The Fragile X Syndrome Protein Represses Activity-Dependent Translation through CYFIP1, a New 4E-BP
Open accessAbstract
Strong evidence indicates that regulated mRNA translation in neuronal dendrites underlies synaptic plasticity and brain development. The fragile X mental retardation protein (FMRP) is involved in this process; here, we show that it acts by inhibiting translation initiation. A binding partner of FMRP, CYFIP1/Sra1, directly binds the translation initiation factor eIF4E through a domain that is structurally related to those present in 4E-BP translational inhibitors. Brain cytoplasmic RNA 1 (BC1), another FMRP binding partner, increases the affinity of FMRP for the CYFIP1-eIF4E complex in the brain. Levels of proteins encoded by known FMRP target mRNAs are increased upon reduction of CYFIP1 in neurons. Translational repression is regulated in an activity-dependent manner because BDNF or DHPG stimulation of neurons causes CYFIP1 to dissociate from eIF4E at synapses, thereby resulting in protein synthesis. Thus, the translational repression activity of FMRP in the brain is mediated, at least in part, by CYFIP1.
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BDNF regulates translation by causing release of CYFIP1 from eIF4E via the action of MNK1.
“It was reported that BDNF regulates translation by causing release of CYFIP1 from eIF4E via the action of MAP kinase interacting serine/threonine kinase 1 (MNK1) (Napoli et al., 2008; Panja et al., 2014).”
From New insights into the regulatory function of CYFIP1 in the context of WAVE- and FMRP-containing complexes (2017) · cites this paper as Napoli et al., 2008
The Summary (p. 1) and the synaptic-stimulation discussion (p. 8) say that BDNF causes CYFIP1 and eIF4E to dissociate, relieving translational repression. Neither passage identifies MNK1 as the mediator, and searches for MNK1 and its full name found no support for that mechanism in our copy. (LLM, conf=0.88)
Experimental — accuracy not yet measuredCYFIP1 has a vital role in the local regulation of spine actin dynamics via WAVE and Arp2/3.
“In addition to previous functions described for CYFIP1 in the regulation of mRNA translation in dendrites and mGluR-long-term depression, our results suggest that CYFIP1 also has a vital role in the local regulation of spine actin dynamics via WAVE and Arp2/3.32,35”
From The autism and schizophrenia associated gene CYFIP1 is critical for the maintenance of dendritic complexity and the stabilization of mature spines (2014) · cites this paper as [32]
The activity-regulation section (p. 7) supports CYFIP1’s role in dendritic mRNA translation, and the Discussion (p. 8) identifies it as a component of the actin-related WAVE complex. The paper reports a response to mGluR stimulation (p. 8), but does not establish a role in mGluR-long-term depression. The spine-actin conclusion is presented as the citing authors’ own result, not a finding attributed to this source. (LLM, conf=0.84)
Experimental — accuracy not yet measuredCYFIP1 couples actin dynamics to other cellular processes, such as carrier vesicle biogenesis in the trans-Golgi network, and, via interactions with FMRP, regulates synaptic mRNA translation in an activity-dependent manner.
“Furthermore, CYFIP1 couples actin dynamics to other cellular processes, such as carrier vesicle biogenesis in the trans-Golgi network, and, via interactions with the FRMP (Fragile X mental retardation protein), regulates synaptic mRNA translation in an activity-dependent manner.32,33”
From The autism and schizophrenia associated gene CYFIP1 is critical for the maintenance of dendritic complexity and the stabilization of mature spines (2014) · cites this paper as [32]
The Discussion (p. 8) identifies CYFIP1 as a component of the actin-polymerization WAVE complex, and the synapse experiments (p. 8) support activity-dependent regulation of translation through the FMRP–CYFIP1 complex. Our copy does not support the further claim that CYFIP1 couples actin dynamics to carrier vesicle biogenesis in the trans-Golgi network. (LLM, conf=0.88)
Experimental — accuracy not yet measuredThe predicted conformational change moves the domain carrying the eIF4E-binding site toward the outside, allowing Lys743 to interact with Glu132 of eIF4E.
