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Article

Separable Functions of the Fission Yeast Spt5 Carboxyl-Terminal Domain (CTD) in Capping Enzyme Binding and Transcription Elongation Overlap with Those of the RNA Polymerase II CTD

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Pages 2353-2364 | Received 29 Jan 2010, Accepted 04 Mar 2010, Published online: 20 Mar 2023

REFERENCES

  • Akhtar, M. S., M. Heidermann, J. R. Tietjen, D. W. Zhang, R. D. Chapman, D. Eick, and A. Z. Ansari. 2009. TFIIH kinase places bivalent marks on the carboxy-terminal domain of RNA polymerase II. Mol. Cell 34:387–393.
  • Andrulis, E. D., E. Guzman, P. Dumloring, J. Werner, and J. T. Lis. 2000. High-resolution localization of Drosophila Spt5 and Spt6 at heat shock genes in vivo: roles in promoter proximal pausing and transcription elongation. Genes Dev. 14:2635–2649.
  • 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.
  • Azuma, Y., M. Yamagashi, R. Ueshima, and A. Ishihama. 1991. Cloning and sequence determination of the Schizosaccharomyces pombe rpb1 gene encoding the largest subunit of RNA polymerase II. Nucleic Acids Res. 19:461–468.
  • Chen, Y., Y. Yamaguchi, Y. Tsugeno, J. Yamamoto, T. Yamada, M. Nakamura, K. Hisatake, and H. Handa. 2009. DISF, the Paf1 complex, and Tat-SF1 have nonredundant, cooperative roles in RNA polymerase II elongation. Genes Dev. 23:2765–2777.
  • Chiu, Y. L., C. K. Ho, N. Saha, B. Schwer, S. Shuman, and T. M. Rana. 2002. Tat stimulates cotranscriptional capping of HIV mRNA. Mol. Cell 10:585–597.
  • Cho, E., 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 carboxyl-terminal domain. Genes Dev. 11:3319–3326.
  • Fabrega, C., V. Shen, S. Shuman, and C. D. Lima. 2003. Structure of an mRNA capping enzyme bound to the phosphorylated carboxyl-terminal domain of RNA polymerase II. Mol. Cell 11:1549–1561.
  • Forsburg, S. L. 1993. Comparison of Schizosaccharomyces pombe expression systems. Nucleic Acids Res. 21:2955–2956.
  • Forsburg, S. L., and D. A. Sherman. 1997. General purpose tagging vectors for fission yeast. Gene 191:191–195.
  • Forsburg, S. L., and N. Rhind. 2006. Basic methods for fission yeast. Yeast 23:173–183.
  • Gao, L., and D. S. Gross. 2008. Sir2 silences gene transcription by targeting the transition between RNA polymerase II initiation and elongation. Mol. Cell. Biol. 28:3979–3994.
  • Guiguen, A., J. Soutourine, M. Dewez, L. Tafforeau, M. Dieu, M. Raes, J. Vandenhaute, M. Werner, and D. Hermand. 2007. Recruitment of P-TEFb (Cdk9-Pch1) to chromatin by the cap-methyl transferase Pcm1 in fission yeast. EMBO J. 26:1552–1559.
  • Guo, M., F. Xu, J. Yamada, T. Egelhofer, Y. Gao, G. A. Hartzog, M. Teng, and L. Niu. 2008. Core structure of the yeast Spt4-Spt5 complex: a conserved module for regulation of transcription elongation. Structure 16:1649–1658.
  • Hagler, J., and S. Shuman. 1992. A freeze-frame view of eukaryotic transcription during elongation and capping of nascent mRNA. Science 255:983–986.
  • Hartzog, G. A., M. A. Basrai, S. L. Ricupero-Hovasse, P. Hieter, and F. Winston. 1996. Identification and analysis of a functional human homolog of the SPT4 gene of Saccharomyces cerevisiae. Mol. Cell. Biol. 16:2848–2856.
  • 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.
  • Ho, C. K., and S. Shuman. 1999. Distinct roles for CTD Ser2 and Ser5 phosphorylation in the recruitment and allosteric activation of mammalian capping enzyme. Mol. Cell 3:405–411.
  • Ho, C. K., V. Sriskanda, S. McCracken, D. Bentley, B. Schwer, and S. Shuman. 1998. The guanylyltransferase domain of mammalian mRNA capping enzyme binds to the phosphorylated carboxyl-terminal domain of RNA polymerase II. J. Biol. Chem. 273:9577–9585.
