Yeast Rpb9 Plays an Important Role in Ubiquitylation and Degradation of Rpb1 in Response to UV-Induced DNA Damage

REFERENCES

• Beaudenon, S. L., M. R. Huacani, G. Wang, D. P. McDonnell, and J. M. Huibregtse. 1999. Rsp5 ubiquitin-protein ligase mediates DNA damage-induced degradation of the large subunit of RNA polymerase II in Saccharomyces cerevisiae. Mol. Cell. Biol. 19:6972–6979.
   PubMed Web of Science ®Google Scholar
• Bergmann, E., and J. M. Egly. 2001. Trichothiodystrophy, a transcription syndrome. Trends Genet. 17:279–286.
   PubMedGoogle Scholar
• Bregman, D. B., R. Halaban, A. J. van Gool, K. A. Henning, E. C. Friedberg, and S. L. Warren. 1996. UV-induced ubiquitination of RNA polymerase II: a novel modification deficient in Cockayne syndrome cells. Proc. Natl. Acad. Sci. USA 93:11586–11590.
   PubMed Web of Science ®Google Scholar
• Cramer, P. 2002. Multisubunit RNA polymerases. Curr. Opin. Struct. Biol. 12:89–97.
   PubMed Web of Science ®Google Scholar
• Cramer, P., D. A. Bushnell, and R. D. Kornberg. 2001. Structural basis of transcription: RNA polymerase II at 2.8 angstrom resolution. Science 292:1863–1876.
   PubMed Web of Science ®Google Scholar
• Einhauer, A., and A. Jungbauer. 2001. The FLAG peptide, a versatile fusion tag for the purification of recombinant proteins. J. Biochem. Biophys. Methods 49:455–465.
   PubMedGoogle Scholar
• Friedberg, E. C., G. C. Walker, W. Siede, R. D. Wood, R. A. Schultz, and T. Ellenberger. 2006. DNA repair and mutagenesis, 2nd ed. ASM Press, Washington, DC.
   Google Scholar
• Furter-Graves, E. M., B. D. Hall, and R. Furter. 1994. Role of a small RNA pol II subunit in TATA to transcription start site spacing. Nucleic Acids Res. 22:4932–4936.
   PubMedGoogle Scholar
• Gelbart, M. E., T. Rechsteiner, T. J. Richmond, and T. Tsukiyama. 2001. Interactions of Isw2 chromatin remodeling complex with nucleosomal arrays: analyses using recombinant yeast histones and immobilized templates. Mol. Cell. Biol. 21:2098–2106.
   PubMed Web of Science ®Google Scholar
• Gnatt, A. L., P. Cramer, J. Fu, D. A. Bushnell, and R. D. Kornberg. 2001. Structural basis of transcription: an RNA polymerase II elongation complex at 3.3 Å resolution. Science 292:1876–1882.
   PubMed Web of Science ®Google Scholar
• Hartzog, G. A., T. Wada, H. Handa, and F. Winston. 1998. Evidence that Spt4, Spt5, and Spt6 control transcription elongation by RNA polymerase II in Saccharomyces cerevisiae. Genes Dev. 12:357–369.
   PubMed Web of Science ®Google Scholar
• Hemming, S. A., D. B. Jansma, P. F. Macgregor, A. Goryachev, J. D. Friesen, and A. M. Edwards. 2000. RNA polymerase II subunit Rpb9 regulates transcription elongation in vivo. J. Biol. Chem. 275:35506–35511.
   PubMedGoogle Scholar
• Hitchcock, A. L., K. Auld, S. P. Gygi, and P. A. Silver. 2003. A subset of membrane-associated proteins is ubiquitinated in response to mutations in the endoplasmic reticulum degradation machinery. Proc. Natl. Acad. Sci. USA 100:12735–12740.
   PubMed Web of Science ®Google Scholar
• Huibregtse, J. M., J. C. Yang, and S. L. Beaudenon. 1997. The large subunit of RNA polymerase II is a substrate of the Rsp5 ubiquitin-protein ligase. Proc. Natl. Acad. Sci. USA 94:3656–3661.
