Splicing of Nascent RNA Coincides with Intron Exit from RNA Polymerase II

Cell

Volumn 165, Issue 2, 2016, Pages 372-381

  Carrillo Oesterreich, Fernando ^a   Herzel, Lydia ^a,b   Straube, Korinna ^a   Hujer, Katja ^b   Howard, Jonathon ^a   Neugebauer, Karla M ^a  

^a YALE UNIVERSITY   (United States)

^b MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

RNA POLYMERASE II;

ARTICLE; GENE EXPRESSION; INTRON; NONHUMAN; PRIORITY JOURNAL; RNA ANALYSIS; RNA SEQUENCE; RNA SPLICING; RNA TRANSCRIPTION; SPLICEOSOME; TRANSCRIPTION ELONGATION; GENETIC TRANSCRIPTION; KINETICS; METABOLISM; PROCEDURES; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES; SEQUENCE ANALYSIS;

INTRONS; KINETICS; RNA POLYMERASE II; RNA SPLICING; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES; SEQUENCE ANALYSIS, RNA; SPLICEOSOMES; TRANSCRIPTION, GENETIC;

EID: 84964040029     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2016.02.045     Document Type: Article

References (53)

1. R.D. Alexander, S.A. Innocente, J.D. Barrass, and J.D. Beggs Splicing-dependent RNA polymerase pausing in yeast Mol. Cell 40 2010 582 593
2. M. Ares Jr., L. Grate, and M.H. Pauling A handful of intron-containing genes produces the lion's share of yeast mRNA RNA 5 1999 1138 1139
3. A. Bar-Even, E. Noor, Y. Savir, W. Liebermeister, D. Davidi, D.S. Tawfik, and R. Milo The moderately efficient enzyme: evolutionary and physicochemical trends shaping enzyme parameters Biochemistry 50 2011 4402 4410
4. N.I. Bieberstein, F. Carrillo Oesterreich, K. Straube, and K.M. Neugebauer First exon length controls active chromatin signatures and transcription Cell Rep. 2 2012 62 68
5. H. Braberg, H. Jin, E.A. Moehle, Y.A. Chan, S. Wang, M. Shales, J.J. Benschop, J.H. Morris, C. Qiu, F. Hu, and et al. From structure to systems: high-resolution, quantitative genetic analysis of RNA polymerase II Cell 154 2013 775 788
6. U. Braunschweig, S. Gueroussov, A.M. Plocik, B.R. Graveley, and B.J. Blencowe Dynamic integration of splicing within gene regulatory pathways Cell 152 2013 1252 1269
7. R.L. Brinster, J.M. Allen, R.R. Behringer, R.E. Gelinas, and R.D. Palmiter Introns increase transcriptional efficiency in transgenic mice Proc. Natl. Acad. Sci. USA 85 1988 836 840
8. M. Brugiolo, L. Herzel, and K.M. Neugebauer Counting on co-transcriptional splicing F1000Prime Rep. 5 2013 9
9. F. Carrillo Oesterreich, S. Preibisch, and K.M. Neugebauer Global analysis of nascent RNA reveals transcriptional pausing in terminal exons Mol. Cell 40 2010 571 581
10. F. Carrillo Oesterreich, N. Bieberstein, and K.M. Neugebauer Pause locally, splice globally Trends Cell Biol. 21 2011 328 335
11. L.S. Churchman, and J.S. Weissman Nascent transcript sequencing visualizes transcription at nucleotide resolution Nature 469 2011 368 373
12. L.S. Churchman, and J.S. Weissman Native elongating transcript sequencing (NET-seq) Curr. Protoc. Mol. Biol. 98:II:4 2012 14.4.1-14.4.17
13. A. Coulon, M.L. Ferguson, V. de Turris, M. Palangat, C.C. Chow, and D.R. Larson Kinetic competition during the transcription cycle results in stochastic RNA processing eLife 3 2014 e03939
14. J.C. Davis-Turak, K. Allison, M.N. Shokhirev, P. Ponomarenko, L.S. Tsimring, C.K. Glass, T.L. Johnson, and A. Hoffmann Considering the kinetics of mRNA synthesis in the analysis of the genome and epigenome reveals determinants of co-transcriptional splicing Nucleic Acids Res. 43 2015 699 707
