Regulation of constitutive and alternative mRNA splicing across the human transcriptome by PRPF8 is determined by 5' splice site strength

Genome Biology

Volumn 16, Issue 1, 2015, Pages

  Wickramasinghe, Vihandha O ^a   Gonzàlez Porta, Mar ^b   Perera, David ^a   Bartolozzi, Arthur R ^a   Sibley, Christopher R ^c   Hallegger, Martina ^c   Ule, Jernej ^c   Marioni, John C ^b   Venkitaraman, Ashok R ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b EUROPEAN BIOINFORMATICS INSTITUTE   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; PRPF8 PROTEIN, HUMAN; RIBONUCLEOPROTEIN; RNA BINDING PROTEIN; RNA SPLICING; TRANSCRIPTOME;

ALTERNATIVE RNA SPLICING; EXON; GENETICS; GENOME; HUMAN; INTRON; MUTATION; PATHOLOGY; RETINITIS PIGMENTOSA; RNA SPLICING; SPLICEOSOME;

ALTERNATIVE SPLICING; EXONS; GENOME; HUMANS; INTRONS; MUTATION; RETINITIS PIGMENTOSA; RIBONUCLEOPROTEINS; RNA SPLICE SITES; RNA, MESSENGER; RNA-BINDING PROTEINS; SPLICEOSOMES; TRANSCRIPTOME;

EID: 84955642673     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/s13059-015-0749-3     Document Type: Article

References (72)

