Dysregulated Metabotropic Glutamate Receptor-Dependent Translation of AMPA Receptor and Postsynaptic Density-95 mRNAs at Synapses in a Mouse Model of Fragile X Syndrome

Muddashetty, Ravi S.; Kelić, Sofija; Gross, Christina; Xu, Mei; Bassell, Gary J.

doi:10.1523/jneurosci.0937-07.2007

Cited by 421Genetics and Neurodevelopmental DisordersNeuroscience and Neuropharmacology ResearchRNA and protein synthesis mechanisms

Dysregulated Metabotropic Glutamate Receptor-Dependent Translation of AMPA Receptor and Postsynaptic Density-95 mRNAs at Synapses in a Mouse Model of Fragile X Syndrome

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Muddashetty, Ravi S., Kelić, Sofija, Gross, Christina, Xu, Mei, Bassell, Gary J.·2007·The Journal of Neuroscience

DOI 10.1523/jneurosci.0937-07.2007PMC PMC6672337

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Abstract

Fragile X syndrome, a common form of inherited mental retardation, is caused by the loss of fragile X mental retardation protein (FMRP), an mRNA binding protein that is hypothesized to regulate local mRNA translation in dendrites downstream of gp1 metabotropic glutamate receptors (mGluRs). However, specific FMRP-associated mRNAs that localize to dendrites in vivo and show altered mGluR-dependent translation at synapses of Fmr1 knock-out mice are unknown so far. Using fluorescence in situ hybridization, we discovered that GluR1/2 and postsynaptic density-95 (PSD-95) mRNAs are localized to dendrites of cortical and hippocampal neurons in vivo . Quantitative analyses of their dendritic mRNA levels in cultured neurons and synaptoneurosomes did not detect differences between wild-type and Fmr1 knock-out (KO) mice. In contrast, PSD-95, GluR1/2, and calcium/calmodulin-dependent kinase IIα (CaMKIIα) mRNA levels in actively translating polyribosomes were dysregulated in synaptoneurosomes from Fmr1 knock-out mice in response to mGluR activation. [ 35 S]methionine incorporation into newly synthesized proteins similarly revealed impaired stimulus-induced protein synthesis of CaMKIIα and PSD-95 in synaptoneurosomes from Fmr1 KO mice. Quantitative analysis of mRNA levels in FMRP-specific immunoprecipitations from synaptoneurosomes demonstrated the association of FMRP with CaMKIIα, PSD-95, and GluR1/2 mRNAs. These findings suggest a novel mechanism whereby FMRP regulates the local synthesis AMPA receptor (AMPAR) subunits, PSD-95, and CaMKIIα downstream of mGluR-activation. Dysregulation of local translation of AMPAR and associated factors at synapses may impair control of the molecular composition of the postsynaptic density and consequently alter synaptic transmission, causing impairments of neuronal plasticity observed in Fmr1 knock-out mice and fragile X syndrome.

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FMRP absence in mouse knockout models upregulates mGluR5 and PSD-95 translation.
“The absence of FMRP in mouse knockout models has demonstrated upregulation of mGluR5 and PSD-95 translation [159, 160].”
From Consensus Paper: Pathological Role of the Cerebellum in Autism (2012) · cites this paper as [159]
FMR1 KO usually has subtle or no overt effects on expression of established FMRP target genes.
“given that FMR1 KO usually has subtle or no overt effects even on expression of “established” FMRP target genes (Bassell and Warren, 2008; Darnell et al., 2005b; Muddashetty et al., 2007).”
From Regulation of Synaptic Structure and Function by FMRP-Associated MicroRNAs miR-125b and miR-132 (2010) · cites this paper as Muddashetty et al., 2007

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Authors: Muddashetty, R. S., Kelić, S., Gross, C., Xu, M., & Bassell, G. J.
Affiliations: Emory University (US)
ORCID: Muddashetty, Ravi S.
Gross, Christina
Xu, Mei
Bassell, Gary J.
Venue: The Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 2007-05-16
Volume: 27
Issue: 20
Pages: 5338-5348
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.0937-07.2007
PMC: PMC6672337
OpenAlex: W1968311418
Cited by: 421
References: 64
Citations by year: 2026: 4 · 2025: 9 · 2024: 8 · 2023: 10 · 2022: 11 · 2021: 16 · 2020: 17 · 2019: 21 · 2018: 20 · 2017: 21 · 2016: 15 · 2015: 26 · 2014: 22 · 2013: 36 · 2012: 45
FWCI: 15.59
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-sa
creativecommons.org/licenses/by-nc-sa/4.0/ (vor, 184 d)
Locations: Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Digital Commons - PCOM (Philadelphia College of Osteopathic Medicine) (submittedVersion)
Journal of Neuroscience Nursing
Funders: Dana Foundation
Emory University
National Institutes of Health (1r01ns039641-01a1)
National Institute of Neurological Disorders and Stroke (NS39641, T32NS007480)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
Keywords: fragile X syndrome, FMRP, metabotropic glutamate receptors, AMPA receptors, PSD-95, CaMKIIα, dendritic mRNA localization, synaptoneurosomes, Fmr1 knockout mice, postsynaptic density, synaptic plasticity, neuroplasticity
MeSH terms: Disks Large Homolog 4 Protein, Animals, Disease Models, Animal, Fragile X Syndrome, Membrane Proteins, Mice, Inbred C57BL, Synapses, Receptors, AMPA, Mice, Knockout, Intracellular Signaling Peptides and Proteins, Mice, Guanylate Kinases, Fragile X Messenger Ribonucleoprotein 1

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Dysregulated Metabotropic Glutamate Receptor-Dependent Translation of AMPA Receptor and Postsynaptic Density-95 mRNAs at Synapses in a Mouse Model of Fragile X Syndrome

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