“The consequence of this conformational change is that the domain carrying the eIF4E-binding site moves toward the outside (Figure 2D), allowing Lys743 to interact with Glu132 of eIF4E (Figure 1A) (Napoli et al., 2008).”
From CYFIP1 Coordinates mRNA Translation and Cytoskeleton Remodeling to Ensure Proper Dendritic Spine Formation (2013) · cites this paper as Napoli et al., 2008
The Figure 2 discussion (p. 4) predicts that CYFIP1 Lys743 is positioned to form a salt bridge with Glu132 of eIF4E. It describes a predicted shape of the binding peptide, but not a conformational change that moves the eIF4E-binding domain outward; that part of the attributed claim is unsupported. (LLM, conf=0.88)
Experimental — accuracy not yet measuredThe BDNF-RAC1-CYFIP1 pathway can increase both the local protein translation and actin polymerization required for synaptic plasticity.
“Thus, the BDNF-RAC1-CYFIP1 pathway can increase both the local protein translation and actin polymerization required for synaptic plasticity66,69.”
From The WAVE complex in developmental and adulthood brain disorders (2025) · cites this paper as [69]
The synapse experiments (p. 8) show that BDNF releases eIF4E from CYFIP1, consistent with increased local translation. The paper also links CYFIP1 to the actin-polymerizing WAVE complex (Discussion, p. 8), but it does not show that BDNF increases actin polymerization through a RAC1–CYFIP1 pathway; a RAC1 role in releasing translational repression is described as speculation (p. 9). (LLM, conf=0.86)
Experimental — accuracy not yet measured
CYFIP1 is involved in distinct FMRP-CYFIP1-eIF4E and WAVE complex functions and thereby coordinates local protein translation and actin polymerization in dendritic spines.
“Thus, CYFIP1 is involved in distinct FMRP-CYFIP1-eIF4E and WAVE complex functions and thereby coordinates local protein translation and actin polymerization in dendritic spines66,69,70.”
From The WAVE complex in developmental and adulthood brain disorders (2025) · cites this paper as [69]
The Discussion (p. 8) identifies CYFIP1 as both an FMRP-interacting factor and a component of the actin-related WAVE complex, while the synaptic experiments (p. 8) support its role in regulating translation through FMRP and eIF4E. The paper does not establish that CYFIP1 coordinates translation and actin polymerization in dendritic spines; the Relevance for the Fragile X Syndrome section (p. 10) only proposes a connection to synapse maturation. (LLM, conf=0.86)
Experimental — accuracy not yet measuredCYFIP1 interacts with FMRP and with the translation initiation factor eIF4E.
“CYFIP1 interacts with the Fragile X mental retardation protein (FMRP, encoded by the FMR1 gene), whose absence causes Fragile X syndrome, and with the translation initiation factor eIF4E.”
From New insights into the regulatory function of CYFIP1 in the context of WAVE- and FMRP-containing complexes (2017) · cites this paper as Napoli et al., 2008
The role of CYFIP1 cannot only be restricted to acting as a co-regulator of the initiation of translation together with FMRP.
“Overall, the role of CYFIP1 cannot only be restricted to the unique function of acting as a co-regulator of the initiation of translation together with FMRP (Napoli et al., 2008).”
From New insights into the regulatory function of CYFIP1 in the context of WAVE- and FMRP-containing complexes (2017) · cites this paper as Napoli et al., 2008
G-quadruplex-containing FMRP target mRNAs are not repressed via interaction with the CYFIP1-eIF4E subcomplex.
“In conclusion, G-quadruplex-containing FMRP target mRNAs are not repressed via interaction with the CYFIP1-eIF4E subcomplex, as proposed for other targets of FMRP (Napoli et al., 2008).”
From New insights into the regulatory function of CYFIP1 in the context of WAVE- and FMRP-containing complexes (2017) · cites this paper as Napoli et al., 2008
mMap1b mRNA is significantly associated with CYFIP1, >1.5 fold compared to mHprt1 mRNA.
