Adventures in time and space: Splicing efficiency and RNA polymerase II elongation rate

RNA Biology

Volumn 11, Issue 4, 2014, Pages 313-319

  Moehle, Erica A ^a,d   Braberg, Hannes ^a,b   Krogan, Nevan J ^a,b,c   Guthrie, Christine ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c GLADSTONE INSTITUTES   (United States)

^d University of California Berkeley   (United States)

Author keywords

Elongation rate; Kinetic coupling; RNA polymerase II; Splicing; Splicing efficiency

Indexed keywords

MESSENGER RNA PRECURSOR; RIBOSOME PROTEIN; RNA POLYMERASE II; TRANSCRIPTION FACTOR;

ALTERNATIVE RNA SPLICING; CONSENSUS SEQUENCE; DROSOPHILA MELANOGASTER; EXON; GENE EXPRESSION; GENE ONTOLOGY; HISTONE ACETYLATION; HISTONE MODIFICATION; INTRON; NONHUMAN; NONSENSE MEDIATED MRNA DECAY; NOTE; NUCLEOSOME; PHENOTYPE; POINT MUTATION; RNA SPLICING; SACCHAROMYCES CEREVISIAE; SPLICING DEFECT; TRANSCRIPTION ELONGATION; TRANSCRIPTION INITIATION; TRANSCRIPTION TERMINATION; GENETIC TRANSCRIPTION; GENETICS; HUMAN; KINETICS; METABOLISM; PHYSIOLOGY;

HUMANS; KINETICS; RNA POLYMERASE II; RNA SPLICING; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION ELONGATION, GENETIC; TRANSCRIPTION, GENETIC;

EID: 84901420191     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.28646     Document Type: Note

References (67)

