Repression of yeast RNA polymerase III by stress leads to ubiquitylation and proteasomal degradation of its largest subunit, C160

Ewa Leśniewska1, Małgorzata Cieśla1, Magdalena Boguta1
1Department of Genetics, Institute of Biochemistry and Biophysics, Polish Academy of Sciences, Pawińskiego 5a, 02-106 Warsaw, Poland

Tài liệu tham khảo

Buratowski, 2009, Progression through the RNA polymerase II CTD cycle, Mol. Cell, 36, 541, 10.1016/j.molcel.2009.10.019 Hoffmann, 2015, Molecular structures of unbound and transcribing RNA polymerase III, Nature, 528, 231, 10.1038/nature16143 Bregman, 1996, UV-induced ubiquitination of RNA polymerase II: a novel modification deficient in Cockayne syndrome cells, Proc. Natl. Acad. Sci., 93, 11586, 10.1073/pnas.93.21.11586 Ratner, 1998, Ultraviolet radiation-induced ubiquitination and proteasomal degradation of the large subunit of rna polymerase II: implications for transcription-coupled DNA repair, J. Biol. Chem., 273, 5184, 10.1074/jbc.273.9.5184 Gillette, 2004, Physical and functional association of RNA polymerase II and the proteasome, Proc. Natl. Acad. Sci., 101, 5904, 10.1073/pnas.0305411101 Auld, 2006, Genomic association of the proteasome demonstrates overlapping gene regulatory activity with transcription factor substrates, Mol. Cell, 21, 861, 10.1016/j.molcel.2006.02.020 Kvint, 2008, Reversal of RNA polymerase II ubiquitylation by the ubiquitin protease Ubp3, Mol. Cell, 30, 498, 10.1016/j.molcel.2008.04.018 Wilson, 2013, Ubiquitylation and degradation of elongating RNA polymerase II: the last resort, Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms., 1829, 151, 10.1016/j.bbagrm.2012.08.002 Huibregtse, 1997, The large subunit of RNA polymerase II is a substrate of the Rsp5 ubiquitin-protein ligase, Proc. Natl. Acad. Sci., 94, 3656, 10.1073/pnas.94.8.3656 Mitsui, 1999, Ubiquitination of RNA polymerase II large subunit signaled by phosphorylation of carboxyl-terminal domain, Proc. Natl. Acad. Sci., 96, 6054, 10.1073/pnas.96.11.6054 Somesh, 2005, Multiple mechanisms confining RNA polymerase II ubiquitylation to polymerases undergoing transcriptional arrest, Cell, 121, 913, 10.1016/j.cell.2005.04.010 Somesh, 2007, Communication between distant sites in RNA polymerase II through ubiquitylation factors and the polymerase CTD, Cell, 129, 57, 10.1016/j.cell.2007.01.046 Anindya, 2007, Damage-induced ubiquitylation of human RNA polymerase II by the ubiquitin ligase Nedd4, but not cockayne syndrome proteins or BRCA1, Mol. Cell, 28, 386, 10.1016/j.molcel.2007.10.008 Harreman, 2009, Distinct ubiquitin ligases act sequentially for RNA polymerase II polyubiquitylation, Proc. Natl. Acad. Sci., 106, 20705, 10.1073/pnas.0907052106 Lafon, 2015, INO80 chromatin remodeler facilitates release of RNA polymerase II from chromatin for ubiquitin-mediated proteasomal degradation, Mol. Cell, 60, 784, 10.1016/j.molcel.2015.10.028 Jouvet, 2011, RNA polymerase II degradation in response to rapamycin is not mediated through ubiquitylation, Biochem. Biophys. Res. Commun., 413, 248, 10.1016/j.bbrc.2011.08.079 Richardson, 2012, A conserved deubiquitinating enzyme controls cell growth by regulating RNA polymerase I stability, Cell Rep., 2, 372, 10.1016/j.celrep.2012.07.009 Peltonen, 2014, A targeting modality for destruction of RNA polymerase I that possesses anticancer activity, Cancer Cell, 25, 77, 10.1016/j.ccr.2013.12.009 Tsang, 2003, Chromatin-mediated regulation of nucleolar structure and RNA Pol I localization by TOR, EMBO J., 22, 6045, 10.1093/emboj/cdg578 Graczyk, 2018, Regulation of tRNA synthesis by the general transcription factors of RNA polymerase III - TFIIIB and TFIIIC, and by the MAF1 protein, Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms., 1861, 320, 10.1016/j.bbagrm.2018.01.011 Pluta, 2001, Maf1p, a negative effector of RNA polymerase III in Saccharomyces cerevisiae, Mol. Cell. Biol., 21, 5031, 10.1128/MCB.21.15.5031-5040.2001 Upadhya, 2002, Maf1 is an essential mediator of diverse signals that repress RNA polymerase III transcription, Mol. Cell, 10, 1489, 10.1016/S1097-2765(02)00787-6 Graczyk, 2011, Casein kinase II-mediated phosphorylation of general repressor Maf1 triggers RNA polymerase III activation, PNAS, 108, 4926, 10.1073/pnas.1010010108 Ciesla, 2018, Function of TFIIIC, RNA polymerase III initiation factor, in activation and repression of tRNA gene transcription, Nucleic Acids Res. Wang, 2018, Defective RNA polymerase III is negatively regulated by the