A comprehensive survey of non-canonical splice sites in the human transcriptome

Nucleic Acids Research

Volumn 42, Issue 16, 2014, Pages 10564-10578

  Parada, Guillermo E ^a   Munita, Roberto ^a   Cerda, Cledi A ^a   Gysling, Katia ^a  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

DINUCLEOTIDE; TRANSCRIPTOME; REGULATORY RNA SEQUENCE; RNA SPLICING;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; GM12878 CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; LYMPHOBLASTOID CELL LINE; MOUSE; NONHUMAN; NUCLEIC ACID ANALYSIS; REGULATORY RNA SEQUENCE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; RNA ANALYSIS; RNA EDITING; RNA SEQUENCE; RNA SPLICING; RNA STRUCTURE; SANGER SEQUENCING; SEQUENCE ANALYSIS; SPECIES DIFFERENCE; U12 NON CANONICAL SPLICE SITE; U2 NON CANONICAL SPLICE SITE; ALTERNATIVE RNA SPLICING; ANIMAL; ARTIFACT; CELL LINE; CONSENSUS SEQUENCE; GENE EXPRESSION PROFILING; INTRON; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; SPLICEOSOME;

ALTERNATIVE SPLICING; ANIMALS; ARTIFACTS; BASE SEQUENCE; CELL LINE; CONSENSUS SEQUENCE; EVOLUTION, MOLECULAR; GENE EXPRESSION PROFILING; HUMANS; INTRONS; MICE; MOLECULAR SEQUENCE ANNOTATION; REGULATORY SEQUENCES, RIBONUCLEIC ACID; RNA EDITING; RNA SPLICE SITES; SEQUENCE ANALYSIS, RNA; SPLICEOSOMES; TRANSCRIPTOME;

EID: 84921334197     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku744     Document Type: Review

References (74)

