Chemopreventive functions of sulforaphane: A potent inducer of antioxidant enzymes and apoptosis

Journal of Functional Foods

Volumn 1, Issue 1, 2009, Pages 23-32

  Yeh, Chi Tai ^a   Yen, Gow Chin ^b  

^a NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^b NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

Author keywords

Apoptosis; Chemopreventive agent; Metallothionein; Signaling pathway; Sulforaphane

Indexed keywords

EID: 67651155826     PISSN: 17564646     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jff.2008.09.002     Document Type: Article

References (100)

1. Adams T.K., Saydam N., Steiner F., Schaffner W., and Freedman J.H. Activation of gene expression by metal-responsive signal transduction pathways. Environmental Health Perspectives 110 (2002) 813-817
2. Adam-Vizi V. Production of reactive oxygen species in brain mitochondria: Contribution by electron transport chain and non-electron transport chain sources. Antioxidants & Redox Signaling 7 (2005) 1140-1149
3. Andrews G.K. Regulation of metallothionein gene expression by oxidative stress and metal ions. Biochemical Pharmacology 59 (2000) 95-104
4. Ashino T., Ozawa S., Numazawa S., and Yoshida T. Tissue-dependent induction of heme oxygenase-1 and metallothionein-1/2 by methyl methanesulfonate. The Journal of Toxicological Sciences 28 (2003) 181-189
5. Bianchini F., and Vainio H. Isothiocyanates in cancer prevention. Drug Metabolism Reviews 36 (2004) 655-667
6. Blagosklonny M.V. Carcinogenesis, cancer therapy and chemoprevention. Cell Death and Differentiation 12 (2005) 592-602
7. Brooks J.D., Paton V.G., and Vidanes G. Potent induction of phase 2 enzymes in human prostate cells by sulforaphane. Cancer Epidemiology, Biomarkers & Prevention 10 (2001) 949-954
8. Cai L., and Cherian M.G. Zinc-metallothionein protects from DNA damage induced by radiation better than glutathione and copper- or cadmium-metallothioneins. Toxicology Letters 136 (2003) 193-198
9. Carrasco J., Penkowa M., Hadberg H., Molinero A., and Hidalgo J. Enhanced seizures and hippocampal neurodegeneration following kainic acid-induced seizures in metallothionein-I + II-deficient mice. The European Journal of Neuroscience 12 (2000) 2311-2322
10. Cho S.D., Li G., Hu H., Jiang C., Kang K.S., Lee Y.S., Kim S.H., and Lu J. Involvement of c-Jun N-terminal kinase in G2/M arrest and caspase-mediated apoptosis induced by sulforaphane in DU145 prostate cancer cells. Nutrition & Cancer 52 (2005) 213-224
11. Chung F.L., Conaway C.C., Rao C.V., and Reddy B.S. Chemoprevention of colonic aberrant crypt foci in Fischer rats by sulforaphane and phenethyl isothiocyanate. Carcinogenesis 21 (2000) 2287-2291
12. Cook J.A., Gius D., Wink D.A., Krishna M.C., Russo A., and Mitchell J.B. Oxidative stress, redox, and the tumor microenvironment. Seminars in Radiation Oncology 14 (2004) 259-266
13. Coyle P., Philcox J.C., Carey L.C., and Rofe A.M. Metallothionein: The multipurpose protein. Cellular and Molecular Life Sciences 59 (2002) 627-647
14. Cuschieri J., and Maier R.V. Mitogen-activated protein kinase (MAPK). Critical Care Medicine 33 (2005) S417-S419
15. Cutler R.G. Oxidative stress and aging: Catalase is a longevity determinant enzyme. Rejuvenation Research 8 (2005) 138-140
16. Dalton T.P., Palmiter R.D., and Andrews G.K. Transcriptional induction of the mouse metallothionein-I gene in hydrogen peroxide treated Hepa cells involve a composite major late transcription factor/antioxidant response element and metal response promoter elements. Nucleic Acids Research 22 (1994) 5016-5023
