Cytotoxicity of arsenic trioxide is enhanced by (-)-epigallocatechin-3-gallate via suppression of ferritin in cancer cells

Toxicology and Applied Pharmacology

Volumn 250, Issue 1, 2011, Pages 69-77

  Lee, Te Chang ^a,c   Cheng, I Cheng ^b   Shue, Jun Jie ^a,c   Wang, T C ^b  

^a INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

^b INSTITUTE OF CELLULAR AND ORGANISMIC BIOLOGY   (Taiwan)

^c NATIONAL YANG MING UNIVERSITY   (Taiwan)

Author keywords

( ) Epigallocatechin 3 gallate; Arsenic trioxide; Caffeic acid phenethyl ester; Ferritin; Heme oxygenase 1

Indexed keywords

ARSENIC TRIOXIDE; EPIGALLOCATECHIN GALLATE; FERRITIN; FERROUS ION; HEME OXYGENASE 1; HYDROGEN PEROXIDE; REACTIVE OXYGEN METABOLITE; WATER;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL CULTURE; CARCINOGENICITY; CATALYSIS; CELL DAMAGE; CELL DEATH; CELL STRAIN APL; CELL STRAIN HL 60; CONTROLLED STUDY; CYTOTOXICITY; FENTON REACTION; HUMAN; HUMAN CELL; MITOCHONDRION; PROMYELOCYTIC LEUKEMIA;

ANTINEOPLASTIC AGENTS; APOPTOSIS; ARSENICALS; CAFFEIC ACIDS; CATECHIN; CELL LINE, TUMOR; CYTOTOXINS; DRUG SYNERGISM; FERRITINS; HEME OXYGENASE (DECYCLIZING); HL-60 CELLS; HUMANS; NEOPLASMS; OXIDES; PHENYLETHYL ALCOHOL;

EID: 78649629031     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2010.10.005     Document Type: Article

References (67)

