The decoy SNARE Tomosyn sets tonic versus phasic release properties and is required for homeostatic synaptic plasticity

Synaptic vesicle (SV) release probability (Pr) is a key presynaptic determinant of synaptic strength established by cell-intrinsic properties and further refined by plasticity. To characterize mechanisms that generate Pr heterogeneity between distinct neuronal populations, we examined glutamatergic...

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Autores principales: Chad W Sauvola, Yulia Akbergenova, Karen L Cunningham, Nicole A Aponte-Santiago, J Troy Littleton
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Publicado: eLife Sciences Publications Ltd 2021
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Acceso en línea:https://doaj.org/article/f89cb7ee2d04449ba8e1a63036a262a4
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spelling oai:doaj.org-article:f89cb7ee2d04449ba8e1a63036a262a42021-11-24T15:06:30ZThe decoy SNARE Tomosyn sets tonic versus phasic release properties and is required for homeostatic synaptic plasticity10.7554/eLife.728412050-084Xe72841https://doaj.org/article/f89cb7ee2d04449ba8e1a63036a262a42021-10-01T00:00:00Zhttps://elifesciences.org/articles/72841https://doaj.org/toc/2050-084XSynaptic vesicle (SV) release probability (Pr) is a key presynaptic determinant of synaptic strength established by cell-intrinsic properties and further refined by plasticity. To characterize mechanisms that generate Pr heterogeneity between distinct neuronal populations, we examined glutamatergic tonic (Ib) and phasic (Is) motoneurons in Drosophila with stereotyped differences in Pr and synaptic plasticity. We found the decoy soluble N-ethylmaleimide sensitive factor attachment protein receptor (SNARE) Tomosyn is differentially expressed between these motoneuron subclasses and contributes to intrinsic differences in their synaptic output. Tomosyn expression enables tonic release in Ib motoneurons by reducing SNARE complex formation and suppressing Pr to generate decreased levels of SV fusion and enhanced resistance to synaptic fatigue. In contrast, phasic release dominates when Tomosyn expression is low, enabling high intrinsic Pr at Is terminals at the expense of sustained release and robust presynaptic potentiation. In addition, loss of Tomosyn disrupts the ability of tonic synapses to undergo presynaptic homeostatic potentiation.Chad W SauvolaYulia AkbergenovaKaren L CunninghamNicole A Aponte-SantiagoJ Troy LittletoneLife Sciences Publications Ltdarticlesynapsesnare complexneurotransmitter releasesynaptic plasticityDrosophilasynaptic vesicleMedicineRScienceQBiology (General)QH301-705.5ENeLife, Vol 10 (2021)
institution DOAJ
collection DOAJ
language EN
topic synapse
snare complex
neurotransmitter release
synaptic plasticity
Drosophila
synaptic vesicle
Medicine
R
Science
Q
Biology (General)
QH301-705.5
spellingShingle synapse
snare complex
neurotransmitter release
synaptic plasticity
Drosophila
synaptic vesicle
Medicine
R
Science
Q
Biology (General)
QH301-705.5
Chad W Sauvola
Yulia Akbergenova
Karen L Cunningham
Nicole A Aponte-Santiago
J Troy Littleton
The decoy SNARE Tomosyn sets tonic versus phasic release properties and is required for homeostatic synaptic plasticity
description Synaptic vesicle (SV) release probability (Pr) is a key presynaptic determinant of synaptic strength established by cell-intrinsic properties and further refined by plasticity. To characterize mechanisms that generate Pr heterogeneity between distinct neuronal populations, we examined glutamatergic tonic (Ib) and phasic (Is) motoneurons in Drosophila with stereotyped differences in Pr and synaptic plasticity. We found the decoy soluble N-ethylmaleimide sensitive factor attachment protein receptor (SNARE) Tomosyn is differentially expressed between these motoneuron subclasses and contributes to intrinsic differences in their synaptic output. Tomosyn expression enables tonic release in Ib motoneurons by reducing SNARE complex formation and suppressing Pr to generate decreased levels of SV fusion and enhanced resistance to synaptic fatigue. In contrast, phasic release dominates when Tomosyn expression is low, enabling high intrinsic Pr at Is terminals at the expense of sustained release and robust presynaptic potentiation. In addition, loss of Tomosyn disrupts the ability of tonic synapses to undergo presynaptic homeostatic potentiation.
format article
author Chad W Sauvola
Yulia Akbergenova
Karen L Cunningham
Nicole A Aponte-Santiago
J Troy Littleton
author_facet Chad W Sauvola
Yulia Akbergenova
Karen L Cunningham
Nicole A Aponte-Santiago
J Troy Littleton
author_sort Chad W Sauvola
title The decoy SNARE Tomosyn sets tonic versus phasic release properties and is required for homeostatic synaptic plasticity
title_short The decoy SNARE Tomosyn sets tonic versus phasic release properties and is required for homeostatic synaptic plasticity
title_full The decoy SNARE Tomosyn sets tonic versus phasic release properties and is required for homeostatic synaptic plasticity
title_fullStr The decoy SNARE Tomosyn sets tonic versus phasic release properties and is required for homeostatic synaptic plasticity
title_full_unstemmed The decoy SNARE Tomosyn sets tonic versus phasic release properties and is required for homeostatic synaptic plasticity
title_sort decoy snare tomosyn sets tonic versus phasic release properties and is required for homeostatic synaptic plasticity
publisher eLife Sciences Publications Ltd
publishDate 2021
url https://doaj.org/article/f89cb7ee2d04449ba8e1a63036a262a4
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