Bur1 Kinase Is Required for Efficient Transcription Elongation by RNA Polymerase II

REFERENCES

• Akoulitchev, S., S. Chuikov, and D. Reinberg. 2000. TFIIH is negatively regulated by cdk8-containing mediator complexes. Nature 407: 102–106.
   PubMed Web of Science ®Google Scholar
• Allison, L. A., M. Moyle, M. Shales, and C. J. Ingles. 1985. Extensive homology among the largest subunits of eukaryotic and prokaryotic RNA polymerases. Cell 42: 599–610.
   PubMed Web of Science ®Google Scholar
• Ansari, A. Z., S. S. Koh, Z. Zaman, C. Bongards, N. Lehming, R. A. Young, and M. Ptashne. 2002. Transcriptional activating regions target a cyclin-dependent kinase. Proc. Natl. Acad. Sci. USA 99: 14706–14709.
   PubMedGoogle Scholar
• Archambault, J., F. Lacroute, A. Ruet, and J. D. Friesen. 1992. Genetic interaction between transcription elongation factor TFIIS and RNA polymerase II. Mol. Cell. Biol. 12: 4142–4152.
   PubMedGoogle Scholar
• Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl. 1991. Current protocols in molecular biology. John Wiley and Sons, New York, N.Y.
   Google Scholar
• Bentley, D. 1999. Coupling RNA polymerase II transcription with pre-mRNA processing. Curr. Opin. Cell Biol. 11: 347–351.
   PubMedGoogle Scholar
• Birse, C. E., B. A. Lee, K. Hansen, and N. J. Proudfoot. 1997. Transcriptional termination signals for RNA polymerase II in fission yeast. EMBO J. 16: 3633–3643.
   PubMed Web of Science ®Google Scholar
• Birse, C. E., L. Minvielle-Sebastia, B. A. Lee, W. Keller, and N. J. Proudfoot. 1998. Coupling termination of transcription to messenger RNA maturation in yeast. Science 280: 298–301.
   PubMed Web of Science ®Google Scholar
• Bortvin, A., and F. Winston. 1996. Evidence that Spt6p controls chromatin structure by a direct interaction with histones. Science 272: 1473–1476.
   PubMed Web of Science ®Google Scholar
• Bourgeois, C. F., Y. K. Kim, M. J. Churcher, M. J. West, and J. Karn. 2002. Spt5 cooperates with human immunodeficiency virus type 1 tat by preventing premature RNA release at terminator sequences. Mol. Cell. Biol. 22: 1079–1093.
   PubMed Web of Science ®Google Scholar
• Cho, E. J., M. S. Kobor, M. Kim, J. Greenblatt, and S. Buratowski. 2001. Opposing effects of Ctk1 kinase and Fcp1 phosphatase at Ser 2 of the RNA polymerase II C-terminal domain. Genes Dev. 15: 3319–3329.
   PubMed Web of Science ®Google Scholar
• Cho, E. J., T. Takagi, C. R. Moore, and S. Buratowski. 1997. mRNA capping enzyme is recruited to the transcription complex by phosphorylation of the RNA polymerase II carboxy-terminal domain. Genes Dev. 11: 3319–3326.
   PubMed Web of Science ®Google Scholar
• Corden, J. L., D. L. Cadena, J. M. Ahearn, and M. E. Dahmus. 1985. A unique structure at the carboxyl terminus of the largest subunit of eukaryotic RNA polymerase II. Proc. Natl. Acad. Sci. USA 82: 7934–7938.
   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.
   Google Scholar
• Dahmus, M. E. 1996. Reversible phosphorylation of the C-terminal domain of RNA polymerase II. J. Biol. Chem. 271: 19009–19012.
   PubMed Web of Science ®Google Scholar
• Dye, M. J., and J. Proudfoot. 2001. Multiple transcript cleavage precedes polymerase release in termination by RNA polymerase II. Cell 105: 669–681.
   PubMedGoogle Scholar
• Enriquez-Harris, P., N. Levitt, D. Briggs, and N. J. Proudfoot. 1991. A pause site for RNA polymerase II is associated with termination of transcription. EMBO J. 10: 1833–1842.