1. Azam S., Hadi N., Khan N.U., Hadi S.M. Prooxidant property of green tea polyphenols epicatechin and epigallocatechin-3-gallate: implications for anticancer properties. Toxicol. In Vitro 2004, 18:555-561.
2. Balogun E., Hoque M., Gong P., Killeen E., Green C.J., Foresti R., Alam J., Motterlini R. Curcumin activates the haem oxygenase-1 gene via regulation of Nrf2 and the antioxidant-responsive element. Biochem. J. 2003, 371:887-895.
3. Baysan A., Yel L., Gollapudi S., Su H., Gupta S. Arsenic trioxide induces apoptosis via the mitochondrial pathway by upregulating the expression of Bax and Bim in human B cells. Int. J. Oncol. 2007, 30:313-318.
4. Bremer E., van Dam G., Kroesen B.J., de Leij L., Helfrich W. Targeted induction of apoptosis for cancer therapy: current progress and prospects. Trends Mol. Med. 2006, 12:382-393.
5. Carmody R.J., Cotter T.G. Signalling apoptosis: a radical approach. Redox Rep. 2001, 6:77-90.
6. Chang M.J. UV absorption as an approximation for cell number in in vitro toxicity testing. Bull. Environ. Contam. Toxicol. 1991, 47:190-197.
7. Chen C.J., Chuang Y.C., Lin T.M., Wu H.Y. Malignant neoplasms among residents of a blackfoot disease-endemic area in Taiwan: high-arsenic artesian well water and cancers. Cancer Res. 1985, 45:5895-5899.
8. Chen G.Q., Zhu J., Shi X.G., Ni J.H., Zhong H.J., Si G.Y., Jin X.L., Tang W., Li X.S., Xong S.M., Shen Z.X., Sun G.L., Ma J., Zhang P., Zhang T.D., Gazin C., Naoe T., Chen S.J., Wang Z.Y., Chen Z. In vitro studies on cellular and molecular mechanisms of arsenic trioxide (As2O3) in the treatment of acute promyelocytic leukemia: As2O3 induces NB4 cell apoptosis with downregulation of Bcl-2 expression and modulation of PML-RAR alpha/PML proteins. Blood 1996, 88:1052-1061.
9. Chen Z., Wang Z.Y., Chen S.J. Acute promyelocytic leukemia: cellular and molecular basis of differentiation and apoptosis. Pharmacol. Ther. 1997, 76:141-149.
10. Cooper K.L., Liu K.J., Hudson L.G. Contributions of reactive oxygen species and mitogen-activated protein kinase signaling in arsenite-stimulated hemeoxygenase-1 production. Toxicol Appl Pharmacol. 2006.
11. Cory S., Adams J.M. The Bcl2 family: regulators of the cellular life-or-death switch. Nat. Rev. Cancer 2002, 2:647-656.
12. Cory S., Huang D.C., Adams J.M. The Bcl-2 family: roles in cell survival and oncogenesis. Oncogene 2003, 22:8590-8607.
13. Davison K., Mann K.K., Miller W.H. Arsenic trioxide: mechanisms of action. Semin. Hematol. 2002, 39:3-7.
14. Diaz Z., Colombo M., Mann K.K., Su H., Smith K.N., Bohle D.S., Schipper H.M., Miller W.H. Trolox selectively enhances arsenic-mediated oxidative stress and apoptosis in APL and other malignant cell lines. Blood 2005, 105:1237-1245.
15. Elbling L., Weiss R.M., Teufelhofer O., Uhl M., Knasmueller S., Schulte-Hermann R., Berger W., Micksche M. Green tea extract and (-)-epigallocatechin-3-gallate, the major tea catechin, exert oxidant but lack antioxidant activities. FASEB J. 2005, 19:807-809.
16. Engel R.H., Evens A.M. Oxidative stress and apoptosis: a new treatment paradigm in cancer. Front. Biosci. 2006, 11:300-312.
17. Evens A.M., Tallman M.S., Gartenhaus R.B. The potential of arsenic trioxide in the treatment of malignant disease: past, present, and future. Leuk. Res. 2004, 28:891-900.
18. Fenton H.J.H. Oxidation of tartaric acid in presence of iron. J. Chem. Soc. Trans. 1894, 65:899-910.
19. Fojo T., Bates S. Arsenic trioxide (As(2)O(3)): still a mystery. Cell Cycle 2002, 1:183-186.
20. Fojo T., Bates S. Strategies for reversing drug resistance. Oncogene 2003, 22:7512-7523.
21. Furukawa A., Oikawa S., Murata M., Hiraku Y., Kawanishi S. (-)-Epigallocatechin gallate causes oxidative damage to isolated and cellular DNA. Biochem. Pharmacol. 2003, 66:1769-1778.
22. Gallagher R.E. Co-biomodulation with arsenic trioxide in multiple myeloma. Leuk. Res. 2001, 25:237-239.
23. Gerl R., Vaux D.L. Apoptosis in the development and treatment of cancer. Carcinogenesis 2005, 26:263-270.
24. Ghobrial I.M., Witzig T.E., Adjei A.A. Targeting apoptosis pathways in cancer therapy. CA Cancer J. Clin. 2005, 55:178-194.