1. Staley JP, Guthrie C. Mechanical devices of the spliceosome: motors, clocks, springs, and things. Cell 1998; 92:315-26; PMID:9476892; http://dx.doi.org/10.1016/S0092-8674(00)80925-3
2. Wahl MC, Will CL, Lührmann R. The spliceosome: design principles of a dynamic RNP machine. Cell 2009; 136:701-18; PMID:19239890; http://dx.doi.org/10.1016/j.cell.2009.02.009
3. Listerman I, Sapra AK, Neugebauer KM. Cotranscriptional coupling of splicing factor recruitment and precursor messenger RNA splicing in mammalian cells. Nat Struct Mol Biol 2006; 13:815-22; PMID:16921380; http://dx.doi.org/10. 1038/nsmb1135
4. Kotovic KM, Lockshon D, Boric L, Neugebauer KM. Cotranscriptional recruitment of the U1 snRNP to intron-containing genes in yeast. Mol Cell Biol 2003; 23:5768-79; PMID:12897147; http://dx.doi.org/10.1128/MCB.23.16.5768-5779. 2003
5. Lacadie SA, Rosbash M. Cotranscriptional spliceosome assembly dynamics and the role of U1 snRNA:5'ss base pairing in yeast. Mol Cell 2005; 19:65-75; PMID:15989965; http://dx.doi.org/10.1016/j.molcel.2005.05.006
6. Görnemann J, Kotovic KM, Hujer K, Neugebauer KM. Cotranscriptional spliceosome assembly occurs in a stepwise fashion and requires the cap binding complex. Mol Cell 2005; 19:53-63; PMID:15989964; http://dx.doi.org/10.1016/j. molcel.2005.05.007
7. Moore MJ, Schwartzfarb EM, Silver PA, Yu MC. Differential recruitment of the splicing machinery during transcription predicts genome-wide patterns of mRNA splicing. Mol Cell 2006; 24:903-15; PMID:17189192; http://dx.doi.org/10. 1016/j.molcel.2006.12.006
8. Tardiff DF, Lacadie SA, Rosbash M. A genome-wide analysis indicates that yeast pre-mRNA splicing is predominantly posttranscriptional. Mol Cell 2006; 24:917-29; PMID:17189193; http://dx.doi.org/10.1016/j.molcel.2006.12.002
9. Churchman LS, Weissman JS. Nascent transcript sequencing visualizes transcription at nucleotide resolution. Nature 2011; 469:368-73; PMID:21248844; http://dx.doi.org/10.1038/nature09652
10. Carrillo Oesterreich F, Preibisch S, Neugebauer KM. Global analysis of nascent RNA reveals transcriptional pausing in terminal exons. Mol Cell 2010; 40:571-81; PMID:21095587; http://dx.doi.org/10.1016/j.molcel.2010.11.004
11. Brugiolo M, Herzel L, Neugebauer KM. Counting on co-transcriptional splicing. F1000Prime Rep 2013; 5:9; PMID:23638305; http://dx.doi.org/10.12703/ P5-9
12. Aitken S, Alexander RD, Beggs JD. Modelling reveals kinetic advantages of co-transcriptional splicing. PLoS Comput Biol 2011; 7:e1002215; PMID:22022255; http://dx.doi.org/10.1371/journal.pcbi.1002215
13. de la Mata M, Alonso CR, Kadener S, Fededa JP, Blaustein M, Pelisch F, Cramer P, Bentley D, Kornblihtt AR; la Mata de M. A slow RNA polymerase II affects alternative splicing in vivo. Mol Cell 2003; 12:525-32; PMID:14536091; http://dx.doi.org/10.1016/j.molcel.2003.08.001
14. Dujardin G, Lafaille C, Petrillo E, Buggiano V, Gómez Acuña LI, Fiszbein A, Godoy Herz MA, Nieto Moreno N, Muñoz MJ, Alló M, et al. Transcriptional elongation and alternative splicing. Biochim Biophys Acta 2013; 1829:134-40; PMID:22975042; http://dx.doi.org/10.1016/j.bbagrm.2012.08.005
15. Howe KJ, Kane CM, Ares M Jr. Perturbation of transcription elongation influences the fidelity of internal exon inclusion in Saccharomyces cerevisiae. RNA 2003; 9:993-1006; PMID:12869710; http://dx.doi.org/10.1261/rna.5390803
16. Engebrecht JA, Voelkel-Meiman K, Roeder GS. Meiosis-specific RNA splicing in yeast. Cell 1991; 66:1257-68; PMID:1840507; http://dx.doi.org/10.1016/0092- 8674(91)90047-3
17. Munding EM, Igel AH, Shiue L, Dorighi KM, Treviño LR, Ares M Jr. Integration of a splicing regulatory network within the meiotic gene expression program of Saccharomyces cerevisiae. Genes Dev 2010; 24:2693-704; PMID:21123654; http://dx.doi.org/10.1101/gad.1977410
18. Bergkessel M, Whitworth GB, Guthrie C. Diverse environmental stresses elicit distinct responses at the level of pre-mRNA processing in yeast. RNA 2011; 17:1461-78; PMID:21697354; http://dx.doi.org/10.1261/rna.2754011
