Direct Interaction between the WD40 Repeat Protein WDR-23 and SKN-1/Nrf Inhibits Binding to Target DNA

REFERENCES

• Sykiotis G, Bohmann D. 2010. Stress-activated cap‘n'collar transcription factors in aging and human disease. Sci. Signal. 3:re3.
   PubMed Web of Science ®Google Scholar
• Wakabayashi N, Itoh K, Wakabayashi J, Motohashi H, Noda S, Takahashi S, Imakado S, Kotsuji T, Otsuka F, Roop DR, Harada T, Engel JD, Yamamoto M. 2003. Keap1-null mutation leads to postnatal lethality due to constitutive Nrf2 activation. Nat. Genet. 35:238–245. http://dx.doi.org/10.1038/ng1248.
   PubMed Web of Science ®Google Scholar
• Leung CK, Wang Y, Deonarine A, Tang L, Prasse S, Choe KP. 2013. A negative feedback loop between the detoxification/antioxidant response factor SKN-1 and its repressor WDR-23 matches organism needs with environmental conditions. Mol. Cell. Biol. 33:3524–3537. http://dx.doi.org/10.1128/MCB.00245-13.
   PubMedGoogle Scholar
• Lee O-H, Jain AK, Papusha V, Jaiswal AK. 2007. An auto-regulatory loop between stress sensors INrf2 and Nrf2 controls their cellular abundance. J. Biol. Chem. 282:36412–36420. http://dx.doi.org/10.1074/jbc.M706517200.
   PubMed Web of Science ®Google Scholar
• Bryan HK, Olayanju A, Goldring CE, Park BK. 2013. The Nrf2 cell defence pathway: Keap1-dependent and -independent mechanisms of regulation. Biochem. Pharmacol. 85:705–717. http://dx.doi.org/10.1016/j.bcp.2012.11.016.
   PubMed Web of Science ®Google Scholar
• An JH, Vranas K, Lucke M, Inoue H, Hisamoto N, Matsumoto K, Blackwell TK. 2005. Regulation of the Caenorhabditis elegans oxidative stress defense protein SKN-1 by glycogen synthase kinase-3. Proc. Natl. Acad. Sci. U. S. A. 102:16275–16280. http://dx.doi.org/10.1073/pnas.0508105102.
   PubMed Web of Science ®Google Scholar
• An JH, Blackwell TK. 2003. SKN-1 links C. elegans mesendodermal specification to a conserved oxidative stress response. Genes Dev. 17:1882–1893. http://dx.doi.org/10.1101/gad.1107803.
   PubMed Web of Science ®Google Scholar
• Choe KP, Przybysz AJ, Strange K. 2009. The WD40 repeat protein WDR-23 functions with the CUL4/DDB1 ubiquitin ligase to regulate nuclear abundance and activity of SKN-1 in Caenorhabditis elegans. Mol. Cell. Biol. 29:2704–2715. http://dx.doi.org/10.1128/MCB.01811-08.
   PubMed Web of Science ®Google Scholar
• Lee J-S, Surh Y-J. 2005. Nrf2 as a novel molecular target for chemoprevention. Cancer Lett. 224:171–184. http://dx.doi.org/10.1016/j.canlet.2004.09.042.
   PubMed Web of Science ®Google Scholar
• Satoh T, Okamoto S-i, Cui J, Watanabe Y, Furuta K, Suzuki M, Tohyama K, Lipton SA. 2006. Activation of the Keap1/Nrf2 pathway for neuroprotection by electrophilic phase II inducers. Proc. Natl. Acad. Sci. U. S. A. 103:768–773. http://dx.doi.org/10.1073/pnas.0505723102.
   PubMed Web of Science ®Google Scholar
• Kundu JK, Surh YJ. 2010. Nrf2-Keap1 signaling as a potential target for chemoprevention of inflammation-associated carcinogenesis. Pharm. Res. 27:999–1013. http://dx.doi.org/10.1007/s11095-010-0096-8.
   PubMed Web of Science ®Google Scholar
• Bowerman B, Eaton BA, Priess JR. 1992. skn-1, a maternally expressed gene required to specify the fate of ventral blastomeres in the early Caenorhabditis elegans embryo. Cell 68:1061–1075. http://dx.doi.org/10.1016/0092-8674(92)90078-Q.
