Synergy between sulforaphane and selenium in the up-regulation of thioredoxin reductase and protection against hydrogen peroxide-induced cell death in human hepatocytes

Food Chemistry

Volumn 133, Issue 2, 2012, Pages 300-307

  Li, Dan ^a,d   Wang, Wei ^b   Shan, Yujuan ^a   Barrera, Lawrence N ^b   Howie, Alexander F ^c   Beckett, Geoffrey J ^c   Wu, Kun ^a   Bao, Yongping ^b  

^a HARBIN MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d SUN YAT SEN UNIVERSITY   (China)

Author keywords

Cruciferous vegetable; Dietary supplement; Hepatocytes; Selenium; Sulforaphane; Thioredoxin reductase

Indexed keywords

ANTIOXIDANT ENZYME; CELL VIABILITY; CHEMOPREVENTIVE AGENTS; DIETARY SUPPLEMENTS; HEPATOCYTES; HEPG2 CELLS; HUMAN HEPATOCYTES; HUMAN HEPATOMAS; ISOTHIOCYANATES; OXIDATIVE DAMAGE; SIGNALLING PATHWAYS; SULFORAPHANE; SYNERGISTIC EFFECT; THIOREDOXIN REDUCTASE; THIOREDOXINS; UP-REGULATION;

CELL DEATH; ENZYMES; FREE RADICALS; HYDROGEN PEROXIDE;

SELENIUM;

FREE RADICAL; HYDROGEN PEROXIDE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; SELENIUM; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; SULFORAPHANE; SYNAPTOPHYSIN; THIOREDOXIN REDUCTASE 1; TRANSCRIPTION FACTOR NRF2; ISOTHIOCYANIC ACID; ISOTHIOCYANIC ACID DERIVATIVE; SULFORAFAN; THIOREDOXIN REDUCTASE;

APOPTOSIS; ARTICLE; CELL IMMORTALIZATION; CELL NUCLEUS; CELL PROTECTION; CELL VIABILITY; CONTROLLED STUDY; ENZYME INDUCTION; GENE SILENCING; GENE TRANSLOCATION; GENETIC TRANSCRIPTION; HEPATOMA CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IC 50; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; CELL DEATH; CELL LINE; CYTOLOGY; DRUG EFFECTS; DRUG POTENTIATION; HEPG2 CELL LINE; LIVER CELL; METABOLISM; UPREGULATION;

CELL DEATH; CELL LINE; DRUG SYNERGISM; HEP G2 CELLS; HEPATOCYTES; HUMANS; HYDROGEN PEROXIDE; ISOTHIOCYANATES; SELENIUM; THIOREDOXIN-DISULFIDE REDUCTASE; UP-REGULATION;

EID: 84862797146     PISSN: 03088146     EISSN: 18737072     Source Type: Journal    
DOI: 10.1016/j.foodchem.2012.01.026     Document Type: Article

References (54)

