Interaction of keap1 modified by 2- tert -butyl-1,4-benzoquinone with GSH: Evidence for S -transarylation

Chemical Research in Toxicology

Volumn 26, Issue 7, 2013, Pages 1080-1087

  Abiko, Yumi ^a   Kumagai, Yoshito ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 BENZOQUINONE DERIVATIVE; 2 TERT BUTYL 1,4 BENZOQUINONE; ACETYLCYSTEINE; BUTHIONINE SULFOXIMINE; GLUTATHIONE; KELCH LIKE ECH ASSOCIATED PROTEIN 1; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; 2-TERT-BUTYL-4-QUINONE; BENZOQUINONE DERIVATIVE; CYTOSKELETON PROTEIN; KEAP1 PROTEIN, MOUSE; RECOMBINANT PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; THIOL DERIVATIVE;

ARTICLE; ARYLATION; CELL STRAIN HEPG2; CONCENTRATION (PARAMETERS); COVALENT BOND; GENE PRODUCT; OXIDATION; PROTEIN PROTEIN INTERACTION; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; DOSE RESPONSE; HEPG2 CELL LINE; HUMAN; METABOLISM; MOUSE; STRUCTURE ACTIVITY RELATION; TUMOR CELL CULTURE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BENZOQUINONES; CYTOSKELETAL PROTEINS; DOSE-RESPONSE RELATIONSHIP, DRUG; GLUTATHIONE; HEP G2 CELLS; HUMANS; MICE; MOLECULAR STRUCTURE; RECOMBINANT PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP; SULFHYDRYL COMPOUNDS; TUMOR CELLS, CULTURED;

EID: 84880278226     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx400085h     Document Type: Article

References (45)

