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Cytoplasmic Rbfox1 Regulates the Expression of Synaptic and Autism-Related Genes
Open accessAbstract
Human genetic studies have identified the neuronal RNA binding protein, Rbfox1, as a candidate gene for autism spectrum disorders. While Rbfox1 functions as a splicing regulator in the nucleus, it is also alternatively spliced to produce cytoplasmic isoforms. To investigate the function of cytoplasmic Rbfox1, we knocked down Rbfox proteins in mouse neurons and rescued with cytoplasmic or nuclear Rbfox1. Transcriptome profiling showed that nuclear Rbfox1 rescued splicing changes, whereas cytoplasmic Rbfox1 rescued changes in mRNA levels. iCLIP-seq of subcellular fractions revealed that Rbfox1 bound predominantly to introns in nascent RNA, while cytoplasmic Rbox1 bound to 3' UTRs. Cytoplasmic Rbfox1 binding increased target mRNA stability and translation, and Rbfox1 and miRNA binding sites overlapped significantly. Cytoplasmic Rbfox1 target mRNAs were enriched in genes involved in cortical development and autism. Our results uncover a new Rbfox1 regulatory network and highlight the importance of cytoplasmic RNA metabolism to cortical development and disease.
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“We also find significant enrichment of splicing changes in targets of two RNA binding proteins that regulate synaptic transmission and whose targets are implicated in both ASD and SCZ, the neuronal splicing regulator RBFOX1 (FDR=5.16×10−11) (32) and the fragile X mental retardation protein (FMRP) (FDR=3.10×10−21) (33).”
From Transcriptome-wide isoform-level dysregulation in ASD, schizophrenia, and bipolar disorder (2018) · cites this paper as [32]
In the citing paper
“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 [32]
In the citing paper
“Here, we find that isoM17 shows greater enrichment for nuclear RBFOX1 targets (Fig 6C), whereas isoM2 shows stronger overlap with cytoplasmic targets (32).”
From Transcriptome-wide isoform-level dysregulation in ASD, schizophrenia, and bipolar disorder (2018) · cites this paper as [32]
In the citing paper
“the protein encoded by RBFOX1 regulates the expression of 15 of the top 40 ranked genes (the probability of this event is p = 3.4e−05) [70].”
From An integrated analysis of genes and functional pathways for aggression in human and rodent models (2019) · cites this paper as [70]
In the citing paper
“many RNA-binding proteins controlling splicing choices also affect the choice of poly-A site and can also be found in the cytoplasm, where they control the translation or stability of target transcripts through binding in 3′ UTRs197”
From The neurogenetics of alternative splicing (2016) · cites this paper as [197]
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Metadata
- Authors
- Lee, J.-A., Damianov, A., Lin, C.-H., Fontes, M., Parikshak, N. N., Anderson, E. S., Geschwind, D. H., Black, D. L., & Martin, K. C.
- Affiliations
- University of California, Los Angeles (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Martin, Kelsey C.
- ORCID
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2016-01
- Volume
- 89
- Issue
- 1
- Pages
- 113-128
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC4858412
- OpenAlex
- W2190411440
- Cited by
- 232
- References
- 65
- Citations by year
- 2026: 10 · 2025: 17 · 2024: 26 · 2023: 22 · 2022: 24 · 2021: 18 · 2020: 31 · 2019: 20 · 2018: 27 · 2017: 19 · 2016: 18
- FWCI
- 9.26
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (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 (4f30ag033993-03)
- National Institute on Aging (F30 AG033993, 4F30AG033993)
- National Institute of Mental Health (F30MH099886, R21MH101684)
- National Institute of General Medical Sciences (R01GM084317)
- National Institute of Neurological Disorders and Stroke (R01NS045324)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (P50HD055784)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA regulation and disease
- Keywords
- RBFOX1, autism spectrum disorder, synaptic genes, alternative splicing, RNA-binding proteins, mRNA stability, translation (biology), 3' untranslated region, microRNA binding sites, cortical development, gene expression profiling
- MeSH terms
- RNA Splicing Factors, Animals, Autistic Disorder, Brain, Cytoplasm, Estriol, Humans, Mice, Inbred C57BL, Neurons, RNA, Messenger, RNA-Binding Proteins, Alternative Splicing, Gene Expression Profiling
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