Different Electrostatic Potentials Define ETGE and DLG Motifs as Hinge and Latch in Oxidative Stress Response

REFERENCES

• Bonizzi, G., and M. Karin. 2004. The two NF-κB activation pathways and their role in innate and adaptive immunity. Trends Immunol. 25:280–288.
   PubMed Web of Science ®Google Scholar
• Brunger, A. T., P. D. Adams, G. M. Clore, W. L. DeLano, P. Gros, R. W. Grosse-Kunstleve, J. S. Jiang, J. Kuszewski, M. Nilges, N. S. Pannu, R. J. Read, L. M. Rice, T. Simonson, and G. L. Warren. 1998. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. Sect. D 54:905–921.
   PubMed Web of Science ®Google Scholar
• Busino, L., M. Donzelli, M. Chiesa, D. Guardavaccaro, D. Ganoth, N. V. Dorrello, A. Hershko, M. Pagano, and G. F. Draetta. 2003. Degradation of Cdc25A by β-TrCP during S phase and in response to DNA damage. Nature 426:87–91.
   PubMed Web of Science ®Google Scholar
• Ciechanover, A. 1994. The ubiquitin-proteasome proteolytic pathway. Cell 79:13–21.
   PubMed Web of Science ®Google Scholar
• Ciechanover, A. 1998. The ubiquitin-proteasome pathway: on protein death and cell life. EMBO J. 17:7151–7160.
   PubMed Web of Science ®Google Scholar
• Collaborative Computational Project, Number 4. 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. Sect. D 50:760–763.
   PubMedGoogle Scholar
• Cullinan, S. B., J. D. Gordan, J. Jin, J. W. Harper, and J. A. Diehl. 2004. 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. 24:8477–8486.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Furukawa, M., and Y. Xiong. 2005. BTB protein Keap1 targets antioxidant transcription factor Nrf2 for ubiquitination by the Cullin 3-Roc1 ligase. Mol. Cell. Biol. 25:162–171.
   PubMed Web of Science ®Google Scholar
• Hart, M., J. P. Concordet, I. Lassot, I. Albert, R. del los Santos, H. Durand, C. Perret, B. Rubinfeld, F. Margottin, R. Benarous, and P. Polakis. 1999. The F-box protein β-TrCP associates with phosphorylated β-catenin and regulates its activity in the cell. Curr. Biol. 9:207–210.
   PubMed Web of Science ®Google Scholar
• Holtzclaw, W. D., A. T. Dinkova-Kostova, and P. Talalay. 2004. Protection against electrophile and oxidative stress by induction of phase 2 genes: the quest for the elusive sensor that responds to inducers. Adv. Enzyme Regul. 44:335–367.
   PubMedGoogle Scholar
• Itoh, K., N. Wakabayashi, Y. Katoh, T. Ishii, K. Igarashi, J. D. Engel, and M. Yamamoto. 1999. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 13:76–86.
   PubMed Web of Science ®Google Scholar
• Itoh, K., K. I. Tong, and M. Yamamoto. 2004. Molecular mechanism activating Nrf2-Keap1 pathway in regulation of adaptive response to electrophiles. Free Radic. Biol. Med. 36:1208–1213.
   PubMed Web of Science ®Google Scholar
• Jones, T. A., J. Y. Zou, S. W. Cowan, and M. Kjeldgaard. 1991. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. Sect. D 47:110–119.
   PubMed Web of Science ®Google Scholar
• Kanemori, Y., K. Uto, and N. Sagata. 2005. β-TrCP recognizes a previously undescribed nonphosphorylated destruction motif in Cdc25A and Cdc25B phosphatases. Proc. Natl. Acad. Sci. USA 102:6279–6284.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Karin, M., and Y. Ben-Neriah. 2000. Phosphorylation meets ubiquitination: the control of NF-κB activity. Annu. Rev. Immunol. 18:621–663.