“mMap1b mRNA, an mRNA previously identified in the CYFIP1 complex21, was significantly associated with CYFIP1, >1.5 fold compared to mHprt1 mRNA”
From CYFIP1 governs the development of cortical axons by modulating calcium availability (2025) · cites this paper as [21]
In the WRC crystal structure, NCKAP1 interacts with CYFIP1 over a large surface, and Lys743, critical for eIF4E binding, is covered by NCKAP1 and not accessible to solvent when CYFIP1 is in the WRC.
“According to the crystal structure of the WRC that includes CYFIP1 (Chen et al., 2010), NCKAP1 interacts with CYFIP1 over a large surface (Figure 1A, upper panel); the lysine critical for the binding to eIF4E (Lys743) (Napoli et al., 2008) is covered by NCKAP1 and therefore is not accessible to solvent when CYFIP1 is in the WRC (Figure 1A, bottom panels, Table S1).”
From CYFIP1 Coordinates mRNA Translation and Cytoskeleton Remodeling to Ensure Proper Dendritic Spine Formation (2013) · cites this paper as Napoli et al., 2008
The CYFIP1 interactors in whole cortical lysates include known partners FMRP and PABP-1 and novel partners ELAV-like proteins, Caprin1, and hnRNPQ/SYNCRIP.
“comprising either known (FMRP and PABP-1) (Napoli et al., 2008, Schenck et al., 2003) or novel (ELAV-like proteins, Caprin1 and hnRNPQ/SYNCRIP) partners”
From CYFIP1 Coordinates mRNA Translation and Cytoskeleton Remodeling to Ensure Proper Dendritic Spine Formation (2013) · cites this paper as Napoli et al., 2008
CYFIP1 is a key functional partner of FMRP.
“A key functional partner of FMRP is the cytoplasmic FMRP-interacting protein 1, CYFIP1 (Napoli et al., 2008, Schenck et al., 2003, Schenck et al., 2001) also known as “specific Rac1-activated” (SRA1) protein (Kobayashi et al., 1998).”
From CYFIP1 Coordinates mRNA Translation and Cytoskeleton Remodeling to Ensure Proper Dendritic Spine Formation (2013) · cites this paper as Napoli et al., 2008
Upon activation of BDNF/TrkB or group I metabotropic glutamate receptors, CYFIP1 is released from eIF4E and translation ensues.
“Upon activation of the brain-derived neurotrophic factor (BDNF)/NT-3 growth factor receptor (TrkB) or group I metabotropic glutamate receptors (mGluRs), CYFIP1 is released from eIF4E and translation ensues (Napoli et al., 2008).”
From CYFIP1 Coordinates mRNA Translation and Cytoskeleton Remodeling to Ensure Proper Dendritic Spine Formation (2013) · cites this paper as Napoli et al., 2008
RNAs (e.g., BC1) can strengthen the FMRP-CYFIP1 interaction.
“confirming previous indications that RNAs (e.g., BC1) can strengthen this interaction (Napoli et al., 2008)”
From CYFIP1 Coordinates mRNA Translation and Cytoskeleton Remodeling to Ensure Proper Dendritic Spine Formation (2013) · cites this paper as Napoli et al., 2008
Together with FMRP, CYFIP1 represses neuronal protein synthesis by sequestering eIF4E, thereby preventing initiation of translation.
“Together with FMRP, CYFIP1 represses neuronal protein synthesis: FMRP tethers specific mRNAs to CYFIP1, which in turn sequesters the cap-binding protein eIF4E, thereby preventing initiation of translation (Napoli et al., 2008).”
From CYFIP1 Coordinates mRNA Translation and Cytoskeleton Remodeling to Ensure Proper Dendritic Spine Formation (2013) · cites this paper as Napoli et al., 2008
CYFIP1 is implicated in intellectual disability, autism spectrum disorder, and schizophrenia.