1. Hoskins, A.A. and Moore, M.J. (2012) The spliceosome: a flexible, reversible macromolecular machine. Trends Biochem. Sci., 37, 179-188.
2. Will, C.L. and Luhrmann, R. (2011) Spliceosome structure and function. Cold Spring Harb. Perspect. Biol., 3.
3. Aebi, M., Hornig, H., Padgett, R.A., Reiser, J. and Weissmann, C. (1986) Sequence requirements for splicing of higher eukaryotic nuclear pre-mRNA. Cell, 47, 555-565.
4. Dietrich, R.C., Fuller, J.D. and Padgett, R.A. (2005) A mutational analysis of U12-dependent splice site dinucleotides. RNA, 11, 1430-1440.
5. Lamond, A.I., Konarska, M.M. and Sharp, P.A. (1987) A mutational analysis of spliceosome assembly: evidence for splice site collaboration during spliceosome formation. Genes Dev., 1, 532-543.
6. Sheth, N., Roca, X., Hastings, M.L., Roeder, T., Krainer, A.R. and Sachidanandam, R. (2006) Comprehensive splice-site analysis using comparative genomics. Nucleic Acids Res., 34, 3955-3967.
7. Patel, A.A. and Steitz, J.A. (2003) Splicing double: insights from the second spliceosome. Nat. Rev. Mol. Cell Biol., 4, 960-970.
8. Twigg, S.R., Burns, H.D., Oldridge, M., Heath, J.K. and Wilkie, A.O. (1998) Conserved use of a non-canonical 5' splice site (/GA) in alternative splicing by fibroblast growth factor receptors 1, 2 and 3. Hum. Mol. Genet., 7, 685-691.
9. Brackenridge, S., Wilkie, A.O. and Screaton, G.R. (2003) Efficient use of a 'dead-end' GA 5' splice site in the human fibroblast growth factor receptor genes. EMBO J., 22, 1620-1631.
10. Quan, F. and Forte, M.A. (1990) Two forms of Drosophila melanogaster Gs alpha are produced by alternate splicing involving an unusual splice site. Mol. Cell. Biol., 10, 910-917.
11. Pollard, A.J., Krainer, A.R., Robson, S.C. and Europe-Finner, G.N. (2002) Alternative splicing of the adenylyl cyclase stimulatory G-protein G alpha(s) is regulated by SF2/ASF and heterogeneous nuclear ribonucleoprotein A1 (hnRNPA1) and involves the use of an unusual TG 3'-splice site. J. Biol. Chem., 277, 15241-15251.
12. Szafranski, K., Schindler, S., Taudien, S., Hiller, M., Huse, K., Jahn, N., Schreiber, S., Backofen, R. and Platzer, M. (2007) Violating the splicing rules: TG dinucleotides function as alternative 3' splice sites in U2-dependent introns. Genome Biol., 8, R154.
13. Burset, M., Seledtsov, I.A. and Solovyev, V.V. (2000) Analysis of canonical and non-canonical splice sites in mammalian genomes. Nucleic Acids Res., 28, 4364-4375.
14. Wang, Z., Gerstein, M. and Snyder, M. (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat. Rev. Genet., 10, 57-63.
15. Pan, Q., Shai, O., Lee, L.J., Frey, B.J. and Blencowe, B.J. (2008) Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat. Genet., 40, 1413-1415.
16. Sultan, M., Schulz, M.H., Richard, H., Magen, A., Klingenhoff, A., Scherf, M., Seifert, M., Borodina, T., Soldatov, A., Parkhomchuk, D. et al. (2008) A global view of gene activity and alternative splicing by deep sequencing of the human transcriptome. Science, 321, 956-960.
17. Wang, E.T., Sandberg, R., Luo, S., Khrebtukova, I., Zhang, L., Mayr, C., Kingsmore, S.F., Schroth, G.P. and Burge, C.B. (2008) Alternative isoform regulation in human tissue transcriptomes. Nature, 456, 470-476.
18. Djebali, S., Davis, C.A., Merkel, A., Dobin, A., Lassmann, T., Mortazavi, A., Tanzer, A., Lagarde, J., Lin, W., Schlesinger, F. et al. (2012) Landscape of transcription in human cells. Nature, 489, 101-108.
19. Rozowsky, J., Abyzov, A., Wang, J., Alves, P., Raha, D., Harmanci, A., Leng, J., Bjornson, R., Kong, Y., Kitabayashi, N. et al. (2011) AlleleSeq: analysis of allele-specific expression and binding in a network framework. Mol. Syst. Biol., 7, 522.
20. Wang, K., Singh, D., Zeng, Z., Coleman, S.J., Huang, Y., Savich, G.L., He, X., Mieczkowski, P., Grimm, S.A., Perou, C.M. et al. (2010) MapSplice: accurate mapping of RNA-seq reads for splice junction discovery. Nucleic Acids Res., 38, e178.
21. Kent, W.J. (2002) BLAT-the BLAST-like alignment tool. Genome Res., 12, 656-664.
22. Kapitonov, V.V. and Jurka, J. (2008) A universal classification of eukaryotic transposable elements implemented in Repbase. Nat. Rev. Genet., 9, 411-412.
23. Morgulis, A., Gertz, E.M., Schaffer, A.A. and Agarwala, R. (2006) A fast and symmetric DUST implementation to mask low-complexity DNA sequences. J. Comput. Biol., 13, 1028-1040.
24. Rhead, B., Karolchik, D., Kuhn, R.M., Hinrichs, A.S., Zweig, A.S., Fujita, P.A., Diekhans, M., Smith, K.E., Rosenbloom, K.R., Raney, B.J. et al. (2010) The UCSC Genome Browser database: update 2010. Nucleic Acids Res., 38, D613-D619.
