNA damage induced by potassium chromate. Toxicol. Appl. Pharmacol. 1999, 161:75-81.
23. Franchini I., Magnani F., Mutti A. Mortality experience among chromeplating workers. Initial findings. Scand. J. Work Environ. Health 1983, 9:247-252.
24. Gambelunghe A., Piccinini R., Abbritti G., Ambrogi M., Ugolini B., Marchetti C., Migliorati G., Balducci C., Muzi G. Chromium VI-induced apoptosis in a human bronchial epithelial cell line (BEAS-2B) and a lymphoblastic leukemia cell line (MOLT-4). J. Occup. Environ. Med. 2006, 48:319-325.
25. Ha L., Ceryak S., Patierno S.R. Generation of S phase-dependent DNA double-strand breaks by Cr(VI) exposure: involvement of ATM in Cr(VI) induction of gamma-H2AX. Carcinogenesis 2004, 25:2265-2274.
26. Hagerman A.E., Dean R.T., Davies M.J. Radical chemistry of epigallocatechin gallate and its relevance to protein damage. Arch. Biochem. Biophys. 2003, 414:115-120.
27. Higdon J.V., Frei B. Tea catechins and polyphenols: health effects, metabolism, and antioxidant functions. Crit. Rev. Food Sci. Nutr. 2003, 43:89-143.
28. Hildesheim J., Fornace A.J. Gadd45a: an elusive yet attractive candidate gene in pancreatic cancer. Clin. Cancer Res. 2002, 8:2475-2479.
29. Hollander M.C., Sheikh M.S., Yu K., Zhan Q., Iglesias M., Woodworth C., Fornace A.J. Activation of Gadd34 by diverse apoptotic signals and suppression of its growth inhibitory effects by apoptotic inhibitors. Int. J. Cancer 2001, 96:22-31.
30. Ishikawa Y., Nakagawa K., Satoh Y., Kitagawa T., Sugano H., Hirano T., Tsuchiya E. Characteristics of chromate workers' cancers, chromium lung deposition and precancerous bronchial lesions: an autopsy study. Br. J. Cancer 1994, 70:160-166.
31. Jeffrey K.L., Camps M., Rommel C., Mackay C.R. Targeting dual-specificity phosphatases: manipulating MAP kinase signalling and immune responses. Nat. Rev. Drug Discov. 2007, 6:391-403.
32. Jiang X., Wang X. Cytochrome C-mediated apoptosis. Annu. Rev. Biochem. 2004, 73:87-106.
33. Jin C.F., Shen S.R., Zhao B.L. Different effects of five catechins on 6-hydroxydopamine-induced apoptosis in PC12 cells. J. Agric. Food Chem. 2001, 49:6033-6038.
34. Johnson M.K., Loo G. Effects of epigallocatechin gallate and quercetin on oxidative damage to cellular DNA. Mutat. Res. 2000, 459:211-218.
35. Jung J.Y., Mo H.C., Yang K.H., Jeong Y.J., Yoo H.G., Choi N.K., Oh W.M., Oh H.K., Kim S.H., Lee J.H., Kim H.J., Kim W.J. Inhibition by epigallocatechin gallate of CoCl2-induced apoptosis in rat PC12 cells. Life Sci. 2007, 80:1355-1363.
36. Koh S.H., Kim S.H., Kwon H., Kim J.G., Kim J.H., Yang K.H., Kim J., Kim S.U., Yu H.J., Do B.R., Kim K.S., Jung H.K. Phosphatidylinositol-3 kinase/Akt and GSK-3 mediated cytoprotective effect of epigallocatechin gallate on oxidative stress-injured neuronal-differentiated N18D3 cells. Neurotoxicology 2004, 25:793-802.
37. Lambert J.D., Lee M.J., Diamond L., Ju J., Hong J., Bose M., Newmark H.L., Yang C.S. Dose-dependent levels of epigallocatechin-3-gallate in human colon cancer cells and mouse plasma and tissues. Drug Metab. Dispos. 2006, 34:8-11.
38. Langard S. One hundred years of chromium and cancer: a review of epidemiological evidence and selected case reports. Am. J. Ind. Med. 1990, 17:189-215.
