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

Biochemical Journal

Volumn 434, Issue 3, 2011, Pages 435-444

  Zhang, Yong ^a   Zhang, Mengmeng ^a   Zhang, Yan ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

C terminal domain; RNA polymerase II; Transcription regulation; Transcription termination; Tyrosine phosphatase

Indexed keywords

CYSTEINE; ESSENTIAL EUKARYOTIC PHOSPHATASE; HEPTAPEPTIDE; MESSENGER RNA; PHOSPHATASE; PROTEIN SSU72; PROTEIN SUBUNIT; PROTEIN TYROSINE PHOSPHATASE; RNA POLYMERASE II; TRANSCRIPTION ELONGATION FACTOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VANADIC ACID;

ARTICLE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CRYSTAL STRUCTURE; DEPHOSPHORYLATION; DROSOPHILA MELANOGASTER; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME SPECIFICITY; ENZYME SUBSTRATE; FLUOROMETRY; MELTING POINT; MOLECULAR WEIGHT; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; RNA PROCESSING; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; TRANSCRIPTION TERMINATION; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; ANIMALS; CARRIER PROTEINS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; HUMANS; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MRNA CLEAVAGE AND POLYADENYLATION FACTORS; MUTATION; OLIGOPEPTIDES; PHOSPHOPROTEIN PHOSPHATASES; PHOSPHORYLATION; PROTEIN CONFORMATION; PROTEIN TYROSINE PHOSPHATASES; RECOMBINANT PROTEINS; RNA POLYMERASE II; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ANALYSIS, PROTEIN;

DROSOPHILA MELANOGASTER; EUKARYOTA;

EID: 79952180042     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20101471     Document Type: Article

References (49)

