The splicing regulator Rbfox1 (A2BP1) controls neuronal excitation in the mammalian brain
Open accessAbstract
The Rbfox family of RNA binding proteins regulates alternative splicing of many important neuronal transcripts, but its role in neuronal physiology is not clear. We show here that central nervous system-specific deletion of the gene encoding Rbfox1 results in heightened susceptibility to spontaneous and kainic acid-induced seizures. Electrophysiological recording revealed a corresponding increase in neuronal excitability in the dentate gyrus of the knockout mice. Whole-transcriptome analyses identified multiple splicing changes in the Rbfox1(-/-) brain with few changes in overall transcript abundance. These splicing changes alter proteins that mediate synaptic transmission and membrane excitation. Thus, Rbfox1 directs a genetic program required in the prevention of neuronal hyperexcitation and seizures. The Rbfox1 knockout mice provide a new model to study the post-transcriptional regulation of synaptic function.
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Disruption of alternative splicing can lead to neurological diseases in human and animal models.
“previous studies have shown that disruption of alternative splicing can lead to neurological diseases in human and animal models (Buckanovich et al., 1996;Yang et al., 1998;Gehman et al., 2011)”
From An RNA-Sequencing Transcriptome and Splicing Database of Glia, Neurons, and Vascular Cells of the Cerebral Cortex (2014) · cites this paper as Gehman et al., 2011
CaMKIV phosphorylation regulates RBFOX1 activity, and RBFOX1 controls alternative splicing and stability of many mRNAs involved in synaptic and neuronal signaling, including CAMK2G, GRIN1, CNTNAP2, NRCAM, and RBFOX1 itself.
“For example, CaMKIV phosphorylation regulates the activity of RBFOX1, a factor that controls the alternative-splicing and stability of many mRNAs involved in synaptic and neuronal signaling, including CAMK2G, GRIN1, CNTNAP2, NRCAM and RBFOX1 itself (Gehman et al., 2011).”
From Unifying Views of Autism Spectrum Disorders: A Consideration of Autoregulatory Feedback Loops (2016) · cites this paper as Gehman et al., 2011
RBFOX1 encodes a splicing regulator mainly expressed in neurons and known to target genes important for neuronal development, including NMDA receptor 1 and voltage-gated calcium channels.
“RBFOX1 (also called A2BP1 ) encodes a splicing regulator mainly expressed in neurons and known to target several genes important to neuronal development, including NMDA receptor 1 and voltage-gated calcium channels (Gandal et al., 2018; Gehman et al., 2011; Hamada et al., 2015).”
From Genomic Relationships, Novel Loci, and Pleiotropic Mechanisms across Eight Psychiatric Disorders (2019) · cites this paper as Gehman et al., 2011
CNS-specific depletion of Rbfox1 increases seizure susceptibility and neuronal over-excitability in the dentate gyrus.
“Central nervous system (CNS)-specific depletion of Rbfox1 results in an increased susceptibility of mice to seizures and in over-excitability of neurons in the dentate gyrus (Gehman et al., 2011).”
From HITS-CLIP and integrative modeling define the Rbfox splicing-regulatory network linked to brain development and autism (2014) · cites this paper as Gehman et al., 2011
WT versus Rbfox1 or Rbfox2 KO brain exon-junction microarray studies identified only 20 and 29 Rbfox-dependent exons, respectively.
“Comparison of wild type (WT) versus Rbfox1 or Rbfox2 KO brains using exon-junction microarrays has identified multiple Rbfox-dependent exons (Gehman et al., 2012; Gehman et al., 2011). However, the number of exons identified using this approach is quite small (20 and 29 exons, respectively)”
From HITS-CLIP and integrative modeling define the Rbfox splicing-regulatory network linked to brain development and autism (2014) · cites this paper as Gehman et al., 2011
The integrative modeling approach employs a Bayesian network to weigh and combine several complementary data types probabilistically.
“This method uses a Bayesian network to probabilistically weigh and combine multiple types of data complementary to each other: bioinformatically predicted motif sites represented by MECS scores, protein-RNA interaction sites mapped by Rbfox HITS-CLIP, Rbfox1-dependent splicing identified by comparison of WT with Rbfox1 KO mouse brain using exon-junction microarrays (Gehman et al., 2011), Rbfox2-”
From HITS-CLIP and integrative modeling define the Rbfox splicing-regulatory network linked to brain development and autism (2014) · cites this paper as Gehman et al., 2011
Of eight exons with detectable inclusion and exclusion isoforms, three showed altered splicing after Rbfox1 depletion (ΔI≥0.1), and these exons were not identified as Rbfox1 targets in a prior genome-wide study.
“Among eight exons for which both the inclusion and exclusion isoforms can be detected, three exons showed altered splicing upon Rbfox1 depletion (ΔI≥0.1; Figure S6 and Table S5), and these were not identified as Rbfox1 targets in the previous genome-wide analysis (Gehman et al., 2011).”
From HITS-CLIP and integrative modeling define the Rbfox splicing-regulatory network linked to brain development and autism (2014) · cites this paper as Gehman et al., 2011
The small number of validated exons is probably explained by Rbfox protein redundancy and a compensatory rise in Rbfox2 in Rbfox1 knockout animals.
“The relatively small number of validated exons is likely due to the redundancy of Rbfox proteins and the compensatory increase of Rbfox2 protein expression in Rbfox1 KO animals (Gehman et al., 2011), although it is possible that some of the predicted targets might represent false positives.”