   PubMed Web of Science ®Google Scholar
• Katoh, Y., K. Iida, M. I. Kang, A. Kobayashi, M. Mizukami, K. I. Tong, M. McMahon, J. D. Hayes, K. Itoh, and M. Yamamoto. 2005. Evolutionary conserved N-terminal domain of Nrf2 is essential for the Keap1-mediated degradation of the protein by proteasome. Arch. Biochem. Biophys. 433:342–350.
   PubMed Web of Science ®Google Scholar
• Kim, W., and W. G. Kaelin, Jr. 2003. The von Hippel-Lindau tumor suppressor protein: new insights into oxygen sensing and cancer. Curr. Opin. Genet. Dev. 13:55–60.
   PubMed Web of Science ®Google Scholar
• Kobayashi, A., M. I. Kang, H. Okawa, M. Ohtsuji, Y. Zenke, T. Chiba, K. Igarashi, and M. Yamamoto. 2004. Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2. Mol. Cell. Biol. 24:7130–7139.
   PubMed Web of Science ®Google Scholar
• Kobayashi, A., M. I. Kang, Y. Watai, K. I. Tong, T. Shibata, K. Uchida, and M. Yamamoto. 2006. Oxidative and electrophilic stresses activate Nrf2 through inhibition of ubiquitination activity of Keap1. Mol. Cell. Biol. 26:221–229.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Lakowski, R. A., M. W. MacArthur, D. S. Moss, and J. M. Thornton. 1993. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26:283–291.
   Google Scholar
• Lo, S. C., X. Li, M. T. Henzl, L. J. Beamer, and M. Hannink. 2006. Structure of the Keap1:Nrf2 interface provides mechanistic insight into Nrf2 signaling. EMBO J. 25:3605–3617.
   PubMed Web of Science ®Google Scholar
• Maniatis, T. 1999. A ubiquitin ligase complex essential for the NF-κB, Wnt/Wingless, and Hedgehog signaling pathways. Genes Dev. 13:505–510.
   PubMedGoogle Scholar
• McMahon, M., N. Thomas, K. Itoh, M. Yamamoto, and J. D. Hayes. 2006. Dimerization of substrate adaptors can facilitate cullin-mediated ubiquitylation of proteins by a “tethering” mechanism: a two-site interaction model for the Nrf2-Keap1 complex. J. Biol. Chem. 281:24756–24768.
   PubMed Web of Science ®Google Scholar
• Motohashi, H., and M. Yamamoto. 2004. Nrf2-Keap1 defines a physiologically important stress response mechanism. Trends Mol. Med. 10:549–557.
   PubMed Web of Science ®Google Scholar
• Murshudov, G. N., A. A. Vagin, and E. J. Dodson. 1997. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. Sect. D 53:240–255.
   PubMed Web of Science ®Google Scholar
• Nash, P., X. Tang, S. Orlicky, Q. Chen, F. B. Gertler, M. D. Mendenhall, F. Sicheri, T. Pawson, and M. Tyers. 2001. Multisite phosphorylation of a CDK inhibitor sets a threshold for the onset of DNA replication. Nature 414:514–521.
   PubMed Web of Science ®Google Scholar
• Orlicky, S., X. Tang, A. Willems, M. Tyers, and F. Sicheri. 2003. Structural basis for phosphodependent substrate selection and orientation by the SCFCdc4 ubiquitin ligase. Cell 112:243–256.
   PubMed Web of Science ®Google Scholar
• Otwinowski, Z., and W. Minor. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:307–326.
   PubMed Web of Science ®Google Scholar
• Padmanabhan, B., M. Scharlock, K. I. Tong, Y. Nakamura, M. I. Kang, A. Kobayashi, T. Matsumoto, A. Tanaka, M. Yamamoto, and S. Yokoyama. 2005. Purification, crystallization and preliminary X-ray diffraction analysis of the Kelch-like motif region of mouse Keap1. Acta Crystallogr. Sect. F 61:153–155.
