An mRNA Capping Enzyme Targets FACT to the Active Gene To Enhance the Engagement of RNA Polymerase II into Transcriptional Elongation

REFERENCES

• Nechaev S, Adelman K. 2011. Pol II waiting in the starting gates: regulating the transition from transcription initiation into productive elongation. Biochim Biophys Acta 1809:34–45. https://doi.org/10.1016/j.bbagrm.2010.11.001.
   PubMed Web of Science ®Google Scholar
• Li J, Gilmour DS. 2011. Promoter proximal pausing and the control of gene expression. Curr Opin Genet Dev 21:231–235. https://doi.org/10.1016/j.gde.2011.01.010.
   PubMed Web of Science ®Google Scholar
• Hirtreiter A, Damsma GE, Cheung AC, Klose D, Grohmann D, Vojnic E, Martin AC, Cramer P, Werner F. 2010. Spt4/5 stimulates transcription elongation through the RNA polymerase clamp coiled-coil motif. Nucleic Acids Res 38:4040–4051. https://doi.org/10.1093/nar/gkq135.
   PubMed Web of Science ®Google Scholar
• Rahl PB, Lin CY, Seila AC, Flynn RA, McCuine S, Burge CB, Sharp PA, Young RA. 2010. c-Myc regulates transcriptional pause release. Cell 141:432–445. https://doi.org/10.1016/j.cell.2010.03.030.
   PubMed Web of Science ®Google Scholar
• Barboric M, Nissen RM, Kanazawa S, Jabrane-Ferrat N, Peterlin BM. 2001. NF-kappaB binds P-TEFb to stimulate transcriptional elongation by RNA polymerase II. Mol Cell 8:327–337. https://doi.org/10.1016/S1097-2765(01)00314-8.
   PubMed Web of Science ®Google Scholar
• Hargreaves DC, Horng T, Medzhitov R. 2009. Control of inducible gene expression by signal-dependent transcriptional elongation. Cell 138:129–145. https://doi.org/10.1016/j.cell.2009.05.047.
   PubMed Web of Science ®Google Scholar
• Donner AJ, Ebmeier CC, Taatjes DJ, Espinosa JM. 2010. CDK8 is a positive regulator of transcriptional elongation within the serum response network. Nat Struct Mol Biol 17:194–201. https://doi.org/10.1038/nsmb.1752.
   PubMed Web of Science ®Google Scholar
• Diribarne G, Bensaude O. 2009. 7SK RNA, a non-coding RNA regulating P-TEFb, a general transcription factor. RNA Biol 6:122–128. https://doi.org/10.4161/rna.6.2.8115.
   PubMed Web of Science ®Google Scholar
• Peterlin BM, Price DH. 2006. Controlling the elongation phase of transcription with P-TEFb. Mol Cell 23:297–305. https://doi.org/10.1016/j.molcel.2006.06.014.
   PubMed Web of Science ®Google Scholar
• Baugh LR, Demodena J, Sternberg PW. 2009. RNA Pol II accumulates at promoters of growth genes during developmental arrest. Science 324:92–94. https://doi.org/10.1126/science.1169628.
   PubMedGoogle Scholar
• Lahudkar S, Durairaj G, Uprety B, Bhaumik SR. 2014. A novel role for Cet1p mRNA 5′-triphosphatase in promoter proximal accumulation of RNA polymerase II in Saccharomyces cerevisiae. Genetics 196:161–176. https://doi.org/10.1534/genetics.113.158535.
   PubMed Web of Science ®Google Scholar
• Kim TS, Liu CL, Yassour M, Holik J, Friedman N, Buratowski S, Rando O. 2010. RNA polymerase mapping during stress responses reveals widespread nonproductive transcription in yeast. Genome Biol 11:R75. https://doi.org/10.1186/gb-2010-11-7-r75.
   PubMed Web of Science ®Google Scholar
• McCracken S, Rosonina E, Fong N, Sikes M, Beyer A, O'Hare K, Shuman S, Bentley D. 1998. Role of RNA polymerase II carboxy-terminal domain in coordinating transcription with RNA processing. Cold Spring Harbor Symp Quant Biol 63:301–309. https://doi.org/10.1101/sqb.1998.63.301.
   PubMedGoogle Scholar
• Rodríguez-Molina JB, Tseng SC, Simonett SP, Taunton J, Ansari AZ. 2016. Engineered covalent inactivation of TFIIH-kinase reveals an elongation checkpoint and results in widespread mRNA stabilization. Mol Cell 63:433–444. https://doi.org/10.1016/j.molcel.2016.06.036.
