DNA damage induced by caffeic acid phenyl ester in the presence of Cu(II) ions: Potential mechanism of its anticancer properties

Cancer Letters

Volumn 263, Issue 1, 2008, Pages 77-88

  Wang, Ting ^a   Chen, Li Xiang ^a   Long, Yuan ^b   Wu, Wei Min ^a,b   Wang, Rui ^a,b  

^a HONG KONG POLYTECHNIC UNIVERSITY   (Hong Kong)

^b LANZHOU UNIVERSITY   (China)

Author keywords

Antioxidant; Caffeic acid phenyl ester; Copper; DNA cleavage; Prooxidant

Indexed keywords

CAFFEIC ACID PHENETHYL ESTER; COPPER ION; DNA;

ANTINEOPLASTIC ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; BINDING KINETICS; COMPLEX FORMATION; DNA DAMAGE; DNA STRAND BREAKAGE; DNA SUPERCOILING; DRUG MECHANISM; GENOTOXICITY; HUMAN; MOLECULAR STABILITY; OXIDATION KINETICS; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; STRUCTURE ACTIVITY RELATION; ULTRAVIOLET SPECTROSCOPY;

ANIMALS; ANTINEOPLASTIC AGENTS; CAFFEIC ACIDS; CATALASE; CATTLE; COPPER; DNA; DNA DAMAGE; EDETIC ACID; ELECTROPHORESIS, AGAR GEL; FREE RADICAL SCAVENGERS; REACTIVE OXYGEN SPECIES; SPECTROMETRY, FLUORESCENCE; SPECTROPHOTOMETRY, ULTRAVIOLET;

EID: 41149165207     PISSN: 03043835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.canlet.2007.12.021     Document Type: Article

References (57)

