The C-Terminal Domain of RNA Polymerase II Functions as a Phosphorylation-Dependent Splicing Activator in a Heterologous Protein

REFERENCES

• Bauren, G., and L. Wieslander. 1994. Splicing of Balbiani ring 1 gene pre-mRNA occurs simultaneously with transcription. Cell 76:183–192.
   PubMed Web of Science ®Google Scholar
• Bentley, D. 2002. The mRNA assembly line: transcription and processing machines in the same factory. Curr. Opin. Cell Biol. 14:336–342.
   PubMed Web of Science ®Google Scholar
• Beyer, A. L., and Y. N. Osheim. 1988. Splice site selection, rate of splicing, and alternative splicing on nascent transcripts. Genes Dev. 2:754–765.
   PubMed Web of Science ®Google Scholar
• Bregman, D. B., L. Du, S. van der Zee, and S. L. Warren. 1995. Transcription-dependent redistribution of the large subunit of RNA polymerase II to discrete nuclear domains. J. Cell Biol. 129:287–298.
   PubMedGoogle Scholar
• Caputi, M., A. Mayeda, A. R. Krainer, and A. M. Zahler. 1999. hnRNP A/B proteins are required for inhibition of HIV-1 pre-mRNA splicing. EMBO J. 18:4060–4067.
   PubMed Web of Science ®Google Scholar
• Chabot, B., S. Bisotto, and M. Vincent. 1995. The nuclear matrix phosphoprotein p255 associates with splicing complexes as part of the [U4/U6. U5] tri-snRNP particle. Nucleic Acids Res. 23:3206–3213.
   PubMed Web of Science ®Google Scholar
• Cheng, C., and P. A. Sharp. 2003. RNA polymerase II accumulation in the promoter-proximal region of the dihydrofolate reductase and γ-actin genes. Mol. Cell. Biol. 23:1961–1967.
   PubMedGoogle 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. 1990. Tails of RNA polymerase II. Trends Biochem. Sci. 15:383–387.
   PubMed Web of Science ®Google Scholar
• Corden, J. L., and M. Patturajan. 1997. A CTD function linking transcription to splicing. Trends Biochem. Sci. 22:413–416.
   PubMedGoogle Scholar
• Crispino, J. D., B. J. Blencowe, and P. A. Sharp. 1994. Complementation by SR proteins of pre-mRNA splicing reactions depleted of U1 snRNP. Science 265:1866–1869.
   PubMed Web of Science ®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
• Das, R., and R. Reed. 1999. Resolution of the mammalian E complex and the ATP-dependent spliceosomal complexes on native agarose mini-gels. RNA 5:1504–1508.
   PubMed Web of Science ®Google Scholar
• Das, R., Z. Zhou, and R. Reed. 2000. Functional association of U2 snRNP with the ATP-independent spliceosomal complex E. Mol. Cell 5:779–787.
   PubMed Web of Science ®Google Scholar
• Dignam, J. D., R. M. Lebovitz, and R. G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475–1489.
   PubMed Web of Science ®Google Scholar
• Dubois, M. F., M. Vincent, M. Vigneron, J. Adamczewski, J. M. Egly, and O. Bensaude. 1997. Heat-shock inactivation of the TFIIH-associated kinase and change in the phosphorylation sites on the C-terminal domain of RNA polymerase II. Nucleic Acids Res. 25:694–700.
   PubMed Web of Science ®Google Scholar
• Emili, A., M. Shales, S. McCracken, W. Xie, P. W. Tucker, R. Kobayashi, B. J. Blencowe, and C. J. Ingles. 2002. Splicing and transcription-associated proteins PSF and p54nrb/nonO bind to the RNA polymerase II CTD. RNA 8:1102–1111.
   PubMed Web of Science ®Google Scholar
• Fong, N., and D. L. Bentley. 2001. Capping, splicing, and 3′ processing are independently stimulated by RNA polymerase II: different functions for different segments of the CTD. Genes Dev. 15:1783–1795.
