Widespread exon skipping triggers degradation by nuclear RNA surveillance in fission yeast

Genome Research

Volumn 25, Issue 6, 2015, Pages 884-896

  Bitton, Danny A ^a   Atkinson, Sophie R ^a   Rallis, Charalampos ^a   Smith, Graeme C ^a   Ellis, David A ^a   Chen, Yuan Y C ^a,d   Malecki, Michal ^a   Codlin, Sandra ^a   Lemay, Jean François ^b   Cotobal, Cristina ^c   Bachand, François ^b   Marguerat, Samuel ^a,e   Mata, Juan ^c   Bähler, Jürg ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF SHERBROOKE   (Canada)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d DUKE NUS MEDICAL SCHOOL   (Singapore)

^e MRC CLINICAL SCIENCES CENTRE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL RNA; NUCLEAR RNA; DHP1PROTEIN, S POMBE; EXORIBONUCLEASE; RNA; RNA, CIRCULAR; SCHIZOSACCHAROMYCES POMBE PROTEIN; TRANSCRIPTOME;

ALTERNATIVE RNA SPLICING; ARTICLE; CONSENSUS SEQUENCE; CONTROLLED STUDY; DNA BASE COMPOSITION; EXON SKIPPING; GENE EXPRESSION; INTRON; MEIOSIS; NONHUMAN; PRIORITY JOURNAL; RNA DEGRADATION; RNA ISOLATION; RNA PROCESSING; RNA SEQUENCE; RNA SPLICING; SCHIZOSACCHAROMYCES POMBE; TRANSCRIPTION REGULATION; EXON; FUNGAL GENOME; GENETICS; METABOLISM; SCHIZOSACCHAROMYCES; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS;

EUKARYOTA; SCHIZOSACCHAROMYCES POMBE; SCHIZOSACCHAROMYCETACEAE;

ALTERNATIVE SPLICING; EXONS; EXORIBONUCLEASES; GENOME, FUNGAL; MEIOSIS; RNA; RNA, NUCLEAR; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, RNA; TRANSCRIPTOME;

EID: 84931828565     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.185371.114     Document Type: Article

References (71)

