An unexpected binding mode for a Pol II CTD peptide phosphorylated at Ser7 in the active site of the CTD phosphatase Ssu72

Genes and Development

Volumn 26, Issue 20, 2012, Pages 2265-2270

  Xiang, Kehui ^a   Manley, James L ^a   Tong, Liang ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Protein phosphatase; Protein structure; RNA polymerase

Indexed keywords

CARBOXY TERMINAL DOMAIN PHOSPHATASE SSU72; PEPTIDE; PHOSPHATASE; RNA POLYMERASE II; SERINE; SYMPLEKIN; UNCLASSIFIED DRUG;

ARTICLE; CRYSTAL STRUCTURE; CRYSTALLIZATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME BINDING; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE;

CARRIER PROTEINS; CATALYTIC DOMAIN; DNA POLYMERASE II; HUMANS; MODELS, MOLECULAR; PEPTIDES; PHOSPHOPROTEIN PHOSPHATASES; PHOSPHORIC MONOESTER HYDROLASES; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY;

EID: 84867726973     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.198853.112     Document Type: Article

References (35)

1. Akhtar MS, Heidemann M, Tietjen JR, Zhang DW, Chapman RD, Eick D, Ansari AZ. 2009. TFIIH kinase places bivalent marks on the carboxyterminal domain of RNA polymerase II. Mol Cell 34: 387-393.
2. Bataille AR, Jeronimo C, Jacques P-E, Laramee L, Fortin M-E, Forest A, Bergeron M, Hanes SD, 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.
3. Becker JW, Marcy AI, Rokosz LL, Axel MG, Burbaum JJ, Fitzgerald PMD, Cameron PM, Esser CK, Hagmann WK, Hermes JD, et al. 1995. Stromelysin-1: Three-dimensional structure of the inhibited catalytic domain and of the C-truncated proenzyme. Protein Sci 4: 1966-1976.
4. Buratowski S. 2009. Progression through the RNA polymerase II CTD cycle. Mol Cell 36: 541-546.
5. Chapman RD, Heidemann M, Albert TK, Mailhammer R, Flatley A, Meisterernst M, Kremmer E, Eick D. 2007. Transcribing RNA polymerase II is phosphorylated at CTD residue serine-7. Science 318: 1780-1782.
6. Egloff S, O'Reilly D, Chapman RD, Taylor A, Tanzhaus K, Pitts L, Eick D, Murphy S. 2007. Serine-7 of the RNA polymerase II CTD is specifically required for snRNA gene expression. Science 318: 1777-1779.
7. Emsley P, Cowtan KD. 2004. Coot: Model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
8. Feng S, Chen JK, Yu H, Simon JA, Schreiber SL. 1994. Two binding orientations for peptides to the Src SH3 domain: Development of a general model for SH3-ligand interactions. Science 266: 1241-1247.
9. Ghazy MA, He X, Singh BN, Hampsey M, Moore C. 2009. The essential N terminus of the Pta1 scaffold protein is required for snoRNA transcription termination and Ssu72 function but is dispensible for pre-mRNA 3'-end processing. Mol Cell Biol 29: 2296-2307.
10. Ghosh A, Shuman S, Lima CD. 2008. The structure of Fcp1, an essential RNA polymerase II CTD phosphatase. Mol Cell 32: 478-490.
11. Glover-Cutter K, Larochelle S, Erickson B, Zhang C, Shokat K, Fisher RP, Bentley DL. 2009. TFIIH-associated Cdk7 kinase functions in phosphorylation of C-terminal domain Ser7 residues, promoter-proximal pausing, and termination by RNA polymerase II. Mol Cell Biol 29: 5455-5464.
12. Hausmann S, Shuman S. 2002. Characterization of the CTD phosphatase Fcp1 from fission yeast. Preferential dephosphorylation of serine 2 versus serine 5. J Biol Chem 277: 21213-21220.
13. Hausmann S, Erdjument-Bromage H, Shuman S. 2004. Schizosaccharomyces pombe carboxyl-terminal domain (CTD) phosphatase Fcp1: Distributive mechanism, minimal CTD substrate, and active site mapping. J Biol Chem 279: 10892-10900.
