Channel-mediated astrocytic glutamate modulates hippocampal synaptic plasticity by activating postsynaptic NMDA receptors

Hyungju Park; Kyung Seok Han; Jinsoo Seo; Jaekwang Lee; Shashank M. Dravid; Junsung Woo; Heejung Chun; Sukhee Cho; Jin Young Bae; Heeyoung An; Woohyun Koh; Bo Eun Yoon; Rolando Berlinguer-Palmini; Guido Mannaioni; Stephen F. Traynelis; Yong Chul Bae; Se Young Choi; C. Justin Lee

doi:10.1186/s13041-015-0097-y

Channel-mediated astrocytic glutamate modulates hippocampal synaptic plasticity by activating postsynaptic NMDA receptors

Hyungju Park, Kyung Seok Han, Jinsoo Seo, Jaekwang Lee, Shashank M. Dravid, Junsung Woo, Heejung Chun, Sukhee Cho, Jin Young Bae, Heeyoung An, Woohyun Koh, Bo Eun Yoon, Rolando Berlinguer-Palmini, Guido Mannaioni, Stephen F. Traynelis, Yong Chul Bae, Se Young Choi, C. Justin Lee

Department of Pharmacology and Neuroscience

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

34 Scopus citations

Abstract

Background: Activation of G protein coupled receptor (GPCR) in astrocytes leads to Ca²⁺-dependent glutamate release via Bestrophin 1 (Best1) channel. Whether receptor-mediated glutamate release from astrocytes can regulate synaptic plasticity remains to be fully understood. Results: We show here that Best1-mediated astrocytic glutamate activates the synaptic N-methyl-D-aspartate receptor (NMDAR) and modulates NMDAR-dependent synaptic plasticity. Our data show that activation of the protease-activated receptor 1 (PAR1) in hippocampal CA1 astrocytes elevates the glutamate concentration at Schaffer collateral-CA1 (SC-CA1) synapses, resulting in activation of GluN2A-containing NMDARs and NMDAR-dependent potentiation of synaptic responses. Furthermore, the threshold for inducing NMDAR-dependent long-term potentiation (LTP) is lowered when astrocytic glutamate release accompanied LTP induction, suggesting that astrocytic glutamate is significant in modulating synaptic plasticity. Conclusions: Our results provide direct evidence for the physiological importance of channel-mediated astrocytic glutamate in modulating neural circuit functions.

Original language	English (US)
Article number	7
Journal	Molecular Brain
Volume	8
Issue number	1
DOIs	https://doi.org/10.1186/s13041-015-0097-y
State	Published - Dec 2015

All Science Journal Classification (ASJC) codes

Molecular Biology
Cellular and Molecular Neuroscience

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10.1186/s13041-015-0097-y

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Park, H., Han, K. S., Seo, J., Lee, J., Dravid, S. M., Woo, J., Chun, H., Cho, S., Bae, J. Y., An, H., Koh, W., Yoon, B. E., Berlinguer-Palmini, R., Mannaioni, G., Traynelis, S. F., Bae, Y. C., Choi, S. Y., & Lee, C. J. (2015). Channel-mediated astrocytic glutamate modulates hippocampal synaptic plasticity by activating postsynaptic NMDA receptors. Molecular Brain, 8(1), [7]. https://doi.org/10.1186/s13041-015-0097-y

Channel-mediated astrocytic glutamate modulates hippocampal synaptic plasticity by activating postsynaptic NMDA receptors. / Park, Hyungju; Han, Kyung Seok; Seo, Jinsoo; Lee, Jaekwang; Dravid, Shashank M.; Woo, Junsung; Chun, Heejung; Cho, Sukhee; Bae, Jin Young; An, Heeyoung; Koh, Woohyun; Yoon, Bo Eun; Berlinguer-Palmini, Rolando; Mannaioni, Guido; Traynelis, Stephen F.; Bae, Yong Chul; Choi, Se Young; Lee, C. Justin.

In: Molecular Brain, Vol. 8, No. 1, 7, 12.2015.

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

Park, H, Han, KS, Seo, J, Lee, J, Dravid, SM, Woo, J, Chun, H, Cho, S, Bae, JY, An, H, Koh, W, Yoon, BE, Berlinguer-Palmini, R, Mannaioni, G, Traynelis, SF, Bae, YC, Choi, SY & Lee, CJ 2015, 'Channel-mediated astrocytic glutamate modulates hippocampal synaptic plasticity by activating postsynaptic NMDA receptors', Molecular Brain, vol. 8, no. 1, 7. https://doi.org/10.1186/s13041-015-0097-y

Park, Hyungju ; Han, Kyung Seok ; Seo, Jinsoo ; Lee, Jaekwang ; Dravid, Shashank M. ; Woo, Junsung ; Chun, Heejung ; Cho, Sukhee ; Bae, Jin Young ; An, Heeyoung ; Koh, Woohyun ; Yoon, Bo Eun ; Berlinguer-Palmini, Rolando ; Mannaioni, Guido ; Traynelis, Stephen F. ; Bae, Yong Chul ; Choi, Se Young ; Lee, C. Justin. / Channel-mediated astrocytic glutamate modulates hippocampal synaptic plasticity by activating postsynaptic NMDA receptors. In: Molecular Brain. 2015 ; Vol. 8, No. 1.