   PubMed Web of Science ®Google Scholar
• Cho EJ, Rodriguez CR, Takagi T, Buratowski S. 1998. Allosteric interactions between capping enzyme subunits and the RNA polymerase II carboxy-terminal domain. Genes Dev 12:3482–3487. https://doi.org/10.1101/gad.12.22.3482.
   PubMedGoogle Scholar
• Rodriguez CR, Takagi T, Cho EJ, Buratowski S. 1999. A Saccharomyces cerevisiae RNA 5′-triphosphatase related to mRNA capping enzyme. Nucleic Acids Res 27:2181–2188. https://doi.org/10.1093/nar/27.10.2181.
   PubMedGoogle Scholar
• Winkler DD, Luger K. 2011. The histone chaperone FACT: structural insights and mechanisms for nucleosome reorganization. J Biol Chem 286:18369–18374. https://doi.org/10.1074/jbc.R110.180778.
   PubMed Web of Science ®Google Scholar
• Formosa T. 2013. The role of FACT in making and breaking nucleosomes. Biochim Biophys Acta 1819:247–255. https://doi.org/10.1016/j.bbagrm.2011.07.009.
   PubMed Web of Science ®Google Scholar
• Reinberg D, Sims RJ, III. 2006. De facto nucleosome dynamics. J Biol Chem 28123297–23301.
   PubMed Web of Science ®Google Scholar
• Fresco LD, Buratowski S. 1996. Conditional mutants of the yeast mRNA capping enzyme show that the cap enhances, but is not required for, mRNA splicing. RNA 2:584–596.
   PubMedGoogle Scholar
• Takase Y, Takagi T, Komarnitsky PB, Buratowski S. 2000. The essential interaction between yeast mRNA capping enzyme subunits is not required for triphosphatase function in vivo. Mol Cell Biol 20:9307–9316. https://doi.org/10.1128/MCB.20.24.9307-9316.2000.
   PubMedGoogle Scholar
• Zheng S, Crickard JB, Srikanth A, Reese JC. 2014. A highly conserved region within H2B is important for FACT to act on nucleosomes. Mol Cell Biol 34:303–314. https://doi.org/10.1128/MCB.00478-13.
   PubMed Web of Science ®Google Scholar
• Duina AA. 2011. Histone chaperones Spt6 and FACT: similarities and differences in modes of action at transcribed genes. Genet Res Int 2011:625210. https://doi.org/10.4061/2011/625210.
   PubMedGoogle Scholar
• Lahudkar S, Shukla A, Bajwa P, Durairaj G, Stanojevic N, Bhaumik SR. 2011. The mRNA cap-binding complex stimulates the formation of pre-initiation complex at the promoter via its interaction with Mot1p in vivo. Nucleic Acids Res 39:2188–2209. https://doi.org/10.1093/nar/gkq1029.
   PubMed Web of Science ®Google Scholar
• Hall DB, Struhl K. 2002. The VP16 activation domain interacts with multiple transcriptional components as determined by protein-protein cross-linking in vivo. J Biol Chem 277:46043–46050. https://doi.org/10.1074/jbc.M208911200.
   PubMedGoogle Scholar
• Sen R, Ferdoush J, Kaja A, Bhaumik SR. 2016. Fine-tuning of FACT by the ubiquitin proteasome system in regulation of transcriptional elongation. Mol Cell Biol 36:1691–1703. https://doi.org/10.1128/MCB.01112-15.
   PubMed Web of Science ®Google Scholar
• Mason PB, Struhl K. 2003. The FACT complex travels with elongating RNA polymerase II and is important for the fidelity of transcriptional initiation in vivo. Mol Cell Biol 23:8323–8333. https://doi.org/10.1128/MCB.23.22.8323-8333.2003.
   PubMed Web of Science ®Google Scholar
• Wyce A, Xiao T, Whelan KA, Kosman C, Walter W, Eick D, Hughes TR, Krogan NJ, Strahl BD, Berger SL. 2007. H2B ubiquitylation acts as a barrier to Ctk1 nucleosomal recruitment prior to removal by Ubp8 within a SAGArelated complex. Mol Cell 27:275–288. https://doi.org/10.1016/j.molcel.2007.01.035.
   PubMed Web of Science ®Google Scholar
• Biswas D, Dutta-Biswas R, Mitra D, Shibata Y, Strahl BD, Formosa T, Stillman DJ. 2006. Opposing roles for Set2 and yFACT in regulating TBP binding at promoters. EMBO J 25:4479–4489. https://doi.org/10.1038/sj.emboj.7601333.
