The CTD code of RNA polymerase II: A structural view

Wiley Interdisciplinary Reviews: RNA

Volumn 4, Issue 1, 2013, Pages 1-16

  Jasnovidova, Olga ^a   Stefl, Richard ^a  

^a MASARYK UNIVERSITY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ARGININE; ASPARTIC ACID; COACTIVATOR ASSOCIATED ARGININE METHYLTRANSFERASE 1; GLUTAMIC ACID; HEPTAPEPTIDE; HYDROXYL GROUP; ISOMERASE; LYSINE; MESSENGER RNA; NUCLEOTIDYLTRANSFERASE; PEPTIDYLPROLYL ISOMERASE PIN1; PHENYLALANINE; PHOSPHATASE; PHOSPHOSERINE; PHOSPHOTRANSFERASE; POSITIVE TRANSCRIPTION ELONGATION FACTOR B; PROLINE; RNA POLYMERASE II; SERINE; SMALL NUCLEAR RNA; SUMO PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ANISOTROPY; CANDIDA ALBICANS; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; ENZYME ACTIVITY; GENE EXPRESSION; GENE MUTATION; GENETIC CONSERVATION; GENETIC TRANSCRIPTION; GLYCOSYLATION; HUMAN; HYDROGEN BOND; HYDROPHOBIC INTERACTION CHROMATOGRAPHY; ISOMERIZATION; MICROTUBULE; NONHUMAN; POSTTRANSCRIPTIONAL GENE SILENCING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; REVIEW; RNA ANALYSIS; RNA BINDING; RNA DEGRADATION; RNA PROCESSING; RNA SEQUENCE; TANDEM REPEAT; TRANSCRIPTION ELONGATION; UBIQUITINATION; YEAST;

AMINO ACID SEQUENCE; CARRIER PROTEINS; METHYLTRANSFERASES; PEPTIDYLPROLYL ISOMERASE; PROLINE; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; RNA POLYMERASE II; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION, GENETIC;

EID: 84871402053     PISSN: 17577004     EISSN: 17577012     Source Type: Journal    
DOI: 10.1002/wrna.1138     Document Type: Review

References (111)

1. van Dijk EL, Chen CL, d' Aubenton-Carafa Y, Gourvennec S, Kwapisz M, Roche V, Bertrand C, Silvain M, Legoix-Né P, Loeillet S, et al. XUTs are a class of Xrn1-sensitive antisense regulatory non-coding RNA in yeast. Nature 2011, 475:114-117.
2. Neil H, Malabat C, d' Aubenton-Carafa Y, Xu Z, Steinmetz LM, Jacquier A. Widespread bidirectional promoters are the major source of cryptic transcripts in yeast. Nature 2009, 457:1038-1042.
3. Xu Z, Wei W, Gagneur J, Perocchi F, Clauder-Munster S, Camblong J, Guffanti E, Stutz F, Huber W, Steinmetz LM. Bidirectional promoters generate pervasive transcription in yeast. Nature 2009, 457:1033-1037.
4. Tisseur M, Kwapisz M, Morillon A. Pervasive transcription - lessons from yeast. Biochimie 2011, 93:1889-1896.
5. Werner M, Thuriaux P, Soutourina J. Structure-function analysis of RNA polymerases I and III. Curr Opin Struct Biol 2009, 19:740-745.
6. Meinhart A, Kamenski T, Hoeppner S, Baumli S, Cramer P. A structural perspective of CTD function. Genes Dev 2005, 19:1401-1415.
7. Phatnani HP, Greenleaf AL. Phosphorylation and functions of the RNA polymerase II CTD. Genes Dev 2006, 20:2922-2936.
8. Muñoz MJ, de la Mata M, Kornblihtt AR. The carboxy terminal domain of RNA polymerase II and alternative splicing. Trends Biochem Sci 2010, 35:497-504.
9. Egloff S, Murphy S. Role of the C-terminal domain of RNA polymerase II in expression of small nuclear RNA genes. Biochem Soc Trans 2008, 36:537.
10. Hirose Y, Ohkuma Y. Phosphorylation of the C-terminal domain of RNA polymerase II plays central roles in the integrated events of eucaryotic gene expression. J Biochem 2007, 141:601-608.
