Intergenic Alu exonisation facilitates the evolution of tissue-specific transcript ends

Nucleic Acids Research

Volumn 43, Issue 21, 2015, Pages 10492-10505

  Tajnik, Mojca ^a,b   Vigilante, Alessandra ^c,d   Braun, Simon ^e   Hänel, Heike ^e   Luscombe, Nicholas M ^c,d,f   Ule, Jernej ^a,g   Zarnack, Kathi ^d,h   König, Julian ^a,e,g  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^e Institute of Molecular Biology gGmbH (IMB)   (Germany)

^f OKINAWA INSTITUTE OF SCIENCE AND TECHNOLOGY GRADUATE UNIVERSITY   (Japan)

^g UNIVERSITY COLLEGE LONDON   (United Kingdom)

^h Buchmann Institute for Molecular Life Sciences   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; 3' UNTRANSLATED REGION; DNA; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN GROUP C; ISOPROTEIN; NUCLEAR PROTEIN; RIBONUCLEOPROTEIN; RNA; SPACER DNA; SPLICING FACTOR U2AF; U2AF2 PROTEIN, HUMAN;

3' UNTRANSLATED REGION; ARTICLE; CONTROLLED STUDY; DNA METABOLISM; EXON; EXONISATION; GENE REPRESSION; GENOME ANALYSIS; INTRON; MOLECULAR GENETICS; POLYADENYLATION; PRIORITY JOURNAL; RNA METABOLISM; RNA STABILITY; TISSUE SPECIFICITY; TRANSCRIPTION REGULATION; ALU SEQUENCE; ANTIBODY SPECIFICITY; CELL LINE; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MOLECULAR EVOLUTION; RNA SPLICING;

3' UNTRANSLATED REGIONS; ALU ELEMENTS; CELL LINE; DNA; DNA, INTERGENIC; EVOLUTION, MOLECULAR; EXONS; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN GROUP C; HUMANS; INTRONS; NUCLEAR PROTEINS; ORGAN SPECIFICITY; POLYADENYLATION; PROTEIN ISOFORMS; RIBONUCLEOPROTEINS; RNA; RNA SPLICING; SPLICING FACTOR U2AF;

EID: 84975074328     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv956     Document Type: Article

References (42)