17. Dick R.A., and Kensler T.W. Chemoprotective potential of phase 2 enzyme inducers. Expert Review of Anticancer Therapy 2 (2002) 581-592
18. Ebadi M., Hiramatsu M., Burke W.J., Folks D.G., and El-Sayed M.A. Metallothionein isoforms provide neuroprotection against 6-hydroxydopamine-generated hydroxyl radicals and superoxide anions. Proceedings of the Western Pharmacology Society 41 (1998) 155-158
19. Fahey J.W., and Talalay P. Antioxidant functions of sulforaphane: A potent inducer of phase II detoxication enzymes. Food and Chemical Toxicology 37 (1999) 973-979
20. Fahey J.W., Haristoy X., Dolan P.M., Kensler T.W., Scholtus I., Stephenson K.K., Talalay P., and Lozniewski A. Sulforaphane inhibits extracellular, intracellular, and antibiotic-resistant strains of Helicobacter pylori and prevents benzo[a]pyrene-induced stomach tumors. Proceedings of the National Academy of Sciences of the United States of America 99 (2002) 7610-7615
21. Fimognari C., Nusse M., Berti F., Iori R., Cantelli-Forti G., and Hrelia P. Sulforaphane modulates cell cycle and apoptosis in transformed and non-transformed human T lymphocytes. Annals of the New York Academy of Sciences 1010 (2002) 393-398
22. Frank G.D., and Eguchi S. Activation of tyrosine kinases by reactive oxygen species in vascular smooth muscle cells: Significance and involvement of EGF receptor transactivation by angiotensin II. Antioxidants & Redox Signaling 5 (2003) 771-780
23. Frydoonfar H.R., McGrath D.R., and Spigelman A.D. Sulforaphane inhibits growth of a colon cancer cell line. Colorectal Disease 6 (2004) 28-31
24. Gills J.J., Jeffery E.H., Matusheski N.V., Moon R.C., Lantvit D.D., and Pezzuto J.M. Sulforaphane prevents mouse skin tumorigenesis during the stage of promotion. Cancer Letters 236 (2006) 72-79
25. Gingras D., Gendron M., Boivin D., Moghrabi A., Theoret Y., and Beliveau R. Induction of medulloblastoma cell apoptosis by sulforaphane, a dietary anticarcinogen from Brassica vegetables. Cancer Letters 203 (2004) 35-43
26. Gross A., McDonnell J.M., and Korsmeyer S.J. Bcl-2 family members and the mitochondria in apoptosis. Genes & Development 13 (1999) 1899-1911
27. Haq F., Mahoney M., and Korpatinck J. Signaling events for metallothionein induction. Mutation Research 533 (2005) 211-226
28. Henderson M.C., Miranda C.L., Stevens J.F., Deinzer M.L., and Buhler D.R. In vitro inhibition of human P450 enzymes by prenylated flavonoids from hops, Humulus lupulus. Xenobiotica 30 (2000) 235-251
29. Hildeman D.A., Mitchell T., Teague T.K., Henson P., Day B.J., Kappler J., and Marrack P.C. Reactive oxygen species regulate activation induced T cell apoptosis. Immunity 10 (1999) 735-744
30. Hintze K.J., Wald K.A., Zeng H., Jeffery E.H., and Finley J.W. Thioredoxin reductase in human hepatoma cells is transcriptionally regulated by sulforaphane and other electrophiles via an antioxidant response element. The Journal of Nutrition 133 (2003) 2721-2727
31. Hong F., Freeman M.L., and Liebler D.C. Identification of sensor cysteines in human keap1 modified by the cancer chemopreventive agent sulforaphane. Chemical Research in Toxicology 18 (2005) 1917-1926
32. Hu R., Hebbar V., Kim B.R., Chen C., Winnik B., Buckley B., Soteropoulos P., Tolias P., Hart R.P., and Kong A.N. In vivo pharmacokinetics and regulation of gene expression profiles by isothiocyanate sulforaphane in the rat. The Journal of Pharmacology and Experimental Therapeutics 310 (2004) 263-271
