Cotranscriptional splicing efficiency differs dramatically between Drosophila and mouse

RNA

Volumn 18, Issue 12, 2012, Pages 2174-2186

  Khodor, Yevgenia L ^a,b   Menet, Jerome S ^a   Tolan, Michael ^a   Rosbash, Michael ^a  

^a BRANDEIS UNIVERSITY   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Cotranscriptional; Mammalian splicing; Nascent sequencing; Pre mRNA splicing

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; DROSOPHILA; EXON; GENE; HIGH THROUGHPUT SCREENING; INTRON; LIVER; MOUSE; NONHUMAN; PRIORITY JOURNAL; RNA SPLICING; SEQUENCE ANALYSIS; SPECIES DIFFERENCE; TRANSCRIPTION REGULATION;

ALTERNATIVE SPLICING; ANIMALS; CELL LINE; DROSOPHILA; EXONS; GENES, INSECT; INTRONS; LIVER; MICE; RNA PRECURSORS; RNA SPLICE SITES; RNA SPLICING; SPECIES SPECIFICITY; TRANSCRIPTION, GENETIC;

EUKARYOTA; MAMMALIA; MUS;

EID: 84869859046     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.034090.112     Document Type: Article

References (73)

1. Alexander RD, Innocente SA, Barrass JD, Beggs JD. 2010. Splicing-dependent RNA polymerase pausing in yeast. Mol Cell 40: 582-593.
2. Ast G. 2004. How did alternative splicing evolve? Nat Rev Genet 5: 773-782. (Pubitemid 39336361)
3. Barta I, Iggo R. 1995. Autoregulation of expression of the yeast Dbp2p 'DEAD-box' protein is mediated by sequences in the conserved DBP2 intron. EMBO J 14: 3800-3808.
4. Bauren G, Wieslander L. 1994. Splicing of Balbiani ring 1 gene premRNA occurs simultaneously with transcription. Cell 76: 183-192. (Pubitemid 24035291)
5. Berget SM. 1995. Exon recognition in vertebrate splicing. J Biol Chem 270: 2411-2414.
6. Beyer AL, Osheim YN. 1988. Splice site selection, rate of splicing, and alternative splicing on nascent transcripts. Genes Dev 2: 754-765.
7. Bourquin JP, Stagljar I, Meier P, Moosmann P, Silke J, Baechi T, Georgiev O, Schaffner W. 1997. A serine/arginine-rich nuclear matrix cyclophilin interacts with the C-terminal domain of RNA polymerase II. Nucleic Acids Res 25: 2055-2061. (Pubitemid 27303438)
8. Brody Y, Neufeld N, Bieberstein N, Causse SZ, Bohnlein EM, Neugebauer KM, Darzacq X, Shav-Tal Y. 2011. The in vivo kinetics of RNA polymerase II elongation during co-transcriptional splicing. PLoS Biol 9: e1000573. doi: 10.1371/journal.pbio.1000573.
9. Burnette JM, Miyamoto-Sato E, Schaub MA, Conklin J, Lopez AJ. 2005. Subdivision of large introns in Drosophila by recursive splicing at nonexonic elements. Genetics 170: 661-674. (Pubitemid 40980668)
10. Carrillo Oesterreich F, Preibisch S, Neugebauer KM. 2010. Global analysis of nascent RNA reveals transcriptional pausing in terminal exons. Mol Cell 40: 571-581.
11. Cheng H, Dufu K, Lee CS, Hsu JL, Dias A, Reed R. 2006. Human mRNA export machinery recruited to the 5′ end of mRNA. Cell 127: 1389-1400. (Pubitemid 44960410)
12. Churchman LS, Weissman JS. 2011. Nascent transcript sequencing visualizes transcription at nucleotide resolution. Nature 469: 368-373.
13. Cooke C, Hans H, Alwine JC. 1999. Utilization of splicing elements and polyadenylation signal elements in the coupling of polyadenylation and last-intron removal. Mol Cell Biol 19: 4971-4979. (Pubitemid 29289536)
14. Custodio N, Carmo-Fonseca M, Geraghty F, Pereira HS, Grosveld F, Antoniou M. 1999. Inefficient processing impairs release of RNA from the site of transcription. EMBO J 18: 2855-2866. (Pubitemid 29233957)
15. Dabeva MD, Post-Beittenmiller MA, Warner JR. 1986. Autogenous regulation of splicing of the transcript of a yeast ribosomal protein gene. Proc Natl Acad Sci 83: 5854-5857. (Pubitemid 16000611)
