Structure and dynamics of the RNAPII CTDsome with Rtt103
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem, audiovizuální média
PubMed
29073019
PubMed Central
PMC5651779
DOI
10.1073/pnas.1712450114
PII: 1712450114
Knihovny.cz E-zdroje
- Klíčová slova
- CTD, RNA polymerase II, Rtt103, structural biology, transcription,
- MeSH
- interakční proteinové domény a motivy MeSH
- krystalografie rentgenová MeSH
- magnetická rezonanční spektroskopie MeSH
- multimerizace proteinu MeSH
- RNA-polymerasa II metabolismus MeSH
- Saccharomyces cerevisiae - proteiny chemie metabolismus MeSH
- sekvence aminokyselin MeSH
- transkripční faktory chemie metabolismus MeSH
- Publikační typ
- audiovizuální média MeSH
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- RNA-polymerasa II MeSH
- Rtt103 protein, S cerevisiae MeSH Prohlížeč
- Saccharomyces cerevisiae - proteiny MeSH
- transkripční faktory MeSH
RNA polymerase II contains a long C-terminal domain (CTD) that regulates interactions at the site of transcription. The CTD architecture remains poorly understood due to its low sequence complexity, dynamic phosphorylation patterns, and structural variability. We used integrative structural biology to visualize the architecture of the CTD in complex with Rtt103, a 3'-end RNA-processing and transcription termination factor. Rtt103 forms homodimers via its long coiled-coil domain and associates densely on the repetitive sequence of the phosphorylated CTD via its N-terminal CTD-interacting domain. The CTD-Rtt103 association opens the compact random coil structure of the CTD, leading to a beads-on-a-string topology in which the long rod-shaped Rtt103 dimers define the topological and mobility restraints of the entire assembly. These findings underpin the importance of the structural plasticity of the CTD, which is templated by a particular set of CTD-binding proteins.
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Eick D, Geyer M. The RNA polymerase II carboxy-terminal domain (CTD) code. Chem Rev. 2013;113:8456–8490. PubMed
Chapman RD, Heidemann M, Hintermair C, Eick D. Molecular evolution of the RNA polymerase II CTD. Trends Genet. 2008;24:289–296. PubMed
Harlen KM, Churchman LS. The code and beyond: Transcription regulation by the RNA polymerase II carboxy-terminal domain. Nat Rev Mol Cell Biol. 2017;18:263–273. PubMed
West ML, Corden JL. Construction and analysis of yeast RNA polymerase II CTD deletion and substitution mutations. Genetics. 1995;140:1223–1233. PubMed PMC
Liu P, Kenney JM, Stiller JW, Greenleaf AL. Genetic organization, length conservation, and evolution of RNA polymerase II carboxyl-terminal domain. Mol Biol Evol. 2010;27:2628–2641. PubMed PMC
Buratowski S. The CTD code. Nat Struct Biol. 2003;10:679–680. PubMed
Mayer A, et al. Uniform transitions of the general RNA polymerase II transcription complex. Nat Struct Mol Biol. 2010;17:1272–1278. PubMed
Mayer A, et al. CTD tyrosine phosphorylation impairs termination factor recruitment to RNA polymerase II. Science. 2012;336:1723–1725. PubMed
Bataille AR, et al. A universal RNA polymerase II CTD cycle is orchestrated by complex interplays between kinase, phosphatase, and isomerase enzymes along genes. Mol Cell. 2012;45:158–170. PubMed
Kim H, et al. Gene-specific RNA polymerase II phosphorylation and the CTD code. Nat Struct Mol Biol. 2010;17:1279–1286. PubMed PMC
Tietjen JR, et al. Chemical-genomic dissection of the CTD code. Nat Struct Mol Biol. 2010;17:1154–1161. PubMed PMC
Heidemann M, Hintermair C, Voß K, Eick D. Dynamic phosphorylation patterns of RNA polymerase II CTD during transcription. Biochim Biophys Acta. 2013;1829:55–62. PubMed
