Unphosphorylated SR-like protein Npl3 stimulates RNA polymerase II elongation

PLoS ONE

Volumn 3, Issue 9, 2008, Pages

  Dermody, Jessica L ^a   Dreyfuss, Jonathan M ^d   Villén, Judit ^a   Ogundipe, Babatunde ^b   Gygi, Steven P ^a   Park, Peter J ^d   Ponticelli, Alfred S ^c   Moore, Claire L ^b   Buratowski, Stephen ^a   Bucheli, Miriam E ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY AT BUFFALO   (United States)

^d LABORATORY FOR MOLECULAR MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASEIN KINASE II; MESSENGER RNA; PROTEIN; PROTEIN NPL3; RNA POLYMERASE II; UNCLASSIFIED DRUG; CLEAVAGE AND POLYADENYLATION SPECIFICITY FACTOR; NPL3 PROTEIN, S CEREVISIAE; NUCLEAR PROTEIN; POLYADENYLIC ACID; RNA BINDING PROTEIN; RNA15 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; GENETIC TRANSCRIPTION; NONHUMAN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN RNA BINDING; REGULATORY MECHANISM; RNA SYNTHESIS; TRANSCRIPTION TERMINATION; BINDING COMPETITION; BIOLOGICAL MODEL; CHEMISTRY; ENZYME ACTIVE SITE; GENE EXPRESSION REGULATION; METABOLISM; PHOSPHORYLATION; PROTEIN TERTIARY STRUCTURE; SACCHAROMYCES CEREVISIAE;

BINDING, COMPETITIVE; CASEIN KINASE II; CATALYTIC DOMAIN; GENE EXPRESSION REGULATION, FUNGAL; MODELS, BIOLOGICAL; MRNA CLEAVAGE AND POLYADENYLATION FACTORS; NUCLEAR PROTEINS; PHOSPHORYLATION; POLY A; PROTEIN STRUCTURE, TERTIARY; RNA POLYMERASE II; RNA, MESSENGER; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION, GENETIC;

EID: 53749085710     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0003273     Document Type: Article

References (60)