   PubMedGoogle Scholar
• Hull, M. W., K. McKune, and N. A. Woychik. 1995. RNA polymerase II subunit RPB9 is required for accurate start site selection. Genes Dev. 9:481–490.
   PubMed Web of Science ®Google Scholar
• Jansen, L. E., H. den Dulk, R. M. Brouns, M. de Ruijter, J. A. Brandsma, and J. Brouwer. 2000. Spt4 modulates Rad26 requirement in transcription-coupled nucleotide excision repair. EMBO J. 19:6498–6507.
   PubMed Web of Science ®Google Scholar
• Jones, E. W. 1991. Tackling the protease problem in Saccharomyces cerevisiae. Methods Enzymol. 194:428–453.
   PubMed Web of Science ®Google Scholar
• Jung, Y., and S. J. Lippard. 2006. RNA polymerase II blockage by cisplatin-damaged DNA. Stability and polyubiquitylation of stalled polymerase. J. Biol. Chem. 281:1361–1370.
   PubMed Web of Science ®Google Scholar
• Lee, D. H., and A. L. Goldberg. 1998. Proteasome inhibitors: valuable new tools for cell biologists. Trends Cell Biol. 8:397–403.
   PubMed Web of Science ®Google Scholar
• Lee, D. H., and A. L. Goldberg. 1996. Selective inhibitors of the proteasome-dependent and vacuolar pathways of protein degradation in Saccharomyces cerevisiae. J. Biol. Chem. 271:27280–27284.
   PubMedGoogle Scholar
• Lee, K. B., D. Wang, S. J. Lippard, and P. A. Sharp. 2002. Transcription-coupled and DNA damage-dependent ubiquitination of RNA polymerase II in vitro. Proc. Natl. Acad. Sci. USA 99:4239–4244.
   PubMed Web of Science ®Google Scholar
• Li, S., B. Ding, R. Chen, C. Ruggiero, and X. Chen. 2006. Evidence that the transcription elongation function of Rpb9 is involved in transcription-coupled DNA repair in Saccharomyces cerevisiae. Mol. Cell. Biol. 26:9430–9441.
   PubMed Web of Science ®Google Scholar
• Li, S., and M. J. Smerdon. 2004. Dissecting transcription-coupled and global genomic repair in the chromatin of yeast GAL1-10 genes. J. Biol. Chem. 279:14418–14426.
   PubMedGoogle Scholar
• Li, S., and M. J. Smerdon. 2002. Rpb4 and Rpb9 mediate subpathways of transcription-coupled DNA repair in Saccharomyces cerevisiae. EMBO J. 21:5921–5929.
   PubMed Web of Science ®Google Scholar
• Lommel, L., and P. C. Hanawalt. 1991. The genetic defect in the Chinese hamster ovary cell mutant UV61 permits moderate selective repair of cyclobutane pyrimidine dimers in an expressed gene. Mutat. Res. 255:183–191.
   PubMedGoogle Scholar
• Lu, Y., Z. Luo, and D. B. Bregman. 2002. RNA polymerase II large subunit is cleaved by caspases during DNA damage-induced apoptosis. Biochem. Biophys. Res. Commun. 296:954–961.
   PubMedGoogle Scholar
• Miller, J., and C. Gordon. 2005. The regulation of proteasome degradation by multi-ubiquitin chain binding proteins. FEBS Lett. 579:3224–3230.
   PubMedGoogle Scholar
• Nakatsu, Y., H. Asahina, E. Citterio, S. Rademakers, W. Vermeulen, S. Kamiuchi, J. P. Yeo, M. C. Khaw, M. Saijo, N. Kodo, T. Matsuda, J. H. Hoeijmakers, and K. Tanaka. 2000. XAB2, a novel tetratricopeptide repeat protein involved in transcription-coupled DNA repair and transcription. J. Biol. Chem. 275:34931–34937.
   PubMedGoogle Scholar
• Nesser, N. K., D. O. Peterson, and D. K. Hawley. 2006. RNA polymerase II subunit Rpb9 is important for transcriptional fidelity in vivo. Proc. Natl. Acad. Sci. USA 103:3268–3273.