1. A. Anwar-Mohamed, and A. El-Kadi Sulforaphane induces CYP1A1 mRNA, protein, and catalytic activity levels via an AhR-dependent pathway in murine hepatoma Hepa 1c1c7 and human HepG2 cells Cancer Letters 275 2009 93 101
2. J.R. Bacon, G. Williamson, R.C. Garner, G. Lappin, S. Langouët, and Y. Bao Sulforaphane and quercetin modulate PhIP-DNA adduct formation in human HepG2 cells and hepatocytes Carcinogenesis 24 2003 1903 1911 (Pubitemid 38008530)
3. J.R. Bacon, G.W. Plumb, A.F. Howie, G.J. Beckett, W. Wang, and Y.P. Bao Dual action of sulforaphane in the regulation of thioredoxin reductase and thioredoxin in human HepG2 and Caco-2 cells Journal of Agricultural and Food Chemistry 55 2007 1170 1176
4. M.A. Beck, O.A. Levander, and J. Handy Selenium deficiency and viral infection Journal of Nutrition 133 Suppl 2003 S1463 S1467
5. L. Campbell, A.F. Howie, J.R. Arthur, F. Nicol, and G. Beckett Selenium and sulforaphane modify the expression of selenoenzymes in the human endothelial cell line EAhy926 and protect cells from oxidative damage Nutrition 23 2007 138 144 (Pubitemid 46096722)
6. F. Caple, E.A. Williams, A. Spiers, J. Tyson, B. Burtle, and A.K. Daly Inter-individual variation in DNA damage and base excision repair in young, healthy non-smokers: Effects of dietary supplementation and genotype British Journal of Nutrition 103 2010 1585 1593
7. B.E. Cavell, S.S. Syed Alwi, A. Donlevy, and G. Packham Anti-angiogenic effects of dietary isothiocyanates: Mechanisms of action and implications for human health Biochemical Pharmacology 81 2011 327 336
8. K. Chan, X.D. Han, and Y.W. Kan An important function of Nrf2 in combating oxidative stress: Detoxification of acetaminophen Proceedings of the National Academy of Sciences of the United States of America 98 2001 4611 4616 (Pubitemid 32295024)
9. K.L. Cheung, and A.N. Kong Molecular targets of dietary phenethyl isothiocyanate and sulforaphane for cancer chemoprevention AAPS Journal 12 2010 87 97
10. L.C. Clark, G.F. Combs Jr., B.W. Turnbull, E.H. Slate, D.K. Chalker, and J. Chow Effects of selenium supplementation for cancer prevention in patients with carcinoma of the skin. A randomized controlled trial. Nutritional prevention of cancer study group JAMA 276 1996 1957 1963 (Pubitemid 26427723)
11. J.D. Clarke, R.H. Dashwood, and E. Ho Multi-targeted prevention of cancer by sulforaphane Cancer Letters 269 2008 291 304
12. R.F. Clayton, A. Rinaldi, E.E. Kandyba, M. Edward, C. Willberg, P. Klenerman, and A.H. Patel Liver cell lines for the study of hepatocyte functions and immunological response Liver International 25 2005 389 402
13. M.S. Crane, A.F. Howie, J.R. Arthur, F. Nicol, L.K. Crosley, and G.J. Beckett Modulation of thioredoxin reductase-2 expression in EAhy926 cells: Implications for endothelial selenoprotein hierarchy Biochimica et Biophysica Acta 1790 2009 1191 1197
14. A.T. Dinkova-Kostova, W.D. Holtzclaw, R.N. Cole, K. Itoh, N. Wakabayashi, Y. Katoh, M. Yamamoto, and P. Talalay Direct evidence that sulfhydryl groups of Keap1 are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxidants Proceedings of the National Academy of Sciences of the United States of America 99 2002 11908 11913 (Pubitemid 34994497)
15. G.R. Fenwick, R.K. Heaney, and W.J. Mullin Glucosinolates and their breakdown products in food and food plants Critical Reviews in Food Science and Nutrition 18 1983 123 201
16. A.V. Gasper, A. Al-Janobi, J.A. Smith, J.R. Bacon, P. Fortun, and C. Atherton Glutathione S-transferase M1 polymorphism and metabolism of sulforaphane from standard and high-glucosinolate broccoli American Journal of Clinical Nutrition 82 2005 1283 1291 (Pubitemid 43779728)
17. A. Gibbs, J. Schwartzman, V. Deng, and J. Alumkal Sulforaphane destabilizes the androgen receptor in prostate cancer cells by inactivating histone deacetylase 6 Proceedings of the National Academy of Sciences of the United States of America 106 2009 16663 16668
18. A. Giudice, and M. Montella Activation of the Nrf2-ARE signaling pathway: A promising strategy in cancer prevention BioEssays 28 2006 169 181