   PubMed Web of Science ®Google Scholar
• Fong, Y. W., and Q. Zhou. 2000. Relief of two built-in autoinhibitory mechanisms in P-TEFb is required for assembly of a multicomponent transcription elongation complex at the human immunodeficiency virus type 1 promoter. Mol. Cell. Biol. 20:5897–5907.
   PubMed Web of Science ®Google Scholar
• Fong, Y. W., and Q. Zhou. 2001. Stimulatory effect of splicing factors on transcriptional elongation. Nature 414:929–933.
   PubMed Web of Science ®Google Scholar
• Fu, X. D. 1993. Specific commitment of different pre-mRNAs to splicing by single SR proteins. Nature 365:82–85.
   PubMed Web of Science ®Google Scholar
• Gozani, O., J. G. Patton, and R. Reed. 1994. A novel set of spliceosome-associated proteins and the essential splicing factor PSF bind stably to pre-mRNA prior to catalytic step II of the splicing reaction. EMBO J. 13:3356–3367.
   PubMedGoogle Scholar
• Graveley, B. R. 2000. Sorting out the complexity of SR protein functions. RNA 6:1197–1211.
   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
• Hirose, Y., and J. L. Manley. 1998. RNA polymerase II is an essential mRNA polyadenylation factor. Nature 395:93–96.
   PubMed Web of Science ®Google Scholar
• Hirose, Y., R. Tacke, and J. L. Manley. 1999. Phosphorylated RNA polymerase II stimulates pre-mRNA splicing. Genes Dev. 13:1234–1239.
   PubMed Web of Science ®Google Scholar
• Ho, C. K., and S. Shuman. 1999. Distinct roles for CTD Ser-2 and Ser-5 phosphorylation in the recruitment and allosteric activation of mammalian mRNA capping enzyme. Mol. Cell 3:405–411.
   PubMed Web of Science ®Google Scholar
• Jamison, S. F., Z. Pasman, J. Wang, C. Will, R. Luhrmann, J. L. Manley, and M. A. Garcia-Blanco. 1995. U1 snRNP-ASF/SF2 interaction and 5′ splice site recognition: characterization of required elements. Nucleic Acids Res. 23:3260–3267.
   PubMed Web of Science ®Google Scholar
• Jurica, M. S., and M. J. Moore. 2003. Pre-mRNA splicing: awash in a sea of proteins. Mol. Cell 12:5–14.
   PubMed Web of Science ®Google Scholar
• Kameoka, S., P. Duque, and M. M. Konarska. 2004. p54(nrb) associates with the 5′ splice site within large transcription/splicing complexes. EMBO J. 23:1782–1791.
   PubMedGoogle Scholar
• Kim, E., L. Du, D. B. Bregman, and S. L. Warren. 1997. Splicing factors associate with hyperphosphorylated RNA polymerase II in the absence of pre-mRNA. J. Cell Biol. 136:19–28.
   PubMed Web of Science ®Google Scholar
• Kohtz, J. D., S. F. Jamison, C. L. Will, P. Zuo, R. Luhrmann, M. A. Garcia-Blanco, and J. L. Manley. 1994. Protein-protein interactions and 5′-splice-site recognition in mammalian mRNA precursors. Nature 368:119–124.
   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
• Krainer, A. R., G. C. Conway, and D. Kozak. 1990. Purification and characterization of pre-mRNA splicing factor SF2 from HeLa cells. Genes Dev. 4:1158–1171.
   PubMed Web of Science ®Google Scholar
• Kramer, A. 1996. The structure and function of proteins involved in mammalian pre-mRNA splicing. Annu. Rev. Biochem. 65:367–409.
   PubMed Web of Science ®Google Scholar
• Maniatis, T., and R. Reed. 2002. An extensive network of coupling among gene expression machines. Nature 416:499–506.
