Rtr1 is a dual specificity phosphatase that dephosphorylates Tyr1 and Ser5 on the RNA polymerase II CTD

Journal of Molecular Biology

Volumn 426, Issue 16, 2014, Pages 2970-2981

  Hsu, Peter L ^a   Yang, Fan ^a   Smith Kinnaman, Whitney ^b   Yang, Wen ^a   Song, Jae Eun ^a   Mosley, Amber L ^b   Varani, Gabriele ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

phosphatase; phosphorylation; RNA PolII CTD; RNA polymerase II; transcription

Indexed keywords

DUAL SPECIFICITY PHOSPHATASE; FUNGAL ENZYME; GLYCEROL 2 PHOSPHATE; RNA POLYMERASE II; RTR1 ENZYME; SERINE; TYROSINE; UNCLASSIFIED DRUG;

ARTICLE; C TERMINAL DOMAIN; CRYSTAL STRUCTURE; DEPHOSPHORYLATION; ENZYME ACTIVITY; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; KLUYVEROMYCES LACTIS; MASS SPECTROMETRY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; SACCHAROMYCES CEREVISIAE; YEAST CELL;

PHOSPHATASE; PHOSPHORYLATION; RNA POLII CTD; RNA POLYMERASE II; TRANSCRIPTION;

AMINO ACID SEQUENCE; CARRIER PROTEINS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; RNA POLYMERASE II; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SERINE; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TYROSINE;

EID: 84904758006     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2014.06.010     Document Type: Article

References (43)