33. min/+ mice by sulforaphane, a natural product derived from cruciferous vegetable. Carcinogenesis 27 (2006) 2038-2046
34. Jakubikova J., Bao Y., and Sedlak J. Isothiocyanates induce cell cycle arrest, apoptosis and mitochondrial potential depolarization in HL-60 and multidrug-resistant cell lines. Anticancer Research 25 (2005) 3375-3386
35. Jeong H.G., Youn C.K., Cho H.J., Kim S.H., Kim M.H., Kim H.B., Chang I.Y., Lee Y.S., Chung M.H., and You H.J. Metallothionein-III prevented gamma-ray-induced 8-oxoguanine accumulation in normal and hOGG1-depleted cells. The Journal of Biological Chemistry 279 (2004) 34138-34149
36. Jin C.Y., Moon D.O., Lee J.D., Heo M.S., Choi Y.H., Lee C.M., Park Y.M., and Kim G.Y. Sulforaphane sensitizes tumor necrosis factor-related apoptosis-inducing ligand-mediated apoptosis through downregulation of ERK and Akt in lung adenocarcinoma A549 cells. Carcinogenesis 28 (2007) 1058-1066
37. Johnson I.T. Glucosinolates: Bioavailability and importance to health. International Journal for Vitamin and Nutrition Research 72 (2002) 26-31
38. Johnstone R.W., Ruefli A.A., and Lowe S.W. Apoptosis: A link between cancer genetics and chemotherapy. Cell 108 (2002) 153-164
39. Juge N., Mithen R.F., and Traka M. Molecular basis for chemoprevention by sulforaphane: A comprehensive review. Cellular and Molecular Life Sciences 64 (2007) 1105-1127
40. Karmakar S., Weinberg M.S., Banik N.L., Patel S.J., and Ray S.K. Activation of multiple molecular mechanisms for apoptosis in human malignant glioblastoma T98G and U87MG cells treated with sulforaphane. Neuroscience 141 (2006) 1265-1280
41. Kaufmann S.H., and Hengartner M.O. Programmed cell death: Alive and well in the new millennium. Trends in Cell Biology 11 (2001) 526-534
42. Kelly E.J., Sandgren E.P., Brinster R.L., and Palmiter R.D. A pair of adjacent glucocorticoid response elements regulated expression of two mouse metallothionein genes. Proceedings of the National Academy of Sciences of the United States of America 94 (1997) 10045-10050
43. Kensler T.W., Curphey T.J., Maxiutenko Y., and Roebuck B.D. Chemoprotection by organosulfur inducers of phase 2 enzymes: Dithiolethiones and dithiins. Drug Metabolism and Drug Interactions 17 (2000) 3-22
44. Keum Y.S., Jeong W.S., and Kong A.N. Chemopreventive functions of isothiocyanates. Drug News & Perspectives 18 (2005) 445-451
45. Keum Y.S., Owuor E.D., Kim B.R., Hu R., and Kong A.N. Involvement of Nrf2 and JNK1 in the activation of antioxidant responsive element (ARE) by chemopreventive agent phenethyl isothiocyanate (PEITC). Pharmaceutical Research 20 (2003) 1351-1356
46. Kim H., Kim E.H., Eom Y.W., Kim W.H., Kwon T.K., Lee S.J., and Choi K.S. Sulforaphane sensitizes tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-resistant hepatoma cells to TRAIL-induced apoptosis through reactive oxygen species-mediated up-regulation of DR5. Cancer Research 66 (2006) 1740-1750
47. Kong A.N., Owuor E., Yu R., Hebbar V., Chen C., Hu R., and Mandlekar S. Induction of xenobiotic enzymes by the MAP kinase pathway and the antioxidant or electrophile response element (ARE/EpRE). Drug Metabolism Reviews 33 (2001) 255-271
48. Kong A.N., Yu R., Hebbar V., Chen C., Owuor E., Hu R., Ee R., and Mandlekar S. Signal transduction events elicited by cancer prevention compounds. Mutation Research 480-481 (2001) 231-241
49. Krishnan K., Campbell S., Abdel-Rahman F., Whaley S., and Stone W.L. Cancer chemoprevention drug targets. Current Drug Targets 4 (2003) 45-54