“CYFIP1 is implicated in ID (Cooper et al., 2011, Napoli et al., 2008, Nowicki et al., 2007, Schenck et al., 2003), ASD (Cooper et al., 2011, Doornbos et al., 2009, Murthy et al., 2007, Nishimura et al., 2007, Sahoo et al., 2006, van der Zwaag et al., 2010, von der Lippe et al., 2010), and SCZ (Tam et al., 2010, Zhao et al., 2012).”
From CYFIP1 Coordinates mRNA Translation and Cytoskeleton Remodeling to Ensure Proper Dendritic Spine Formation (2013) · cites this paper as Napoli et al., 2008
CYFIP1 directly binds to FMR1 and mediates the repressive activity of FMRP in dendritic protein translation.
“CYFIP1 directly binds to fragile X messenger ribonucleoprotein 1 (FMR1 or FMRP) and mediates the repressive activity of FMRP in dendritic protein translation.”
From The WAVE complex in developmental and adulthood brain disorders (2025) · cites this paper as [69]
BDNF or DHPG causes the dissociation of CYFIP1 from eIF4E, suggesting a pivotal role of the FMRP-CYFIP1 complex in neuronal activity-induced local protein synthesis.
“Importantly, BDNF or DHPG, a Group I metabotropic glutamate receptor agonist, causes the dissociation of CYFIP1 from eIF4E, suggesting a pivotal role of the FMRP-CYFIP1 complex in neuronal activity-induced local protein synthesis69.”
From The WAVE complex in developmental and adulthood brain disorders (2025) · cites this paper as [69]
CYFIP1/Sra1 directly binds to eIF4E and thereby inhibits translational initiation.
“CYFIP1/Sra1 directly binds to eIF4E (eukaryotic translation initiation factor 4E) and thereby inhibits translational initiation69.”
From The WAVE complex in developmental and adulthood brain disorders (2025) · cites this paper as [69]
CYFIP1 downregulation or genetic alterations in CYFIP1 might alter the FMRP-CYFIP1-eIF4E-mediated repression of local protein synthesis in neurons.
“CYFIP1 downregulation or genetic alterations in CYFIP1 might alter the FMRP-CYFIP1-eIF4E-mediated repression of local protein synthesis in neurons69.”
From The WAVE complex in developmental and adulthood brain disorders (2025) · cites this paper as [69]
Dysregulation or mutations of FMRP-interacting proteins such as CYFIP1, eIF4E, and a subset of FMRP mRNA targets may contribute to the autism spectrum disorder phenotype observed in fragile X syndrome.
“Recent evidence indicates that dysregulation and or mutations of FMRP-interacting proteins, such as the cytoplasmic FMRP-interacting protein 1 (CYFIP1) (52-55), eukaryotic initiation factor 4 (eIF4E) (56,57), and a subset of FMRP mRNA targets (58), may contribute to the ASD phenotype observed in FXS.”
From Fragile X syndrome: causes, diagnosis, mechanisms, and therapeutics (2012) · cites this paper as [52]
Amyloid β-protein precursor is upregulated in the fragile X syndrome mouse model.
“Interestingly, the amyloid β-protein precursor (AβPP) is upregulated in the FXS mouse model (52,73).”
From Fragile X syndrome: causes, diagnosis, mechanisms, and therapeutics (2012) · cites this paper as [52]
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Self-citationRole of Purα in targeting mRNA to sites of translation in hippocampal neuronal dendrites
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Behavioral alterations in mice lacking the translation repressor 4E-BP2
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Self-citationTranslational Control by Neuroguidin, a Eukaryotic Initiation Factor 4E and CPEB Binding Protein
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Self-citation
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“49 CYFIP1 also regulates translation of CAMKII, 49 a key component of NMDAR complexes.”