1. van Acker S.A., van den Berg D.J., Tromp M.N., Griffioen D.H., van Bennekom W.P., van der Vijgh W.J., and Bast A. Structural aspects of antioxidant activity of flavonoids. Free Radic. Biol. Med. 20 (1996) 331-342
2. Rice-Evans C.A., Miller N.J., and Paganga G. Structure-antioxidant activity relationships of flavonoids and phenolic acids. Free Radic. Biol. Med. 20 (1996) 933-956
3. Korkina L.G., and Afanas'ev I.B. Antioxidant and chelating properties of flavonoids. Adv. Pharmacol. 38 (1997) 151-163
4. Cao G., Sofic E., and Prior R.L. Antioxidant and prooxidant behavior of flavonoids: structure-activity relationships. Free Radic. Biol. Med. 22 (1997) 749-760
5. Middleton E.J., Kandaswami C., and immunity T.i.o.p.f.o.m.b.: i.f. inflammation and cancer. In: Harborne J.B. (Ed). The Flavonoids: Advances in Research Since 1986 (1993), Chapman and Hall, London 619-652
6. Ahsan H., Parveen N., Khan N.U., and Hadi S.M. Pro-oxidant, anti-oxidant and cleavage activities on DNA of curcumin and its derivatives demethoxycurcumin and bisdemethoxycurcumin. Chem. Biol. Interact 121 (1999) 161-175
7. Oikawa S., Hirosawa I., Hirakawa K., and Kawanishi S. Site specificity and mechanism of oxidative DNA damage induced by carcinogenic catechol. Carcinogenesis 22 (2001) 1239-1245
8. Nagao M., Morita N., Yahagi T., Shimizu M., Kuroyanagi M., Fukuoka M., Yoshihira K., Natori S., Fujino T., and Sugimura T. Mutagenicities of 61 flavonoids and 11 related compounds. Environ. Mutagen. 3 (1981) 401-419
9. Elliger C.A., Henika P.R., and MacGregor J.T. Mutagenicity of flavones, chromones and acetophenones in Salmonella typhimurium. New structure-activity relationships. Mutat. Res. 135 (1984) 77-86
10. Zhu B.T., and Liehr J.G. Quercetin increases the severity of estradiol-induced tumorigenesis in hamster kidney. Toxicol. Appl. Pharmacol. 125 (1994) 149-158
11. Pereira M.A., Grubbs C.J., Barnes L.H., Li H., Olson G.R., Eto I., Juliana M., Whitaker L.M., Kelloff G.J., Steele V.E., and Lubet R.A. Effects of the phytochemicals, curcumin and quercetin, upon azoxymethane-induced colon cancer and 7,12-dimethylbenz[a]anthracene-induced mammary cancer in rats. Carcinogenesis 17 (1996) 1305-1311
12. Hadi S.M., Asad S.F., Singh S., and Ahmad A. Putative mechanism for anticancer and apoptosis-inducing properties of plant-derived polyphenolic compounds. IUBMB Life 50 (2000) 167-171
13. Kaufmann S.H. Induction of endonucleolytic DNA cleavage in human acute myelogenous leukemia cells by etoposide, camptothecin, and other cytotoxic anticancer drugs: a cautionary note. Cancer Res. 49 (1989) 5870-5878
14. Rahman A., Shahabuddin S., Hadi S.M., and Parish J.H. Complexes involving quercetin, DNA and Cu(II). Carcinogenesis 11 (1990) 2001-2003
15. Yamashita N., Murata M., Inoue S., Burkitt M.J., Milne L., and Kawanishi S. Alpha-tocopherol induces oxidative damage to DNA in the presence of copper(II) ions. Chem. Res. Toxicol. 11 (1998) 855-862
16. 2. J. Biol. Chem. 266 (1991) 20175-20184
17. Li Y., and Trush M.A. Reactive oxygen-dependent DNA damage resulting from the oxidation of phenolic compounds by a copper-redox cycle mechanism. Cancer Res. 54 (1994) s1895-s1898
18. Parlakpinar H., Sahna E., Acet A., Mizrak B., and Polat A. Protective effect of caffeic acid phenethyl ester (CAPE) on myocardial ischemia-reperfusion-induced apoptotic cell death. Toxicology 209 (2005) 1-14
19. Grunberger D., Banerjee R., Eisinger K., Oltz E.M., Efros L., Caldwell M., Estevez V., and Nakanishi K. Preferential cytotoxicity on tumor cells by caffeic acid phenethyl ester isolated from propolis. Experientia 44 (1988) 230-232
20. Lee Y.J., Liao P.H., Chen W.K., and Yang C.Y. Preferential cytotoxicity of caffeic acid phenethyl ester analogues on oral cancer cells. Cancer Lett. 153 (2000) 51-56
21. Chen Y.J., Shiao M.S., Hsu M.L., Tsai T.H., and Wang S.Y. Effect of caffeic acid phenethyl ester, an antioxidant from propolis, on inducing apoptosis in human leukemic HL-60 cells. J. Agric. Food Chem. 49 (2001) 5615-5619
