Direct interaction between the WD40 repeat protein WDR-23 and SKN-1/Nrf inhibits binding to target DNA

Molecular and Cellular Biology

Volumn 34, Issue 16, 2014, Pages 3156-3167

  Leung, Chi K ^a   Hasegawa, Koichi ^b   Wang, Ying ^a   Deonarine, Andrew ^a   Tang, Lanlan ^a   Miwa, Johji ^b   Choea, Keith P ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b CHUBU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEASOME; PROTEIN; PROTEIN VARIANT; PROTEIN WDR 23; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NRF1; TRANSCRIPTION FACTOR NRF2; TRANSCRIPTION FACTOR SKN 1; UBIQUITIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BETA SHEET; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DNA SEQUENCE; MISSENSE MUTATION; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN DNA INTERACTION; PROTEIN FOLDING; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; REGULATORY MECHANISM; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; STRESS; XENOBIOTIC METABOLISM;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DNA, PROTOZOAN; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; LARVA; LONGEVITY; PROTEIN BINDING; PROTEIN FOLDING; REPRESSOR PROTEINS; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS;

EID: 84904489105     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00114-14     Document Type: Article

References (62)

1. Sykiotis G, Bohmann D. 2010. Stress-activated cap'n'collar transcription factors in aging and human disease. Sci. Signal. 3:re3.
2. 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.
3. 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.
4. 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.
5. 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.
6. 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.
7. 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.
8. 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.
9. 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.
10. 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.
11. 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.
12. 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.
13. Tullet JMA, Hertweck M, An JH, Baker J, Hwang JY, Liu S, Oliveira RP, Baumeister R, Blackwell TK. 2008. Direct inhibition of the longevitypromoting 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.
14. Wang J, Robida-Stubbs S, Tullet JM, Rual JF, Vidal M, Blackwell TK. 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.
15. Robida-Stubbs S, Glover-Cutter K, Lamming DW, Mizunuma M, Narasimhan SD, Neumann-Haefelin E, Sabatini DM, Blackwell TK. 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.
16. 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.
17. 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.
18. 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.
19. Bishop NA, Guarente L. 2007. Two neurons mediate diet-restrictioninduced longevity in Caenorhabditis elegans. Nature 447:545-549. http://dx.doi.org/10.1038/nature05904.
20. 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.
21. 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.
22. 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.
23. 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.
24. 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.
25. 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.
26. 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.
27. 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.
28. 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.
29. 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.
30. Brenner S. 1974. The genetics of Caenorhabditis elegans. Genetics 77:71-94.
31. 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.
32. AbramoffMD, Magelhaes PJ, Ram SJ. 2004. Image processing with ImageJ. Biophotonics Int. 11:36-42.
33. 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.
34. 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.
35. 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.
36. Hall DH, Altun ZF. 2008. Caenorhabditis elegans atlas. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
37. 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.
38. 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.
39. 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.
40. 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.
41. 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.
42. 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.
43. Kiefer F, Arnold K, Kunzli M, Bordoli L, Schwede T. 2009. The SWISSMODEL repository and associated resources. Nucleic Acids Res. 37: D387-D392. http://dx.doi.org/10.1093/nar/gkn750.
44. 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.
45. 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.
46. 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.
47. 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.
48. Rodriguez CE, Shinyashiki M, Froines J, Yu RC, Fukuto JM, Cho AK. 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.
49. 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.
50. 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.
51. Brouette C, Betz N, Kobs G. 2002. Optimized gene expression with the T7 sample system. Promega Notes 80:10-13.
52. 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'collarrelated basic leucine zipper proteins. J. Biol. Chem. 275:22166-22171. http://dx.doi.org/10.1074/jbc. M001746200.
53. 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 redoxinsensitive neh6 degron. J. Biol. Chem. 279:31556-31567. http://dx.doi.org/10.1074/jbc. M403061200.
54. 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.
55. 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.
56. 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.
57. 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.
58. 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.
59. 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.
60. 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.
61. 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.
62. Aiken CT, Kaake RM, Wang X, Huang L. 2011. Oxidative stressmediated regulation of proteasome complexes. Mol. Cell. Proteomics 10: R110.006924. http://dx.doi.org/10.1074/mcp. M110.006924.