11. Buratowski S. The CTD code. Nat Struct Mol Biol 2003, 10:679-680.
12. Chapman RD, Heidemann M, Hintermair C, Eick D. Molecular evolution of the RNA polymerase II CTD. Trends Genet 2008, 24:289-296.
13. 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.
14. Stiller JW, McConaughy BL, Hall BD. Evolutionary complementation for polymerase II CTD function. Yeast 2000, 16:57-64.
15. West ML, Corden JL. Construction and analysis of yeast RNA polymerase II CTD deletion and substitution mutations. Genetics 1995, 140:1223-1233.
16. Schwer B, Shuman S. Deciphering the RNA polymerase II CTD code in fission yeast. Mol Cell 2011, 43:311-318.
17. Coudreuse D, van Bakel H, Dewez M, Soutourina J, Parnell T, Vandenhaute J, Cairns B, Werner M, Hermand D. A gene-specific requirement of RNA polymerase II CTD phosphorylation for sexual differentiation in S. pombe. Curr Biol 2010, 20:1053-1064.
18. Akhtar MS, Heidemann M, Tietjen J, Zhang D, Chapman RD, Eick D, Ansari AZ. TFIIH kinase places bivalent marks on the carboxyl-terminal domain of RNA polymerase II. Mol Cell 2009, 34:387-393.
19. Kim M, Suh H, Cho E-J, Buratowski S. Phosphorylation of the Yeast Rpb1 C-terminal Domain at Serines 2, 5, and 7. J Biol Chem 2009, 284:26421-26426.
20. Kim H, Erickson B, Luo W, Seward D, Graber JH, Pollock DD, Megee PC, Bentley DL. Gene-specific RNA polymerase II phosphorylation and the CTD code. Nat Struct Mol Biol 2010, 17:1279-1286.
21. Tietjen JR, Zhang DW, Rodriguez-Molina JB, White BE, Akhtar MS, Heidemann M, Li X, Chapman RD, Shokat K, Keles S, et al. Chemical-genomic dissection of the CTD code. Nat Struct Mol Biol 2010, 17:1154-1161.
22. Chapman RD, Heidemann M, Albert TK, Mailhammer R, Flatley A, Meisterernst M, Kremmer E, Eick D. Transcribing RNA polymerase II is phosphorylated at CTD residue serine-7. Science 2007, 318:1780-1782.
23. Egloff S, O'Reilly D, Chapman RD, Taylor A, Tanzhaus K, Pitts L, Eick D, Murphy S. Serine-7 of the RNA polymerase II CTD is specifically required for snRNA gene expression. Science 2007, 318:1777-1779.
24. Egloff S, Szczepaniak SA, Dienstbier M, Taylor A, Knight S, Murphy S. The integrator complex recognizes a new double mark on the RNA polymerase II carboxyl-terminal domain. J Biol Chem 2010, 285:20564-20569.
25. Egloff S, Zaborowska J, Laitem C, Kiss T, Murphy S. Ser7 phosphorylation of the CTD recruits the RPAP2 Ser5 phosphatase to snRNA genes. Mol Cell 2012, 45:111-122.
26. Stiller JW, Cook MS. Functional unit of the RNA polymerase II C-terminal domain lies within Heptapeptide pairs. Eukaryot Cell 2004, 3:735-740.
27. Liu P, Greenleaf AL, Stiller JW. The essential sequence elements required for RNAP II carboxyl-terminal domain function in yeast and their evolutionary conservation. Mol Biol Evol 2008, 25:719-727.
28. Maniatis T, Reed R. An extensive network of coupling among gene expression machines. Nature 2002, 416:499-506.
29. Moore MJ, Proudfoot NJ. Pre-mRNA processing reaches back to transcription and ahead to translation. Cell 2009, 136:688-700.
30. Hsin J-P, Sheth A, Manley JL. RNAP II CTD phosphorylated on threonine-4 is required for histone mRNA 3′ end processing. Science 2011, 334:683-686.