39. Langard S. Role of chemical species and exposure characteristics in cancer among persons occupationally exposed to chromium compounds. Scand. J. Work Environ. Health 1993, 19(Suppl. 1):81-89.
40. Lee M.J., Maliakal P., Chen L., Meng X., Bondoc F.Y., Prabhu S., Lambert G., Mohr S., Yang C.S. Pharmacokinetics of tea catechins after ingestion of green tea and (-)-epigallocatechin-3-gallate by humans: formation of different metabolites and individual variability. Cancer Epidemiol. Biomarkers Prev. 2002, 11:1025-1032.
41. Li Q., Suen T.C., Sun H., Arita A., Costa M. Nickel compounds induce apoptosis in human bronchial epithelial Beas-2B cells by activation of c-Myc through ERK pathway. Toxicol. Appl. Pharmacol. 2009, 235:191-198.
42. Luo H., Lu Y., Shi X., Mao Y., Dalal N.S. Chromium (IV)-mediated fenton-like reaction causes DNA damage: implication to genotoxicity of chromate. Ann. Clin. Lab. Sci. 1996, 26:185-191.
43. Manning F.C., Blankenship L.J., Wise J.P., Xu J., Bridgewater L.C., Patierno S.R. Induction of internucleosomal DNA fragmentation by carcinogenic chromate: relationship to DNA damage, genotoxicity, and inhibition of macromolecular synthesis. Environ. Health Perspect. 1994, 102(Suppl. 3):159-167.
44. Mattagajasingh S.N., Misra H.P. Analysis of EDTA-chelatable proteins from DNA-protein crosslinks induced by a carcinogenic chromium(VI) in cultured intact human cells. Mol. Cell. Biochem. 1999, 199:149-162.
45. Miller C.A., Costa M. Analysis of proteins cross-linked to DNA after treatment of cells with formaldehyde, chromate, and cis-diamminedichloroplatinum(II). Mol. Toxicol. 1989, 2:11-26.
46. Nagle D.G., Ferreira D., Zhou Y.D. Epigallocatechin-3-gallate (EGCG): chemical and biomedical perspectives. Phytochemistry 2006, 67:1849-1855.
47. Nie G., Cao Y., Zhao B. Protective effects of green tea polyphenols and their major component, (-)-epigallocatechin-3-gallate (EGCG), on 6-hydroxydopamine-induced apoptosis in PC12 cells. Redox Rep. 2002, 7:171-177.
48. O'Brien T.J., Ceryak S., Patierno S.R. Complexities of chromium carcinogenesis: role of cellular response, repair and recovery mechanisms. Mutat. Res. 2003, 533:3-36.
49. O'Brien T.J., Brooks B.R., Patierno S.R. Nucleotide excision repair functions in the removal of chromium-induced DNA damage in mammalian cells. Mol. Cell. Biochem. 2005, 279:85-95.
50. O'Reilly M.A., Staversky R.J., Watkins R.H., Maniscalco W.M., Keng P.C. p53-independent induction of GADD45 and GADD153 in mouse lungs exposed to hyperoxia. Am. J. Physiol. Lung Cell. Mol. Physiol. 2000, 278:L552-L559.
51. Powolny A., Takahashi K., Hopkins R.G., Loo G. Induction of GADD gene expression by phenethylisothiocyanate in human colon adenocarcinoma cells. J. Cell. Biochem. 2003, 90:1128-1139.
52. Reynolds M., Peterson E., Quievryn G., Zhitkovich A. Human nucleotide excision repair efficiently removes chromium-DNA phosphate adducts and protects cells against chromate toxicity. J. Biol. Chem. 2004, 279:30419-30424.
53. Russo P., Catassi A., Cesario A., Imperatori A., Rotolo N., Fini M., Granone P., Dominioni L. Molecular mechanisms of hexavalent chromium-induced apoptosis in human bronchoalveolar cells. Am. J. Respir. Cell Mol. Biol. 2005, 33:589-600.
54. Salah N., Miller N.J., Paganga G., Tijburg L., Bolwell G.P., Rice-Evans C. Polyphenolic flavanols as scavengers of aqueous phase radicals and as chain-breaking antioxidants. Arch. Biochem. Biophys. 1995, 322:339-346.
