Dynamics of Nrf2 and Keap1 in ARE-mediated NQO1 expression by wasabi 6-(methylsulfinyl)hexyl isothiocyanate

Journal of Agricultural and Food Chemistry

Volumn 59, Issue 22, 2011, Pages 11975-11982

  Hou, De Xing ^a,b   Korenori, Yoshimi ^b   Tanigawa, Shunsuke ^b   Yamada Kato, Tomoe ^c   Nagai, Masashi ^c   He, Xi ^a   He, Jianhua ^a  

^a HUNAN AGRICULTURAL UNIVERSITY   (China)

^b KAGOSHIMA UNIVERSITY   (Japan)

^c Kinjirushi Co Ltd   (Japan)

Author keywords

6 MSITC; Keap1; modification; NQO1; Nrf2; ubiquitination

Indexed keywords

6-MSITC; KEAP1; MODIFICATION; NQO1; NRF2; UBIQUITINATION;

DISEASES; GENES;

TRANSCRIPTION;

6 (METHYLSULFINYL)HEXYL ISOTHIOCYANATE; 6-(METHYLSULFINYL)HEXYL ISOTHIOCYANATE; ISOTHIOCYANIC ACID DERIVATIVE; KEAP1 PROTEIN, HUMAN; NQO1 PROTEIN, HUMAN; PLANT EXTRACT; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); SIGNAL PEPTIDE; TRANSCRIPTION FACTOR NRF2;

ARTICLE; CELL LINE; CHEMISTRY; DNA RESPONSIVE ELEMENT; DRUG EFFECT; EUTREMA; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; PROTEIN BINDING; REPORTER GENE; TRANSCRIPTION INITIATION;

CELL LINE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENES, REPORTER; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; ISOTHIOCYANATES; NAD(P)H DEHYDROGENASE (QUINONE); NF-E2-RELATED FACTOR 2; PLANT EXTRACTS; PROTEIN BINDING; RESPONSE ELEMENTS; TRANSCRIPTIONAL ACTIVATION; WASABIA;

EUTREMA WASABI;

EID: 81255138105     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf2032439     Document Type: Article

References (36)