16. Damgaard CK, Kahns S, Lykke-Andersen S, Nielsen AL, Jensen TH, Kjems J. 2008. A 5′ splice site enhances the recruitment of basal transcription initiation factors in vivo. Mol Cell 29: 271-278. (Pubitemid 351172825)
17. Das R, Dufu K, Romney B, Feldt M, Elenko M, Reed R. 2006. Functional coupling of RNAP II transcription to spliceosome assembly. Genes Dev 20: 1100-1109.
18. 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. (Pubitemid 44684848)
19. de la Mata M, Alonso CR, Kadener S, Fededa JP, Blaustein M, Pelisch F, Cramer P, Bentley D, Kornblihtt AR. 2003. A slow RNA polymerase II affects alternative splicing in vivo. Mol Cell 12: 525-532. (Pubitemid 37238937)
20. de la Mata M, Lafaille C, Kornblihtt AR. 2010. First come, first served revisited: Factors affecting the same alternative splicing event have different effects on the relative rates of intron removal. RNA 16: 904-912.
21. Dye MJ, Proudfoot NJ. 1999. Terminal exon definition occurs cotranscriptionally and promotes termination of RNA polymerase II. Mol Cell 3: 371-378. (Pubitemid 29290677)
22. Farlow A, Dolezal M, Hua L, Schlotterer C. 2012. The genomic signature of splicing-coupled selection differs between long and short introns. Mol Biol Evol 29: 21-24.
23. Flicek P, Amode MR, Barrell D, Beal K, Brent S, Carvalho-Silva D, Clapham P, Coates G, Fairley S, Fitzgerald S, et al. 2012. Ensembl 2012. Nucleic Acids Res 40: D84-D90.
24. Fox-Walsh KL, Dou Y, Lam BJ, Hung SP, Baldi PF, Hertel KJ. 2005. The architecture of pre-mRNAs affects mechanisms of splice-site pairing. Proc Natl Acad Sci 102: 16176-16181. (Pubitemid 41688887)
25. Gelfman S, Burstein D, Penn O, Savchenko A, Amit M, Schwartz S, Pupko T, Ast G. 2012. Changes in exon-intron structure during vertebrate evolution affect the splicing pattern of exons. Genome Res 22: 35-50.
26. Gornemann J, Kotovic KM, Hujer K, Neugebauer KM. 2005. Cotranscriptional spliceosome assembly occurs in a stepwise fashion and requires the cap binding complex. Mol Cell 19: 53-63. (Pubitemid 40884657)
27. Harr B, Turner LM. 2010. Genome-wide analysis of alternative splicing evolution among Mus subspecies. Mol Ecol (Suppl 1) 19: 228-239.
28. Hirose Y, Tacke R, Manley JL. 1999. Phosphorylated RNA polymerase II stimulates pre-mRNA splicing. Genes Dev 13: 1234-1239. (Pubitemid 29250190)
29. Ip JY, Schmidt D, Pan Q, Ramani AK, Fraser AG, Odom DT, Blencowe BJ. 2011. Global impact of RNA polymerase II elongation inhibition on alternative splicing regulation. Genome Res 21: 390-401.
30. Kadener S, Cramer P, Nogues G, Cazalla D, de la Mata M, Fededa JP, Werbajh SE, Srebrow A, Kornblihtt AR. 2001. Antagonistic effects of T-Ag and VP16 reveal a role for RNA pol II elongation on alternative splicing. EMBO J 20: 5759-5768. (Pubitemid 33010051)
31. Kessler O, Jiang Y, Chasin LA. 1993. Order of intron removal during splicing of endogenous adenine phosphoribosyltransferase and dihydrofolate reductase pre-mRNA. Mol Cell Biol 13: 6211-6222. (Pubitemid 23292615)
32. Khodor YL, Rodriguez J, Abruzzi KC, Tang CH, Marr MT II, Rosbash M. 2011. Nascent-seq indicates widespread cotranscriptional premRNA splicing in Drosophila. Genes Dev 25: 2502-2512.
33. Kim E, Du L, Bregman DB, Warren SL. 1997. Splicing factors associate with hyperphosphorylated RNA polymerase II in the absence of pre-mRNA. J Cell Biol 136: 19-28. (Pubitemid 27044801)
