Architecture of the RNA polymerase II-Paf1C-TFIIS transcription elongation complex

Nature Communications

Volumn 8, Issue , 2017, Pages

  Xu, Youwei ^a   Bernecky, Carrie ^a   Lee, Chung Tien ^a,b   Maier, Kerstin C ^a   Schwalb, Björn ^a   Tegunov, Dimitry ^a   Plitzko, Jürgen M ^c   Urlaub, Henning ^a,b   Cramer, Patrick ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^c MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ELONGATION FACTOR; ELONGATION FACTOR TFIIS; INITIATION FACTOR; INITIATION FACTOR TFIIF; MESSENGER RNA; POLYMERASE ASSOCIATED FACTOR 1 COMPLEX; PROTEIN; RECOMBINANT ENZYME; RNA POLYMERASE II; RPB2 PROTEIN; RPB3 PROTEIN; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; CROSS LINKING REAGENT; CTR9 PROTEIN, S CEREVISIAE; LEO1 PROTEIN, S CEREVISIAE; MULTIPROTEIN COMPLEX; NUCLEAR PROTEIN; PAF1 PROTEIN, S CEREVISIAE; RECOMBINANT PROTEIN; RNA BINDING PROTEIN; RPB2 PROTEIN, S CEREVISIAE; RPB3 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; TRANSCRIPTION ELONGATION FACTOR; TRANSCRIPTION FACTOR S-II;

CHEMICAL BINDING; ELECTRON MICROSCOPY; ENZYME; GENOME; RNA; YEAST;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CHROMATIN; CRYOELECTRON MICROSCOPY; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION ELONGATION; BINDING COMPETITION; CHEMISTRY; GENETICS; METABOLISM; PROTEIN CONFORMATION;

SACCHAROMYCES CEREVISIAE;

BINDING, COMPETITIVE; CELL CYCLE PROTEINS; CROSS-LINKING REAGENTS; CRYOELECTRON MICROSCOPY; MULTIPROTEIN COMPLEXES; NUCLEAR PROTEINS; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; RNA POLYMERASE II; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ELONGATION FACTORS;

EID: 85020418489     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms15741     Document Type: Article

References (80)