SUMO-ubiquitin-Cdc48 pathway, elife, 7, 10.7554/eLife.35447 Bonneaud, 1991, A family of low and high copy replicative, integrative and single-stranded S. cerevisiae/E. coli shuttle vectors, Yeast, 7, 609, 10.1002/yea.320070609 Morvan, 2004, The ubiquitin ligase Rsp5p is required for modification and sorting of membrane proteins into multivesicular bodies, Traffic, 383, 10.1111/j.1398-9219.2004.00183.x Towpik, 2008, Derepression of RNA polymerase III transcription by phosphorylation and nuclear export of its negative regulator, Maf1, J. Biol. Chem., 283, 17168, 10.1074/jbc.M709157200 Kaiser, 2005, Is this protein ubiquitinated?, 243, 10.1016/S0076-6879(05)99016-2 Cieśla, 2015, Rbs1, a new protein implicated in RNA polymerase III biogenesis in yeast Saccharomyces cerevisiae, Mol. Cell. Biol., 35, 1169, 10.1128/MCB.01230-14 Ren, 2000, Genome-wide location and function of DNA binding proteins, Science, 290, 2306, 10.1126/science.290.5500.2306 Foretek, 2016, Control of Saccharomyces cerevisiae pre-tRNA processing by environmental conditions, RNA, 22, 339, 10.1261/rna.054973.115 Wu, 2013, A rapid and sensitive non-radioactive method applicable for genome-wide analysis of Saccharomyces cerevisiae genes involved in small RNA biology, Yeast, 30, 119, 10.1002/yea.2947 Chymkowitch, 2017, TORC1-dependent sumoylation of Rpc82 promotes RNA polymerase III assembly and activity, Proc. Natl. Acad. Sci. U. S. A., 10.1073/pnas.1615093114 Boguta, 2013, Maf1, a general negative regulator of RNA polymerase III in yeast, Biochim. Biophys. Acta, 1829, 376, 10.1016/j.bbagrm.2012.11.004 Oficjalska-Pham, 2006, General repression of RNA polymerase III transcription is triggered by protein phosphatase type 2A-mediated dephosphorylation of Maf1, Mol. Cell, 22, 623, 10.1016/j.molcel.2006.04.008 Exinger, 1992, 6-Azauracil inhibition of GTP biosynthesis in Saccharomyces cerevisiae, Curr. Genet., 22, 9, 10.1007/BF00351735 Escobar-Henriques, 2001, Proteome analysis and morphological studies reveal multiple effects of the immunosuppressive drug mycophenolic acid specifically resulting from Guanylic nucleotide depletion, J. Biol. Chem., 276, 46237, 10.1074/jbc.M103416200 Gómez-Herreros, 2013, Balanced production of ribosome components is required for proper G1/S transition in Saccharomyces cerevisiae, J. Biol. Chem., 288, 31689, 10.1074/jbc.M113.500488 Shaw, 2000, Saccharomyces cerevisiae transcription elongation mutants are defective in PUR5 induction in response to nucleotide depletion, Mol. Cell. Biol., 20, 7427, 10.1128/MCB.20.20.7427-7437.2000 Kwapisz, 2008, Mutations of RNA polymerase II activate key genes of the nucleoside triphosphate biosynthetic pathways, EMBO J., 27, 2411, 10.1038/emboj.2008.165 Cieśla, 2007, Maf1 is involved in coupling carbon metabolism to RNA polymerase III transcription, Mol. Cell. Biol., 27, 7693, 10.1128/MCB.01051-07 Karkusiewicz, 2011, Maf1 protein, repressor of RNA polymerase III, indirectly affects tRNA processing, J. Biol. Chem., 286, 39478, 10.1074/jbc.M111.253310 Mayor, 2007, Quantitative profiling of ubiquitylated proteins reveals proteasome substrates and the substrate repertoire influenced by the Rpn10 receptor pathway, Mol. Cell. Proteomics, 6, 1885, 10.1074/mcp.M700264-MCP200 Swaney, 2013, Global analysis of phosphorylation and ubiquitylation crosstalk in protein degradation, Nat. Methods, 10, 10.1038/nmeth.2519 Iesmantavicius, 2014, Convergence of ubiquitylation and phosphorylation signaling in rapamycin-treated yeast cells, Mol. Cell. Proteomics, 13, 1979, 10.1074/mcp.O113.035683 Beaudenon, 1999, Rsp5 ubiquitin-protein ligase mediates DNA damage-induced degradation of the large subunit of RNA polymerase II in Saccharomyces cerevisiae, Mol. Cell. Biol., 19, 6972, 10.1128/MCB.19.10.6972 Kwapisz, 2005, Rsp5 ubiquitin ligase modulates translation accuracy in yeast Saccharomyces cerevisiae, RNA, 11, 1710, 10.1261/rna.2131605 French, 2008, Visual analysis of the yeast 5S rRNA gene transcriptome: regulation and role of La protein, Mol. Cell. Biol., 28, 4576, 10.1128/MCB.00127-08 Wei, 2018, Small-molecule targeting of RNA polymerase I activates a conserved transcription elongation checkpoint, Cell Rep., 23, 404, 10.1016/j.celrep.2018.03.066 Lee, 2015, Differential phosphorylation of RNA polymerase III and the initiation factor TFIIIB in Saccharomyces cerevisiae, PLoS One, 10 Wrobel, 2015, Mistargeted mitochondrial proteins activate a proteostatic response in the cytosol, Nature, 524, 485, 10.1038/nature14951