19. K.E. Harris, and E.H. Jeffery Sulforaphane and erucin increase MRP1 and MRP2 in human carcinoma cell lines Journal of Nutritional Biochemistry 19 2008 246 254 (Pubitemid 351313891)
20. J.D. Hayes, and M. McMahon NRF2 and KEAP1 mutations: Permanent activation of an adaptive response in cancer Trends in Biochemical Sciences 34 2009 176 188
21. K.J. Hintze, A.S. Keck, J.W. Finley, and E.H. Jeffery Induction of hepatic thioredoxin reductase activity by sulforaphane, both in Hepa1c1c7 cells and in male Fisher 344 rats Journal of Nutritional Biochemistry 14 2003 173 179 (Pubitemid 36543004)
22. J.V. Higdon, B. Delage, D.E. Williams, and R.H. Dashwood Cruciferous vegetables and human cancer risk: Epidemiologic evidence and mechanistic basis Pharmacological Research 55 2007 224 236 (Pubitemid 46518152)
23. A. Holmgren, and M. Björnstedt Thioredoxin and thioredoxin reductase Methods in Enzymology 252 1995 199 208
24. J. Jakubíková, J. Sedlák, R. Mithen, and Y. Bao Role of PI3K/Akt and MEK/ERK signaling pathways in sulforaphane- and erucin-induced phase II enzymes and MRP2 transcription, G2/M arrest and cell death in Caco-2 cells Biochemical Pharmacology 69 2005 1543 1552 (Pubitemid 40719490)
25. J. Jakubíková, J. Sedlák, J. Bod'o, and Y. Bao Effect of isothiocyanates on nuclear accumulation of NF-kappaB, Nrf2, and thioredoxin in Caco-2 cells Journal of Agricultural and Food Chemistry 54 2006 1656 1662
26. E.S. Kang, I.S. Woo, H.J. Kim, S.Y. Eun, K.S. Paek, and H.J. Kim Up-regulation of aldose reductase expression mediated by phosphatidylinositol 3-kinase/Akt and Nrf2 is involved in the protective effect of curcumin against oxidative damage Free Radical Biology and Medicine 43 2007 535 545 (Pubitemid 47058231)
27. A. Kobayashi, M.I. Kang, H. Okawa, M. Ohtsuji, Y. Zenke, and T. Chiba Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2 Molecular and Cellular Biology 24 2004 7130 7139 (Pubitemid 39014439)
28. D. Li, K. Wu, A.F. Howie, G.J. Beckett, W. Wang, and Y. Bao Synergy between broccoli sprout extract and selenium in the upregulation of thioredoxin reductase in human hepatocytes Food Chemistry 110 2008 193 198
29. K.J. Livak, and T.D. Schmittgen Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method Methods 25 2001 402 408 (Pubitemid 34164012)
30. J. Lu, and A. Holmgren Selenoproteins Journal of Biological Chemistry 284 2009 723 727
31. L. Mastrangelo, A. Cassidy, F. Mulholland, W. Wang, and Y. Bao Serotonin receptors, novel targets of sulforaphane identified by proteomic analysis in Caco-2 cells Cancer Research 68 2008 5487 5491
32. S. Miller, S.W. Walker, J.R. Arthur, F. Nicol, K. Pickard, and M.H. Lewin Selenite protects human endothelial cells from oxidative damage and induces thioredoxin reductase Clinical Science (London) 100 2001 543 550 (Pubitemid 32434120)
33. I. Misiewicz, K. Skupińska, E. Kowalska, J. Lubiński, and T. Kasprzycka-Guttman Sulforaphane-mediated induction of a phase 2 detoxifying enzyme NAD(P)H:quinone reductase and apoptosis in human lymphoblastoid cells Acta Biochimica Polonica 51 2004 711 721 (Pubitemid 39296925)
34. D. Nacamulli, C. Mian, D. Petricca, F. Lazzarotto, S. Barollo, and D. Pozza Influence of physiological dietary selenium supplementation on the natural course of autoimmune thyroiditis Clin Endocrinol (Oxford) 73 2010 535 539
35. T. Nguyen, P.J. Sherratt, H.C. Huang, C.S. Yang, and C.B. Pickett Increased protein stability as a mechanism that enhances Nrf2-mediated transcriptional activation of the antioxidant response element. Degradation of Nrf2 by the 26 S proteasome Journal of Biological Chemistry 278 2003 4536 4541 (Pubitemid 36800950)
36. E.D. Owuor, and A.N. Kong Antioxidants and oxidants regulated signal transduction pathways Biochemical Pharmacology 64 2002 765 770 (Pubitemid 35238028)
37. L.V. Papp, J. Lu, A. Holmgren, and K.K. Khanna From selenium to selenoproteins: Synthesis, identity, and their role in human health Antioxidants Redox Signaling 9 2007 775 806 (Pubitemid 46919583)