   PubMed Web of Science ®Google Scholar
• Tullet JMA, Hertweck M, An JH, Baker J, Hwang JY, Liu S, Oliveira RP, Baumeister R, Blackwell TK. 2008. Direct inhibition of the longevity-promoting factor SKN-1 by insulin-like signaling in Caenorhabditis elegans. Cell 132:1025–1038. http://dx.doi.org/10.1016/j.cell.2008.01.030.
   PubMed Web of Science ®Google Scholar
• Wang J, Robida-Stubbs S, Tullet JM, Rual JF, Vidal M, Blackwell TK. 2010. RNAi screening implicates a SKN-1-dependent transcriptional response in stress resistance and longevity deriving from translation inhibition. PLoS Genet. 6:e1001048. http://dx.doi.org/10.1371/journal.pgen.1001048.
   PubMedGoogle Scholar
• Robida-Stubbs S, Glover-Cutter K, Lamming DW, Mizunuma M, Narasimhan SD, Neumann-Haefelin E, Sabatini DM, Blackwell TK. 2012. TOR signaling and rapamycin influence longevity by regulating SKN-1/Nrf and DAF-16/FoxO. Cell Metab. 15:713–724. http://dx.doi.org/10.1016/j.cmet.2012.04.007.
   PubMed Web of Science ®Google Scholar
• Choe KP, Leung CK, Miyamoto MM. 2012. Unique structure and regulation of the nematode detoxification gene regulator, SKN-1: implications to understanding and controlling drug resistance. Drug Metab. Rev. 44:209–223. http://dx.doi.org/10.3109/03602532.2012.684799.
   PubMed Web of Science ®Google Scholar
• Leung CK, Wang Y, Malany S, Deonarine A, Nguyen K, Vasile S, Choe KP. 2013. An ultra-high-throughput, whole-animal screen for small molecule modulators of a specific genetic pathway in Caenorhabditis elegans. PLoS One 8:e62166. http://dx.doi.org/10.1371/journal.pone.0062166.
   PubMed Web of Science ®Google Scholar
• Glover-Cutter KM, Lin S, Blackwell TK. 2013. Integration of the unfolded protein and oxidative stress responses through SKN-1/Nrf. PLoS Genet. 9:e1003701. http://dx.doi.org/10.1371/journal.pgen.1003701.
   PubMedGoogle Scholar
• Bishop NA, Guarente L. 2007. Two neurons mediate diet-restriction-induced longevity in Caenorhabditis elegans. Nature 447:545–549. http://dx.doi.org/10.1038/nature05904.
   PubMed Web of Science ®Google Scholar
• Inoue H, Hisamoto N, An JH, Oliveira RP, Nishida E, Blackwell TK, Matsumoto K. 2005. The Caenorhabditis elegans p38 MAPK pathway regulates nuclear localization of the transcription factor SKN-1 in oxidative stress response. Genes Dev. 19:2278–2283. http://dx.doi.org/10.1101/gad.1324805.
   PubMed Web of Science ®Google Scholar
• Kell A, Ventura N, Kahn N, Johnson TE. 2007. Activation of SKN-1 by novel kinases in Caenorhabditis elegans. Free Rad Biol. Med. 43:1560–1566. http://dx.doi.org/10.1016/j.freeradbiomed.2007.08.025.
   PubMed Web of Science ®Google Scholar
• Okuyama T, Inoue H, Ookuma S, Satoh T, Kano K, Honjoh S, Hisamoto N, Matsumoto K, Nishida E. 2010. The ERK-MAPK pathway regulates longevity through SKN-1 and insulin-like signaling in Caenorhabditis elegans. J. Biol. Chem. 285:30274–30281. http://dx.doi.org/10.1074/jbc.M110.146274.
   PubMed Web of Science ®Google Scholar
• Hasegawa K, Miwa J. 2010. Genetic and cellular characterization of Caenorhabditis elegans mutants abnormal in the regulation of many phase II enzymes. PLoS One 5:e11194. http://dx.doi.org/10.1371/journal.pone.0011194.