1. Elkon, R., Ugalde, A.P. and Agami, R. (2013) Alternative cleavage and polyadenylation: extent, regulation and function. Nat. Rev. Genet., 14, 496-506.
2. Batzer, M.A. and Deininger, P.L. (2002) Alu repeats and human genomic diversity. Nat. Rev. Genet., 3, 370-379.
3. Keren, H., Lev-Maor, G. and Ast, G. (2010) Alternative splicing and evolution: diversification, exon definition and function. Nat. Rev. Genet., 11, 345-355.
4. Deininger, P. (2011) Alu elements: know the SINEs. Genome Biol., 12, 236.
5. Vorechovsky, I. (2010) Transposable elements in disease-associated cryptic exons. Hum. Genet., 127, 135-154.
6. Sorek, R., Ast, G. and Graur, D. (2002) Alu-containing exons are alternatively spliced. Genome Res., 12, 1060-1067.
7. Zarnack, K., König, J., Tajnik, M., Martincorena, I., Eustermann, S., Stevant, I., Reyes, A., Anders, S., Luscombe, N.M. and Ule, J. (2013) Direct competition between hnRNP C and U2AF65 protects the transcriptome from the exonization of Alu elements. Cell, 152, 453-466.
8. König, J., Zarnack, K., Rot, G., Curk, T., Kayikci, M., Zupan, B., Turner, D.J., Luscombe, N.M. and Ule, J. (2010) iCLIP reveals the function of hnRNP particles in splicing at individual nucleotide resolution. Nat. Struct. Mol. Biol., 17, 909-915.
9. Trapnell, C., Pachter, L. and Salzberg, S.L. (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics, 25, 1105-1111.
10. Trapnell, C., Williams, B.A., Pertea, G., Mortazavi, A., Kwan, G., van Baren, M.J., Salzberg, S.L., Wold, B.J. and Pachter, L. (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol., 28, 511-515.
11. Huang da, W., Sherman, B.T. and Lempicki, R.A. (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc., 4, 44-57.
12. Supek, F., Bosnjak, M., Skunca, N. and Smuc, T. (2011) REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS One, 6, e21800.
13. Smoot, M.E., Ono, K., Ruscheinski, J., Wang, P.L. and Ideker, T. (2011) Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics, 27, 431-432.
14. Scotto-Lavino, E., Du, G. and Frohman, M.A. (2006) 3′ end cDNA amplification using classic RACE. Nat. Protoc., 1, 2742-2745.
15. Vilella, A.J., Severin, J., Ureta-Vidal, A., Heng, L., Durbin, R. and Birney, E. (2009) EnsemblCompara GeneTrees: Complete, duplication-aware phylogenetic trees in vertebrates. Genome Res., 19, 327-335.
16. 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.
17. Bianchi, V., Colantoni, A., Calderone, A., Ausiello, G., Ferre, F. and Helmer-Citterich, M. (2013) DBATE: database of alternative transcripts expression. Database (Oxford), 2013, bat050.
18. 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.
19. Lian, Z., Karpikov, A., Lian, J., Mahajan, M.C., Hartman, S., Gerstein, M., Snyder, M. and Weissman, S.M. (2008) A genomic analysis of RNA polymerase II modification and chromatin architecture related to 3′ end RNA polyadenylation. Genome Res., 18, 1224-1237.
20. Huang, M., Rech, J.E., Northington, S.J., Flicker, P.F., Mayeda, A., Krainer, A.R. and LeStourgeon, W.M. (1994) The C-protein tetramer binds 230 to 240 nucleotides of pre-mRNA and nucleates the assembly of 40S heterogeneous nuclear ribonucleoprotein particles. Mol. Cell Biol., 14, 518-533.
21. Bentley, D.L. (2014) Coupling mRNA processing with transcription in time and space. Nat. Rev. Genet., 15, 163-175.
22. Lowe, C.B., Bejerano, G. and Haussler, D. (2007) Thousands of human mobile element fragments undergo strong purifying selection near developmental genes. Proc. Natl. Acad. Sci. U S A, 104, 8005-8010.
23. Lee, J.Y., Ji, Z. and Tian, B. (2008) Phylogenetic analysis of mRNA polyadenylation sites reveals a role of transposable elements in evolution of the 3′-end of genes. Nucleic Acids Res., 36, 5581-5590.
24. Chen, C., Ara, T. and Gautheret, D. (2009) Using Alu elements as polyadenylation sites: A case of retroposon exaptation. Mol. Biol. Evol., 26, 327-334.
25. Kaer, K. and Speek, M. (2012) Intronic retroelements: Not just 'speed bumps' for RNA polymerase II. Mob. Genet. Elements, 2, 154-157.
26. Buratti, E., Stuani, C., De Prato, G. and Baralle, F.E. (2007) SR protein-mediated inhibition of CFTR exon 9 inclusion: molecular characterization of the intronic splicing silencer. Nucleic Acids Res., 35, 4359-4368.
27. Havlioglu, N., Wang, J., Fushimi, K., Vibranovski, M.D., Kan, Z., Gish, W., Fedorov, A., Long, M. and Wu, J.Y. (2007) An intronic signal for alternative splicing in the human genome. PLoS One, 2, e1246.
28. Lev-Maor, G., Ram, O., Kim, E., Sela, N., Goren, A., Levanon, E.Y. and Ast, G. (2008) Intronic Alus influence alternative splicing. PLoS Genet., 4, e1000204.
29. Gal-Mark, N., Schwartz, S. and Ast, G. (2008) Alternative splicing of Alu exons-two arms are better than one. Nucleic Acids Res., 36, 2012-2023.
30. Millevoi, S., Decorsiere, A., Loulergue, C., Iacovoni, J., Bernat, S., Antoniou, M. and Vagner, S. (2009) A physical and functional link between splicing factors promotes pre-mRNA 3′ end processing. Nucleic Acids Res., 37, 4672-4683.
31. Tikhonov, M., Georgiev, P. and Maksimenko, O. (2013) Competition within Introns: Splicing Wins over Polyadenylation via a General Mechanism. Acta Naturae, 5, 52-61.
32. Berg, M.G., Singh, L.N., Younis, I., Liu, Q., Pinto, A.M., Kaida, D., Zhang, Z., Cho, S., Sherrill-Mix, S., Wan, L. et al. (2012) U1 snRNP determines mRNA length and regulates isoform expression. Cell, 150, 53-64.
33. Kaida, D., Berg, M.G., Younis, I., Kasim, M., Singh, L.N., Wan, L. and Dreyfuss, G. (2010) U1 snRNP protects pre-mRNAs from premature cleavage and polyadenylation. Nature, 468, 664-668.
34. Barrett, L.W., Fletcher, S. and Wilton, S.D. (2012) Regulation of eukaryotic gene expression by the untranslated gene regions and other non-coding elements. Cell Mol. Life Sci., 69, 3613-3634.
35. Lianoglou, S., Garg, V., Yang, J.L., Leslie, C.S. and Mayr, C. (2013) Ubiquitously transcribed genes use alternative polyadenylation to achieve tissue-specific expression. Genes Dev., 27, 2380-2396.
36. Pesole, G., Mignone, F., Gissi, C., Grillo, G., Licciulli, F. and Liuni, S. (2001) Structural and functional features of eukaryotic mRNA untranslated regions. Gene, 276, 73-81.
37. Chatterjee, S. and Pal, J.K. (2009) Role of 5'- and 3′-untranslated regions of mRNAs in human diseases. Biol. Cell, 101, 251-262.
38. An, H.J., Lee, D., Lee, K.H. and Bhak, J. (2004) The association of Alu repeats with the generation of potential AU-rich elements (ARE) at 3′ untranslated regions. BMC Genomics, 5, 97.
39. Hoffman, Y., Dahary, D., Bublik, D.R., Oren, M. and Pilpel, Y. (2013) The majority of endogenous microRNA targets within Alu elements avoid the microRNA machinery. Bioinformatics, 29, 894-902.
40. Kelley, D.R., Hendrickson, D.G., Tenen, D. and Rinn, J.L. (2014) Transposable elements modulate human RNA abundance and splicing via specific RNA-protein interactions. Genome Biol., 15, 537.
41. Ray, D., Kazan, H., Cook, K.B., Weirauch, M.T., Najafabadi, H.S., Li, X., Gueroussov, S., Albu, M., Zheng, H., Yang, A. et al. (2013) A compendium of RNA-binding motifs for decoding gene regulation. Nature, 499, 172-177.
42. John, B., Enright, A.J., Aravin, A., Tuschl, T., Sander, C. and Marks, D.S. (2004) Human MicroRNA targets. PLoS Biol., 2, e363.