1. Miura, T. et al. (2011) Chem. Res. Toxicol. 24, 1836 -1844
2. Itoh, K., Chiba, T., Takahashi, S., Ishii, T., Igarashi, K., Katoh, Y., Oyake, T., Hayashi, N., Satoh, K., Hatayama, I., Yamamoto, M., and Nabeshima, Y. (1997) An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements Biochem. Biophys. Res. Commun. 236, 313-322
3. Hayes, J. D., Chanas, S. A., Henderson, C. J., McMahon, M., Sun, C., Moffat, G. J., Wolf, C. R., and Yamamoto, M. (2000) The Nrf2 transcription factor contributes both to the basal expression of glutathione S-transferases in mouse liver and to their induction by the chemopreventive synthetic antioxidants, butylated hydroxyanisole and ethoxyquin Biochem. Soc. Trans. 28, 33-41
4. Lee, J. M., Moehlenkamp, J. D., Hanson, J. M., and Johnson, J. A. (2001) Nrf2-dependent activation of the antioxidant responsive element by tert-butylhydroquinone is independent of oxidative stress in IMR-32 human neuroblastoma cells Biochem. Biophys. Res. Commun. 280, 286-292
5. Li, J., Johnson, D., Calkins, M., Wright, L., Svendsen, C., and Johnson, J. (2005) Stabilization of Nrf2 by tBHQ confers protection against oxidative stress-induced cell death in human neural stem cells Toxicol. Sci. 83, 313-328
6. Verhagen, H., Furnee, C., Schutte, B., Hermans, R. J., Bosman, F. T., Blijham, G. H., ten Hoor, F., Henderson, P. T., and Kleinjans, J. C. (1989) Butylated hydroxyanisole-induced alterations in cell kinetic parameters in rat forestomach in relation to its oxidative cytochrome P-450-mediated metabolism Carcinogenesis 10, 1947-1951
7. Aono, J., Yanagawa, T., Itoh, K., Li, B., Yoshida, H., Kumagai, Y., Yamamoto, M., and Ishii, T. (2003) Activation of Nrf2 and accumulation of ubiquitinated A170 by arsenic in osteoblasts Biochem. Biophys. Res. Commun. 305, 271-277
8. 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. U.S.A. 97, 12475-12480
9. Stewart, D., Killeen, E., Naquin, R., Alam, S., and Alam, J. (2003) Degradation of transcription factor Nrf2 via the ubiquitin-proteasome pathway and stabilization by cadmium J. Biol. Chem. 278, 2396-2402
10. Bryan, H. K., Olayanju, A., Goldring, C. E., and Park, B. K. (2013) The Nrf2 cell defence pathway: Keap1-dependent and -independent mechanisms of regulation Biochem. Pharmacol. 85, 705-717
11. Kobayashi, M. and Yamamoto, M. (2006) Nrf2-Keap1 regulation of cellular defense mechanisms against electrophiles and reactive oxygen species Adv. Enzyme Regul. 46, 113-140
12. Abiko, Y., Miura, T., Phuc, B. H., Shinkai, Y., and Kumagai, Y. (2011) Participation of covalent modification of Keap1 in the activation of Nrf2 by tert-butylbenzoquinone, an electrophilic metabolite of butylated hydroxyanisole Toxicol. Appl. Pharmacol. 255, 32-39
13. Wang, X. J., Hayes, J. D., Higgins, L. G., Wolf, C. R., and Dinkova-Kostova, A. T. (2010) Activation of the NRF2 signaling pathway by copper-mediated redox cycling of para- and ortho-hydroquinones Chem. Biol. 17, 75-85
14. Miura, T. and Kumagai, Y. (2010) Immunochemical method to detect proteins that undergo selective modification by 1,2-naphthoquinone derived from naphthalene through metabolic activation J. Toxicol. Sci. 35, 843-852
15. Iwamoto, N., Sumi, D., Ishii, T., Uchida, K., Cho, A. K., Froines, J. R., and Kumagai, Y. (2007) Chemical knockdown of protein-tyrosine phosphatase 1B by 1,2-naphthoquinone through covalent modification causes persistent transactivation of epidermal growth factor receptor J. Biol. Chem. 282, 33396-33404
16. Miura, T., Shinkai, Y., Jiang, H. Y., Iwamoto, N., Sumi, D., Taguchi, K., Yamamoto, M., Jinno, H., Tanaka-Kagawa, T., Cho, A. K., and Kumagai, Y. (2011) Initial response and cellular protection through the Keap1/Nrf2 system during the exposure of primary mouse hepatocytes to 1,2-naphthoquinone Chem. Res. Toxicol. 24, 559-567
17. Miura, T., Kakehashi, H., Shinkai, Y., Egara, Y., Hirose, R., Cho, A. K., and Kumagai, Y. (2011) GSH-mediated S-transarylation of a quinone glyceraldehyde-3-phosphate dehydrogenase conjugate Chem. Res. Toxicol. 24, 1836-1844
18. Takayama, N., Iwamoto, N., Sumi, D., Shinkai, Y., Tanaka-Kagawa, T., Jinno, H., and Kumagai, Y. (2011) Peroxiredoxin 6 is a molecular target for 1,2-naphthoquinone, an atmospheric electrophile, in human pulmonary epithelial A549 cells J. Toxicol. Sci. 36, 817-821
19. Penning, T. M., Burczynski, M. E., Hung, C. F., McCoull, K. D., Palackal, N. T., and Tsuruda, L. S. (1999) Dihydrodiol dehydrogenases and polycyclic aromatic hydrocarbon activation: generation of reactive and redox active o-quinones Chem. Res. Toxicol. 12, 1-18
20. Dinkova-Kostova, A. T., 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. U.S.A. 99, 11908-11913
21. Toyama, T., Shinkai, Y., Kaji, T., and Kumagai, T. (2013) A convenient method to assess chemical modification of protein thiols by electrophilic metals J. Toxicol. Sci. 38, 477-484
