Postsynaptic BDNF‐TrkB signaling in synapse maturation, plasticity, and disease

Yoshii, Akira; Constantine‐Paton, Martha

doi:10.1002/dneu.20765

Cited by 744Nerve injury and regenerationNeuroscience and Neuropharmacology ResearchGenetics and Neurodevelopmental Disorders

Postsynaptic BDNF‐TrkB signaling in synapse maturation, plasticity, and disease

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Yoshii, Akira, Constantine‐Paton, Martha·2010·Developmental Neurobiology

DOI 10.1002/dneu.20765PMC PMC2923204

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Abstract

Brain-derived neurotrophic factor (BDNF) is a prototypic neurotrophin that regulates diverse developmental events from the selection of neural progenitors to the terminal dendritic differentiation and connectivity of neurons. We focus here on activity-dependent synaptic regulation by BDNF and its receptor, full length TrkB. BDNF-TrkB signaling is involved in transcription, translation, and trafficking of proteins during various phases of synaptic development and has been implicated in several forms of synaptic plasticity. These functions are carried out by a combination of the three signaling cascades triggered when BDNF binds TrkB: The mitogen-activated protein kinase (MAPK), the phospholipase Cgamma (PLC PLCgamma), and the phosphatidylinositol 3-kinase (PI3K) pathways. MAPK and PI3K play crucial roles in both translation and/or trafficking of proteins induced by synaptic activity, whereas PLCgamma regulates intracellular Ca(2+) that can drive transcription via cyclic AMP and a protein kinase C. Conversely, the abnormal regulation of BDNF is implicated in various developmental and neurodegenerative diseases that perturb neural development and function. We will discuss the current state of understanding BDNF signaling in the context of synaptic development and plasticity with a focus on the postsynaptic cell and close with the evidence that basic mechanisms of BDNF function still need to be understood to effectively treat genetic disruptions of these pathways that cause devastating neurodevelopmental diseases.

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Local consolidation is coupled to long-range stabilization through TrkB signaling endosomes that traffic to the soma and engage CREB and mTOR-dependent transcription.
“Local consolidation is coupled to long-range stabilization through TrkB signaling endosomes that traffic to the soma and engage CREB and mTOR-dependent transcription [106,109,112].”
From Synaptic Plasticity—Intrinsic Excitability and Antidepressant Discovery (2026) · cites this paper as [112]
The Regulation of BDNF/TrkB Signaling Pathway section (page not provided) links TrkB signaling to CREB-mediated transcription and mTOR-dependent protein translation. The Synaptic Tagging section describes local BDNF stimulation affecting PSD-95 trafficking across dendrites, but our copy does not describe TrkB signaling endosomes traveling to the soma or engaging CREB and mTOR-dependent transcription there. (LLM, conf=0.86)
Experimental — accuracy not yet measured
Upon BDNF-TrkB binding, the complex is internalized into the neuron and serves as a docking site for signaling cascades, protein phosphorylation cascades, and secondary signaling systems.
“Upon binding, the BDNF-TrkB complex is then internalized into the neuron and serves as a docking site for numerous signaling cascades, protein phosphorylation cascades, and secondary signaling systems (Huang and Reichardt, 2003; Nykjaer et al., 2005; Yoshii and Constantine-Paton, 2010; for review of signaling pathways see Phillips et al., 2014).”
From Exercise-Mediated Neurogenesis in the Hippocampus via BDNF (2018) · cites this paper as Yoshii and Constantine-Paton, 2010
The Regulation of BDNF / TrkB Signaling Pathway section (page not supplied) says ligand binding phosphorylates intracellular TrkB domains and triggers MAPK, PI3K, and PLCγ cascades; its PLCγ subsection describes recruitment at a phosphorylated TrkB site. The passages do not establish that the BDNF–TrkB complex is internalized or that an internalized complex serves as the docking site. (LLM, conf=0.85)
Experimental — accuracy not yet measured
Activity of receptor tyrosine kinases, metabotropic glutamic receptors and NMDA receptors leads to activation of PI3K/AKT and RAS/ERK signaling pathways, and thereby influences synaptic plasticity by mediating expression and trafficking of AMPA receptors in excitatory synapses and controlling LTD and LTP responses.
“Activity of receptor tyrosine kinases, metabotropic glutamic receptors and NMDA receptors lead to the activation of PI3K/AKT and RAS/ERK signaling pathways [185, 189], and thereby influence synaptic plasticity by mediating expression and trafficking of AMPA receptors in excitatory synapses and controlling long-term depression (LTD) and long-term potentiation (LTP) responses [188–190].”
From The ASD Living Biology: from cell proliferation to clinical phenotype (2019) · cites this paper as [185]
PI3K/AKT, RAS/ERK, WNT and β-catenin pathways control soma size, dendritic arborization, axon generation, spine development and synapse function.
“These pathways control soma size, dendritic arborization, axon generation, spine development and synapse function [184–188].”
From The ASD Living Biology: from cell proliferation to clinical phenotype (2019) · cites this paper as [185]
D1 receptor- and BDNF-mediated pathways interact in the activation of ERK1/2.
“Experimental results suggest that D1 receptor- and BDNF-mediated pathways interact in the activation of extracellular-signal regulated kinase (ERK) 1/2 [mitogen activated kinase (MAPK)] activity [87].”
From A neoHebbian framework for episodic memory; role of dopamine-dependent late LTP (2011) · cites this paper as [87]