22. Watabe M., Hishikawa K., Takayanagi A., Shimizu N., and Nakaki T. Caffeic acid phenethyl ester induces apoptosis by inhibition of NFkappaB and activation of Fas in human breast cancer MCF-7 cells. J. Biol. Chem. 279 (2004) 6017-6026
23. Michaluart P., Masferrer J.L., Carothers A.M., Subbaramaiah K., Zweifel B.S., Koboldt C., Mestre J.R., Grunberger D., Sacks P.G., Tanabe T., and Dannenberg A.J. Inhibitory effects of caffeic acid phenethyl ester on the activity and expression of cyclooxygenase-2 in human oral epithelial cells and in a rat model of inflammation. Cancer Res. 59 (1999) 2347-2352
24. Orban Z., Mitsiades N., Burke Jr. T.R., Tsokos M., and Chrousos G.P. Caffeic acid phenethyl ester induces leukocyte apoptosis, modulates nuclear factor-kappa B and suppresses acute inflammation. Neuroimmunomodulation 7 (2000) 99-105
25. Natarajan K., Singh S., Burke Jr. T.R., Grunberger D., and Aggarwal B.B. Caffeic acid phenethyl ester is a potent and specific inhibitor of activation of nuclear transcription factor NF-kappa B. Proc. Natl. Acad. Sci. USA 93 (1996) 9090-9095
26. Fitzpatrick L.R., Wang J., and Le T. Caffeic acid phenethyl ester, an inhibitor of nuclear factor-kappaB, attenuates bacterial peptidoglycan polysaccharide-induced colitis in rats. J. Pharmacol. Exp. Ther. 299 (2001) 915-920
27. Kimura Y., Okuda H., Okuda T., Hatano T., Agata I., and Arichi S. Studies on the activities of tannins and related compounds from medicinal plants and drugs. VII. Effects of extracts of leaves of Artemisia species, and caffeic acid and chlorogenic acid on lipid metabolic injury in rats fed peroxidized oil. Chem. Pharm. Bull. (Tokyo) 33 (1985) 2028-2034
28. Chiao C., Carothers A.M., Grunberger D., Solomon G., Preston G.A., and Barrett J.C. Apoptosis and altered redox state induced by caffeic acid phenethyl ester (CAPE) in transformed rat fibroblast cells. Cancer Res. 55 (1995) 3576-3583
29. Guarini L., Su Z.Z., Zucker S., Lin J., Grunberger D., and Fisher P.B. Growth inhibition and modulation of antigenic phenotype in human melanoma and glioblastoma multiforme cells by caffeic acid phenethyl ester (CAPE). Cell Mol. Biol. 38 (1992) 513-527
30. Burke Jr. T.R., Fesen M.R., Mazumder A., Wang J., Carothers A.M., Grunberger D., Driscoll J., Kohn K., and Pommier Y. Hydroxylated aromatic inhibitors of HIV-1 integrase. J. Med. Chem. 38 (1995) 4171-4178
31. Jung Y., and Surh Y. Oxidative DNA damage and cytotoxicity induced by copper-stimulated redox cycling of salsolinol, a neurotoxic tetrahydroisoquinoline alkaloid. Free Radic. Biol. Med. 30 (2001) 1407-1417
32. Richmond R., Halliwell B., Chauhan J., and Darbre A. Superoxide-dependent formation of hydroxyl radicals: detection of hydroxyl radicals by the hydroxylation of aromatic compounds. Anal. Biochem. 118 (1981) 328-335
33. Itoh S., Taniguchi M., Takada N., Nagatomo S., Kitagawa T., and Fukuzumi S. Effects of metal ions on the electronic, redox, and catalytic properties of cofactor TTQ of quinoprotein amine dehydrogenases. J. Am. Chem. Soc. 122 (2000) 12087-12097
34. Barcelo F., Barcelo I., Gavilanes F., Ferragut J.A., Yanovich S., and Gonzalez-Ros J.M. Interaction of anthracyclines with nucleotides and related compounds studied by spectroscopy. Biochim. Biophys. Acta 884 (1986) 172-181
35. Fukuhara K., Nagakawa M., Nakanishi I., Ohkubo K., Imai K., Urano S., Fukuzumi S., Ozawa T., Ikota N., Mochizuki M., Miyata N., and Okuda H. Structural basis for DNA-cleaving activity of resveratrol in the presence of Cu(II). Bioorg. Med. Chem. 14 (2006) 1437-1443
36. Toda S., Miyase T., Arichi H., Tanizawa H., and Takino Y. Natural antioxidants. III. Antioxidative components isolated from rhizome of Curcuma longa L. Chem. Pharm. Bull. (Tokyo) 33 (1985) 1725-1728
37. Sharma O.P. Antioxidant activity of curcumin and related compounds. Biochem. Pharmacol. 25 (1976) 1811-1812