38. J. Pi, Y. Bai, J.M. Reece, J. Williams, and D. Liu Molecular mechanism of human Nrf2 activation and degradation: Role of sequential phosphorylation by protein kinase CK2 Free Radical Biology and Medicine 42 2007 1797 1806 (Pubitemid 46754754)
39. M. Ramos-Gomez, M.K. Kwak, P.M. Dolan, K. Itoh, M. Yamamoto, P. Talalay, and T.W. Kensler Sensitivity to carcinogenesis is increased and chemoprotective efficacy of enzyme inducers is lost in Nrf2 transcription factor-deficient mice Proceedings of the National Academy of Sciences of the United States of America 98 2001 3410 3415 (Pubitemid 32220859)
40. M. Salazar, A.I. Rojo, D. Velasco, R.M. de Sagarra, and A. Cuadrado Glycogen synthase kinase-3beta inhibits the xenobiotic and antioxidant cell response by direct phosphorylation and nuclear exclusion of the transcription factor Nrf2 Journal of Biological Chemistry 281 2006 14841 14851 (Pubitemid 43855189)
41. P. Sestili, M. Paolillo, M. Lenzi, E. Colombo, L. Vallorani, and L. Casadei Sulforaphane induces DNA single strand breaks in cultured human cells Mutation Research 689 2010 65 73
42. S. Stranges, J.R. Marshall, R. Natarajan, R.P. Donahue, M. Trevisan, and G.F. Combs Effects of long-term selenium supplementation on the incidence of type 2 diabetes: A randomized trial Annals of Internal Medicine 147 2007 217 223 (Pubitemid 351664577)
43. S.R. Subramaniam, and E.M. Ellis Esculetin-induced protection of human hepatoma HepG2 cells against hydrogen peroxide is associated with the Nrf2-dependent induction of the NAD(P)H: Quinone oxidoreductase 1 gene Toxicology and Applied Pharmacology 250 2010 130 136
44. Z. Sun, Z. Huang, and D.D. Zhang Phosphorylation of Nrf2 at multiple sites by MAP kinases has a limited contribution in modulating the Nrf2-dependent antioxidant response PLoS One 4 2009 e6588
45. Y.J. Surh Cancer chemoprevention with dietary phytochemicals Nature Reviews Cancer 10 2003 768 780
46. L. Tang, G.R. Zirpoli, K. Guru, K.B. Moysich, Y. Zhang, C.B. Ambrosone, and S.E. McCann Consumption of raw cruciferous vegetables is inversely associated with bladder cancer risk Cancer Epidemiology, Biomarkers and Prevention 17 2008 938 944 (Pubitemid 351536426)
47. A. Tarozzi, F. Morroni, A. Merlicco, S. Hrelia, C. Angeloni, G. Cantelli-Forti, and P. Hrelia Sulforaphane as an inducer of glutathione prevents oxidative stress-induced cell death in a dopaminergic-like neuroblastoma cell line Journal of Neurochemistry 111 2009 1161 1171
48. L. Valgimigli, and R. Iori Antioxidant and pro-oxidant capacities of ITCs Environmental and Molecular Mutagenesis 50 2009 222 237
49. W. Wang, S.R. Wang, A.F. Howie, G.J. Beckett, R. Mithen, and Y. Bao Sulforaphane, erucin, and iberin up-regulate thioredoxin reductase 1 expression in human MCF-7 cells Journal of Agricultural and Food Chemistry 53 2005 1417 1421 (Pubitemid 40322128)
50. W.M. Westerink, and W.G. Schoonen Phase II enzyme levels in HepG2 cells and cryopreserved primary human hepatocytes and their induction in HepG2 cells Toxicology in Vitro 21 2007 1592 1602 (Pubitemid 350103539)
51. C. Xu, X. Yuan, Z. Pan, G. Shen, J.H. Kim, and S. Yu Mechanism of action of isothiocyanates: The induction of ARE-regulated genes is associated with activation of ERK and JNK and the phosphorylation and nuclear translocation of Nrf2 Molecular Cancer Therapeutics 5 2006 1918 1926 (Pubitemid 44336562)
52. R. Yu, C. Chen, Y.Y. Mo, V. Hebbar, E.D. Owuor, T.H. Tan, and A.N. Kong Activation of mitogen-activated protein kinase pathways induces antioxidant response element-mediated gene expression via a Nrf2-dependent mechanism Journal of Biological Chemistry 275 2000 39907 39913 (Pubitemid 32064611)
53. H. Zeng, and G.F. Combs Jr. Selenium as an anticancer nutrient: Roles in cell proliferation and tumor cell invasion Journal of Nutritional Biochemistry 19 2008 1 7 (Pubitemid 350213396)
54. J.S. Zhang, V. Svehlíková, Y.P. Bao, A.F. Howie, G.J. Beckett, and G. Williamson Synergy between sulforaphane and selenium in the induction of thioredoxin reductase 1 requires both transcriptional and translational modulation Carcinogenesis 24 2003 497 503 (Pubitemid 36432646)