CELF4 regulates translation and local abundance of a vast set of mRNAs, including genes associated with regulation of synaptic function
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RNA-binding proteins have emerged as causal agents of complex neurological diseases. Mice deficient for neuronal RNA-binding protein CELF4 have a complex neurological disorder with epilepsy as a prominent feature. Human CELF4 has recently been associated with clinical features similar to those seen in mutant mice. CELF4 is expressed primarily in excitatory neurons, including large pyramidal cells of the cerebral cortex and hippocampus, and it regulates excitatory but not inhibitory neurotransmission. We examined mechanisms underlying neuronal hyperexcitability in Celf4 mutants by identifying CELF4 target mRNAs and assessing their fate in the absence of CELF4 in view of their known functions. CELF4 binds to at least 15%-20% of the transcriptome, with striking specificity for the mRNA 3' untranslated region. CELF4 mRNA targets encode a variety of proteins, many of which are well established in neuron development and function. While the overall abundance of these mRNA targets is often dysregulated in Celf4 deficient mice, the actual expression changes are modest at the steady-state level. In contrast, by examining the transcriptome of polysome fractions and the mRNA distribution along the neuronal cell body-neuropil axis, we found that CELF4 is critical for maintaining mRNA stability and availability for translation. Among biological processes associated with CELF4 targets that accumulate in neuropil of mutants, regulation of synaptic plasticity and transmission are the most prominent. Together with a related study of the impact of CELF4 loss on sodium channel Na(v)1.6 function, we suggest that CELF4 deficiency leads to abnormal neuronal function by combining a specific effect on neuronal excitation with a general impairment of synaptic transmission. These results also expand our understanding of the vital roles RNA-binding proteins play in regulating and shaping the activity of neural circuits.
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RNA targets of FMRP and CELF4 are significantly enriched for ASD genes, and ASD candidate genes are enriched among their common targets.
“RNA targets of both FMRP (Darnell et al., 2011) and CELF4 (Wagnon et al., 2012) were reported to be significantly enriched for ASD genes, and ASD candidate genes were further enriched among the common targets of FMRP and CELF4 (Wagnon et al., 2012).”
From Getting to the cores of autism (2019) · cites this paper as Wagnon et al., 2012
FMRP is a seminal example of an ASD-associated RNA-binding protein; other ASD-associated RBPs include CELF4, ELAVL3, and GIGYF1.
“A seminal example is the Fragile X mental retardation protein (FMRP) (Darnell et al., 2011), and other RBPs that are associated with ASD include CELF4 (Wagnon et al., 2012), ELAVL3 (Ince-Dunn et al., 2012) and GIGYF1 (Peter et al., 2017).”
From Getting to the cores of autism (2019) · cites this paper as Wagnon et al., 2012
Genes encoding CELF4-bound mRNAs also showed enrichment of dURVs in schizophrenia cases (OR=1.14; 95% CI=1.09-1.19; P=6.6e-4), greater than average but less than FMRP-bound genes.
“The genes encoding CELF4-bound mRNAs also showed an enrichment of dURVs in schizophrenia cases; this enrichment (OR=1.14; 95% CI=1.09–1.19; P = 6.6 × 10−4) was greater than that of the average gene though less strong than that of genes encoding FMRP-bound RNAs.”
From Increased burden of ultra-rare protein-altering variants among 4,877 individuals with schizophrenia (2016) · cites this paper as [28]
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Farris, S., Dynes, J. L., & Steward, O. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.21108-5 · Cited by 2 · see citing works
Genetic and structural evidence links Ca 2+ dysregulation and ATP2B2 to neuropsychiatric illnessPreprint
Gerges, S., Straarup, N. C., El-Brolosy, M. A., Satterstrom, F. K., Kamitaki, N., Yuan, J., Ling, E., Gelze, C., Lin, R., Goldman, M., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.08.25.672202 · Cited by 2 · see citing works
- Authors
- Wagnon, J. L., Briese, M., Sun, W., Mahaffey, C. L., Curk, T., Rot, G., Ule, J., & Frankel, W. N.
- Affiliations
- Jackson Laboratory (US)
- MRC Laboratory of Molecular Biology (GB)
- University of Ljubljana (SI)
- Corresponding author
- Frankel, Wayne N.
- Venue
- PLoS Genetics
- Publisher
- Public Library of Science (PLoS)
- Published
- 2012-11-29
- Volume
- 8
- Issue
- 11
- Pages
- e1003067
- ISSN
- 1553-7390 (ISSN-L)
- 1553-7404
- PMC
- PMC3510034
- OpenAlex
- W1998831398
- Cited by
- 125
- References
- 78
- Citations by year
- 2026: 11 · 2025: 10 · 2024: 9 · 2023: 8 · 2022: 8 · 2021: 7 · 2020: 19 · 2019: 8 · 2018: 11 · 2017: 12 · 2016: 5 · 2015: 7 · 2014: 2 · 2013: 7 · 2012: 1
- FWCI
- 2.19
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Genetics (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Repository of the University of Ljubljana (University of Ljubljana) (publishedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- UCL Discovery (University College London) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- The Mouseion at the JAXlibrary (Jackson Laboratory) (submittedVersion)
- Funders
- Epilepsy Foundation
- Wellcome Trust (089701)
- Javna Agencija za Raziskovalno Dejavnost RS
- National Institutes of Health
- Medical Research Council
- 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 › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- CELF4, RNA-binding proteins, 3' untranslated region, mRNA stability, translational regulation, polysome fractionation, neuronal hyperexcitability, epilepsy, synaptic plasticity, synaptic transmission, excitatory neurons
- MeSH terms
- CELF Proteins, Animals, Cerebral Cortex, Epilepsy, Hippocampus, Humans, Synaptic Transmission, Neurons, RNA, Messenger, Synapses, Protein Biosynthesis, RNA-Binding Proteins, Pyramidal Cells, RNA Stability, Mice, Transcriptome, NAV1.6 Voltage-Gated Sodium Channel
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