The interactome of the atypical phosphatase Rtr1 in Saccharomyces cerevisiae

Molecular BioSystems

Volumn 10, Issue 7, 2014, Pages 1730-1741

  Smith Kinnaman, Whitney R ^a   Berna, Michael J ^a   Hunter, Gerald O ^a   True, Jason D ^a   Hsu, Peter ^b   Cabello, Gabriela I ^a   Fox, Melanie J ^a   Varani, Gabriele ^a,b   Mosley, Amber L ^a,c  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CTDK-I PROTEIN COMPLEX, S CEREVISIAE; PROTEIN KINASE; RNA POLYMERASE II; RTR1 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; SERINE; TRANSCRIPTION FACTOR;

ENZYME ACTIVE SITE; GENETICS; METABOLISM; PHOSPHORYLATION; PROTEOMICS; SACCHAROMYCES CEREVISIAE;

CATALYTIC DOMAIN; PHOSPHORYLATION; PROTEIN KINASES; PROTEOMICS; RNA POLYMERASE II; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SERINE; TRANSCRIPTION FACTORS;

EID: 84901851275     PISSN: 1742206X     EISSN: 17422051     Source Type: Journal    
DOI: 10.1039/c4mb00109e     Document Type: Article

References (79)

1. D. Eick M. Geyer The RNA Polymerase II Carboxy-Terminal Domain (CTD) Code Chem. Rev. 2013 113 11 8456 8490
2. M. Heidemann C. Hintermair K. Voss D. Eick Dynamic phosphorylation patterns of RNA polymerase II CTD during transcription Biochim. Biophys. Acta 2013 1829 1 55 62
3. S. Buratowski Progression through the RNA polymerase II CTD cycle Mol. Cell 2009 36 4 541 546
4. J. M. Ahearn, Jr. M. S. Bartolomei M. L. West L. J. Cisek J. L. Corden Cloning and sequence analysis of the mouse genomic locus encoding the largest subunit of RNA polymerase II J. Biol. Chem. 1987 262 22 10695 10705
5. A. L. Mosley G. O. Hunter M. E. Sardiu M. Smolle J. L. Workman L. Florens M. P. Washburn Quantitative proteomics demonstrates that the RNA polymerase II subunits Rpb4 and Rpb7 dissociate during transcriptional elongation Mol. Cell. Proteomics 2013 12 6 1530 1538
6. S. Trigon H. Serizawa J. W. Conaway R. C. Conaway S. P. Jackson M. Morange Characterization of the residues phosphorylated in vitro by different C-terminal domain kinases J. Biol. Chem. 1998 273 12 6769 6775
7. R. D. Chapman M. Heidemann T. K. Albert R. Mailhammer A. Flatley M. Meisterernst E. Kremmer D. Eick Transcribing RNA polymerase II is phosphorylated at CTD residue serine-7 Science 2007 318 5857 1780 1782
8. S. Egloff D. O'Reilly R. D. Chapman A. Taylor K. Tanzhaus L. Pitts D. Eick S. Murphy Serine-7 of the RNA polymerase II CTD is specifically required for snRNA gene expression Science 2007 318 5857 1777 1779
9. M. S. Akhtar M. Heidemann J. R. Tietjen D. W. Zhang R. D. Chapman D. Eick A. Z. Ansari TFIIH kinase places bivalent marks on the carboxy-terminal domain of RNA polymerase II Mol. Cell 2009 34 3 387 393
10. M. Heidemann D. Eick Tyrosine-1 and threonine-4 phosphorylation marks complete the RNA polymerase II CTD phospho-code RNA Biol. 2012 9 9 55 62
11. A. Mayer M. Heidemann M. Lidschreiber A. Schreieck M. Sun C. Hintermair E. Kremmer D. Eick P. Cramer CTD tyrosine phosphorylation impairs termination factor recruitment to RNA polymerase II Science 2012 336 6089 1723 1725