31. Hintermair C, Heidemann M, Koch F, Descostes N, Gut M, Gut I, Fenouil R, Ferrier P, Flatley A, Kremmer E, et al. Threonine-4 of mammalian RNA polymerase II CTD is targeted by Polo-like kinase 3 and required for transcriptional elongation. EMBO J 2012, 31:2784-2797.
32. Baskaran R, Dahmus ME, Wang JY. Tyrosine phosphorylation of mammalian RNA polymerase II carboxyl-terminal domain. Proc Natl Acad Sci U S A 1993, 90:11167-11171.
33. Mayer A, Heidemann M, Lidschreiber M, Schreieck A, Sun M, Hintermair C, Kremmer E, Eick D, Cramer P. CTD tyrosine phosphorylation impairs termination factor recruitment to RNA polymerase II. Science 2012, 336:1723-1725.
34. Kelly WG, Dahmus ME, Hart GW. RNA polymerase II is a glycoprotein. Modification of the COOH-terminal domain by O-GlcNAc. J Biol Chem 1993, 268:10416-10424.
35. Comer FI, Hart GW. Reciprocity between O-GlcNAc and O-phosphate on the carboxyl terminal domain of RNA polymerase II. Biochemistry 2001, 40:7845-7852.
36. Ranuncolo SM, Ghosh S, Hanover JA, Hart GW, Lewis BA. Evidence of the involvement of O-GlcNAc-modified human RNA polymerase II CTD in transcription in vitro and in vivo. J Biol Chem 2012, 287:23549-23561.
37. Sims RJ, Rojas LA, Beck D, Bonasio R, Schüller R, Drury WJ, Eick D, Reinberg D. The C-Terminal domain of RNA polymerase II is modified by site-specific methylation. Science 2011, 332:99-103.
38. Li H, Zhang Z, Wang B, Zhang J, Zhao Y, Jin Y. Wwp2-mediated ubiquitination of the RNA polymerase II large subunit in mouse embryonic pluripotent stem cells. Mol Cell Biol 2007, 27:5296-5305.
39. Lu KP, Finn G, Lee TH, Nicholson LK. Prolyl cis-trans isomerization as a molecular timer. Nat Chem Biol 2007, 3:619-629.
40. Shaw PE. Peptidyl-prolyl isomerases: a new twist to transcription. EMBO Rep 2002, 3:521-526.
41. Shaw PE. Peptidyl-prolyl cis/trans isomerases and transcription: is there a twist in the tail? EMBO Rep 2007, 8:40-45.
42. Fanghänel J, Fischer G. Insights into the catalytic mechanism of peptidyl prolyl cis/trans isomerases. Front Biosci 2004, 9:3453-3478.
43. Egloff S, Dienstbier M, Murphy S. Updating the RNA polymerase CTD code: adding gene-specific layers. Trends Genet 2012, 7:333-341.
44. Buratowski S. Progression through the RNA polymerase II CTD cycle. Mol Cell 2009, 36:541-546.
45. Borggrefe T, Yue X. Interactions between subunits of the mediator complex with gene-specific transcription factors. Sem Cell Dev Biol 2011, 22:759-768.
46. Myers LC, Kornberg RD. Mediator of transcriptional regulation. Annu Rev Biochem 2000, 69:729-749.
47. Max T, Søgaard M, Svejstrup JQ. Hyperphosphorylation of the C-terminal repeat domain of RNA polymerase II facilitates dissociation of its complex with mediator. J Biol Chem 2007, 282:14113-14120.
48. Gu M, Lima CD. Processing the message: structural insights into capping and decapping mRNA. Curr Opin Struct Biol 2005, 15:99-106.
49. Hampsey M, Reinberg D. Tails of intrigue: phosphorylation of RNA polymerase II mediates histone methylation. Cell 2003, 113:429-432.
50. Brès V, Yoh SM, Jones KA. The multi-tasking P-TEFb complex. Curr Opin Cell Biol 2008, 20:334-340.
51. Ahn SH, Kim M, Buratowski S. Phosphorylation of serine 2 within the RNA polymerase II C-terminal domain couples transcription and 3′ end processing. Mol Cell 2004, 13:67-76.
