Basic Leucine Zipper Protein Cnc-C Is a Substrate and Transcriptional Regulator of the Drosophila 26S Proteasome

REFERENCES

• Anisimova, M., and O. Gascuel. 2006. Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst. Biol. 55:539–552.
   PubMed Web of Science ®Google Scholar
• Beedholm, R., B. F. Clark, and S. I. Rattan. 2004. Mild heat stress stimulates 20S proteasome and its 11S activator in human fibroblasts undergoing aging in vitro. Cell Stress Chaperones 9:49–57.
   PubMedGoogle Scholar
• Beskow, A., et al. 2009. A conserved unfoldase activity for the p97 AAA-ATPase in proteasomal degradation. J. Mol. Biol. 394:732–746.
   PubMed Web of Science ®Google Scholar
• Chan, J. Y., et al. 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.
   PubMed Web of Science ®Google Scholar
• Chan, K., R. Lu, J. C. Chang, and Y. W. Kan. 1996. NRF2, a member of the NFE2 family of transcription factors, is not essential for murine erythropoiesis, growth, and development. Proc. Natl. Acad. Sci. U. S. A. 93:13943–13948.
   PubMed Web of Science ®Google 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
• Dahlmann, B. 2007. Role of proteasomes in disease. BMC Biochem. 8 (Suppl. 1):S3.
   PubMed Web of Science ®Google Scholar
• Dantuma, N. P., K. Lindsten, R. Glas, M. Jellne, and M. G. Masucci. 2000. Short-lived green fluorescent proteins for quantifying ubiquitin/proteasome-dependent proteolysis in living cells. Nat. Biotechnol. 18:538–543.
   PubMed Web of Science ®Google Scholar
• DasGupta, R., and F. C. Gonsalves. 2008. High-throughput RNAi screen in Drosophila. Methods Mol. Biol. 469:163–184.
   PubMedGoogle Scholar
• Do, C. B., M. S. Mahabhashyam, M. Brudno, and S. Batzoglou. 2005. ProbCons: probabilistic consistency-based multiple sequence alignment. Genome Res. 15:330–340.
   PubMed Web of Science ®Google Scholar
• Dohmen, R. J., I. Willers, and A. J. Marques. 2007. Biting the hand that feeds: Rpn4-dependent feedback regulation of proteasome function. Biochim. Biophys. Acta 1773:1599–1604.
   PubMedGoogle Scholar
• Farmer, S. C., C. W. Sun, G. E. Winnier, B. L. Hogan, and T. M. Townes. 1997. The bZIP transcription factor LCR-F1 is essential for mesoderm formation in mouse development. Genes Dev. 11:786–798.
   PubMedGoogle Scholar
• Felsenstein, J. 1978. Cases in which parsimony or compatibility methods will be positively misleading. Syst. Zool. 27:401–410.
   Google Scholar
• Fuchs, D., C. Berges, G. Opelz, V. Daniel, and C. Naujokat. 2008. Increased expression and altered subunit composition of proteasomes induced by continuous proteasome inhibition establish apoptosis resistance and hyperproliferation of Burkitt lymphoma cells. J. Cell. Biochem. 103:270–283.
   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
• Giot, L., et al. 2003. A protein interaction map of Drosophila melanogaster. Science 302:1727–1736.
   PubMed Web of Science ®Google Scholar
• Glickman, M. H., and A. Ciechanover. 2002. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol. Rev. 82:373–428.
   PubMed Web of Science ®Google Scholar
• Groll, M., et al. 2000. A gated channel into the proteasome core particle. Nat. Struct. Biol. 7:1062–1067.
   PubMedGoogle Scholar
• Guindon, S., and O. Gascuel. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52:696–704.
   PubMed Web of Science ®Google Scholar
• Hordijk, W., and O. Gascuel. 2005. Improving the efficiency of SPR moves in phylogenetic tree search methods based on maximum likelihood. Bioinformatics 21:4338–4347.
   PubMed Web of Science ®Google Scholar
• Itoh, K., K. Igarashi, N. Hayashi, M. Nishizawa, and M. Yamamoto. 1995. Cloning and characterization of a novel erythroid cell-derived CNC family transcription factor heterodimerizing with the small Maf family proteins. Mol. Cell. Biol. 15:4184–4193.
   PubMed Web of Science ®Google Scholar
• Johnsen, O., P. Murphy, H. Prydz, and A. B. Kolsto. 1998. Interaction of the CNC-bZIP factor TCF11/LCR-F1/Nrf1 with MafG: binding-site selection and regulation of transcription. Nucleic Acids Res. 26:512–520.