  • Hong, S. W., S. M. Hong, J. W. Yoo, Y. C. Lee, S. Kim, J. T. Lis, and D. Kee. 2009. Phosphorylation of the RNA polymerase II C-terminal domain by TFIIH kinase is not essential for transcription of Saccharomyces cerevisiae genome. Proc. Natl. Acad. Sci. U. S. A. 106:14276–14280.
  • Jennings, B. H., S. Shah, Y. Yamaguchi, M. Seki, R. G. Phillips, H. Handa, and D. Ish-Horowicz. 2004. Locus-specific requirements for Spt5 in transcriptional activation and repression in Drosophila. Curr. Biol. 14:1680–1684.
  • Kanin, E. I., R. T. Kipp, C. Kung, M. Slattery, A. Viale, S. Hahn, K. M. Shokat, and A. Z. Ansari. 2007. Chemical inhibition of the THIIH-associated kinase Cdk7/Kin28 does not impair global mRNA synthesis. Proc. Natl. Acad. Sci. U. S. A. 104:5812–5817.
  • Karagiannis, J., and M. K. Balasubramanian. 2007. A cyclin-dependent kinase that promotes cytokinesis through modulating phosphorylation of the carboxy terminal domain of the RNA Pol II Rpb1p subunit. PLoS One 2:e433.
  • Komori, T., N. Inukai, T. Yamada, Y. Yamaguchi, and H. Handa. 2009. Role of human transcription elongation factor DSIF in the suppression of senescence and apoptosis. Genes Cells 14:343–354.
  • Krishnan, K., N. Salomonis, and S. Guo. 2008. Identification of Spt5 target genes in zebrafish development reveals its dual activity in vivo. PLoS One 3:e3621.
  • Liu, Y., L. Warfield, C. Zhang, J. Luo, J. Allen, W. H. Lang, J. Ranish, K. M. Shokat, and S. Hahn. 2009. Phosphorylation of the transcription factor Spt5 by yeast Bur1 kinase stimulates recruitment of the PAF complex. Mol. Cell. Biol. 29:4852–4963.
  • Mandal, S. S., C. Chu, T. Wada, H. Handa, A. J. Shatkin, and D. Reinberg. 2004. Functional interaction of RNA-capping enzyme with factors that positively and negatively regulate promoter escape by RNA polymerase II. Proc. Natl. Acad. Sci. U. S. A. 101:7572–7577.
  • Mason, P. B., and K. Struhl. 2005. Distinction and relationship between elongation rate and processivity of RNA polymerase II in vivo. Mol. Cell 17:831–840.
  • McCracken, S., N. Fong, E. Rosonina, K. Yankulov, G. Brothers, D. Siderovski, A. Hessel, S. Foster, S. Shuman, and D. L. Bentley. 1997. 5′ Capping enzymes are targeted to pre-mRNA by binding to the phosphorylated C-terminal domain of RNA polymerase II. Genes Dev. 11:3306–3318.
  • Meinhart, A., T. Kamenski, S. Hoeppner, S. Baumli, and P. Cramer. 2005. A structural perspective of CTD function. Genes Dev. 19:1401–1415.
  • Nonet, M., D. Sweetser, and R. A. Young. 1987. Functional redundancy and structural polymorphism in the large subunit of RNA polymerase II. Cell 50:909–915.
  • Pei, Y., and S. Shuman. 2002. Interactions between fission yeast mRNA capping enzymes and elongation factor Spt5. J. Biol. Chem. 277:19639–19648.
  • Pei, Y., and S. Shuman. 2003. Characterization of the Schizosaccharomyces pombe Cdk9/Pch1 protein kinase: Spt5 phosphorylation, autophosphorylation and mutational analysis. J. Biol. Chem. 278:43346–43356.
  • Pei, Y., S. Hausmann, C. K. Ho, B. Schwer, and S. Shuman. 2001. The length, phosphorylation state, and primary structure of the RNA polymerase II carboxyl-terminal domain dictate interactions with mRNA capping enzymes. J. Biol. Chem. 276:28075–28082.
  • 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.
  • Pei, Y., H. Du, J. Singer, St. C. Amour, S. Granitto, S. Shuman, and R. P. Fisher. 2006. Cdk9 of fission yeast is activated by the CDK-activating kinase Csk1, overlaps functionally with the TFIIH-associated kinase Mcs6, and associates with the cap methyltransferase Pcm1 in vivo. Mol. Cell. Biol. 26:777–788.
  • Phatnani, H. P., and A. L. Greenleaf. 2006. Phosphorylation and functions of the RNA polymerase II CTD. Genes Dev. 20:2922–2936.