Suh H, et al. Direct analysis of phosphorylation sites on the Rpb1 C-terminal domain of RNA polymerase II. Mol Cell. 2016;61:297–304. PubMed PMC
Schüller R, et al. Heptad-specific phosphorylation of RNA polymerase II CTD. Mol Cell. 2016;61:305–314. PubMed
Harlen KM, et al. Comprehensive RNA polymerase II interactomes reveal distinct and varied roles for each phospho-CTD residue. Cell Rep. 2016;15:2147–2158. PubMed PMC
Cramer P, et al. Architecture of RNA polymerase II and implications for the transcription mechanism. Science. 2000;288:640–649. PubMed
Cramer P, Bushnell DA, Kornberg RD. Structural basis of transcription: RNA polymerase II at 2.8 angstrom resolution. Science. 2001;292:1863–1876. PubMed
Spåhr H, Calero G, Bushnell DA, Kornberg RD. Schizosacharomyces pombe RNA polymerase II at 3.6-A resolution. Proc Natl Acad Sci USA. 2009;106:9185–9190. PubMed PMC
Meinhart A, Kamenski T, Hoeppner S, Baumli S, Cramer P. A structural perspective of CTD function. Genes Dev. 2005;19:1401–1415. PubMed
Meredith GD, et al. The C-terminal domain revealed in the structure of RNA polymerase II. J Mol Biol. 1996;258:413–419. PubMed
Tsai K-L, et al. A conserved Mediator-CDK8 kinase module association regulates Mediator-RNA polymerase II interaction. Nat Struct Mol Biol. 2013;20:611–619. PubMed PMC
Portz B, et al. Structural heterogeneity in the intrinsically disordered RNA polymerase II C-terminal domain. Nat Commun. 2017;8:15231. PubMed PMC
Gibbs EB, et al. Phosphorylation induces sequence-specific conformational switches in the RNA polymerase II C-terminal domain. Nat Commun. 2017;8:15233. PubMed PMC
Jasnovidova O, Stefl R. The CTD code of RNA polymerase II: A structural view. Wiley Interdiscip Rev RNA. 2013;4:1–16. PubMed
Barillà D, Lee BA, Proudfoot NJ. Cleavage/polyadenylation factor IA associates with the carboxyl-terminal domain of RNA polymerase II in Saccharomyces cerevisiae. Proc Natl Acad Sci USA. 2001;98:445–450. PubMed PMC
Meinhart A, Cramer P. Recognition of RNA polymerase II carboxy-terminal domain by 3′-RNA-processing factors. Nature. 2004;430:223–226. PubMed
Ni Z, et al. RPRD1A and RPRD1B are human RNA polymerase II C-terminal domain scaffolds for Ser5 dephosphorylation. Nat Struct Mol Biol. 2014;21:686–695. PubMed PMC
Grigoryan G, Degrado WF. Probing designability via a generalized model of helical bundle geometry. J Mol Biol. 2011;405:1079–1100. PubMed PMC
Lunde BM, et al. Cooperative interaction of transcription termination factors with the RNA polymerase II C-terminal domain. Nat Struct Mol Biol. 2010;17:1195–1201. PubMed PMC
Jasnovidova O, Krejcikova M, Kubicek K, Stefl R. Structural insight into recognition of phosphorylated threonine-4 of RNA polymerase II C-terminal domain by Rtt103p. EMBO Rep. 2017;18:906–913. PubMed PMC
Tria G, Mertens HDT, Kachala M, Svergun DI. Advanced ensemble modelling of flexible macromolecules using X-ray solution scattering. IUCrJ. 2015;2:207–217. PubMed PMC
Franke D, Svergun DI. DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering. J Appl Crystallogr. 2009;42:342–346. PubMed PMC
Petoukhov MV, et al. New developments in the ATSAS program package for small-angle scattering data analysis. J Appl Crystallogr. 2012;45:342–350. PubMed PMC
Vasiljeva L, Kim M, Mutschler H, Buratowski S, Meinhart A. The Nrd1-Nab3-Sen1 termination complex interacts with the Ser5-phosphorylated RNA polymerase II C-terminal domain. Nat Struct Mol Biol. 2008;15:795–804. PubMed PMC