1. Alexander R, Beggs JD. 2010. Cross-talk in transcription, splicing and chro-matin: who makes the first call? Biochem Soc Trans 38: 1251-1256.
2. Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biol 11: R106.
3. ′ exonucleases of the exosome complex. EMBO J 17: 1497-1506.
4. Arribas-Layton M, Wu D, Lykke-Andersen J, Song H. 2013. Structural and functional control of the eukaryotic mRNA decapping machinery. Biochim Biophys Acta 1829: 580-589.
5. Ashwal-Fluss R, Meyer M, Pamudurti NR, Ivanov A, Bartok O, Hanan M, Evantal N, Memczak S, RajewskyN, KadenerS. 2014. circRNA biogenesis competes with pre-mRNA splicing. Mol Cell 56: 55-66.
6. Awan AR, Manfredo A, Pleiss JA. 2013. Lariat sequencing in a unicellular yeast identifies regulated alternative splicing of exons that are evolu-tionarily conserved with humans. Proc Natl Acad Sci 110: 12762-12767.
7. Barbosa-Morais NL, Irimia M, Pan Q, Xiong HY, Gueroussov S, Lee LJ, Slobodeniuc V, Kutter C, Watt S, Çolak R, et al. 2012. The evolutionary landscape of alternative splicing in vertebrate species. Science 338: 1587-1593.
8. Bentley DL. 2014. Coupling mRNA processing with transcription in time and space. Nat Rev Genet 15: 163-175.
9. Bitton DA, Rallis C, Jeffares DC, Smith GC, Chen YY, Codlin S, Marguerat S, Bähler J. 2014. LaSSO, a strategy for genome-wide mapping of intronic lariats and branch-points using RNA-seq. Genome Res 24: 1169-1179.
10. Boutz PL, Bhutkar A, Sharp PA. 2015. Detained introns are a novel, widespread class of post-transcriptionally spliced introns. Genes Dev 29: 63-80.
11. Braunschweig U, Gueroussov S, Plocik AM, Graveley BR, Blencowe BJ. 2013. Dynamic integration of splicing within gene regulatory pathways. Cell 152: 1252-1269.
12. Braunschweig U, Barbosa-Morais NL, Pan Q, Nachman EN, Alipanahi B, Gonatopoulos-Pournatzis T, Frey B, Irimia M, Blencowe BJ. 2014. Widespread intron retention in mammals functionally tunes transcrip-tomes. Genome Res 24: 1774-1786.
13. Cooper TA, Wan L, Dreyfuss G. 2009. RNA and disease. Cell 136: 777-793.
14. Crooks GE, Hon G, Chandonia JM, Brenner SE. 2004. WebLogo: a sequence logo generator. Genome Res 14: 1188-1190.
15. DeGennaro CM, Alver BH, Marguerat S, Stepanova E, Davis CP, Bähler J, Park PJ, Winston F. 2013. Spt6 regulates intragenic and antisense transcription, nucleosome positioning, and histone modifications genome-wide in fission yeast. Mol Cell Biol 33: 4779-4792.
16. Demir E, Dickson BJ. 2005. fruitless splicing specifies male courtship behavior in Drosophila. Cell 121: 785-794.
17. Drabenstot SD, Kupfer DM, White JD, Dyer DW, Roe BA, Buchanan KL, Murphy JW. 2003. FELINES: a utility for extracting and examining EST-defined introns and exons. Nucleic Acids Res 31: e141.
18. Duncan CD, Mata J. 2014. The translational landscape of fission-yeast mei-osis and sporulation. Nat Struct Mol Biol 21: 641-647.
19. Egecioglu DE, Kawashima TR, Chanfreau GF. 2012. Quality control of MATa1 splicing and exon skipping by nuclear RNA degradation. Nucleic Acids Res 40: 1787-1796.
20. Fairbrother WG, Yeh RF, Sharp PA, Burge CB. 2002. Predictive identification of exonic splicing enhancers in human genes. Science 297: 1007-1013.
21. Flicek P, Amode MR, Barrell D, Beal K, Billis K, Brent S, Carvalho-Silva D, Clapham P, Coates G, Fitzgerald S, et al. 2014. Ensembl 2014. Nucleic Acids Res 42: D749-D755.
22. Frenk S, Oxley D, Houseley J. 2014. The nuclear exosome is active and important during budding yeast meiosis. PLoS One 9: e107648.
23. Frischmeyer PA, van HoofA, O'Donnell K, Guerrerio AL, Parker R, Dietz HC. 2002. An mRNA surveillance mechanism that eliminates transcripts lacking termination codons. Science 295: 2258-2261.
24. Garneau NL, WiluszJ, Wilusz CJ. 2007. The highways and byways of mRNA decay. Nat Rev Mol Cell Biol 8: 113-126.