1. Tomson, B. N. & Arndt, K. M. The many roles of the conserved eukaryotic Paf1 complex in regulating transcription, histone modifications, and disease states. Biochim. Biophys. Acta 1829, 116-126 (2013).
2. Wade, P. A. et al. A novel collection of accessory factors associated with yeast RNA polymerase II. Protein Expr. Purif. 8, 85-90 (1996).
3. Shi, X. et al. Cdc73p and Paf1p are found in a novel RNA polymerase IIcontaining complex distinct from the Srbp-containing holoenzyme. Mol. Cell Biol. 17, 1160-1169 (1997).
4. Jaehning, J. A. The Paf1 complex: platform or player in RNA polymerase II transcription? Biochim. Biophys. Acta 1799, 379-388 (2010).
5. Squazzo, S. L. et al. The Paf1 complex physically and functionally associates with transcription elongation factors in vivo. EMBO J. 21, 1764-1774 (2002).
6. Pokholok, D. K., Hannett, N. M. & Young, R. A. Exchange of RNA polymerase II initiation and elongation factors during gene expression in vivo. Mol. Cell 9, 799-809 (2002).
7. Rondon, A. G., Gallardo, M., Garcia-Rubio, M. & Aguilera, A. Molecular evidence indicating that the yeast PAF complex is required for transcription elongation. EMBO Rep. 5, 47-53 (2004).
8. Krogan, N. J. et al. The Paf1 complex is required for histone H3 methylation by COMPASS and Dot1p: linking transcriptional elongation to histone methylation. Mol. Cell 11, 721-729 (2003).
9. Simic, R. et al. Chromatin remodeling protein Chd1 interacts with transcription elongation factors and localizes to transcribed genes. EMBO J. 22, 1846-1856 (2003).
10. Ng, H. H., Dole, S. & Struhl, K. The Rtf1 component of the Paf1 transcriptional elongation complex is required for ubiquitination of histone H2B. J Biol Chem 278, 33625-33628 (2003).
11. Wood, A., Schneider, J., Dover, J., Johnston, M. & Shilatifard, A. The Paf1 complex is essential for histone monoubiquitination by the Rad6-Bre1 complex, which signals for histone methylation by COMPASS and Dot1p. J. Biol. Chem. 278, 34739-34742 (2003).
12. Xiao, T. et al. Histone H2B ubiquitylation is associated with elongating RNA polymerase II. Mol. Cell Biol. 25, 637-651 (2005).
13. Warner, M. H., Roinick, K. L. & Arndt, K. M. Rtf1 is a multifunctional component of the Paf1 complex that regulates gene expression by directing cotranscriptional histone modification. Mol. Cell Biol. 27, 6103-6115 (2007).
14. Tenney, K. et al. Drosophila Rtf1 functions in histone methylation, gene expression, and Notch signaling. Proc. Natl Acad. Sci. USA 103, 11970-11974 (2006).
15. Wu, J. & Xu, W. Histone H3R17me2a mark recruits human RNA polymeraseassociated factor 1 complex to activate transcription. Proc. Natl Acad. Sci. USA 109, 5675-5680 (2012).
16. Sheldon, K. E., Mauger, D. M. & Arndt, K. M. A requirement for the Saccharomyces cerevisiae Paf1 complex in snoRNA 30 end formation. Mol. Cell 20, 225-236 (2005).
17. Penheiter, K. L., Washburn, T. M., Porter, S. E., Hoffman, M. G. & Jaehning, J. A. A posttranscriptional role for the yeast Paf1-RNA polymerase II complex is revealed by identification of primary targets. Mol. Cell 20, 213-223 (2005).
18. Rozenblatt-Rosen, O. et al. The tumor suppressor Cdc73 functionally associates with CPSF and CstF 30 mRNA processing factors. Proc. Natl Acad. Sci. USA 106, 755-760 (2009).
19. Chu, Y., Simic, R., Warner, M. H., Arndt, K. M. & Prelich, G. Regulation of histone modification and cryptic transcription by the Bur1 and Paf1 complexes. EMBO J. 26, 4646-4656 (2007).
20. Kubota, Y. et al. The PAF1 complex is involved in embryonic epidermal morphogenesis in Caenorhabditis elegans. Dev. Biol. 391, 43-53 (2014).
21. Chaudhary, K., Deb, S., Moniaux, N., Ponnusamy, M. P. & Batra, S. K. Human RNA polymerase II-Associated factor complex: dysregulation in cancer. Oncogene 26, 7499-7507 (2007).
22. Tan, J., Muntean, A. G. & Hess, J. L. PAFc, a key player in MLL-rearranged leukemogenesis. Oncotarget 1, 461-465 (2010).
23. Takahashi, A. et al. SHP2 tyrosine phosphatase converts parafibromin/Cdc73 from a tumor suppressor to an oncogenic driver. Mol. Cell 43, 45-56 (2011).
24. Kowalik, K. M. et al. The Paf1 complex represses small-RNA-mediated epigenetic gene silencing. Nature 520, 248-252 (2015).
25. Verrier, L. et al. Global regulation of heterochromatin spreading by Leo1. Open Biol. 5, 150045 (2015).