50. Lampe J.W., and Peterson S. Brassica, biotransformation and cancer risk: Genetic polymorphisms alter the preventive effects of cruciferous vegetables. The Journal of Nutrition 132 (2002) 2991-2994
51. Lee J.S., and Surh Y.J. Nrf2 as a novel molecular target for chemoprevention. Cancer Letters 224 (2005) 171-184
52. Li J.J., Oberley L.W., Fan M., and Colburn N.H. Inhibition of AP-1 and NF-kappaB by manganese-containing superoxide dismutase in human breast cancer cells. The FASEB Journal 12 (1998) 1713-1723
53. Lichtlen P., and Schaffner W. Putting a finger on stressful situations: The heavy metal-regulatory transcription factor MTF-1. Bioassays 23 (2001) 1010-1017
54. Links M., and Lewis C. Chemoprotectants: A review of their clinical pharmacology and therapeutic efficacy. Drugs 57 (1999) 293-308
55. Masters B.A., Quaife C.J., Erickson J.C., Kelly E.J., Forelick G.J., Zambrowicz B.P., Brinster R.L., and Palmiter R.D. Metallothionein III is expressed in neurons that sequester zinc in synaptic vesicles. The Journal of Neuroscience 14 (1994) 5844-5857
56. McWalter G.K., Higgins L.G., McLellan L.I., Henderson C.J., Song L., Thornalley P.J., Itoh K., Yamamoto M., and Hayes J.D. Transcription factor Nrf2 is essential for induction of NAD(P) H:quinone oxidoreductase 1, glutathione S-transferases, and glutamate cysteine ligase by broccoli seeds and isothiocyanates. The Journal of Nutrition 134 (2004) 3499S-3506S
57. Misiewicz I., Skupinska K., and Kasprzycka-Guttman T. Sulforaphane and 2-oxohexyl isothiocyanate induce cell growth arrest and apoptosis in L-1210 leukemia and ME-18 melanoma cells. Oncology Reports 10 (2003) 2045-2050
58. Montague J.W., and Cidlowski J.A. Cellular catabolism in apoptosis: DNA degradation and endonuclease activation. Experientia 52 (1996) 957-962
59. Motohashi H., Katsuoka F., Engel J.D., and Yamamoto M. Small Maf proteins serve as transcriptional cofactors for keratinocyte differentiation in the Keap1-Nrf2 regulatory pathway. Proceedings of the National Academy of Sciences of the United States of America 27 (2004) 6379-6384
60. Myzak M.C., Karplus P.A., Chung F.L., and Dashwood R.H. A novel mechanism of chemoprotection by sulforaphane: Inhibition of histone deacetylase. Cancer Research 64 (2004) 5767-5774
61. Myzak M.C., Dashwood W.M., Orner G.A., Ho E., and Dashwood R.H. Sulforaphane inhibits histone deacetylase in vivo and suppresses tumorigenesis in Apc-minus mice. The FASEB Journal 20 (2006) 506-508
62. Myzak M.C., Tong P., Dashwood W.M., Dashwood R.H., and Ho E. Sulforaphane retards the growth of human PC-3 xenografts and inhibits HDAC activity in human subjects. Experimental Biology and Medicine 232 (2007) 227-234
63. Nicco C., Laurent A., Chereau C., Weill B., and Batteux F. Differential modulation of normal and tumor cell proliferation by reactive oxygen species. Biomedicine & Pharmacotherapy 59 (2005) 169-174
64. Nicholson D.W., Ali A., and Thornberry N.A. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 376 (1995) 37-43
65. Owuor E.D., and Kong A.N. Antioxidants and oxidants regulated signal transduction pathways. Biochemical Pharmacology 64 (2002) 765-770
66. Palmiter R.D. Regulation of metallothionein genes by heavy metals appears to be mediated by a zinc-sensitive inhibitor that interacts with a constitutively active transcription factor, MTF-1. Proceedings of the National Academy of Sciences of the United States of America 91 (1994) 1219-1223