   PubMed Web of Science ®Google Scholar
• Kapranov, A. B., et al. 2001. Isolation and identification of PACE-binding protein rpn4: a new transcription activator, participating in regulation of 26S proteosome and other genes. Mol. Biol. (Mosk.) 35:420–431. (In Russian.)
   PubMedGoogle Scholar
• Kobayashi, A., et al. 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, M., et al. 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
• Kumatori, A., et al. 1990. Abnormally high expression of proteasomes in human leukemic cells. Proc. Natl. Acad. Sci. U. S. A. 87:7071–7075.
   PubMed Web of Science ®Google Scholar
• Kwak, M. K., N. Wakabayashi, J. L. Greenlaw, M. Yamamoto, and T. W. Kensler. 2003. Antioxidants enhance mammalian proteasome expression through the Keap1-Nrf2 signaling pathway. Mol. Cell. Biol. 23:8786–8794.
   PubMed Web of Science ®Google Scholar
• Le, S. Q., and O. Gascuel. 2008. An improved general amino acid replacement matrix. Mol. Biol. Evol. 25:1307–1320.
   PubMed Web of Science ®Google Scholar
• Lundgren, J., P. Masson, Z. Mirzaei, and P. Young. 2005. Identification and characterization of a Drosophila proteasome regulatory network. Mol. Cell. Biol. 25:4662–4675.
   PubMed Web of Science ®Google Scholar
• Mannhaupt, G., and H. Feldmann. 2007. Genomic evolution of the proteasome system among hemiascomycetous yeasts. J. Mol. Evol. 65:529–540.
   PubMedGoogle Scholar
• Mannhaupt, G., R. Schnall, V. Karpov, I. Vetter, and H. Feldmann. 1999. Rpn4p acts as a transcription factor by binding to PACE, a nonamer box found upstream of 26S proteasomal and other genes in yeast. FEBS Lett. 450:27–34.
   PubMed Web of Science ®Google Scholar
• Mayor, T., J. Graumann, J. Bryan, M. J. MacCoss, and R. J. Deshaies. 2007. Quantitative profiling of ubiquitylated proteins reveals proteasome substrates and the substrate repertoire influenced by the Rpn10 receptor pathway. Mol. Cell. Proteomics 6:1885–1895.
   PubMedGoogle Scholar
• McGinnis, N., E. Ragnhildstveit, A. Veraksa, and W. McGinnis. 1998. A cap 'n’ collar protein isoform contains a selective Hox repressor function. Development 125:4553–4564.
   PubMedGoogle Scholar
• Meiners, S., et al. 2003. Inhibition of proteasome activity induces concerted expression of proteasome genes and de novo formation of mammalian proteasomes. J. Biol. Chem. 278:21517–21525.
   PubMed Web of Science ®Google Scholar
• Mohler, J., J. W. Mahaffey, E. Deutsch, and K. Vani. 1995. Control of Drosophila head segment identity by the bZIP homeotic gene cnc. Development 121:237–247.
   PubMedGoogle Scholar
• Mohler, J., K. Vani, S. Leung, and A. Epstein. 1991. Segmentally restricted, cephalic expression of a leucine zipper gene during Drosophila embryogenesis. Mech. Dev. 34:3–9.
   PubMedGoogle Scholar
• Nioi, P., M. McMahon, K. Itoh, M. Yamamoto, and J. D. Hayes. 2003. Identification of a novel Nrf2-regulated antioxidant response element (ARE) in the mouse NAD(P)H:quinone oxidoreductase 1 gene: reassessment of the ARE consensus sequence. Biochem. J. 374:337–348.
   PubMed Web of Science ®Google Scholar
• Nouhi, Z., G. Chevillard, A. Derjuga, and V. Blank. 2007. Endoplasmic reticulum association and N-linked glycosylation of the human Nrf3 transcription factor. FEBS Lett. 581:5401–5406.
   PubMedGoogle Scholar
• Oyake, T., et al. 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.
   PubMed Web of Science ®Google Scholar
• Rabl, J., et al. 2008. Mechanism of gate opening in the 20S proteasome by the proteasomal ATPases. Mol. Cell 30:360–368.
   PubMedGoogle Scholar
• Radhakrishnan, S. K., et al. 2010. Transcription factor Nrf1 mediates the proteasome recovery pathway after proteasome inhibition in mammalian cells. Mol. Cell 38:17–28.
