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PMID: 21685335 Published · ppublish English Journal Article

Using positional distribution to identify splicing elements and predict pre-mRNA processing defects in human genes.

Lim KH, Ferraris L, Filloux ME, Raphael BJ, Fairbrother WG

Abstract

We present an intuitive strategy for predicting the effect of sequence variation on splicing. In contrast to transcriptional elements, splicing elements appear to be strongly position dependent. We demonstrated that exonic binding of the normally intronic splicing factor, U2AF65, inhibits splicing. Reasoning that the positional distribution of a splicing element is a signature of its function, we developed a method for organizing all possible sequence motifs into clusters based on the genomic profile of their positional distribution around splice sites. Binding sites for serine/arginine rich (SR) proteins tended to be exonic whereas heterogeneous ribonucleoprotein (hnRNP) recognition elements were mostly intronic. In addition to the known elements, novel motifs were returned and validated. This method was also predictive of splicing mutations. A mutation in a motif creates a new motif that sometimes has a similar distribution shape to the original motif and sometimes has a different distribution. We created an intraallelic distance measure to capture this property and found that mutations that created large intraallelic distances disrupted splicing in vivo whereas mutations with small distances did not alter splicing. Analyzing the dataset of human disease alleles revealed known splicing mutants to have high intraallelic distances and suggested that 22% of disease alleles that were originally classified as missense mutations may also affect splicing. This category together with mutations in the canonical splicing signals suggest that approximately one third of all disease-causing mutations alter pre-mRNA splicing.

