Kainate induces mobilization of synaptic vesicles at the growth cone through the activation of protein kinase A

Giuliana Gelsomino, Elisabetta Menna, Flavia Antonucci, Simona Rodighiero, Loredana Riganti, Christophe Mulle, Fabio Benfenati, Flavia Valtorta, Claudia Verderio, Michela Matteoli

Research output: Contribution to journalArticle

Abstract

Activation of protein kinase A (PKA) pathway at presynaptic terminals plays a crucial role in the supply of synaptic vesicles (SVs) from the reserve pool, affecting the steady-state level of activity and the reconstitution of the readily releasable pool after intense stimulation. However, the identity of the stimuli activating this pathway is undefined. Using fluorescence resonance energy transfer and molecular genetic, we show that kainate, through the activation of presynaptic kainate receptors, induces PKA activation and enhances synapsin I phosphorylation at PKA-specific residues. This leads to a dispersion of synapsin I immunoreactivity, which is accompanied by a PKA-dependent increase in the rate of SV recycling at the growth cone and by an enhanced miniature excitatory postsynaptic currents frequency in mature networks. Selective activation of this pathway is induced by the native neurotransmitter glutamate, when applied in the high nanomolar range. These data identify glutamate, specifically acting on KARs, as one of the stimuli able to induce phosphorylation of synapsin at PKA sites, both at the axonal growth cone and at the mature synapse, thus increasing SV availability and contributing to plasticity phenomena.

Original languageEnglish
Pages (from-to)531-541
Number of pages11
JournalCerebral Cortex
Volume23
Issue number3
DOIs
Publication statusPublished - 2013

Fingerprint

Growth Cones
Synaptic Vesicles
Kainic Acid
Cyclic AMP-Dependent Protein Kinases
Synapsins
Glutamic Acid
Phosphorylation
Presynaptic Receptors
Kainic Acid Receptors
Fluorescence Resonance Energy Transfer
Excitatory Postsynaptic Potentials
Presynaptic Terminals
Synapses
Neurotransmitter Agents
Molecular Biology

Keywords

  • kainate receptors
  • PKA
  • presynaptic terminal
  • synapsin I
  • synaptic vesicles recycling

ASJC Scopus subject areas

  • Cognitive Neuroscience
  • Cellular and Molecular Neuroscience

Cite this

Kainate induces mobilization of synaptic vesicles at the growth cone through the activation of protein kinase A. / Gelsomino, Giuliana; Menna, Elisabetta; Antonucci, Flavia; Rodighiero, Simona; Riganti, Loredana; Mulle, Christophe; Benfenati, Fabio; Valtorta, Flavia; Verderio, Claudia; Matteoli, Michela.

In: Cerebral Cortex, Vol. 23, No. 3, 2013, p. 531-541.

Research output: Contribution to journalArticle

Gelsomino, Giuliana ; Menna, Elisabetta ; Antonucci, Flavia ; Rodighiero, Simona ; Riganti, Loredana ; Mulle, Christophe ; Benfenati, Fabio ; Valtorta, Flavia ; Verderio, Claudia ; Matteoli, Michela. / Kainate induces mobilization of synaptic vesicles at the growth cone through the activation of protein kinase A. In: Cerebral Cortex. 2013 ; Vol. 23, No. 3. pp. 531-541.
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