Abstract
Gene expression is tightly regulated at the post-transcriptional level through splicing, transport, translation, and decay. RNA-binding proteins (RBPs) play key roles in post-transcriptional gene regulation, and genetic variants that alter RBP-RNA interactions can affect gene products and functions. We developed a computational method ASPRIN (Allele-Specific Protein-RNA Interaction) that uses a joint analysis of CLIP-seq (cross-linking and immunoprecipitation followed by high-throughput sequencing) and RNA-seq data to identify genetic variants that alter RBP-RNA interactions by directly observing the allelic preference of RBP from CLIP-seq experiments as compared to RNA-seq. We used ASPRIN to systematically analyze CLIP-seq and RNA-seq data for 166 RBPs in two ENCODE (Encyclopedia of DNA Elements) cell lines. ASPRIN identified genetic variants that alter RBP-RNA interactions by modifying RBP binding motifs within RNA. Moreover, through an integrative ASPRIN analysis with population-scale RNA-seq data, we showed that ASPRIN can help reveal potential causal variants that affect alternative splicing via allele-specific protein-RNA interactions.
Keywords
CLIP-seq
RNA-seq
alternative splicing
bioinformatics
genetic variation
post-transcriptional regulation
protein-RNA interactions
single-nucleotide polymorphism
transcriptomics
MeSH Terms
Alleles
Alternative Splicing
Computational Biology/methods
High-Throughput Nucleotide Sequencing
Humans
RNA/genetics,metabolism
RNA-Binding Proteins/genetics,metabolism
Sequence Analysis, RNA/methods
Transcriptome
Chemicals
RNA-Binding Proteins
RNA
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Bahrami-Samani Emad
Department of Microbiology, Immunology & Molecular Genetics, University of California, Los Angeles, Los Angeles, CA 90095, USA; Center for Computational and Genomic Medicine, The Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA.
Xing Yi
Department of Microbiology, Immunology & Molecular Genetics, University of California, Los Angeles, Los Angeles, CA 90095, USA; Center for Computational and Genomic Medicine, The Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA; Department of Pathology and Laboratory Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA. Electronic address:
[email protected].
References (30)
30 references, click to expand
-
RADAR: a rigorously annotated database of A-to-I RNA editing.
Nucleic Acids Res. 2014 Jan;42(Database issue):D109-13
PMID: 24163250
-
Repbase Update, a database of repetitive elements in eukaryotic genomes.
Mob DNA. 2015 Jun 02;6:11
PMID: 26045719
-
The Expanding Landscape of Alternative Splicing Variation in Human Populations.
Am J Hum Genet. 2018 Jan 4;102(1):11-26
PMID: 29304370
-
dbSNP: the NCBI database of genetic variation.
Nucleic Acids Res. 2001 Jan 1;29(1):308-11
PMID: 11125122
-
Genome Sequencing and RNA-Motif Analysis Reveal Novel Damaging Noncoding Mutations in Human Tumors.
Mol Cancer Res. 2018 Jul;16(7):1112-1124
PMID: 29592900
-
GLiMMPS: robust statistical model for regulatory variation of alternative splicing using RNA-seq data.
Genome Biol. 2013 Jul 22;14(7):R74
PMID: 23876401
-
Rbfox Proteins Regulate Splicing as Part of a Large Multiprotein Complex LASR.
Cell. 2016 Apr 21;165(3):606-19
PMID: 27104978
-
Human genomics: Cracking the regulatory code.
Nature. 2017 Oct 11;550(7675):190-191
PMID: 29022577
-
Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP.
Cell. 2010 Apr 2;141(1):129-41
PMID: 20371350
-
A brave new world of RNA-binding proteins.
Nat Rev Mol Cell Biol. 2018 May;19(5):327-341
PMID: 29339797
-
The NHGRI GWAS Catalog, a curated resource of SNP-trait associations.
Nucleic Acids Res. 2014 Jan;42(Database issue):D1001-6
PMID: 24316577
-
Statistical significance of cis-regulatory modules.
BMC Bioinformatics. 2007 Jan 22;8:19
PMID: 17241466
-
Robust transcriptome-wide discovery of RNA-binding protein binding sites with enhanced CLIP (eCLIP).
Nat Methods. 2016 Jun;13(6):508-14
PMID: 27018577
-
HITS-CLIP yields genome-wide insights into brain alternative RNA processing.
Nature. 2008 Nov 27;456(7221):464-9
PMID: 18978773
-
From birth to death: the complex lives of eukaryotic mRNAs.
Science. 2005 Sep 2;309(5740):1514-8
PMID: 16141059
-
In silico prediction of splice-altering single nucleotide variants in the human genome.
Nucleic Acids Res. 2014 Dec 16;42(22):13534-44
PMID: 25416802
-
The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data.
Genome Res. 2010 Sep;20(9):1297-303
PMID: 20644199
-
Computational challenges, tools, and resources for analyzing co- and post-transcriptional events in high throughput.
Wiley Interdiscip Rev RNA. 2015 May-Jun;6(3):291-310
PMID: 25515586
-
RNA and disease.
Cell. 2009 Feb 20;136(4):777-93
PMID: 19239895
-
Site identification in high-throughput RNA-protein interaction data.
Bioinformatics. 2012 Dec 1;28(23):3013-20
PMID: 23024010
-
Splicing in disease: disruption of the splicing code and the decoding machinery.
Nat Rev Genet. 2007 Oct;8(10):749-61
PMID: 17726481
-
STAR: ultrafast universal RNA-seq aligner.
Bioinformatics. 2013 Jan 1;29(1):15-21
PMID: 23104886
-
Leveraging cross-link modification events in CLIP-seq for motif discovery.
Nucleic Acids Res. 2015 Jan;43(1):95-103
PMID: 25505146
-
A global reference for human genetic variation.
Nature. 2015 Oct 1;526(7571):68-74
PMID: 26432245
-
RNA-binding proteins in human genetic disease.
Trends Genet. 2008 Aug;24(8):416-25
PMID: 18597886
-
PLINK: a tool set for whole-genome association and population-based linkage analyses.
Am J Hum Genet. 2007 Sep;81(3):559-75
PMID: 17701901
-
RBP-Var: a database of functional variants involved in regulation mediated by RNA-binding proteins.
Nucleic Acids Res. 2016 Jan 4;44(D1):D154-63
PMID: 26635394
-
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
-
RNA-binding proteins and post-transcriptional gene regulation.
FEBS Lett. 2008 Jun 18;582(14):1977-86
PMID: 18342629
-
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