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title = "Channel-mediated astrocytic glutamate modulates hippocampal synaptic plasticity by activating postsynaptic NMDA receptors",

abstract = "Background: Activation of G protein coupled receptor (GPCR) in astrocytes leads to Ca2+-dependent glutamate release via Bestrophin 1 (Best1) channel. Whether receptor-mediated glutamate release from astrocytes can regulate synaptic plasticity remains to be fully understood. Results: We show here that Best1-mediated astrocytic glutamate activates the synaptic N-methyl-D-aspartate receptor (NMDAR) and modulates NMDAR-dependent synaptic plasticity. Our data show that activation of the protease-activated receptor 1 (PAR1) in hippocampal CA1 astrocytes elevates the glutamate concentration at Schaffer collateral-CA1 (SC-CA1) synapses, resulting in activation of GluN2A-containing NMDARs and NMDAR-dependent potentiation of synaptic responses. Furthermore, the threshold for inducing NMDAR-dependent long-term potentiation (LTP) is lowered when astrocytic glutamate release accompanied LTP induction, suggesting that astrocytic glutamate is significant in modulating synaptic plasticity. Conclusions: Our results provide direct evidence for the physiological importance of channel-mediated astrocytic glutamate in modulating neural circuit functions.",

author = "Hyungju Park and Han, {Kyung Seok} and Jinsoo Seo and Jaekwang Lee and Dravid, {Shashank M.} and Junsung Woo and Heejung Chun and Sukhee Cho and Bae, {Jin Young} and Heeyoung An and Woohyun Koh and Yoon, {Bo Eun} and Rolando Berlinguer-Palmini and Guido Mannaioni and Traynelis, {Stephen F.} and Bae, {Yong Chul} and Choi, {Se Young} and Lee, {C. Justin}",

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doi = "10.1186/s13041-015-0097-y",

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AU - Park, Hyungju

AU - Han, Kyung Seok

AU - Seo, Jinsoo

AU - Lee, Jaekwang

AU - Dravid, Shashank M.

AU - Woo, Junsung

AU - Chun, Heejung

AU - Cho, Sukhee

AU - Bae, Jin Young

AU - An, Heeyoung

AU - Koh, Woohyun

AU - Yoon, Bo Eun

AU - Berlinguer-Palmini, Rolando

AU - Mannaioni, Guido

AU - Traynelis, Stephen F.

AU - Bae, Yong Chul

AU - Choi, Se Young

AU - Lee, C. Justin

PY - 2015/12

Y1 - 2015/12

N2 - Background: Activation of G protein coupled receptor (GPCR) in astrocytes leads to Ca2+-dependent glutamate release via Bestrophin 1 (Best1) channel. Whether receptor-mediated glutamate release from astrocytes can regulate synaptic plasticity remains to be fully understood. Results: We show here that Best1-mediated astrocytic glutamate activates the synaptic N-methyl-D-aspartate receptor (NMDAR) and modulates NMDAR-dependent synaptic plasticity. Our data show that activation of the protease-activated receptor 1 (PAR1) in hippocampal CA1 astrocytes elevates the glutamate concentration at Schaffer collateral-CA1 (SC-CA1) synapses, resulting in activation of GluN2A-containing NMDARs and NMDAR-dependent potentiation of synaptic responses. Furthermore, the threshold for inducing NMDAR-dependent long-term potentiation (LTP) is lowered when astrocytic glutamate release accompanied LTP induction, suggesting that astrocytic glutamate is significant in modulating synaptic plasticity. Conclusions: Our results provide direct evidence for the physiological importance of channel-mediated astrocytic glutamate in modulating neural circuit functions.

AB - Background: Activation of G protein coupled receptor (GPCR) in astrocytes leads to Ca2+-dependent glutamate release via Bestrophin 1 (Best1) channel. Whether receptor-mediated glutamate release from astrocytes can regulate synaptic plasticity remains to be fully understood. Results: We show here that Best1-mediated astrocytic glutamate activates the synaptic N-methyl-D-aspartate receptor (NMDAR) and modulates NMDAR-dependent synaptic plasticity. Our data show that activation of the protease-activated receptor 1 (PAR1) in hippocampal CA1 astrocytes elevates the glutamate concentration at Schaffer collateral-CA1 (SC-CA1) synapses, resulting in activation of GluN2A-containing NMDARs and NMDAR-dependent potentiation of synaptic responses. Furthermore, the threshold for inducing NMDAR-dependent long-term potentiation (LTP) is lowered when astrocytic glutamate release accompanied LTP induction, suggesting that astrocytic glutamate is significant in modulating synaptic plasticity. Conclusions: Our results provide direct evidence for the physiological importance of channel-mediated astrocytic glutamate in modulating neural circuit functions.

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Channel-mediated astrocytic glutamate modulates hippocampal synaptic plasticity by activating postsynaptic NMDA receptors

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