1. Proudfoot NJ (1989) How RNA polymerase II terminates transcription in higher eukaryotes. Trends Biochem Sci 14: 105-110.
2. Hirose Y, Manley JL (2000) RNA polymerase II and the integration of nuclear events. Genes Dev 14: 1415-1429.
3. McCracken S, Fong N, Yankulov K, Ballantyne S, Pan G, et al. (1997) The C-terminal domain of RNA polymerase II couples mRNA processing to transcription. Nature 385: 357-361.
4. Zhao J, Hyman L, Moore C (1999) Formation of mRNA 3′ ends in eukaryotes: mechanism, regulation, and interrelationships with other steps in mRNA synthesis. Microbiol Mol Biol Rev 63: 405-445.
5. Sadowski M, Dichtl B, Hubner W, Keller W (2003) Independent functions of yeast Pcf11p in pre-mRNA 3′ end processing and in transcription termination. Embo J 22: 2167-2177.
6. Rosonina E, Kaneko S, Manley JL (2006) Terminating the transcript breaking up is hard to do. Genes Dev 20: 1050-1056.
7. Gross S, Moore CL (2001) Rna15 interaction with the A-rich yeast polyadenylation signal is an essential step in mRNA 3′-end formation. Mol Cell Biol 21: 8045-8055.
8. Gilbert W, Siebel CW, Guthrie C (2001) Phosphorylation by Sky1p promotes Np13p shuttling and mRNA dissociation. Rna 7: 302-313.
9. Lei EP, Krebber H, Silver PA (2001) Messenger RNAs are recruited for nuclear export during transcription. Genes Dev 15: 1771-1782.
10. Gilbert W, Guthrie C (2004) The Glc7p nuclear phosphatase promotes mRNA export by facilitating association of Mex67p with mRNA. Mol Cell 13: 201-212.
11. Bucheli ME, Buratowski S (2005) Npl3 is an antagonist of mRNA 3′ end formation by RNA polymerase II. Embo J 24: 2150-2160.
12. Bucheli ME, He X, Kaplan CD, Moore CL, Buratowski S (2007) Polyadenylation site choice in yeast is affected by competition between Npl3 and polyadenylation factor CFI. Rna.
13. Wong CM, Qiu H, Hu C, Dong J, Hinnebusch AG (2007) Yeast cap binding complex (CBC) impedes recruitment of cleavage factor IA to weak termination sites. Mol Cell Biol.
14. 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.
15. Phatnani HP, Greenleaf AL (2006) Phosphorylation and functions of the RNA polymerase II CTD. Genes Dev 20: 2922-2936.
16. Bentley DL (2005) Rules of engagement co-transcriptional recruitment of pre-mRNA processing factors. Curr Opin Cell Biol 17: 251-256.
17. Buratowski S (2003) The CTD code. Nat Struct Biol 10: 679-680.
18. Krogan NJ, Kim M, Ahn SH, Zhong G, Kobor MS, et al. (2002) RNA polymerase II elongation factors of Saccharomyces cerevisiae: a targeted proteomics approach. Mol Cell Biol 22: 6979-6992.
19. Krogan NJ, Peng WT, Cagney G, Robinson MD, Haw R, et al. (2004) High-definition macromolecular composition of yeast RNA-processing complexes. Mol Cell 13: 225-239.
20. Meggio F, Pinna LA (2003) One-thousand-and-one substrates of protein kinase CK2? Faseb J 17: 349-368.
21. Lewis BA, Sims RJ, 3rd, Lane WS, Reinberg D (2005) Functional characterization of core promoter elements: DPE-specific transcription requires the protein kinase CK2 and the PC4 coactivator. Mol Cell 18: 471-481.
22. Calvo O, Manley JL (2005) The transcriptional coactivator PC4/Subl has multiple functions in RNA polymerase II transcription. Embo J 24: 1009-1020.
23. Thomas MC, Chiang CM (2006) The general transcription machinery and general cofactors. Crit Rev Biochem Mol Biol 41: 105-178.
24. He X, Moore C (2005) Regulation of yeast mRNA 3′ end processing by phosphorylation. Mol Cell 19: 619-629.
25. Ryan K (2007) Pre-mRNA 3′ cleavage is reversibly inhibited in vitro by cleavage factor dephosphorylation. RNA Biol 4: 26-33.
26. Kadesch TR, Chamberlin MJ (1982) Studies of in vitro transcription by calf thymus RNA polymerase II using a novel duplex DNA template. J Biol Chem 257: 5286-5295.
27. Ziegler LM, Khaperskyy DA, Ammerman ML, Ponticelli AS (2003) Yeast RNA polymerase II lacking the Rpb9 subunit is impaired for interaction with transcription factor IIF. J Biol Chem 278: 48950-48956.
28. Kong SE, Banks CA, Shilatifard A, Conaway JW, Conaway RC (2005) ELL-associated factors 1 and 2 are positive regulators of RNA polymerase II elongation factor ELL. Proc Natl Acad Sci U S A 102: 10094-10098.
29. Misteli T, Caceres JF, Clement JQ, Krainer AR, Wilkinson MF, et al. (1998) Serine phosphorylation of SR proteins is required for their recruitment to sites of transcription in vivo. J Cell Biol 143: 297-307.
30. Xiao SH, Manley JL (1997) Phosphorylation of the ASF/SF2 RS domain affects both potein-protein and protein-RNA interactions and is necessary for splicing. Genes Dev 11: 334-344.
31. Shen H, Green MR (2004) A pathway of sequential arginine-serine-rich domain-splicing signal interactions during mammalian spliceosome assembly. Mol Cell 16: 363-373.
32. Lund MK, Kress TL, Guthrie C (2008) Autoregulation of Npl3, a yeast SR potein, requires a novel downstream region and serine-phosphorylation. Mol Cell Biol.
