Synergy between sulforaphane and selenium in the induction of thioredoxin reductase 1 requires both transcriptional and translational modulation

Carcinogenesis

Volumn 24, Issue 3, 2003, Pages 497-503

  Zhang, Jingsong ^a,b   Švehlíková, Vanda ^a   Bao, Yongping ^a   Howie, A Forbes ^c   Beckett, Geoffrey J ^c   Williamson, Gary ^a  

^a INSTITUTE OF FOOD RESEARCH   (United Kingdom)

^b UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^c ROYAL INFIRMARY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

1 (5 ISOQUINOLINESULFONYL) 2 METHYLPIPERAZINE; BUTHIONINE SULFOXIMINE; DACTINOMYCIN; GLUTATHIONE; ISOTHIOCYANIC ACID; MESSENGER RNA; PARAQUAT; PROTEIN KINASE C; PROTEIN KINASE C INHIBITOR; SODIUM SELENITE; SULFORAPHANE; THIOREDOXIN REDUCTASE;

CELL PROTECTION; CONTROLLED STUDY; DRUG POTENTIATION; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME INDUCTION; ENZYME LOCALIZATION; GENETIC TRANSCRIPTION; GLUTATHIONE METABOLISM; HUMAN; HUMAN CELL; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; RNA TRANSLATION; TRANSCRIPTION TERMINATION;

CELL LINE; DRUG SYNERGISM; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; PARAQUAT; PROTEIN BIOSYNTHESIS; RNA, MESSENGER; SELENIUM; THIOCYANATES; THIOREDOXIN REDUCTASE (NADPH); TRANSCRIPTION, GENETIC;

EID: 0345700812     PISSN: 01433334     EISSN: None     Source Type: Journal    
DOI: 10.1093/carcin/24.3.497     Document Type: Review

References (54)