   PubMed Web of Science ®Google Scholar
• Manley, J. L., and R. Tacke. 1996. SR proteins and splicing control. Genes Dev. 10:1569–1579.
   PubMed Web of Science ®Google Scholar
• McCracken, S., N. Fong, K. Yankulov, S. Ballantyne, G. 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
• Michaud, S., and R. Reed. 1991. An ATP-independent complex commits pre-mRNA to the mammalian spliceosome assembly pathway. Genes Dev. 5:2534–2546.
   PubMedGoogle Scholar
• Morris, D. P., and A. L. Greenleaf. 2000. The splicing factor, Prp40, binds the phosphorylated carboxyl-terminal domain of RNA polymerase II. J. Biol. Chem. 275:39935–39943.
   PubMed Web of Science ®Google Scholar
• Mortillaro, M. J., B. J. Blencowe, X. Wei, H. Nakayasu, L. Du, S. L. Warren, P. A. Sharp, and R. Berezney. 1996. A hyperphosphorylated form of the large subunit of RNA polymerase II is associated with splicing complexes and the nuclear matrix. Proc. Natl. Acad. Sci. USA 93:8253–8257.
   PubMed Web of Science ®Google Scholar
• Nilsen, T. W. 2003. The spliceosome: the most complex macromolecular machine in the cell. Bioessays 25:1147–1149.
   PubMed Web of Science ®Google Scholar
• Patton, J. G., E. B. Porro, J. Galceran, P. Tempst, and B. Nadal-Ginard. 1993. Cloning and characterization of PSF, a novel pre-mRNA splicing factor. Genes Dev. 7:393–406.
   PubMed Web of Science ®Google Scholar
• Patturajan, M., R. J. Schulte, 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
• Patturajan, M., X. Wei, R. Berezney, and J. L. Corden. 1998. A nuclear matrix protein interacts with the phosphorylated C-terminal domain of RNA polymerase II. Mol. Cell. Biol. 18:2406–2415.
   PubMed Web of Science ®Google Scholar
• Perriman, R., and M. Ares, Jr. 2000. ATP can be dispensable for prespliceosome formation in yeast. Genes Dev. 14:97–107.
   PubMed Web of Science ®Google Scholar
• Peterson, S. R., A. Dvir, C. W. Anderson, and W. S. Dynan. 1992. DNA binding provides a signal for phosphorylation of the RNA polymerase II heptapeptide repeats. Genes Dev. 6:426–438.
   PubMedGoogle Scholar
• Proudfoot, N. J., A. Furger, and M. J. Dye. 2002. Integrating mRNA processing with transcription. Cell 108:501–512.
   PubMed Web of Science ®Google Scholar
• Ramanathan, Y., S. M. Rajpara, S. M. Reza, E. Lees, S. Shuman, M. B. Mathews, and T. Pe'ery. 2001. Three RNA polymerase II carboxyl-terminal domain kinases display distinct substrate preferences. J. Biol. Chem. 276:10913–10920.
   PubMed Web of Science ®Google Scholar
• Reed, R. 1990. Protein composition of mammalian spliceosomes assembled in vitro. Proc. Natl. Acad. Sci. USA 87:8031–8035.
   PubMed Web of Science ®Google Scholar
• Sharp, P. A. 1994. Split genes and RNA splicing. Cell 77:805–815.
   PubMed Web of Science ®Google Scholar
• Staknis, D., and R. Reed. 1994. SR proteins promote the first specific recognition of pre-mRNA and are present together with the U1 small nuclear ribonucleoprotein particle in a general splicing enhancer complex. Mol. Cell. Biol. 14:7670–7682.
   PubMed Web of Science ®Google Scholar
• Tacke, R., and J. L. Manley. 1995. The human splicing factors ASF/SF2 and SC35 possess distinct, functionally significant RNA binding specificities. EMBO J. 14:3540–3551.
