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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...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
National Academy of Sciences
2022
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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. |
format | Online Article Text |
id | pubmed-9659372 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
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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