BackgroundAdvancing the understanding of autism disease mechanisms through genetics
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Autism-related deficits via dysregulated eIF4E-dependent translational control
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Self-citationThe translation of translational control by FMRP: therapeutic targets for FXS
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The Pathophysiology of Fragile X (and What It Teaches Us about Synapses)
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Translational control in synaptic plasticity and cognitive dysfunction
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Self-citationBDNF mechanisms in late LTP formation: A synthesis and breakdown
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Self-citationDysregulation and restoration of translational homeostasis in fragile X syndrome
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The FXG: a presynaptic fragile X granule expressed in a subset of developing brain circuits
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Altered mTOR signaling and enhanced CYFIP2 expression levels in subjects with fragile X syndrome
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Autism genetics: searching for specificity and convergence
Berg, J. M., & Geschwind, D. H. (2012) · Genome Biology · doi:10.1186/gb-2012-13-7-247 · Cited by 192 · see citing works
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Deregulation of <i>EIF4E</i>: a novel mechanism for autism
Neves-Pereira, M., Müller, B., Massie, D., Williams, J. H. G., O’Brien, P. C. M., Hughes, A., Shen, S.-B., Clair, D. S., & Miedzybrodzka, Z. (2009) · Journal of Medical Genetics · doi:10.1136/jmg.2009.066852 · Cited by 142 · see citing works
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Self-citationSantini, E., & Klann, E. (2014) · Science Signaling · doi:10.1126/scisignal.2005832 · Cited by 118 · see citing works
Wagnon, J. L., Briese, M., Sun, W., Mahaffey, C. L., Curk, T., Rot, G., Ule, J., & Frankel, W. N. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1003067 · Cited by 125 · see citing works
Davenport, E. C., Szulc, B. R., Drew, J., Taylor, J., Morgan, T., Higgs, N. F., López-Doménech, G., & Kittler, J. T. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.01.092 · Cited by 125 · see citing works
New perspectives on the biology of fragile X syndrome
Wang, T., Bray, S. M., & Warren, S. T. (2012) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2012.02.002 · Cited by 116 · see citing works
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The Fragile X mental retardation protein regulates matrix metalloproteinase 9 mRNA at synapses.
Janusz, A., Miłek, J., Perycz, M., Pacini, L., Bagni, C., Kaczmarek, L., & Dziembowska, M. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.2207-13.2013 · Cited by 112 · see citing works
Self-citationCYFIP family proteins between autism and intellectual disability: links with Fragile X syndrome
Abekhoukh, S., & Bardoni, B. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00081 · Cited by 110 · see citing works
Therapeutic Strategies in Fragile X Syndrome: From Bench to Bedside and Back
Gross, C., Hoffmann, A., Bassell, G. J., & Berry-Kravis, E. M. (2015) · Neurotherapeutics · doi:10.1007/s13311-015-0355-9 · Cited by 105 · see citing works
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The Role of DNA Copy Number Variation in Schizophrenia
Tam, G. W. C., Redon, R., Carter, N. P., & Grant, S. G. N. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.07.027 · Cited by 98 · see citing works
Postsynaptic localization of PSD-95 is regulated by all three pathways downstream of TrkB signaling
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FMR1 premutation and full mutation molecular mechanisms related to autism
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Dendritic spine actin cytoskeleton in autism spectrum disorder
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Abekhoukh, S., Sahin, H. B., Grossi, M., Zongaro, S., Maurin, T., Madrigal, I., Kazue-Sugioka, D., Raas-Rothschild, A., Doulazmi, M., Carrera, P., et al. (2017) · Disease Models & Mechanisms · doi:10.1242/dmm.025809 · Cited by 59 · see citing works
“It was reported that BDNF regulates translation by causing release of CYFIP1 from eIF4E via the action of MAP kinase interacting serine/threonine kinase 1 (MNK1) (Napoli et al., 2008; Panja et al., 2014).”
InfluentialSpatiotemporally resolved protein synthesis as a molecular framework for memory consolidation
Shrestha, P., & Klann, E. (2022) · Trends in Neurosciences · doi:10.1016/j.tins.2022.01.004 · Cited by 54 · see citing works
Hyperexcitability and homeostasis in fragile X Syndrome.