   PubMed Web of Science ®Google Scholar
• Ransom M, Williams SK, Dechassa ML, Das C, Linger J, Adkins M, Liu C, Bartholomew B, Tyler JK. 2009. FACT and the proteasome promote promoter chromatin disassembly and transcriptional initiation. J Biol Chem 284:23461–23471. https://doi.org/10.1074/jbc.M109.019562.
   PubMed Web of Science ®Google Scholar
• Fleming AB, Kao CF, Hillyer C, Pikaart M, Osley MA. 2008. H2B ubiquitylation plays a role in nucleosome dynamics during transcription elongation. Mol Cell 31:57–66. https://doi.org/10.1016/j.molcel.2008.04.025.
   PubMed Web of Science ®Google Scholar
• Durairaj G, Chaurasia P, Lahudkar S, Malik S, Shukla A, Bhaumik SR. 2010. Regulation of chromatin assembly/disassembly by Rtt109p, a histone H3 Lys56-specific acetyltransferase, in vivo. J Biol Chem 285:30472–30479. https://doi.org/10.1074/jbc.M110.113225.
   PubMed Web of Science ®Google Scholar
• Jaehning JA. 2010. The Paf1 complex: platform or player in RNA polymerase II transcription? Biochim Biophys Acta 1799:379–388. https://doi.org/10.1016/j.bbagrm.2010.01.001.
   PubMed Web of Science ®Google Scholar
• Squazzo SL, Costa PJ, Lindstrom DL, Kumer KE, Simic R, Jennings JL, Link AJ, Arndt KM, Hartzog GA. 2002. The Paf1 complex physically and functionally associates with transcription elongation factors in vivo. EMBO J 21:1764–1774. https://doi.org/10.1093/emboj/21.7.1764.
   PubMed Web of Science ®Google Scholar
• Krogan NJ, Peng WT, Cagney G, Robinson MD, Haw R, Zhong G, Guo X, Zhang X, Canadien V, Richards DP, Beattie BK, Lalev A, Zhang W, Davierwala AP, Mnaimneh S, Starostine A, Tikuisis AP, Grigull J, Datta N, Bray JE, Hughes TR, Emili A, Greenblatt JF. 2004. High-definition macromolecular composition of yeast RNA-processing complexes. Mol Cell 13:225–239. https://doi.org/10.1016/S1097-2765(04)00003-6.
   PubMed Web of Science ®Google Scholar
• Krogan NJ, Cagney G, Yu H, Zhong G, Guo X, Ignatchenko A, Li J, Pu S, Datta N, Tikuisis AP, Punna T, Peregrín-Alvarez JM, Shales M, Zhang X, Davey M, Robinson MD, Paccanaro A, Bray JE, Sheung A, Beattie B, Richards DP, Canadien V, Lalev A, Mena F, Wong P, Starostine A, Canete MM, Vlasblom J, Wu S, Orsi C, Collins SR, Chandran S, Haw R, Rilstone JJ, Gandi K, Thompson NJ, Musso G, St Onge P, Ghanny S, Lam MH, Butland G, Altaf-Ul AM, Kanaya S, Shilatifard A, O'Shea E, Weissman JS, Ingles CJ, Hughes TR, Parkinson J, Gerstein M, Wodak SJ, Emili A, Greenblatt JF. 2006. Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 440:637–643. https://doi.org/10.1038/nature04670.
   PubMed Web of Science ®Google Scholar
• Krogan NJ, Kim M, Ahn SH, Zhong G, Kobor MS, Cagney G, Emili A, Shilatifard A, Buratowski S, Greenblatt JF. 2002. RNA polymerase II elongation factors of Saccharomyces cerevisiae: a targeted proteomics approach. Mol Cell Biol 22:6979–6992. https://doi.org/10.1128/MCB.22.20.6979-6992.2002.
   PubMed Web of Science ®Google Scholar
• Gavin AC, Aloy P, Grandi P, Krause R, Boesche M, Marzioch M, Rau C, Jensen LJ, Bastuck S, Dümpelfeld B, Edelmann A, Heurtier MA, Hoffman V, Hoefert C, Klein K, Hudak M, Michon AM, Schelder M, Schirle M, Remor M, Rudi T, Hooper S, Bauer A, Bouwmeester T, Casari G, Drewes G, Neubauer G, Rick JM, Kuster B, Bork P, Russell RB, Superti-Furga G. 2006. Proteome survey reveals modularity of the yeast cell machinery. Nature 440:631–636. https://doi.org/10.1038/nature04532.