15. G. Dujardin, C. Lafaille, M. de la Mata, L.E. Marasco, M.J. Muñoz, C. Le Jossic-Corcos, L. Corcos, and A.R. Kornblihtt How slow RNA polymerase II elongation favors alternative exon skipping Mol. Cell 54 2014 683 690
16. P. Eser, L. Wachutka, K.C. Maier, C. Demel, M. Boroni, S. Iyer, P. Cramer, and J. Gagneur Determinants of RNA metabolism in the Schizosaccharomyces pombe genome Mol. Syst. Biol. 12 2015 857
17. N. Fong, H. Kim, Y. Zhou, X. Ji, J. Qiu, T. Saldi, K. Diener, K. Jones, X.D. Fu, and D.L. Bentley Pre-mRNA splicing is facilitated by an optimal RNA polymerase II elongation rate Genes Dev. 28 2014 2663 2676
18. X.D. Fu, and M. Ares Jr. Context-dependent control of alternative splicing by RNA-binding proteins Nat. Rev. Genet. 15 2014 689 701
19. O. Gahura, C. Hammann, A. Valentová, F. Půta, and P. Folk Secondary structure is required for 3′ splice site recognition in yeast Nucleic Acids Res. 39 2011 9759 9767
20. J. Görnemann, K.M. Kotovic, K. Hujer, and K.M. Neugebauer Cotranscriptional spliceosome assembly occurs in a stepwise fashion and requires the cap binding complex Mol. Cell 19 2005 53 63
21. F.Q. Gunderson, and T.L. Johnson Acetylation by the transcriptional coactivator Gcn5 plays a novel role in co-transcriptional spliceosome assembly PLoS Genet. 5 2009 e1000682
22. L. Herzel, and K.M. Neugebauer Quantification of co-transcriptional splicing from RNA-Seq data Methods 85 2015 36 43
23. A.A. Hoskins, L.J. Friedman, S.S. Gallagher, D.J. Crawford, E.G. Anderson, R. Wombacher, N. Ramirez, V.W. Cornish, J. Gelles, and M.J. Moore Ordered and dynamic assembly of single spliceosomes Science 331 2011 1289 1295
24. K.J. Howe, C.M. Kane, and M. Ares Jr. Perturbation of transcription elongation influences the fidelity of internal exon inclusion in Saccharomyces cerevisiae RNA 9 2003 993 1006
25. M. Huranová, I. Ivani, A. Benda, I. Poser, Y. Brody, M. Hof, Y. Shav-Tal, K.M. Neugebauer, and D. Staněk The differential interaction of snRNPs with pre-mRNA reveals splicing kinetics in living cells J. Cell Biol. 191 2010 75 86
26. I. Jonkers, H. Kwak, and J.T. Lis Genome-wide dynamics of Pol II elongation and its interplay with promoter proximal pausing, chromatin, and exons eLife 3 2014 e02407
27. C.D. Kaplan, H. Jin, I.L. Zhang, and A. Belyanin Dissection of Pol II trigger loop function and Pol II activity-dependent control of start site selection in vivo PLoS Genet. 8 2012 e1002627
28. S.A. Lacadie, and M. Rosbash Cotranscriptional spliceosome assembly dynamics and the role of U1 snRNA:5'ss base pairing in yeast Mol. Cell 19 2005 65 75
29. S.A. Lacadie, D.F. Tardiff, S. Kadener, and M. Rosbash In vivo commitment to yeast cotranscriptional splicing is sensitive to transcription elongation mutants Genes Dev. 20 2006 2055 2066
30. R.F. Luco, M. Allo, I.E. Schor, A.R. Kornblihtt, and T. Misteli Epigenetics in alternative pre-mRNA splicing Cell 144 2011 16 26
31. R.M. Martin, J. Rino, C. Carvalho, T. Kirchhausen, and M. Carmo-Fonseca Live-cell visualization of pre-mRNA splicing with single-molecule sensitivity Cell Rep. 4 2013 1144 1155
32. F.W. Martinez-Rucobo, R. Kohler, M. van de Waterbeemd, A.J. Heck, M. Hemann, F. Herzog, H. Stark, and P. Cramer Molecular basis of transcription-coupled pre-mRNA capping Mol. Cell 58 2015 1079 1089
33. P.B. Mason, and K. Struhl Distinction and relationship between elongation rate and processivity of RNA polymerase II in vivo Mol. Cell 17 2005 831 840
34. M. Meyer, M. Plass, J. Pérez-Valle, E. Eyras, and J. Vilardell Deciphering 3'ss selection in the yeast genome reveals an RNA thermosensor that mediates alternative splicing Mol. Cell 43 2011 1033 1039
