← Back to search

Large-scale evaluation of the ability of RNA-binding proteins to activate exon inclusion.

Nature biotechnology · 2024 · Vol. 42 (9) · pp. 1429-1441

Abstract

RNA-binding proteins (RBPs) modulate alternative splicing outcomes to determine isoform expression and cellular survival. To identify RBPs that directly drive alternative exon inclusion, we developed tethered function luciferase-based splicing reporters that provide rapid, scalable and robust readouts of exon inclusion changes and used these to evaluate 718 human RBPs. We performed enhanced cross-linking immunoprecipitation, RNA sequencing and affinity purification-mass spectrometry to investigate a subset of candidates with no prior association with splicing. Integrative analysis of these assays indicates surprising roles for TRNAU1AP, SCAF8 and RTCA in the modulation of hundreds of endogenous splicing events. We also leveraged our tethering assays and top candidates to identify potent and compact exon inclusion activation domains for splicing modulation applications. Using these identified domains, we engineered programmable fusion proteins that outperform current artificial splicing factors at manipulating inclusion of reporter and endogenous exons. This tethering approach characterizes the ability of RBPs to induce exon inclusion and yields new molecular parts for programmable splicing control.

Publication Types

["Journal Article"]

Keywords

[]

MeSH Terms

["Humans", "Exons", "RNA-Binding Proteins", "Alternative Splicing", "HEK293 Cells"]

Funding

U24 HG009889 NHGRI NIH HHS (United States)
S10 OD026929 NIH HHS (United States)
R01 HG004659 NHGRI NIH HHS (United States)
U54 CA209891 NCI NIH HHS (United States)
T32 CA067754 NCI NIH HHS (United States)
DGE-2038238 National Science Foundation (NSF)
R01 HG012216 NHGRI NIH HHS (United States)
R35 GM128802 NIGMS NIH HHS (United States)
R01 AG071869 NIA NIH HHS (United States)
P41 GM103504 NIGMS NIH HHS (United States)
R01HG012216 U.S. Department of Health & Human Services | National Institutes of Health (NIH)
R01AG071869 U.S. Department of Health & Human Services | National Institutes of Health (NIH)
R35GM128802 U.S. Department of Health & Human Services | National Institutes of Health (NIH)
2224211 National Science Foundation (NSF)
PGS D-532649-2019 Gouvernement du Canada | Natural Sciences and Engineering Research Council of Canada (Conseil de Recherches en Sciences Naturelles et en Génie du Canada)
T32CA067754 U.S. Department of Health & Human Services | National Institutes of Health (NIH)

Linked Datasets (3)

GSE232599 GSE via ncbi_elink
GEO

Systematic identification of RNA-binding proteins and tethered domains that activate exon splicing inclusion

Homo sapiens
GSE232598 GSE via ncbi_elink
GEO

Systematic identification of RNA-binding proteins and tethered domains that activate exon splicing inclusion [RNA-seq]

Homo sapiens
30 data files
FileTypeSize
shNT_1_R1.fastq.gz RNA-Seq 5.0 GB
shNT_1_R1.fastq.gz RNA-Seq 5.0 GB
shNT_2_R1.fastq.gz RNA-Seq 5.2 GB
shNT_2_R1.fastq.gz RNA-Seq 5.2 GB
shNT_3_R1.fastq.gz RNA-Seq 6.3 GB
shNT_3_R1.fastq.gz RNA-Seq 6.3 GB
shRTCA_1_R1.fastq.gz RNA-Seq 5.3 GB
shRTCA_1_R1.fastq.gz RNA-Seq 5.3 GB
shRTCA_2_R1.fastq.gz RNA-Seq 4.7 GB
shRTCA_2_R1.fastq.gz RNA-Seq 4.7 GB
shRTCA_3_R1.fastq.gz RNA-Seq 5.0 GB
shRTCA_3_R1.fastq.gz RNA-Seq 5.0 GB
shSCAF8_1_R1.fastq.gz RNA-Seq 4.9 GB
shSCAF8_1_R1.fastq.gz RNA-Seq 4.9 GB
shSCAF8_2_R1.fastq.gz RNA-Seq 5.3 GB
shSCAF8_2_R1.fastq.gz RNA-Seq 5.3 GB
shSCAF8_3_R1.fastq.gz RNA-Seq 4.8 GB
shSCAF8_3_R1.fastq.gz RNA-Seq 4.8 GB
shSTAU2_1_R1.fastq.gz RNA-Seq 4.8 GB
shSTAU2_1_R1.fastq.gz RNA-Seq 4.8 GB
shSTAU2_2_R1.fastq.gz RNA-Seq 4.6 GB
shSTAU2_2_R1.fastq.gz RNA-Seq 4.6 GB
shSTAU2_3_R1.fastq.gz RNA-Seq 4.7 GB
shSTAU2_3_R1.fastq.gz RNA-Seq 4.7 GB
shTRNAU1AP_1_R1.fastq.gz RNA-Seq 5.6 GB
shTRNAU1AP_1_R1.fastq.gz RNA-Seq 5.6 GB
shTRNAU1AP_2_R1.fastq.gz RNA-Seq 4.8 GB
shTRNAU1AP_2_R1.fastq.gz RNA-Seq 4.8 GB
shTRNAU1AP_3_R1.fastq.gz RNA-Seq 5.6 GB
shTRNAU1AP_3_R1.fastq.gz RNA-Seq 5.6 GB
GSE232597 GSE via ncbi_elink
GEO

