Bax and bak are required for apoptosis induction by sulforaphane, a cruciferous vegetable-derived cancer chemopreventive agent

Cancer Research

Volumn 65, Issue 5, 2005, Pages 2035-2043

  Choi, Sunga ^a   Singh, Shivendra V ^a  

^a UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOTIC PROTEASE ACTIVATING FACTOR 1; CASPASE 3; CASPASE 9; CYTOCHROME C; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; SULFORAPHANE; X LINKED INHIBITOR OF APOPTOSIS;

ANIMAL CELL; APOPTOSIS; ARTICLE; CANCER CHEMOTHERAPY; CELL DEATH; CELL TRANSFORMATION; CONTROLLED STUDY; CRUCIFERA; CYTOSOL; DOSE RESPONSE; EMBRYO; ENZYME ACTIVATION; ENZYME RELEASE; FIBROBLAST; HUMAN; HUMAN CELL; KNOCKOUT MOUSE; MALE; MITOCHONDRION; MOUSE; NONHUMAN; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FAMILY; REGULATORY MECHANISM; SIMIAN VIRUS 40; WILD TYPE;

ANIMALS; ANTICARCINOGENIC AGENTS; APOPTOSIS; APOPTOTIC PROTEASE-ACTIVATING FACTOR 1; BCL-2 HOMOLOGOUS ANTAGONIST-KILLER PROTEIN; BCL-2-ASSOCIATED X PROTEIN; CARRIER PROTEINS; CASPASE 3; CASPASE 9; CASPASES; CELL PROLIFERATION; CELLS, CULTURED; CHEMOPREVENTION; COMPLEMENT SYSTEM PROTEINS; CYTOCHROMES C; ENZYME ACTIVATION; EPITHELIAL CELLS; FIBROBLASTS; GLYCOPROTEINS; MALE; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; PROSTATE; PROSTATIC NEOPLASMS; PROTEIN CONFORMATION; PROTEIN TRANSPORT; PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; THIOCYANATES;

EID: 16444382033     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-04-3616     Document Type: Article

References (53)

