Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2

Molecular and Cellular Biology

Volumn 24, Issue 16, 2004, Pages 7130-7139

  Kobayashi, Akira ^a   Kang, Moon Il ^a   Okawa, Hiromi ^a   Ohtsuji, Makiko ^a   Zenke, Yukari ^b   Chiba, Tomoki ^c   Igarashi, Kazuhiko ^b   Yamamoto, Masayuki ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b HIROSHIMA UNIVERSITY   (Japan)

^c TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; ANTIOXIDANT; CUL3 BASED E3 LIGASE; CULLIN 3; HEAT SHOCK PROTEIN; LIGASE; PROTEASOME; PROTEIN KEAP1; PROTEIN ROC1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NRF2; UBIQUITIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOPLASM; DEGRADATION KINETICS; ENZYME SUBSTRATE; HALF LIFE TIME; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; REGULATOR GENE; STIMULUS RESPONSE;

ANIMALS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CELL CYCLE PROTEINS; CELL LINE; CULLIN PROTEINS; CYSTEINE ENDOPEPTIDASES; DNA-BINDING PROTEINS; FANCONI ANEMIA COMPLEMENTATION GROUP PROTEINS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MACROMOLECULAR SUBSTANCES; MICE; MULTIENZYME COMPLEXES; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN STRUCTURE, TERTIARY; PROTEINS; RECOMBINANT FUSION PROTEINS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES;

ANIMALIA; MAMMALIA; STAPHYLOCOCCUS PHAGE 3A;

EID: 3543008924     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.16.7130-7139.2004     Document Type: Article

References (33)

