Pharmacogenetic inhibition of eIF4E-dependent Mmp9 mRNA translation reverses fragile X syndrome-like phenotypes
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Fragile X syndrome (FXS) is the leading genetic cause of autism. Mutations in Fmr1 (fragile X mental retardation 1 gene) engender exaggerated translation resulting in dendritic spine dysmorphogenesis, synaptic plasticity alterations, and behavioral deficits in mice, which are reminiscent of FXS phenotypes. Using postmortem brains from FXS patients and Fmr1 knockout mice (Fmr1(-/y)), we show that phosphorylation of the mRNA 5' cap binding protein, eukaryotic initiation factor 4E (eIF4E), is elevated concomitant with increased expression of matrix metalloproteinase 9 (MMP-9) protein. Genetic or pharmacological reduction of eIF4E phosphorylation rescued core behavioral deficits, synaptic plasticity alterations, and dendritic spine morphology defects via reducing exaggerated translation of Mmp9 mRNA in Fmr1(-/y) mice, whereas MMP-9 overexpression produced several FXS-like phenotypes. These results uncover a mechanism of regulation of synaptic function by translational control of Mmp-9 in FXS, which opens the possibility of new treatment avenues for the diverse neurological and psychiatric aspects of FXS.
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MMP-9 is elevated in the cortex and hippocampus of both humans with Fragile X Syndrome and Fmr1 knockout mice.
“MMP-9 is elevated in the cortex and hippocampus of both humans with FXS and Fmr1 KO mice (Sidhu et al., 2014; Gkogkas et al., 2014).”
From Matrix metalloproteinase-9 deletion rescues auditory evoked potential habituation deficit in a mouse model of Fragile X Syndrome (2016) · cites this paper as Gkogkas et al., 2014
MMP-9 levels are high in cortex and hippocampus of humans with FXS and Fmr1 KO mice (Sidhu et al., 2014; Gkogkas et al., 2014).
“MMP-9 levels are high in the cortex and hippocampus of humans with FXS and Fmr1 KO mice (Sidhu et al., 2014; Gkogkas et al., 2014).”
From Matrix metalloproteinase-9 deletion rescues auditory evoked potential habituation deficit in a mouse model of Fragile X Syndrome (2016) · cites this paper as Gkogkas et al., 2014
Genetic deletion of MMP-9 rescues several other fragile X syndrome phenotypes, including improper dendritic spine maturation, enhanced mGluR5-dependent long-term depression, abnormal social behavior, and macroorchidism.
“Genetic deletion of MMP-9 rescues several other FXS phenotypes, including improper dendritic spine maturation, enhanced mGluR5-dependent-LTD, abnormal social behavior and macroorchidism (Sidhu et al. 2014)”
From Genetic Reduction of Matrix Metalloproteinase-9 Promotes Formation of Perineuronal Nets Around Parvalbumin-Expressing Interneurons and Normalizes Auditory Cortex Responses in Developing Fmr1 Knock-Out Mice (2018) · cites this paper as Gkogkas et al. 2014
MMP-9 levels are elevated in fragile X syndrome human brains and in the hippocampus of Fmr1 knockout mice.
“MMP-9 levels are elevated in FXS human brains and the hippocampus of Fmr1 KO mice (Dziembowska et al., 2013;Sidhu et al. 2014;Gkogkas et al. 2014).”
From Genetic Reduction of Matrix Metalloproteinase-9 Promotes Formation of Perineuronal Nets Around Parvalbumin-Expressing Interneurons and Normalizes Auditory Cortex Responses in Developing Fmr1 Knock-Out Mice (2018) · cites this paper as Gkogkas et al. 2014
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Self-citation
- Authors
- Gkogkas, C. G., Khoutorsky, A., Cao, R., Jafarnejad, S. M., Prager-Khoutorsky, M., Giannakas, N., Kaminari, A., Fragkouli, A., Nader, K., Price, T. J., Konicek, B. W., Graff, J. R., Tzinia, A. K., Lacaille, J.-C., & Sonenberg, N.
- Affiliations
- McGill University (CA)
- National Centre of Scientific Research "Demokritos" (GR)
- The University of Texas at Dallas (US)
- Eli Lilly (United States) (US)
- Université de Montréal (CA)
- Corresponding author
- Gkogkas, Christos G.
- Sonenberg, Nahum
- ORCID
- Venue
- Cell Reports
- Publisher
- Elsevier BV
- Published
- 2014-12
- Volume
- 9
- Issue
- 5
- Pages
- 1742-1755
- ISSN
- 2211-1247 (ISSN-L)
- PMC
- PMC4294557
- OpenAlex
- W2151299944
- Cited by
- 201
- References
- 50
- Citations by year
- 2026: 5 · 2025: 10 · 2024: 14 · 2023: 15 · 2022: 15 · 2021: 18 · 2020: 21 · 2019: 16 · 2018: 28 · 2017: 22 · 2016: 19 · 2015: 17
- FWCI
- 12.70
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Cell Reports (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion, cc-by-nc-nd)
- PubMed Central (acceptedVersion, cc-by-nc-nd)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- eScholarship@McGill (McGill) (submittedVersion)
- Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, cc-by-nc-nd)
- Research Portal (Queen's University Belfast) (submittedVersion, cc-by-nc-nd)
- Funders
- Eli Lilly and Company
- Fondation Brain Canada
- Wellcome Trust
- Azrieli Foundation
- Canadian Institutes of Health Research (125985_1, MOP-114994), 125985)
- Fonds de Recherche du Québec - Santé
- National Institute of Mental Health (R24MH068855)
- National Institute of Neurological Disorders and Stroke (R01NS065926)
- 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, eIF4E phosphorylation, MMP-9, mRNA translation, translational regulation, FMR1 gene, dendritic spine morphology, synaptic plasticity, autism spectrum disorder, Fmr1 knockout mice, behavioral deficits
- MeSH terms
- Copper-Transporting ATPases, Adenosine Triphosphatases, Animals, Autistic Disorder, Benzofurans, Brain, Cells, Cultured, Enzyme Induction, Female, Fragile X Syndrome, Humans, Male, Mice, Inbred C57BL, Mice, Transgenic, Phenotype, Phosphorylation, Protein Processing, Post-Translational, Protein Biosynthesis, Receptors, Metabotropic Glutamate, Matrix Metalloproteinase 9, Cation Transport Proteins, Eukaryotic Initiation Factor-4E, Dendritic Spines
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