   PubMed Web of Science ®Google Scholar
• Exinger, F., and F. Lacroute. 1992. 6-Azauracil inhibition of GTP biosynthesis in Saccharomyces cerevisiae. Curr. Genet. 22: 9–11.
   PubMedGoogle Scholar
• Gietz, D., A. St. Jean, R. A. Woods, and R. Schiestl. 1992. Improved method for high-efficiency transformation of intact yeast cells. Nucleic Acids Res. 20: 1425.
   PubMed Web of Science ®Google Scholar
• Gu, W., S. Malik, M. Ito, C.-X. Yuan, J. D. Fondell, X. Zhang, E. Martinex, J. Qin, and R. G. Roeder. 1999. A novel human SRB/MED containing cofactor complex, SMCC, involved in transcription regulation. Mol. Cell 3: 97–108.
   PubMed Web of Science ®Google Scholar
• Guthrie, C., and G. R. Fink (ed.). 1991. Methods in enzymology, vol. 194. Guide to yeast genetics and molecular biology. Academic Press, Inc., Boston, Mass.
   Google Scholar
• Hampsey, M. 1998. Molecular genetics of the RNA polymerase II general transcriptional machinery. Microbiol. Mol. Biol. Rev. 62: 465–503.
   PubMed Web of Science ®Google Scholar
• Hampsey, M., and D. Reinberg. 1999. RNA polymerase II as a control panel for multiple coactivator complexes. Curr. Opin. Genet. Dev. 9: 132–139.
   PubMed Web of Science ®Google Scholar
• Happel, A. M., M. S. Swanson, and F. Winston. 1991. The SNF2, SNF5 and SNF6 genes are required for Ty transcription in Saccharomyces cerevisiae. Genetics 128: 69–77.
   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
• Hengartner, C. J., V. E. Myer, S.-M. Liao, C. J. Wilson, S. S. Koh, and R. A. Young. 1998. Temporal regulation of RNA polymerase II by Srb10 and Kin28 cyclin-dependent kinases. Mol. Cell 2: 43–53.
   PubMed Web of Science ®Google Scholar
• Hirose, Y., and J. L. Manley. 2000. RNA polymerase II and the integration of nuclear events. Genes Dev. 14: 1415–1429.
   PubMed Web of Science ®Google Scholar
• Hirst, M., M. S. Kobor, N. Kuriakose, J. Greenblatt, and I. Sadowski. 1999. GAL4 is regulated by the RNA polymerase II holoenzyme-associated cyclin-dependent protein kinase SRB10/CDK8. Mol. Cell 3: 673–678.
   PubMed Web of Science ®Google Scholar
• Ho, S. N., H. D. Hunt, R. M. Horton, J. K. Pullen, and L. R. Pease. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77: 51–59.
   PubMed Web of Science ®Google Scholar
• Irie, K., S. Nomoto, I. Miyajima, and K. Matsumoto. 1991. SGV1 encodes a CDC28/cdc2-related kinase required for a G alpha subunit-mediated adaptive response to pheromone in S. cerevisiae. Cell 65: 785–795.
   Google Scholar
• Isel, C., and J. Karn. 1999. Direct evidence that HIV-1 Tat stimulates RNA polymerase II carboxyl-terminal domain hyperphosphorylation during transcriptional elongation. J. Mol. Biol. 290: 924–941.
   Google Scholar
• Jeffrey, P. D., A. A. Russo, K. Polyak, E. Gibbs, J. Hurwitz, J. Massague, and N. P. Pavletich. 1995. Mechanism of CDK activation revealed by the structure of a cyclinA-CDK2 complex. Nature 376: 313–320.
   PubMed Web of Science ®Google Scholar
• Jona, G., B. O. Wittschieben, J. Q. Svejstrup, and O. Gileadi. 2001. Involvement of yeast carboxy-terminal domain kinase I (CTDK-I) in transcription elongation in vivo. Gene 267: 31–36.
   PubMedGoogle Scholar
• Keogh, M.-C., E.-J. Cho, V. Podolny, and S. Buratowski. 2002. Kin28 is found within TFIIH and a Kin28-Ccl1-Tfb3 trimer complex with differential sensitivities to T-loop phosphorylation. Mol. Cell. Biol. 22: 1288–1297.