19. Pleiss JA, Whitworth GB, Bergkessel M, Guthrie C. Rapid, transcript-specific changes in splicing in response to environmental stress. Mol Cell 2007; 27:928-37; PMID:17889666; http://dx.doi.org/10.1016/j.molcel.2007. 07.018
20. Braberg H, Jin H, Moehle EA, Chan YA, Wang S, Shales M, Benschop JJ, Morris JH, Qiu C, Hu F, et al. From structure to systems: high-resolution, quantitative genetic analysis of RNA polymerase II. Cell 2013; 154:775-88; PMID:23932120; http://dx.doi.org/10.1016/j.cell.2013.07.033
21. Kaplan CD, Jin H, Zhang IL, Belyanin A. Dissection of Pol II trigger loop function and Pol II activity-dependent control of start site selection in vivo. PLoS Genet 2012; 8:e1002627; PMID:22511879; http://dx.doi.org/10.1371/journal. pgen.1002627
22. Pleiss JA, Whitworth GB, Bergkessel M, Guthrie C. Transcript specificity in yeast pre-mRNA splicing revealed by mutations in core spliceosomal components. PLoS Biol 2007; 5:e90; PMID:17388687; http://dx.doi.org/10.1371/ journal.pbio.0050090
23. Malagon F, Kireeva ML, Shafer BK, Lubkowska L, Kashlev M, Strathern JN. Mutations in the Saccharomyces cerevisiae RPB1 gene conferring hypersensitivity to 6-azauracil. Genetics 2006; 172:2201-9; PMID:16510790; http://dx.doi.org/10. 1534/genetics.105.052415
24. Kaplan CD, Larsson K-M, Kornberg RD. The RNA polymerase II trigger loop functions in substrate selection and is directly targeted by α-amanitin. Mol Cell 2008; 30:547-56; PMID:18538653; http://dx.doi.org/10.1016/j.molcel. 2008.04.023
25. nd, Rosbash M. Nascent-seq indicates widespread cotranscriptional pre-mRNA splicing in Drosophila. Genes Dev 2011; 25:2502-12; PMID:22156210; http://dx.doi.org/10. 1101/gad.178962.111
26. Mischo HE, Proudfoot NJ. Disengaging polymerase: terminating RNA polymerase II transcription in budding yeast. Biochim Biophys Acta 2013; 1829:174-85; PMID:23085255; http://dx.doi.org/10.1016/j.bbagrm.2012.10.003
27. Dye MJ, Proudfoot NJ. Terminal exon definition occurs cotranscriptionally and promotes termination of RNA polymerase II. Mol Cell 1999; 3:371-8; PMID:10198639; http://dx.doi.org/10.1016/S1097-2765(00)80464-5
28. Vagner S, Rüegsegger U, Gunderson SI, Keller W, Mattaj IW. Position-dependent inhibition of the cleavage step of pre-mRNA 3′-end processing by U1 snRNP. RNA 2000; 6:178-88; PMID:10688357; http://dx.doi.org/10. 1017/S1355838200991854
29. Rigo F, Martinson HG. Functional coupling of lastintron splicing and 3′-end processing to transcription in vitro: the poly(A) signal couples to splicing before committing to cleavage. Mol Cell Biol 2008; 28:849-62; PMID:17967872; http://dx.doi.org/10.1128/MCB.01410-07
30. Martins SB, Rino J, Carvalho T, Carvalho C, Yoshida M, Klose JM, de Almeida SF, Carmo-Fonseca M. Spliceosome assembly is coupled to RNA polymerase II dynamics at the 3′ end of human genes. Nat Struct Mol Biol 2011; 18:1115-23; PMID:21892168; http://dx.doi.org/10.1038/nsmb.2124
31. Noble SM, Guthrie C. Identification of novel genes required for yeast pre-mRNA splicing by means of cold-sensitive mutations. Genetics 1996; 143:67-80; PMID:8722763
32. Chanfreau G, Noble SM, Guthrie C. Essential yeast protein with unexpected similarity to subunits of mammalian cleavage and polyadenylation specificity factor (CPSF). Science 1996; 274:1511-4; PMID:8929408; http://dx.doi.org/10. 1126/science.274.5292.1511
33. Burckin T, Nagel R, Mandel-Gutfreund Y, Shiue L, Clark TA, Chong J-L, Chang T-H, Squazzo S, Hartzog G, Ares M Jr. Exploring functional relationships between components of the gene expression machinery. Nat Struct Mol Biol 2005; 12:175-82; PMID:15702072; http://dx.doi.org/10.1038/nsmb891
34. Munding EM, Shiue L, Katzman S, Donohue JP, Ares M Jr. Competition between pre-mRNAs for the splicing machinery drives global regulation of splicing. Mol Cell 2013; 51:338-48; PMID:23891561; http://dx.doi.org/10.1016/j. molcel.2013.06.012
