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

Research output: Contribution to journalArticle

25 Citations (Scopus)

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 languageEnglish
Article number7
JournalMolecular Brain
Volume8
Issue number1
DOIs
StatePublished - 2015

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Neuronal Plasticity
N-Methyl-D-Aspartate Receptors
Glutamic Acid
Astrocytes
Long-Term Potentiation
PAR-1 Receptor
Glutamate Receptors
G-Protein-Coupled Receptors
Synapses
Hippocampus

All Science Journal Classification (ASJC) codes

  • Cellular and Molecular Neuroscience
  • Molecular Biology
  • Medicine(all)

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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, 2015.

Research output: Contribution to journalArticle

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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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

Y1 - 2015

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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