Rbfox proteins regulate alternative mRNA splicing through evolutionarily conserved RNA bridges
Open accessAbstract
Alternative splicing (AS) enables programmed diversity of gene expression across tissues and development. We show here that binding in distal intronic regions (>500 nucleotides (nt) from any exon) by Rbfox splicing factors important in development is extensive and is an active mode of splicing regulation. Similarly to exon-proximal sites, distal sites contain evolutionarily conserved GCATG sequences and are associated with AS activation and repression upon modulation of Rbfox abundance in human and mouse experimental systems. As a proof of principle, we validated the activity of two specific Rbfox enhancers in KIF21A and ENAH distal introns and showed that a conserved long-range RNA-RNA base-pairing interaction (an RNA bridge) is necessary for Rbfox-mediated exon inclusion in the ENAH gene. Thus we demonstrate a previously unknown RNA-mediated mechanism for AS control by distally bound RNA-binding proteins.
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We identified 15,222 and 15,805 chimeric clusters in two replicates, respectively, for the 20 miRNAs with the greatest number of chimeric reads.
“First, we utilized the CLIPper algorithm (Lovci et al., 2013) to find clusters of chimeric reads for the 20 miRNAs with the greatest number of chimeric reads, identifying 15,222 and 15,805 chimeric clusters in two replicates, respectively.”
From Scalable and deep profiling of mRNA targets for individual microRNAs with chimeric eCLIP (2022) · cites this paper as Lovci et al., 2013
Previous experimental perturbation of Rbfox1, SRRM4, and PTBP1 shows strong overlap with the differential splicing changes found in ASD cortex.
“Previous experimental perturbation of three splicing factors, Rbfox1 (ref. 18), SRRM4 (ref. 19), and PTBP1 (ref. 20), shows strong overlap with the differential splicing changes found in ASD cortex, further supporting these predicted relationships (Fig. 1h, Extended Data Fig. 5b).”
From Genome-wide changes in lncRNA, splicing, and regional gene expression patterns in autism (2016) · cites this paper as [18]
Relatively few splicing and expression changes were detected in the Rbfox1−/− whole brain.
“Relatively few splicing and expression changes were detected in the Rbfox1−/− whole brain”
From The neurogenetics of alternative splicing (2016) · cites this paper as [132]
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Self-citationAjith, S., Gazzara, M. R., Cole, B. S., Shankarling, G. S., Martínez, N. M., Mallory, M. J., & Lynch, K. W. (2016) · RNA Biology · doi:10.1080/15476286.2016.1176663 · Cited by 49 · see citing works
Concentration-dependent splicing is enabled by Rbfox motifs of intermediate affinity
Begg, B. E., Jens, M., Wang, P. Y., Minor, C. M., & Burge, C. B. (2020) · Nature Structural & Molecular Biology · doi:10.1038/s41594-020-0475-8 · Cited by 54 · see citing works
- Authors
- Lovci, M. T., Ghanem, D., Marr, H., Arnold, J., Gee, S., Parra, M., Liang, T. Y., Stark, T. J., Gehman, L. T., Hoon, S., Massirer, K. B., Pratt, G. A., Black, D. L., Gray, J. W., Conboy, J. G., & Yeo, G. W.
- Affiliations
- University of California San Diego (US)
- Lawrence Berkeley National Laboratory (US)
- Howard Hughes Medical Institute (US)
- Agency for Science, Technology and Research (SG)
- Oregon Health & Science University (US)
- Corresponding author
- Conboy, John G
- Yeo, Gene W
- ORCID
- Venue
- Nature Structural & Molecular Biology
- Published
- 2013-11-10
- Volume
- 20
- Issue
- 12
- Pages
- 1434-1442
- ISSN
- 1545-9985 (ISSN-L)
- 1545-9993
- PMC
- PMC3918504
- OpenAlex
- W1985217779
- Cited by
- 385
- References
- 70
- Citations by year
- 2026: 30 · 2025: 25 · 2024: 32 · 2023: 32 · 2022: 27 · 2021: 46 · 2020: 40 · 2019: 19 · 2018: 40 · 2017: 27 · 2016: 36 · 2015: 16 · 2014: 15
- FWCI
- 10.00
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Structural & Molecular Biology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Science Foundation
- Howard Hughes Medical Institute
- U.S. Department of Energy (DE‐AC02‐05CH1123, AC02-05CH1123, DE-AC02-)
- National Institutes of Health (DE-AC02-05CH1123, RO1 GM49662)
- Genentech
- Office of Science (DE‐AC02‐05CH1123, DE-AC02)
- National Heart, Lung, and Blood Institute (R01HL045182, R56HL045182, HL045182)
- National Human Genome Research Institute (R01HG004659, U54HG007005)
- National Cancer Institute (CA-112970, U24CA126551, P30CA023100, U54CA112970, CA 126551)
- National Institute of General Medical Sciences (R01 GM 49662, R01GM084317, T32GM008666, R01GM049662)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK094699, P01DK032094, R01DK094699, DK032094)
- National Institute of Neurological Disorders and Stroke (R01NS075449)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA regulation and disease
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Keywords
- alternative splicing, RNA-RNA base pairing, RNA-binding proteins, ENAH, KIF21A, tissue-specific splicing
- MeSH terms
- RNA Splicing Factors, Animals, Base Sequence, Binding Sites, Cell Line, Humans, Microfilament Proteins, Models, Genetic, Nucleic Acid Conformation, RNA, Messenger, Kinesins, RNA-Binding Proteins, Conserved Sequence, Alternative Splicing, Base Pairing, Regulatory Sequences, Ribonucleic Acid, Mice
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