1. Verhoeven DT, Goldbohm RA, van Poppel G, Verhagen H, van den Brandt PA. Epidemiological studies on Brassica vegetables and cancer risk. Cancer Epidemiol Biomarkers Prev 1996;5:733-48.
2. Cohen JH, Kristal AR, Stanford JL. Fruit and vegetable intakes and prostate cancer risk. J Natl Cancer Inst 2000;92:61-8.
3. Zhang SM, Hunter DJ, Rosner BA, et al. Intakes of fruits, vegetables, and related nutrients and the risk of non-Hodgkin's lymphoma among women. Cancer Epidemiol Biomarkers Prev 2000;9:477-85.
4. Ambrosone CB, McCann SE, Freudenheim JL, Marshall JR, Zhang Y, Shields PG. Breast cancer risk in premenopausal women is inversely associated with consumption of broccoli, a source of isothiocyanates, but is not modified by GST genotype. J Nutr 2004;134:1134-8.
5. Hecht SS. Inhibition of carcinogenesis by isothiocyanates. Drug Metab Rev 2000;32:390-411.
6. Talalay P, Fahey JW. Phytochemicals from cruciferous plants protect against cancer by modulating carcinogen metabolism. J Nutr 2001;131:3027-33s.
7. Fahey JW, Zalcmann AT, Talalay P. The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry 2001;56:5-51.
8. Conaway CC, Yang YM, Chung FL. Isothiocyanates as cancer chemopreventive agents: their biological activities and metabolism in rodents and humans. Curr Drug Metab 2002;3:233-55.
9. Wattenberg LW. Inhibition of carcinogenic effects of polycyclic hydrocarbons by benzyl isothiocyanate and related compounds. J Natl Cancer Inst 1977;58:395-8.
10. Stoner GD, Morrissey DT, Heur YH, Daniel EM, Galati AJ, Wagner SA. Inhibitory effects of phenethyl isothiocyanate on N-nitrosobenzylmethylamine carcinogenesis in the rat esophagus. Cancer Res 1991;51:2063-8.
11. Morse MA, Wang CX, Stoner GD, et al. Inhibition of 4-(methylnitrosamino)- 1-(3-pyridyl)-1-butanone-induced DNA adduct formation and tumorigenicity in the lung of F344 rats by dietary phenethyl isothiocyanate. Cancer Res 1989;49:549-53.
12. Jiao D, Smith TJ, Yang CS, et al. Chemopreventive activity of thiol conjugates of isothiocyanates for lung tumorigenesis. Carcinogenesis 1997;18:2143-7.
13. Yang YM, Conaway CC, Chiao JW, et al. Inhibition of benzo(a)pyrene- induced lung tumorigenesis in A/J mice by dietary N-acetylcysteine conjugates of benzyl and phenethyl isothiocyanates during the postinitiation phase is associated with activation of mitogen-activated protein kinases and p53 activity and induction of apoptosis. Cancer Res 2002;62:2-7.
14. Zhang Y, Talalay P, Cho CG, Posner GH. A major inducer of anticarcinogenic protective enzymes from broccoli: isolation and elucidation of structure. Proc Natl Acad Sci U S A 1992;89:2399-403.
15. Zhang Y, Kensler TW, Cho CG, Posner GH, Talalay P. Anticarcinogenic activities of sulforaphane and structurally related synthetic norbornyl isothiocyanates. Proc Natl Acad Sci U S A 1994;91:3147-50.
16. Fahey JW, Zhang Y, Talalay P. Broccoli sprouts: an exceptionally rich source of inducers of enzymes that protect against chemical carcinogens. Proc Natl Acad Sci U S A 1997;94:10367-72.
17. Chung FL, Conaway CC, Rao CV, Reddy BS. Chemoprevention of colonic aberrant crypt foci in Fischer rats by sulforaphane and phenethyl isothiocyanate. Carcinogenesis 2000;21:2287-91.
18. Fahey JW, Haristoy X, Dolan PM, et al. Sulforaphane inhibits extracellular, intracellular, and antibiotic-resistant strains of Helicobacter pylori and prevents benzo[a]pyrene-induced stomach tumors. Proc Natl Acad Sci U S A 2002;99:7610-5.
19. Haristoy X, Angioi-Duprez K, Duprez A. Lozniewski A. Efficacy of sulforaphane in eradicating Helicobacter pylori human gastric xenografts implanted in nude mice. Antimicrob Agents Chemother 2003;47:3982-4.
20. Gamet-Payrastre L, Li P, Lumeau S, et al. Sulforaphane, a naturally occurring isothiocyanate, induces cell cycle arrest and apoptosis in HT29 human colon cancer cells. Cancer Res 2000;60:1426-33.
21. Fimognari C, Nüsse M, Cesari R, Iori R, Cantelli-Forti G, Hrelia P. Growth inhibition, cell-cycle arrest and apoptosis in human T-cell leukemia by the isothiocyanate sulforaphane. Carcinogenesis 2002;23:581-6.
22. Misiewicz I, Skupinska K, Kasprzycka-Guttman T. Sulforaphane and 2-oxohexyl isothiocyanate induce cell growth arrest and apoptosis in L-1210 leukemia and ME-18 melanoma cells. Oncol Rep 2003;10:2045-50.
23. Gingras D, Gendron M, Boivin D, Moghrabi A, Theoret Y, Beliveau R. Induction of medulloblastoma cell apoptosis by sulforaphane, a dietary anticarcinogen from Brassica vegetables. Cancer Lett 2004;203:35-43.