   PubMed Web of Science ®Google Scholar
• Gavin AC, Bösche M, Krause R, Grandi P, Marzioch M, Bauer A, Schultz J, Rick JM, Michon AM, Cruciat CM, Remor M, Höfert C, Schelder M, Brajenovic M, Ruffner H, Merino A, Klein K, Hudak M, Dickson D, Rudi T, Gnau V, Bauch A, Bastuck S, Huhse B, Leutwein C, Heurtier MA, Copley RR, Edelmann A, Querfurth E, Rybin V, Drewes G, Raida M, Bouwmeester T, Bork P, Seraphin B, Kuster B, Neubauer G, Superti-Furga G. 2002. Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415:141–147. https://doi.org/10.1038/415141a.
   PubMed Web of Science ®Google Scholar
• Dronamraju R, Strahl BD. 2014. A feed forward circuit comprising Spt6, Ctk1 and PAF regulates Pol II CTD phosphorylation and transcription elongation. Nucleic Acids Res 42:870–881. https://doi.org/10.1093/nar/gkt1003.
   PubMed Web of Science ®Google Scholar
• Kaplan CD, Laprade L, Winston F. 2003. Transcription elongation factors repress transcription initiation from cryptic sites. Science 301:1096–1099. https://doi.org/10.1126/science.1087374.
   PubMed Web of Science ®Google Scholar
• DeGennaro CM, Alver BH, Marguerat S, Stepanova E, Davis CP, Bähler J, Park PJ, Winston F. 2013. Spt6 regulates intragenic and antisense transcription, nucleosome positioning, and histone modifications genome-wide in fission yeast. Mol Cell Biol 33:4779–4792. https://doi.org/10.1128/MCB.01068-13.
   PubMed Web of Science ®Google Scholar
• McCullough L, Connell Z, Petersen C, Formosa T. 2015. The abundant histone chaperones Spt6 and FACT collaborate to assemble, inspect, and maintain chromatin structure in Saccharomyces cerevisiae. Genetics 201:1031–1045. https://doi.org/10.1534/genetics.115.180794.
   PubMed Web of Science ®Google Scholar
• Liu Y, Warfield L, Zhang C, Luo J, Allen J, Lang WH, Ranish J, Shokat KM, Hahn S. 2009. Phosphorylation of the transcription elongation factor Spt5 by yeast Bur1 kinase stimulates recruitment of the PAF complex. Mol Cell Biol 29:4852–4863. https://doi.org/10.1128/MCB.00609-09.
   PubMed Web of Science ®Google Scholar
• Pruneski JA, Hainer SJ, Petrov KO, Martens JA. 2011. The Paf1 complex represses SER3 transcription in Saccharomyces cerevisiae by facilitating intergenic transcription-dependent nucleosome occupancy of the SER3 promoter. Eukaryot Cell 10:1283–1294. https://doi.org/10.1128/EC.05141-11.
   PubMedGoogle Scholar
• Yu M, Yang W, Ni T, Tang Z, Nakadai T, Zhu J, Roeder RG. 2015. RNA polymerase II-associated factor 1 regulates the release and phosphorylation of paused RNA polymerase II. Science 350:1383–1386. https://doi.org/10.1126/science.aad2338.
   PubMed Web of Science ®Google Scholar
• Longtine MS, McKenzie A, Demarini DJ, III, Shah NG, Wach A, Brachat A, Philippsen P, Pingle JR. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14:953–961.
   PubMed Web of Science ®Google Scholar
• Uprety B, Lahudkar S, Malik S, Bhaumik SR. 2012. The 19S proteasome subcomplex promotes the targeting of NuA4 HAT to the promoters of ribosomal protein genes to facilitate the recruitment of TFIID for transcriptional initiation in vivo. Nucleic Acids Res 40:1969–1983. https://doi.org/10.1093/nar/gkr977.
   PubMed Web of Science ®Google Scholar
• Malik S, Shukla A, Sen P, Bhaumik SR. 2009. The 19S proteasome subcomplex establishes a specific protein interaction network at the promoter for stimulated transcriptional initiation in vivo. J Biol Chem 284:35714–35724. https://doi.org/10.1074/jbc.M109.035709.
   PubMed Web of Science ®Google Scholar
• Durairaj G, Sen R, Uprety B, Shukla A, Bhaumik SR. 2014. Sus1p facilitates pre-initiation complex formation at the SAGA-regulated genes independently of histone H2B de-ubiquitylation. J Mol Biol 426:2928–2941. https://doi.org/10.1016/j.jmb.2014.05.028.
   PubMed Web of Science ®Google Scholar
• Bhaumik SR, Green MR. 2003. Interaction of Gal4p with components of transcription machinery in vivo. Methods Enzymol 370:445–454. https://doi.org/10.1016/S0076-6879(03)70038-X.
