Metabotropic action of postsynaptic kainate receptors triggers hippocampal long-term potentiation

Milos Petrovic; Silvia Viana da Silva; James P Clement; Ladislav Vyklicky; Christopher Mulle; Maria Inmaculada Gonzalez; Jeremy M Henley

doi:10.1038/nn.4505

Metabotropic action of postsynaptic kainate receptors triggers hippocampal long-term potentiation

Milos Petrovic, Silvia Viana da Silva, James P Clement, Ladislav Vyklicky, Christopher Mulle, Maria Inmaculada Gonzalez, Jeremy M Henley

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Abstract

Long-term potentiation (LTP) in the rat hippocampus is the most extensively studied cellular model for learning and memory. Induction of classical LTP involves an NMDA-receptor- and calcium-dependent increase in functional synaptic AMPA receptors, mediated by enhanced recycling of internalized AMPA receptors back to the postsynaptic membrane. Here we report a physiologically relevant NMDA-receptor-independent mechanism that drives increased AMPA receptor recycling and LTP. This pathway requires the metabotropic action of kainate receptors and activation of G protein, protein kinase C and phospholipase C. Like classical LTP, kainate-receptor-dependent LTP recruits recycling endosomes to spines, enhances synaptic recycling of AMPA receptors to increase their surface expression and elicits structural changes in spines, including increased growth and maturation. These data reveal a new and, to our knowledge, previously unsuspected role for postsynaptic kainate receptors in the induction of functional and structural plasticity in the hippocampus.

Original language	English
Pages (from-to)	529–539
Number of pages	11
Journal	Nature Neuroscience
Volume	20
Issue number	4
Early online date	13 Feb 2017
DOIs	https://doi.org/10.1038/nn.4505
Publication status	Published - Apr 2017

Keywords

Hippocampus
Long-term potentiation
Membrane proteins

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10.1038/nn.4505

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Roles of protein SUMOylation in AMPA receptor trafficking, synaptic dysfunction and cognitive impairment in dementia
Henley, J. M.
1/03/14 → 30/06/18
Project: Research
PROTEIN INTERACTIONS AND POST TRANSATIONAL MODIFICATION IN THE TRAFFICKING OF NEURONAL KAINATE RECEPTORS
Henley, J. M.
1/01/08 → 1/10/11
Project: Research

Wolfson Bioimaging Facility
Mark Jepson (Manager)
Faculty of Life Sciences
Facility/equipment: Facility

Professor Jeremy M Henley
- J.M.Henleybristol.acuk
- School of Biochemistry - Professor of Molecular Neuroscience
- Dynamic Cell Biology
- Bristol Neuroscience
Person: Academic , Member

Cite this

@article{235552d1be1a472897b40e4441da5ec0,

title = "Metabotropic action of postsynaptic kainate receptors triggers hippocampal long-term potentiation",

abstract = "Long-term potentiation (LTP) in the rat hippocampus is the most extensively studied cellular model for learning and memory. Induction of classical LTP involves an NMDA-receptor- and calcium-dependent increase in functional synaptic AMPA receptors, mediated by enhanced recycling of internalized AMPA receptors back to the postsynaptic membrane. Here we report a physiologically relevant NMDA-receptor-independent mechanism that drives increased AMPA receptor recycling and LTP. This pathway requires the metabotropic action of kainate receptors and activation of G protein, protein kinase C and phospholipase C. Like classical LTP, kainate-receptor-dependent LTP recruits recycling endosomes to spines, enhances synaptic recycling of AMPA receptors to increase their surface expression and elicits structural changes in spines, including increased growth and maturation. These data reveal a new and, to our knowledge, previously unsuspected role for postsynaptic kainate receptors in the induction of functional and structural plasticity in the hippocampus.",

keywords = "Hippocampus, Long-term potentiation, Membrane proteins",

author = "Milos Petrovic and Silva, {Silvia Viana da} and Clement, {James P} and Ladislav Vyklicky and Christopher Mulle and Gonzalez, {Maria Inmaculada} and Henley, {Jeremy M}",

year = "2017",

month = apr,

doi = "10.1038/nn.4505",

language = "English",

volume = "20",

pages = "529–539",

journal = "Nature Neuroscience",

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T1 - Metabotropic action of postsynaptic kainate receptors triggers hippocampal long-term potentiation

AU - Petrovic, Milos

AU - Silva, Silvia Viana da

AU - Clement, James P

AU - Vyklicky, Ladislav

AU - Mulle, Christopher

AU - Gonzalez, Maria Inmaculada

AU - Henley, Jeremy M

PY - 2017/4

Y1 - 2017/4

N2 - Long-term potentiation (LTP) in the rat hippocampus is the most extensively studied cellular model for learning and memory. Induction of classical LTP involves an NMDA-receptor- and calcium-dependent increase in functional synaptic AMPA receptors, mediated by enhanced recycling of internalized AMPA receptors back to the postsynaptic membrane. Here we report a physiologically relevant NMDA-receptor-independent mechanism that drives increased AMPA receptor recycling and LTP. This pathway requires the metabotropic action of kainate receptors and activation of G protein, protein kinase C and phospholipase C. Like classical LTP, kainate-receptor-dependent LTP recruits recycling endosomes to spines, enhances synaptic recycling of AMPA receptors to increase their surface expression and elicits structural changes in spines, including increased growth and maturation. These data reveal a new and, to our knowledge, previously unsuspected role for postsynaptic kainate receptors in the induction of functional and structural plasticity in the hippocampus.

AB - Long-term potentiation (LTP) in the rat hippocampus is the most extensively studied cellular model for learning and memory. Induction of classical LTP involves an NMDA-receptor- and calcium-dependent increase in functional synaptic AMPA receptors, mediated by enhanced recycling of internalized AMPA receptors back to the postsynaptic membrane. Here we report a physiologically relevant NMDA-receptor-independent mechanism that drives increased AMPA receptor recycling and LTP. This pathway requires the metabotropic action of kainate receptors and activation of G protein, protein kinase C and phospholipase C. Like classical LTP, kainate-receptor-dependent LTP recruits recycling endosomes to spines, enhances synaptic recycling of AMPA receptors to increase their surface expression and elicits structural changes in spines, including increased growth and maturation. These data reveal a new and, to our knowledge, previously unsuspected role for postsynaptic kainate receptors in the induction of functional and structural plasticity in the hippocampus.

KW - Hippocampus

KW - Long-term potentiation

KW - Membrane proteins

U2 - 10.1038/nn.4505

DO - 10.1038/nn.4505

M3 - Article (Academic Journal)

C2 - 28192396

SN - 1097-6256

VL - 20

SP - 529

EP - 539

JO - Nature Neuroscience

JF - Nature Neuroscience

IS - 4

ER -

Metabotropic action of postsynaptic kainate receptors triggers hippocampal long-term potentiation

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Roles of protein SUMOylation in AMPA receptor trafficking, synaptic dysfunction and cognitive impairment in dementia

PROTEIN INTERACTIONS AND POST TRANSATIONAL MODIFICATION IN THE TRAFFICKING OF NEURONAL KAINATE RECEPTORS

Equipment

Wolfson Bioimaging Facility

Profiles

Professor Jeremy M Henley

Cite this