   PubMed Web of Science ®Google Scholar
• Hasegawa K, Miwa J. 2010. Transcriptome analysis of the xrep-1(RNAi) phenocopy in Caenorhabditis elegans. Annu. Rep. Res. Inst. Biol. Funct. 10:72–80.
   Google Scholar
• Staab TA, Griffen TC, Corcoran C, Evgrafov O, Knowles JA, Sieburth D. 2013. The conserved SKN-1/Nrf2 stress response pathway regulates synaptic function in Caenorhabditis elegans. PLoS Genet. 9:e1003354. http://dx.doi.org/10.1371/journal.pgen.1003354.
   PubMedGoogle Scholar
• Stirnimann CU, Petsalaki E, Russell RB, Muller CW. 2010. WD40 proteins propel cellular networks. Trends Biochem. Sci. 35:565–574. http://dx.doi.org/10.1016/j.tibs.2010.04.003.
   PubMed Web of Science ®Google Scholar
• Suganuma T, Workman JL. 2010. WD40 repeats arrange histone tails for spreading of silencing. J. Mol. Cell. Biol. 2:81–83. http://dx.doi.org/10.1093/jmcb/mjp046.
   PubMedGoogle Scholar
• Migliori V, Mapelli M, Guccione E. 2012. On WD40 proteins: propelling our knowledge of transcriptional control? Epigenetics 7:815–822. http://dx.doi.org/10.4161/epi.21140.
   PubMed Web of Science ®Google Scholar
• Kahn NW, Rea SL, Moyle S, Kell A, Johnson TE. 2008. Proteasomal dysfunction activates the transcription factor SKN-1 and produces a selective oxidative-stress response in Caenorhabditis elegans. Biochem. J. 409:205–213. http://dx.doi.org/10.1042/BJ20070521.
   PubMed Web of Science ®Google Scholar
• Brenner S. 1974. The genetics of Caenorhabditis elegans. Genetics 77:71–94.
   PubMed Web of Science ®Google Scholar
• Maine EM, Kimble J. 1989. Identification of genes that interact with glp-1, a gene required for inductive cell interactions in Caenorhabditis elegans. Dev. 106:133–143.
   PubMedGoogle Scholar
• Abramoff MD, Magelhaes PJ, Ram SJ. 2004. Image processing with ImageJ. Biophotonics Int. 11:36–42.
   Google Scholar
• Hasegawa K, Miwa S, Tsutsumiuchi K, Miwa J. 2010. Allyl isothiocyanate that induces GST and UGT expression confers oxidative stress resistance on Caenorhabditis elegans, as demonstrated by nematode biosensor. PLoS One 5:e9267. http://dx.doi.org/10.1371/journal.pone.0009267.
   PubMed Web of Science ®Google Scholar
• Tops BB, Tabara H, Sijen T, Simmer F, Mello CC, Plasterk RH, Ketting RF. 2005. RDE-2 interacts with MUT-7 to mediate RNA interference in Caenorhabditis elegans. Nucleic Acids Res. 33:347–355. http://dx.doi.org/10.1093/nar/gki183.
   PubMedGoogle Scholar
• Kelley LA, Sternberg MJ. 2009. Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4:363–371. http://dx.doi.org/10.1038/nprot.2009.2.
   PubMed Web of Science ®Google Scholar
• Hall DH, Altun ZF. 2008. Caenorhabditis elegans atlas. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
   Google Scholar
• Oliveira RP, Abate JP, Dilks K, Landis J, Ashraf J, Murphy CT, Blackwell TK. 2009. Condition-adapted stress and longevity gene regulation by Caenorhabditis elegans SKN-1/Nrf. Aging Cell 8:524–541. http://dx.doi.org/10.1111/j.1474-9726.2009.00501.x.
   PubMed Web of Science ®Google Scholar
• Paek J, Lo JY, Narasimhan SD, Nguyen TN, Glover-Cutter K, Robida-Stubbs S, Suzuki T, Yamamoto M, Blackwell TK, Curran SP. 2012. Mitochondrial SKN-1/Nrf mediates a conserved starvation response. Cell Metab. 16:526–537. http://dx.doi.org/10.1016/j.cmet.2012.09.007.