12. E. J. Cho T. Takagi C. R. Moore S. Buratowski mRNA capping enzyme is recruited to the transcription complex by phosphorylation of the RNA polymerase II carboxy-terminal domain Genes Dev. 1997 11 24 3319 3326
13. P. Komarnitsky E. J. Cho S. Buratowski Different phosphorylated forms of RNA polymerase II and associated mRNA processing factors during transcription Genes Dev. 2000 14 19 2452 2460
14. C. R. Rodriguez E. J. Cho M. C. Keogh C. L. Moore A. L. Greenleaf S. Buratowski Kin28, the TFIIH-associated carboxy-terminal domain kinase, facilitates the recruitment of mRNA processing machinery to RNA polymerase II Mol. Cell. Biol. 2000 20 1 104 112
15. M. C. Keogh E. J. Cho V. Podolny S. Buratowski Kin28 is found within TFIIH and a Kin28-Ccl1-Tfb3 trimer complex with differential sensitivities to T-loop phosphorylation Mol. Cell. Biol. 2002 22 5 1288 1297
16. S. H. Ahn M. Kim S. Buratowski Phosphorylation of serine 2 within the RNA polymerase II C-terminal domain couples transcription and 3' end processing Mol. Cell 2004 13 1 67 76
17. M. Kim S. H. Ahn N. J. Krogan J. F. Greenblatt S. Buratowski Transitions in RNA polymerase II elongation complexes at the 3' ends of genes EMBO J. 2004 23 2 354 364
18. J. R. Tietjen D. W. Zhang J. B. Rodriguez-Molina B. E. White M. S. Akhtar M. Heidemann X. Li R. D. Chapman K. Shokat S. Keles D. Eick A. Z. Ansari Chemical-genomic dissection of the CTD code Nat. Struct. Mol. Biol. 2010 17 9 1154 1161
19. D. W. Zhang A. L. Mosley S. R. Ramisetty J. B. Rodriguez-Molina M. P. Washburn A. Z. Ansari Ssu72 phosphatase-dependent erasure of phospho-Ser7 marks on the RNA polymerase II C-terminal domain is essential for viability and transcription termination J. Biol. Chem. 2012 287 11 8541 8551
20. A. R. Bataille C. Jeronimo P. E. Jacques L. Laramee M. E. Fortin A. Forest M. Bergeron S. D. Hanes F. Robert A universal RNA polymerase II CTD cycle is orchestrated by complex interplays between kinase, phosphatase and isomerase enzymes along genes Mol. Cell 2012 45 2 158 170
21. C. Hintermair M. Heidemann F. Koch N. Descostes M. Gut I. Gut R. Fenouil P. Ferrier A. Flatley E. Kremmer R. D. Chapman J. C. Andrau D. Eick Threonine-4 of mammalian RNA polymerase II CTD is targeted by Polo-like kinase 3 and required for transcriptional elongation EMBO J. 2012 31 12 2784 2797
22. J. P. Hsin A. Sheth J. L. Manley RNAP II CTD phosphorylated on threonine-4 is required for histone mRNA 3′ end processing Science 2011 334 6056 683 686
23. R. Baskaran G. G. Chiang T. Mysliwiec G. D. Kruh J. Y. Wang Tyrosine phosphorylation of RNA polymerase II carboxyl-terminal domain by the Abl-related gene product J. Biol. Chem. 1997 272 30 18905 18909
24. A. L. Mosley S. G. Pattenden M. Carey S. Venkatesh J. M. Gilmore L. Florens J. L. Workman M. P. Washburn Rtr1 is a CTD phosphatase that regulates RNA polymerase II during the transition from serine 5 to serine 2 phosphorylation Mol. Cell 2009 34 2 168 178