26. Chen, F. X. et al. PAF1, a molecular regulator of promoter-proximal pausing by rna polymerase II. Cell 162, 1003-1015 (2015).
27. Yu, M. et al. RNA polymerase II-Associated factor 1 regulates the release and phosphorylation of paused RNA polymerase II. Science 350, 1383-1386 (2015).
28. Poli, J. et al. Mec1, INO80, and the PAF1 complex cooperate to limit transcription replication conflicts through RNAPII removal during replication stress. Genes Dev. 30, 337-354 (2016).
29. Mayer, A. et al. Uniform transitions of the general RNA polymerase II transcription complex. Nat. Struct. Mol. Biol. 17, 1272-1278 (2010).
30. Laribee, R. N. et al. BUR kinase selectively regulates H3 K4 trimethylation and H2B ubiquitylation through recruitment of the PAF elongation complex. Curr. Biol. 15, 1487-1493 (2005).
31. Qiu, H., Hu, C., Wong, C. M. & Hinnebusch, A. G. The Spt4p subunit of yeast DSIF stimulates association of the Paf1 complex with elongating RNA polymerase II. Mol. Cell Biol. 26, 3135-3148 (2006).
32. Qiu, H., Hu, C., Gaur, N. A. & Hinnebusch, A. G. Pol II CTD kinases Bur1 and Kin28 promote Spt5 CTR-independent recruitment of Paf1 complex. EMBO J. 31, 3494-3505 (2012).
33. Mayekar, M. K., Gardner, R. G. & Arndt, K. M. The recruitment of the Saccharomyces cerevisiae Paf1 complex to active genes requires a domain of Rtf1 that directly interacts with the Spt4-Spt5 complex. Mol. Cell Biol. 33, 3259-3273 (2013).
34. Cao, Q. F. et al. Characterization of the human transcription elongation factor Rtf1: evidence for nonoverlapping functions of Rtf1 and the Paf1 Complex. Mol. Cell Biol. 35, 3459-3470 (2015).
35. Mbogning, J. et al. The PAF complex and Prf1/Rtf1 delineate distinct Cdk9-dependent pathways regulating transcription elongation in fission yeast. PLoS Genet. 9, e1004029 (2013).
36. Amrich, C. G. et al. Cdc73 subunit of Paf1 complex contains C-Terminal Raslike domain that promotes association of Paf1 complex with chromatin. J. Biol. Chem. 287, 10863-10875 (2012).
37. Dermody, J. L. & Buratowski, S. Leo1 subunit of the yeast paf1 complex binds RNA and contributes to complex recruitment. J. Biol. Chem. 285, 33671-33679 (2010).
38. Chu, X. et al. Structural insights into Paf1 complex assembly and histone binding. Nucleic Acids Res. 41, 10619-10629 (2013).
39. Chen, H. et al. Crystallographic analysis of the conserved C-Terminal domain of transcription factor Cdc73 from Saccharomyces cerevisiae reveals a GTPase-like fold. Acta Crystallogr. D 68, 953-959 (2012).
40. de Jong, R. N. et al. Structure and DNA binding of the human Rtf1 Plus3 domain. Structure 16, 149-159 (2008).
41. Wier, A. D., Mayekar, M. K., Heroux, A., Arndt, K. M. & VanDemark, A. P. Structural basis for Spt5-mediated recruitment of the Paf1 complex to chromatin. Proc. Natl Acad. Sci. USA 110, 17290-17295 (2013).
42. Letunic, I., Doerks, T. & Bork, P. SMART: recent updates, new developments and status in 2015. Nucleic Acids Res. 43, D257-D260 (2015).
43. Alva, V., Nam, S. Z., Soding, J. & Lupas, A. N. The MPI bioinformatics Toolkit as an integrative platform for advanced protein sequence and structure analysis. Nucleic Acids Res. 44, W410-W415 (2016).
44. Van Oss, S. B. et al. The histone modification domain of Paf1 complex subunit Rtf1 directly stimulates H2B ubiquitylation through an interaction with Rad6. Mol. Cell 64, 815-825 (2016).
45. Kim, J., Guermah, M. & Roeder, R. G. The human PAF1 complex acts in chromatin transcription elongation both independently and cooperatively with SII/TFIIS. Cell 140, 491-503 (2010).
46. Kettenberger, H., Armache, K. J. & Cramer, P. Architecture of the RNA polymerase II-TFIIS complex and implications for mRNA cleavage. Cell 114, 347-357 (2003).
47. Sydow, J. F. et al. Structural basis of transcription: mismatch-specific fidelity mechanisms and paused RNA polymerase II with frayed RNA. Mol. Cell 34, 710-721 (2009).
48. Bernecky, C., Herzog, F., Baumeister, W., Plitzko, J. M. & Cramer, P. Structure of transcribing mammalian RNA polymerase II. Nature 529, 551-554 (2016).
49. Cheung, A. C. & Cramer, P. Structural basis of RNA polymerase II backtracking, arrest and reactivation. Nature 471, 249-253 (2011).