Systematic identification of RNA-binding proteins and tethered domains that activate exon splicing inclusion [eCLIP-seq]

Homo sapiens
40 data files
FileTypeSize
FLAG_IN1.fastq.gz RIP-Seq 928.9 MB
FLAG_IN1.fastq.gz RIP-Seq 928.9 MB
FLAG_IN2.fastq.gz RIP-Seq 1.0 GB
FLAG_IN2.fastq.gz RIP-Seq 1.0 GB
FLAG_IP1.fastq.gz RIP-Seq 864.1 MB
FLAG_IP1.fastq.gz RIP-Seq 864.1 MB
FLAG_IP2.fastq.gz RIP-Seq 802.7 MB
FLAG_IP2.fastq.gz RIP-Seq 802.7 MB
RTCA_IN1.fastq.gz RIP-Seq 824.8 MB
RTCA_IN1.fastq.gz RIP-Seq 824.8 MB
RTCA_IN2.fastq.gz RIP-Seq 808.7 MB
RTCA_IN2.fastq.gz RIP-Seq 808.7 MB
RTCA_IP1.fastq.gz RIP-Seq 816.4 MB
RTCA_IP1.fastq.gz RIP-Seq 816.4 MB
RTCA_IP2.fastq.gz RIP-Seq 858.7 MB
RTCA_IP2.fastq.gz RIP-Seq 858.7 MB
SCAF8_IN1.fastq.gz RIP-Seq 746.9 MB
SCAF8_IN1.fastq.gz RIP-Seq 746.9 MB
SCAF8_IN2.fastq.gz RIP-Seq 882.8 MB
SCAF8_IN2.fastq.gz RIP-Seq 882.8 MB
SCAF8_IP1.fastq.gz RIP-Seq 782.9 MB
SCAF8_IP1.fastq.gz RIP-Seq 782.9 MB
SCAF8_IP2.fastq.gz RIP-Seq 852.6 MB
SCAF8_IP2.fastq.gz RIP-Seq 852.6 MB
STAU2_IN1.fastq.gz RIP-Seq 805.7 MB
STAU2_IN1.fastq.gz RIP-Seq 805.7 MB
STAU2_IN2.fastq.gz RIP-Seq 902.6 MB
STAU2_IN2.fastq.gz RIP-Seq 902.6 MB
STAU2_IP1.fastq.gz RIP-Seq 925.0 MB
STAU2_IP1.fastq.gz RIP-Seq 925.0 MB
STAU2_IP2.fastq.gz RIP-Seq 876.9 MB
STAU2_IP2.fastq.gz RIP-Seq 876.9 MB
TRNAU1AP_IN1.fastq.gz RIP-Seq 652.9 MB
TRNAU1AP_IN1.fastq.gz RIP-Seq 652.9 MB
TRNAU1AP_IN2.fastq.gz RIP-Seq 493.3 MB
TRNAU1AP_IN2.fastq.gz RIP-Seq 493.3 MB
TRNAU1AP_IP1.fastq.gz RIP-Seq 514.1 MB
TRNAU1AP_IP1.fastq.gz RIP-Seq 514.1 MB
TRNAU1AP_IP2.fastq.gz RIP-Seq 819.3 MB
TRNAU1AP_IP2.fastq.gz RIP-Seq 819.3 MB

Potentially Related Datasets (1)

These accessions were text-mined from the PMC full text. They may be referenced for comparison, cited from other studies, or otherwise mentioned without being primary data for this paper.

Systematic identification of RNA-binding proteins and tethered domains that activate exon splicing inclusion

Analysis Pipelines (3)

eCLIP geo_data_processing GSE232597
RNA-seq geo_data_processing GSE232598
eCLIP geo_data_processing GSE232599