1. Kornblihtt AR, Schor IE, Allo M, Dujardin G, Petrillo E, Munoz MJ. Alternative splicing: a pivotal step between eukaryotic transcription and translation. Nat Rev Mol Cell Biol. 2013;14:153-65.
2. Nilsen TW, Graveley BR. Expansion of the eukaryotic proteome by alternative splicing. Nature. 2010;463:457-63.
3. Matera AG, Wang Z. A day in the life of the spliceosome. Nat Rev Mol Cell Biol. 2014;15:108-21.
4. Wahl MC, Will CL, Luhrmann R. The spliceosome: design principles of a dynamic RNP machine. Cell. 2009;136:701-18.
5. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, et al. Initial sequencing and analysis of the human genome. Nature. 2001;409:860-921.
6. Braunschweig U, Gueroussov S, Plocik AM, Graveley BR, Blencowe BJ. Dynamic integration of splicing within gene regulatory pathways. Cell. 2013;152:1252-69.
7. Pleiss JA, Whitworth GB, Bergkessel M, Guthrie C. Transcript specificity in yeast pre-mRNA splicing revealed by mutations in core spliceosomal components. PLoS Biol. 2007;5, e90.
8. Clark TA, Sugnet CW, Ares Jr M. Genomewide analysis of mRNA processing in yeast using splicing-specific microarrays. Science. 2002;296:907-10.
9. Saltzman AL, Pan Q, Blencowe BJ. Regulation of alternative splicing by the core spliceosomal machinery. Genes Dev. 2011;25:373-84.
10. Park JW, Parisky K, Celotto AM, Reenan RA, Graveley BR. Identification of alternative splicing regulators by RNA interference in Drosophila. Proc Natl Acad Sci U S A. 2004;101:15974-9.
11. Grainger RJ, Beggs JD. Prp8 protein: at the heart of the spliceosome. RNA. 2005;11:533-57.
12. Schellenberg MJ, Wu T, Ritchie DB, Fica S, Staley JP, Atta KA, et al. A conformational switch in PRP8 mediates metal ion coordination that promotes pre-mRNA exon ligation. Nat Struct Mol Biol. 2013;20:728-34.
13. Reyes JL, Gustafson EH, Luo HR, Moore MJ, Konarska MM. The C-terminal region of hPrp8 interacts with the conserved GU dinucleotide at the 5' splice site. RNA. 1999;5:167-79.
14. Collins CA, Guthrie C. Allele-specific genetic interactions between Prp8 and RNA active site residues suggest a function for Prp8 at the catalytic core of the spliceosome. Genes Dev. 1999;13:1970-82.
15. Chiara MD, Gozani O, Bennett M, Champion-Arnaud P, Palandjian L, Reed R. Identification of proteins that interact with exon sequences, splice sites, and the branchpoint sequence during each stage of spliceosome assembly. Mol Cell Biol. 1996;16:3317-26.
16. Umen JG, Guthrie C. A novel role for a U5 snRNP protein in 3' splice site selection. Genes Dev. 1995;9:855-68.
17. Teigelkamp S, Newman AJ, Beggs JD. Extensive interactions of PRP8 protein with the 5' and 3' splice sites during splicing suggest a role in stabilization of exon alignment by U5 snRNA. EMBO J. 1995;14:2602-12.
18. MacMillan AM, Query CC, Allerson CR, Chen S, Verdine GL, Sharp PA. Dynamic association of proteins with the pre-mRNA branch region. Genes Dev. 1994;8:3008-20.
19. Li X, Zhang W, Xu T, Ramsey J, Zhang L, Hill R, et al. Comprehensive in vivo RNA-binding site analyses reveal a role of Prp8 in spliceosomal assembly. Nucleic Acids Res. 2013;41:3805-18.
20. Galej WP, Oubridge C, Newman AJ, Nagai K. Crystal structure of Prp8 reveals active site cavity of the spliceosome. Nature. 2013;493:638-43.
21. McKie AB, McHale JC, Keen TJ, Tarttelin EE, Goliath R, van Lith-Verhoeven JJ, et al. Mutations in the pre-mRNA splicing factor gene PRPC8 in autosomal dominant retinitis pigmentosa (RP13). Hum Mol Genet. 2001;10:1555-62.
22. Li N, Mei H, MacDonald IM, Jiao X, Hejtmancik JF. Mutations in ASCC3L1 on 2q11.2 are associated with autosomal dominant retinitis pigmentosa in a Chinese family. Invest Ophthal Visual Sci. 2010;51:1036-43.
23. Zhao C, Bellur DL, Lu S, Zhao F, Grassi MA, Bowne SJ, et al. Autosomal-dominant retinitis pigmentosa caused by a mutation in SNRNP200, a gene required for unwinding of U4/U6 snRNAs. Am J Hum Genet. 2009;85:617-27.