25. J. Archambault R. S. Chambers M. S. Kobor Y. Ho M. Cartier D. Bolotin B. Andrews C. M. Kane J. Greenblatt An essential component of a C-terminal domain phosphatase that interacts with transcription factor IIF in Saccharomyces cerevisiae Proc. Natl. Acad. Sci. U. S. A. 1997 94 26 14300 14305
26. M. S. Kobor J. Archambault W. Lester F. C. Holstege O. Gileadi D. B. Jansma E. G. Jennings F. Kouyoumdjian A. R. Davidson R. A. Young J. Greenblatt An unusual eukaryotic protein phosphatase required for transcription by RNA polymerase II and CTD dephosphorylation in S. cerevisiae Mol. Cell 1999 4 1 55 62
27. E. J. Cho M. S. Kobor M. Kim J. Greenblatt S. Buratowski Opposing effects of Ctk1 kinase and Fcp1 phosphatase at Ser 2 of the RNA polymerase II C-terminal domain Genes Dev. 2001 15 24 3319 3329
28. A. Ghosh S. Shuman C. D. Lima The structure of Fcp1, an essential RNA polymerase II CTD phosphatase Mol. Cell 2008 32 4 478 490
29. S. Krishnamurthy X. He M. Reyes-Reyes C. Moore M. Hampsey Ssu72 Is an RNA polymerase II CTD phosphatase Mol. Cell 2004 14 3 387 394
30. M. Reyes-Reyes M. Hampsey Role for the Ssu72 C-terminal domain phosphatase in RNA polymerase II transcription elongation Mol. Cell. Biol. 2007 27 3 926 936
31. K. Xiang T. Nagaike S. Xiang T. Kilic M. M. Beh J. L. Manley L. Tong Crystal structure of the human symplekin-Ssu72-CTD phosphopeptide complex Nature 2010 467 7316 729 733
32. D. W. Zhang A. L. Mosley S. R. Ramisetty J. B. Rodriguez-Molina M. P. Washburn A. Z. Ansari Ssu72 phosphatase dependent erasure of phospho-Ser7 marks on the RNA Polymerase II C-terminal domain is essential for viability and transcription termination J. Biol. Chem. 2012 287 11 8541 8551
33. A. Schreieck A. D. Easter S. Etzold K. Wiederhold M. Lidschreiber P. Cramer L. A. Passmore RNA polymerase II termination involves C-terminal-domain tyrosine dephosphorylation by CPF subunit Glc7 Nat. Struct. Mol. Biol. 2014 21 2 175 179
34. N. J. Krogan M. Kim A. Tong A. Golshani G. Cagney V. Canadien D. P. Richards B. K. Beattie A. Emili C. Boone A. Shilatifard S. Buratowski J. Greenblatt Methylation of histone H3 by Set2 in Saccharomyces cerevisiae is linked to transcriptional elongation by RNA polymerase II Mol. Cell. Biol. 2003 23 12 4207 4218
35. K. Kubicek H. Cerna P. Holub J. Pasulka D. Hrossova F. Loehr C. Hofr S. Vanacova R. Stefl Serine phosphorylation and proline isomerization in RNAP II CTD control recruitment of Nrd1 Genes Dev. 2012 26 17 1891 1896
36. Y. Zhang M. 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. 2011 434 3 435 444
37. J. W. Werner-Allen C. J. Lee P. Liu N. I. Nicely S. Wang A. L. Greenleaf P. Zhou cis-Proline-mediated Ser(P)5 dephosphorylation by the RNA polymerase II C-terminal domain phosphatase Ssu72 J. Biol. Chem. 2011 286 7 5717 5726
38. D. Forget A. A. Lacombe P. Cloutier M. Lavallee-Adam M. Blanchette 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 41 14 6881 6891
39. K. Xiang J. L. Manley L. Tong The yeast regulator of transcription protein Rtr1 lacks an active site and phosphatase activity Nat. Commun. 2012 3 946
40. S. Egloff J. Zaborowska C. Laitem T. Kiss S. Murphy Ser7 phosphorylation of the CTD recruits the RPAP2 Ser5 phosphatase to snRNA genes Mol. Cell 2012 45 1 111 122