14. Hausmann S, Koiwa H, Krishnamurthy S, Hampsey M, Shuman S. 2005. Different strategies for carboxyl-terminal domain (CTD) recognition by serine 5-specific CTD phosphatases. J Biol Chem 280: 37681-37688.
15. Hsin J-P, Sheth A, Manley JL. 2011. RNAP II CTD phosphorylated on threonine-4 is required for histone mRNA 3′ end processing. Science 334: 683-686.
16. Kamenski T, Heilmeier S, Meinhart A, Cramer P. 2004. Structure and mechanism of RNA polymerase II CTD phosphatases. Mol Cell 15: 399-407.
17. Kim M, Suh H, Cho EJ, Buratowski S. 2009. Phosphorylation of the yeast Rpb1 C-terminal domain at serines 2, 5, and 7. J Biol Chem 284: 26421-26426.
18. Kim H, Erickson B, Luo W, Seward D, Graber JH, Pollock DD, Megee PC, Bentley DL. 2010. Gene-specific RNA polymerase II phosphorylation and the CTD code. Nat Struct Mol Biol 17: 1279-1286.
19. Komarnitsky P, Cho EJ, Buratowski S. 2000. Different phosphorylated forms of RNA polymerase II and associated mRNA processing factors during transcription. Genes Dev 14: 2452-2460.
20. Krishnamurthy S, He X, Reyes-Reyes M, Moore CL, Hampsey M. 2004. Ssu72 is an RNA polymerase II CTD phosphatase. Mol Cell 14: 387-394.
21. + adaptor protein SspB. Nat Struct Mol Biol 12: 520-525.
22. Lim WA, Richards FM, Fox RO. 1994. Structural determinants of peptidebinding orientation and of sequence specificity in SH3 domains. Nature 372: 375-379.
23. Mayer A, Lidschreiber M, Siebert M, Leike K, Soding J, Cramer P. 2010. Uniform transitions of the general RNA polymerase II transcription complex. Nat Struct Mol Biol 17: 1272-1278.
24. Mayer A, Heidemann M, Lidschreiber M, Schreieck A, Sun M, Hintermair C, Kremmer E, Eick D, Cramer P. 2012. CTD tyrosine phosphorylation impairs termination factor recruitment to RNA polymerase II. Science 336: 1723-1725.
25. Meinhart A, Kamenski T, Hoeppner S, Baumli S, Cramer P. 2005. A structural perspective of CTD function. Genes Dev 19: 1401-1415.
26. Murshudov GN, Vagin AA, Dodson EJ. 1997. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255.
27. Otwinowski Z, Minor W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276: 307-326.
28. Phatnani HP, Greenleaf AL. 2006. Phosphorylation and functions of the RNA polymerase II CTD. Genes Dev 20: 2922-2936.
29. Qin J, Clore GM, Kennedy WP, Kuszewski J, Gronenborn AM. 1996. The solution structure of human thioredoxin complexed with its target from Ref-1 reveals peptide chain reversal. Structure 4: 613-620.
30. Schroeder SC, Schwer B, Shuman S, Bentley D. 2000. Dynamic association of capping enzymes with transcribing RNA polymerase II. Genes Dev 14: 2435-2440.
31. Takagaki Y, Manley JL. 2000. Complex protein interactions within the human polyadenylation machinery identify a novel component. Mol Cell Biol 20: 1515-1525.
32. Tietjen JR, Zhang DW, Rodriguez-Molina JB, White BE, Akhtar MS, Heidemann M, Li X, Chapman RD, Shokat K, Keles S, et al. 2010. Chemical-genomic dissection of the CTD code. Nat Struct Mol Biol 17: 1154-1161.
33. Werner-Allen JW, Lee C-J, Liu P, Nicely NI, Wang S, Greenleaf AL, 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.
34. Xiang K, Nagaike T, Xiang S, Kilic T, Behav MM, Manley JL, Tong L. 2010. Crystal structure of the human symplekin-Ssu72-CTD phosphopeptide complex. Nature 467: 729-733.
35. Zhang DW, Mosley AL, Ramisetty SR, Rodriguez-Molina JB, Washburn MP, Ansari AZ. 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.