52. Licatalosi DD, Geiger G, Minet M, Schroeder S, Cilli K, McNeil JB, Bentley DL. Functional interaction of yeast pre-mRNA 3′ end processing factors with RNA polymerase II. Mol Cell 2002, 9:1101-1111.
53. Rosonina E, Kaneko S, Manley JL. Terminating the transcript: breaking up is hard to do. Genes Dev 2006, 20:1050-1056.
54. Bataille AR, Jeronimo C, Jacques P-É, Laramée L, Fortin M-È, Forest A, Bergeron M, Hanes SD, Robert F. 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.
55. Mayer A, Lidschreiber M, Siebert M, Leike K, Soding J, Cramer P. Uniform transitions of the general RNA polymerase II transcription complex. Nat Struct Mol Biol 2010, 17:1272-1278.
56. Cramer P, Srebrow A, Kadener S, Werbajh S, de la Mata M, Melen G, Nogués G, Kornblihtt AR. Coordination between transcription and pre-mRNA processing. FEBS Letters 2001, 498:179-182.
57. Cagas PM, Corden JL. Structural studies of a synthetic peptide derived from the carboxyl-terminal domain of RNA polymerase II. Proteins 1995, 21:149-160.
58. Kumaki Y, Matsushima N, Yoshida H, Nitta K, Hikichi K. Structure of the YSPTSPS repeat containing two SPXX motifs in the CTD of RNA polymerase II: NMR studies of cyclic model peptides reveal that the SPTS turn is more stable than SPSY in water. Biochim Biophys Acta 2001, 1548:81-93.
59. Bienkiewicz EA, Moon Woody A-Y, Woody RW. Conformation of the RNA polymerase II C-terminal domain: circular dichroism of long and short fragments. J Mol Biol 2000, 297:119-133.
60. Dobbins JR, Murali N, Long EC. Structural redesign and stabilization of the overlapping tandem β-turns of RNA polymerase II. Int J Pept Protein Res 1996, 47:260-268.
61. Gerber H-P, Hagmann M, Seipel K, Georgiev O, West MAL, Litingtung Y, Schaffner W, Corden JL. RNA polymerase II C-terminal domain required for enhancer-driven transcription. Nature 1995, 374:660-662.
62. Meinhart A, Cramer P. Recognition of RNA polymerase II carboxy-terminal domain by 3′-RNA-processing factors. Nature 2004, 430:223-226.
63. Fabrega C, Shen V, Shuman S, Lima CD. Structure of an mRNA capping enzyme bound to the phosphorylated carboxy-terminal domain of RNA polymerase II. Mol Cell 2003, 11:1549-1561.
64. 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.
65. Lunde BM, Reichow SL, Kim M, Suh H, Leeper TC, Yang F, Mutschler H, Buratowski S, Meinhart A, Varani G. Cooperative interaction of transcription termination factors with the RNA polymerase II C-terminal domain. Nat Struct Mol Biol 2010, 17:1195-1201.
66. Zhang Y, Kim Y, Genoud N, Gao J, Kelly JW, Pfaff SL, Gill GN, Dixon JE, Noel JP. Determinants for dephosphorylation of the RNA polymerase II C-terminal domain by Scp1. Mol Cell 2006, 24:759-770.
67. Werner-Allen JW, Lee C-J, Liu P, Nicely NI, Wang S, Greenleaf AL, Zhou P. cis-proline-mediated Ser(P)5 dephosphorylation by the RNA polymerase II C-terminal domain phosphatase Ssu72. J Biol Chem 2011, 286:5717-5726.
68. Xiang K, Nagaike T, Xiang S, Kilic T, Beh MM, Manley JL, Tong L. Crystal structure of the human symplekin-Ssu72-CTD phosphopeptide complex. Nature 2010, 467:729-733.
69. Ghosh A, Shuman S, Lima CD. Structural insights to how mammalian capping enzyme reads the CTD code. Mol Cell 2011, 43:299-310.
70. Kubicek K, Cerna H, Holub P, Pasulka J, Hrossova D, Loehr F, Hofr C, Vanacova S, Stefl R. Serine phosphorylation and proline isomerization in RNAP II CTD control recruitment of Nrd1. Genes Dev 2012, 26:1891-1896.