25. Langmead, B., Trapnell, C., Pop, M. and Salzberg, S.L. (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol., 10, R25.
26. Fairbrother, W.G., Yeh, R.F., Sharp, P.A. and Burge, C.B. (2002) Predictive identification of exonic splicing enhancers in human genes. Science, 297, 1007-1013.
27. Wang, Z., Rolish, M.E., Yeo, G., Tung, V., Mawson, M. and Burge, C.B. (2004) Systematic identification and analysis of exonic splicing silencers. Cell, 119, 831-845.
28. Wang, Y., Ma, M., Xiao, X. and Wang, Z. (2012) Intronic splicing enhancers, cognate splicing factors and context-dependent regulation rules. Nat. Struct. Mol. Biol., 19, 1044-1052.
29. Wang, Y., Xiao, X., Zhang, J., Choudhury, R., Robertson, A., Li, K., Ma, M., Burge, C.B. and Wang, Z. (2013) A complex network of factors with overlapping affinities represses splicing through intronic elements. Nat. Struct. Mol. Biol., 20, 36-45.
30. Zhang, C., Li, W.H., Krainer, A.R. and Zhang, M.Q. (2008) RNA landscape of evolution for optimal exon and intron discrimination. Proc. Natl. Acad. Sci. U.S.A., 105, 5797-5802.
31. Korbie, D.J. and Mattick, J.S. (2008) Touchdown PCR for increased specificity and sensitivity in PCR amplification. Nat. Protoc., 3, 1452-1456.
32. Gruber, A.R., Lorenz, R., Bernhart, S.H., Neubock, R. and Hofacker, I.L. (2008) The Vienna RNA websuite. Nucleic Acids Res., 36, W70-W74.
33. Byun, Y. and Han, K. (2009) PseudoViewer3: generating planar drawings of large-scale RNA structures with pseudoknots. Bioinformatics, 25, 1435-1437.
34. Sherry, S.T., Ward, M.H., Kholodov, M., Baker, J., Phan, L., Smigielski, E.M. and Sirotkin, K. (2001) dbSNP: the NCBI database of genetic variation. Nucleic Acids Res., 29, 308-311.
35. Engstrom, P.G., Steijger, T., Sipos, B., Grant, G.R., Kahles, A., Consortium, R., Alioto, T., Behr, J., Bertone, P., Bohnert, R. et al. (2013) Systematic evaluation of spliced alignment programs for RNA-seq data. Nat. Methods, 10, 1185-1191.
36. Li, H. and Homer, N. (2010) A survey of sequence alignment algorithms for next-generation sequencing. Brief. Bioinform., 11, 473-483.
37. Ameur, A., Wetterbom, A., Feuk, L. and Gyllensten, U. (2010) Global and unbiased detection of splice junctions from RNA-seq data. Genome Biol., 11, R34.
38. The UniProt Consortium. (2013) Update on activities at the Universal Protein Resource (UniProt) in 2013. Nucleic Acids Res., 41, D43-D47.
39. Barash, Y., Calarco, J.A., Gao, W., Pan, Q., Wang, X., Shai, O., Blencowe, B.J. and Frey, B.J. (2010) Deciphering the splicing code. Nature, 465, 53-59.
40. Wang, Y. and Wang, Z. (2014) Systematical identification of splicing regulatory cis-elements and cognate trans-factors. Methods, 65, 350-358.
41. Rueter, S.M., Dawson, T.R. and Emeson, R.B. (1999) Regulation of alternative splicing by RNA editing. Nature, 399, 75-80.
42. Lev-Maor, G., Sorek, R., Levanon, E.Y., Paz, N., Eisenberg, E. and Ast, G. (2007) RNA-editing-mediated exon evolution. Genome Biol., 8, R29.
43. Athanasiadis, A., Rich, A. and Maas, S. (2004) Widespread A-to-I RNA editing of Alu-containing mRNAs in the human transcriptome. PLoS Biol., 2, e391.
44. Trapnell, C., Pachter, L. and Salzberg, S.L. (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics, 25, 1105-1111.
45. Au, K.F., Jiang, H., Lin, L., Xing, Y. and Wong, W.H. (2010) Detection of splice junctions from paired-end RNA-seq data by SpliceMap. Nucleic Acids Res., 38, 4570-4578.
46. Lou, S.K., Ni, B., Lo, L.Y., Tsui, S.K., Chan, T.F. and Leung, K.S. (2011) ABMapper: a suffix array-based tool for multi-location searching and splice-junction mapping. Bioinformatics, 27, 421-422.
47. Wu, J., Anczukow, O., Krainer, A.R., Zhang, M.Q. and Zhang, C. (2013) OLego: fast and sensitive mapping of spliced mRNA-Seq reads using small seeds. Nucleic Acids Res., 41, 5149-5163.
48. Huang, S., Zhang, J., Li, R., Zhang, W., He, Z., Lam, T.W., Peng, Z. and Yiu, S.M. (2011) SOAPsplice: Genome-Wide ab initio Detection of Splice Junctions from RNA-Seq Data. Front. Genet., 2, 46.
49. Denoeud, F., Aury, J.M., Da Silva, C., Noel, B., Rogier, O., Delledonne, M., Morgante, M., Valle, G., Wincker, P., Scarpelli, C. et al. (2008) Annotating genomes with massive-scale RNA sequencing. Genome Biol., 9, R175.
50. Trapnell, C., Roberts, A., Goff, L., Pertea, G., Kim, D., Kelley, D.R., Pimentel, H., Salzberg, S.L., Rinn, J.L. and Pachter, L. (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc., 7, 562-578.