Xu X, Pérébaskine N, Minvielle-Sébastia L, Fribourg S, Mackereth CD. Chemical shift assignments of a new folded domain from yeast Pcf11. Biomol NMR Assign. 2015;9:421–425. PubMed
Mei K, et al. Structural basis for the recognition of RNA polymerase II C-terminal domain by CREPT and p15RS. Sci China Life Sci. 2014;57:97–106. PubMed
Becker R, Loll B, Meinhart A. Snapshots of the RNA processing factor SCAF8 bound to different phosphorylated forms of the carboxyl-terminal domain of RNA polymerase II. J Biol Chem. 2008;283:22659–22669. PubMed
Kubicek K, et al. Serine phosphorylation and proline isomerization in RNAP II CTD control recruitment of Nrd1. Genes Dev. 2012;26:1891–1896. PubMed PMC
Noble CG, et al. Key features of the interaction between Pcf11 CID and RNA polymerase II CTD. Nat Struct Mol Biol. 2005;12:144–151. PubMed
Svergun DI. Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing. Biophys J. 1999;76:2879–2886. PubMed PMC
Mossessova E, Lima CD. Ulp1-SUMO crystal structure and genetic analysis reveal conserved interactions and a regulatory element essential for cell growth in yeast. Mol Cell. 2000;5:865–876. PubMed
Svergun D, Barberato C, Koch MHJ. CRYSOL–A program to evaluate X-ray solution scattering of biological macromolecules from atomic coordinates. J Appl Crystallogr. 1995;28:768–773.
Kozin MB, Svergun DI. Automated matching of high- and low-resolution structural models. J Appl Crystallogr. 2001;34:33–41.
Kuzmic P. DynaFit–A software package for enzymology. Methods Enzymol. 2009;467:247–280. PubMed
Kabsch W. XDS. Acta Crystallogr D Biol Crystallogr. 2010;66:125–132. PubMed PMC
Evans P. Scaling and assessment of data quality. Acta Crystallogr D Biol Crystallogr. 2006;62:72–82. PubMed
Winn MD, et al. Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr. 2011;67:235–242. PubMed PMC
Adams PD, et al. The Phenix software for automated determination of macromolecular structures. Methods. 2011;55:94–106. PubMed PMC
McCoy AJ, Storoni LC, Read RJ. Simple algorithm for a maximum-likelihood SAD function. Acta Crystallogr D Biol Crystallogr. 2004;60:1220–1228. PubMed
Grosse-Kunstleve RW, Adams PD. Substructure search procedures for macromolecular structures. Acta Crystallogr D Biol Crystallogr. 2003;59:1966–1973. PubMed
Terwilliger T. SOLVE and RESOLVE: Automated structure solution, density modification and model building. J Synchrotron Radiat. 2004;11:49–52. PubMed
Terwilliger TC, et al. Decision-making in structure solution using Bayesian estimates of map quality: The PHENIX AutoSol wizard. Acta Crystallogr D Biol Crystallogr. 2009;65:582–601. PubMed PMC
Cowtan K. The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr D Biol Crystallogr. 2006;62:1002–1011. PubMed
Emsley P, Cowtan K. Coot: Model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr. 2004;60:2126–2132. PubMed
McCoy AJ, et al. Phaser crystallographic software. J Appl Crystallogr. 2007;40:658–674. PubMed PMC
Afonine PV, et al. Towards automated crystallographic structure refinement with phenix.refine. Acta Crystallogr D Biol Crystallogr. 2012;68:352–367. PubMed PMC
Pettersen EF, et al. UCSF Chimera–A visualization system for exploratory research and analysis. J Comput Chem. 2004;25:1605–1612. PubMed
Walshaw J, Woolfson DN. Socket: A program for identifying and analysing coiled-coil motifs within protein structures. J Mol Biol. 2001;307:1427–1450. PubMed
Larkin MA, et al. Clustal W and Clustal X version 2.0. Bioinformatics. 2007;23:2947–2948. PubMed
Sequence and structural determinants of RNAPII CTD phase-separation and phosphorylation by CDK7
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PDB
5M48, 5M9D