Widespread alternative and aberrant splicing revealed by lariat sequencing

Nucleic Acids Research

Volumn 43, Issue 17, 2015, Pages 8488-8501

  Stepankiw, Nicholas ^a   Raghavan, Madhura ^a   Fogarty, Elizabeth A ^a   Grimson, Andrew ^a   Pleiss, Jeffrey A ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALTERNATIVE RNA SPLICING; ARTICLE; CONTROLLED STUDY; EXON SKIPPING; GENE EXPRESSION PROFILING; GENE FREQUENCY; INTRON; NONHUMAN; PRIORITY JOURNAL; RNA SEQUENCE; SCHIZOSACCHAROMYCES POMBE; SEQUENCE ANALYSIS; SPLICEOSOME; VALIDATION PROCESS; GENE EXPRESSION REGULATION; GENETICS; RNA SPLICING; SCHIZOSACCHAROMYCES;

RNA SPLICING;

ALTERNATIVE SPLICING; GENE EXPRESSION REGULATION, FUNGAL; INTRONS; RNA SPLICE SITES; SCHIZOSACCHAROMYCES; SEQUENCE ANALYSIS, RNA;

EID: 84949035555     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv763     Document Type: Article

References (44)

1. Lee, Y. and Rio, D.C. (2015) Mechanisms and regulation of alternative pre-mRNA splicing. Annu. Rev. Biochem., 84, 291-323.
2. Moore, M., Query, C. and Sharp, P. (1993) Splicing of precursors to messenger RNAs by the spliceosome. In: The RNA World. Cold Spring Harbor Laboratory Press, NY, Vol. 1, pp. 303-357.
3. Domdey, H., Apostol, B., Lin, R.-J., Newman, A., Brody, E. and Abelson, J. (1984) Lariat structures are in vivo intermediates in yeast pre-mRNA splicing. Cell, 39, 611-621.
4. Nilsen, T.W. and Graveley, B.R. (2010) Expansion of the eukaryotic proteome by alternative splicing. Nature, 463, 457-463.
5. Chen, M. and Manley, J.L. (2009) Mechanisms of alternative splicing regulation: insights from molecular and genomics approaches. Nat. Rev. Mol. Cell Biol., 10, 741-754.
6. Lim, L.P. and Burge, C.B. (2001) A computational analysis of sequence features involved in recognition of short introns. Proc. Natl. Acad. Sci. U.S.A., 98, 11193-11198.
7. Hamid, F.M. and Makeyev, E.V. (2014) Emerging functions of alternative splicing coupled with nonsense-mediated decay. Biochem. Soc. Trans., 42, 1168-1173.
8. Fox-Walsh, K.L. and Hertel, K.J. (2009) Splice-site pairing is an intrinsically high fidelity process. Proc. Natl. Acad. Sci. U.S.A., 106, 1766-1771.
9. Melamud, E. and Moult, J. (2009) Stochastic noise in splicing machinery. Nucleic Acids Res., 37, 4873-4886.
10. Pickrell, J.K., Pai, A.A., Gilad, Y. and Pritchard, J.K. (2010) Noisy splicing drives mRNA isoform diversity in human cells. PLoS Genet., 6, e1001236.
11. Wood, V., Gwilliam, R., Rajandream, M.-A., Lyne, M., Lyne, R., Stewart, A., Sgouros, J., Peat, N., Hayles, J., Baker, S. et al. (2002) The genome sequence of Schizosaccharomyces pombe. Nature, 415, 871-880.
12. Kuhn, A.N. and Käufer, N.F. (2002) Pre-mRNA splicing in Schizosaccharomyces pombe. Curr. Genet., 42, 241-251.
13. Awan, A.R., Manfredo, A. and Pleiss, J.A. (2013) Lariat sequencing in a unicellular yeast identifies regulated alternative splicing of exons that are evolutionarily conserved with humans. Proc. Natl. Acad. Sci. U.S.A., 110, 12762-12767.
14. Gilbert, W. (1978) Why genes in pieces? Nature, 271, 501-501.
15. Forsburg, S.L. and Rhind, N. (2006) Basic methods for fission yeast. Yeast Chichester Engl., 23, 173-183.
16. Bolger, A.M., Lohse, M. and Usadel, B. (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinforma. Oxf. Engl., 30, 2114-2120.
17. Langmead, B. and Salzberg, S.L. (2012) Fast gapped-read alignment with Bowtie 2. Nat. Methods, 9, 357-359.
18. Taggart, A.J., DeSimone, A.M., Shih, J.S., Filloux, M.E. and Fairbrother, W.G. (2012) Large-scale mapping of branchpoints in human pre-mRNA transcripts in vivo. Nat. Struct. Mol. Biol., 19, 719-721.
19. Rhind, N., Chen, Z., Yassour, M., Thompson, D.A., Haas, B.J., Habib, N., Wapinski, I., Roy, S., Lin, M.F., Heiman, D.I. et al. (2011) Comparative functional genomics of the fission yeasts. Science, 332, 930-936.
20. Crooks, G.E., Hon, G., Chandonia, J.-M. and Brenner, S.E. (2004) WebLogo: a sequence logo generator. Genome Res., 14, 1188-1190.
21. Bitton, D.A., Rallis, C., Jeffares, D.C., Smith, G.C., Chen, Y.Y.C., Codlin, S., Marguerat, S. and Bähler, J. (2014) LaSSO, a strategy for genome-wide mapping of intronic lariats and branch points using RNA-seq. Genome Res., 24, 1169-1179.
