Novel modifications on C-terminal domain of RNA polymerase II can fine-tune the phosphatase activity of Ssu72

ACS Chemical Biology

Volumn 8, Issue 9, 2013, Pages 2042-2052

  Luo, Yonghua ^a   Yogesha, S D ^a   Cannon, Joe R ^a   Yan, Wupeng ^a   Ellington, Andrew D ^a   Brodbelt, Jennifer S ^a   Zhang, Yan ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATASE; PROTEIN SSU72; RNA POLYMERASE II; SERINE; THREONINE; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; DROSOPHILA; ENZYME ACTIVITY; ENZYME MODIFICATION; HYDROGEN BOND; MASS SPECTROMETRY; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DEPHOSPHORYLATION; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; TRANSCRIPTION REGULATION;

AMINO ACID SEQUENCE; ANIMALS; CRYSTALLOGRAPHY, X-RAY; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MRNA CLEAVAGE AND POLYADENYLATION FACTORS; PEPTIDES; PHOSPHORYLATION; PROTEIN CONFORMATION; PROTEIN TYROSINE PHOSPHATASES; RNA POLYMERASE II;

EID: 84884621009     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb400229c     Document Type: Article

References (44)

1. Dahmus, M. E. (1996) Reversible phosphorylation of the C-terminal domain of RNA polymerase II J. Biol. Chem. 271, 19009-19012
2. Meinhart, A., Silberzahn, T., and Cramer, P. (2003) The mRNA transcription/processing factor Ssu72 is a potential tyrosine phosphatase J. Biol. Chem. 278, 15917-15921
3. Palancade, B. and Bensaude, O. (2003) Investigating RNA polymerase II carboxyl-terminal domain (CTD) phosphorylation Eur. J. Biochem. 270, 3859-3870
4. Egloff, S., Dienstbier, M., and Murphy, S. (2012) Updating the RNA polymerase CTD code: Adding gene-specific layers Trends Genet. 28, 333-341
5. Zhang, D. W., Rodriguez-Molina, J. B., Tietjen, J. R., Nemec, C. M., and Ansari, A. Z. (2012) Emerging views on the CTD code Genet. Res. Int. 2012, 347214
6. Jasnovidova, O. and Stefl, R. (2013) The CTD code of RNA polymerase II: A structural view Wiley Interdiscip Rev. RNA 4, 1-16
7. Corden, J. L. (1990) Tails of RNA polymerase II Trends Biochem. Sci. 15, 383-387
8. Fuda, N. J., Ardehali, M. B., and Lis, J. T. (2009) Defining mechanisms that regulate RNA polymerase II transcription in vivo Nature 461, 186-192
9. Xu, Y. X., Hirose, Y., Zhou, X. Z., Lu, K. P., and Manley, J. L. (2003) Pin1 modulates the structure and function of human RNA polymerase II Genes Dev. 17, 2765-2776
10. Xu, Y. X. and Manley, J. L. (2004) Pinning down transcription: Regulation of RNA polymerase II activity during the cell cycle Cell Cycle 3, 432-435
11. Palancade, B., Marshall, N. F., Tremeau-Bravard, A., Bensaude, O., Dahmus, M. E., and Dubois, M. F. (2004) Dephosphorylation of RNA polymerase II by CTD-phosphatase FCP1 is inhibited by phospho-CTD associating proteins J. Mol. Biol. 335, 415-424
12. Lu, P. J., Zhou, X. Z., Shen, M., and Lu, K. P. (1999) Function of WW domains as phosphoserine- or phosphothreonine-binding modules Science 283, 1325-1328
13. Verdecia, M. A., Bowman, M. E., Lu, K. P., Hunter, T., and Noel, J. P. (2000) Structural basis for phosphoserine-proline recognition by group IV WW domains Nat. Struct. Biol. 7, 639-643
14. Zhang, M., Wang, X. J., Chen, X., Bowman, M. E., Luo, Y., Noel, J. P., Ellington, A. D., Etzkorn, F. A., and Zhang, Y. (2012) Structural and kinetic analysis of prolyl-isomerization/phosphorylation cross-talk in the CTD code ACS Chem. Biol. 7, 1462-1470
15. Xiang, K., Nagaike, T., Xiang, S., Kilic, T., Beh, M. M., Manley, J. L., and Tong, L. (2010) Crystal structure of the human symplekin-Ssu72-CTD phosphopeptide complex Nature 467, 729-733
16. Werner-Allen, J. W., Lee, C. J., Liu, P., Nicely, N. I., Wang, S., Greenleaf, A. L., and Zhou, P. (2011) cis-Proline-mediated Ser(P)5 dephosphorylation by the RNA polymerase II C-terminal domain phosphatase Ssu72 J. Biol. Chem. 286, 5717-5726
17. He, X., Khan, A. U., Cheng, H., Pappas, D. L., Jr., Hampsey, M., and Moore, C. L. (2003) Functional interactions between the transcription and mRNA 3′ end processing machineries mediated by Ssu72 and Sub1 Genes Dev. 17, 1030-1042
18. Krishnamurthy, S., He, X., Reyes-Reyes, M., Moore, C., and Hampsey, M. (2004) Ssu72 Is an RNA Polymerase II CTD Phosphatase Mol. Cell 14, 387-394
19. Kennedy, S. A., Frazier, M. L., Steiniger, M., Mast, A. M., Marzluff, W. F., and Redinbo, M. R. (2009) Crystal structure of the HEAT domain from the Pre-mRNA processing factor Symplekin J. Mol. Biol. 392, 115-128
20. Heidemann, M. and Eick, D. (2012) Tyrosine-1 and threonine-4 phosphorylation marks complete the RNA polymerase II CTD phospho-code RNA Biol 9, 1144-1146