24. Tanackovic G, Ransijn A, Thibault P, Abou Elela S, Klinck R, Berson EL, et al. PRPF mutations are associated with generalized defects in spliceosome formation and pre-mRNA splicing in patients with retinitis pigmentosa. Hum Mol Genet. 2011;20:2116-30.
25. Pena V, Liu S, Bujnicki JM, Luhrmann R, Wahl MC. Structure of a multipartite protein-protein interaction domain in splicing factor prp8 and its link to retinitis pigmentosa. Mol Cell. 2007;25:615-24.
26. Mozaffari-Jovin S, Wandersleben T, Santos KF, Will CL, Luhrmann R, Wahl MC. Inhibition of RNA helicase Brr2 by the C-terminal tail of the spliceosomal protein Prp8. Science. 2013;341:80-4.
27. Konig J, Zarnack K, Rot G, Curk T, Kayikci M, Zupan B, et al. iCLIP reveals the function of hnRNP particles in splicing at individual nucleotide resolution. Nat Struct Mol Biol. 2010;17:909-15.
28. Kambach C, Walke S, Young R, Avis JM, de la Fortelle E, Raker VA, et al. Crystal structures of two Sm protein complexes and their implications for the assembly of the spliceosomal snRNPs. Cell. 1999;96:375-87.
29. Dix I, Russell CS, O'Keefe RT, Newman AJ, Beggs JD. Protein-RNA interactions in the U5 snRNP of Saccharomyces cerevisiae. RNA. 1998;4:1675-86.
30. Garnett MJ, Mansfeld J, Godwin C, Matsusaka T, Wu J, Russell P, et al. UBE2S elongates ubiquitin chains on APC/C substrates to promote mitotic exit. Nat Cell Biol. 2009;11:1363-9.
31. Neumann B, Walter T, Heriche JK, Bulkescher J, Erfle H, Conrad C, et al. Phenotypic profiling of the human genome by time-lapse microscopy reveals cell division genes. Nature. 2010;464:721-7.
32. Achsel T, Ahrens K, Brahms H, Teigelkamp S, Luhrmann R. The human U5-220kD protein (hPrp8) forms a stable RNA-free complex with several U5-specific proteins, including an RNA unwindase, a homologue of ribosomal elongation factor EF-2, and a novel WD-40 protein. Mol Cell Biol. 1998;18:6756-66.
33. Yeo G, Burge CB. Maximum entropy modeling of short sequence motifs with applications to RNA splicing signals. J Comput Biol. 2004;11:377-94.
34. Amit M, Donyo M, Hollander D, Goren A, Kim E, Gelfman S, et al. Differential GC content between exons and introns establishes distinct strategies of splice-site recognition. Cell Rep. 2012;1:543-56.
35. Shepard PJ, Choi EA, Busch A, Hertel KJ. Efficient internal exon recognition depends on near equal contributions from the 3' and 5' splice sites. Nucleic Acids Res. 2011;39:8928-37.
36. Romano M, Marcucci R, Baralle FE. Splicing of constitutive upstream introns is essential for the recognition of intra-exonic suboptimal splice sites in the thrombopoietin gene. Nucleic Acids Res. 2001;29:886-94.
37. Singh J, Padgett RA. Rates of in situ transcription and splicing in large human genes. Nat Struct Mol Biol. 2009;16:1128-33.
38. Brugiolo M, Herzel L, Neugebauer KM. Counting on co-transcriptional splicing. F1000Prime Rep. 2013;5:9.
39. Schmidt U, Basyuk E, Robert MC, Yoshida M, Villemin JP, Auboeuf D, et al. Real-time imaging of cotranscriptional splicing reveals a kinetic model that reduces noise: implications for alternative splicing regulation. J Cell Biol. 2011;193:819-29.
40. Ameur A, Zaghlool A, Halvardson J, Wetterbom A, Gyllensten U, Cavelier L, et al. Total RNA sequencing reveals nascent transcription and widespread co-transcriptional splicing in the human brain. Nat Struct Mol Biol. 2011;18:1435-40.
41. Girard C, Will CL, Peng J, Makarov EM, Kastner B, Lemm I, et al. Post-transcriptional spliceosomes are retained in nuclear speckles until splicing completion. Nat Commun. 2012;3:994.
42. Carrillo Oesterreich F, Preibisch S, Neugebauer KM. Global analysis of nascent RNA reveals transcriptional pausing in terminal exons. Mol Cell. 2010;40:571-81.
43. Tilgner H, Knowles DG, Johnson R, Davis CA, Chakrabortty S, Djebali S, et al. Deep sequencing of subcellular RNA fractions shows splicing to be predominantly co-transcriptional in the human genome but inefficient for lncRNAs. Genome Res. 2012;22:1616-25.
44. Price DH. P-TEFb, a cyclin-dependent kinase controlling elongation by RNA polymerase II. Mol Cell Biol. 2000;20:2629-34.