25. Gianni M., Kalac Y., Ponzanelli I., Rambaldi A., Terao M., Garattini E. Tyrosine kinase inhibitor STI571 potentiates the pharmacologic activity of retinoic acid in acute promyelocytic leukemia cells: effects on the degradation of RARalpha and PML-RARalpha. Blood 2001, 97:3234-3243.
26. Grignani F., Ferrucci P.F., Testa U., Talamo G., Fagioli M., Alcalay M., Mencarelli A., Peschle C., Nicoletti I., et al. The acute promyelocytic leukemia-specific PML-RAR alpha fusion protein inhibits differentiation and promotes survival of myeloid precursor cells. Cell 1993, 74:423-431.
27. Gupta S., Yel L., Kim D., Kim C., Chiplunkar S., Gollapudi S. Arsenic trioxide induces apoptosis in peripheral blood T lymphocyte subsets by inducing oxidative stress: a role of Bcl-2. Mol. Cancer Ther. 2003, 2:711-719.
28. Halliwell B., Gutteridge J.M. Role of free radicals and catalytic metal ions in human disease: an overview. Meth. Enzymol. 1990, 186:1-85.
29. Hengartner M.O. The biochemistry of apoptosis. Nature 2000, 407:770-776.
30. Hii C.S.T., Huang Z.H., Bilney A., Costabile M., Murray A.W., Rathjen D.A., Der C.J., Ferrante A. Stimulation of p38 Phosphorylation and Activity by Arachidonic Acid in HeLa Cells, HL60 Promyelocytic Leukemic Cells, and Human Neutrophils. J. Biol. Chem. 1998, 273:19277-19282.
31. Horng S.B., Kuo H.H., Lin M.Y., Lin W.W., Wang T.C. Human gastric cells resistant to (-)-epigallocatechin gallate show cross-resistance to several environmental pollutants. Food Chem. Toxicol. 2007, 45:2171-2178.
32. Hu C., Kitts D.D. Evaluation of antioxidant activity of epigallocatechin gallate in biphasic model systems in vitro. Mol. Cell. Biochem. 2001, 218:147-155.
33. Jiang X., Wong B., Yuen S., Jiang S., Cho C., Lai K., Lin M., Kung H., Lam S. Arsenic trioxide induces apoptosis in human gastric cancer cells through up-regulation of p53 and activation of caspase-3. Int. J. Cancer 2001, 91:173-179.
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. Kanadzu M., Lu Y., Morimoto K. Dual function of (-)-epigallocatechin gallate (EGCG) in healthy human lymphocytes. Cancer Lett. 2006, 241:250-255.
36. Kumamoto M., Sonda T., Nagayama K., Tabata M. Effects of pH and metal ions on antioxidative activities of catechins. Biosci. Biotechnol. Biochem. 2001, 65:126-132.
37. Kuo H.H., Shyu S.S., Wang T.C. Genotoxicity of low dose N-nitroso propoxur to human gastric cells. Food Chem. Toxicol. 2008, 46:1619-1626.
38. Lee T.C., Ho I.C. Modulation of cellular antioxidant defense activities by sodium arsenite in human fibroblasts. Arch. Toxicol. 1995, 69:498-504.
39. Lu M., Levin J., Sulpice E., Sequeira-Le Grand A., Alemany M., Caen J.P., Han Z.C. Effect of arsenic trioxide on viability, proliferation, and apoptosis in human megakaryocytic leukemia cell lines. Exp. Hematol. 1999, 27:845-852.
40. Miller J.W. Molecular targets of arsenic trioxide in malignant cells. Oncologist 2002, 7:14-19.
41. Miller W.H., Schipper H.M., Lee J.S., Singer J., Waxman S. Mechanisms of action of arsenic trioxide. Cancer Res. 2002, 62:3893-3903.
42. Mologni L., Marchesi E., Nielsen P.E., Gambacorti-Passerini C. Inhibition of promyelocytic leukemia (PML)/retinoic acid receptor-alpha and PML expression in acute promyelocytic leukemia cells by anti-PML peptide nucleic acid. Cancer Res. 2001, 61:5468-5473.
43. Nagle D.G., Ferreira D., Zhou Y.D. Epigallocatechin-3-gallate (EGCG): chemical and biomedical perspectives. Phytochemistry 2006, 67:1849-1855.
44. Nakagawa H., Wachi M., Woo J.T., Kato M., Kasai S., Takahashi F., Lee I.S., Nagai K. Fenton reaction is primarily involved in a mechanism of (-)-epigallocatechin-3-gallate to induce osteoclastic cell death. Biochem. Biophys. Res. Commun. 2002, 292:94-101.
45. Nakagawa H., Hasumi K., Woo J.T., Nagai K., Wachi M. Generation of hydrogen peroxide primarily contributes to the induction of Fe(II)-dependent apoptosis in Jurkat cells by (-)-epigallocatechin gallate. Carcinogenesis 2004, 25:1567-1574.
46. Nakazato T., Ito K., Miyakawa Y., Kinjo K., Yamada T., Hozumi N., Ikeda Y., Kizaki M. Catechin, a green tea component, rapidly induces apoptosis of myeloid leukemia cells via modulation of reactive oxygen species production in vitro and inhibits tumor growth in vivo. Haematologica 2005, 90:317-325.
47. Perona R., Sanchez-Perez I. Control of oncogenesis and cancer therapy resistance. Br. J. Cancer 2004, 90.