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The Role of Brain-Derived Neurotrophic Factor Receptors in the Mature Hippocampus: Modulation of Long-Term Potentiation through a Presynaptic Mechanism involving TrkB
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Inhibition of GABAASynaptic Responses by Brain-Derived Neurotrophic Factor (BDNF) in Rat Hippocampus
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“…evidence suggests that BDNF facilitates activity of glutamatergic synapses and is crucial for the maintenance of L-LTP but BDNF does not, by itself, induce L-LTP (Figurov et al., 1996; Patterson et al., 1996; Tanaka et al., 1997; Frerking et al., 1998; Gottschalk et al., 1998; Huber et al., 1998).”
The Neuronal Rho-GEF Kalirin-7 Interacts with PDZ Domain–Containing Proteins and Regulates Dendritic Morphogenesis
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Virus-mediated gene transfer into hippocampal CA1 region restores long-term potentiation in brain-derived neurotrophic factor mutant mice.
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BDNF Induces Transport of PSD-95 to Dendrites Through PI3K-AKT Signaling After NMDA Receptor Activation
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Activation of PI3-Kinase Is Required for AMPA Receptor Insertion during LTP of mEPSCs in Cultured Hippocampal Neurons
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Postsynaptic Density-95 Mimics and Occludes Hippocampal Long-Term Potentiation and Enhances Long-Term Depression
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Some Forms of cAMP-Mediated Long-Lasting Potentiation Are Associated with Release of BDNF and Nuclear Translocation of Phospho-MAP Kinase
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Gene Expression Profiling of Facilitated L-LTP in VP16-CREB Mice Reveals that BDNF Is Critical for the Maintenance of LTP and Its Synaptic Capture
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Cyclic AMP controls BDNF-induced TrkB phosphorylation and dendritic spine formation in mature hippocampal neurons
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PSD‐95 regulates synaptic transmission and plasticity in rat cerebral cortex
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The induction of LTP increases BDNF and NGF mRNA but decreases NT-3 mRNA in the dentate gyrus
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Blockade of Endogenous Ligands of TrkB Inhibits Formation of Ocular Dominance Columns
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Evidence for a Relationship Between Genetic Variants at the Brain-Derived Neurotrophic Factor (BDNF) Locus and Major Depression
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Conditional Deletion of TrkB but Not BDNF Prevents Epileptogenesis in the Kindling Model
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MeCP2 dysfunction in Rett syndrome and related disorders
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The p75 neurotrophin receptor negatively modulates dendrite complexity and spine density in hippocampal neurons
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Presynaptic Modulation of Synaptic Transmission and Plasticity by Brain-Derived Neurotrophic Factor in the Developing Hippocampus
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Miniature synaptic transmission and BDNF modulate dendritic spine growth and form in rat CA1 neurones
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t Brain-Derived Neurotrophic Factor Overexpression Induces Precocious Critical Period in Mouse Visual Cortex
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A Chemical-Genetic Approach to Studying Neurotrophin Signaling
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Relative Contribution of Endogenous Neurotrophins in Hippocampal Long-Term Potentiation
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Acute Intrahippocampal Infusion of BDNF Induces Lasting Potentiation of Synaptic Transmission in the Rat Dentate Gyrus
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Brain-Derived Neurotrophic Factor (BDNF) Modulates Inhibitory, But Not Excitatory, Transmission in the CA1 Region of the Hippocampus
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Brain-Derived Neurotrophic Factor Modulation of GABAergic Synapses by Postsynaptic Regulation of Chloride Transport
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Synaptic Tagging and Cross-Tagging: The Role of Protein Kinase M in Maintaining Long-Term Potentiation But Not Long-Term Depression
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Multiple functions of precursor BDNF to CNS neurons: negative regulation of neurite growth, spine formation and cell survival
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Brain-derived neurotrophic factor restores synaptic plasticity in a knock-in mouse model of Huntington's disease
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The neurotrophin receptor p75 NTR modulates long-term depression and regulates the expression of AMPA receptor subunits in the hippocampus