50. Stark, H. GraFix: stabilization of fragile macromolecular complexes for single particle cryo-EM. Methods Enzymol. 481, 109-126 (2010).
51. Scheres, S. H. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519-530 (2012).
52. Barnes, C. O. et al. Crystal structure of a transcribing RNA polymerase II complex reveals a complete transcription bubble. Mol. Cell 59, 258-269 (2015).
53. Pettersen, E. F. et al. UCSF Chimera-A visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
54. Plaschka, C. et al. Transcription initiation complex structures elucidate DNA opening. Nature 533, 353-358 (2016).
55. Eser, P. et al. Determinants of RNA metabolism in the Schizosaccharomyces pombe genome. Mol. Syst. Biol. 12, 857 (2016).
56. Miller, C. et al. Dynamic transcriptome analysis measures rates of mRNA synthesis and decay in yeast. Mol. Syst. Biol. 7, 458 (2011).
57. Schulz, D. et al. Transcriptome surveillance by selective termination of noncoding RNA synthesis. Cell 155, 1075-1087 (2013).
58. Schwalb, B. et al. TT-seq maps the human transient transcriptome. Science 352, 1225-1228 (2016).
59. Guo, J. & Price, D. H. RNA polymerase II transcription elongation control. Chem. Rev. 113, 8583-8603 (2013).
60. Kwak, H. & Lis, J. T. Control of transcriptional elongation. Annu. Rev. Genet. 47, 483-508 (2013).
61. Grohmann, D. et al. The initiation factor TFE and the elongation factor Spt4/5 compete for the RNAP clamp during transcription initiation and elongation. Mol. Cell 43, 263-274 (2011).
62. Martinez-Rucobo, F. W., Sainsbury, S., Cheung, A. C. & Cramer, P. Architecture of the RNA polymerase-Spt4/5 complex and basis of universal transcription processivity. EMBO J. 30, 1302-1310 (2011).
63. Zawel, L., Kumar, K. P. & Reinberg, D. Recycling of the general transcription factors during RNA polymerase II transcription. Genes Dev. 9, 1479-1490 (1995).
64. Yang, B. et al. Identification of cross-linked peptides from complex samples. Nat. Methods 9, 904-906 (2012).
65. Combe, C. W., Fischer, L. & Rappsilber, J. xiNET: cross-link network maps with residue resolution. Mol. Cell Proteomics 14, 1137-1147 (2015).
66. Korinek, A., Beck, F., Baumeister, W., Nickell, S. & Plitzko, J. M. Computer controlled cryo-electron microscopy-TOM(2) a software package for highthroughput applications. J. Struct. Biol. 175, 394-405 (2011).
67. Li, X., Zheng, S. Q., Egami, K., Agard, D. A. & Cheng, Y. Influence of electron dose rate on electron counting images recorded with the K2 camera. J. Struct. Biol. 184, 251-260 (2013).
68. Mindell, J. A. & Grigorieff, N. Accurate determination of local defocus and specimen tilt in electron microscopy. J. Struct. Biol. 142, 334-347 (2003).
69. Rohou, A. & Grigorieff, N. CTFFIND4: fast and accurate defocus estimation from electron micrographs. J. Struct. Biol. 192, 216-221 (2015).
70. Tang, G. et al. EMAN2: An extensible image processing suite for electron microscopy. J. Struct. Biol. 157, 38-46 (2007).
71. Scheres, S. H. Semi-Automated selection of cryo-EM particles in RELION-1.3. J. Struct. Biol. 189, 114-122 (2015).
72. Scheres, S. H. Beam-induced motion correction for sub-megadalton cryo-EM particles. Elife 3, e03665 (2014).
73. Cardone, G., Heymann, J. B. & Steven, A. C. One number does not fit all: mapping local variations in resolution in cryo-EM reconstructions. J. Struct. Biol. 184, 226-236 (2013).
74. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486-501 (2010).
75. Sun, M. et al. Comparative dynamic transcriptome analysis (cDTA) reveals mutual feedback between mRNA synthesis and degradation. Genome Res. 22, 1350-1359 (2012).
76. Dolken, L. et al. High-resolution gene expression profiling for simultaneous kinetic parameter analysis of RNA synthesis and decay. RNA 14, 1959-1972 (2008).
77. Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15-21 (2013).
78. Anders, S., Pyl, P. T. & Huber, W. HTSeq-A Python framework to work with high-Throughput sequencing data. Bioinformatics 31, 166-169 (2015).
79. Love, M. I., Anders, S., Kim, V. & Huber, W. RNA-Seq workflow: gene-level exploratory analysis and differential expression. F1000Res 4, 1070 (2015).
80. Cramer, P. et al. Architecture of RNA polymerase II and implications for the transcription mechanism. Science 288, 640-649 (2000).