Liu, X., Kumar, V., Tsai, N.-P., & Auerbach, B. D. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.805929 · Cited by 53 · see citing works
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Self-citationDefects in translational regulation contributing to human cognitive and behavioral disease
Darnell, J. (2011) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2011.05.002 · Cited by 43 · see citing works
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Reduced Complexity Cross Design for Behavioral Genetics
Bryant, C. D., Ferris, M. T., De Villena, F. P. M., Damaj, M. I., Kumar, V., & Mulligan, M. K. (2018) · Molecular-Genetic and Statistical Techniques for Behavioral and Neural Research · doi:10.1016/b978-0-12-804078-2.00008-8 · Cited by 24 · see citing works
15q11.2 microdeletion and FMR1 premutation in a family with intellectual disabilities and autism
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The WAVE complex in developmental and adulthood brain disorders
Kim, H.-G., Berdasco, C., Nairn, A. C., & Kim, Y. (2025) · Experimental & Molecular Medicine · doi:10.1038/s12276-024-01386-w · Cited by 8 · see citing works
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“Cytoplasmic FMRP - interacting protein 1 ( CYFIP1 ) is a gene with clinical associations with schizophrenia, ASDs, epilepsy, ADHD, and neurodevelopmental delay (15).”
CYFIP1 governs the development of cortical axons by modulating calcium availability
Ricci, C., Midroit, M. J., Caicci, F., Achsel, T., Domínguez-Iturza, N., & Bagni, C. (2025) · Nature Communications · doi:10.1038/s41467-025-65801-0 · Cited by 1 · see citing works
“In its alternative role, CYFIP1 binds FMRP and eIF4E repressing translation of target mRNAs 21 – 23 .”
InfluentialSelf-citation
- Authors
- Napoli, I., Mercaldo, V., Boyl, P. P., Eleuteri, B., Zalfa, F., De Rubeis, S., Di Marino, D., Mohr, E., Massimi, M., Falconi, M., Witke, W., Costa-Mattioli, M., Sonenberg, N., Achsel, T., & Bagni, C.
- Affiliations
- University of Rome Tor Vergata (IT)
- Fondazione Santa Lucia (IT)
- KU Leuven (BE)
- University Medical Center Hamburg-Eppendorf (DE)
- European Molecular Biology Laboratory (IT)
- McGill University (CA)
- Corresponding author
- Bagni, Claudia
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2008-09
- Volume
- 134
- Issue
- 6
- Pages
- 1042-1054
- ISSN
- 0092-8674 (ISSN-L)
- OpenAlex
- W2062535336
- Cited by
- 609
- References
- 66
- Citations by year
- 2026: 8 · 2025: 28 · 2024: 29 · 2023: 26 · 2022: 31 · 2021: 30 · 2020: 44 · 2019: 34 · 2018: 34 · 2017: 33 · 2016: 40 · 2015: 40 · 2014: 46 · 2013: 46 · 2012: 43
- FWCI
- 18.24
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 1780 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Lirias (submittedVersion, other-oa)
- Cineca Institutional Research Information System (Tor Vergata University) (submittedVersion)
- eScholarship@McGill (McGill) (submittedVersion, cc-by-nc-nd)
- Università Politecnica delle Marche (Università Politecnica delle Marche) (submittedVersion)
- Funders
- Vlaamse regering
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- fragile X syndrome, FMRP, CYFIP1, 4E-BP, eIF4E, protein synthesis inhibition, dendritic translation, synaptic plasticity, brain-derived neurotrophic factor, DHPG, translation initiation, neurons
- MeSH terms
- Amino Acid Sequence, Animals, Brain, Cells, Cultured, Mice, Inbred C57BL, Models, Molecular, Molecular Sequence Data, Nerve Tissue Proteins, Neurons, Synapses, Protein Biosynthesis, Sequence Alignment, Mice, Knockout, Eukaryotic Initiation Factor-4E, Adaptor Proteins, Signal Transducing, Mice, Fragile X Messenger Ribonucleoprotein 1
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