   PubMed Web of Science ®Google Scholar
• Park, J. S., M. T. Marr, and J. W. Roberts. 2002. E. coli transcription repair coupling factor (Mfd protein) rescues arrested complexes by promoting forward translocation. Cell 109:757–767.
   PubMed Web of Science ®Google Scholar
• Prakash, S., and L. Prakash. 2000. Nucleotide excision repair in yeast. Mutat. Res. 451:13–24.
   PubMed Web of Science ®Google Scholar
• Ratner, J. N., B. Balasubramanian, J. Corden, S. L. Warren, and D. B. Bregman. 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. 273:5184–5189.
   PubMed Web of Science ®Google Scholar
• Reardon, J. T., and A. Sancar. 2005. Nucleotide excision repair. Prog. Nucleic Acid Res. Mol. Biol. 79:183–235.
   PubMedGoogle Scholar
• Reid, J., and J. Q. Svejstrup. 2004. DNA damage-induced Def1-RNA polymerase II interaction and Def1 requirement for polymerase ubiquitylation in vitro. J. Biol. Chem. 279:29875–29878.
   PubMedGoogle Scholar
• Ribar, B., L. Prakash, and S. Prakash. 2007. ELA1 and CUL3 are required along with ELC1 for RNA polymerase II polyubiquitylation and degradation in DNA-damaged yeast cells. Mol. Cell. Biol. 27:3211–3216.
   PubMedGoogle Scholar
• Ribar, B., L. Prakash, and S. Prakash. 2006. Requirement of ELC1 for RNA polymerase II polyubiquitylation and degradation in response to DNA damage in Saccharomyces cerevisiae. Mol. Cell. Biol. 26:3999–4005.
   PubMedGoogle Scholar
• Rondon, A. G., M. Garcia-Rubio, S. Gonzalez-Barrera, and A. Aguilera. 2003. Molecular evidence for a positive role of Spt4 in transcription elongation. EMBO J. 22:612–620.
   PubMed Web of Science ®Google Scholar
• Sambrook, J., and D. W. Russell. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
   Google Scholar
• Schindler, D., and J. Davies. 1975. Inhibitors of macromolecular synthesis in yeast. Methods Cell Biol. 12:17–38.
   PubMedGoogle Scholar
• Selby, C. P., and A. Sancar. 1993. Molecular mechanism of transcription-repair coupling. Science 260:53–58.
   PubMed Web of Science ®Google Scholar
• Sikorski, R. S., and P. Hieter. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:19–27.
   PubMed Web of Science ®Google Scholar
• Somesh, B. P., J. Reid, W. F. Liu, T. M. Sogaard, H. Erdjument-Bromage, P. Tempst, and J. Q. Svejstrup. 2005. Multiple mechanisms confining RNA polymerase II ubiquitylation to polymerases undergoing transcriptional arrest. Cell 121:913–923.
   PubMed Web of Science ®Google Scholar
• Sun, Z. W., A. Tessmer, and M. Hampsey. 1996. Functional interaction between TFIIB and the Rpb9 (Ssu73) subunit of RNA polymerase II in Saccharomyces cerevisiae. Nucleic Acids Res. 24:2560–2566.
   PubMedGoogle Scholar
• Svejstrup, J. Q. 2003. Rescue of arrested RNA polymerase II complexes. J. Cell Sci. 116:447–451.
   PubMedGoogle Scholar
• Swanson, M. S., and F. Winston. 1992. SPT4, SPT5 and SPT6 interactions: effects on transcription and viability in Saccharomyces cerevisiae. Genetics 132:325–336.
   PubMed Web of Science ®Google Scholar
• Troelstra, C., A. van Gool, J. de Wit, W. Vermeulen, D. Bootsma, and J. H. Hoeijmakers. 1992. ERCC6, a member of a subfamily of putative helicases, is involved in Cockayne's syndrome and preferential repair of active genes. Cell 71:939–953.
