CLIP-seq of eIF4AIII reveals transcriptome-wide mapping of the human exon junction complex

Nature Structural and Molecular Biology

Volumn 19, Issue 11, 2012, Pages 1124-1131

  Saulière, Jérôme ^a,b,c   Murigneux, Valentine ^a,b,c   Wang, Zhen ^a,b,c   Marquenet, Emélie ^a,b,c   Barbosa, Isabelle ^a,b,c   Le Tonquèze, Olivier ^d,e   Audic, Yann ^d   Paillard, Luc ^d   Crollius, Hugues Roest ^a,b,c   Le Hir, Hervé ^a,b,c  

^a ECOLE NORMALE SUPÉRIEURE   (France)

^b CNRS   (France)

^c INSERM   (France)

^d UNIVERSITÉ DE RENNES 1   (France)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEAD BOX PROTEIN; EIF4AIII PROTEIN; MESSENGER RNA; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CELL JUNCTION; COUPLED TO HIGH THROUGHPUT SEQUENCING; CROSS LINKING; EXON JUNCTION COMPLEX; GENE EXPRESSION; GENE EXPRESSION REGULATION; HELA CELL; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PROCESSING; PROTEIN TARGETING; RNA SPLICING;

BINDING SITES; CHROMOSOME MAPPING; EUKARYOTIC INITIATION FACTOR-4A; EXONS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; IMMUNOPRECIPITATION; MULTIPROTEIN COMPLEXES; RNA, MESSENGER; TRANSCRIPTOME;

EID: 84869087484     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2420     Document Type: Article

References (53)