35. Hazelbaker DZ, Marquardt S, Wlotzka W, Buratowski S. Kinetic competition between RNA Polymerase II and Sen1-dependent transcription termination. Mol Cell 2013; 49:55-66; PMID:23177741
36. Alexander RD, Innocente SA, Barrass JD, Beggs JD. Splicing-dependent RNA polymerase pausing in yeast. Mol Cell 2010; 40:582-93; PMID:21095588; http://dx.doi.org/10.1016/j.molcel.2010.11.005
37. rd, Millhouse S, Chen C-F, Lewis BA, Erdjument-Bromage H, Tempst P, Manley JL, Reinberg D. Recognition of trimethylated histone H3 lysine 4 facilitates the recruitment of transcription postinitiation factors and pre-mRNA splicing. Mol Cell 2007; 28:665-76; PMID:18042460; http://dx.doi.org/10.1016/j.molcel.2007.11.010
38. Luco RF, Pan Q, Tominaga K, Blencowe BJ, Pereira-Smith OM, Misteli T. Regulation of alternative splicing by histone modifications. Science 2010; 327:996-1000; PMID:20133523; http://dx.doi.org/10.1126/science.1184208
39. Gunderson FQ, Johnson TL. Acetylation by the transcriptional coactivator Gcn5 plays a novel role in co-transcriptional spliceosome assembly. PLoS Genet 2009; 5:e1000682; PMID:19834536; http://dx.doi.org/10.1371/journal.pgen.1000682
40. Gunderson FQ, Merkhofer EC, Johnson TL. Dynamic histone acetylation is critical for cotranscriptional spliceosome assembly and spliceosomal rearrangements. Proc Natl Acad Sci U S A 2011; 108:2004-9; PMID:21245291; http://dx.doi.org/10.1073/pnas.1011982108
41. Albulescu L-O, Sabet N, Gudipati M, Stepankiw N, Bergman ZJ, Huffaker TC, Pleiss JAA. A quantitative, high-throughput reverse genetic screen reveals novel connections between Pre-mRNA splicing and 5′ and 3′ end transcript determinants. PLoS Genet 2012; 8:e1002530; PMID:22479188; http://dx.doi.org/10.1371/journal.pgen.1002530
42. Moehle EA, Ryan CJ, Krogan NJ, Kress TL, Guthrie C. The yeast SR-like protein Npl3 links chromatin modification to mRNA processing. PLoS Genet 2012; 8:e1003101; PMID:23209445; http://dx.doi.org/10.1371/journal.pgen.1003101
43. Hnilicová J, Hozeifi S, Dušková E, Icha J, Tománková T, Staněk D. Histone deacetylase activity modulates alternative splicing. PLoS One 2011; 6:e16727; PMID:21311748; http://dx.doi.org/10.1371/journal.pone.0016727
44. Zhang Z, Jones A, Joo HY, Zhou D, Cao Y, Chen S, Erdjument-Bromage H, Renfrow M, He H, Tempst P, et al. USP49 deubiquitinates histone H2B and regulates cotranscriptional pre-mRNA splicing. Genes Dev 2013; 27:1581-95; PMID:23824326; http://dx.doi.org/10.1101/gad.211037.112
45. Zhang F, Yu X. WAC, a functional partner of RNF20/40, regulates histone H2B ubiquitination and gene transcription. Mol Cell 2011; 41:384-97; PMID:21329877; http://dx.doi.org/10.1016/j.molcel.2011.01.024
46. Luco RF, Alló M, Schor IE, Kornblihtt AR, Misteli T. Epigenetics in alternative pre-mRNA splicing. Cell 2011; 144:16-26; PMID:21215366; http://dx.doi.org/10.1016/j.cell.2010.11.056
47. Jaehning JA. The Paf1 complex: platform or player in RNA polymerase II transcription? Biochim Biophys Acta 2010; 1799:379-88; PMID:20060942; http://dx.doi.org/10.1016/j.bbagrm.2010.01.001
48. Mason PB, Struhl K. Distinction and relationship between elongation rate and processivity of RNA polymerase II in vivo. Mol Cell 2005; 17:831-40; PMID:15780939; http://dx.doi.org/10.1016/j.molcel.2005.02.017
49. Lacadie SA, Tardiff DF, Kadener S, Rosbash M. In vivo commitment to yeast cotranscriptional splicing is sensitive to transcription elongation mutants. Genes Dev 2006; 20:2055-66; PMID:16882983; http://dx.doi.org/10.1101/gad.1434706
50. Knaus R, Pollock R, Guarente L. Yeast SUB1 is a suppressor of TFIIB mutations and has homology to the human co-activator PC4. EMBO J 1996; 15:1933-40; PMID:8617240
51. García A, Collin A, Calvo O. Sub1 associates with Spt5 and influences RNA polymerase II transcription elongation rate. Mol Biol Cell 2012; 23:4297-312; PMID:22973055; http://dx.doi.org/10.1091/mbc.E12-04-0331