  • Qiu, H., C. Hu, and A. G. Hinnebusch. 2009. Phosphorylation of the Pol II CTD by KIN29 enhances BUR1/BUR2 recruitment and Ser2 CTD phosphorylation near promoters. Mol. Cell 33:752–762.
  • Renner, D. B., Y. Yamaguchi, T. Wada, H. Handa, and D. H. Price. 2001. A highly purified RNA polymerase II elongation control system. J. Biol. Chem. 276:42601–42609.
  • Schramke, V., D. M. Sheedy, A. M. Denli, C. Bonila, K. Ekwall, G. J. Hannon, and R. C. Allshire. 2005. RNA-interference-directed chromatin modification coupled to RNA polymerase II transcription. Nature 435:1275–1279.
  • Schwer, B., X. Mao, and S. Shuman. 1998. Accelerated mRNA decay in conditional mutants of yeast mRNA capping enzyme. Nucleic Acids Res. 26:2050–2057.
  • Schwer, B., S. Schneider, Y. Pei, A. Aronova, and S. Shuman. 2009. Characterization of the Schizosaccharomyces pombe Spt5-Spt4 complex. RNA. 15:1241–1250.
  • Shaw, R. J., and D. Reines. 2000. Saccharomyces cerevisiae transcription elongation mutants are defective in PUR5 induction in response to nucleotide depletion. Mol. Cell. Biol. 20:7427–7437.
  • Shim, E. Y., A. K. Walker, Y. Shi, and K. T. 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.
  • Sims, R. J., R. Belotserkovskaya, and D. Reinberg. 2004. Elongation by RNA polymerase II: the short and long of it. Genes Dev. 18:2437–2468.
  • 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.
  • 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.
  • Thompson, C. M., A. J. Koleske, D. M. Chao, and R. A. Young. 1993. A multisubunit complex associated with the RNA polymerase II CTD and TATA-binding protein in yeast. Cell 73:1361–1375.
  • Viladevall, L., St. C. V. Amour, A. Rosebrock, S. Schneider, C. Zhang, J. J. Allen, K. M. Shokat, B. Schwer, J. K. Leatherwood, and R. P. Fisher. 2009. TFIIH and P-TEFb coordinate transcription with capping enzyme recruitment at specific genes in fission yeast. Mol. Cell 33:738–751.
  • Wada, T., T. Takagi, Y. Yamaguchi, A. Ferdous, T. Imai, S. Hirose, S. Sugimoto, K. Yano, G. A. Hartzog, F. Winston, S. Buratowski, and H. Handa. 1998. DSIF, a novel transcription elongation factor that regulates RNA polymerase II processivity, is composed of human Spt4 and Spt5 homologs. Genes Dev. 12:343–356.
  • 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.
  • Wen, Y., and A. J. Shatkin. 1999. Transcription elongation factor hSpt5 stimulates mRNA capping. Genes Dev. 13:1774–1779.
  • Wenzel, S., B. M. Martins, P. Rörsch, and B. M. Wöhrli. 2010. Crystal structure of the human transcription elongation factor DSIF hSpt4 subunit in complex with the hSpt5 dimerization interface. Biochem. J. 425:373–380.
  • West, M. L., and J. L. Corden. 1995. Construction and analysis of yeast RNA polymerase II CTD deletion and substitution mutations. Genetics 140:1223–1233.
  • Wu, C. H., Y. Yamaguchi, L. R. Benjamin, M. Horvat-Gordon, J. Washinky, E. Enerly, J. Larsson, A. Lambertsson, H. Handa, and D. Gilmour. 2003. NELF and DSIF cause promoter proximal pausing on the hsp70 promoter in Drosophila. Genes Dev. 17:1402–1414.
  • Yamada, T., Y. Yamaguchi, N. Inukai, S. Okamoto, T. Mura, and H. Handa. 2006. P-TEFb-mediated phosphorylation of hSpt5 C-terminal repeats is critical for processive transcription elongation. Mol. Cell 21:227–237.
  • Yue, Z., E. Maldonado, R. Pillutla, H. Cho, D. Reinberg, and A. J. Shatkin. 1997. Mammalian capping enzyme complements mutant S. cerevisiae lacking mRNA guanylyltransferase and selectively binds the elongating form of RNA polymerase II. Proc. Natl. Acad. Sci. U. S. A. 94:12898–12903.
  • Zhou, K., W. H. W. Kuo, J. Fillingham, and J. F. Greenblatt. 2009. Control of transcriptional histone modification by the yeast BUR kinase substrate Spt5. Proc. Natl. Acad. Sci. U. S. A. 106:6956–6961.

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