1. Moore, M.J. & Proudfoot, N.J. Pre-mRNA processing reaches back to transcription and ahead to translation. Cell 136, 688-700 (2009).
2. Le Hir, H., Izaurralde, E., Maquat, L.E. & Moore, M.J. The spliceosome deposits multiple proteins 20-24 nucleotides upstream of mRNA exon-exon junctions. EMBO J. 19, 6860-6869 (2000). (Pubitemid 32011679)
3. Tange, T.Ø., Nott, A. & Moore, M.J. The ever-increasing complexities of the exon junction complex. Curr. Opin. Cell Biol. 16, 279-284 (2004). (Pubitemid 38610408)
4. Le Hir, H. & Andersen, G.R. Structural insights into the exon junction complex. Curr. Opin. Struct. Biol. 18, 112-119 (2008).
5. Andersen, C.B. et al. Structure of the exon junction core complex with a trapped DEAD-box ATPase bound to RNA. Science 313, 1968-1972 (2006). (Pubitemid 44498005)
6. Ballut, L. et al. The exon junction core complex is locked onto RNA by inhibition of eIF4AIII ATPase activity. Nat. Struct. Mol. Biol. 12, 861-869 (2005). (Pubitemid 41486709)
7. Bono, F., Ebert, J., Lorentzen, E. & Conti, E. The crystal structure of the exon junction complex reveals how it maintains a stable grip on mRNA. Cell 126, 713-725 (2006). (Pubitemid 44233638)
8. Nielsen, K.H. et al. Mechanism of ATP turnover inhibition in the EJC. RNA 15, 67-75 (2009).
9. Gehring, N.H., Lamprinaki, S., Hentze, M.W. & Kulozik, A.E. The hierarchy of exon-junction complex assembly by the spliceosome explains key features of mammalian nonsense-mediated mRNA decay. PLoS Biol. 7, e1000120 (2009).
10. Merz, C., Urlaub, H., Will, C.L. & Luhrmann, R. Protein composition of human mRNPs spliced in vitro and differential requirements for mRNP protein recruitment. RNA 13, 116-128 (2007). (Pubitemid 46026186)
11. Reichert, V.L., Le Hir, H., Jurica, M.S. & Moore, M.J. 5′ exon interactions within the human spliceosome establish a framework for exon junction complex structure and assembly. Genes Dev. 16, 2778-2791 (2002). (Pubitemid 35253146)
12. Zhang, Z. & Krainer, A.R. Splicing remodels messenger ribonucleoprotein architecture via eIF4A3-dependent and-independent recruitment of exon junction complex components. Proc. Natl. Acad. Sci. USA 104, 11574-11579 (2007). (Pubitemid 47175054)
13. Barbosa, I. et al. Human CWC22 escorts the helicase eIF4AIII to spliceosomes and promotes exon junction complex assembly. Nat. Struct. Mol. Biol. 19, 983-990 (2012).
14. Gehring, N.H., Lamprinaki, S., Kulozik, A.E. & Hentze, M.W. Disassembly of exon junction complexes by PYM. Cell 137, 536-548 (2009).
15. Hwang, J. & Maquat, L.E. Nonsense-mediated mRNA decay (NMD) in animal embryogenesis: to die or not to die, that is the question. Curr. Opin. Genet. Dev. 21, 422-430 (2011).
16. Rebbapragada, I. & Lykke-Andersen, J. Execution of nonsense-mediated mRNA decay: what defines a substrate? Curr. Opin. Cell Biol. 21, 394-402 (2009).
17. Isken, O. & Maquat, L.E. The multiple lives of NMD factors: balancing roles in gene and genome regulation. Nat. Rev. Genet. 9, 699-712 (2008).
18. Saulière, J. et al. The exon junction complex differentially marks spliced junctions. Nat. Struct. Mol. Biol. 17, 1269-1271 (2010).
19. Ashton-Beaucage, D. et al. The exon junction complex controls the splicing of MAPK and other long intron-containing transcripts in Drosophila. Cell 143, 251-262 (2010).
20. Michelle, L. et al. Proteins associated with the exon junction complex also control the alternative splicing of apoptotic regulators. Mol. Cell. Biol. 32, 954-967 (2012).
21. Roignant, J.Y. & Treisman, J.E. Exon junction complex subunits are required to splice Drosophila MAP kinase, a large heterochromatic gene. Cell 143, 238-250 (2010).
22. Hachet, O. & Ephrussi, A. Splicing of oskar RNA in the nucleus is coupled to its cytoplasmic localization. Nature 428, 959-963 (2004). (Pubitemid 38560311)
23. Haremaki, T., Sridharan, J., Dvora, S. & Weinstein, D.C. Regulation of vertebrate embryogenesis by the exon junction complex core component Eif4a3. Dev. Dyn. 239, 1977-1987 (2010).
24. Silver, D.L. et al. The exon junction complex component Magoh controls brain size by regulating neural stem cell division. Nat. Neurosci. 13, 551-558 (2010).
25. Albers, C.A. et al. Compound inheritance of a low-frequency regulatory SNP and a rare null mutation in exon-junction complex subunit RBM8A causes TAR syndrome. Nat. Genet. 44, 435-439 (2012).
26. Darnell, R.B. HITS-CLIP: panoramic views of protein-RNA regulation in living cells. Wiley Interdiscip Rev. RNA 1, 266-286 (2010).