34. Kim E, Magen A, Ast G. 2007. Different levels of alternative splicing among eukaryotes. Nucleic Acids Res 35: 125-131. (Pubitemid 46189837)
35. Kim S, Kim H, Fong N, Erickson B, Bentley DL. 2011. Pre-mRNA splicing is a determinant of histone H3K36 methylation. Proc Natl Acad Sci 108: 13564-13569.
36. Kiseleva E, Wurtz T, Visa N, Daneholt B. 1994. Assembly and disassembly of spliceosomes along a specific pre-messenger RNP fiber. EMBO J 13: 6052-6061.
37. Kohler A, Hurt E. 2007. Exporting RNA from the nucleus to the cytoplasm. Nat Rev Mol Cell Biol 8: 761-773. (Pubitemid 47462133)
38. Kolasinska-Zwierz P, Down T, Latorre I, Liu T, Liu XS, Ahringer J. 2009. Differential chromatin marking of introns and expressed exons by H3K36me3. Nat Genet 41: 376-381.
39. Kuo H, Nasim FH, Grabowski PJ. 1991. Control of alternative splicing by the differential binding of U1 small nuclear ribonucleoprotein particle. Science 251: 1045-1050. (Pubitemid 21926196)
40. Kwek KY, Murphy S, Furger A, Thomas B, O'Gorman W, Kimura H, Proudfoot NJ, Akoulitchev A. 2002. U1 snRNA associates with TFIIH and regulates transcriptional initiation. Nat Struct Biol 9: 800-805. (Pubitemid 35257777)
41. Lacadie SA, Rosbash M. 2005. Cotranscriptional spliceosome assembly dynamics and the role of U1 snRNA:5′ss base pairing in yeast. Mol Cell 19: 65-75. (Pubitemid 40884658)
42. Lacadie SA, Tardiff DF, Kadener S, Rosbash M. 2006. In vivo commitment to yeast cotranscriptional splicing is sensitive to transcription elongation mutants. Genes Dev 20: 2055-2066. (Pubitemid 44157457)
43. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25. doi: 10.1186/gb-2009-10-3-r25.
44. LeMaire MF, Thummel CS. 1990. Splicing precedes polyadenylation during Drosophila E74A transcription. Mol Cell Biol 10: 6059-6063.
45. Lewis JD, Izaurralde E, Jarmolowski A, McGuigan C, Mattaj IW. 1996. A nuclear cap-binding complex facilitates association of U1 snRNP with the cap-proximal 5′ splice site. Genes Dev 10: 1683-1698. (Pubitemid 26268872)
46. Listerman I, Sapra AK, Neugebauer KM. 2006. Cotranscriptional coupling of splicing factor recruitment and precursor messenger RNA splicing in mammalian cells. Nat Struct Mol Biol 13: 815-822. (Pubitemid 44338776)
47. McCracken S, Fong N, Yankulov K, Ballantyne S, Pan G, Greenblatt J, Patterson SD, Wickens M, Bentley DL. 1997. The C-terminal domain of RNA polymerase II couples mRNA processing to transcription. Nature 385: 357-361.
48. Menet JS, Rodriguez J, Abruzzi KC, Rosbash M. 2012. Nascent-seq reveals novel features of mouse circadian transcriptional regulation. eLife (in press).
49. Mount SM, Burks C, Hertz G, Stormo GD, White O, Fields C. 1992. Splicing signals in Drosophila: Intron size, information content, and consensus sequences. Nucleic Acids Res 20: 4255-4262.
50. Nilsen TW, Graveley BR. 2010. Expansion of the eukaryotic proteome by alternative splicing. Nature 463: 457-463.
51. Niwa M, Berget SM. 1991. Mutation of the AAUAAA polyadenylation signal depresses in vitro splicing of proximal but not distal introns. Genes Dev 5: 2086-2095. (Pubitemid 21905900)
52. Oesterreich FC, Bieberstein N, Neugebauer KM. 2011. Pause locally, splice globally. Trends Cell Biol 21: 328-335.
53. Pandya-Jones A, Black DL. 2009. Co-transcriptional splicing of constitutive and alternative exons. RNA 15: 1896-1908.
54. Parenteau J, Durand M, Veronneau S, Lacombe AA, Morin G, Guerin V, Cecez B, Gervais-Bird J, Koh CS, Brunelle D, et al. 2008. Deletion of many yeast introns reveals a minority of genes that require splicing for function. Mol Biol Cell 19: 1932-1941.
