Activation of the TRPC1 cation channel by metabotropic glutamate receptor mGluR1

Sang Jeong Kim, Yu Shin Kim, Joseph P. Yuan, Ronald S. Petralia, Paul F. Worley, David J. Linden

Research output: Contribution to journalArticleResearchpeer-review

272 Citations (Scopus)

Abstract

Group I metabotropic glutamate receptors (consisting of mGluR1 and mGluR5) are G-protein-coupled neurotransmitter receptors that are found in the perisynaptic region of the postsynaptic membrane. These receptors are not activated by single synaptic volleys but rather require bursts of activity. They are implicated in many forms of neural plasticity including hippocampal long-term potentiation and depressions, cerebellar long-term depression, associative learning, and cocaine addiction. When activated, group I mGluRs engage two G-protein-dependent signalling mechanisms: stimulation of phospholipase C and activation of an unidentified, mixed-cation excitatory postsynaptic conductance (EPSC), displaying slow activation, in the plasma membrane. Here we report that the mGluR1-evoked slow EPSC is mediated by the TRPC1 cation channel. TRPC1 is expressed in perisynaptic regions of the cerebellar parallel fibre-Purkinje cell synapse and is physically associated with mGluR1. Manipulations that interfere with TRPC1 block the mGluR1-evoked slow EPSC in Purkinje cells; however, fast transmission mediated by AMPA-type glutamate receptors remains unaffected. Furthermore, co-expression of mGluR1 and TRPC1 in a heterologous system reconstituted a mGluR1-evoked conductance that closely resembles the slow EPSC in Purkinje cells.

Original languageEnglish
Pages (from-to)285-291
Number of pages7
JournalNature
Volume426
Issue number6964
DOIs
StatePublished - 20 Nov 2003

Fingerprint

Metabotropic Glutamate Receptors
Cations
Purkinje Cells
Metabotropic Glutamate 5 Receptor
Depression
Cocaine-Related Disorders
Neurotransmitter Receptor
Neuronal Plasticity
AMPA Receptors
Long-Term Potentiation
Glutamate Receptors
Type C Phospholipases
G-Protein-Coupled Receptors
GTP-Binding Proteins
Synapses
metabotropic glutamate receptor type 1
Cell Membrane
Learning
Membranes

Cite this

Kim, S. J., Kim, Y. S., Yuan, J. P., Petralia, R. S., Worley, P. F., & Linden, D. J. (2003). Activation of the TRPC1 cation channel by metabotropic glutamate receptor mGluR1. Nature, 426(6964), 285-291. https://doi.org/10.1038/nature02162
Kim, Sang Jeong ; Kim, Yu Shin ; Yuan, Joseph P. ; Petralia, Ronald S. ; Worley, Paul F. ; Linden, David J. / Activation of the TRPC1 cation channel by metabotropic glutamate receptor mGluR1. In: Nature. 2003 ; Vol. 426, No. 6964. pp. 285-291.
@article{c92e56cd7c4242eba260cf773d16a6af,
title = "Activation of the TRPC1 cation channel by metabotropic glutamate receptor mGluR1",
abstract = "Group I metabotropic glutamate receptors (consisting of mGluR1 and mGluR5) are G-protein-coupled neurotransmitter receptors that are found in the perisynaptic region of the postsynaptic membrane. These receptors are not activated by single synaptic volleys but rather require bursts of activity. They are implicated in many forms of neural plasticity including hippocampal long-term potentiation and depressions, cerebellar long-term depression, associative learning, and cocaine addiction. When activated, group I mGluRs engage two G-protein-dependent signalling mechanisms: stimulation of phospholipase C and activation of an unidentified, mixed-cation excitatory postsynaptic conductance (EPSC), displaying slow activation, in the plasma membrane. Here we report that the mGluR1-evoked slow EPSC is mediated by the TRPC1 cation channel. TRPC1 is expressed in perisynaptic regions of the cerebellar parallel fibre-Purkinje cell synapse and is physically associated with mGluR1. Manipulations that interfere with TRPC1 block the mGluR1-evoked slow EPSC in Purkinje cells; however, fast transmission mediated by AMPA-type glutamate receptors remains unaffected. Furthermore, co-expression of mGluR1 and TRPC1 in a heterologous system reconstituted a mGluR1-evoked conductance that closely resembles the slow EPSC in Purkinje cells.",
author = "Kim, {Sang Jeong} and Kim, {Yu Shin} and Yuan, {Joseph P.} and Petralia, {Ronald S.} and Worley, {Paul F.} and Linden, {David J.}",
year = "2003",
month = "11",
day = "20",
doi = "10.1038/nature02162",
language = "English",
volume = "426",
pages = "285--291",
journal = "Nature",
issn = "0028-0836",
publisher = "Nature Publishing Group",
number = "6964",