25. Gonzàlez-Porta M, Frankish A, Rung J, Harrow J, Brazma A. 2013. Transcriptome analysis of human tissues and cell lines reveals one dominant transcript per gene. Genome Biol 14: R70.
26. Guan Q, Zheng W, Tang S, Liu X, Zinkel RA, Tsui KW, Yandell BS, Culbertson MR. 2006. Impact of nonsense-mediated mRNA decay on the global expression profile of budding yeast. PLoS Genet 2: e203.
27. Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B, Damgaard CK, Kjems J. 2013. Natural RNA circles function as efficient microRNA sponges. Nature 495: 384-388.
28. Hilleren PJ, Parker R. 2003. Cytoplasmic degradation of splice-defective pre-mRNAs and intermediates. Mol Cell 12: 1453-1465.
29. Houseley J, TollerveyD. 2009. The many pathways of RNA degradation. Cell 136: 763-776.
30. Houseley J, LaCava J, Tollervey D. 2006. RNA-quality control by the exo-some. Nat Rev Mol Cell Biol 7: 529-539.
31. Ivanov A, Memczak S, Wyler E, Torti F, Porath HT, Orejuela MR, Piechotta M, Levanon EY, Landthaler M, Dieterich C, et al. 2014. Analysis of in-tron sequences reveals hallmarks of circular RNA biogenesis in animals. Cell Rep 10: 170-177.
32. Jeck WR, Sorrentino JA, Wang K, Slevin MK, Burd CE, Liu J, Marzluff WF, Sharpless NE. 2013. Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA 19: 141-157.
33. Käufer NF, Potashkin J. 2000. Analysis of the splicing machinery in fission yeast: a comparison with budding yeast and mammals. Nucleic Acids Res 28: 3003-3010.
34. Kawashima T, Douglass S, Gabunilas J, Pellegrini M, Chanfreau GF. 2014. Widespread use of non-productive alternative splice sites in Saccharomyces cerevisiae. PLoS Genet 10: e1004249.
35. Keren H, Lev-Maor G, AstG. 2010. Alternative splicing and evolution: diversification, exon definition and function. Nat Rev Genet 11: 345-355.
36. LaCava J, Houseley J, Saveanu C, Petfalski E, Thompson E, Jacquier A, Tollervey D. 2005. RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell 121: 713-724.
37. 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.
38. Lardenois A, Liu Y, Walther T, Chalmel F, Evrard B, Granovskaia M, Chu A, Davis RW, Steinmetz LM, Primig M. 2011. Execution of the meiotic noncoding RNA expression program and the onset of gametogenesis in yeast require the conserved exosome subunit Rrp6. Proc Natl Acad Sci 108: 1058-1063.
39. Lasda E, Parker R. 2014. Circular RNAs: diversity of form and function. RNA 20: 1829-1842.
40. Le Hir H, Nott A, Moore MJ. 2003. How introns influence and enhance eu-karyotic gene expression. Trends Biochem Sci 28: 215-220.
41. Lemieux C, Marguerat S, Lafontaine J, Barbezier N, Bähler J, Bachand F. 2011. A pre-mRNA degradation pathway that selectively targets in-tron-containing genes requires the nuclear poly(A)-binding protein. Mol Cell 44: 108-119.
42. Liang D, Wilusz JE. 2014. Short intronic repeat sequences facilitate circular RNA production. Genes Dev 28: 2233-2247.
43. Livesay SB, Collier SE, Bitton DA, Bähler J, Ohi MD. 2013. Structural and functional characterization of the N terminus of Schizosaccharomyces pombe Cwf10. Eukaryot Cell 12: 1472-1489.
44. Magen A, Ast G. 2005. The importance of being divisible by three in alternative splicing. Nucleic Acids Res 33: 5574-5582.
45. Malecki M, Viegas SC, Carneiro T, Golik P, Dressaire C, Ferreira MG, Arraiano CM. 2013. The exoribonuclease Dis3L2 defines a novel eukary-otic RNA degradation pathway. EMBO J 32: 1842-1854.
46. Marguerat S, Schmidt A, Codlin S, Chen W, Aebersold R, Bähler J. 2012. Quantitative analysis of fission yeast transcriptomes and proteomes in proliferating and quiescent cells. Cell 151: 671-683.
47. Mata J, Lyne R, Burns G, Bähler J. 2002. The transcriptional program of mei-osis and sporulation in fission yeast. Nat Genet 32: 143-147.