   PubMedGoogle Scholar
• Padmanabhan, B., K. I. Tong, T. Ohta, Y. Nakamura, M. Scharlock, M. Ohtsuji, M. I. Kang, A. Kobayashi, S. Yokoyama, and M. Yamamoto. 2006. Structural basis for defects of Keap1 activity provoked by its point mutations in lung cancer. Mol. Cell 21:689–700.
   PubMed Web of Science ®Google Scholar
• Pickart, C. M., and M. J. Eddins. 2004. Ubiquitin: structures, functions, mechanisms. Biochim. Biophys. Acta 1695:55–72.
   PubMed Web of Science ®Google Scholar
• Schofield, C. J., and P. J. Ratcliffe. 2005. Signalling hypoxia by HIF hydroxylases. Biochem. Biophys. Res. Commun. 338:617–626.
   PubMed Web of Science ®Google Scholar
• Semenza, G. L. 2000. HIF-1 and human disease: one highly involved factor. Genes Dev. 14:1983–1991.
   PubMed Web of Science ®Google Scholar
• Skowyra, D., K. L. Craig, M. Tyers, S. J. Elledge, and J. W. Harper. 1997. F-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin-ligase complex. Cell 91:209–219.
   PubMed Web of Science ®Google Scholar
• Tempé, D., M. Casas, S. Karaz, M. F. Blanchet-Tournier, and J. P. Concordet. 2006. Multisite protein kinase A and glycogen synthase kinase 3β phosphorylation leads to Gli3 ubiquitination by SCFβTrCP. Mol. Cell. Biol. 26:4316–4326.
   PubMed Web of Science ®Google Scholar
• Tong, K. I., Y. Katoh, H. Kusunoki, K. Itoh, T. Tanaka, and M. Yamamoto. 2006. Keap1 recruits Neh2 through binding to ETGE and DLG motifs: characterization of the two-site molecular recognition model. Mol. Cell. Biol. 26:2887–2900.
   PubMed Web of Science ®Google Scholar
• Tong, K. I., A. Kobayashi, F. Katsuoka, and M. Yamamoto. 2006. Two-site substrate recognition model for the Keap1-Nrf2 system: a hinge and latch mechanism. Biol. Chem. 387:1311–1320.
   PubMed Web of Science ®Google Scholar
• Watai, Y., A. Kobayashi, H. Nagase, M. Mizukami, K. Itoh, and M. Yamamoto. Subcellular localization and cytoplasmic complex status of endogenous Keap1. Genes Cells, in press.
   Google Scholar
• Watanabe, N., H. Arai, Y. Nishihara, M. Taniguchi, N. Watanabe, T. Hunter, and H. Osada. 2004. M-phase kinases induce phospho-dependent ubiquitination of somatic Wee1 by SCFβ-TrCP. Proc. Natl. Acad. Sci. USA 101:4419–4424.
   PubMed Web of Science ®Google Scholar
• Willems, A. R., T. Goh, L. Taylor, I. Chernushevich, A. Shevchenko, and M. Tyers. 1999. SCF ubiquitin protein ligases and phosphorylation-dependent proteolysis. Philos. Trans. R Soc. Lond. B 354:1533–1550.
   PubMedGoogle Scholar
• Winston, J. T., P. Strack, P. Beer-Romero, C. Y. Chu, S. J. Elledge, and J. W. Harper. 1999. The SCFβ-TRCP-ubiquitin ligase complex associates specifically with phosphorylated destruction motifs in IκBα and β-catenin and stimulates IκBα ubiquitination in vitro. Genes Dev. 13:270–283.
   PubMed Web of Science ®Google Scholar
• Zhang, D. D., S.-C. Lo, J. V. Cross, D. J. Templeton, and M. Hannink. 2004. Keap1 is a redox-regulated substrate adaptor protein for a Cul3-dependent ubiquitin ligase complex. Mol. Cell. Biol. 24:10941–10953.
   PubMed Web of Science ®Google Scholar