The Probability of Neurotransmitter Release Governs AMPA Receptor Trafficking via Activity-Dependent Regulation of mGluR1 Surface Expression

Thomas M. Sanderson; Clarrisa A. Bradley; John Georgiou; Yun Hwa Hong; Ai Na Ng; Yeseul Lee; Hee Dae Kim; Doyeon Kim; Mascia Amici; Gi Hoon Son; Min Zhuo; Kyungjin Kim; Bong Kiun Kaang; Sang Jeong Kim; Graham L. Collingridge

doi:10.1016/j.celrep.2018.12.010

The Probability of Neurotransmitter Release Governs AMPA Receptor Trafficking via Activity-Dependent Regulation of mGluR1 Surface Expression

Thomas M. Sanderson, Clarrisa A. Bradley, John Georgiou, Yun Hwa Hong, Ai Na Ng, Yeseul Lee, Hee Dae Kim, Doyeon Kim, Mascia Amici, Gi Hoon Son, Min Zhuo, Kyungjin Kim, Bong Kiun Kaang, Sang Jeong Kim, Graham L. Collingridge

Department of Biomedical Sciences

Research output: Contribution to journal › Article › peer-review

12 Citations (Scopus)

Abstract

A major mechanism contributing to synaptic plasticity involves alterations in the number of AMPA receptors (AMPARs) expressed at synapses. Hippocampal CA1 synapses, where this process has been most extensively studied, are highly heterogeneous with respect to their probability of neurotransmitter release, P(r). It is unknown whether there is any relationship between the extent of plasticity-related AMPAR trafficking and the initial P(r) of a synapse. To address this question, we induced metabotropic glutamate receptor (mGluR) dependent long-term depression (mGluR-LTD) and assessed AMPAR trafficking and P(r) at individual synapses, using SEP-GluA2 and FM4-64, respectively. We found that either pharmacological or synaptic activation of mGluR1 reduced synaptic SEP-GluA2 in a manner that depends upon P(r); this process involved an activity-dependent reduction in surface mGluR1 that selectively protects high-P(r) synapses from synaptic weakening. Consequently, the extent of postsynaptic plasticity can be pre-tuned by presynaptic activity.

Original language	English
Pages (from-to)	3631-3646.e3
Journal	Cell Reports
Volume	25
Issue number	13
DOIs	https://doi.org/10.1016/j.celrep.2018.12.010
Publication status	Published - 2018 Dec 26

Bibliographical note

Funding Information:
This study was supported by the World-Class University (WCU) program through the National Research Foundation of Korea (R32-10142), a National Research Foundation of Korea (NRF) grant funded by the Korean government (Ministry of Science, ICT and Future Planning [MSIP]) (2018R1A5A2025964), U.K. Medical Research Council (MRC) grant MR/K023098/1, Biotechnology and Biological Sciences Research Council (BBSRC) grant BB/K019899/1, European Union (EU) grant 341089-HippoKAR, and Canadian Institutes of Health Research (CIHR) Foundation grant 154276. This work was also supported by the Brain Canada Foundation through the Canada Brain Research Fund, with the financial support of Health Canada.

Funding Information:
This study was supported by the World-Class University (WCU) program through the National Research Foundation of Korea ( R32-10142 ), a National Research Foundation of Korea (NRF) grant funded by the Korean government ( Ministry of Science, ICT and Future Planning [MSIP]) ( 2018R1A5A2025964 ), U.K. Medical Research Council (MRC) grant MR/K023098/1 , Biotechnology and Biological Sciences Research Council (BBSRC) grant BB/K019899/1 , European Union (EU) grant 341089-HippoKAR , and Canadian Institutes of Health Research (CIHR) Foundation grant 154276 . This work was also supported by the Brain Canada Foundation through the Canada Brain Research Fund , with the financial support of Health Canada .

Publisher Copyright:
© 2018 The Authors

Keywords

AMPA
DHPG
FM dye
LTD
Long-term depression
P(r)
mGluR
metabotropic
probability of release
theta burst

ASJC Scopus subject areas

Biochemistry, Genetics and Molecular Biology(all)

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10.1016/j.celrep.2018.12.010

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Sanderson, T. M., Bradley, C. A., Georgiou, J., Hong, Y. H., Ng, A. N., Lee, Y., Kim, H. D., Kim, D., Amici, M., Son, G. H., Zhuo, M., Kim, K., Kaang, B. K., Kim, S. J., & Collingridge, G. L. (2018). The Probability of Neurotransmitter Release Governs AMPA Receptor Trafficking via Activity-Dependent Regulation of mGluR1 Surface Expression. Cell Reports, 25(13), 3631-3646.e3. https://doi.org/10.1016/j.celrep.2018.12.010

Sanderson, TM, Bradley, CA, Georgiou, J, Hong, YH, Ng, AN, Lee, Y, Kim, HD, Kim, D, Amici, M, Son, GH, Zhuo, M, Kim, K, Kaang, BK, Kim, SJ & Collingridge, GL 2018, 'The Probability of Neurotransmitter Release Governs AMPA Receptor Trafficking via Activity-Dependent Regulation of mGluR1 Surface Expression', Cell Reports, vol. 25, no. 13, pp. 3631-3646.e3. https://doi.org/10.1016/j.celrep.2018.12.010