   PubMedGoogle Scholar
• Leung CK, Empinado H, Choe KP. 2012. Depletion of a nucleolar protein activates xenobiotic detoxification genes in Caenorhabditis elegans via Nrf/SKN-1 and p53/CEP-1. Free Radic. Biol. Med. 52:937–950. http://dx.doi.org/10.1016/j.freeradbiomed.2011.12.009.
   PubMedGoogle Scholar
• Bowerman B, Draper BW, Mello CC, Priess JR. 1993. The maternal gene skn-1 encodes a protein that is distributed unequally in early Caenorhabditis elegans embryos. Cell 74:443–452. http://dx.doi.org/10.1016/0092-8674(93)80046-H.
   PubMedGoogle Scholar
• Arnold K, Bordoli L, Kopp J, Schwede T. 2006. The SWISS-MODEL workspace: a web-based environment for protein structure homology modeling. Bioinformatics 22:195–201. http://dx.doi.org/10.1093/bioinformatics/bti770.
   PubMed Web of Science ®Google Scholar
• Bordoli L, Kiefer F, Arnold K, Benkert P, Battey J, Schwede T. 2009. Protein structure homology modeling using SWISS-MODEL workspace. Nat. Protoc. 4:1–13.
   PubMed Web of Science ®Google Scholar
• Kiefer F, Arnold K, Kunzli M, Bordoli L, Schwede T. 2009. The SWISS-MODEL repository and associated resources. Nucleic Acids Res. 37:D387–D392. http://dx.doi.org/10.1093/nar/gkn750.
   PubMed Web of Science ®Google Scholar
• Bordoli L, Schwede T. 2012. Automated protein structure modeling with SWISS-MODEL workspace and the protein model portal. Methods Mol. Biol. 857:107–136. http://dx.doi.org/10.1007/978-1-61779-588-6_5.
   PubMedGoogle Scholar
• Wu XH, Wang Y, Zhuo Z, Jiang F, Wu YD. 2012. Identifying the hot spots on the top faces of WD40-repeat proteins from their primary sequences by beta-bulges and DHSW tetrads. PLoS One 7:e43005. http://dx.doi.org/10.1371/journal.pone.0043005.
   PubMed Web of Science ®Google Scholar
• Rupert PB, Daughdrill GW, Bowerman B, Matthews BW. 1998. A new DNA-binding motif in the Skn-1 binding domain-DNA complex. Nat. Struct. Biol. 5:484–491. http://dx.doi.org/10.1038/nsb0698-484.
   PubMedGoogle Scholar
• Curran SP, Ruvkun G. 2007. Lifespan regulation by evolutionarily conserved genes essential for viability. PLoS Genet. 3:e56. http://dx.doi.org/10.1371/journal.pgen.0030056.
   PubMed Web of Science ®Google Scholar
• Rodriguez CE, Shinyashiki M, Froines J, Yu RC, Fukuto JM, Cho AK. 2004. An examination of quinone toxicity using the yeast Saccharomyces cerevisiae model system. J. Toxicol. 201:185–196. http://dx.doi.org/10.1016/j.tox.2004.04.016.
   Google Scholar
• Aithal KB, Kumar S, Rao BN, Udupa N, Rao SB. 2011. Tumor growth inhibitory effect of juglone and its radiation sensitizing potential: in vivo and in vitro studies. Integr. Cancer Ther. 11:68–80. http://dx.doi.org/10.1177/1534735411403477.
   PubMedGoogle Scholar
• Blackwell TK, Bowerman B, Priess JR, Weintraub H. 1994. Formation of a monomeric DNA binding domain by SKN-1 bZIP and homeodomain elements. Science 266:621–628. http://dx.doi.org/10.1126/science.7939715.
   PubMed Web of Science ®Google Scholar
• Brouette C, Betz N, Kobs G. 2002. Optimized gene expression with the T7 sample system. Promega Notes 80:10–13.