33. Deka P, Bucheli ME, Moore C, Buratowski S, Varani G (2008) Structure of the yeast SR protein Npl3 and Interaction with mRNA 3′-end processing signals. J Mol Biol 375: 136-150.
34. Li X, Gerber SA, Rudner AD, Beausoleil SA, Haas W, et al. (2007) Large-scale phosphorylation analysis of alpha-factor-arrested Saccharomyces cerevisiae. J Proteome Res 6: 1190-1197.
35. Ficarro SB, McCleland ML, Stukenberg PT, Burke DJ, Ross MM, et al. (2002) Phosphoproteome analysis by mass spectrometry and its application to Saccharomyces cerevisiae. Nat Biotechnol 20: 301-305.
36. Zielinski R, Hellman U, Kubinski K, Szyszka R (2006) Fip1-an essential component of the Saccharomyces cerevisiae polyadenylation machinery is phosophorylated by protein kinase CK2. Mol Cell Biochem 286: 191-197.
37. Sarno S, Vaglio P, Marin O, Issinger OG, Ruffato K, et al. (1997) Mutational analysis of residues implicated in the interaction between protein kinase CK2 and peptide substrates. Biochemistry 36: 11717-11724.
38. McBride AE, Cook JT, Stemmler EA, Rutledge KL, McGrath KA, et al. (2005) Arginine methylation of yeast mRNA-binding protein Npl3 directly affects its function, nuclear export, and intranuclear protein interactions. J Biol Chem 280: 30888-30898.
39. Pike AC, Rellos P, Niesen FH, Turnbull A, Oliver AW, et al. (2008) Activation segment dimerization: a mechanism for kinase autophosphorylation of non-consensus sites. Embo J 27: 704-714.
40. Sawa C, Nedea E, Krogan N, Wada T, Handa H, et al. (2004) Bromodomain factor 1 (Bdf1) is phosphorylated by protein kinase CK2. Mol Cell Biol 24: 4734-4742.
41. Flach J, Bossie M, Vogel J, Corbett A, Jinks T, et al. (1994) A yeast RNA-binding protein shuttles between the nucleus and the cytoplasm. Mol Cell Biol 14: 8399-8407.
42. Takagaki Y, Manley JL (1997) RNA recognition by the human polyadenylation factor CstF. Mol Cell Biol 17: 3907-3914.
43. Affymetrix (2005) GeneChip® Whole Transcript (WT) Sense Target Labeling Assay Manual .
44. Birse CE, Minvielle-Sebastia L, Lee BA, Keller W, Proudfoot NJ (1998) Coupling termination of transcription to messenger RNA maturation in yeast. Science 280: 298-301.
45. Aranda A, Proudfoot N (2001) Transcriptional termination factors for RNA polymerase II in yeast. Mol Cell 7: 1003-1011.
46. Torchet C, Bousquet-Antonelli C, Milligan L, Thompson E, Kufel J, et al. (2002) Processing of 3′-extended read-through transcripts by the exosome can generate functional mRNAs. Mol Cell 9: 1285-1296.
47. Shankar S, Hatoum A, Roberts JW (2007) A transcription antiterminator constructs a NusA-dependent shield to the emerging transcript. Mol Cell 27: 914-927.
48. de la Mata M, Kornblihtt AR (2006) RNA polymerase II C-terminal domain mediates regulation of alternative splicing by SRp20. Nat Struct Mol Biol 13: 973-980.
49. Kornblihtt AR, de la Mata M, Fededa JP, Munoz MJ, Nogues G (2004) Multiple links between transcription and splicing. Rna 10: 1489-1498.
50. Kaneko S, Manley JL (2005) The mammalian RNA polymerase II C-terminal domain interacts with RNA to suppress transcription-coupled 3′ end formation. Mol Cell 20: 91-103.
51. Tacke R, Chen Y, Manley JL (1997) Sequence-specific RNA binding by an SR protein requires RS domain phosphorylation: creation of an SRp40-specific splicing enhancer. Proc Natl Acad Sci U S A 94: 1148-1153.
52. Shen H, Green MR (2006) RS domains contact splicing signals and promote splicing by a common mechanism in yeast through humans. Genes Dev 20: 1755-1765.
53. Xiao SH, Manley JL (1998) Phosphorylation-dephosphorylation differentially affects activities of splicing factor ASF/5F2. Embo J 17: 6359-6367.
54. Velazquez-Dones A, Hagopian JC, Ma CT, Zhong XY, Zhou H, et al. (2005) Mass spectrometric and kinetic analysis of ASF/SF2 phosphorylation by SRPK1 and Clk/Sty. J Biol Chem 280: 41761-41768.
55. Huang CJ, Tang Z, Lin RJ, Tucker PW (2007) Phosphorylation by SR kinases regulates the binding of PTB-associated splicing factor (PSF) to the pre-mRNA polypyrimidine tract. FEBS Lett 581: 223-232.
56. Steinmetz EJ, Warren CL, Kuehner JN, Panbehi B, Ansari AZ, et al. (2006) Genome-wide distribution of yeast RNA polymerase II and its control by Sen1 helicase. Mol Cell 24: 735-746.
57. Kim M, Krogan NJ, Vasiljeva L, Rando OJ, Nedea E, et al. (2004) The yeast Rat1 exonuclease pomotes transcription termination by RNA polymerase II. Nature 432: 517-522.
58. Zhao J, Kessler M, Helmling S, O'Connor JP, Moore C (1999) Pta1, a component of yeast CF II, is required for both cleavage and poly(A) addition of mRNA precursor. Mol Cell Biol 19: 7733-7740.
59. Kim M, Vasiljeva L, Rando OJ, Zhelkovsky A, Moore C, et al. (2006) Distinct pathways for snoRNA and mRNA termination. Mol Cell 24: 723-734.
60. Team RDC (2007) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.