Cited by 120Neuroscience and Neuropharmacology ResearchGenetics and Neurodevelopmental DisordersTreatment of Major Depression

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Brain-Derived Neurotrophic Factor Activation of CaM-Kinase Kinase via Transient Receptor Potential Canonical Channels Induces the Translation and Synaptic Incorporation of GluA1-Containing Calcium-Permeable AMPA Receptors

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Fortin, D. A., Srivastava, T., Dwarakanath, D., Pierre, P., Nygaard, S., Derkach, V. A., Soderling, T. R.·2012·Journal of Neuroscience

DOI 10.1523/jneurosci.6034-11.2012PMC PMC3390208

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Abstract

Glutamatergic synapses in early postnatal development transiently express calcium-permeable AMPA receptors (CP-AMPARs). Although these GluA2-lacking receptors are essential and are elevated in response to brain-derived neurotrophic factor (BDNF), little is known regarding molecular mechanisms that govern their expression and synaptic insertion. Here we show that BDNF-induced GluA1 translation in rat primary hippocampal neurons requires the activation of mammalian target of rapamycin (mTOR) via calcium calmodulin-dependent protein kinase kinase (CaMKK). Specifically, BDNF-mediated phosphorylation of threonine 308 (T308) in AKT, a known substrate of CaMKK and an upstream activator of mTOR-dependent translation, was prevented by (1) pharmacological inhibition of CaMKK with STO-609, (2) overexpression of a dominant-negative CaMKK, or (3) short hairpin-mediated knockdown of CaMKK. GluA1 surface expression induced by BDNF, as assessed by immunocytochemistry using an extracellular N-terminal GluA1 antibody or by surface biotinylation, was impaired following knockdown of CaMKK or treatment with STO-609. Activation of CaMKK by BDNF requires transient receptor potential canonical (TRPC) channels as SKF-96365, but not the NMDA receptor antagonist d-APV, prevented BDNF-induced GluA1 surface expression as well as phosphorylation of CaMKI, AKT(T308), and mTOR. Using siRNA we confirmed the involvement of TRPC5 and TRPC6 subunits in BDNF-induced AKT(T308) phosphorylation. The BDNF-induced increase in mEPSC was blocked by IEM-1460, a selected antagonist of CP-AMPARs, as well as by the specific repression of acute GluA1 translation via siRNA to GluA1 but not GluA2. Together these data support the conclusion that newly synthesized GluA1 subunits, induced by BDNF, are readily incorporated into synapses where they enhance the expression of CP-AMPARs and synaptic strength.

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Authors: Fortin, D. A., Srivastava, T., Dwarakanath, D., Pierre, P., Nygaard, S., Derkach, V. A., & Soderling, T. R.
Affiliations: Oregon Health & Science University (US)
Aix-Marseille Université (FR)
Corresponding author: Fortin, D. A.
ORCID: Pierre, P.
Nygaard, S.
Venue: Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 2012-06-13
Volume: 32
Issue: 24
Pages: 8127-8137
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.6034-11.2012
PMC: PMC3390208
OpenAlex: W1965868120
Cited by: 120
References: 87
Citations by year: 2026: 5 · 2025: 3 · 2024: 2 · 2023: 8 · 2022: 10 · 2021: 9 · 2020: 7 · 2019: 2 · 2018: 9 · 2017: 12 · 2016: 8 · 2015: 8 · 2014: 15 · 2013: 19 · 2012: 3
FWCI: 5.93
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Journal of Neuroscience (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute of Neurological Disorders and Stroke (R01NS027037, NS027037)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
Health Sciences › Medicine › Pharmacology (medical) › Treatment of Major Depression
Keywords: brain-derived neurotrophic factor, calcium-permeable AMPA receptors, CaMKK, mTOR signaling, Akt phosphorylation, TRPC5, TRPC6, TRPC channels, glutamatergic synapses, hippocampal neurons, STO-609
MeSH terms: Adamantane, Animals, Benzimidazoles, Calcium Channel Blockers, Enzyme Inhibitors, Female, Hippocampus, Imidazoles, Male, Neurons, 2-Amino-5-phosphonovalerate, Rats, Sprague-Dawley, Receptors, AMPA, Excitatory Amino Acid Antagonists, Brain-Derived Neurotrophic Factor, RNA, Small Interfering, TRPC Cation Channels, Rats, Naphthalimides, Calcium-Calmodulin-Dependent Protein Kinase Kinase, Miniature Postsynaptic Potentials, Gene Knockdown Techniques, TOR Serine-Threonine Kinases, Primary Cell Culture

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Brain-Derived Neurotrophic Factor Activation of CaM-Kinase Kinase via Transient Receptor Potential Canonical Channels Induces the Translation and Synaptic Incorporation of GluA1-Containing Calcium-Permeable AMPA Receptors

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