1. J.-P. Hsin, and J.L. Manley The RNA polymerase II CTD coordinates transcription and RNA processing Genes Dev 26 2012 2119 2137
2. K. Kubicek, H. Cerna, P. Holub, J. Pasulka, D. Hrossova, and F. Loehr et al. Serine phosphorylation and proline isomerization in RNAP II CTD control recruitment of Nrd1 Genes Dev 26 2012 1891 1896
3. A. Meinhart, T. Kamenski, S. Hoeppner, S. Baumli, and P. Cramer A structural perspective of CTD function Genes Dev 19 2005 1401 1415
4. D.P. Morris, H.P. Phatnani, and A.L. Greenleaf Phospho-carboxyl-terminal domain binding and the role of a prolyl isomerase in pre-mRNA 3′-end formation J Biol Chem 274 1999 31583 31587
5. K. Xiang, T. Nagaike, S. Xiang, T. Kilic, M.M. Beh, and J.L. Manley et al. Crystal structure of the human symplekin-Ssu72-CTD phosphopeptide complex Nature 467 2010 729 733
6. M. Zhang, X.J. Wang, X. Chen, M.E. Bowman, Y. Luo, and J.P. Noel et al. Structural and kinetic analysis of prolyl-isomerization/phosphorylation cross-talk in the CTD code ACS Chem Biol 7 2012 1462 1470
7. R.D. Chapman, M. Heidemann, T.K. Albert, R. Mailhammer, A. Flatley, and M. Meisterernst et al. Transcribing RNA polymerase II is phosphorylated at CTD residue serine-7 Science 318 2007 1780 1782
8. J.-P. Hsin, A. Sheth, and J.L. Manley RNAP II CTD phosphorylated on threonine-4 is required for histone mRNA 3′ end processing Science 334 2011 683 686
9. A. Mayer, M. Heidemann, M. Lidschreiber, A. Schreieck, M. Sun, and C. Hintermair et al. CTD tyrosine phosphorylation impairs termination factor recruitment to RNA polymerase II Science 336 2012 1723 1725
10. S. Buratowski The CTD code Nat Struct Biol 10 2003 679 680
11. S. Buratowski Progression through the RNA polymerase II CTD cycle Mol Cell 36 2009 541 546
12. B. Schwer, and S. Shuman Deciphering the RNA polymerase II CTD code in fission yeast Mol Cell 2011 10.1016/j.molcel.2011.05.024
13. P. Komarnitsky, E.J. Cho, and S. Buratowski Different phosphorylated forms of RNA polymerase II and associated mRNA processing factors during transcription Genes Dev 14 2000 2452 2460
14. A. Ghosh, S. Shuman, and C.D. Lima Structural insights to how mammalian capping enzyme reads the CTD code Mol Cell 43 2011 299 310
15. A. Mayer, M. Lidschreiber, M. Siebert, K. Leike, J. Söding, and P. Cramer Uniform transitions of the general RNA polymerase II transcription complex Nat Struct Mol Biol 17 2010 1272 1278
16. L. Vasiljeva, M. Kim, H. Mutschler, S. Buratowski, and A. Meinhart The Nrd1-Nab3-Sen1 termination complex interacts with the Ser5-phosphorylated RNA polymerase II C-terminal domain Nat Struct Mol Biol 15 2008 795 804
17. S.H. Ahn, M. Kim, and S. Buratowski Phosphorylation of serine 2 within the RNA polymerase II C-terminal domain couples transcription and 3′ end processing Mol Cell 13 2004 67 76
18. B. Gu, D. Eick, and O. Bensaude CTD serine-2 plays a critical role in splicing and termination factor recruitment to RNA polymerase II in vivo Nucleic Acids Res 41 2013 1591 1603
19. B.M. Lunde, S.L. Reichow, M. Kim, H. Suh, T.C. Leeper, and F. Yang et al. Cooperative interaction of transcription termination factors with the RNA polymerase II C-terminal domain Nat Struct Mol Biol 17 2010 1195 1201
20. A.L. Mosley, S.G. Pattenden, M. Carey, S. Venkatesh, J.M. Gilmore, and L. Florens et al. Rtr1 is a CTD phosphatase that regulates RNA polymerase II during the transition from serine 5 to serine 2 phosphorylation Mol Cell 34 2009 168 178
21. S. Egloff, J. Zaborowska, C. Laitem, T. Kiss, and S. Murphy Ser7 phosphorylation of the CTD recruits the RPAP2 Ser5 phosphatase to snRNA genes Mol Cell 45 2012 111 122
22. K. Xiang, J.L. Manley, and L. Tong The yeast regulator of transcription protein Rtr1 lacks an active site and phosphatase activity Nat Commun 3 2012 946
23. M. Wilson, C. Hogstrand, and W. Maret Picomolar concentrations of free zinc(II) ions regulate receptor protein-tyrosine phosphatase β activity J Biol Chem 287 2012 9322 9326
24. P.A. Gibney, T. Fries, S.M. Bailer, and K.A. Morano Rtr1 is the Saccharomyces cerevisiae homolog of a novel family of RNA polymerase II-binding proteins Eukaryot Cell 7 2008 938 948
25. R. Baskaran, G.G. Chiang, T. Mysliwiec, G.D. Kruh, and J.Y. Wang Tyrosine phosphorylation of RNA polymerase II carboxyl-terminal domain by the Abl-related gene product J Biol Chem 272 1997 18905 18909
26. J.W. Werner-Allen, C.-J. Lee, P. Liu, N.I. Nicely, S. Wang, and A.L. Greenleaf et al. cis-Proline-mediated Ser(P)5 dephosphorylation by the RNA polymerase II C-terminal domain phosphatase Ssu72 J Biol Chem 286 2011 5717 5726
27. S. Egloff, J. Zaborowska, C. Laitem, T. Kiss, and S. Murphy Ser7 phosphorylation of the CTD recruits the RPAP2 Ser5 phosphatase to snRNA genes Mol Cell 2012 10.1016/j.molcel.2011.11.006
28. Y. Zhang, Y. Kim, N. Genoud, J. Gao, J.W. Kelly, and S.L. Pfaff et al. Determinants for dephosphorylation of the RNA polymerase II C-terminal domain by Scp1 Mol Cell 24 2006 759 770
29. Y. Zhang, M. Zhang, and Y. Zhang Crystal structure of Ssu72, an essential eukaryotic phosphatase specific for the C-terminal domain of RNA polymerase II, in complex with a transition state analogue Biochem J 434 2011 435 444
30. S. Hausmann, and S. Shuman Characterization of the CTD phosphatase Fcp1 from fission yeast. Preferential dephosphorylation of serine 2 versus serine 5 J Biol Chem 277 2002 21213 21220
31. A.L. Mosley, G.O. Hunter, M.E. Sardiu, M. Smolle, J.L. Workman, and L. Florens et al. Quantitative proteomics demonstrates that the RNA polymerase II subunits Rpb4 and Rpb7 dissociate during transcriptional elongation Mol Cell Proteomics 12 2013 1530 1538
32. S. Egloff, S.A. Szczepaniak, M. Dienstbier, A. Taylor, S. Knight, and S. Murphy The integrator complex recognizes a new double mark on the RNA polymerase II carboxyl-terminal domain J Biol Chem 285 2010 20564 20569
33. D. Forget, A.-A. Lacombe, P. Cloutier, M. Lavallée-Adam, M. Blanchette, and B. Coulombe Nuclear import of RNA polymerase II is coupled with nucleocytoplasmic shuttling of the RNA polymerase II-associated protein 2 Nucleic Acids Res 2013 10.1093/nar/gkt455
34. M.K. Rosen, K.H. Gardner, R.C. Willis, W.E. Parris, T. Pawson, and L.E. Kay Selective methyl group protonation of perdeuterated proteins J Mol Biol 263 1996 627 636
35. F. Delaglio, S. Grzesiek, G.W. Vuister, G. Zhu, J. Pfeifer, and A. Bax NMRPipe: a multidimensional spectral processing system based on UNIX pipes J Biomol NMR 6 1995 277 293
36. W.F. Vranken, W. Boucher, T.J. Stevens, R.H. Fogh, A. Pajon, and M. Llinas et al. The CCPN data model for NMR spectroscopy: development of a software pipeline Proteins 59 2005 687 696
37. Z. Otwinowski, and W. Minor [20] Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol 276 1997 307 326
38. T.C. Terwilliger, and J. Berendzen Automated MAD and MIR structure solution Acta Crystallogr Sect D Biol Crystallogr 55 1999 849 861
39. A.T. Brünger, P.D. Adams, G.M. Clore, W.L. DeLano, P. Gros, and R.W. Grosse-Kunstleve et al. Crystallography & NMR system: a new software suite for macromolecular structure determination Acta Crystallogr Sect D Biol Crystallogr 54 1998 905 921
40. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr Sect D Biol Crystallogr 60 2004 2126 2132
41. M.D. Winn, C.C. Ballard, K.D. Cowtan, E.J. Dodson, P. Emsley, and P.R. Evans et al. Overview of the CCP4 suite and current developments Acta Crystallogr Sect D Biol Crystallogr 67 2011 235 242
42. T.S. Walter, C. Meier, R. Assenberg, K.-F. Au, J. Ren, and A. Verma et al. Lysine methylation as a routine rescue strategy for protein crystallization Structure 14 2006 1617 1622
43. O. Puig, F. Caspary, G. Rigaut, B. Rutz, E. Bouveret, and E. Bragado-Nilsson et al. The tandem affinity purification (TAP) method: a general procedure of protein complex purification Methods 24 2001 218 229