   PubMed Web of Science ®Google Scholar
• Kim, J. B., and P. A. Sharp. 2001. Positive transcription elongation factor b phosphorylates hSPT5 and RNA polymerase II carboxy-terminal domain independently of cyclin dependent kinase activating kinase. J. Biol. Chem. 276: 12317–12323.
   PubMed Web of Science ®Google Scholar
• Komarnitsky, P., E.-J. Cho, and S. Buratowski. 2000. Different phosphorylated forms of RNA polymerase II and associated mRNA processing factors during transcription. Genes Dev. 14: 2452–2460.
   PubMed Web of Science ®Google Scholar
• Krogan, N. J., M. Kim, S. H. Ahn, G. Zhong, M. S. Kobor, G. Cagney, A. Emili, A. Shilatifard, S. Buratowski, and J. F. Greenblatt. 2002. RNA polymerase II elongation factors of Saccharomyces cerevisiae: a targeted proteomics approach. Mol. Cell. Biol. 22: 6979–6992.
   PubMed Web of Science ®Google Scholar
• Kuchin, S., and M. Carlson. 1998. Functional relationships of Srb10-Srb11 kinase, carboxy-terminal domain kinase CTDK-I, and transcriptional corepressor Ssn6-Tup1. Mol. Cell. Biol. 18: 1163–1171.
   PubMedGoogle Scholar
• Kuras, L., and K. Struhl. 1999. Binding of TBP to promoters in vivo is stimulated by activators and requires PolII holoenzyme. Nature 399: 609–613.
   PubMedGoogle Scholar
• Lavoie, S. B., A. L. Albert, H. Handa, M. Vincent, and O. Bensaude. 2001. The peptidyl-prolyl isomerase Pin1 interacts with hSpt5 phosphorylated by Cdk9. J. Mol. Biol. 312: 675–685.
   PubMed Web of Science ®Google Scholar
• Lee, J. M., and A. L. Greenleaf. 1991. CTD kinase large subunit is encoded by CTK1, a gene required for normal growth of Saccharomyces cerevisiae. Gene Expr. 1: 149–167.
   PubMed Web of Science ®Google Scholar
• Lee, J. M., and A. L. Greenleaf. 1997. Modulation of RNA polymerase II elongation efficiency by C-terminal heptapeptide repeat domain kinase I. J. Biol. Chem. 272: 10990–10993.
   Google Scholar
• Lennon, J. C., III, M. Wind, L. Saunders, M. B. Hock, and D. Reines. 1998. Mutations in RNA polymerase II and elongation factor SII severely reduce mRNA levels in Saccharomyces cerevisiae. Mol. Cell. Biol. 18: 5771–5779.
   PubMedGoogle Scholar
• Lindstrom, D. L., and G. Hartzog. 2001. Genetic interactions of Spt4-Spt5 and TFIIS with the RNA polymerase II CTD and CTD modifying enzymes in Saccharomyces cerevisiae. Genetics 159: 487–497.
   PubMed Web of Science ®Google Scholar
• Marshall, N. F., J. Peng, Z. Xie, and D. H. Price. 1996. Control of RNA polymerase II elongation potential by a novel carboxy-terminal domain kinase. J. Biol. Chem. 271: 27176–27183.
   PubMed Web of Science ®Google Scholar
• McCracken, S., N. Fong, E. Rosonina, K. Yankulov, G. Brothers, D. Siderovski, A. Hessel, S. Foster, A. E. program, S. Shuman, and D. L. Bentley. 1997. 5-Capping enzymes are targeted to pre-mRNA by binding to the phosphorylated carboxy-terminal domain of RNA polymerase II. Genes Dev. 11: 3306–3318.
   PubMed Web of Science ®Google Scholar
• McCracken, S., N. Fong, K. Yankulov, G. Ballantyne, J. Pan, J. Greenblatt, S. D. Patterson, M. Wickens, and D. L. Bentley. 1997. The C-terminal domain of RNA polymerase II couples mRNA processing to transcription. Nature 385: 357–361.
   PubMed Web of Science ®Google Scholar
• Murray, S., R. Udupa, S. Yao, G. Hartzog, and G. Prelich. 2001. Phosphorylation of the RNA polymerase II carboxy-terminal domain by the Bur1 cyclin-dependent kinase. Mol. Cell. Biol. 21: 4089–4096.