   Google Scholar
• Walker AK, See R, Batchelder C, Kophengnavong T, Gronniger JT, Shi Y, Blackwell TK. 2000. A conserved transcription motif suggesting functional parallels between Caenorhabditis elegans SKN-1 and cap‘n'collar-related basic leucine zipper proteins. J. Biol. Chem. 275:22166–22171. http://dx.doi.org/10.1074/jbc.M001746200.
   PubMedGoogle Scholar
• McMahon M, Thomas N, Itoh K, Yamamoto M, Hayes JD. 2004. Redox-regulated turnover of Nrf2 is determined by at least two separate protein domains, the redox-sensitive neh2 degron and the redox-insensitive neh6 degron. J. Biol. Chem. 279:31556–31567. http://dx.doi.org/10.1074/jbc.M403061200.
   PubMed Web of Science ®Google Scholar
• Chan JY, Kwong M, Lu R, Chang J, Wang B, Yen TSB, Kan YW. 1998. Targeted disruption of the ubiquitous CNC-bZIP transcription factor, Nrf-1, results in anemia and embryonic lethality in mice. EMBO J. 17:1779–1787. http://dx.doi.org/10.1093/emboj/17.6.1779.
   PubMed Web of Science ®Google Scholar
• Han W, Ming M, Zhao R, Pi J, Wu C, He YY. 2012. Nrf1 CNC-bZIP protein promotes cell survival and nucleotide excision repair through maintaining glutathione homeostasis. J. Biol. Chem. 287:18788–18795. http://dx.doi.org/10.1074/jbc.M112.363614.
   PubMedGoogle Scholar
• Chen L, Kwong M, Lu R, Ginzinger D, Lee C, Leung L, Chan JY. 2003. Nrf1 is critical for redox balance and survival of liver cells during development. Mol. Cell. Biol. 23:4673–4686. http://dx.doi.org/10.1128/MCB.23.13.4673-4686.2003.
   PubMed Web of Science ®Google Scholar
• Lee CS, Lee C, Hu T, Nguyen JM, Zhang J, Martin MV, Vawter MP, Huang EJ, Chan JY. 2011. Loss of nuclear factor E2-related factor 1 in the brain leads to dysregulation of proteasome gene expression and neurodegeneration. Proc. Natl. Acad. Sci. U. S. A. 108:8408–8413. http://dx.doi.org/10.1073/pnas.1019209108.
   PubMed Web of Science ®Google Scholar
• Biswas M, Phan D, Watanabe M, Chan JY. 2011. The Fbw7 tumor suppressor regulates nuclear factor E2-related factor 1 transcription factor turnover through proteasome-mediated proteolysis. J. Biol. Chem. 286:39282–39289. http://dx.doi.org/10.1074/jbc.M111.253807.
   PubMed Web of Science ®Google Scholar
• Tsuchiya Y, Morita T, Kim M, Iemura S, Natsume T, Yamamoto M, Kobayashi A. 2011. Dual regulation of the transcriptional activity of Nrf1 by beta-TrCP- and Hrd1-dependent degradation mechanisms. Mol. Cell. Biol. 31:4500–4512. http://dx.doi.org/10.1128/MCB.05663-11.
   PubMed Web of Science ®Google Scholar
• Angers S, Li T, Yi X, MacCoss MJ, Moon RT, Zheng N. 2006. Molecular architecture and assembly of the DDB1-CUL4A ubiquitin ligase machinery. Nature 443:590–593. http://dx.doi.org/10.1038/nature05175.
   PubMed Web of Science ®Google Scholar
• Lee J-H, Terzaghi W, Gusmaroli G, Charron J-BF, Yoon H-J, Chen H, He YJ, Xiong Y, Deng XW. 2008. Characterization of Arabidopsis and rice DWD proteins and their roles as substrate receptors for CUL4-RING E3 ubiquitin ligases. Plant Cell 20:152–167. http://dx.doi.org/10.1105/tpc.107.055418.
   PubMed Web of Science ®Google Scholar
• Aiken CT, Kaake RM, Wang X, Huang L. 2011. Oxidative stress-mediated regulation of proteasome complexes. Mol. Cell. Proteomics 10:R110.006924. http://dx.doi.org/10.1074/mcp.M110.006924.
   PubMed Web of Science ®Google Scholar