1. Kong,A.N., Owuor,E., Yu,R., Hebbar,V., Chen,C., Hu,R. and Mandlekar,S. (2001) Induction of xenobiotic enzymes by the map kinase pathway and the antioxidant or electrophile response element (ARE/EpRE). Drug Metab. Rev., 33, 255-271.
2. Primiano,T., Sutter,T.R. and Kensler,T.W. (1997) Redox regulation of genes that protect against carcinogens. Comp. Biochem. Phys. B, 118, 487-497.
3. Bao,Y.P. and Williamson,G. (1996) Metabolism of hydroperoxy-phospholipids in human hepatoma HepG2 cells. J. Lipid Res., 37, 2351-2360.
4. Daniels,L.A. (1996) Selenium metabolism and bioavailability. Biol. Trace Element Res., 54, 185-199.
5. Zhong,L.W. and Holmgren,A. (2000) Essential role of selenium in the catalytic activities of mammalian thioredoxin reductase revealed by characterization of recombinant enzymes with selenocysteine mutations. J. Biol. Chem., 275, 18121-18128.
6. Mustacich,D. and Powis,G. (2000) Thioredoxin reductase. Biochem. J., 346, 1-8.
7. Arner,E.S., Zhong,L. and Holmgren,A. (1999) Preparation and assay of mammalian thioredoxin and thioredoxin reductase. Methods Enzymol., 300, 226-239.
8. Rigobello,M.P., Callegaro,M.T., Barzon,E., Benetti,M. and Bindoli,A. (1998) Purification of mitochondrial thioredoxin reductase and its involvement in the redox regulation of membrane permeability. Free Rad. Biol. Med., 24, 370-376.
9. Oberley,T.D., Verwiebe,E., Zhong,W.X., Kang,S.W. and Rhee,S.G. (2001) Localization of the thioredoxin system in normal rat kidney. Free Rad. Biol. Med., 30, 412-424.
10. O 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.
11. Fahey,J.W. and Talalay,P. (1999) Antioxidant functions of sulforaphane: a potent inducer of phase II detoxification enzymes. Food Chem. Toxicol., 37, 973-979.
12. Faulkner,K., Mitten,R. and Williamson,G. (1998) Selective increase of the potential anticarcinogen 4-methylsulphinylbutyl glucosinolate in broccoli. Carcinogenesis, 19, 605-609.
13. Taqfiq,N., Heaney,R.K., Plumb,J.A., Fenwick,G.R., Musk,S.R.R. and Williamson,G. (1995) Dietary glucosinolates as blocking-agents against carcinogensis-glucosinolate breakdown products assessed by induction of quinone reductase activity in murine Hepa 1c1c7 cells. Carcinogenesis, 16, 1191-1194.
14. Basten,G.B., Bao,Y,P. and Williamson,G. (2002) Sulforaphane and its glutathione conjugate but not sulforaphane nitrile induce UDP-glucuronosyl transferase (UGT1A1) and glutathione transferase (GSTA1) in cultured cells. Carcinogenesis, 23, 1399-1404.
15. Gamet-Payrastre,L., Li,P.F., Lumeau,S., Cassar,G., Dupont,M.A., Chevolleau,S., Gasc,N., Tulliez,J. and Tercé,F. (2000) Sulforaphane, a naturally occurring isothiocyanate, induces cell cycle arrest and apoptosis in HT29 human colon cancer cells. Cancer Res., 60, 1426-1433.
16. Zhang,Y. and Callaway,C. (2002) High cellular accumulation of sulforaphane, a dietary anticarcinogen, is followed by rapid transporter-mediated export as a glutathione conjugate. Biochem. J., 364, 301-307.
17. Clark,L.C., Combs,G.R, Turnbull,B.W. et al. (1996) Effects of selenium supplementation for cancer prevention in patients with carcinoma of the skin. J. Am. Med. Assoc., 276, 1957-1963.
18. Ganther,H.E. (1999) Selenium metabolism, selenoproteins and mechanisms of cancer prevention: complexities with thioredoxin reductase. Carcinogenesis, 20, 1657-1666.
19. Combs,G.F. Jr and Clark,L.C. (1997) Selenium and cancer prevention. In Garewal,H., ed. Antioxidant Nutrients and Disease Prevention. CRC Press, Boca Raton, pp. 97-113.
20. Yang,J.G., Hill,K.E. and Burk,R.F. (1989) Dietary selenium intake controls rat plasma selenoprotein P concentration. J. Nutr., 119, 1010-1012.
21. Behne,D., Kyriakoplulos,A., Cessner,H., Walzog,B. and Meinhold,H. (1992) Type I iodothyronine deiodinase activity after high selenium intake and relations between selenium and iodine metabolism in rats. J. Nutr., 122, 1542-1546.
22. Finley,J.W., Ip,C., Lisk,D.J., Davis,C.D., Hintze,K.J. and Whanger,P.D. (2001) Cancer-protective properties of high-selenium broccoli. J. Agric. Food Chem., 49, 2679-2683.
23. Davis,C.D., Zeng,H. and Finley,J.W. (2002) Selenium-enriched broccoli decreases intestinal tumorigenesis in multiple intestinal neoplasia mice. J. Nutr., 132, 307-309.
24. Bradford,M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein, utilizing the principle of protein-dye binding. Anal. Biochem., 72, 248-254.
25. Holmgren,A. and Bjornstedt,M. (1995) Thioredoxin and thioredoxin reductase. Methods Enzymol., 252, 199-208.
26. Miller,S., Walker,S.W., Arthur,J.R., Nicol,F., Pickard,K., Lewin,M.H., Howie,A.F. and Beckett,G.J. (2001) Selenite protects human endothelial cells from oxidative damage and induces thioredoxin reductase. Clin. Sci., 100, 543-550.
27. Söderberg,A., Sahaf,B. and Rosén,A. (2000) Thioredoxin reductase, a redox-active selenoprotein, is secreted by normal and neoplastic cells: presence in human plasma. Cancer Res., 60, 2281-2289.
28. Gasdaska,J.R., Gasdaska,P.Y., Gallegos,A. and Powis,G. (1996) Human thioredoxin reductase gene localization to chromosomal position 12q23-q24.1 and mRNA distribution in human tissue. Genomics, 37, 257-259.
29. Gasdaska,P.Y., Berggren,M.M., Berry,M.J. and Powis,G. (1999) Cloning, sequencing and functional expression of a novel human thioredoxin reductase. FEBS Lett., 442, 105-111.