51. Yoshida, H., Matsui, T., Yamamoto, A., Okada, T. and Mori, K. (2001) XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell, 107, 881-891.
52. Cocquet, J., Chong, A., Zhang, G. and Veitia, R.A. (2006) Reverse transcriptase template switching and false alternative transcripts. Genomics, 88, 127-131.
53. Mader, R.M., Schmidt, W.M., Sedivy, R., Rizovski, B., Braun, J., Kalipciyan, M., Exner, M., Steger, G.G. and Mueller, M.W. (2001) Reverse transcriptase template switching during reverse transcriptase-polymerase chain reaction: artificial generation of deletions in ribonucleotide reductase mRNA. J. Lab. Clin. Med., 137, 422-428.
54. Roy, S.W. and Irimia, M. (2008) When good transcripts go bad: artifactual RT-PCR 'splicing' and genome analysis. Bioessays, 30, 601-605.
55. Houseley, J. and Tollervey, D. (2010) Apparent non-canonical trans-splicing is generated by reverse transcriptase in vitro. PLoS One, 5, e12271.
56. 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.
57. Ast, G. (2004) How did alternative splicing evolve? Nat. Rev. Genet., 5, 773-782.
58. Lewis, B.P., Green, R.E. and Brenner, S.E. (2003) Evidence for the widespread coupling of alternative splicing and nonsense-mediated mRNA decay in humans. Proc. Natl. Acad. Sci. U.S.A., 100, 189-192.
59. Baek, D. and Green, P. (2005) Sequence conservation, relative isoform frequencies, and nonsense-mediated decay in evolutionarily conserved alternative splicing. Proc. Natl. Acad. Sci. U.S.A., 102, 12813-12818.
60. Saltzman, A.L., Kim, Y.K., Pan, Q., Fagnani, M.M., Maquat, L.E. and Blencowe, B.J. (2008) Regulation of multiple core spliceosomal proteins by alternative splicing-coupled nonsense-mediated mRNA decay. Mol. Cell. Biol., 28, 4320-4330.
61. Matlin, A.J., Clark, F. and Smith, C.W. (2005) Understanding alternative splicing: towards a cellular code. Nat. Rev. Mol. Cell Biol., 6, 386-398.
62. Wang, Z., Xiao, X., Van Nostrand, E. and Burge, C.B. (2006) General and specific functions of exonic splicing silencers in splicing control. Mol. Cell, 23, 61-70.
63. Yu, Y., Maroney, P.A., Denker, J.A., Zhang, X.H., Dybkov, O., Luhrmann, R., Jankowsky, E., Chasin, L.A. and Nilsen, T.W. (2008) Dynamic regulation of alternative splicing by silencers that modulate 5' splice site competition. Cell, 135, 1224-1236.
64. Roca, X., Krainer, A.R. and Eperon, I.C. (2013) Pick one, but be quick: 5' splice sites and the problems of too many choices. Genes Dev., 27, 129-144.
65. D'Souza-Li, L., Canaff, L., Janicic, N., Cole, D.E. and Hendy, G.N. (2001) An acceptor splice site mutation in the calcium-sensing receptor (CASR) gene in familial hypocalciuric hypercalcemia and neonatal severe hyperparathyroidism. Hum. Mutat., 18, 411-421.
66. Lee, H.H. and Chang, S.F. (2001) Multiple transcripts of the CYP21 gene are generated by the mutation of the splicing donor site in intron 2 from GT to AT in 21-hydroxylase deficiency. J. Endocrinol., 171, 397-402.
67. D'Andrea, G., Di Perna, P., Brancaccio, V., Faioni, E.M., Castaman, G., Cibelli, G., Di Minno, G. and Margaglione, M. (2003) A novel G-to-A mutation in the intron-N of the protein S gene leading to abnormal RNA splicing in a patient with protein S deficiency. Haematologica, 88, 459-464.
68. Scheckenbach, K., Balz, V., Wagenmann, M. and Hoffmann, T.K. (2008) An intronic alteration of the fibroblast growth factor 10 gene causing ALSG-(aplasia of lacrimal and salivary glands) syndrome. BMC Med. Genet., 9, 114.
69. Baralle, D. and Baralle, M. (2005) Splicing in action: assessing disease causing sequence changes. J. Med. Genet., 42, 737-748.
70. Frilander, M.J. and Steitz, J.A. (1999) Initial recognition of U12-dependent introns requires both U11/5' splice-site and U12/branchpoint interactions. Genes Dev., 13, 851-863.
71. Harrow, J., Denoeud, F., Frankish, A., Reymond, A., Chen, C.K., Chrast, J., Lagarde, J., Gilbert, J.G., Storey, R., Swarbreck, D. et al. (2006) GENCODE: producing a reference annotation for ENCODE. Genome Biol., 7(Suppl. 1), S4.
72. Sorek, R. and Safer, H.M. (2003) A novel algorithm for computational identification of contaminated EST libraries. Nucleic Acids Res., 31, 1067-1074.
73. Bonizzoni, P., Rizzi, R. and Pesole, G. (2005) ASPIC: a novel method to predict the exon-intron structure of a gene that is optimally compatible to a set of transcript sequences. BMC Bioinformatics, 6, 244.
74. Minoche, A.E., Dohm, J.C. and Himmelbauer, H. (2011) Evaluation of genomic high-throughput sequencing data generated on Illumina HiSeq and genome analyzer systems. Genome Biol., 12, R112.