β-phenylethyl isothiocyanate-mediated apoptosis in hepatoma HepG2 cells

Cellular and Molecular Life Sciences

Volumn 60, Issue 7, 2003, Pages 1489-1503

  Rose, P ^a   Whiteman, M ^a   Huang, S H ^a   Halliwell, B ^a   Ong, C N ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

phenylethyl isothiocyanate; Apoptosis; Cell cycle arrest; Oxidative stress

Indexed keywords

ASCORBIC ACID; CASPASE 3; CYCLIN B1; FREE RADICAL; MANNITOL; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PHENETHYL ISOTHIOCYANATE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; TROLOX C; URIC ACID;

APOPTOSIS; ARTICLE; CELL CYCLE G2 PHASE; CONCENTRATION RESPONSE; DETOXIFICATION; DNA SYNTHESIS; ENZYME ACTIVITY; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; HYDROLYSIS; LIVER CELL CARCINOMA; NICK END LABELING; OXIDATIVE STRESS; STEM CELL;

ANTICARCINOGENIC AGENTS; APOPTOSIS; BROMODEOXYURIDINE; CARCINOMA, HEPATOCELLULAR; CELL CYCLE; CELL SURVIVAL; DNA REPLICATION; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; IN SITU NICK-END LABELING; ISOTHIOCYANATES; KINETICS; LIVER NEOPLASMS; METABOLIC DETOXICATION, DRUG; SUPEROXIDES; TUMOR CELLS, CULTURED;

LETHRINIDAE;

EID: 0042368855     PISSN: 1420682X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00018-003-3150-4     Document Type: Article

References (59)

