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Rapid active zone remodeling consolidates presynaptic potentiation

Neuronal communication across synapses relies on neurotransmitter release from presynaptic active zones (AZs) followed by postsynaptic transmitter detection. Synaptic plasticity homeostatically maintains functionality during perturbations and enables memory formation. Postsynaptic plasticity targets...

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Autores principales: Böhme, Mathias A., McCarthy, Anthony W., Grasskamp, Andreas T., Beuschel, Christine B., Goel, Pragya, Jusyte, Meida, Laber, Desiree, Huang, Sheng, Rey, Ulises, Petzoldt, Astrid G., Lehmann, Martin, Göttfert, Fabian, Haghighi, Pejmun, Hell, Stefan W., Owald, David, Dickman, Dion, Sigrist, Stephan J., Walter, Alexander M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6403334/
https://www.ncbi.nlm.nih.gov/pubmed/30842428
http://dx.doi.org/10.1038/s41467-019-08977-6
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author Böhme, Mathias A.
McCarthy, Anthony W.
Grasskamp, Andreas T.
Beuschel, Christine B.
Goel, Pragya
Jusyte, Meida
Laber, Desiree
Huang, Sheng
Rey, Ulises
Petzoldt, Astrid G.
Lehmann, Martin
Göttfert, Fabian
Haghighi, Pejmun
Hell, Stefan W.
Owald, David
Dickman, Dion
Sigrist, Stephan J.
Walter, Alexander M.
author_facet Böhme, Mathias A.
McCarthy, Anthony W.
Grasskamp, Andreas T.
Beuschel, Christine B.
Goel, Pragya
Jusyte, Meida
Laber, Desiree
Huang, Sheng
Rey, Ulises
Petzoldt, Astrid G.
Lehmann, Martin
Göttfert, Fabian
Haghighi, Pejmun
Hell, Stefan W.
Owald, David
Dickman, Dion
Sigrist, Stephan J.
Walter, Alexander M.
author_sort Böhme, Mathias A.
collection PubMed
description Neuronal communication across synapses relies on neurotransmitter release from presynaptic active zones (AZs) followed by postsynaptic transmitter detection. Synaptic plasticity homeostatically maintains functionality during perturbations and enables memory formation. Postsynaptic plasticity targets neurotransmitter receptors, but presynaptic mechanisms regulating the neurotransmitter release apparatus remain largely enigmatic. By studying Drosophila neuromuscular junctions (NMJs) we show that AZs consist of nano-modular release sites and identify a molecular sequence that adds modules within minutes of inducing homeostatic plasticity. This requires cognate transport machinery and specific AZ-scaffolding proteins. Structural remodeling is not required for immediate potentiation of neurotransmitter release, but necessary to sustain potentiation over longer timescales. Finally, mutations in Unc13 disrupting homeostatic plasticity at the NMJ also impair short-term memory when central neurons are targeted, suggesting that both plasticity mechanisms utilize Unc13. Together, while immediate synaptic potentiation capitalizes on available material, it triggers the coincident incorporation of modular release sites to consolidate synaptic potentiation.
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spelling pubmed-64033342019-03-08 Rapid active zone remodeling consolidates presynaptic potentiation Böhme, Mathias A. McCarthy, Anthony W. Grasskamp, Andreas T. Beuschel, Christine B. Goel, Pragya Jusyte, Meida Laber, Desiree Huang, Sheng Rey, Ulises Petzoldt, Astrid G. Lehmann, Martin Göttfert, Fabian Haghighi, Pejmun Hell, Stefan W. Owald, David Dickman, Dion Sigrist, Stephan J. Walter, Alexander M. Nat Commun Article Neuronal communication across synapses relies on neurotransmitter release from presynaptic active zones (AZs) followed by postsynaptic transmitter detection. Synaptic plasticity homeostatically maintains functionality during perturbations and enables memory formation. Postsynaptic plasticity targets neurotransmitter receptors, but presynaptic mechanisms regulating the neurotransmitter release apparatus remain largely enigmatic. By studying Drosophila neuromuscular junctions (NMJs) we show that AZs consist of nano-modular release sites and identify a molecular sequence that adds modules within minutes of inducing homeostatic plasticity. This requires cognate transport machinery and specific AZ-scaffolding proteins. Structural remodeling is not required for immediate potentiation of neurotransmitter release, but necessary to sustain potentiation over longer timescales. Finally, mutations in Unc13 disrupting homeostatic plasticity at the NMJ also impair short-term memory when central neurons are targeted, suggesting that both plasticity mechanisms utilize Unc13. Together, while immediate synaptic potentiation capitalizes on available material, it triggers the coincident incorporation of modular release sites to consolidate synaptic potentiation. Nature Publishing Group UK 2019-03-06 /pmc/articles/PMC6403334/ /pubmed/30842428 http://dx.doi.org/10.1038/s41467-019-08977-6 Text en © The Author(s) 2019 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Böhme, Mathias A.
McCarthy, Anthony W.
Grasskamp, Andreas T.
Beuschel, Christine B.
Goel, Pragya
Jusyte, Meida
Laber, Desiree
Huang, Sheng
Rey, Ulises
Petzoldt, Astrid G.
Lehmann, Martin
Göttfert, Fabian
Haghighi, Pejmun
Hell, Stefan W.
Owald, David
Dickman, Dion
Sigrist, Stephan J.
Walter, Alexander M.
Rapid active zone remodeling consolidates presynaptic potentiation
title Rapid active zone remodeling consolidates presynaptic potentiation
title_full Rapid active zone remodeling consolidates presynaptic potentiation
title_fullStr Rapid active zone remodeling consolidates presynaptic potentiation
title_full_unstemmed Rapid active zone remodeling consolidates presynaptic potentiation
title_short Rapid active zone remodeling consolidates presynaptic potentiation
title_sort rapid active zone remodeling consolidates presynaptic potentiation
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6403334/
https://www.ncbi.nlm.nih.gov/pubmed/30842428
http://dx.doi.org/10.1038/s41467-019-08977-6
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