67. Palmiter R.D. The elusive function of metallothioneins. Proceedings of the National Academy of Sciences of the United States of America 95 (1998) 8428-8430
68. Palmiter R.D., Findley S.D., Whitmore T.E., and Durnam D.M. MT-III, a brain-specific member of the metallothionein gene family. Proceedings of the National Academy of Sciences of the United States of America 89 (1992) 6333-6337
69. Papi A., Orlandi M., Bartolini G., Barillari J., Iori R., Paolini M., Ferroni F., Grazia Fumo M., Pedulli G.F., and Valgimigli L. Cytotoxic and antioxidant activity of 4-methylthio-3-butenyl isothiocyanate from Raphanus sativus L. (Kaiware Daikon) sprouts. Journal of Agricultural and Food Chemistry 56 (2008) 875-883
70. Pham N.A., Jacobberger J.W., Schimmer A.D., Cao P., Gronda M., and Hedley D.W. The dietary isothiocyanate sulforaphane targets pathways of apoptosis, cell cycle arrest, and oxidative stress in human pancreatic cancer cells and inhibits tumor growth in severe combined immunodeficient mice. Molecular Cancer Therapeutics 3 (2004) 1239-1248
71. Phillipson R.P., Tobi S.E., Morris J.A., and McMillan T.J. UV-A induces persistent genomic instability in human keratinocytes through an oxidative stress mechanism. Free Radical Biology & Medicine 32 (2002) 474-480
72. Quafe C.J., Findley S.D., Erickson J.C., Froelick G.J., Kelly E.J., Zambrowicz B.P., and Palmiter R.D. Induction of new metallothionein isoform (MT-IV) occurs during differentiation of stratified squamous epithelia. Biochemistry 33 (1994) 7250-7259
73. Rahman I. Oxidative stress, transcription factors and chromatin remodelling in lung inflammation. Biochemical Pharmacology 64 (2002) 935-942
74. Ramos-Gomez M., Dolan P.M., Itoh K., Yamamoto M., and Kensler T.W. Interactive effects of Nrf2 genotype and oltipraz on benzo[a]pyrene-DNA adducts and tumor yield in mice. Carcinogenesis 24 (2003) 461-467
75. Rokhlin O., Guseva W.N., Tagiyev A., Knudson C.M., and Cohen M.B. Bcl-2 oncoprotein protects the human prostatic carcinoma cell line PC3 from TRAIL-mediated apoptosis. Oncogene 20 (2001) 2836-2843
76. Saydam N., Georgiev O., Nakano M.Y., Greber U.F., and Schaffner W. Nucleo-cytoplasmic trafficking of metal-regulatory transcription factor 1 is regulated by diverse stress signals. The Journal of Biological Chemistry 276 (2001) 25487-25495
77. min/+ mouse. Cancer Research 67 (2007) 9937-9944
78. Shen G., Hebbar V., Nair S., Xu C., Li W., Lin W., Keum Y.S., Han J., Gallo M.A., and Kong A.N. Regulation of Nrf2 transactivation domain activity. The differential effects of mitogen-activated protein kinase cascades and synergistic stimulatory effect of Raf and CREB binding protein. The Journal of Biological Chemistry 279 (2004) 23052-23060
79. Singh A.V., Xiao D., Lew K.L., Dhir R., and Singh S.V. Sulforaphane induces caspase-mediated apoptosis in cultured PC-3 human prostate cancer cells and retards growth of PC-3 xenografts in vivo. Carcinogenesis 25 (2004) 83-90
80. Singh S.V., Herman-Antosiewicz A., Singh A.V., Lew K.L., Srivastava S.K., Kamath R., Brown K.D., and Baskaran R. Sulforaphane-induced G2/M phase cell cycle arrest involves checkpoint kinase 2-mediated phosphorylation of cell division cycle 25C. The Journal of Biological Chemistry 279 (2004) 25813-25822
81. Singletary K., and MacDonald C. Inhibition of benzo[a]pyrene- and 1,6-dinitropyrene-DNA adduct formation in human mammary epithelial cells by dibenzoylmethane and sulforaphane. Cancer Letters 155 (2000) 47-54