1. Block G., Patterson B. and Subar A. (1992) Fruit, vegetables and cancer prevention: a review of the epidemiological evidence. Nutr. Cancer 1: 1-29
2. Verhoeven D. T., Verhagen H., Goldbohm R. A. and Van Poppel G. (1997) A review of the mechanisms underlying anticarcino-genicity by brassica vegetables. Chem. Biol. Interact. 103: 79-129
3. Rask L., Andreasson E., Ekbom B., Eriksson S., Pontoppidan B. and Meijer J. (2000) Myrosinase: gene family evolution and herbivore defence in Brassicaceae. Plant. Mol. Biol. 42: 93-113
4. Fahey J. W., Zalcmann A. T. and Talalay P. (2001) The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry 56: 5-51
5. Zhang Y. and Talalay P. (1994) Anticarcinogenic activities of organic isothiocyanates: chemistry and mechanisms. Cancer Res. 54: 1976s-1981s.
6. Zhang Y. and Talalay P. (1998) Mechansim of differential potencies of isothiocyanates as inducers of anticarcinogenic phase 2 enzymes. Cancer Res. 58: 4632-4639
7. Rose P., Faulkner K., Williamson G. and Mithen R. (2000) 7-Methylsulphinylheptyl and 8-methylsulphinyloctyl isothiocyanates from watercress are potent inducers of phase II enzymes. Carcinogenesis 21: 1983-1988
8. Hecht S. S., Carmella S. G. and Murphy S. E. (1999) Effects of watercress on urinary metabolites of nicotine in smokers. Cancer Epidemiol. Biomarkers Prev. 8: 907-913
9. London S. J., Yuan J. M., Chung F. L., Gao Y. T., Coetzee G. A., Ross R. K. et al. (2000) Isothiocyanates, glutathione-S-transferase M1 and T1 polymorphisms, and lung cancer risk: a prospective study of men in Shanghai, China. Lancet 356: 724-729
10. Zhao B., Seow A., Lee E. J., Poh W. T., The M., Eng P. et al. (2001) Dietary isothiocyanates, glutathione-S-transferase-M1, -T1 polymorphisms and lung cancer risk among Chinese women in Singapore. Cancer Epidemiol. Biomarkers Prev. 10: 1063-1067
11. Lin H. J., Probst-Hensch N. M., Louie A. D., Kau I. H., Witte J. S., Ingles S. et al. (1998) Glutathione transferase null genotype, broccoli, and lower prevalence of colorectal cancer. Cancer Epidemiol. Biomarkers Prev. 8: 647-652
12. Gamet-Payrastre L., Li P., Lumeau S., Cassar G., Dupont M. A., Chevolleau S. et al. (2000) Sulforaphane, a naturally occurring isothiocyanate, induces cell cycle arrest and apoptosis in HT29 human colon cancer cells. Cancer Res. 60: 1426-1433
13. Chiao J. W., Chung F. L, Kancherla R., Ahmed T., Mittelman A. and Conaway C. C. (2002) Sulforaphane and its metabolite mediate growth arrest and apoptosis in human prostate cancer cells. Int. J. Oncol. 20: 631-636
14. Chen Y.-R., Wang W., Kong A. N. and Tan T-H. (1998). Molecular mechanisms of c-jun N-terminal kinase-mediated apoptosis induced by anticarcinogenic isothiocyanates. J. Biol. Chem. 273: 1769-1775
15. Haung C., Ma W. Y., Li J., Hecht S. S. and Dong Z. (1998) Essential role of p53 in phenylethyl isothiocyanate induced apoptosis. Cancer Res. 58: 4102-4106
16. Xiao D. and Singh S. V. (2002) Phenylethyl isothiocyanate induced apoptosis in p53 deficient PC 3 human prostate cancer cell line is mediated by extracellular signal regulated kinase. Cancer Res. 62: 3615-3619
17. Xu K. and Thornalley P. J. (2000) Studies on the mechanism of the inhibition of human leukemia cell growth by dietary isothiocyanates and their cysteine adducts in vitro. Biochem. Pharmacol. 60: 221-231
18. Xu K. and Thornalley P. J. (2001) Signal transduction activated by cancer chemopreventive isothiocyanates: cleavage of BID protein, tyrosine phosphorylation and activation of JNK Br. J. Cancer. 84: 670-673
19. Yang Y. M., Conaway C. C., Chiao J. W., Wang C. X., Amin S., Whysner J. et al. (2002) Inhibition of benzo[a]pyrene induced lung tumorigenesis in A/J mice by dietary N-acetylcysteine conjugates of benzyl and phenylethyl isothiocyanates during the postinitiation phase is associated with the activation of mitogen activated protein kinases and p53 activity and induction of apoptosis. Cancer Res. 62: 2-7
20. Kulms D., Zeise E., Poppelmann B. and Schwarz T. (2002) DNA damage, death receptor activation and reactive oxygen species contribute to ultraviolet radiation-induced apoptosis in an essential and independent way. Oncogene. 21: 5844-5851