71. Verdecia MA, Bowman ME, Lu KP, Hunter T, Noel JP. Structural basis for phosphoserine-proline recognition by group IV WW domains. Nat Struct Mol Biol 2000, 7:639-643.
72. Kim M, Krogan NJ, Vasiljeva L, Rando OJ, Nedea E, Greenblatt JF, Buratowski S. The yeast Rat1 exonuclease promotes transcription termination by RNA polymerase II. Nature 2004, 432:517-522.
73. Patturajan M, Wei X, Berezney R, Corden JL. A nuclear matrix protein interacts with the phosphorylated C-terminal domain of RNA polymerase II. Mol Cell Biol 1998, 18:2406-2415.
74. 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 U S A 2001, 98:445-450.
75. Sadowski M, Dichtl B, Hübner W, Keller W. Independent functions of yeast Pcf11p in pre-mRNA 3′ end processing and in transcription termination. EMBO J 2003, 22:2167-2177.
76. Steinmetz EJ, Brow DA. Control of pre-mRNA accumulation by the essential yeast protein Nrd1 requires high-affinity transcript binding and a domain implicated in RNA polymerase II association. Proc Nat Acad Sci 1998, 95:6699-6704.
77. 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.
78. Noble CG, Hollingworth D, Martin SR, Ennis-Adeniran V, Smerdon SJ, Kelly G, Taylor IA, Ramos A. Key features of the interaction between Pcf11 CID and RNA polymerase II CTD. Nat Struct Mol Biol 2005, 12:144-151.
79. Hausmann S, Shuman S. Characterization of the CTD phosphatase Fcp1 from fission yeast. J Biol Chem 2002, 277:21213-21220.
80. Suh M-H, Ye P, Zhang M, Hausmann S, Shuman S, Gnatt AL, Fu J. Fcp1 directly recognizes the C-terminal domain (CTD) and interacts with a site on RNA polymerase II distinct from the CTD. Proc Natl Acad Sci U S A 2005, 102:17314-17319.
81. Yeo M, Lin PS, Dahmus ME, Gill GN. A novel RNA polymerase II C-terminal domain phosphatase that preferentially dephosphorylates serine 5. J Biol Chem 2003, 278:26078-26085.
82. Wrighton KH, Willis D, Long J, Liu F, Lin X, Feng X-H. Small C-terminal domain phosphatases dephosphorylate the regulatory linker regions of Smad2 and Smad3 to enhance transforming growth factor-β signaling. J Biol Chem 2006, 281:38365-38375.
83. Ghosh A, Shuman S, Lima CD. The structure of Fcp1, an essential RNA polymerase II CTD phosphatase. Mol Cell 2008, 32:478-490.
84. Hausmann S, Erdjument-Bromage H, Shuman S. Schizosaccharomyces pombe carboxyl-terminal domain (CTD) phosphatase Fcp1: distributive mechanism, minimal CTD substrate, and active site mapping. J Biol Chem 2004, 279:10892-10900.
85. Zorio DAR, Bentley DL. The link between mRNA processing and transcription: communication works both ways. Exp Cell Res 2004, 296:91-97.
86. Proudfoot NJ, Furger A, Dye MJ. Integrating mRNA processing with transcription. Cell 2002, 108:501-512.
87. Pei Y, Hausmann S, Ho CK, Schwer B, Shuman S. The length, phosphorylation state, and primary structure of the RNA polymerase II carboxyl-terminal domain dictate interactions with mRNA capping enzymes. J Biol Chem 2001, 276:28075-28082.
88. Shuman S. Structure, mechanism, and evolution of the mRNA capping apparatus. Prog Nucleic Acid Res Mol Biol 2001, 66:1-40.
89. Ho CK, Shuman S. Distinct roles for CTD Ser-2 and Ser-5 phosphorylation in the recruitment and allosteric activation of mammalian mRNA capping enzyme. Mol Cell 1999, 3:405-411.
90. Wen Y, Shatkin AJ. Transcription elongation factor hSPT5 stimulates mRNA capping. Genes Dev 1999, 13:1774-1779.
91. Lippens G, Landrieu I, Smet C. Molecular mechanisms of the phospho-dependent prolyl cis/trans isomerase Pin1. FEBS J 2007, 274:5211-5222.