}

Kim, SJ, Kim, YS, Yuan, JP, Petralia, RS, Worley, PF & Linden, DJ 2003, 'Activation of the TRPC1 cation channel by metabotropic glutamate receptor mGluR1', Nature, vol. 426, no. 6964, pp. 285-291. https://doi.org/10.1038/nature02162

Activation of the TRPC1 cation channel by metabotropic glutamate receptor mGluR1. / Kim, Sang Jeong; Kim, Yu Shin; Yuan, Joseph P.; Petralia, Ronald S.; Worley, Paul F.; Linden, David J.

In: Nature, Vol. 426, No. 6964, 20.11.2003, p. 285-291.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Activation of the TRPC1 cation channel by metabotropic glutamate receptor mGluR1

AU - Kim, Sang Jeong

AU - Kim, Yu Shin

AU - Yuan, Joseph P.

AU - Petralia, Ronald S.

AU - Worley, Paul F.

AU - Linden, David J.

PY - 2003/11/20

Y1 - 2003/11/20

N2 - Group I metabotropic glutamate receptors (consisting of mGluR1 and mGluR5) are G-protein-coupled neurotransmitter receptors that are found in the perisynaptic region of the postsynaptic membrane. These receptors are not activated by single synaptic volleys but rather require bursts of activity. They are implicated in many forms of neural plasticity including hippocampal long-term potentiation and depressions, cerebellar long-term depression, associative learning, and cocaine addiction. When activated, group I mGluRs engage two G-protein-dependent signalling mechanisms: stimulation of phospholipase C and activation of an unidentified, mixed-cation excitatory postsynaptic conductance (EPSC), displaying slow activation, in the plasma membrane. Here we report that the mGluR1-evoked slow EPSC is mediated by the TRPC1 cation channel. TRPC1 is expressed in perisynaptic regions of the cerebellar parallel fibre-Purkinje cell synapse and is physically associated with mGluR1. Manipulations that interfere with TRPC1 block the mGluR1-evoked slow EPSC in Purkinje cells; however, fast transmission mediated by AMPA-type glutamate receptors remains unaffected. Furthermore, co-expression of mGluR1 and TRPC1 in a heterologous system reconstituted a mGluR1-evoked conductance that closely resembles the slow EPSC in Purkinje cells.

AB - Group I metabotropic glutamate receptors (consisting of mGluR1 and mGluR5) are G-protein-coupled neurotransmitter receptors that are found in the perisynaptic region of the postsynaptic membrane. These receptors are not activated by single synaptic volleys but rather require bursts of activity. They are implicated in many forms of neural plasticity including hippocampal long-term potentiation and depressions, cerebellar long-term depression, associative learning, and cocaine addiction. When activated, group I mGluRs engage two G-protein-dependent signalling mechanisms: stimulation of phospholipase C and activation of an unidentified, mixed-cation excitatory postsynaptic conductance (EPSC), displaying slow activation, in the plasma membrane. Here we report that the mGluR1-evoked slow EPSC is mediated by the TRPC1 cation channel. TRPC1 is expressed in perisynaptic regions of the cerebellar parallel fibre-Purkinje cell synapse and is physically associated with mGluR1. Manipulations that interfere with TRPC1 block the mGluR1-evoked slow EPSC in Purkinje cells; however, fast transmission mediated by AMPA-type glutamate receptors remains unaffected. Furthermore, co-expression of mGluR1 and TRPC1 in a heterologous system reconstituted a mGluR1-evoked conductance that closely resembles the slow EPSC in Purkinje cells.

UR - http://www.scopus.com/inward/record.url?scp=0344443184&partnerID=8YFLogxK

U2 - 10.1038/nature02162

DO - 10.1038/nature02162

M3 - Article

VL - 426

SP - 285

EP - 291

JO - Nature

JF - Nature

SN - 0028-0836

IS - 6964

ER -