41. Z. Ni J. B. Olsen X. Guo G. Zhong E. D. Ruan E. Marcon P. Young H. Guo J. Li J. Moffat A. Emili J. F. Greenblatt Control of the RNA polymerase II phosphorylation state in promoter regions by CTD interaction domain-containing proteins RPRD1A and RPRD1B Transcription 2011 2 5 237 242
42. S. Ghaemmaghami W. K. Huh K. Bower R. W. Howson A. Belle N. Dephoure E. K. O'Shea J. S. Weissman Global analysis of protein expression in yeast Nature 2003 425 6959 737 741
43. A. L. Mosley M. E. Sardiu S. G. Pattenden J. L. Workman L. Florens M. P. Washburn Highly reproducible label free quantitative proteomic analysis of RNA polymerase complexes Mol. Cell. Proteomics 2010 10 2 M110000687
44. M. Khanna T. Imasaki V. M. Chikwana S. Perez-Miller G. O. Hunter A. Mosley Y. Takagi T. D. Hurley Expression and purification of functional human glycogen synthase-1 (hGYS1) in insect cells Protein Expression Purif. 2013 90 2 78 83
45. G. Teo G. Liu J. Zhang A. I. Nesvizhskii A. C. Gingras H. Choi SAINTexpress: Improvements and Additional Features in Significance Analysis of Interactome Software J. Proteomics 2013 10.1016/j.jprot.2013.10.023
46. H. Choi G. Liu D. Mellacheruvu M. Tyers A. C. Gingras A. I. Nesvizhskii Analyzing protein-protein interactions from affinity purification-mass spectrometry data with SAINT Curr. Protoc. Bioinf. 2012
47. H. Choi T. Glatter M. Gstaiger A. I. Nesvizhskii SAINT-MS1: protein-protein interaction scoring using label-free intensity data in affinity purification-mass spectrometry experiments J. Proteome Res. 2012 11 4 2619 2624
48. D. V. Skarra M. Goudreault H. Choi M. Mullin A. I. Nesvizhskii A. C. Gingras R. E. Honkanen Label-free quantitative proteomics and SAINT analysis enable interactome mapping for the human Ser/Thr protein phosphatase 5 Proteomics 2011 11 8 1508 1516
49. H. Choi B. Larsen Z. Y. Lin A. Breitkreutz D. Mellacheruvu D. Fermin Z. S. Qin M. Tyers A. C. Gingras A. I. Nesvizhskii SAINT: probabilistic scoring of affinity purification-mass spectrometry data Nat. Methods 2011 8 1 70 73
50. D. Mellacheruvu Z. Wright A. L. Couzens J. P. Lambert N. A. St-Denis T. Li Y. V. Miteva S. Hauri M. E. Sardiu T. Y. Low V. A. Halim R. D. Bagshaw N. C. Hubner A. Al-Hakim A. Bouchard D. Faubert D. Fermin W. H. Dunham M. Goudreault Z. Y. Lin B. G. Badillo T. Pawson D. Durocher B. Coulombe R. Aebersold G. Superti-Furga J. Colinge A. J. Heck H. Choi M. Gstaiger S. Mohammed I. M. Cristea K. L. Bennett M. P. Washburn B. Raught R. M. Ewing A. C. Gingras A. I. Nesvizhskii The CRAPome: a contaminant repository for affinity purification-mass spectrometry data Nat. Methods 2013 10 8 730 736
51. A. Breitkreutz H. Choi J. R. Sharom L. Boucher V. Neduva B. Larsen Z. Y. Lin B. J. Breitkreutz C. Stark G. Liu J. Ahn D. Dewar-Darch T. Reguly X. Tang R. Almeida Z. S. Qin T. Pawson A. C. Gingras A. I. Nesvizhskii M. Tyers A global protein kinase and phosphatase interaction network in yeast Science 2010 328 5981 1043 1046