55. Sheng R., Gu Z.L., Xie M.L., Zhou W.X., Guo C.Y. EGCG inhibits cardiomyocyte apoptosis in pressure overload-induced cardiac hypertrophy and protects cardiomyocytes from oxidative stress in rats. Acta Pharmacol. Sin. 2007, 28:191-201.
56. Sheng R., Gu Z.L., Xie M.L., Zhou W.X., Guo C.Y. Epigallocatechin gallate protects H9c2 cardiomyoblasts against hydrogen dioxides-induced apoptosis and telomere attrition. Eur. J. Pharmacol. 2010, 641:199-206.
57. Shi X.L., Dalal N.S. Chromium (V) and hydroxyl radical formation during the glutathione reductase-catalyzed reduction of chromium (VI). Biochem. Biophys. Res. Commun. 1989, 163:627-634.
58. Shi X.G., Sun X.L., Gannett P.M., Dalal N.S. Deferoxamine inhibition of Cr(V)-mediated radical generation and deoxyguanine hydroxylation: ESR and HPLC evidence. Arch. Biochem. Biophys. 1992, 293:281-286.
59. Shi X., Mao Y., Knapton A.D., Ding M., Rojanasakul Y., Gannett P.M., Dalal N., Liu K. Reaction of Cr(VI) with ascorbate and hydrogen peroxide generates hydroxyl radicals and causes DNA damage: role of a Cr(IV)-mediated Fenton-like reaction. Carcinogenesis 1994, 15:2475-2478.
60. Shi X., Chiu A., Chen C.T., Halliwell B., Castranova V., Vallyathan V. Reduction of chromium(VI) and its relationship to carcinogenesis. J. Toxicol. Environ. Health B Crit. Rev. 1999, 2:87-104.
61. Shi X., Ye J., Leonard S.S., Ding M., Vallyathan V., Castranova V., Rojanasakul Y., Dong Z. Antioxidant properties of (-)-epicatechin-3-gallate and its inhibition of Cr(VI)-induced DNA damage and Cr(IV)- or TPA-stimulated NF-kappaB activation. Mol. Cell. Biochem. 2000, 206:125-132.
62. Shi H., Hudson L.G., Liu K.J. Oxidative stress and apoptosis in metal ion-induced carcinogenesis. Free Radic. Biol. Med. 2004, 37:582-593.
63. Shimizu M., Deguchi A., Lim J.T., Moriwaki H., Kopelovich L., Weinstein I.B. (-)-Epigallocatechin gallate and polyphenon E inhibit growth and activation of the epidermal growth factor receptor and human epidermal growth factor receptor-2 signaling pathways in human colon cancer cells. Clin. Cancer Res. 2005, 11:2735-2746.
64. Simonato L., Fletcher A.C., Andersen A., Anderson K., Becker N., Chang-Claude J., Ferro G., Gerin M., Gray C.N., Hansen K.S., et al. A historical prospective study of European stainless steel, mild steel, and shipyard welders. Br. J. Ind. Med. 1991, 48:145-154.
65. Slade P.G., Hailer M.K., Martin B.D., Sugden K.D. Guanine-specific oxidation of double-stranded DNA by Cr(VI) and ascorbic acid forms spiroiminodihydantoin and 8-oxo-2'-deoxyguanosine. Chem. Res. Toxicol. 2005, 18:1140-1149.
66. Son Y., Cheong Y.K., Kim N.H., Chung H.T., Kang D.G., Pae H.O. Mitogen-activated protein kinases and reactive oxygen species: how can ROS activate MAPK pathways?. J. Signal Transduct. 2011, 2011:792639.
67. Son Y.O., Hitron J.A., Cheng S., Budhraja A., Zhang Z., Lan Guo N., Lee J.C., Shi X. The dual roles of c-Jun NH2-terminal kinase signaling in Cr(VI)-induced apoptosis in JB6 cells. Toxicol. Sci. 2011, 119:335-345.
68. Standeven A.M., Wetterhahn K.E. Possible role of glutathione in chromium(VI) metabolism and toxicity in rats. Pharmacol. Toxicol. 1991, 68:469-476.