52. Tavenet A, Suleau A, Dubreuil G, Ferrari R, Ducrot C, Michaut M, Aude J-C, Dieci G, Lefebvre O, Conesa C, et al. Genome-wide location analysis reveals a role for Sub1 in RNA polymerase III transcription. Proc Natl Acad Sci U S A 2009; 106:14265-70; PMID:19706510; http://dx.doi.org/10.1073/pnas.0900162106
53. Hebbes TR, Thorne AW, Crane-Robinson C. A direct link between core histone acetylation and transcriptionally active chromatin. EMBO J 1988; 7:1395-402; PMID:3409869
54. de la Mata M, Muñoz MJ, Alló M, Fededa JP, Schor IE, Kornblihtt AR. RNA Polymerase II Elongation at the Crossroads of Transcription and Alternative Splicing. Genet Res Int 2011; 2011:309865; PMID:22567350; http://dx.doi.org/10.4061/2011/309865
55. Eperon LP, Graham IR, Griffiths AD, Eperon IC. Effects of RNA secondary structure on alternative splicing of pre-mRNA: is folding limited to a region behind the transcribing RNA polymerase? Cell 1988; 54:393-401; PMID:2840206; http://dx.doi.org/10.1016/0092-8674(88)90202-4
56. Lewicki BT, Margus T, Remme J, Nierhaus KH. Coupling of rRNA transcription and ribosomal assembly in vivo. Formation of active ribosomal subunits in Escherichia coli requires transcription of rRNA genes by host RNA polymerase which cannot be replaced by bacteriophage T7 RNA polymerase. J Mol Biol 1993; 231:581-93; PMID:8515441; http://dx.doi.org/10.1006/jmbi.1993.1311
57. Rouskin S, Zubradt M, Washietl S, Kellis M, Weissman JS. Genome-wide probing of RNA structure reveals active unfolding of mRNA structures in vivo. Nature 2014; 505:701-5; PMID:24336214; http://dx.doi.org/10.1038/nature12894
58. Ding Y, Tang Y, Kwok CK, Zhang Y, Bevilacqua PC, Assmann SM. In vivo genome-wide profiling of RNA secondary structure reveals novel regulatory features. Nature 2014; 505:696-700; PMID:24270811; http://dx.doi.org/10.1038/ nature12756
59. Volanakis A, Passoni M, Hector RD, Shah S, Kilchert C, Granneman S, Vasiljeva L. Spliceosome-mediated decay (SMD) regulates expression of nonintronic genes in budding yeast. Genes Dev 2013; 27:2025-38; PMID:24065768; http://dx.doi.org/10.1101/gad.221960.113
60. Sayani S, Chanfreau GF. Sequential RNA degradation pathways provide a fail-safe mechanism to limit the accumulation of unspliced transcripts in Saccharomyces cerevisiae. RNA 2012; 18:1563-72; PMID:22753783; http://dx.doi.org/10.1261/rna.033779.112
61. Gudipati RK, Xu Z, Lebreton A, Séraphin B, Steinmetz LM, Jacquier A, Libri D. Extensive degradation of RNA precursors by the exosome in wild-type cells. Mol Cell 2012; 48:409-21; PMID:23000176; http://dx.doi.org/10.1016/j. molcel.2012.08.018
62. Pandya-Jones A, Black DL. Co-transcriptional splicing of constitutive and alternative exons. RNA 2009; 15:1896-908; PMID:19656867; http://dx.doi.org/10. 1261/rna.1714509
63. Brody Y, Neufeld N, Bieberstein N, Causse SZ, Böhnlein E-M, Neugebauer KM, Darzacq X, Shav-Tal Y. The in vivo kinetics of RNA polymerase II elongation during co-transcriptional splicing. PLoS Biol 2011; 9:e1000573; PMID:21264352; http://dx.doi.org/10.1371/journal.pbio.1000573
64. Rhee HS, Pugh BF. Genome-wide structure and organization of eukaryotic pre-initiation complexes. Nature 2012; 483:295-301; PMID:22258509; http://dx.doi.org/10.1038/nature10799
65. Bhatt DM, Pandya-Jones A, Tong A-J, Barozzi I, Lissner MM, Natoli G, Black DL, Smale ST. Transcript dynamics of proinflammatory genes revealed by sequence analysis of subcellular RNA fractions. Cell 2012; 150:279-90; PMID:22817891; http://dx.doi.org/10.1016/j.cell.2012.05.043
66. Core LJ, Waterfall JJ, Lis JT. Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science 2008; 322:1845-8; PMID:19056941; http://dx.doi.org/10.1126/science.1162228
67. Schor IE, Fiszbein A, Petrillo E, Kornblihtt AR. Intragenic epigenetic changes modulate NCAM alternative splicing in neuronal differentiation. EMBO J 2013; 32:2264-74; PMID:23892457; http://dx.doi.org/10.1038/emboj.2013.167