45. Sakabe NJ, de Souza SJ. Sequence features responsible for intron retention in human. BMC Genomics. 2007;8:59.
46. Fu XD, Ares Jr M. Context-dependent control of alternative splicing by RNA-binding proteins. Nat Rev Genet. 2014;15:689-701.
47. Will CL, Rumpler S, Klein Gunnewiek J, van Venrooij WJ, Luhrmann R. In vitro reconstitution of mammalian U1 snRNPs active in splicing: the U1-C protein enhances the formation of early (E) spliceosomal complexes. Nucleic Acids Res. 1996;24:4614-23.
48. Bentley DL. Coupling mRNA processing with transcription in time and space. Nat Rev Genet. 2014;15:163-75.
49. Yu Y, Maroney PA, Denker JA, Zhang XH, Dybkov O, Luhrmann R, et al. Dynamic regulation of alternative splicing by silencers that modulate 5' splice site competition. Cell. 2008;135:1224-36.
50. Konarska MM, Vilardell J, Query CC. Repositioning of the reaction intermediate within the catalytic center of the spliceosome. Mol Cell. 2006;21:543-53.
51. Query CC, Konarska MM. Suppression of multiple substrate mutations by spliceosomal prp8 alleles suggests functional correlations with ribosomal ambiguity mutants. Mol Cell. 2004;14:343-54.
52. Smith DJ, Query CC, Konarska MM. "Nought may endure but mutability": spliceosome dynamics and the regulation of splicing. Mol Cell. 2008;30:657-66.
53. Papasaikas P, Tejedor JR, Vigevani L, Valcarcel J. Functional splicing network reveals extensive regulatory potential of the core spliceosomal machinery. Mol Cell. 2015;57:7-22.
54. Small EC, Leggett SR, Winans AA, Staley JP. The EF-G-like GTPase Snu114p regulates spliceosome dynamics mediated by Brr2p, a DExD/H box ATPase. Mol Cell. 2006;23:389-99.
55. Grosso AR, Gomes AQ, Barbosa-Morais NL, Caldeira S, Thorne NP, Grech G, et al. Tissue-specific splicing factor gene expression signatures. Nucleic Acids Res. 2008;36:4823-32.
56. Wan J, Masuda T, Hackler Jr L, Torres KM, Merbs SL, Zack DJ, et al. Dynamic usage of alternative splicing exons during mouse retina development. Nucleic Acids Res. 2011;39:7920-30.
57. Cao H, Wu J, Lam S, Duan R, Newnham C, Molday RS, et al. Temporal and tissue specific regulation of RP-associated splicing factor genes PRPF3, PRPF31 and PRPC8--implications in the pathogenesis of RP. PLoS One. 2011;6, e15860.
58. Mordes D, Luo X, Kar A, Kuo D, Xu L, Fushimi K, et al. Pre-mRNA splicing and retinitis pigmentosa. Mol Vis. 2006;12:1259-71.
59. Kurtovic-Kozaric A, Przychodzen B, Singh J, Konarska MM, Clemente MJ, Otrock ZK, et al. PRPF8 defects cause missplicing in myeloid malignancies. Leukemia. 2015;29:126-36.
60. van der Lelij P, Stocsits RR, Ladurner R, Petzold G, Kreidl E, Koch B, et al. SNW1 enables sister chromatid cohesion by mediating the splicing of sororin and APC2 pre-mRNAs. EMBO J. 2014;33:2643-58.
61. Huppertz I, Attig J, D'Ambrogio A, Easton LE, Sibley CR, Sugimoto Y, et al. iCLIP: protein-RNA interactions at nucleotide resolution. Methods. 2014;65:274-87.
62. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009;10:R25.
63. Flicek P, Amode MR, Barrell D, Beal K, Brent S, Carvalho-Silva D, et al. Ensembl 2012. Nucleic Acids Res. 2012;40:D84-90.
64. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics. 2009;25:1105-11.
65. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26:841-2.
66. Anders S, Reyes A, Huber W. Detecting differential usage of exons from RNA-seq data. Genome Res. 2012;22:2008-17.
67. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B. 1995;57:289-300.
68. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell. 2010;38:576-89.
69. da Huang W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4:44-57.
70. Wang J, Duncan D, Shi Z, Zhang B. WEB-based GEne SeT AnaLysis Toolkit (WebGestalt): update 2013. Nucleic Acids Res. 2013;41:W77-83.
71. Benjamini Y, Yekutieli D. The control of the false discovery rate in multiple testing under dependency. Ann Stat. 2001;29:1165-88.
72. Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010;11:R106.