22. Mercer, T.R., Clark, M.B., Andersen, S.B., Brunck, M.E., Haerty, W., Crawford, J., Taft, R.J., Nielsen, L.K., Dinger, M.E. and Mattick, J.S. (2015) Genome-wide discovery of human splicing branchpoints. Genome Res., 25, 290-303.
23. Wood, V., Harris, M.A., McDowall, M.D., Rutherford, K., Vaughan, B.W., Staines, D.M., Aslett, M., Lock, A., Bähler, J., Kersey, P.J. et al. (2012) PomBase: a comprehensive online resource for fission yeast. Nucleic Acids Res., 40, D695-D699.
24. Aebi, M. and Weissman, C. (1987) Precision and orderliness in splicing. Trends Genet., 3, 102-107.
25. Webb, C.J., Romfo, C.M., van Heeckeren, W.J. and Wise, J.A. (2005) Exonic splicing enhancers in fission yeast: functional conservation demonstrates an early evolutionary origin. Genes Dev., 19, 242-254.
26. Pérez-Valle, J. and Vilardell, J. (2012) Intronic features that determine the selection of the 3' splice site. Wiley Interdiscip. Rev. RNA, 3, 707-717.
27. Bitton, D.A., Atkinson, S.R., Rallis, C., Smith, G.C., Ellis, D.A., Chen, Y.Y.C., Malecki, M., Codlin, S., Lemay, J.-F., Cotobal, C. et al. (2015) Widespread exon skipping triggers degradation by nuclear RNA surveillance in fission yeast. Genome Res., doi:10.1101/gr.185371.114.
28. Romfo, C.M., Alvarez, C.J., van Heeckeren, W.J., Webb, C.J. and Wise, J.A. (2000) Evidence for Splice Site Pairing via Intron Definition in Schizosaccharomyces pombe. Mol. Cell. Biol., 20, 7955-7970.
29. Kim, D., Pertea, G., Trapnell, C., Pimentel, H., Kelley, R. and Salzberg, S.L. (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol., 14, R36.
30. Venables, J.P., Klinck, R., Bramard, A., Inkel, L., Dufresne-Martin, G., Koh, C., Gervais-Bird, J., Lapointe, E., Froehlich, U., Durand, M. et al. (2008) Identification of Alternative Splicing Markers for Breast Cancer. Cancer Res., 68, 9525-9531.
31. Cooper, T.A., Wan, L. and Dreyfuss, G. (2009) RNA and disease. Cell, 136, 777-793.
32. Xiong, H.Y., Alipanahi, B., Lee, L.J., Bretschneider, H., Merico, D., Yuen, R.K.C., Hua, Y., Gueroussov, S., Najafabadi, H.S., Hughes, T.R. et al. (2015) RNA splicing. The human splicing code reveals new insights into the genetic determinants of disease. Science, 347, 1254806.
33. Wang, Z. and Burge, C.B. (2008) Splicing regulation: from a parts list of regulatory elements to an integrated splicing code. RNA N. Y. N, 14, 802-813.
34. Kim, E., Magen, A. and Ast, G. (2007) Different levels of alternative splicing among eukaryotes. Nucleic Acids Res., 35, 125-131.
35. De Conti, L., Baralle, M. and Buratti, E. (2013) Exon and intron definition in pre-mRNA splicing. Wiley Interdiscip. Rev. RNA, 4, 49-60.
36. Shao, W., Kim, H.-S., Cao, Y., Xu, Y.-Z. and Query, C.C. (2012) A U1-U2 snRNP interaction network during intron definition. Mol. Cell. Biol., 32, 470-478.
37. Volanakis, A., Passoni, M., Hector, R.D., Shah, S., Kilchert, C., Granneman, S. and Vasiljeva, L. (2013) Spliceosome-mediated decay (SMD) regulates expression of nonintronic genes in budding yeast. Genes Dev., 27, 2025-2038.
38. Roy, K. and Chanfreau, G. (2014) Stress-induced nuclear RNA degradation pathways regulate yeast bromodomain factor 2 to promote cell survival. PLoS Genet., 10, e1004661.
39. Kawashima, T., Douglass, S., Gabunilas, J., Pellegrini, M. and Chanfreau, G.F. (2014) Widespread Use of Non-productive Alternative Splice Sites in Saccharomyces cerevisiae. PLoS Genet, 10, e1004249.
40. Box, J.A., Bunch, J.T., Tang, W. and Baumann, P. (2008) Spliceosomal cleavage generates the 3' end of telomerase RNA. Nature, 456, 910-914.
41. Chanfreau, G. (2003) Conservation of RNase III Processing Pathways and Specificity in Hemiascomycetes. Eukaryot. Cell, 2, 901-909.
42. Gagnon, J., Lavoie, M., Catala, M., Malenfant, F. and Elela, S.A. (2015) Transcriptome wide annotation of eukaryotic RNase III reactivity and degradation signals. PLoS Genet, 11, e1005000.
43. Merkin, J., Russell, C., Chen, P. and Burge, C.B. (2012) Evolutionary dynamics of gene and isoform regulation in mammalian tissues. Science, 338, 1593-1599.
44. Barbosa-Morais, N.L., Irimia, M., Pan, Q., Xiong, H.Y., Gueroussov, S., Lee, L.J., Slobodeniuc, V., Kutter, C., Watt, S., Colak, R. et al. (2012) The evolutionary landscape of alternative splicing in vertebrate species. Science, 338, 1587-1593.