92. Joseph JD, Yeh ES, Swenson KI, Winkler MAR. The peptidyl-prolyl isomerase Pin1. Prog Cell Cycle Res 2003, 5:477-487.
93. Wulf G, Finn G, Suizu F, Lu KP. Phosphorylation-specific prolyl isomerization: is there an underlying theme? Nat Cell Biol 2005, 7:435-441.
94. Xu Y-X, Manley JL. Pin1 modulates RNA polymerase II activity during the transcription cycle. Genes Dev 2007, 21:2950-2962.
95. Wulf G, Ryo A, Liou Y-C, Lu KP. The prolyl isomerase Pin1 in breast development and cancer. Breast Cancer Res 2003, 5:76-82.
96. Lu KP. Pinning down cell signaling, cancer and Alzheimer's disease. Trend Biochem Sci 2004, 29:200-209.
97. Butterfield DA, Abdul HM, Opii W, Newman SF, Joshi G, Ansari MA, Sultana R. Review: Pin1 in Alzheimer's disease. J Neurochem 2006, 98:1697-1706.
98. Hutchins JRA, Clarke PR. Many fingers on the mitotic trigger: post-translational regulation of the Cdc25C phosphatase. Cell Cycle 2004, 3:41-45.
99. Zhou XZ, Kops O, Werner A, Lu P-J, Shen M, Stoller G, Küllertz G, Stark M, Fischer G, Lu KP. Pin1-dependent prolyl isomerization regulates dephosphorylation of Cdc25C and Tau proteins. Mol Cell 2000, 6:873-883.
100. Koren J, Jinwal UK, Davey Z, Kiray J, Arulselvam K, Dickey CA. Bending tau into shape: the emerging role of peptidyl-prolyl isomerases in tauopathies. Mol Neurobiol 2011, 44:65-70.
101. Morris DP, Phatnani HP, Greenleaf AL. Phospho-carboxyl-terminal domain binding and the role of a prolyl isomerase in Pre-mRNA 3′-end formation. J Biol Chem 1999, 274:31583-31587.
102. Macias MJ, Wiesner S, Sudol M. WW and SH3 domains, two different scaffolds to recognize proline-rich ligands. FEBS Lett 2002, 513:30-37.
103. Ilsley JL, Sudol M, Winder SJ. The WW domain: linking cell signalling to the membrane cytoskeleton. Cell Signal 2002, 14:183-189.
104. Sudol M, Hunter T. NeW wrinkles for an old domain. Cell 2000, 103:1001-1004.
105. Meinhart A, Silberzahn T, Cramer P. The mRNA transcription/processing factor Ssu72 is a potential tyrosine phosphatase. J Biol Chem 2003, 278:15917-15921.
106. Dichtl B, Blank D, Ohnacker M, Friedlein A, Roeder D, Langen H, Keller W. A role for SSU72 in balancing RNA polymerase II transcription elongation and termination. Mol Cell 2002, 10:1139-1150.
107. Krishnamurthy S, He X, Reyes-Reyes M, Moore C, Hampsey M. Ssu72 Is an RNA polymerase II CTD phosphatase. Mol Cell 2004, 14:387-394.
108. Steinmetz EJ, Brow DA. Ssu72 protein mediates both poly(A)-coupled and poly(a)-independent termination of RNA polymerase II transcription. Mol Cell Biol 2003, 23:6339-6349.
109. Hausmann S, Koiwa H, Krishnamurthy S, Hampsey M, Shuman S. Different strategies for carboxyl-terminal domain (CTD) recognition by Serine 5-specific CTD phosphatases. J Biol Chem 2005, 280:37681-37688.
110. Singh N, Ma Z, Gemmill T, Wu X, DeFiglio H, Rossettini A, Rabeler C, Beane O, Morse R, Palumbo MJ, et al. The Ess1 prolyl isomerase is required for transcription termination of small non-coding RNAs via the Nrd1 pathway. Mol Cell 2009, 36:255-266.
111. Zhang DW, Rodríguez-Molina JB, Tietjen JR, Nemec CM, Ansari AZ. Emerging views on the CTD code. Genet Res Int 2012, 2012:347214.