   PubMed Web of Science ®Google Scholar
• van Gool, A. J., R. Verhage, S. M. Swagemakers, P. van de Putte, J. Brouwer, C. Troelstra, D. Bootsma, and J. H. Hoeijmakers. 1994. RAD26, the functional S. cerevisiae homolog of the Cockayne syndrome B gene ERCC6. EMBO J. 13:5361–5369.
   PubMed Web of Science ®Google Scholar
• van Hoffen, A., A. T. Natarajan, L. V. Mayne, A. A. van Zeeland, L. H. Mullenders, and J. Venema. 1993. Deficient repair of the transcribed strand of active genes in Cockayne's syndrome cells. Nucleic Acids Res. 21:5890–5895.
   PubMed Web of Science ®Google Scholar
• Van Mullem, V., M. Wery, M. Werner, J. Vandenhaute, and P. Thuriaux. 2002. The Rpb9 subunit of RNA polymerase II binds transcription factor TFIIE and interferes with the SAGA and elongator histone acetyltransferases. J. Biol. Chem. 277:10220–10225.
   PubMedGoogle Scholar
• Venema, J., L. H. Mullenders, A. T. Natarajan, A. A. van Zeeland, and L. V. Mayne. 1990. The genetic defect in Cockayne syndrome is associated with a defect in repair of UV-induced DNA damage in transcriptionally active DNA. Proc. Natl. Acad. Sci. USA 87:4707–4711.
   PubMed Web of Science ®Google Scholar
• Venema, J., A. van Hoffen, V. Karcagi, A. T. Natarajan, A. A. van Zeeland, and L. H. Mullenders. 1991. Xeroderma pigmentosum complementation group C cells remove pyrimidine dimers selectively from the transcribed strand of active genes. Mol. Cell. Biol. 11:4128–4134.
   PubMed Web of Science ®Google Scholar
• Venema, J., A. van Hoffen, A. T. Natarajan, A. A. van Zeeland, and L. H. Mullenders. 1990. The residual repair capacity of xeroderma pigmentosum complementation group C fibroblasts is highly specific for transcriptionally active DNA. Nucleic Acids Res. 18:443–448.
   PubMedGoogle Scholar
• Verhage, R., A. M. Zeeman, N. de Groot, F. Gleig, D. D. Bang, P. van de Putte, and J. Brouwer. 1994. The RAD7 and RAD16 genes, which are essential for pyrimidine dimer removal from the silent mating type loci, are also required for repair of the nontranscribed strand of an active gene in Saccharomyces cerevisiae. Mol. Cell. Biol. 14:6135–6142.
   PubMedGoogle Scholar
• Wada, T., G. Orphanides, J. Hasegawa, D. K. Kim, D. Shima, Y. Yamaguchi, A. Fukuda, K. Hisatake, S. Oh, D. Reinberg, and H. Handa. 2000. FACT relieves DSIF/NELF-mediated inhibition of transcriptional elongation and reveals functional differences between P-TEFb and TFIIH. Mol. Cell 5:1067–1072.
   PubMed Web of Science ®Google Scholar
• Weinberger, M., L. Ramachandran, and W. C. Burhans. 2003. Apoptosis in yeasts. IUBMB Life 55:467–472.
   PubMed Web of Science ®Google Scholar
• Woudstra, E. C., C. Gilbert, J. Fellows, L. Jansen, J. Brouwer, H. Erdjument-Bromage, P. Tempst, and J. Q. Svejstrup. 2002. A Rad26-Def1 complex coordinates repair and RNA pol II proteolysis in response to DNA damage. Nature 415:929–933.
   PubMedGoogle Scholar
• Yamaguchi, Y., T. Takagi, T. Wada, K. Yano, A. Furuya, S. Sugimoto, J. Hasegawa, and H. Handa. 1999. NELF, a multisubunit complex containing RD, cooperates with DSIF to repress RNA polymerase II elongation. Cell 97:41–51.
   PubMed Web of Science ®Google Scholar
• Ziegler, L. M., D. A. Khaperskyy, M. L. Ammerman, and A. S. Ponticelli. 2003. Yeast RNA polymerase II lacking the Rpb9 subunit is impaired for interaction with transcription factor IIF. J. Biol. Chem. 278:48950–48956.
   PubMedGoogle Scholar