1. Zhang, M., Gill, G. and Zhang, Y. (2010) Bio-molecular architects: a scaffold provided by the C-terminal domain of eukaryotic RNA polymerase II. Nano Rev. 1, doi: 10.3402/nano.vli0.5502
2. Corden, J. L. (1990) Tails of RNA polymerase II. Trends Biochem. Sci. 15, 383-387
3. Hausmann, S., Schwer, B. and Shuman, S. (2004) An encephalitozoon cuniculi ortholog of the RNA polymerase II carboxyl-terminal domain (CTD) serine phosphatase Fcp1. Biochemistry 43, 7111-7120 (Pubitemid 38720528)
4. Phatnani, H. P. and Greenleaf, A. L. (2006) Phosphorylation and functions of the RNA polymerase II CTD. Genes Dev. 20, 2922-2936
5. Egloff, S., O'Reilly, D., Chapman, R. D., Taylor, A., Tanzhaus, K., Pitts, L., Eick, D. and Murphy, S. (2007) Serine-7 of the RNA Polymerase II CTD is specifically required for snRNA gene expression. Science 318, 1777-1779
6. Buratowski, S. (2003) The CTD code. Nat. Struct. Mol. Biol. 10, 679-680
7. 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
8. Majello, B. and Napolitano, G. (2001) Control of RNA polymerase II activity by dedicated CTD kinases and phosphatases. Front. Biosci. 6, D1358-D1368
9. Archambault, J., Chambers, R. S., Kobor, M. S., Ho, Y., Cartier, M., Bolotin, D., Andrews, B., Kane, C. M. and Greenblatt, J. (1997) 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. 94, 14300-14305
10. Yeo, M., Lin, P. S., Dahmus, M. E. and Gill, G. N. (2003) A novel RNA polymerase II C-terminal domain phosphatase that preferentially dephosphorylates serine 5. J. Biol. Chem. 278, 26078-26085
11. Yeo, M., Lee, S.-K., Lee, B., Ruiz, E. C., Pfaff, S. L. and Gill, G. N. (2005) Small CTD phosphatases function in silencing neuronal gene expression. Science 307, 596-600
12. Ghosh, A., Shuman, S. and Lima, C. D. (2008) The structure of Fcp1, an essential RNA polymerase II CTD phosphatase. Mol. Cell 32, 478-490
13. 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
14. Zhang, M., Liu, J., Kim, Y., Dixon, J. E., Pfaff, S. L., Gill, G. N., Noel, J. P. and Zhang, Y. (2010) Structural and functional analysis of the phosphoryl transfer reaction mediated by the human small C-terminal domain phosphatase, Scp1. Protein Sci. 19, 974-986
15. 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
16. 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 (Pubitemid 38591409)
17. He, X., Khan, A. U., Cheng, H., Pappas, Jr, D. L., 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 (Pubitemid 36459455)
18. Kim, M., Vasiljeva, L., Rando, O. J., Zhelkovsky, A., Moore, C. and Buratowski, S. (2006) Distinct pathways for snoRNA and mRNA termination. Mol. Cell 24, 723-734 (Pubitemid 44839221)
19. Krishnamurthy, S., Ghazy, M. A., Moore, C. and Hampsey, M. (2009) Functional interaction of the Ess1 prolyl isomerase with components of the RNA polymerase II initiation and termination machineries. Mol. Cell. Biol. 29, 2925-2934
20. Mosley, A. L., Pattenden, S. G., Carey, M., Venkatesh, S., Gilmore, J. M., Florens, L., Workman, J. L. and Washburn, M. P. (2009) Rtr1 is a CTD phosphatase that regulates RNA polymerase II during the transition from serine 5 to serine 2 phosphorylation. Mol. Cell 34, 168-178
21. Aslanidis, C. and de Jong, P. J. (1990) Ligation-independent cloning of PCR products (LIC-PCR). Nucleic Acids Res. 18, 6069-6074
22. Walker, P. A., Leong, L. E., Ng, P. W., Tan, S. H., Waller, S., Murphy, D. and Porter, A. G. (1994) Efficient and rapid affinity purification of proteins using recombinant fusion proteases. Nat. Biotechnol. 12, 601-605
23. CCP4 (1994) Collaborative Computational Project, Number 4. The CCP4 Suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763
24. Adams, P. D., Grosse-Kunstleve, R. W., Hung, L.-W., Ioerger, T. R., McCoy, A. J., Moriarty, N. W., Read, R. J., Sacchettini, J. C., Sauter, N. K. and Terwilliger, T. C. (2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D Biol. Crystallogr. 58, 1948-1954
25. Brunger, A. T. (1992) Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature 355, 472-475
26. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132
27. Laskowski, R. A., MacArthur, M. W., Moss, D.S. and Thornton, J.M. (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291
28. Reference deleted
29. Geladopoulos, T. P., Sotiroudis, T. G. and Evangelopoulos, A. E. (1991) A malachite green colorimetric assay for protein phosphatase activity. Anal. Biochem. 192, 112-116
30. 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
31. Denu, J. M. and Dixon, J. E. (1995) A catalytic mechanism for the dual-specific phosphatases. Proc. Natl. Acad. Sci. U.S.A. 92, 5910-5914
32. Tonks, N. K. (2006) Protein tyrosine phosphatases: from genes, to function, to disease. Nat. Rev. Mol. Cell Biol. 7, 833-846
33. Shi, Y. (2009) Serine/threonine phosphatases: mechanism through structure. Cell 139, 468-484
34. Allen, K. N. and Dunaway-Mariano, D. (2004) Phosphoryl group transfer: evolution of a catalytic scaffold. Trends Biochem. Sci. 29, 495-503
35. Ramponi, G. and Stefani, M. (1997) Structure and function of the low Mr phosphotyrosine protein phosphatases. Biochim. Biophys. Acta 1341, 137-156
36. Holm, L. and Rosenstrom, P. (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res. 38, W545-W549
37. Lindqvist, Y., Schneider, G. and Vihko, P. (1994) Crystal structures of rat acid phosphatase complexed with the transition-state analogs vanadate and molybdate. Implications for the reaction mechanism. Eur. J. Biochem. 221, 139-142
38. Zhang, M., Zhou, M., van Etten, R. L. and Stauffacher, C. V. (1997) Crystal structure of bovine low molecular weight phosphotyrosyl phosphatase complexed with the transition state analog vanadate. Biochemistry 36, 15-23
39. Zhang, Z. Y. (2002) Protein tyrosine phosphatases: structure and function, substrate specificity, and inhibitor development. Annu. Rev. Pharmacol. Toxicol. 42, 209-234
40. Zhang, Z. Y., Davis, J. P. and Van Etten, R. L. (1992) Covalent modification and active site-directed inactivation of a low molecular weight phosphotyrosyl protein phosphatase. Biochemistry 31, 1701-1711
41. Peters, G.H., Frimurer, T.M. and Olsen, O.H. (1998) Electrostatic evaluation of the signature motif (H/V)CX5R(S/T) in protein-tyrosine phosphatases. Biochemistry 37, 5383-5393 (Pubitemid 28241919)
42. Zhang, Z. Y., Wang, Y. and Dixon, J. E. (1994) Dissecting the catalytic mechanism of protein-tyrosine phosphatases. Proc. Natl. Acad. Sci. U.S.A. 91, 1624-1627
43. Niesen, F. H., Berglund, H. and Vedadi, M. (2007) The use of differential scanning fluorimetry to detect ligand interactions that promote protein stability. Nat. Protoc. 2, 2212-2221
44. 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
45. Chiarugi, P., Cirri, P., Marra, F., Raugei, G., Camici, G., Manao, G. and Ramponi, G. (1997) LMW-PTP is a negative regulator of insulin-mediated mitotic and metabolic signalling. Biochem. Biophys. Res. Commun. 238, 676-682
46. Stein, E., Lane, A. A., Cerretti, D. P., Schoecklmann, H. O., Schroff, A. D., van Etten, R. L. and Daniel, T. O. (1998) Eph receptors discriminate specific ligand oligomers to determine alternative signaling complexes, attachment, and assembly responses. Genes Dev. 12, 667-678
47. Rigacci, S., Rovida, E., Bagnoli, S., Dello Sbarba, P. and Berti, A. (1999) Low Mr phosphotyrosine protein phosphatase activity on fibroblast growth factor receptor is not associated with enzyme translocation. FEBS Lett. 459, 191-194 (Pubitemid 29475028)
48. Bucciantini, M., Chiarugi, P., Cirri, P., Taddei, L., Stefani, M., Raugei, G., Nordlund, P. and Ramponi, G. (1999) The low Mr phosphotyrosine protein phosphatase behaves differently when phosphorylated at Tyr131 or Tyr132 by Src kinase. FEBS Lett. 456, 73-78 (Pubitemid 29339044)
49. 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