MeSH Terms
Algorithms Alleles Base Sequence Cluster Analysis Exons Genetic Variation Humans Mutation Nuclear Proteins/metabolism RNA Precursors/genetics,metabolism RNA Splicing/genetics Ribonucleoproteins/metabolism Splicing Factor U2AF
Chemicals
Nuclear Proteins RNA Precursors Ribonucleoproteins Splicing Factor U2AF U2AF2 protein, human
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Lim Kian Huat
Department of Molecular and Cellular Biology and Biochemistry, Brown University, 70 Ship Street, Providence, RI 02903, USA.
Ferraris Luciana
Filloux Madeleine E
Raphael Benjamin J
Fairbrother William G
References (44)
44 references, click to expand
  1. The splicing factors 9G8 and SRp20 transactivate splicing through different and specific enhancers.
    RNA. 1999 Mar;5(3):468-83 PMID: 10094314
  2. SR protein splicing factors interact with the Rous sarcoma virus negative regulator of splicing element.
    J Virol. 1996 Feb;70(2):1163-72 PMID: 8551577
  3. Heritability of alternative splicing in the human genome.
    Genome Res. 2007 Aug;17(8):1210-8 PMID: 17671095
  4. Purification and characterization of native spliceosomes suitable for three-dimensional structural analysis.
    RNA. 2002 Apr;8(4):426-39 PMID: 11991638
  5. Next-generation SELEX identifies sequence and structural determinants of splicing factor binding in human pre-mRNA sequence.
    RNA. 2009 Dec;15(12):2385-97 PMID: 19861426
  6. Comprehensive proteomic analysis of the human spliceosome.
    Nature. 2002 Sep 12;419(6903):182-5 PMID: 12226669
  7. An RNA code for the FOX2 splicing regulator revealed by mapping RNA-protein interactions in stem cells.
    Nat Struct Mol Biol. 2009 Feb;16(2):130-7 PMID: 19136955
  8. Regulation of alternative splicing by a transcriptional enhancer through RNA pol II elongation.
    Proc Natl Acad Sci U S A. 2002 Jun 11;99(12):8185-90 PMID: 12060763
  9. Inhibition by SR proteins of splicing of a regulated adenovirus pre-mRNA.
    Nature. 1996 Jun 6;381(6582):535-8 PMID: 8632829
  10. Genetic analysis of the SR protein ASF/SF2: interchangeability of RS domains and negative control of splicing.
    Genes Dev. 1998 Jul 15;12(14):2222-33 PMID: 9679066
  11. Multiple splicing defects in an intronic false exon.
    Mol Cell Biol. 2000 Sep;20(17):6414-25 PMID: 10938119
  12. The human splicing factors ASF/SF2 and SC35 possess distinct, functionally significant RNA binding specificities.
    EMBO J. 1995 Jul 17;14(14):3540-51 PMID: 7543047
  13. Loss of exon identity is a common mechanism of human inherited disease.
    Genome Res. 2011 Oct;21(10):1563-71 PMID: 21750108
  14. SR protein and snRNP requirements for assembly of the Rous sarcoma virus negative regulator of splicing complex in vitro.
    Virology. 1998 Mar 1;242(1):211-20 PMID: 9501036
  15. Comparative analysis identifies exonic splicing regulatory sequences--The complex definition of enhancers and silencers.
    Mol Cell. 2006 Jun 23;22(6):769-781 PMID: 16793546
  16. A computational analysis of sequence features involved in recognition of short introns.
    Proc Natl Acad Sci U S A. 2001 Sep 25;98(20):11193-8 PMID: 11572975
  17. Inference of splicing regulatory activities by sequence neighborhood analysis.
    PLoS Genet. 2006 Nov 24;2(11):e191 PMID: 17121466
  18. Systematic identification and analysis of exonic splicing silencers.
    Cell. 2004 Dec 17;119(6):831-45 PMID: 15607979
  19. The determinants of RNA-binding specificity of the heterogeneous nuclear ribonucleoprotein C proteins.
    J Biol Chem. 1994 Sep 16;269(37):23074-8 PMID: 8083209
  20. Distinct binding specificities and functions of higher eukaryotic polypyrimidine tract-binding proteins.
    Science. 1995 May 26;268(5214):1173-6 PMID: 7761834
  21. Direct selection for mutations affecting specific splice sites in a hamster dihydrofolate reductase minigene.
    Mol Cell Biol. 1993 Jan;13(1):289-300 PMID: 8417332
  22. An RNA map predicting Nova-dependent splicing regulation.
    Nature. 2006 Nov 30;444(7119):580-6 PMID: 17065982
  23. Proteomic analysis of in vivo-assembled pre-mRNA splicing complexes expands the catalog of participating factors.
    Nucleic Acids Res. 2007;35(12):3928-44 PMID: 17537823
  24. SR proteins and splicing control.
    Genes Dev. 1996 Jul 1;10(13):1569-79 PMID: 8682289
  25. Serine/arginine-rich protein-dependent suppression of exon skipping by exonic splicing enhancers.
    Proc Natl Acad Sci U S A. 2005 Apr 5;102(14):5002-7 PMID: 15753297
  26. Three-dimensional structure of C complex spliceosomes by electron microscopy.
    Nat Struct Mol Biol. 2004 Mar;11(3):265-9 PMID: 14981503
  27. TFIIS enhances transcriptional elongation through an artificial arrest site in vivo.
    Mol Cell Biol. 2001 Jul;21(13):4162-8 PMID: 11390645
  28. The spliceosome: no assembly required?
    Mol Cell. 2002 Jan;9(1):8-9 PMID: 11804581
  29. The spliceosome: the most complex macromolecular machine in the cell?
    Bioessays. 2003 Dec;25(12):1147-9 PMID: 14635248
  30. Are splicing mutations the most frequent cause of hereditary disease?
    FEBS Lett. 2005 Mar 28;579(9):1900-3 PMID: 15792793
  31. Exon inclusion is dependent on predictable exonic splicing enhancers.
    Mol Cell Biol. 2005 Aug;25(16):7323-32 PMID: 16055740
  32. Intronic binding sites for hnRNP A/B and hnRNP F/H proteins stimulate pre-mRNA splicing.
    PLoS Biol. 2006 Feb;4(2):e21 PMID: 16396608
  33. Determination of the RNA binding specificity of the heterogeneous nuclear ribonucleoprotein (hnRNP) H/H'/F/2H9 family.
    J Biol Chem. 2001 Nov 23;276(47):43850-9 PMID: 11571276
  34. An intronic splicing enhancer binds U1 snRNPs to enhance splicing and select 5' splice sites.
    Mol Cell Biol. 2000 Dec;20(24):9225-35 PMID: 11094074
  35. Predictive identification of exonic splicing enhancers in human genes.
    Science. 2002 Aug 9;297(5583):1007-13 PMID: 12114529
  36. Mutations affecting mRNA splicing are the most common molecular defects in patients with neurofibromatosis type 1.
    Hum Mol Genet. 2000 Jan 22;9(2):237-47 PMID: 10607834
  37. Human Gene Mutation Database (HGMD): 2003 update.
    Hum Mutat. 2003 Jun;21(6):577-81 PMID: 12754702
  38. RNA binding specificity of hnRNP proteins: a subset bind to the 3' end of introns.
    EMBO J. 1988 Nov;7(11):3519-29 PMID: 3208740
  39. Intronic CA-repeat and CA-rich elements: a new class of regulators of mammalian alternative splicing.
    EMBO J. 2005 Jun 1;24(11):1988-98 PMID: 15889141
  40. Antisense correction of SMN2 splicing in the CNS rescues necrosis in a type III SMA mouse model.
    Genes Dev. 2010 Aug 1;24(15):1634-44 PMID: 20624852
  41. iCLIP reveals the function of hnRNP particles in splicing at individual nucleotide resolution.
    Nat Struct Mol Biol. 2010 Jul;17(7):909-15 PMID: 20601959
  42. Genome-wide analysis of transcript isoform variation in humans.
    Nat Genet. 2008 Feb;40(2):225-31 PMID: 18193047
  43. Variation in sequence and organization of splicing regulatory elements in vertebrate genes.
    Proc Natl Acad Sci U S A. 2004 Nov 2;101(44):15700-5 PMID: 15505203
  44. RNA binding specificity of hnRNP A1: significance of hnRNP A1 high-affinity binding sites in pre-mRNA splicing.
    EMBO J. 1994 Mar 1;13(5):1197-204 PMID: 7510636
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2011-07-05
Epub
2011-00-17
Pages
11093-8
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC3131313
Subset
IM
Grants
NIGMS NIH HHS · R01 GM095612 · United States
NHGRI NIH HHS · R01 HG005690 · United States
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