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TrkB Signaling Modulates Spine Density and Morphology Independent of Dendrite Structure in Cultured Neonatal Purkinje Cells
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Brain-derived neurotrophic factor expression after long-term potentiation
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Hippocampal Long-Term Potentiation Is Supported by Presynaptic and Postsynaptic Tyrosine Receptor Kinase B-Mediated Phospholipase Cγ Signaling
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Brain-Derived Neurotrophic Factor Causes cAMP Response Element-Binding Protein Phosphorylation in Absence of Calcium Increases in Slices and Cultured Neurons from Rat Visual Cortex
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Eye opening induces a rapid dendritic localization of PSD-95 in central visual neurons
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Brain-derived neurotrophic factor variants are associated with childhood-onset mood disorder: confirmation in a Hungarian sample
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Functional trkB neurotrophin receptors are intrinsic components of the adult brain postsynaptic density
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Brain-derived neurotrophic factor alters the synaptic modification threshold in visual cortex
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Mutation at the TrkB PLCγ-docking site affects hippocampal LTP and associative learning in conscious micePreprint
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The Dynamic Distribution of TrkB Receptors before, during, and after Synapse Formation between Cortical Neurons
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TrkB kinase is required for recovery, but not loss, of cortical responses following monocular deprivation
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BDNF increases synapse density in dendrites of developing tectal neurons in vivo
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Postsynaptic TrkB signaling has distinct roles in spine maintenance in adult visual cortex and hippocampus
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Endogenous Brain-Derived Neurotrophic Factor Triggers Fast Calcium Transients at Synapses in Developing Dendrites
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Brain-Derived Neurotrophic Factor Prevents Low-Frequency Inputs from Inducing Long-Term Depression in the Developing Visual Cortex
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Monocular deprivation decreases brain-derived neurotrophic factor immunoreactivity in the rat visual cortex
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Differential effects of neurotrophins on ocular dominance plasticity in developing and adult cat visual cortex
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Long-Term Potentiation in the Juvenile Superior Colliculus Requires Simultaneous Activation of NMDA Receptors and L-type Ca2+ Channels and Reflects Addition of Newly Functional Synapses
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NMDA receptor activation induces differential epigenetic modification of Bdnf promoters in hippocampal neurons
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Effects of dark rearing on phosphorylation of neurotrophin Trk receptors
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Authors: Yoshii, A., & Constantine‐Paton, M.
Affiliations: McGovern Institute for Brain Research (US)
Corresponding author: Constantine‐Paton, Martha
ORCID: Yoshii, Akira
Venue: Developmental Neurobiology
Publisher: Wiley
Published: 2010-02-22
Volume: 70
Issue: 5
Pages: 304-322
ISSN: 1932-8451 (ISSN-L)
1932-846X
DOI: 10.1002/dneu.20765
PMC: PMC2923204
OpenAlex: W1536780881
Cited by: 744
References: 125
Citations by year: 2026: 46 · 2025: 33 · 2024: 36 · 2023: 39 · 2022: 59 · 2021: 46 · 2020: 60 · 2019: 64 · 2018: 55 · 2017: 50 · 2016: 50 · 2015: 41 · 2014: 38 · 2013: 47 · 2012: 38
FWCI: 3.63
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Developmental Neurobiology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc-sa)
PubMed Central
Funders: National Institutes of Health (5r01ey014074-21)
National Eye Institute (R01-EY014074, R01EY006039)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nerve injury and regeneration
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
Keywords: brain-derived neurotrophic factor, TrkB receptor, postsynaptic signaling, synapse maturation, synaptic plasticity, MAPK signaling, PLCγ signaling, PI3K signaling, intracellular calcium, mRNA translation, protein trafficking, neurodevelopmental disorders, neurodegenerative diseases, neural development
MeSH terms: Animals, Developmental Disabilities, Humans, Models, Neurological, Nervous System Diseases, Neurons, Synapses, Brain-Derived Neurotrophic Factor, Receptor, trkB

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Postsynaptic BDNF‐TrkB signaling in synapse maturation, plasticity, and disease

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