38. Sestili P., Diamantini G., Bedini A., Cerioni L., Tommasini I., Tarzia G., and Cantoni O. Plant-derived phenolic compounds prevent the DNA single-strand breakage and cytotoxicity induced by tert-butylhydroperoxide via an iron-chelating mechanism. Biochem. J. 364 (2002) 121-128
39. Huang M.T., Ma W., Yen P., Xie J.G., Han J., Frenkel K., Grunberger D., and Conney A.H. Inhibitory effects of caffeic acid phenethyl ester (CAPE) on 12-O-tetradecanoylphorbol-13-acetate-induced tumor promotion in mouse skin and the synthesis of DNA, RNA and protein in HeLa cells. Carcinogenesis 17 (1996) 761-765
40. Huang M.T., Lysz T., Ferraro T., Abidi T.F., Laskin J.D., and Conney A.H. Inhibitory effects of curcumin on in vitro lipoxygenase and cyclooxygenase activities in mouse epidermis. Cancer Res. 51 (1991) 813-819
41. Speit G., Hochsattel R., and Vogel W. The contribution of DNA single-strand breaks to the formation of chromosome aberrations and SCEs. Basic Life Sci. 29 Pt A (1984) 229-244
42. Foti M., and Ruberto G. Kinetic solvent effects on phenolic antioxidants determined by spectrophotometric measurements. J. Agric. Food Chem. 49 (2001) 342-348
43. Wright J.S., Johnson E.R., and DiLabio G.A. Predicting the activity of phenolic antioxidants: theoretical method, analysis of substituent effects, and application to major families of antioxidants. J. Am. Chem. Soc. 123 (2001) 1173-1183
44. Halliwell B., and Gutteridge J.M.C. Free radicals, ageing and disease. In: Halliwell B., and Gutteridge J.M.C. (Eds). Free Radicals in Biology and Medicine (1989), Clarendon Press, Oxford 448-487
45. Linder M.C. Nutrition and metabolism of the trace elements. In: Linder M.C. (Ed). Nutritional Biochemistry and Metabolism with Clinical Applications (1991), Elsevier, New York 215-276
46. Dijkwel P.A., and Wenink P.W. Structural integrity of the nuclear matrix: differential effects of thiol agents and metal chelators. J. Cell Sci. 84 (1986) 53-67
47. Oikawa S., and Kawanishi S. Distinct mechanisms of site-specific DNA damage induced by endogenous reductants in the presence of iron(III) and copper(II). Biochim. Biophys. Acta 1399 (1998) 19-30
48. Oikawa S., and Kawanishi S. Site-specific DNA damage induced by NADH in the presence of copper(II): role of active oxygen species. Biochemistry 35 (1996) 4584-4590
49. Badwey J.A., and Karnovsky M.L. Active oxygen species and the functions of phagocytic leukocytes. Annu. Rev. Biochem. 49 (1980) 695-726
50. Ahsan H., and Hadi S.M. Strand scission in DNA induced by curcumin in the presence of Cu(II). Cancer Lett. 124 (1998) 23-30
51. Kawanishi S., Hiraku Y., and Oikawa S. Mechanism of guanine-specific DNA damage by oxidative stress and its role in carcinogenesis and aging. Mutat. Res. 488 (2001) 65-76
52. Dizdaroglu M., Rao G., Halliwell B., and Gajewski E. Damage to the DNA bases in mammalian chromatin by hydrogen peroxide in the presence of ferric and cupric ions. Arch. Biochem. Biophys. 285 (1991) 317-324
53. Yoshie Y., and Ohshima H. Synergistic induction of DNA strand breakage by catechol-estrogen and nitric oxide: implications for hormonal carcinogenesis. Free Radic Biol. Med. 24 (1998) 341-348
54. Yamashita N., Tanemura H., and Kawanishi S. Mechanism of oxidative DNA damage induced by quercetin in the presence of Cu(II). Mutat. Res. 425 (1999) 107-115
55. Hiraku Y., Yamashita N., Nishiguchi M., and Kawanishi S. Catechol estrogens induce oxidative DNA damage and estradiol enhances cell proliferation. Int. J. Cancer 92 (2001) 333-337
56. Gali H.U., Perchellet E.M., Klish D.S., Johnson J.M., and Perchellet J.P. Hydrolyzable tannins: potent inhibitors of hydroperoxide production and tumor promotion in mouse skin treated with 12-O-tetradecanoylphorbol-13-acetate in vivo. Int. J. Cancer 51 (1992) 425-432
57. Piwocka K., Zablocki K., Wieckowski M.R., Skierski J., Feiga I., Szopa J., Drela N., Wojtczak L., and Sikora E. A novel apoptosis-like pathway, independent of mitochondria and caspases, induced by curcumin in human lymphoblastoid T (Jurkat) cells. Exp. Cell Res. 249 (1999) 299-307