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title = "The Probability of Neurotransmitter Release Governs AMPA Receptor Trafficking via Activity-Dependent Regulation of mGluR1 Surface Expression",

abstract = "A major mechanism contributing to synaptic plasticity involves alterations in the number of AMPA receptors (AMPARs) expressed at synapses. Hippocampal CA1 synapses, where this process has been most extensively studied, are highly heterogeneous with respect to their probability of neurotransmitter release, P(r). It is unknown whether there is any relationship between the extent of plasticity-related AMPAR trafficking and the initial P(r) of a synapse. To address this question, we induced metabotropic glutamate receptor (mGluR) dependent long-term depression (mGluR-LTD) and assessed AMPAR trafficking and P(r) at individual synapses, using SEP-GluA2 and FM4-64, respectively. We found that either pharmacological or synaptic activation of mGluR1 reduced synaptic SEP-GluA2 in a manner that depends upon P(r); this process involved an activity-dependent reduction in surface mGluR1 that selectively protects high-P(r) synapses from synaptic weakening. Consequently, the extent of postsynaptic plasticity can be pre-tuned by presynaptic activity.",

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author = "Sanderson, {Thomas M.} and Bradley, {Clarrisa A.} and John Georgiou and Hong, {Yun Hwa} and Ng, {Ai Na} and Yeseul Lee and Kim, {Hee Dae} and Doyeon Kim and Mascia Amici and Son, {Gi Hoon} and Min Zhuo and Kyungjin Kim and Kaang, {Bong Kiun} and Kim, {Sang Jeong} and Collingridge, {Graham L.}",

note = "Funding Information: This study was supported by the World-Class University (WCU) program through the National Research Foundation of Korea (R32-10142), a National Research Foundation of Korea (NRF) grant funded by the Korean government (Ministry of Science, ICT and Future Planning [MSIP]) (2018R1A5A2025964), U.K. Medical Research Council (MRC) grant MR/K023098/1, Biotechnology and Biological Sciences Research Council (BBSRC) grant BB/K019899/1, European Union (EU) grant 341089-HippoKAR, and Canadian Institutes of Health Research (CIHR) Foundation grant 154276. This work was also supported by the Brain Canada Foundation through the Canada Brain Research Fund, with the financial support of Health Canada. Funding Information: This study was supported by the World-Class University (WCU) program through the National Research Foundation of Korea ( R32-10142 ), a National Research Foundation of Korea (NRF) grant funded by the Korean government ( Ministry of Science, ICT and Future Planning [MSIP]) ( 2018R1A5A2025964 ), U.K. Medical Research Council (MRC) grant MR/K023098/1 , Biotechnology and Biological Sciences Research Council (BBSRC) grant BB/K019899/1 , European Union (EU) grant 341089-HippoKAR , and Canadian Institutes of Health Research (CIHR) Foundation grant 154276 . This work was also supported by the Brain Canada Foundation through the Canada Brain Research Fund , with the financial support of Health Canada . Publisher Copyright: {\textcopyright} 2018 The Authors",

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AU - Bradley, Clarrisa A.

AU - Georgiou, John

AU - Hong, Yun Hwa

AU - Ng, Ai Na

AU - Lee, Yeseul

AU - Kim, Hee Dae

AU - Kim, Doyeon

AU - Amici, Mascia

AU - Son, Gi Hoon

AU - Zhuo, Min

AU - Kim, Kyungjin

AU - Kaang, Bong Kiun

AU - Kim, Sang Jeong

AU - Collingridge, Graham L.

N1 - Funding Information: This study was supported by the World-Class University (WCU) program through the National Research Foundation of Korea (R32-10142), a National Research Foundation of Korea (NRF) grant funded by the Korean government (Ministry of Science, ICT and Future Planning [MSIP]) (2018R1A5A2025964), U.K. Medical Research Council (MRC) grant MR/K023098/1, Biotechnology and Biological Sciences Research Council (BBSRC) grant BB/K019899/1, European Union (EU) grant 341089-HippoKAR, and Canadian Institutes of Health Research (CIHR) Foundation grant 154276. This work was also supported by the Brain Canada Foundation through the Canada Brain Research Fund, with the financial support of Health Canada. Funding Information: This study was supported by the World-Class University (WCU) program through the National Research Foundation of Korea ( R32-10142 ), a National Research Foundation of Korea (NRF) grant funded by the Korean government ( Ministry of Science, ICT and Future Planning [MSIP]) ( 2018R1A5A2025964 ), U.K. Medical Research Council (MRC) grant MR/K023098/1 , Biotechnology and Biological Sciences Research Council (BBSRC) grant BB/K019899/1 , European Union (EU) grant 341089-HippoKAR , and Canadian Institutes of Health Research (CIHR) Foundation grant 154276 . This work was also supported by the Brain Canada Foundation through the Canada Brain Research Fund , with the financial support of Health Canada . Publisher Copyright: © 2018 The Authors

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N2 - A major mechanism contributing to synaptic plasticity involves alterations in the number of AMPA receptors (AMPARs) expressed at synapses. Hippocampal CA1 synapses, where this process has been most extensively studied, are highly heterogeneous with respect to their probability of neurotransmitter release, P(r). It is unknown whether there is any relationship between the extent of plasticity-related AMPAR trafficking and the initial P(r) of a synapse. To address this question, we induced metabotropic glutamate receptor (mGluR) dependent long-term depression (mGluR-LTD) and assessed AMPAR trafficking and P(r) at individual synapses, using SEP-GluA2 and FM4-64, respectively. We found that either pharmacological or synaptic activation of mGluR1 reduced synaptic SEP-GluA2 in a manner that depends upon P(r); this process involved an activity-dependent reduction in surface mGluR1 that selectively protects high-P(r) synapses from synaptic weakening. Consequently, the extent of postsynaptic plasticity can be pre-tuned by presynaptic activity.

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KW - LTD

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KW - mGluR

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KW - probability of release

KW - theta burst

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ER -

The Probability of Neurotransmitter Release Governs AMPA Receptor Trafficking via Activity-Dependent Regulation of mGluR1 Surface Expression

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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