24. Wang L, Liu D, Ahmed T, Chung FL, Conaway CC, Chiao JW. Targeting cell cycle machinery as a molecular mechanism of sulforaphane in prostate cancer prevention. Int J Oncol 2004;24:187-92.
25. Jackson SJT, Singletary KW. Sulforaphane: a naturally occurring mammary carcinoma mitotic inhibitor, which disrupts tubulin polymerization. Carcinogenesis 2004;25:219-27.
26. Myzak MC, Karplus PA, Chung FL, Dashwood RH. A novel mechanism of chemoprotection by sulforaphane: inhibition of histone deacetylase. Cancer Res 2004;64:5767-74.
27. Parnaud G, Li P, Cassar G, et al. Mechanism of sulforaphane-induced cell cycle arrest and apoptosis in human colon cancer cells. Nutr Cancer 2004;48:198-206.
28. Singh AV, Xiao D, Lew KL, Dhir R, Singh SV. Sulforaphane induces caspase-mediated apoptosis in cultured PC-3 human prostate cancer cells and retards growth of PC-3 xenografts in vivo. Carcinogenesis 2004;25:83-90.
29. 2-M phase cell cycle arrest involves checkpoint kinase 2 mediated phosphorylation of Cdc25C. J Biol Chem 2004;279:25813-22.
30. Hartwell LH, Kastan MB. Cell cycle control and cancer. Science 1994;266:1821-8.
31. Wei MC, Zong WX, Cheng EH, et al. Proapoptotic Bax and Bak: a requisite gateway to mitochondrial dysfunction and death. Science 2001;292:727-30.
32. Xiao D, Choi S, Johnson DE, et al. Diallyl trisulfide-induced apoptosis in human prostate cancer cells involves c-Jun N-terminal kinase and extracellular-signal regulated kinase-mediated phosphorylation of Bcl-2. Oncogene 2004;23:5594-606.
33. Green DR, Reed JC. Mitochondria and apoptosis. Science 1998;281:1309-12.
34. Hengartner MO. The biochemistry of apoptosis. Nature 2000;407:770-6.
35. Liu X, Kim C, Yang J, Jemmerson R, Wang X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 1996;86:147-57.
36. Susin SA, Lorenzo HK, Zamzami N, et al. Molecular characterization of mitochondrial apoptosis-inducing factors. Nature 1999;397:441-6.
37. Du C, Fang M, Li Y, Li L, Wang X. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 2000;102:33-42.
38. Thornberry N, Lazebnick Y. Caspases: enemies within. Science 1998;281:1312-6.
39. Wolf BB, Green DR. Suicidal tendencies: apoptotic cell death by caspase family proteinases. J Biol Chem 1999;274:20049-52.
40. Verhagen AM, Ekert PG, Pakusch M, et al. Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell 2000;102:43-53.
41. Salvesen GS, Duckett CS. IAP proteins: blocking the road to death's door. Nat Rev Mol Cell Biol 2002;3:401-10.
42. Wolter KG, Hsu YT, Smith CL, Nechushtan A, Xi XG, Youle RJ. Movement of Bax from the cytosol to mitochondria during apoptosis. J Cell Biol 1997;139:1281-92.
43. Yamaguchi H, Wang HG. The protein kinase PKB/Akt regulates cell survival and apoptosis by inhibiting Bax conformational change. Oncogene 2001;20:7779-86.
44. Hockenbery D, Nunez G, Milliman C, Schreiber RD, Korsmeyer SJ. Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature 1990;348:334-6.
45. Reed JC. Bcl-2 family proteins: regulators of apoptosis and chemoresistance in hematologic malignancies. Semin Hematol 1997;34:9-19.
46. Chao DT, Korsmeyer SJ. Bcl-2 family: regulators of cell death. Annu Rev Immunol 1998;16:395-419.
47. Adams JM, Cory S. The Bcl-2 protein family: arbiters of cell survival. Science 1998;281:1322-6.
48. Martinou JC, Green DR. Breaking the mitochondrial barrier. Nat Rev Mol Cell Biol 2001;2:63-7.
49. Kandasamy K, Srinivasula SM, Alnemri ES, et al. Involvement of proapoptotic molecules Bax and Bak in tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-induced mitochondrial disruption and apoptosis: differential regulation of cytochrome c and Smac/DIABLO release. Cancer Res 2003;63:1712-21.
50. Yamaguchi H, Chen J, Bhalla K, Wang HG. Regulation of Bax activation and apoptotic response to microtubule-damaging agents by p53 transcription-dependent and -independent pathways. J Biol Chem 2004;279:39431-7.
51. Hu R, Hebbar V, Kim BR, et al. In vivo pharmacokinetics and regulation of gene expression profiles for isothiocyanate sulforaphane in the rat. J Pharmacol Exp Ther 2004;310:263-71.
52. Liebes L, Conaway CC, Hochster H, et al. High-performance liquid chromatography-based determination of total isothiocyanate levels in human plasma: application to studies with 2-phenethyl isothiocyanate. Anal Biochem 2001;291:279-89.
53. Ji Y, Morris ME. Determination of phenethyl isothiocyanate in human plasma and urine by ammonia derivatization and liquid chromatography-tandem mass spectrometry. Anal Biochem 2003;323:39-47.