   PubMed Web of Science ®Google Scholar
• Ramadan, N., I. Flockhart, M. Booker, N. Perrimon, and B. Mathey-Prevot. 2007. Design and implementation of high-throughput RNAi screens in cultured Drosophila cells. Nat. Protoc. 2:2245–2264.
   PubMed Web of Science ®Google Scholar
• Richardson, P. G., T. Hideshima, and K. C. Anderson. 2003. Bortezomib (PS-341): a novel, first-in-class proteasome inhibitor for the treatment of multiple myeloma and other cancers. Cancer Control 10:361–369.
   PubMedGoogle Scholar
• Shah, J. J., and R. Z. Orlowski. 2009. Proteasome inhibitors in the treatment of multiple myeloma. Leukemia 23:1964–1979.
   PubMed Web of Science ®Google Scholar
• Steffen, J., M. Seeger, A. Koch, and E. Kruger. 2010. Proteasomal degradation is transcriptionally controlled by TCF11 via an ERAD-dependent feedback loop. Mol. Cell 40:147–158.
   PubMed Web of Science ®Google Scholar
• Sykiotis, G. P., and D. Bohmann. 2008. Keap1/Nrf2 signaling regulates oxidative stress tolerance and lifespan in Drosophila. Dev. Cell 14:76–85.
   PubMed Web of Science ®Google Scholar
• Sykiotis, G. P., and D. Bohmann. 2010. Stress-activated cap'n'collar transcription factors in aging and human disease. Sci. Signal. 3:re3.
   PubMed Web of Science ®Google Scholar
• Szlanka, T., et al. 2003. Deletion of proteasomal subunit S5a/Rpn10/p54 causes lethality, multiple mitotic defects and overexpression of proteasomal genes in Drosophila melanogaster. J. Cell Sci. 116:1023–1033.
   PubMed Web of Science ®Google Scholar
• Taylor, D. M., E. Kabashi, J. N. Agar, S. Minotti, and H. D. Durham. 2005. Proteasome activity or expression is not altered by activation of the heat shock transcription factor Hsf1 in cultured fibroblasts or myoblasts. Cell Stress Chaperones 10:230–241.
   PubMedGoogle Scholar
• Venugopal, R., and A. K. Jaiswal. 1996. Nrf1 and Nrf2 positively and c-Fos and Fra1 negatively regulate the human antioxidant response element-mediated expression of NAD(P)H:quinone oxidoreductase1 gene. Proc. Natl. Acad. Sci. U. S. A. 93:14960–14965.
   PubMed Web of Science ®Google Scholar
• Veraksa, A., N. McGinnis, X. Li, J. Mohler, and W. McGinnis. 2000. Cap 'n’ collar B cooperates with a small Maf subunit to specify pharyngeal development and suppress deformed homeotic function in the Drosophila head. Development 127:4023–4037.
   PubMedGoogle Scholar
• Verma, R., R. Oania, J. Graumann, and R. J. Deshaies. 2004. Multiubiquitin chain receptors define a layer of substrate selectivity in the ubiquitin-proteasome system. Cell 118:99–110.
   PubMed Web of Science ®Google Scholar
• Xie, Y., and A. Varshavsky. 2001. RPN4 is a ligand, substrate, and transcriptional regulator of the 26S proteasome: a negative feedback circuit. Proc. Natl. Acad. Sci. U. S. A. 98:3056–3061.
   PubMed Web of Science ®Google Scholar
• Xu, Z., et al. 2005. Liver-specific inactivation of the Nrf1 gene in adult mouse leads to nonalcoholic steatohepatitis and hepatic neoplasia. Proc. Natl. Acad. Sci. U. S. A. 102:4120–4125.
   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
• Zhang, Y., D. H. Crouch, M. Yamamoto, and J. D. Hayes. 2006. Negative regulation of the Nrf1 transcription factor by its N-terminal domain is independent of Keap1: Nrf1, but not Nrf2, is targeted to the endoplasmic reticulum. Biochem. J. 399:373–385.
   PubMedGoogle Scholar
• Zhang, Y., J. M. Lucocq, M. Yamamoto, and J. D. Hayes. 2007. The NHB1 (N-terminal homology box 1) sequence in transcription factor Nrf1 is required to anchor it to the endoplasmic reticulum and also to enable its asparagine-glycosylation. Biochem. J. 408:161–172.
   PubMed Web of Science ®Google Scholar