   PubMed Web of Science ®Google Scholar
• Neigeborn, L., J. L. Celenza, and M. Carlson. 1987. SSN20 is an essential gene with mutant alleles that suppress defects in SUC2 transcription in Saccharomyces cerevisiae. Mol. Cell. Biol. 7: 672–678.
   PubMedGoogle Scholar
• Nelson, C., S. Goto, K. Lund, W. Hung, and I. Sadowski. 2003. Srb10/Cdk8 regulates yeast filamentous growth by phosphorylating the transcription factor Ste12. Nature 421: 187–190.
   PubMed Web of Science ®Google Scholar
• Orlando, V. 2000. Mapping chromosomal proteins in vivo by formaldehyde-crosslinked-chromatin immunoprecipitation. Trends Biochem. Sci. 25: 99–104.
   PubMed Web of Science ®Google Scholar
• Orlando, V., H. Strutt, and R. Paro. 1997. Analysis of chromatin structure by in vivo formaldehyde cross-linking. Methods 11: 205–214.
   PubMed Web of Science ®Google Scholar
• Patturajan, M., R. J. Schultz, B. M. Sefton, R. Berezney, M. Vincent, O. Bensaude, S. L. Warren, and J. L. Corden. 1998. Growth related changes in phosphorylation of yeast RNA polymerase II. J. Biol. Chem. 273: 4689–4694.
   PubMedGoogle Scholar
• Pei, Y., B. Schwer, and S. Shuman. 2003. Interactions between fission yeast Cdk9, its cyclin partner Pch1, and mRNA capping enzyme Pct1 suggest an elongation checkpoint for mRNA quality control. J. Biol. Chem. 278: 7180–7188.
   PubMed Web of Science ®Google Scholar
• Ping, Y. H., and T. M. Rana. 2001. DSIF and NELF interact with RNA polymerase II elongation complex and HIV-1 Tat stimulates P-TEFb-mediated phosphorylation of RNA polymerase II and DSIF during transcription elongation. J. Biol. Chem. 276: 12951–12958.
   PubMed Web of Science ®Google Scholar
• Ping, Y. H., and T. M. Rana. 1999. Tat-associated kinase (P-TEFb): a component of transcription preinitiation and elongation complexes. J. Biol. Chem. 274: 7399–7404.
   PubMed Web of Science ®Google Scholar
• Prelich, G., and F. Winston. 1993. Mutations that suppress the deletion of an upstream activating sequence in yeast: involvement of a protein kinase and histone H3 in repressing transcription in vivo. Genetics 135: 665–676.
   PubMed Web of Science ®Google Scholar
• Price, D. H. 2000. P-TEFb, a cyclin dependent kinase controlling elongation by RNA polymerase II. Mol. Cell. Biol. 20: 2629–2634.
   PubMed Web of Science ®Google Scholar
• Puig, O., B. Rutz, B. G. Luukkonen, S. Kandels-Lewis, E. Bragado-Nilsson, and B. Seraphin. 1998. New constructs and strategies for efficient PCR-based gene manipulations in yeast. Yeast 14: 1139–1146.
   PubMedGoogle Scholar
• Ramanathan, Y., S. M. Rajpara, S. M. Reza, E. Lees, S. Shuman, M. B. Mathews, and T. Pe'ery. 2001. Three distinct RNA polymerase II carboxy-terminal domain kinases display distinct substrate preferences. J. Biol. Chem. 276: 10913–10920.
   PubMed Web of Science ®Google Scholar
• Ranish, J. A., E. C. Yi, D. M. Leslie, S. O. Purvine, D. R. Goodlett, J. Eng, and R. Aebersold. 2003. The study of macromolecular complexes by quantitative proteomics. Nat. Genet. 33: 349–355.
   PubMed Web of Science ®Google Scholar
• Rodriguez, C. R., E.-J. Cho, M.-C. Keogh, C. L. Moore, A. L. Greenleaf, and S. Buratowski. 2000. Kin28, the TFIIH-associated carboxy-terminal domain kinase, facilitates the recruitment of mRNA processing machinery to RNA polymerase II. Mol. Cell. Biol. 20: 104–112.