52. Y. Kwon A. Vinayagam X. Sun N. Dephoure S. P. Gygi P. Hong N. Perrimon The Hippo signaling pathway interactome Science 2013 342 6159 737 740
53. T. Beissbarth T. P. Speed GOstat: find statistically overrepresented gene ontologies within a group of genes Bioinformatics 2004 20 9 1464 1465
54. Y. Li S. Bjorklund Y. W. Jiang Y. J. Kim W. S. Lane D. J. Stillman R. D. Kornberg Yeast global transcriptional regulators Sin4 and Rgr1 are components of mediator complex/RNA polymerase II holoenzyme Proc. Natl. Acad. Sci. U. S. A. 1995 92 24 10864 10868
55. L. Staresincic J. Walker A. B. Dirac-Svejstrup R. Mitter J. Q. Svejstrup GTP-dependent binding and nuclear transport of RNA polymerase II by Npa3 protein J. Biol. Chem. 2011 286 41 35553 35561
56. P. Cloutier R. Al-Khoury M. Lavallee-Adam D. Faubert H. Jiang C. Poitras A. Bouchard D. Forget M. Blanchette B. Coulombe High-resolution mapping of the protein interaction network for the human transcription machinery and affinity purification of RNA polymerase II-associated complexes Methods 2009 48 4 381 386
57. D. Forget A. A. Lacombe P. Cloutier R. Al-Khoury A. Bouchard M. Lavallee-Adam D. Faubert C. Jeronimo M. Blanchette B. Coulombe The protein interaction network of the human transcription machinery reveals a role for the GTPase RPAP4/GPN1 and microtubule assembly in nuclear import and biogenesis of RNA polymerase II Mol. Cell. Proteomics 2010 9 12 2827 2839
58. C. L. Mueller J. A. Jaehning Ctr9, Rtf1 and Leo1 are components of the Paf1/RNA polymerase II complex Mol. Cell. Biol. 2002 22 7 1971 1980
59. K. Duvel A. Santhanam S. Garrett L. Schneper J. R. Broach Multiple roles of Tap42 in mediating rapamycin-induced transcriptional changes in yeast Mol. Cell 2003 11 6 1467 1478
60. C. J. Di Como K. T. Arndt Nutrients, via the Tor proteins, stimulate the association of Tap42 with type 2A phosphatases Genes Dev. 1996 10 15 1904 1916
61. B. Alonso C. Beraud S. Meguellati S. W. Chen J. L. Pellequer J. Armengaud C. Godon Eukaryotic GPN-loop GTPases paralogs use a dimeric assembly reminiscent of archeal GPN Cell Cycle 2013 12 3 463 472
62. T. Glatter A. Wepf R. Aebersold M. Gstaiger An integrated workflow for charting the human interaction proteome: insights into the PP2A system Mol. Syst. Biol. 2009 5 237
63. J. Mok H. Im M. Snyder Global identification of protein kinase substrates by protein microarray analysis Nat. Protoc. 2009 4 12 1820 1827
64. J. Fasolo A. Sboner M. G. Sun H. Yu R. Chen D. Sharon P. M. Kim M. Gerstein M. Snyder Diverse protein kinase interactions identified by protein microarrays reveal novel connections between cellular processes Genes Dev. 2011 25 7 767 778
65. C. Michaelis R. Ciosk K. Nasmyth Cohesins: chromosomal proteins that prevent premature separation of sister chromatids Cell 1997 91 1 35 45
66. L. Benard K. Carroll R. C. Valle R. B. Wickner Ski6p is a homolog of RNA-processing enzymes that affects translation of non-poly(A) mRNAs and 60S ribosomal subunit biogenesis Mol. Cell. Biol. 1998 18 5 2688 2696
67. R. J. Dohmen R. Stappen J. P. McGrath H. Forrova J. Kolarov A. Goffeau A. Varshavsky An essential yeast gene encoding a homolog of ubiquitin-activating enzyme J. Biol. Chem. 1995 270 30 18099 18109