21. Moreno-Manzano V., Ishikawa Y., Lucio-Cazana J. and Kitamura M. (2000) Selective involvement of superoxide anion, but not downstream compounds hydrogen peroxide and peroxynitrite in tumor necrosis factor alpha induced apoptosis in rat mesangial cells. J. Biol. Chem. 275: 12684-12691
22. Groninger E., Meeuwsen-De Boer G. J., De Graaf S. S., Kamps W. A. and DeBont E. S. (2002) Vincristine induced apoptosis in acute lymphoblastic leukaemia cells: a mitochondrial controlled pathway regulated by reactive oxygen species? Int. J. Oncol. 21: 1339-1345
23. Luo J., Sun Y., Lin H., Qian Y., Li Z., Leonard S. S. et al. (2003) Activation of c-jun NH2-terminal kinase (JNK) by vanadate induces FADD-dependant death of cerebellar granule progenitors in vitro. J. Biol. Chem. 278: 4542-4551
24. Nakamura Y., Kawakami M., Yoshihiro A., Miyoshi N., Ohigashi H., Kawai K. et al. (2002) Involvement of the mitochondrial death pathway in chemopreventive benzyl isothiocyanate induced apoptosis. J. Biol. Chem. 277: 8492-8499
25. Nicoletti I., Migliorati G., Pagliacci M. C., Grignani F. and Riccardi C. (1991) A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J. Immunol. Methods 139: 271-279
26. Shen H. M., Yang C. F. and Ong C. N. (1999) Sodium selenite induced oxidative stress and apoptosis in human HepG2 cells. Int. J. Cancer. 81: 820-828
27. Hansen M. B., Nielsen S. E. and Berg K. (1989) Re-examination and further development of a precise and rapid dye method for measuring cell growth/cell kill. J. Immunol. Methods. 119: 203-210
28. LeBel C. P., Ischiopoulos H. and Bondy S. C. (1992) Evaluation of the probe 2′,7′-dichlorofluorescin as indicator of reactive oxygen species formation and oxidative stress. Chem. Res. Toxicol. 5: 227-231
29. Roche G. and Valet G. (1990) Flow cytometry analysis of respiratory burst activity in phagocytes with hydroethidine and 2′7′ dichlorofluorescein. J. Leukoc. Biol. 47: 440-448
30. Jenner A., England T. G., Aruoma O. I. and Halliwell B. (1998) Measurement of oxidative DNA damage by gas chromatography-mass spectrometry: ethanethiol prevents artifactual generation of oxidized DNA bases. Biochem. J. 331: 365-369
31. England T. G., Jenner A., Aruoma O. I. and Halliwell B. (1998) Detection of oxidative DNA base damage by gas chromatography-mass spectrometry: effects of derivatization conditions on artifactual formation of certain base oxidation products. Free. Radic. Res. 29: 321-330
32. Whiteman M., Hong S. H., Jenner A. and Halliwell B. (2002) Loss of oxidized and chlorinated bases in DNA treated with reactive oxygen species: implications for assessment of oxidative damage in vivo. Biochem Biophys. Res. Commun. 296: 883-889
33. King R. W. and Jackson P. K. (1994) Mitosis in transition. Cell 79: 563-571
34. Halliwell B. and Gutteridge J. M. C. (1999) Free Radicals in Biology and Medicine, 3rd edn, Clarendon, Oxford
35. Spencer J. P., Jenner A., Chimel K., Aruoma O. I., Cross C. E., Wu R. et al. (1996) DNA strand breakage and base modification induced by hydrogen peroxide of human respiratory tract epithelial cells. FEBS. Lett. 374: 233-236
36. Wu D. and Cederbaum A. I. (2002) Cyclosporin A protects against arachidonic acid toxicity in rat hepatocytes: role of CYP2E1 and mitochondria. Hepatology 35: 1420-1430
37. Jones D. C., Gunasekar P. G., Borowitz J. L. and Isom G. E. (2000) Dopamine induced apoptosis is mediated by oxidative stress and is enhanced by cyanide in differentiated PC12 cells. J. Neurochem. 74: 2296-2304
38. Huang R. F., Huang S. M., Lin B. S., Hung C. Y. and Lu H. T. (2002) N-acetylcysteine, vitamin C and vitamin E diminish homocysteine thiolactone induced apoptosis in human promyeloid HL-60 cells. J. Nutr. 132: 2151-2156
39. Patel M. (1998) Inhibition of neural apoptosis by a metalloporphyrin superoxide dismutase mimic. J. Neurochem. 71: 1068-1074
40. Choi I. Y., Lee S. J., Ju C., Nam W., Kim H. C., Ko K. H. et al. (2000) Protection by a manganese porphyrin of endogeneous peroxynitrite induced death in glial cells via inhibition of mitochondrial transmembrane potential decrease. Glia. 31: 155-164