55. Perales R, Bentley D. 2009. "Cotranscriptionality" - the transcription elongation complex as a nexus for nuclear transactions. Mol Cell 36: 178-191.
56. Preker PJ, Kim KS, Guthrie C. 2002. Expression of the essential mRNA export factor Yra1p is autoregulated by a splicing-dependent mechanism. RNA 8: 969-980.
57. Pruitt KD, Tatusova T, Klimke W, Maglott DR. 2009. NCBI Reference Sequences: Current status, policy and new initiatives. Nucleic Acids Res 37: D32-D36.
58. Rigo F, Kazerouninia A, Nag A, Martinson HG. 2005. The RNA tether from the poly(A) signal to the polymerase mediates coupling of transcription to cleavage and polyadenylation. Mol Cell 20: 733-745. (Pubitemid 41740695)
59. Robberson BL, Cote′ GJ, Berget SM. 1990. Exon definition may facilitate splice site selection in RNAs with multiple exons. Mol Cell Biol 10: 84-94.
60. Robert F, Blanchette M, Maes O, Chabot B, Coulombe B. 2002. A human RNA polymerase II-containing complex associated with factors necessary for spliceosome assembly. J Biol Chem 277: 9302- 9306.
61. Sharov AA, Dudekula DB, Ko MS. 2005. Genome-wide assembly and analysis of alternative transcripts in mouse. Genome Res 15: 748-754. (Pubitemid 41043646)
62. Spies N, Nielsen CB, Padgett RA, Burge CB. 2009. Biased chromatin signatures around polyadenylation sites and exons. Mol Cell 36: 245-254.
63. Sterner DA, Carlo T, Berget SM. 1996. Architectural limits on split genes. Proc Natl Acad Sci 93: 15081-15085. (Pubitemid 27009555)
64. Talerico M, Berget SM. 1994. Intron definition in splicing of small Drosophila introns. Mol Cell Biol 14: 3434-3445. (Pubitemid 24132754)
65. Tanner S, Stagljar I, Georgiev O, Schaffner W, Bourquin JP. 1997. A novel SR-related protein specifically interacts with the carboxyterminal domain (CTD) of RNA polymerase II through a conserved interaction domain. Biol Chem 378: 565-571. (Pubitemid 27296333)
66. Tardiff DF, Lacadie SA, Rosbash M. 2006. A genome-wide analysis indicates that yeast pre-mRNA splicing is predominantly posttranscriptional. Mol Cell 24: 917-929. (Pubitemid 44960098)
67. Trapnell C, Pachter L, Salzberg SL. 2009. TopHat: Discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111.
68. Vargas DY, Shah K, Batish M, Levandoski M, Sinha S, Marras SA, Schedl P, Tyagi S. 2011. Single-molecule imaging of transcriptionally coupled and uncoupled splicing. Cell 147: 1054-1065.
69. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP, Burge CB. 2008. Alternative isoform regulation in human tissue transcriptomes. Nature 456: 470-476. (Pubitemid 352759009)
70. Waterston RH, Lindblad-Toh K, Birney E, Rogers J, Abril JF, Agarwal P, Agarwala R, Ainscough R, Alexandersson M, An P, et al. 2002. Initial sequencing and comparative analysis of the mouse genome. Nature 420: 520-562. (Pubitemid 35477048)
71. Wetterberg I, Bauren G, Wieslander L. 1996. The intranuclear site of excision of each intron in Balbiani ring 3 pre-mRNA is influenced by the time remaining to transcription termination and different excision efficiencies for the various introns. RNA 2: 641-651. (Pubitemid 26374216)
72. Wuarin J, Schibler U. 1994. Physical isolation of nascent RNA chains transcribed by RNA polymerase II: Evidence for cotranscriptional splicing. Mol Cell Biol 14: 7219-7225. (Pubitemid 24326386)
73. Zhang G, Taneja KL, Singer RH, Green MR. 1994. Localization of pre-mRNA splicing in mammalian nuclei. Nature 372: 809-812.