How an mRNA capping enzyme reads distinct RNA polymerase II and Spt5 CTD phosphorylation codes

Genes and Development

Volumn 28, Issue 12, 2014, Pages 1323-1336

  Doamekpor, Selom K ^a   Sanchez, Ana M ^b   Schwer, Beate ^b   Shuman, Stewart ^a   Lima, Christopher D ^a,c  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

mRNA capping; Regulation; RNA polymerase II; Spt5; Transcription

Indexed keywords

AMINO ACID; ELONGATION FACTOR; ENZYME; GUANYLYLTRANSFERASE; MESSENGER RNA; NUCLEOTIDYLTRANSFERASE; PROTEIN SPT5; RNA POLYMERASE II; SERINE; THREONINE; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL GROWTH; CELL VIABILITY; CRYSTAL STRUCTURE; IN VIVO STUDY; MOLECULAR BIOLOGY; MOLECULAR DOCKING; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RNA CAPPING; RNA TRANSCRIPTION; SCHIZOSACCHAROMYCES;

MRNA CAPPING; REGULATION; RNA POLYMERASE II; SPT5; TRANSCRIPTION;

GENETIC CODE; MODELS, MOLECULAR; NUCLEOTIDYLTRANSFERASES; PHOSPHORYLATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; RNA POLYMERASE II; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; THREONINE; TRANSCRIPTIONAL ELONGATION FACTORS;

EID: 84902519559     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.242768.114     Document Type: Article

References (39)

1. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, et al. 2010. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66: 213-221.
2. Buratowski S. 2009. Progression through the RNA polymerase II CTD cycle. Mol Cell 36: 541-546.
3. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, et al. 1998. Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54: 905-921.
4. Chang JH, Jiao X, Chiba K, Oh C, Martin CE, Kiledjian M, Tong L. 2012. Dxo1 is a new type of eukaryotic enzyme with both decapping and 59-39 exoribonuclease activity. Nat Struct Mol Biol 19: 1011-1017.
5. Changela A, Ho CK, Martins A, Shuman S, Mondragon A. 2001. Structure and mechanism of the RNA triphosphatase component of mammalian mRNA capping enzyme. EMBO J 20: 2575-2586.
6. Chen VB, Arendall WB 3rd, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC. 2010. MolProbity: all-atom structure validation for mac-romolecular crystallography. Acta Crystallogr D Biol Crystallogr 66: 12-21.
7. Chiu YL, Ho CK, Saha N, Schwer B, Shuman S, Rana TM. 2002. Tat stimulates cotranscriptional capping of HIV mRNA. Mol Cell 10: 585-597.
8. Corden JL. 2013. RNA polymerase II C-terminal domain: tethering transcription to transcript and template. Chem Rev 113: 8423-8455.
9. Eick D, Geyer M. 2013. The RNA polymerase II carboxy-terminal domain (CTD) code. Chem Rev 113: 8456-8490.
10. Emsley P, Lohkamp B, Scott WG, Cowtan K. 2010. Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66: 486-581.
11. Fabrega C, Shen V, Shuman S, Lima CD. 2003. Structure of an mRNA capping enzyme bound to the phosphorylated carboxy-terminal domain of RNA polymerase II. Mol Cell 11: 1549-1561.
12. Geronimo C, Bataille AR, Robert F. 2013. The writers, readers, and functions of the RNA polymerase II C-terminal domain code. Chem Rev 113: 8491-8522.
13. Ghosh A, Shuman S, Lima CD. 2011. Structural insights to how mammalian capping enzyme reads the CTD code. Mol Cell 43: 299-310.
14. Gu M, Lima CD. 2005. Processing the message: structural insights into capping and decapping mRNA. Curr Opin Struct Biol 15: 99-106.
15. Gu M, Rajashankar KR, Lima CD. 2010. Structure of the Saccharomyces cerevisiae Cet1-Ceg1 mRNA capping apparatus. Structure 18: 216-227.
16. Hakansson K, Doherty AJ, Shuman S, Wigley DB. 1997. X-ray crystallography reveals a large conformational change during guanyl transfer by mRNA capping enzymes. Cell 89: 545-553.
17. Hartzog GA, Fu J. 2013. The Spt4-Spt5 complex: a multi-faceted regulator of transcription elongation. Biochim Biophys Acta 1829: 105-115.
18. Ho CK, Shuman S. 1999. Distinct roles for CTD Ser2 and Ser5 phosphorylation in the recruitment and allosteric activation of mammalian capping enzyme. Mol Cell 3: 405-411.
19. Ho CK, Lehman K, Shuman S. 1999. An essential surface motif (WAQKW) of yeast RNA triphosphatase mediates formation of the mRNA capping enzyme complex with RNA guanylyl-transferase. Nucleic Acids Res 27: 4671-4678.
20. Jiao X, Xiang S, Oh C, Martin CE, Tong L, Kiledjian M. 2010. Identification of a quality-control mechanism for mRNA 59-end capping. Nature 467: 608-611.
21. Jiao X, Chang JH, Kilic T, Tong L, Kiledjian M. 2013. A mammalian pre-mRNA 59 end capping quality control mechanism and an unexpected link of capping to pre-mRNA processing. Mol Cell 50: 104-115.
22. Lima CD, Wang LK, Shuman S. 1999. Structure and mechanism of yeast RNA triphosphatase: an essential component of the mRNA capping apparatus. Cell 99: 533-543.
23. Lidschreiber M, Leike K, Cramer P. 2013. Cap completion and C-terminal repeat domain kinase recruitment underlie the initiation-elongation transition of RNA polymerase II. Mol Cell Biol 33: 3805-3816.
24. Lundblad JR, Laurance M, Goodman RH. 1996. Fluorescence polarization analysis of protein-DNA and protein-protein interactions. Mol Endocrinol 10: 607-612.
25. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. 2007. Phaser crystallographic software. J Appl Crystallogr 40: 658-674.
26. Mossessova E, Lima CD. 2000. Ulp1-SUMO crystal structure and genetic analysis reveal conserved interactions and a regulatory element essential for cell growth in yeast. Mol Cell 5: 865-876.
27. Otwinowski Z, Minor W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276: 307-326.
28. Pei Y, Shuman S. 2002. Interactions between fission yeast mRNA capping enzymes and elongation factor Spt5. J Biol Chem 277: 19639-19648.
29. Pei Y, Shuman S. 2003. Characterization of the Schizosaccha-romyces pombe Cdk9/Pch1 protein kinase: Spt5 phosphory-lation, autophosphorylation and mutational analysis. J Biol Chem 278: 43346-43356.
30. Pei Y, Hausmann S, Ho CK, Schwer B, Shuman S. 2001. The length, phosphorylation state, and primary structure of the RNA polymerase II carboxyl-terminal domain dictate interactions with mRNA capping enzymes. J Biol Chem 276: 28075-28082.
31. Pei Y, Du H, Singer J, St Amour C, Granitto S, Shuman S, Fisher RP. 2006. Cyclin-dependent kinase 9 (Cdk9) of fission yeast is activated by the CDK-activating kinase Csk1, overlaps functionally with the TFIIH-associated kinase Mcs6, and associates with the mRNA cap methyltransferase Pcm1 in vivo. Mol Cell Biol 26: 777-788.
32. Schneider S, Pei Y, Shuman S, Schwer B. 2010. Separable functions of the fission yeast Spt5 carboxyl-terminal domain (CTD) in capping enzyme binding and transcription elongation overlap with those of the RNA polymerase II CTD. Mol Cell Biol 30: 2353-2364.
33. Schwer B, Shuman S. 2011. Deciphering the RNA polymerase II CTD code in fission yeast. Mol Cell 43: 311-318.
34. Schwer B, Sanchez AM, Shuman S. 2012. Puncuation and syntax of the RNA polymerase II CTD code in fission yeast. Proc Natl Acad Sc i 109: 18024-18029.
35. Schwer B, Bitton DA, Sanchez AM, Bahler J, Shuman S. 2014. Individual letters of the RNA polymerase II CTD code govern distinct gene expression programs in fission yeast. Proc Natl Acad Sci 111: 4185-4190.
36. Shuman S, Lima CD. 2004. The polynucleotide ligase and RNA capping enzyme superfamily of covalent nucleotidyltrans-ferases. Curr Opin Struct Biol 14: 757-764.
37. St Amour CV, Sansó M, Bosken CA, Lee KM, Larochelle S, Zhang C, Shokat KM, Geyer M, Fisher RP. 2012. Separate domains of fission yeast Cdk9 (P-TEFb) are required for capping enzyme recruitment and primed (Ser7-phosphory-lated) Rpb1 carboxyl-terminal domain substrate recognition. Mol Cell Biol 32: 2372-2383.
38. Viladevall L, St Amour CV, Rosebrock A, Schneider S, Zhang C, Allen JJ, Shokat KM, Schwer B, Leatherwood JK, Fisher RP. 2009. TFIIH and P-TEFb coordinate transcription with capping enzyme recruitment at specific genes in fission yeast. Mol Cell 33: 738-751.
39. Wen Y, Shatkin AJ. 1999. Transcription elongation factor hSPT5 stimulates mRNA capping. Genes & Dev 13: 1774-1779.