30. Cafferata,E.G., Gonzalez-Guerrico,A.M., Giordano,L., Pivetta,O.H. and Santa-Coloma,T.A. (2000) Interleukin-1 beta regulates CFTR expression in human intestinal T84 cells. Biochem. Biophys. Acta, 1500, 241-248.
31. 2-terminal kinase pathway in human colon cancer cells. Cancer Res., 59, 2445-2450.
32. Domenicotti,C., Paola,D., Vitali,A. et al. (2000) Glutathione depletion induces apoptosis of rat hepatocytes through activation of protein kinase C novel isoforms and dependent increase in AP-1 nuclear binding. Free Rad. Biol. Med., 29, 1280-1290.
33. Zhang,Y. (2000) Role of glutathione in the accumulation of anticarcinogenic isothiocyanates and their glutathione conjugates by murine hepatoma cells. Carcinogenesis, 21, 1175-1182.
34. Zhang,Y. (2001) Molecular mechanism of rapid cellular accumulation of anticarcinogenic isothiocyanates. Carcinogenesis, 22, 425-431.
35. de Haan,J.B., Bladier,C., Griffiths,P. et al. (1998) Mice with a homozygous null mutation for the most abundant glutathione peroxidase, GPx1, show increased susceptibility to the oxidative stress-inducing agents paraquat and hydrogen peroxide. J. Biol. Chem., 273, 22528-22536.
36. Isowa,N., Yoshimura,T., Kosaka,S., Liu,M., Hitomis,S., Yodoi,J. and Wada,H. (2000) Human thioredoxin attenuates hypoxia-reoxygenation injury of murine endothelial cells in a thio-free condition. J. Cell Physiol., 182, 33-40.
37. Hori,K., Katayama,M., Sato,N., Ishii,K., Waga,S. and Yodoi,J. (1994) Neuroprotection by glial-cells through adult T-cell leukemia-derived factor/ human thioredoxin (ADF/TRX). Brain Res., 652, 304-310.
38. Bjornstedt,M., Odlander,B., Kuprin,S., Claesson,H.E. and Holmgren,A. (1996) Selenite incubated with NADPH and mammalian thioredoxin reductase yields selenide, which inhibits lipoxygenase and changes the electron spin resonance spectrum of the active site iron. Biochemistry, 35, 8511-8616.
39. Bjornstedt,M., Hamberg,M., Kumar,S., Xue,J. and Holmgren,A. (1995) Human thioredoxin reductase directly reduces lipid hydroperoxides by NADPH and selenocystine strongly stimulates the reaction via catalytically generated selenols. J. Biol. Chem., 270, 11761-11764.
40. Arteel,G. E., Briviba,K. and Sies,H. (1999) Function of thioredoxin reductase as peroxynitrite reductase using selenocystine or ebselen. Chem. Res. Toxicol., 12, 264-269.
41. Nishinaka,Y., Nakamura,H., Masutani,H. and Yodoi,J. (2001) Redox control of cellular function by thioredoxin; a new therapeutic direction in host defence. Arch. Immunol. Therap. Experimental., 49, 285-292.
42. Gallegos,A., Berggren,M., Gasdaska,J.R. and Powis,G. (1997) Mechanisms of the regulation of thioredoxin reductase activity in cancer cells by the chemopreventive agent selenium. Cancer Res., 57, 4965-4970.
43. Anema,S.M., Walker,S.W., Howie,A.F., Arthur,J.R., Nicol,F. and Beckett,G.J. (1999) Thioredoxin reductase is the major selenoprotein expression in human umbilical-vein endothelial cells and is regulated by protein kinase C. Biochem. J., 342, 111-117.
44. Kumar,S. and Holmgren,A. (1999) Induction of thioredoxin, thioredoxin reductase and glutaredoxin activity in mouse skin by TPA, a calcium ionophore and other tumor promoters. Carcinogenesis, 20, 1761-1767.
45. Howie,A.F., Arthur,J.R., Nicol,F., Walker,S.W., Beech,S.G. and Beckett,G.J. (1998) Identification of a 57-kilodalton selenoprotein in human thyrocytes as thioredoxin reductase and evidence that its expression is regulated through the calcium-phosphoinositol signaling pathway. J. Clin. Endocrinol. Metab., 83, 2052-2058.
46. Rundlöf,A.K., Carlsten,M. and Arnér,E.S.J. (2001) The core promoter of human thioredoxin reductase 1. J. Biol. Chem., 276, 30542-30551.
47. Chen,C.Y.A. and Shyu,A.B. (1995) AU-rich elements - characterization and importance in messenger-RNA degradation. Trends Biochem. Sci., 20, 465-470.
48. WAF1-Cip1) transcription through Sp1 sites by histone deacetylase inhibitor apicidin - involvement of protein kinase C. J. Biol. Chem., 276, 42084-42090.
49. Huang,H.C., Nguyen,T. and Pickett,C.B. (2000) Regulation of the antioxidant response element by protein kinase C-mediated phosphorylation of NF-E2-related factor 2. Proc. Natl Acad. Sci. USA, 97, 12475-12480.
50. Ramos-Gomez,M., Kwak,M.K., Dolan,P.M., Itoh,K., Yamamoto,M., Talalay,P. and Kensler,T.W. (2001) Sensitivity to carcinogenesis is increased and chemoprotective efficacy of enzyme inducers is lost in nrf2 transcription factor-deficient mice. Proc. Natl Acad. Sci. USA, 98, 3410-3415.
51. Kwak,M.K., Itoh,K., Yamamoto,M., Sutter,T.R. and Kensler,T.W. (2001) Role of transcription factor Nrf2 in the induction of hepatic phase 2 and antioxidative enzymes in vivo by the cancer chemoprotective agent, 3H-1,2-dithiole-3-thione. Mol. Med., 7, 135-145.
52. Dinkova-Kostova,A., Holtzclaw,W.D., Cole,R.N., Itoh,K., Wakabayashi,N., Katoh,Y., Yamamoto,M. and Talalay,P. (2002) Direct evidence that sulfhydryl groups of Keap1 are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxidants. Proc. Natl Acad. Sci. USA, 18, 11908-11913.
53. Berggren,M.M., Mangin,J.F., Gasdaska,J.R. and Powis,G. (1998) Effect of selenium on rat thioredoxin reductase activity. Biochem. Pharmacol., 57, 187-193.
54. Ganther,H.E. and Ip,C. (2001) Thioredoxin reductase activity in rat liver is not affected by supranutritional levels of monomethylated selenium in vivo and is inhibited only by high levels of selenium in vitro. J. Nutr., 131, 301-304.