21. Tietjen, J. R., Zhang, D. W., Rodriguez-Molina, J. B., White, B. E., Akhtar, M. S., Heidemann, M., Li, X., Chapman, R. D., Shokat, K., Keles, S., Eick, D., and Ansari, A. Z. (2010) Chemical-genomic dissection of the CTD code Nat. Struct. Mol. Biol. 17, 1154-1161
22. Bataille, A. R., Jeronimo, C., Jacques, P. E., Laramee, L., Fortin, M. E., Forest, A., Bergeron, M., Hanes, S. D., and Robert, F. (2012) A universal RNA polymerase II CTD cycle is orchestrated by complex interplays between kinase, phosphatase, and isomerase enzymes along genes Mol. Cell 45, 158-170
23. Zhang, D. W., Mosley, A. L., Ramisetty, S. R., Rodriguez-Molina, J. B., Washburn, M. P., and Ansari, A. Z. (2012) 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. 287, 8541-8551
24. Hsin, J. P. and Manley, J. L. (2012) The RNA polymerase II CTD coordinates transcription and RNA processing Genes Dev. 26, 2119-2137
25. Hintermair, C., Heidemann, M., Koch, F., Descostes, N., Gut, M., Gut, I., Fenouil, R., Ferrier, P., Flatley, A., Kremmer, E., Chapman, R. D., Andrau, J. C., and Eick, D. (2012) Threonine-4 of mammalian RNA polymerase II CTD is targeted by Polo-like kinase 3 and required for transcriptional elongation EMBO J. 31, 2784-2797
26. Stiller, J. W., McConaughy, B. L., and Hall, B. D. (2000) Evolutionary complementation for polymerase II CTD function Yeast 16, 57-64
27. Schwer, B., Lehman, K., Saha, N., and Shuman, S. (2001) Characterization of the mRNA capping apparatus of Candida albicans J. Biol. Chem. 276, 1857-1864
28. Zhang, Y., Zhang, M., and Zhang, Y. (2011) 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, 435-444
29. Han, S. W., Lee, S. W., Bahar, O., Schwessinger, B., Robinson, M. R., Shaw, J. B., Madsen, J. A., Brodbelt, J. S., and Ronald, P. C. (2012) Tyrosine sulfation in a gram-negative bacterium Nat. Commun. 3, 1153
30. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray Diffraction Data Collected in Oscillation Mode Methods Enzymol. 276, 307-326
31. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics Acta Crystallogr., Sect. D: Biol. Crystallogr. 60, 2126-2132
32. Vonrhein, C., Flensburg, C., Keller, P., Sharff, A., Smart, O., Paciorek, W., Womack, T., and Bricogne, G. (2011) Data processing and analysis with the autoPROC toolbox Acta Crystallogr., Sect. D: Biol. Crystallogr. 67, 293-302
33. Chen, V. B., Arendall, W. B., 3rd, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity: All-atom structure validation for macromolecular crystallography Acta Crystallogr., Sect. D: Biol. Crystallogr. 66, 12-21
34. Laskowski, R. A., Moss, D. S., and Thornton, J. M. (1993) Main-chain bond lengths and bond angles in protein structures J. Mol. Biol. 231, 1049-1067
35. Zhang, Y. L., Yao, Z. J., Sarmiento, M., Wu, L., Burke, T. R., Jr., and Zhang, Z. Y. (2000) Thermodynamic study of ligand binding to protein-tyrosine phosphatase 1B and its substrate-trapping mutants J. Biol. Chem. 275, 34205-34212
36. Zhang, Y., Kim, Y., Genoud, N., Gao, J., Kelly, J. W., Pfaff, S. L., Gill, G. N., Dixon, J. E., and Noel, J. P. (2006) Determinants for dephosphorylation of the RNA polymerase II C-terminal domain by Scp1 Mol. Cell 24, 759-770
37. Xiang, K., Manley, J. L., and Tong, L. (2012) An unexpected binding mode for a Pol II CTD peptide phosphorylated at Ser7 in the active site of the CTD phosphatase Ssu72 Genes Dev. 26, 2265-2270
38. Hausmann, S., Koiwa, H., Krishnamurthy, S., Hampsey, M., and Shuman, S. (2005) Different strategies for carboxyl-terminal domain (CTD) recognition by serine 5-specific CTD phosphatases J. Biol. Chem. 280, 37681-37688
39. Meinhart, A. and Cramer, P. (2004) Recognition of RNA polymerase II carboxy-terminal domain by 3′-RNA-processing factors Nature 430, 223-226
40. Becker, R., Loll, B., and Meinhart, A. (2008) Snapshots of the RNA processing factor SCAF8 bound to different phosphorylated forms of the carboxyl-terminal domain of RNA polymerase II J. Biol. Chem. 283, 22659-22669
41. Bushnell, D. A. and Kornberg, R. D. (2003) Complete, 12-subunit RNA polymerase II at 4.1-A resolution: Implications for the initiation of transcription Proc. Natl. Acad. Sci. U.S.A. 100, 6969-6973
42. Sun, Z. W. and Hampsey, M. (1996) Synthetic enhancement of a TFIIB defect by a mutation in SSU72, an essential yeast gene encoding a novel protein that affects transcription start site selection in vivo Mol. Cell. Biol. 16, 1557-1566
43. Reyes-Reyes, M. and Hampsey, M. (2007) Role for the Ssu72 C-terminal domain phosphatase in RNA polymerase II transcription elongation Mol. Cell. Biol. 27, 926-936
44. Dichtl, B., Blank, D., Ohnacker, M., Friedlein, A., Roeder, D., Langen, H., and Keller, W. (2002) A role for SSU72 in balancing RNA polymerase II transcription elongation and termination Mol. Cell 10, 1139-1150