82. Smith J.J., Tully P., and Padberg R.M. Chemoprevention: A primary cancer prevention strategy. Seminars in Oncology Nursing 21 (2005) 243-251
83. Sporn M.B., and Liby K.T. Cancer chemoprevention: Scientific promise, clinical uncertainty. Nature Clinical Practice: Oncology 2 (2005) 518-525
84. Stoner G.D., Morse M.A., and Kelloff G.J. Perspectives in cancer chemoprevention. Environmental Health Perspectives 4 (1997) 945-954
85. Sun S.Y., Hail Jr. N., and Lotan R. Apoptosis as a novel target for cancer chemoprevention. Journal of the National Cancer Institute 96 (2004) 662-672
86. Sung H.J., Eskin S.G., Sakurai Y., Yee A., Kataoka N., and McIntire L.V. Oxidative stress produced with cell migration increases synthetic phenotype of vascular smooth muscle cells. Annals of Biomedical Engineering 33 (2005) 1546-1554
87. Surh Y.J., Kundu J.K., Na H.K., and Lee J.S. Redox-sensitive transcription factors as prime targets for chemoprevention with anti-inflammatory and antioxidative phytochemicals. The Journal of Nutrition 135 (2005) 2993S-3001S
88. Tang L., and Zhang Y. Mitochondria are the primary target in isothiocyanate-induced apoptosis in human bladder cancer cells. Molecular Cancer Therapeutics 4 (2005) 1250-1259
89. Thimmulappa R.K., Mai H., Srisuma S., Kensler T.W., Yamamoto M., and Biswal S. Identification of Nrf2-regulated genes induced by the chemopreventive agent sulforaphane by oligonucleotide microarray. Cancer Research 62 (2002) 5196-5203
90. Thornalley P.J. Isothiocyanates: Mechanism of cancer chemopreventive action. Anti-cancer Drugs 13 (2002) 331-338
91. Thornberry N.A., and Lazebnik Y. Caspases: Enemies within. Science 281 (1998) 1312-1316
92. Vasak M. Advances in metallothionein structure and functions. Journal of Trace Elements in Medicine and Biology 19 (2005) 13-17
93. Wang L., Liu D., Ahmed T., Chung F.L., Conaway C., and Chiao J.W. Targeting cell cycle machinery as a molecular mechanism of sulforaphane in prostate cancer prevention. International Journal of Oncology 24 (2004) 187-192
94. Yeh C.T., and Yen G.C. Effect of sulforaphane on metallothionein expression and induction of apoptosis in human hepatoma HepG2 cells. Carcinogenesis 26 (2005) 2138-2148
95. You H.J., Oh D.H., Choi C.Y., Lee D.G., Hahm K.S., Moon A.R., and Jeong H.G. Protective effect of metallothionein-III on DNA damage in response to reactive oxygen species. Biochimica et Biophysica Acta 1573 (2002) 33-38
96. Yu R., Chen C., Mo Y.Y., Hebbar V., Owuor E.D., Tan T.H., and Kong A.N. Activation of mitogen-activated protein kinase pathways induces antioxidant response element-mediate gene expression via a Nrf2-dependent mechanism. The Journal of Biological Chemistry 275 (2001) 39907-39913
97. Yu R., Jiao J.J., Duh J.L., Tan T.H., and Kong A.N. Phenethyl isothiocyanate, a natural chemopreventive agent, activates c-Jun N-terminal kinase. Cancer Research 56 (1996) 2954-2959
98. Zafarullah M., Li W.Q., Sylvester J., and Ahmad M. Molecular mechanisms of N-acetylcysteine actions. Cellular and Molecular Life Sciences 60 (2003) 6-20
99. Zhang Y. Cancer-preventive isothiocyanates: Measurement of human exposure and mechanism of action. Mutation Research 555 (2004) 173-190
100. Zhang Y., Talalay P., Cho C.G., and Posner G.H. A major inducer of anticarcinogenic protective enzymes from broccoli: Isolation and elucidation of structure. Proceedings of the National Academy of Sciences of the United States of America 89 (1992) 2399-2403