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Rapid homeostatic modulation of transsynaptic nanocolumn rings

Robust neural information transfer relies on a delicate molecular nano-architecture of chemical synapses. Neurotransmitter release is controlled by a specific arrangement of proteins within presynaptic active zones. How the specific presynaptic molecular architecture relates to postsynaptic organiza...

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Autores principales: Muttathukunnel, Paola, Frei, Patrick, Perry, Sarah, Dickman, Dion, Müller, Martin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9659372/
https://www.ncbi.nlm.nih.gov/pubmed/36322725
http://dx.doi.org/10.1073/pnas.2119044119
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author Muttathukunnel, Paola
Frei, Patrick
Perry, Sarah
Dickman, Dion
Müller, Martin
author_facet Muttathukunnel, Paola
Frei, Patrick
Perry, Sarah
Dickman, Dion
Müller, Martin
author_sort Muttathukunnel, Paola
collection PubMed
description Robust neural information transfer relies on a delicate molecular nano-architecture of chemical synapses. Neurotransmitter release is controlled by a specific arrangement of proteins within presynaptic active zones. How the specific presynaptic molecular architecture relates to postsynaptic organization and how synaptic nano-architecture is transsynaptically regulated to enable stable synaptic transmission remain enigmatic. Using time-gated stimulated emission-depletion microscopy at the Drosophila neuromuscular junction, we found that presynaptic nanorings formed by the active-zone scaffold Bruchpilot (Brp) align with postsynaptic glutamate receptor (GluR) rings. Individual rings harbor approximately four transsynaptically aligned Brp-GluR nanocolumns. Similar nanocolumn rings are formed by the presynaptic protein Unc13A and GluRs. Intriguingly, acute GluR impairment triggers transsynaptic nanocolumn formation on the minute timescale during homeostatic plasticity. We reveal distinct phases of structural transsynaptic homeostatic plasticity, with postsynaptic GluR reorganization preceding presynaptic Brp modulation. Finally, homeostatic control of transsynaptic nano-architecture and neurotransmitter release requires the auxiliary GluR subunit Neto. Thus, transsynaptic nanocolumn rings provide a substrate for rapid homeostatic stabilization of synaptic efficacy.
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spelling pubmed-96593722022-11-15 Rapid homeostatic modulation of transsynaptic nanocolumn rings Muttathukunnel, Paola Frei, Patrick Perry, Sarah Dickman, Dion Müller, Martin Proc Natl Acad Sci U S A Biological Sciences Robust neural information transfer relies on a delicate molecular nano-architecture of chemical synapses. Neurotransmitter release is controlled by a specific arrangement of proteins within presynaptic active zones. How the specific presynaptic molecular architecture relates to postsynaptic organization and how synaptic nano-architecture is transsynaptically regulated to enable stable synaptic transmission remain enigmatic. Using time-gated stimulated emission-depletion microscopy at the Drosophila neuromuscular junction, we found that presynaptic nanorings formed by the active-zone scaffold Bruchpilot (Brp) align with postsynaptic glutamate receptor (GluR) rings. Individual rings harbor approximately four transsynaptically aligned Brp-GluR nanocolumns. Similar nanocolumn rings are formed by the presynaptic protein Unc13A and GluRs. Intriguingly, acute GluR impairment triggers transsynaptic nanocolumn formation on the minute timescale during homeostatic plasticity. We reveal distinct phases of structural transsynaptic homeostatic plasticity, with postsynaptic GluR reorganization preceding presynaptic Brp modulation. Finally, homeostatic control of transsynaptic nano-architecture and neurotransmitter release requires the auxiliary GluR subunit Neto. Thus, transsynaptic nanocolumn rings provide a substrate for rapid homeostatic stabilization of synaptic efficacy. National Academy of Sciences 2022-11-02 2022-11-08 /pmc/articles/PMC9659372/ /pubmed/36322725 http://dx.doi.org/10.1073/pnas.2119044119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by/4.0/This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY) (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Biological Sciences
Muttathukunnel, Paola
Frei, Patrick
Perry, Sarah
Dickman, Dion
Müller, Martin
Rapid homeostatic modulation of transsynaptic nanocolumn rings
title Rapid homeostatic modulation of transsynaptic nanocolumn rings
title_full Rapid homeostatic modulation of transsynaptic nanocolumn rings
title_fullStr Rapid homeostatic modulation of transsynaptic nanocolumn rings
title_full_unstemmed Rapid homeostatic modulation of transsynaptic nanocolumn rings
title_short Rapid homeostatic modulation of transsynaptic nanocolumn rings
title_sort rapid homeostatic modulation of transsynaptic nanocolumn rings
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9659372/
https://www.ncbi.nlm.nih.gov/pubmed/36322725
http://dx.doi.org/10.1073/pnas.2119044119
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