69. Sugden K.D., Stearns D.M. The role of chromium(V) in the mechanism of chromate-induced oxidative DNA damage and cancer. J. Environ. Pathol. Toxicol. Oncol. 2000, 19:215-230.
70. Sun H., Clancy H.A., Kluz T., Zavadil J., Costa M. Comparison of gene expression profiles in chromate transformed BEAS-2B cells. PLoS One 2011, 6:e17982.
71. Tachibana H., Koga K., Fujimura Y., Yamada K. A receptor for green tea polyphenol EGCG. Nat. Struct. Mol. Biol. 2004, 11:380-381.
72. Thiel G., Cibelli G. Regulation of life and death by the zinc finger transcription factor Egr-1. J. Cell. Physiol. 2002, 193:287-292.
73. Thyss R., Virolle V., Imbert V., Peyron J.F., Aberdam D., Virolle T. NF-kappaB/Egr-1/Gadd45 are sequentially activated upon UVB irradiation to mediate epidermal cell death. EMBO J. 2005, 24:128-137.
74. Umeda D., Yano S., Yamada K., Tachibana H. Green tea polyphenol epigallocatechin-3-gallate signaling pathway through 67-kDa laminin receptor. J. Biol. Chem. 2008, 283:3050-3058.
75. Vasant C., Balamurugan K., Rajaram R., Ramasami T. Apoptosis of lymphocytes in the presence of Cr(V) complexes: role in Cr(VI)-induced toxicity. Biochem. Biophys. Res. Commun. 2001, 285:1354-1360.
76. Waalkes M.P., Fox D.A., States J.C., Patierno S.R., McCabe M.J. Metals and disorders of cell accumulation: modulation of apoptosis and cell proliferation. Toxicol. Sci. 2000, 56:255-261.
77. Wakeman T.P., Wyczechowska D., Xu B. Involvement of the p38 MAP kinase in Cr(VI)-induced growth arrest and apoptosis. Mol. Cell. Biochem. 2005, 279:69-73.
78. Wang S., Chen F., Zhang Z., Jiang B.H., Jia L., Shi X. NF-kappaB prevents cells from undergoing Cr(VI)-induced apoptosis. Mol. Cell. Biochem. 2004, 255:129-137.
79. Yao K., Ye P., Zhang L., Tan J., Tang X., Zhang Y. Epigallocatechin gallate protects against oxidative stress-induced mitochondria-dependent apoptosis in human lens epithelial cells. Mol. Vis. 2008, 14:217-223.
80. Ye J., Wang S., Leonard S.S., Sun Y., Butterworth L., Antonini J., Ding M., Rojanasakul Y., Vallyathan V., Castranova V., Shi X. Role of reactive oxygen species and p53 in chromium(VI)-induced apoptosis. J. Biol. Chem. 1999, 274:34974-34980.
81. Yin J., Thomas F., Lang J.C., Chaum E. Modulation of oxidative stress responses in the human retinal pigment epithelium following treatment with vitamin C. J. Cell. Physiol. 2010, 226:2025-2032.
82. Zhang D.D. Mechanistic studies of the Nrf2-Keap1 signaling pathway. Drug Metab. Rev. 2006, 38:769-789.
83. Zhang Z., Leonard S.S., Wang S., Vallyathan V., Castranova V., Shi X. Cr (VI) induces cell growth arrest through hydrogen peroxide-mediated reactions. Mol. Cell. Biochem. 2001, 222:77-83.
84. Zhang Q., Kluz T., Salnikow K., Costa M. Comparison of the cytotoxicity, cellular uptake, and DNA-protein crosslinks induced by potassium chromate in lymphoblast cell lines derived from three different individuals. Biol. Trace Elem. Res. 2002, 86:11-22.
85. Zhitkovich A., Costa M. A simple, sensitive assay to detect DNA-protein crosslinks in intact cells and in vivo. Carcinogenesis 1992, 13:1485-1489.
86. Zhitkovich A., Voitkun V., Kluz T., Costa M. Utilization of DNA-protein cross-links as a biomarker of chromium exposure. Environ. Health Perspect. 1998, 106(Suppl. 4):969-974.