1. Isshiki, K.; Tokuoka, K.; Mori, R.; Chiba, S. Preliminary examination of allyl isothiocyanate vapor for food preservation Biosci., Biotechnol., Biochem. 1992, 56, 1476-1477
2. Kumagai, H.; Kashima, N.; Seki, T.; Sakurai, H.; Ishii, K.; Ariga, T. Analysis of components in essential oil of upland wasabi and their inhibitory effects on platelet aggregation Biosci., Biotechnol., Biochem. 1994, 58, 2131-2135
3. Etoh, H.; Nishimura, A.; Takasawa, R.; Yagi, A.; Saito, K.; Sakata, K.; Kishima, I.; Ina, K. Methylsulfinylalkyl isothiocyanates in wasabi, Wasabia japonica MATSUM Agric. Biol. Chem. 1990, 54, 1587-1591
4. Ono, H.; Tesaki, S.; Tanabe, S.; Watanabe, M. 6-Methylsulfinylhexyl isothiocyanate and its homologues as food-originated compounds with antibacterial activity against Escherichia coli and Staphylococcus aureus Biosci., Biotechnol., Biochem. 1998, 62, 363-365
5. Hou, D.-X.; Fukuda, M.; Fujii, M.; Fuke, Y. Transcriptional regulation of nicotinamide adenine dinucleotide phosphate: quinone oxidoreductase in murine hepatoma cells by 6-(methylsulfinyl)hexyl isothiocyanate, an active principle of wasabi (Eutrema wasabi Maxim.) Cancer Lett. 2000, 20, 195-200
6. Hou, D.-X.; Fukuda, M.; Fujii, M.; Fuke, Y. Induction of NADPH: quinone oxidoreductase in murine hepatoma cells by methysulfinyl isothiocyanates: Methyl chain length-activity study Int. J. Mol. Med. 2000, 6, 441-444
7. Hayes, J. D.; McMahon, M. Molecular basis for the contribution of the antioxidant responsive element to cancer chemoprevention Cancer Lett. 2011, 174, 103-113
8. Venugopal, R.; Jaiswal, A. K. Nrf1 and Nrf2 positively and c-Fos and Fra1 negatively regulate the human antioxidant response element-mediated expression of NAD(P)H:quinone oxidoreductase 1 gene Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 14960-14965 (Pubitemid 26419078)
9. Wasserman, W. W.; Fahl, W. E. Functional antioxidant responsive elements Proc. Natl. Acad. Sci. U.S.A. 1997, 94, 5361-5366 (Pubitemid 27214788)
10. Itoh, K.; Chiba, T.; Takahashi, S.; Ishii, T.; Igarashi, K.; Katoh, Y.; Oyake, T.; Hayashi, N.; Satoh, K.; Hatayama, I.; Yamamoto, M.; Nabeshima, Y. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements Biochem. Biophys. Res. Commun. 1997, 236, 313-322 (Pubitemid 27373291)
11. Nguyen, T.; Huang, H. C.; Pickett, C. B. Transcriptional regulation of the antioxidant response element: Activation by Nrf2 and repression by MafK J. Biol. Chem. 2000, 275, 15466-15473 (Pubitemid 30337278)
12. Itoh, K.; Wakabayashi, N.; Katoh, Y.; Ishii, T.; Igarashi, K.; Engel, J. D.; Yamamoto, M. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain Genes Dev. 1999, 13, 76-86 (Pubitemid 29045117)
13. Nguyen, T.; Sherratt, P. J.; Huang, H. C.; Yang, C. S.; Pickett, C. B. Increased protein stability as a mechanism that enhances Nrf2-mediated transcriptional activation of the antioxidant response element: Degradation of Nrf2 by the 26S proteasome J. Biol. Chem. 2003, 278, 4536-4541 (Pubitemid 36800950)
14. Kobayashi, A.; Kang, M. I.; Okawa, H.; Ohtsuji, M.; Zenke, Y.; Chiba, T.; Igarashi, K.; Yamamoto, M. Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2 Mol. Cell. Biol. 2004, 24, 7130-7139 (Pubitemid 39014439)
15. Zhang, D. D.; Lo, S. C.; Cross, J. V.; Templeton, D. J.; Hannink, M. Keap1 is a redox-regulated substrate adaptor protein for a Cul3-dependent ubiquitin ligase complex Mol. Cell. Biol. 2004, 24, 10941-10953 (Pubitemid 39603148)
16. Cullinan, S. B.; Gordan, J. D.; Jin, J.; Harper, J. W.; Diehl, J. A. The Keap1-BTB protein is an adaptor that bridges Nrf2 to a Cul3-based E3 ligase: Oxidative stress sensing by a Cul3-Keap1 ligase Mol. Cell. Biol. 2004, 24, 8477-8486 (Pubitemid 39245070)
17. Furukawa, M.; Xiong, Y. BTB protein Keap1 targets antioxidant transcription factor Nrf2 for ubiquitination by the Cullin 3-Roc1 ligase Mol. Cell. Biol. 2005, 25, 162-171 (Pubitemid 40039808)
18. Zhang, D. D.; Lo, S. C.; Sun, Z.; Habib, G. M.; Lieberman, M. W.; Hannink, M. Ubiquitination of Keap1, a BTB-Kelch substrate adaptor protein for Cul3, targets Keap1 for degradation by a proteasome independent pathway J. Biol. Chem. 2005, 280, 30091-30099 (Pubitemid 41216185)