22. Shertzer, H. G., Vasiliou, V., Liu, R. M., Tabor, M. W., and Nebert, D. W. (1995) Enzyme induction by l -buthionine (S,R)-sulfoximine in cultured mouse hepatoma cells Chem. Res. Toxicol. 8, 431-436
23. Zegura, B., Lah, T. T., and Filipic, M. (2006) Alteration of intracellular GSH levels and its role in microcystin-LR-induced DNA damage in human hepatoma HepG2 cells Mutat. Res. 611, 25-33
24. van Ommen, B., Koster, A., Verhagen, H., and van Bladeren, P. J. (1992) The glutathione conjugates of tert-butyl hydroquinone as potent redox cycling agents and possible reactive agents underlying the toxicity of butylated hydroxyanisole Biochem. Biophy. Res. Commun. 189, 309-314
25. Peters, M. M., Lau, S. S., Dulik, D., Murphy, D., van Ommen, B., van Bladeren, P. J., and Monks, T. J. (1996) Metabolism of tert-butylhydroquinone to S-substituted conjugates in the male Fischer 344 rat Chem. Res. Toxicol. 9, 133-139
26. Song, Y., Wagner, B. A., Witmer, J. R., Lehmler, H. J., and Buettner, G. R. (2009) Nonenzymatic displacement of chlorine and formation of free radicals upon the reaction of glutathione with PCB quinones Proc. Natl. Acad. Sci. U.S.A. 106, 9725-9730
27. Slaughter, D. E. and Hanzlik, R. P. (1991) Identification of epoxide- and quinone-derived bromobenzene adducts to protein sulfur nucleophiles Chem. Res. Toxicol. 4, 349-359
28. Slaughter, D. E., Zheng, J., Harriman, S., and Hanzlik, R. P. (1993) Identification of covalent adducts to protein sulfur nucleophiles by alkaline permethylation Anal. Biochem. 208, 288-295
29. Sumi, D., Numasawa, Y., Endo, A., Iwamoto, N., and Kumagai, Y. (2009) Catechol estrogens mediated activation of Nrf2 through covalent modification of its quinone metabolite to Keap1 J. Toxicol. Sci. 34, 627-635
30. Endo, A., Sumi, D., Iwamoto, N., and Kumagai, Y. (2011) Inhibition of DNA binding activity of cAMP response element-binding protein by 1,2-naphthoquinone through chemical modification of Cys-286 Chem.-Biol. Interact. 192, 272-277
31. Taguchi, K., Fujikawa, N., Komatsu, M., Ishii, T., Unno, M., Akaike, T., Motohashi, H., and Yamamoto, M. (2012) Keap1 degradation by autophagy for the maintenance of redox homeostasis Proc. Natl. Acad. Sci. U.S.A. 109, 13561-13566
32. Kumagai, Y., Shinkai, Y., Miura, T., and Cho, A. K. (2012) The chemical biology of naphthoquinones and its environmental implications Annu. Rev. Pharmacol. Toxicol. 52, 221-247
33. Marnett, L. J., Riggins, J. N., and West, J. D. (2003) Endogenous generation of reactive oxidants and electrophiles and their reactions with DNA and protein J. Clin. Invest. 111, 583-593
34. Liebler, D. C. (2008) Protein damage by reactive electrophiles: targets and consequences Chem. Res. Toxicol. 21, 117-128
35. Evans, D. C., Watt, A. P., Nicoll-Griffith, D. A., and Baillie, T. A. (2004) Drug-protein adducts: an industry perspective on minimizing the potential for drug bioactivation in drug discovery and development Chem. Res. Toxicol. 17, 3-16
36. Lin, D., Saleh, S., and Liebler, D. C. (2008) Reversibility of covalent electrophile-protein adducts and chemical toxicity Chem. Res. Toxicol. 21, 2361-2369
37. Toyama, T., Sumi, D., Shinkai, Y., Yasutake, A., Taguchi, K., Tong, K. I., Yamamoto, M., and Kumagai, Y. (2007) Cytoprotective role of Nrf2/Keap1 system in methylmercury toxicity Biochem. Biophys. Res. Commun. 363, 645-650
38. Dinkova-Kostova, A. T., Holtzclaw, W. D., and Kensler, T. W. (2005) The role of Keap1 in cellular protective responses Chem. Res. Toxicol. 18, 1779-1791
39. Zhang, Y. (2000) Role of glutathione in the accumulation of anticarcinogenic isothiocyanates and their glutathione conjugates by murine hepatoma cells Carcinogenesis 21, 1175-1182
40. Hu, C., Eggler, A. L., Mesecar, A. D., and van Breemen, R. B. (2011) Modification of keap1 cysteine residues by sulforaphane Chem. Res. Toxicol. 24, 515-521
41. Hu, C., Nikolic, D., Eggler, A. L., Mesecar, A. D., and van Breemen, R. B. (2012) Screening for natural chemoprevention agents that modify human Keap1 Anal. Biochem. 421, 108-114
42. Buetler, T. M., Gallagher, E. P., Wang, C., Stahl, D. L., Hayes, J. D., and Eaton, D. L. (1995) Induction of phase I and phase II drug-metabolizing enzyme mRNA, protein, and activity by BHA, ethoxyquin, and oltipraz Toxicol. Appl. Pharmacol. 135, 45-57
43. Satoh, T., Saitoh, S., Hosaka, M., and Kosaka, K. (2009) Simple ortho- and para-hydroquinones as compounds neuroprotective against oxidative stress in a manner associated with specific transcriptional activation Biochem. Biophys. Res. Commun. 379, 537-541
44. Itoh, K., Wakabayashi, N., Katoh, Y., Ishii, T., Igarashi, K., Engel, J. D., and Yamamoto, M. (1999) Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain Genes. Dev. 13, 76-86
45. Nguyen, T., Sherratt, P. J., Huang, H. C., Yang, C. S., and Pickett, C. B. (2003) 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 J. Biol. Chem. 278, 4536-4541