48. Raza H., John A. Green tea polyphenol epigallocatechin-3-gallate differentially modulates oxidative stress in PC12 cell compartments. Toxicol. Appl. Pharmacol. 2005, 207:212-220.
49. Rossman T.G., Uddin A.N., Burns F.J., Bosland M.C. Arsenite cocarcinogenesis: an animal model derived from genetic toxicology studies. Environ. Health Perspect. 2002, 110(Suppl 5):749-752.
50. Ryter S.W., Tyrrell R.M. The heme synthesis and degradation pathways: role in oxidant sensitivity. Heme oxygenase has both pro- and antioxidant properties. Free Radic. Biol. Med. 2000, 28:289-309.
51. Sakagami H., Arakawa H., Maeda M., Satoh K., Kadofuku T., Fukuchi K., Gomi K. Production of hydrogen peroxide and methionine sulfoxide by epigallocatechin gallate and antioxidants. Anticancer Res. 2001, 21:2633-2641.
52. Sanchez Y., Calle C., de Blas E., Aller P. Modulation of arsenic trioxide-induced apoptosis by genistein and functionally related agents in U937 human leukemia cells. Regulation by ROS and mitogen-activated protein kinase. Chem. Biol. Interact. 2009, 182:37-44.
53. Sasaki A., Oshima Y., Fujimura A. An approach to elucidate potential mechanism of renal toxicity of arsenic trioxide. Exp. Hematol. 2007, 35:252-262.
54. Scapagnini G., Foresti R., Calabrese V., Giuffrida Stella A.M., Green C.J., Motterlini R. Caffeic acid phenethyl ester and curcumin: a novel class of heme oxygenase-1 inducers. Mol. Pharmacol. 2002, 61:554-561.
55. Simon H.U., Haj-Yehia A., Levi-Schaffer F. Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 2000, 5:415-418.
56. Suzuki K., Tanaka I., Nakanishi I., Kurematsu A., Yakumaru H., Ikota N., Ishihara H. Drastic effect of several caffeic acid derivatives on the induction of heme oxygenase-1 expression revealed by quantitative real-time RT-PCR. Biofactors 2006, 28:151-158.
57. Tian B., Sun Z., Xu Z., Hua Y. Chemiluminescence analysis of the prooxidant and antioxidant effects of epigallocatechin-3-gallate. Asia Pac. J. Clin. Nutr. 2007, 16(Suppl 1):153-157.
58. Tseng W.P., Chu H.M., How S.W., Fong J.M., Lin C.S., Yeh S. Prevalence of skin cancer in an endemic area of chronic arsenicism in Taiwan. J. Natl Cancer Inst. 1968, 40:453-463.
59. Urbanski N.K., Beresewicz A. Generation of *OH initiated by interaction of Fe2+ and Cu+ with dioxygen; comparison with the Fenton chemistry. Acta Biochim. Pol. 2000, 47:951-962.
60. Vittal R., Selvanayagam Z.E., Sun Y., Hong J., Liu F., Chin K.V., Yang C.S. Gene expression changes induced by green tea polyphenol (-)-epigallocatechin-3-gallate in human bronchial epithelial 21BES cells analyzed by DNA microarray. Mol. Cancer Ther. 2004, 3:1091-1099.
61. Weisburg J.H., Weissman D.B., Sedaghat T., Babich H. In vitro cytotoxicity of epigallocatechin gallate and tea extracts to cancerous and normal cells from the human oral cavity. Basic Clin. Pharmacol. Toxicol. 2004, 95:191-200.
62. Yamamoto T., Hsu S., Lewis J., Wataha J., Dickinson D., Singh B., Bollag W.B., Lockwood P., Ueta E., Osaki T., Schuster G. Green tea polyphenol causes differential oxidative environments in tumor versus normal epithelial cells. J. Pharmacol. Exp. Ther. 2003, 307:230-236.
63. Yang G.Y., Liao J., Li C., Chung J., Yurkow E.J., Ho C.T., Yang C.S. Effect of black and green tea polyphenols on c-jun phosphorylation and H(2)O(2) production in transformed and non-transformed human bronchial cell lines: possible mechanisms of cell growth inhibition and apoptosis induction. Carcinogenesis 2000, 21:2035-2039.
64. Yih L.H., Peck K., Lee T.C. Changes in gene expression profiles of human fibroblasts in response to sodium arsenite treatment. Carcinogenesis 2002, 23:867-876.
65. Yu H.J., Tsai T.C., Hsieh T.S., Chiu T.Y. Characterization of a newly established human bladder carcinoma cell line, NTUB1. J. Formos. Med. Assoc. 1992, 91:608-613.
66. Zhang T.C., Cao E.H., Li J.F., Ma W., Qin J.F. Induction of apoptosis and inhibition of human gastric cancer MGC-803 cell growth by arsenic trioxide. Eur. J. Cancer 1999, 35:1258-1263.
67. Zhu J., Koken M.H., Quignon F., Chelbi-Alix M.K., Degos L., Wang Z.Y., Chen Z., de The H. Arsenic-induced PML targeting onto nuclear bodies: implications for the treatment of acute promyelocytic leukemia. Proc. Natl Acad. Sci. USA 1997, 94:3978-3983.