35. E.A. Moehle, H. Braberg, N.J. Krogan, and C. Guthrie Adventures in time and space: splicing efficiency and RNA polymerase II elongation rate RNA Biol. 11 2014 313 319
36. M.J. Muñoz, M.S. Pérez Santangelo, M.P. Paronetto, M. de la Mata, F. Pelisch, S. Boireau, K. Glover-Cutter, C. Ben-Dov, M. Blaustein, J.J. Lozano, and et al. DNA damage regulates alternative splicing through inhibition of RNA polymerase II elongation Cell 137 2009 708 720
37. S. Naftelberg, I.E. Schor, G. Ast, and A.R. Kornblihtt Regulation of alternative splicing through coupling with transcription and chromatin structure Annu. Rev. Biochem. 84 2015 165 198
38. Y.N. Osheim, O.L. Miller Jr., and A.L. Beyer RNP particles at splice junction sequences on Drosophila chorion transcripts Cell 43 1985 143 151
39. A. Pandya-Jones, and D.L. Black Co-transcriptional splicing of constitutive and alternative exons RNA 15 2009 1896 1908
40. P.J. Preker, and C. Guthrie Autoregulation of the mRNA export factor Yra1p requires inefficient splicing of its pre-mRNA RNA 12 2006 994 1006
41. M. Rabani, R. Raychowdhury, M. Jovanovic, M. Rooney, D.J. Stumpo, A. Pauli, N. Hacohen, A.F. Schier, P.J. Blackshear, N. Friedman, and et al. High-resolution sequencing and modeling identifies distinct dynamic RNA regulatory strategies Cell 159 2014 1698 1710
42. H. Saeki, and J.Q. Svejstrup Stability, flexibility, and dynamic interactions of colliding RNA polymerase II elongation complexes Mol. Cell 35 2009 191 205
43. U. Schmidt, E. Basyuk, M.C. Robert, M. Yoshida, J.P. Villemin, D. Auboeuf, S. Aitken, and E. Bertrand Real-time imaging of cotranscriptional splicing reveals a kinetic model that reduces noise: implications for alternative splicing regulation J. Cell Biol. 193 2011 819 829
44. I.E. Schor, N. Rascovan, F. Pelisch, M. Alló, and A.R. Kornblihtt Neuronal cell depolarization induces intragenic chromatin modifications affecting NCAM alternative splicing Proc. Natl. Acad. Sci. USA 106 2009 4325 4330
45. B. Schwer A conformational rearrangement in the spliceosome sets the stage for Prp22-dependent mRNA release Mol. Cell 30 2008 743 754
46. I. Shcherbakova, A.A. Hoskins, L.J. Friedman, V. Serebrov, I.R. Corrêa Jr., M.Q. Xu, J. Gelles, and M.J. Moore Alternative spliceosome assembly pathways revealed by single-molecule fluorescence microscopy Cell Rep. 5 2013 151 165
47. J. Singh, and R.A. Padgett Rates of in situ transcription and splicing in large human genes Nat. Struct. Mol. Biol. 16 2009 1128 1133
48. D.F. Tardiff, and M. Rosbash Arrested yeast splicing complexes indicate stepwise snRNP recruitment during in vivo spliceosome assembly RNA 12 2006 968 979
49. A. Veloso, K.S. Kirkconnell, B. Magnuson, B. Biewen, M.T. Paulsen, T.E. Wilson, and M. Ljungman Rate of elongation by RNA polymerase II is associated with specific gene features and epigenetic modifications Genome Res. 24 2014 896 905
50. M.C. Wahl, C.L. Will, and R. Lührmann The spliceosome: design principles of a dynamic RNP machine Cell 136 2009 701 718
51. C.M. Weber, S. Ramachandran, and S. Henikoff Nucleosomes are context-specific, H2A.Z-modulated barriers to RNA polymerase Mol. Cell 53 2014 819 830
52. I. Wetterberg, J. Zhao, S. Masich, L. Wieslander, and U. Skoglund In situ transcription and splicing in the Balbiani ring 3 gene EMBO J. 20 2001 2564 2574
53. C. Yan, J. Hang, R. Wan, M. Huang, C.C. Wong, and Y. Shi Structure of a yeast spliceosome at 3.6-angstrom resolution Science 349 2015 1182 1191