Maturation of a PKG-dependent retrograde mechanism for exoendocytic coupling of synaptic vesicles

Neuron
Kohgaku EguchiTomoyuki Takahashi

Abstract

At presynaptic terminals vesicular membranes are fused into plasma membrane upon exocytosis and retrieved by endocytosis. During a sustained high-frequency transmission, exoendocytic coupling is critical for the maintenance of synaptic transmission. Here, we show that this homeostatic coupling is supported by cGMP-dependent protein kinase (PKG) at the calyx of Held. This mechanism starts to operate after hearing onset during the second postnatal week, when PKG expression becomes upregulated in the brainstem. Pharmacological tests with capacitance measurements revealed that presynaptic PKG activity is supported by a retrograde signal cascade mediated by NO that is released by activation of postsynaptic NMDA receptors. Activation of PKG also upregulates phosphatidylinositol-4,5-bisphosphate, thereby accelerating endocytosis. Furthermore, presynaptic PKG activity upregulates synaptic fidelity during high-frequency transmission. We conclude that maturation of the PKG-dependent retrograde signal cascade strengthens the homeostatic plasticity for the maintenance of high-frequency synaptic transmission at the fast glutamatergic synapse.

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Citations

Mar 29, 2016·Hearing Research·Maryna BaydyukLing-Gang Wu
Nov 29, 2013·Developmental Neurobiology·Hiroki Akiyama, Hiroyuki Kamiguchi
May 15, 2015·Development, Growth & Differentiation·Takuro Tojima, Hiroyuki Kamiguchi
Nov 13, 2012·Neuron·Tetsuya Hori, Tomoyuki Takahashi
Jul 22, 2015·Proceedings of the Japan Academy. Series B, Physical and Biological Sciences·Tomoyuki Takahashi
Nov 2, 2016·The Journal of Physiology·Chihiro TakamiTomoyuki Takahashi
Nov 7, 2018·British Journal of Pharmacology·John Garthwaite
Jan 3, 2014·Physiological Reviews·Emmanuel BourinetGerald W Zamponi
Sep 10, 2020·Scientific Reports·Yusaku IkedaYasushi Sako
Jun 20, 2019·Proceedings of the National Academy of Sciences of the United States of America·Jeffrey S DasonMarla B Sokolowski
Nov 8, 2020·Neuroscience Research·Natsumi Ageta-Ishihara, Makoto Kinoshita
Jul 10, 2021·Neuropharmacology·Maria GurmaLu-Yang Wang

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