19. Moehlenkamp, J. D.; Johnson, J. A. Activation of antioxidant/ electrophile-responsive elements in IMR-32 human neuroblastoma cells Arch. Biochem. Biophys. 1999, 363, 98-106 (Pubitemid 29394335)
20. Tanigawa, S.; Fujii, M.; Hou, D.-X. Action of Nrf2 and Keap1 in ARE-mediated NQO1 expression by quercetin Free Radical Biol. Med. 2007, 42, 1690-1703 (Pubitemid 46617147)
21. Akimaru, H.; Hou, D.-X.; Ishii, S. Drosophila CBP is required for dorsal-dependent twist gene expression Nat. Genet. 1997, 17, 211-214
22. Stewart, D.; Killeen, E.; Naquin, R.; Alam, S.; Alam, J. Degradation of transcription factor Nrf2 via the ubiquitin-proteasome pathway and stabilization by cadmium J. Biol. Chem. 2003, 278, 2396-2402 (Pubitemid 36801313)
23. Kobayashi, A.; Kang, M. I.; Watai, Y.; Tong, K. I.; Shibata, T.; Uchida, K.; Yamamoto, M. Oxidative and electrophilic stresses activate Nrf2 through inhibition of ubiquitination activity of Keap1 Mol. Cell. Biol. 2006, 26, 221-229
24. Martin, S. J.; Lennon, S. V.; Bonham, A. M.; Cotter, T. G. Induction of apoptosis (programmed cell death) in human leukemic HL-60 cells by inhibition of RNA or protein synthesis J. Immunol. 1990, 145, 1859-1867 (Pubitemid 20336755)
25. McMahon, M.; Itoh, K.; Yamamoto, M.; Hayes, J. D. Keap1-dependent proteasomal degradation of transcription factor Nrf2 contributes to the negative regulation of antioxidant response element-driven gene expression J. Biol. Chem. 2003, 278, 21592-21600 (Pubitemid 36792558)
26. Zhang, D. D.; Hannink, M. Distinct cysteine residues in Keap1 are required for Keap1-dependent ubiquitination of Nrf2 and for stabilization of Nrf2 by chemopreventive agents and oxidative stress Mol. Cell. Biol. 2003, 23, 8137-8151 (Pubitemid 37377505)
27. Hong, F.; Freeman, M. L.; Liebler, D. C. Identification of sensor cysteines in human Keap1 modified by the cancer chemopreventive agent sulforaphane Chem. Res. Toxicol. 2005, 18, 1917-1926 (Pubitemid 43023050)
28. Sakurai, T.; Kanayama, M.; Shibata, T.; Itoh, K.; Kobayashi, A.; Yamamoto, M.; Uchida, K. Ebselen, a seleno-organic antioxidant, as an electrophile Chem. Res. Toxicol. 2006, 19, 1196-1204 (Pubitemid 44454036)
29. Dinkova-Kostova, A. T.; Holtzclaw, W. D.; Cole, R. N.; Itoh, K.; Wakabayashi, N.; Katoh, Y.; Yamamoto, M.; Talalay, P. 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. U.S.A. 2002, 99, 11908-11913 (Pubitemid 34994497)
30. Dhakshinamoorthy, S.; Jaiswal, A. K. Functional characterization and role of INrf2 in antioxidant response element-mediated expression and antioxidant induction of NAD(P)H:quinone oxidoreductase 1 gene Oncogene 2001, 20, 3906-3917 (Pubitemid 32646201)
31. He, X.; Chen, M. G.; Lin, G. X.; Ma, Q. Arsenic induces NAD(P)Hquinone oxidoreductase I by disrupting the Nrf2/Keap1/Cul3 complex and recruiting Nrf2/Maf to the antioxidant response element enhancer J. Biol. Chem. 2006, 281, 23620-23631 (Pubitemid 44274137)
32. Zhang, Y. Molecular mechanism of rapid cellular accumulation of anticaricinogenic isothiocyanates Carcinogenesis 2001, 22, 425-431 (Pubitemid 32203821)
33. Morimitsu, Y.; Nakagawa, Y.; Hayashi, K.; Fujii, H.; Kumagai, T.; Nakamura, Y.; Osawa, T.; Horio, F.; Itoh, K.; Iida, K.; Yamamoto, M.; Uchida, K. A Sulforaphane Analogue That Potently Activates the Nrf2-dependent Detoxification Pathway J. Biol. Chem. 2006, 277, 3456-3463 (Pubitemid 34953214)
34. Hu, R.; Hebbar, V.; Kim, B. R.; Chen, C.; Winnik, B.; Buckley, B.; Soteropoulos, P.; Tolias, P.; Hart, R. P.; Kong, A. N. In vivo pharmacokinetics and regulation of gene expression profiles by isothiocyanate sulforaphane in the rat J. Pharmacol. Exp. Ther. 2004, 310, 263-271 (Pubitemid 38812720)
35. Ye, L.; Dinkova-Kostova, A. T.; Wade, K. L.; Zhang, Y.; Shapiro, T. A.; Talalay, P. Quantitative determination of dithiocarbamates in human plasma, serum, erythrocytes and urine: Pharmacokinetics of broccoli sprout isothiocyanates in humans Clin. Chim. Acta 2002, 316, 43-53 (Pubitemid 34028187)
36. Clarke, J. D.; Dashwood, R. H.; Ho, E. Multi-targeted prevention of cancer by sulforaphane Cancer Lett. 2008, 269, 291-304