68. F. W. Martinez-Rucobo S. Sainsbury A. C. Cheung P. Cramer Architecture of the RNA polymerase-Spt4/5 complex and basis of universal transcription processivity EMBO J. 2011 30 7 1302 1310
69. Z. A. Chen A. Jawhari L. Fischer C. Buchen S. Tahir T. Kamenski M. Rasmussen L. Lariviere J. C. Bukowski-Wills M. Nilges P. Cramer J. Rappsilber Architecture of the RNA polymerase II-TFIIF complex revealed by cross-linking and mass spectrometry EMBO J. 2010 29 4 717 726
70. A. Hirtreiter G. E. Damsma A. C. Cheung D. Klose D. Grohmann E. Vojnic A. C. Martin P. Cramer F. Werner Spt4/5 stimulates transcription elongation through the RNA polymerase clamp coiled-coil motif Nucleic Acids Res. 2010 38 2 585 596
71. A. Mayer M. Lidschreiber M. Siebert K. Leike J. Soding P. Cramer Uniform transitions of the general RNA polymerase II transcription complex Nat. Struct. Mol. Biol. 2010 17 10 1272 1278
72. A. Mayer M. Lidschreiber M. Siebert K. Leike J. Soding P. Cramer Uniform transitions of the general RNA polymerase II transcription complex Nat. Struct. Mol. Biol. 2010 17 10 1272 1278
73. E. A. Winzeler D. D. Shoemaker A. Astromoff H. Liang K. Anderson B. Andre R. Bangham R. Benito J. D. Boeke H. Bussey A. M. Chu C. Connelly K. Davis F. Dietrich S. W. Dow M. El Bakkoury F. Foury S. H. Friend E. Gentalen G. Giaever J. H. Hegemann T. Jones M. Laub H. Liao N. Liebundguth D. J. Lockhart A. Lucau-Danila M. Lussier N. M'Rabet P. Menard M. Mittmann C. Pai C. Rebischung J. L. Revuelta L. Riles C. J. Roberts P. Ross-MacDonald B. Scherens M. Snyder S. Sookhai-Mahadeo R. K. Storms S. Veronneau M. Voet G. Volckaert T. R. Ward R. Wysocki G. S. Yen K. Yu K. Zimmermann P. Philippsen M. Johnston R. W. Davis Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis Science 1999 285 5429 901 906
74. O. Puig F. Caspary G. Rigaut B. Rutz E. Bouveret E. Bragado-Nilsson M. Wilm B. Seraphin The tandem affinity purification (TAP) method: a general procedure of protein complex purification Methods 2001 24 3 218 229
75. A. L. Mosley M. E. Sardiu S. G. Pattenden J. L. Workman L. Florens M. P. Washburn Highly reproducible label free quantitative proteomic analysis of RNA polymerase complexes Mol. Cell. Proteomics 2011 10 2 M110 000687
76. G. Rigaut A. Shevchenko B. Rutz M. Wilm M. Mann B. Seraphin A generic protein purification method for protein complex characterization and proteome exploration Nat. Biotechnol. 1999 17 10 1030 1032
77. L. Florens M. P. Washburn Proteomic analysis by multidimensional protein identification technology Methods Mol. Biol. 2006 328 159 175
78. L. Kall J. D. Canterbury J. Weston W. S. Noble M. J. MacCoss Semi-supervised learning for peptide identification from shotgun proteomics datasets Nat. Methods 2007 4 11 923 925
79. M. Patturajan N. K. Conrad D. B. Bregman J. L. Corden Yeast carboxyl-terminal domain kinase I positively and negatively regulates RNA polymerase II carboxyl-terminal domain phosphorylation J. Biol. Chem. 1999 274 39 27823 27828