1. Cope, G. A., and R. J. Deshaies. 2003. COP9 signalosome: a multifunctional regulator of SCF and other cullin-based ubiquitin ligases. Cell 114:663-671.
2. Cullinan, S. B., D. Zhang, M. Hannink, E. Arvisais, R. J. Kaufman, and J. A. Diehl. 2003. Nrf2 is a direct PERK substrate and effector of PERK-dependent cell survival. Mol. Cell. Biol. 23:7198-7209.
3. Dinkova-Kostova, A. T., W. D. Holtzclaw, R. N. Cole, K. Itoh, N. Wakabayashi, Y. Katoh, M. Yamamoto, and P. Talalay. 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 99:11908-11913.
4. Furukawa, M., Y. J. He, C. Borchers, and Y. Xiong. 2003. Targeting of protein ubiquitination by BTB-Cullin 3-Roc1 ubiquitin ligases. Nat. Cell Biol. 5:1001-1007.
5. Geyer, R., S. Wee, S. Andersen, J. Yates, and D. A. Wolf. 2003. BTB/POZ domain proteins are putative substrate adaptors for cullin 3 ubiquitin ligases. Mol. Cell 12:783-790.
6. Hayes, J. D., S. A. Chanas, C. J. Henderson, M. McMahon, C. Sun, G. J. Moffat, C. R. Wolf, and M. Yamamoto. 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.
7. Hershko, A., and A. Ciechanover. 1998. The ubiquitin system. Annu. Rev. Biochem. 67:425-479.
8. Hori, T., F. Osaka, T. Chiba, C. Miyamoto, K. Okabayashi, N. Shimbara, S. Kato, and K. Tanaka. 1999. Covalent modification of all members of human cullin family proteins by NEDD8. Oncogene 18:6829-6834.
9. Itoh, K., N. Wakabayashi, Y. Katoh, T. Ishii, T. O'Connor, and M. Yamamoto. 2003. Keap1 regulates both cytoplasmic-nuclear shuttling and degradation of Nrf2 in response to electrophiles. Genes Cells 8:379-391.
10. Itoh, K., T. Ishii, N. Wakabayashi, and M. Yamamoto. 1999. Regulatory mechanisms of cellular response to oxidative stress. Free Radic. Res. 31:319-324.
11. Kaelin, W. G., Jr. 2002. Molecular basis of the VHL hereditary cancer syndrome. Nat. Rev. Cancer 2:673-682.
12. Kang, M.-I., A. Kobayashi, N. Wakabayashi, S. G. Kim, and M. Yamamoto. 2004. Scaffolding of Keap1 to the actin cytoskeleton controls the function of Nrf2 as key regulator of cytoprotective phase 2 genes. Proc. Natl. Acad. Sci. USA 101:2046-2051.
13. Kobayashi, M., K. Itoh, T. Suzuki, H. Osanai, K. Nishikawa, Y. Katoh, Y. Takagi, and M. Yamamoto. 2002. Identification of the interactive interface and phylogenic conservation of the Nrf2-Keap1 system. Genes Cells 7:807-820.
14. Levonen, A. L., A. Landar, A. Ramachandran, E. K. Ceaser, D. A. Dickinson, G. Zanoni, J. D. Morrow, and V. M. Darley-Usmar. 2004. Cellular mechanisms of redox cell signaling: role of cysteine modification in controlling antioxidant defenses in response to electrophilic lipid oxidation products. Biochem. J. 378:373-382.
15. McMahon, M., K. Itoh, M. Yamamoto, and J. D. Hayes. 2003. Keap1-dependent proteasomal degradation of transcription factor Nrf2 contributes to the negative regulation of antioxidant response element-driven gene expression. J. Biol. Chem. 278:21592-21600.
16. Nguyen, T., P. J. Sherratt, and C. B. Pickett. 2003. Regulatory mechanisms controlling gene expression mediated by the antioxidant response element. Annu. Rev. Pharmacol. Toxicol. 43:233-260.
17. Nguyen, T., P. J. Sherratt, H. C. Huang, C. S. Yang, and C. B. Pickett. 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.
18. Oyake, T., K. Itoh, H. Motohashi, N. Hayashi, H. Hoshino, M. Nishizawa, M. Yamamoto, and K. Igarashi. 1996. Bach proteins belong to a novel family of BTB-basic leucine zipper transcription factors that interact with MafK and regulate transcription through the NF-E2 site. Mol. Cell. Biol. 16:6083-6095.
19. Pickart, C. M. 2001. Ubiquitin enters the new millennium. Mol. Cell 8:499-504.
20. Pintard, L., T. Kurz, S. Glaser, J. H. Willis, M. Peter, and B. Bowerman. 2003. Neddylation and deneddylation of CUL-3 is required to target MEI-1/katanin for degradation at the meiosis-to-mitosis transition in C. elegans. Curr. Biol. 13:911-921.
21. Pintard, L., J. H. Willis, A. Willems, J. L. Johnson, M. Srayko, T. Kurz, S. Glaser, P. E. Mains, M. Tyers, B. Bowerman, and M. Peter. 2003. The BTB protein MEL-26 is a substrate-specific adaptor of the CUL-3 ubiquitin-ligase. Nature 425:311-316.
22. Sekhar, K. R., S. R. Soltaninassab, M. J. Borrelli, Z. Q. Xu, M. J. Meredith, F. E. Domann, and M. L. Freeman. 2000. Inhibition of the 26S proteasome induces expression of GLCLC, the catalytic subunit for gamma-glutamylcysteine synthetase. Biochem. Biophys. Res. Commun. 270:311-317.
23. Semenza, G. L. 2001. HIF-1 and mechanisms of hypoxia sensing. Curr. Opin. Cell Biol. 13:167-171.
24. Singer, J. D., M. Gurian-West, B. Clurman, and J. M. Roberts. 1999. Cullin-3 targets cyclin E for ubiquitination and controls S phase in mammalian cells. Genes Dev. 13:2375-2387.
25. Stewart, D., E. Killeen, R. Naquin, S. Alam, and J. Alam. 2003. Degradation of transcription factor Nrf2 via the ubiquitin-proteasome pathway and stabilization by cadmium. J. Biol. Chem. 278:2396-2402.
26. Treier, M., L. M. Staszewski, and D. Bohmann. 1994. Ubiquitin-dependent c-Jun degradation in vivo is mediated by the delta domain. Cell 78:787-798.
27. Wakabayashi, N., A. T. Dinkova-Kostova. W. D. Holtzclaw, M-I. Kang, A. Kobayashi, M. Yamamoto, T. W. Kensler, and P. Talalay. 2004. Protection against electrophile and oxidant stress by induction of the phase 2 response: Fate of cysteines of the Keap1 sensor modified by inducers. Proc. Natl. Acad. Sci. USA 101:2040-2045.
28. Wall, M. A., D. E. Coleman, E. Lee, J. A. Iniguez-Lluhi, B. A. Posner, A. G. Gilman, and S. R. Sprang. 1995. The structure of the G protein heterotrimer Gi alpha 1 beta 1 gamma 2. Cell 83:1047-1058.
29. Wolf, D. A., C. Zhou, and S. Wee. 2003. The COP9 signalosome: an assembly and maintenance platform for cullin ubiquitin ligases? Nat. Cell Biol. 5:1029-1033.
30. Xu, L., Y. Wei, J. Reboul, P. Vaglio, T. H. Shin, M. Vidai, S. J. Elledge, and J. W. Harper. 2003. BTB proteins are substrate-specific adaptors in an SCF-like modular ubiquitin ligase containing CUL-3. Nature 425:316-321.
31. Zhang, D. D., and M. Hannink. 2003. 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. 23:8137-8151.
32. Zheng, N., B. A. Schulman, L. Song, J. J. Miller, P. D. Jeffrey, P. Wang, C. Chu, D. M. Koepp, S. J. Elledge, M. Pagano, R. C. Conaway, J. W. Conaway, J. W. Harper, and N. P. Pavletich. 2002. Structure of the Cull-Rbx1-Skp1-F boxSkp2 SCF ubiquitin ligase complex. Nature 416:703-709.
33. Zipper, L. M., and R. T. Mulcahy. 2002. The Keap1 BTB/POZ dimerization function is required to sequester Nrf2 in cytoplasm. J. Biol. Chem. 277:36544-36552.