   PubMed Web of Science ®Google Scholar
• Shukla A, Stanojevic N, Duan Z, Sen P, Bhaumik SR. 2006. Ubp8p, a histone deubiquitinase whose association with SAGA is mediated by Sgf11p, differentially regulates lysine 4 methylation of histone H3 in vivo. Mol Cell Biol 26:3339–3352. https://doi.org/10.1128/MCB.26.9.3339-3352.2006.
   PubMed Web of Science ®Google Scholar
• Shukla A, Stanojevic N, Duan Z, Shadle T, Bhaumik SR. 2006. Functional analysis of H2B-Lys-123 ubiquitination in regulation of H3-Lys-4 methylation and recruitment of RNA polymerase II at the coding sequences of several active genes in vivo. J Biol Chem 281:19045–19054. https://doi.org/10.1074/jbc.M513533200.
   PubMed Web of Science ®Google Scholar
• Bhaumik SR, Green MR. 2002. Differential requirement of SAGA components for recruitment of TATA-box-binding protein to promoters in vivo. Mol Cell Biol 22:7365–7371. https://doi.org/10.1128/MCB.22.21.7365-7371.2002.
   PubMed Web of Science ®Google Scholar
• Uprety B, Sen R, Bhaumik SR. 2015. Eaf1p is required for recruitment of NuA4 in targeting TFIID to the promoters of the ribosomal protein genes for transcriptional initiation in vivo. Mol Cell Biol 35:2947–2964. https://doi.org/10.1128/MCB.01524-14.
   PubMed Web of Science ®Google Scholar
• Sen R, Malik S, Frankland-Searby S, Uprety B, Lahudkar S, Bhaumik SR. 2014. Rrd1p, an RNA polymerase II-specific prolyl isomerase and activator of phosphoprotein phosphatase, promotes transcription independently of rapamycin response. Nucleic Acids Res 42:9892–9907. https://doi.org/10.1093/nar/gku703.
   PubMed Web of Science ®Google Scholar
• Durairaj G, Lahudkar S, Bhaumik SR. 2014. A new regulatory pathway of mRNA export by an F-box protein, Mdm30. RNA 20:133–142. https://doi.org/10.1261/rna.042325.113.
   PubMed Web of Science ®Google Scholar
• Peterson CL, Kruger W, Herskowitz I. 1991. A functional interaction between the C-terminal domain of RNA polymerase II and the negative regulator SIN1. Cell 64:1135–1143. https://doi.org/10.1016/0092-8674(91)90268-4.
   PubMed Web of Science ®Google Scholar
• Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Struhl K. 2001. Current protocols in molecular biology. Wiley, New York, NY.
   Google Scholar
• Malik S, Durairaj G, Bhaumik SR. 2013. Mechanisms of antisense transcription initiation from the 3-end of the GAL10 coding sequence in vivo. Mol Cell Biol 33:3549–3567. https://doi.org/10.1128/MCB.01715-12.
   PubMed Web of Science ®Google Scholar
• Bhaumik SR. 2011. Distinct regulatory mechanisms of eukaryotic transcriptional activation by SAGA and TFIID. Biochim Biophys Acta 1809:97–108. https://doi.org/10.1016/j.bbagrm.2010.08.009.
   PubMed Web of Science ®Google Scholar
• Bhaumik SR, Malik S. 2008. Diverse regulatory mechanisms of eukaryotic transcriptional activation by the proteasome complex. Crit Rev Biochem Mol Biol 43:419–433. https://doi.org/10.1080/10409230802605914.
   PubMed Web of Science ®Google Scholar
• Sen R, Lahudkar S, Durairaj G, Bhaumik SR. 2013. Functional analysis of Bre1p, an E3 ligase for histone H2B ubiquitylation, in regulation of RNA polymerase II association with active genes and transcription in vivo. J Biol Chem 288:9619–9633. https://doi.org/10.1074/jbc.M113.450403.
   PubMed Web of Science ®Google Scholar
• Sen R, Bhaumik SR. 2013. Transcriptional stimulatory and repressive functions of histone H2B ubiquitin ligase. Transcription 4:221–226. https://doi.org/10.4161/trns.26623.
   PubMedGoogle Scholar
• Kim J, Roeder RG. 2009. Direct Bre1-Paf1 complex interactions and RING finger-independent Bre1-Rad6 interactions mediate histone H2B ubiquitylation in yeast. J Biol Chem 284:20582–20592. https://doi.org/10.1074/jbc.M109.017442.
   PubMed Web of Science ®Google Scholar