   PubMed Web of Science ®Google Scholar
• Russo, A. A., P. D. Jeffrey, and N. P. Pavletich. 1996. Structural basis of cyclin-dependent kinase activation by phosphorylation. Nat. Struct. Biol. 3: 696–700.
   PubMedGoogle Scholar
• Schroeder, S. C., B. Schwer, S. Shuman, and D. Bentley. 2000. Dynamic association of capping enzymes with transcribing RNA polymerase II. Genes Dev. 14: 2435–2440.
   PubMed Web of Science ®Google Scholar
• Shaw, R. J., J. L. Wilson, K. T. Smith, and D. Reines. 2001. Regulation of an IMP dehydrogenase gene and its overexpression in drug-sensitive transcription elongation mutants of yeast. J. Biol. Chem. 276: 32905–32916.
   PubMedGoogle Scholar
• Shim, E. Y., A. K. Walker, Y. Shi, and T. K. Blackwell. 2002. CDK-9/cyclin T (P-TEFb) is required in two postinitiation pathways for transcription in the C. elegans embryo. Genes Dev. 16: 2135–2146.
   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
• Solomon, M. J., and P. Kaldis. 1998. Regulation of Cdks by phosphorylation. Results Probl. Cell Differ. 22: 79–109.
   PubMedGoogle Scholar
• Squazzo, S. L., P. J. Costa, D. L. Lindstrom, K. E. Kumer, R. Simic, J. L. Jennings, A. J. Link, K. M. Arndt, and G. A. Hartzog. 2002. The Paf1 complex physically and functionally associates with transcription elongation factors in vivo. EMBO J. 21: 1764–1774.
   PubMed Web of Science ®Google Scholar
• Sterner, D. E., J. M. Lee, S. E. Hardin, and A. L. Greenleaf. 1995. The yeast carboxyl-terminal repeat domain kinase CTDK-I is a divergent cyclin-cyclin-dependent kinase complex. Mol. Cell. Biol. 15: 5716–5724.
   PubMed Web of Science ®Google 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
• Swanson, M. S., E. A. Malone, and F. Winston. 1991. SPT5, an essential gene important for normal transcription in Saccharomyces cerevisiae, encodes an acidic nuclear protein with a carboxy-terminal repeat. Mol. Cell. Biol. 11: 3009–3019.
   PubMedGoogle Scholar
• Uptain, S. M., C. M. Kane, and M. J. Chamberlin. 1997. Basic mechanisms of transcript elongation and its regulation. Annu. Rev. Biochem. 66: 117–172.
   PubMed Web of Science ®Google Scholar
• Wada, T., T. Takagi, Y. Yamaguchi, D. Watanabe, and H. Handa. 1998. Evidence that p-TEFb alleviates the negative effect of DSIF on RNA polymerase II-dependent transcription in vitro. EMBO J. 17: 7395–7403.
   PubMed Web of Science ®Google Scholar
• Winston, F. 1992. Analysis of SPT genes: a genetic approach to analysis of TFIID, histones and other transcription factors of yeast, p. 1271–1293. In S. L. McKnight and K. R. Yamamoto (ed.), Transcriptional regulation. Cold Spring Harbor Laboratory Press, New York, N.Y.
   Google Scholar
• Yao, S., A. Neiman, and G. Prelich. 2000. BUR1 and BUR2 encode a divergent cyclin-dependent kinase-cyclin complex important for transcription in vivo. Mol. Cell. Biol. 20: 7080–7087.
   PubMed Web of Science ®Google Scholar
• Yao, S., and G. Prelich. 2002. Activation of the Bur1-Bur2 cyclin-dependent kinase complex by Cak1. Mol. Cell. Biol. 22: 6750–6758.
   PubMed Web of Science ®Google Scholar
• Zhou, M., M. A. Halanski, M. F. Radonovich, F. Kashanchi, J. Peng, D. H. Price, and J. N. Brady. 2000. Tat modifies the activity of CDK9 to phosphorylate serine 5 of the RNA polymerase II carboxy-terminal domain during human immunodeficiency virus type 1 transcription. Mol. Cell. Biol. 20: 5077–5086.
   PubMed Web of Science ®Google Scholar