From HITS-CLIP and integrative modeling define the Rbfox splicing-regulatory network linked to brain development and autism (2014) · cites this paper as Gehman et al., 2011
Previous efforts lacked a genome-wide, high-resolution map of in vivo Rbfox interaction sites in the brain.
“An important piece of information missing in previous efforts toward this aim [e.g., (Fogel et al., 2012; Gehman et al., 2012; Gehman et al., 2011; Ray et al., 2013; Zhang et al., 2008)] is a genome-wide, high-resolution map ofin vivo Rbfox interaction sites in the brain.”
From HITS-CLIP and integrative modeling define the Rbfox splicing-regulatory network linked to brain development and autism (2014) · cites this paper as Gehman et al., 2011
Mouse experiments indicate RBFOX1 has distinct nuclear and cytoplasmic isoforms with differing functions.
“Experiments in mouse indicate that RBFOX1 has distinct nuclear and cytoplasmic isoforms with differing functions, the nuclear isoform primarily regulating pre-mRNA alternative splicing, and the cytoplasmic isoform binding to the 3’ UTR to stabilize target transcripts involved in regulation of neuronal excitability (28, 32, 58, 60).”
From Transcriptome-wide isoform-level dysregulation in ASD, schizophrenia, and bipolar disorder (2018) · cites this paper as [60]
All three Rbfox genes are broadly expressed in the brain, with individual neuronal cell types expressing different combinations at different developmental times.
“All three Rbfox genes are broadly expressed in the brain, with individual neuronal cell types expressing different combinations at different developmental times51–55.”
From The neurogenetics of alternative splicing (2016) · cites this paper as [53]
The mutually exclusive expression pattern of SLM1 and SLM2 is enforced by their cross-regulation via alternative splicing coupled with NMD.
“The mutually exclusive expression pattern of SLM1 and SLM2 is enforced by their cross-regulation via alternative splicing coupled with NMD, as seen with other paralogous pairs of RNA-binding proteins15,20,21,49,53,85,86.”
From The neurogenetics of alternative splicing (2016) · cites this paper as [53]
Pan-neuronal deletion of Rbfox1 leads to increased susceptibility to spontaneous seizures and kainic acid-induced seizures.
“Pan-neuronal deletion of Rbfox1 (Rbfox1loxp/loxp; Nestin-Cre) leads to increased susceptibility to spontaneous seizures and seizures induced by kainic acid”
From The neurogenetics of alternative splicing (2016) · cites this paper as [53]
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 [53]
Pan-neuronal deletion of Rbfox1 leads to hyperexcitation in the dentate gyrus.
“as well as hyperexcitation in the dentate gyrus53.”
From The neurogenetics of alternative splicing (2016) · cites this paper as [53]
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“Moreover, previous studies have shown that disruption of alternative splicing can lead to neurological diseases in human and animal models (Buckanovich et al., 1996; Yang et al., 1998; Gehman et al., 2011), and our splicing dataset provides a resource for understanding the cell type-specific contributions to these dis…”
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“RBFOX1 (also called A2BP1 ) encodes a splicing regulator mainly expressed in neurons and known to target several genes important to neuronal development, including NMDA receptor 1 and voltage-gated calcium channels (Gandal et al., 2018; Gehman et al., 2011; Hamada et al., 2015).”
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- Authors
- Gehman, L. T., Stoilov, P., Maguire, J., Damianov, A., Lin, C.-H., Shiue, L., Ares, M., Mody, I., & Black, D. L.
- Affiliations
- University of California, Los Angeles (US)
- West Virginia University (US)
- Tufts University (US)
- University of California, Santa Cruz (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Black, Douglas L
- ORCID
- Venue
- Nature Genetics
- Published
- 2011-05-29
- Volume
- 43
- Issue
- 7
- Pages
- 706-711
- ISSN
- 1061-4036 (ISSN-L)
- 1546-1718
- PMC
- PMC3125461
- OpenAlex
- W2085063270
- Cited by
- 331
- References
- 48
- Citations by year
- 2026: 21 · 2025: 16 · 2024: 15 · 2023: 13 · 2022: 16 · 2021: 20 · 2020: 22 · 2019: 16 · 2018: 30 · 2017: 25 · 2016: 26 · 2015: 32 · 2014: 20 · 2013: 34 · 2012: 16
- FWCI
- 9.38
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Genetics (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institutes of Health (NS30549)
- University of California, San Diego
- Institute of Molecular and Cell Biology
- National Institute of Mental Health (R01MH076994)
- National Institute of General Medical Sciences (R01GM084317, R01GM049369, R01GM049662)
- National Institute of Neurological Disorders and Stroke (R37NS030549)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Health Sciences › Medicine › Psychiatry and Mental health › Epilepsy research and treatment
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- RBFOX1, A2BP1, alternative splicing, RNA-binding proteins, neuronal excitability, seizures, kainic acid-induced seizures, spontaneous seizures, dentate gyrus, post-transcriptional regulation, synaptic transmission, splicing isoforms
- MeSH terms
- RNA Splicing Factors, Animals, Brain, Electrophysiology, Female, Gene Expression Regulation, Immunoenzyme Techniques, Kainic Acid, Male, Mice, Inbred C57BL, Synaptic Transmission, Neurons, RNA, Messenger, Seizures, Blotting, Western, Biomarkers, RNA-Binding Proteins, Apoptosis, Alternative Splicing, Mice, Knockout, Reverse Transcriptase Polymerase Chain Reaction, Oligonucleotide Array Sequence Analysis, Gene Expression Profiling, Cell Proliferation, Mice
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