27. Ule, J., Jensen, K., Mele, A. & Darnell, R.B. CLIP: a method for identifying protein-RNA interaction sites in living cells. Methods 37, 376-386 (2005). (Pubitemid 41682508)
28. Ule, J. et al. CLIP identifies Nova-regulated RNA networks in the brain. Science 302, 1212-1215 (2003). (Pubitemid 37421026)
29. Kent, W.J. BLAT-the BLAST-like alignment tool. Genome Res. 12, 656-664 (2002).
30. Zhang, C. & Darnell, R.B. Mapping in vivo protein-RNA interactions at single-nucleotide resolution from HITS-CLIP data. Nat. Biotechnol. 29, 607-614 (2011).
31. Fejes, A.P. et al. FindPeaks 3.1: a tool for identifying areas of enrichment from massively parallel short-read sequencing technology. Bioinformatics 24, 1729-1730 (2008).
32. Patel, A.A. & Steitz, J.A. Splicing double: insights from the second spliceosome. Nat. Rev. Mol. Cell Biol. 4, 960-970 (2003). (Pubitemid 37493644)
33. Hirose, T., Shu, M.D. & Steitz, J.A. Splicing of U12-type introns deposits an exon junction complex competent to induce nonsense-mediated mRNA decay. Proc. Natl. Acad. Sci. USA 101, 17976-17981 (2004). (Pubitemid 40054060)
34. Dostie, J. & Dreyfuss, G. Translation is required to remove Y14 from mRNAs in the cytoplasm. Curr. Biol. 12, 1060-1067 (2002). (Pubitemid 34766927)
35. Lejeune, F., Ishigaki, Y., Li, X. & Maquat, L.E. The exon junction complex is detected on CBP80-bound but not eIF4E-bound mRNA in mammalian cells: dynamics of mRNP remodeling. EMBO J. 21, 3536-3545 (2002). (Pubitemid 34760583)
36. Dennis, G. Jr. et al. DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol. 4, 3 (2003).
37. Huang, W., Sherman, B.T. & Lempicki, R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57 (2009).
38. Sanford, J.R. et al. Splicing factor SFRS1 recognizes a functionally diverse landscape of RNA transcripts. Genome Res. 19, 381-394 (2009).
39. Bailey, T.L., Boden, M., Whitington, T. & Machanick, P. The value of position-specific priors in motif discovery using MEME. BMC Bioinformatics 11, 179 (2010).
40. Long, J.C. & Caceres, J.F. The SR protein family of splicing factors: master regulators of gene expression. Biochem. J. 417, 15-27 (2009).
41. Markham, N.R. & Zuker, M. DINAMelt web server for nucleic acid melting prediction. Nucleic Acids Res. 33, W577-W581 (2005). (Pubitemid 44529988)
42. Markham, N.R. & Zuker, M. UNAFold: software for nucleic acid folding and hybridization. Methods Mol. Biol. 453, 3-31 (2008).
43. Mishler, D.M., Christ, A.B. & Steitz, J.A. Flexibility in the site of exon junction complex deposition revealed by functional group and RNA secondary structure alterations in the splicing substrate. RNA 14, 2657-2670 (2008).
44. Budiman, M.E. et al. Eukaryotic initiation factor 4a3 is a selenium-regulated RNA-binding protein that selectively inhibits selenocysteine incorporation. Mol. Cell 35, 479-489 (2009).
45. Le Hir, H. & Seraphin, B. EJCs at the heart of translational control. Cell 133, 213-216 (2008). (Pubitemid 351508309)
46. Nagy, E. & Maquat, L.E. A rule for termination-codon position within intron-containing genes: when nonsense affects RNA abundance. Trends Biochem. Sci. 23, 198-199 (1998). (Pubitemid 28302613)
47. Bühler, M., Paillusson, A. & Muhlemann, O. Efficient downregulation of immunoglobulin mu mRNA with premature translation-termination codons requires the 5′-half of the VDJ exon. Nucleic Acids Res. 32, 3304-3315 (2004). (Pubitemid 39117447)
48. Carter, M.S., Li, S. & Wilkinson, M.F. A splicing-dependent regulatory mechanism that detects translation signals. EMBO J. 15, 5965-5975 (1996). (Pubitemid 26375518)
49. Holbrook, J.A., Neu-Yilik, G., Hentze, M.W. & Kulozik, A.E. Nonsense-mediated decay approaches the clinic. Nat. Genet. 36, 801-808 (2004). (Pubitemid 39014096)
50. Viegas, M.H., Gehring, N.H., Breit, S., Hentze, M.W. & Kulozik, A.E. The abundance of RNPS1, a protein component of the exon junction complex, can determine the variability in efficiency of the nonsense mediated decay pathway. Nucleic Acids Res. 35, 4542-4551 (2007). (Pubitemid 47244605)
51. Zetoune, A.B. et al. Comparison of nonsense-mediated mRNA decay efficiency in various murine tissues. BMC Genet. 9, 83 (2008).
52. Zhang, Z. & Krainer, A.R. Involvement of SR proteins in mRNA surveillance. Mol. Cell 16, 597-607 (2004). (Pubitemid 39531882)
53. Daguenet, E. et al. Perispeckles are major assembly sites for the exon junction core complex. Mol. Biol. Cell 23, 1765-1782 (2012).