41. Szabo C., Day B. J. and Salzman A. L. (1996) Evaluation of the relative contribution of nitric oxide and peroxynitrite to the suppression of mitochondrial respiration in immunohistostimulated macrophages using a manganese mesoporphyrin superoxide dismutase mimetic and peroxynitrite scavenger. FEBS. Lett. 381: 82-86
42. Perez M. J. and Cederbaum A. I. (2002) Antioxidant and pro-oxidant effects of a manganese porphyrin complex against CYP2E1 toxicity. Free. Radic. Biol. Med. 33: 111-127
43. Chung F. L., Kelloff G., Steele V., Pittman B., Zang E., Jiao D. et al. (1996) Chemopreventive efficacy of aryalkyl isothiocyanates and N-acetylcysteine for lung tumorigenesis in Fischer rats. Cancer Res. 56: 772-778
44. Chung F. L., Conaway C. C., Rao C. V. and Reddy B. S. (2000) Chemoprevention of colonic aberrant crypt loci in Fischer rats by sulforaphane and phenylethyl isothiocyanate. Carcinogenesis 21: 2287-2291
45. Conaway C. C., Jiao D. and Chung F. L. (1996) Inhibition of rat liver cytochrome P450 isoenzymes by isothiocyanates and their conjugates: a structure activity relationship study. Carcinogenesis 17: 2423-2427
46. Higuchi Y. and Yoshimoto T. (2002) Arachidonic acid converts the glutahtione depletion induced apoptosis to necrosis by promoting lipid peroxidation and reducing caspase 3 activity in rat glioma cells. Arch. Biochem. Biophys. 400: 133-140
47. Lopez-Marure R., Gutierrez G., Mendoza C., Ventura J. L., Sanchez L., Reyes Maldonado E. et al. (2002) Ceramide promotes the death of human cervical tumor cells in the absence of biochemical and morphological markers. Biochem. Biophys. Res. Commun. 293: 1028-1036
48. Grasl-Kraupp B., Ruttkay-Nedecky B., Koudelka H., Bukowska K., Bursch W. and Schulte-Hermann R. (1995) In situ detection of fragmented DNA (TUNEL assay) fails to discriminate among apoptosis, necrosis and autolytic cell death: a cautionary note. Hepatology 21: 1465-1468
49. Aytac U., Claret F. X., Kazuya S., Ohnuma K., Mills G. B., Cabanillas F. et al. (2001) Expression of CD26 and its associated dipeptidyl peptidase IV enzyme activity enhances sensitivity to doxorubicin induced cell cycle arrest at the G2/M checkpoint. Cancer Res. 61: 7204-7210
50. Tyagi A. K., Singh P. R., Agarwal C., Chan D. C. F. and Agarwal R. (2002) Silibinin strongly synergizes human prostate carcinoma DU145 cells to doxorubicin induced growth inhibition, G2/M arrest and apoptosis. Clin. Cancer Res. 8: 3512-3519
51. Murata M., Yamashita N., Inoue S. and Kawanishi S. (2000) Mechanism of oxidative DNA damage induced by carcinogenic allyl isothiocyanate. Free Radic. Biol. Med. 28: 797-805
52. Kassie F., Pool-Zobel B., Parzefall W. and Knasmuller S. (1999) Genotoxic effects of benzyl isothiocyanate, a natural chemopreventive agent. Mutagenesis 14: 595-604
53. Miko M. and Chance B. (1975) Isothiocyanates: a new class of uncouplers. Biochim. Biophys. Acta 396: 165-174
54. Li N., Ragheb K. E., Lawler G., Sturgis J., Rajwa B., Melendez J. A. and Robinson J. P. (2002) Mitochondrial complex I inhibitor rotenone induces apoptosis through enhancing mitochondrial reactive oxygen species production. J. Biol. Chem. 278: 8516-8525
55. Dussmann M., Kogel D., Rehm M. and Prehn J. H. (2003) Mitochondrial membrane permeabilization and superoxide production during apoptosis: a single-cell analysis. J. Biol. Chem. 278: 12645-12649
56. Chung F.-L., Morse M. A., Eklind K. L. and Lewis J. (1992) Quantitation of human uptake of the anticarcinogen phenylethyl isothiocyanate after a watercress meal. Cancer Epidemiol. Biomarkers Prev. 1: 383-388
57. Zhang Y. (2000) Role of glutathione in the accumulation of anticarcinogenic isothiocyanates and their glutathione conjugates by murine hepatoma cells. Carcinogenesis 21: 1175-1182
58. Gray R. H., Adam-Rodwell G. A., Maris D., Haskins J. R. and Stoner G. D (1995) Quantitative microscopy of hepatic changes induced by β-phenethyl isothiocyanate in Fischer-344 rats fed either a cereal based diet or a purified diet. Toxicol. Pathol. 23: 644-652
59. Long L. H., Clement M. V. and Halliwell B. (2002) Artifacts in cell culture: rapid generation of hydrogen peroxide on addition of (-)epigallocatechin, (-)epigallocatechin gallate, (+)catechin and quercetin to commonly used cell culture media. Biochem. Biophys. Res. Commun. 273: 50-53