   PubMed Web of Science ®Google Scholar
• Tacke, R., M. Tohyama, S. Ogawa, and J. L. Manley. 1998. Human Tra2 proteins are sequence-specific activators of pre-mRNA splicing. Cell 93:139–148.
   PubMed Web of Science ®Google Scholar
• Tange, T. O., and J. Kjems. 2001. SF2/ASF binds to a splicing enhancer in the third HIV-1 tat exon and stimulates U2AF binding independently of the RS domain. J. Mol. Biol. 312:649–662.
   PubMed Web of Science ®Google Scholar
• Trigon, S., H. Serizawa, J. W. Conaway, R. C. Conaway, S. P. Jackson, and M. Morange. 1998. Characterization of the residues phosphorylated in vitro by different C-terminal domain kinases. J. Biol. Chem. 273:6769–6775.
   PubMed Web of Science ®Google Scholar
• Vincent, M., P. Lauriault, M. F. Dubois, S. Lavoie, O. Bensaude, and B. Chabot. 1996. The nuclear matrix protein p255 is a highly phosphorylated form of RNA polymerase II largest subunit which associates with spliceosomes. Nucleic Acids Res. 24:4649–4652.
   PubMedGoogle Scholar
• Watakabe, A., K. Tanaka, and Y. Shimura. 1993. The role of exon sequences in splice site selection. Genes Dev. 7:407–418.
   PubMed Web of Science ®Google Scholar
• Wu, J. Y., and T. Maniatis. 1993. Specific interactions between proteins implicated in splice site selection and regulated alternative splicing. Cell 75:1061–1070.
   PubMed Web of Science ®Google Scholar
• Yan, D., R. Perriman, H. Igel, K. J. Howe, M. Neville, and M. Ares, Jr. 1998. CUS2, a yeast homolog of human Tat-SF1, rescues function of misfolded U2 through an unusual RNA recognition motif. Mol. Cell. Biol. 18:5000–5009.
   PubMed Web of Science ®Google Scholar
• Yuryev, A., M. Patturajan, Y. Litingtung, R. V. Joshi, C. Gentile, M. Gebara, and J. L. Corden. 1996. The C-terminal domain of the largest subunit of RNA polymerase II interacts with a novel set of serine/arginine-rich proteins. Proc. Natl. Acad. Sci. USA 93:6975–6980.
   PubMed Web of Science ®Google Scholar
• Zeng, C., and S. M. Berget. 2000. Participation of the C-terminal domain of RNA polymerase II in exon definition during pre-mRNA splicing. Mol. Cell. Biol. 20:8290–8301.
   PubMed Web of Science ®Google Scholar
• Zhang, J., and J. L. Corden. 1991. Identification of phosphorylation sites in the repetitive carboxyl-terminal domain of the mouse RNA polymerase II largest subunit. J. Biol. Chem. 266:2290–2296.
   PubMedGoogle Scholar
• Zhang, J., and J. L. Corden. 1991. Phosphorylation causes a conformational change in the carboxyl-terminal domain of the mouse RNA polymerase II largest subunit. J. Biol. Chem. 266:2297–2302.
   PubMedGoogle 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 carboxyl-terminal domain during human immunodeficiency virus type 1 transcription. Mol. Cell. Biol. 20:5077–5086.
   PubMed Web of Science ®Google Scholar
• Zhu, J., A. Mayeda, and A. R. Krainer. 2001. Exon identity established through differential antagonism between exonic splicing silencer-bound hnRNP A1 and enhancer-bound SR proteins. Mol. Cell 8:1351–1361.
   PubMedGoogle Scholar
• Zuo, P., and J. L. Manley. 1993. Functional domains of the human splicing factor ASF/SF2. EMBO J. 12:4727–4737.
   PubMed Web of Science ®Google Scholar
• Zuo, P., and J. L. Manley. 1994. The human splicing factor ASF/SF2 can specifically recognize pre-mRNA 5′ splice sites. Proc. Natl. Acad. Sci. USA 91:3363–3367.
   PubMedGoogle Scholar