48. Melamud E, Moult J. 2009. Stochastic noise in splicing machinery. Nucleic Acids Res 37: 4873-4886.
49. Memczak S, Jens M, Elefsinioti A, Torti F, Krueger J, Rybak A, Maier L, Mackowiak SD, Gregersen LH, Munschauer M, et al. 2013. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 495: 333-338.
50. Merkin J, Russell C, ChenP, Burge CB. 2012. Evolutionary dynamics of gene and isoform regulation in Mammalian tissues. Science 338: 1593-1599.
51. Moldón A, Malapeira J, Gabrielli N, Gogol M, Gómez-Escoda B, Ivanova T, Seidel C, Ayté J. 2008. Promoter-driven splicing regulation in fission yeast. Nature 455: 997-1000.
52. Murakami H, Goto DB, Toda T, Chen ES, Grewal SI, Martienssen RA, Yanagida M. 2007. Ribonuclease activity of Dis3 is required for mitotic progression and provides a possible link between heterochromatin and kinetochore function. PLoS One 2: e317.
53. Pickrell JK, Pai AA, Gilad Y, Pritchard JK. 2010. Noisy splicing drives mRNA isoform diversity in human cells. PLoS Genet 6: e1001236.
54. Rhind N, Chen Z, Yassour M, Thompson DA, Haas BJ, Habib N, Wapinski I, Roy S, Lin MF, Heiman DI, et al. 2011. Comparative functional geno-mics of the fission yeasts. Science 332: 930-936.
55. Rice P, Longden I, Bleasby A. 2000. EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 16: 276-277.
56. Salzman J, Gawad C, Wang PL, Lacayo N, Brown PO. 2012. Circular RNAs are the predominant transcript isoform from hundreds of human genes in diverse cell types. PLoS One 7: e30733.
57. Sayani S, Chanfreau GF. 2012. Sequential RNA degradation pathways provide a fail-safe mechanism to limit the accumulation of unspliced transcripts in Saccharomyces cerevisiae. RNA 18: 1563-1572.
58. Sayani S, Janis M, Lee CY, Toesca I, Chanfreau GF. 2008. Widespread impact of nonsense-mediated mRNA decay on the yeast intronome. Mol Cell 31: 360-370.
59. Schmid M, Jensen TH. 2008. The exosome: a multipurpose RNA-decay machine. Trends Biochem Sci 33: 501-510.
60. Schmidt K, Butler JS. 2013. Nuclear RNA surveillance: roleof TRAMP in controlling exosome specificity. Wiley Interdiscip Rev RNA 4: 217-231.
61. Schneider C, Tollervey D. 2013. Threading the barrel of the RNA exosome. Trends Biochem Sci 38: 485-493.
62. Schwartz S, Ast G. 2010. Chromatin density and splicing destiny: on the cross-talk between chromatin structure and splicing. EMBO J 29: 1629-1636.
63. Schwer B, Bitton DA, Sanchez AM, Bähler 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.
64. Stamm S, Ben-Ari S, Rafalska I, Tang Y, Zhang Z, Toiber D, Thanaraj TA, Soreq H. 2005. Function of alternative splicing. Gene 344: 1-20.
65. Volanakis A, Passoni M, Hector RD, Shah S, Kilchert C, Granneman S, Vasiljeva L. 2013. Spliceosome-mediated decay (SMD) regulates expression of nonintronic genes in budding yeast. Genes Dev 27: 2025-2038.
66. Wang Z, Burge CB. 2008. Splicing regulation: from a parts list of regulatory elements to an integrated splicing code. RNA 14: 802-813.
67. Wang ET, SandbergR, Luo S, KhrebtukovaI, ZhangL, MayrC, KingsmoreSF, Schroth GP, Burge CB. 2008. Alternative isoform regulation in human tissue transcriptomes. Nature 456: 470-476.
68. Wang PL, Bao Y, Yee MC, Barrett SP, Hogan GJ, Olsen MN, Dinneny JR, Brown PO, Salzman J.2014. Circular RNA is expressed across the eukary-otic tree of life. PLoS One 9: e90859.
69. Wood V, Gwilliam R, Rajandream MA, Lyne M, LyneR, Stewart A, Sgouros J, Peat N, Hayles J, Baker S, et al. 2002. The genome sequence of Schizosaccharomyces pombe. Nature 415: 871-880.
70. Yeo GW, Van Nostrand EL, Liang TY. 2007. Discovery and analysis of evo-lutionarily conserved intronic splicing regulatory elements. PLoS Genet 3: e85.
71. Zhang XO, Wang HB, Zhang Y, Lu X, Chen LL, Yang L. 2014. Complementary sequence-mediated exon circularization. Cell 159: 134-147.