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Calcium modeling of spine apparatus-containing human dendritic spines demonstrates an “all-or-nothing” communication switch between the spine head and dendrite
Dendritic spines are highly dynamic neuronal compartments that control the synaptic transmission between neurons. Spines form ultrastructural units, coupling synaptic contact sites to the dendritic shaft and often harbor a spine apparatus organelle, composed of smooth endoplasmic reticulum, which is...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9071165/ https://www.ncbi.nlm.nih.gov/pubmed/35468131 http://dx.doi.org/10.1371/journal.pcbi.1010069 |
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author | Rosado, James Bui, Viet Duc Haas, Carola A. Beck, Jürgen Queisser, Gillian Vlachos, Andreas |
author_facet | Rosado, James Bui, Viet Duc Haas, Carola A. Beck, Jürgen Queisser, Gillian Vlachos, Andreas |
author_sort | Rosado, James |
collection | PubMed |
description | Dendritic spines are highly dynamic neuronal compartments that control the synaptic transmission between neurons. Spines form ultrastructural units, coupling synaptic contact sites to the dendritic shaft and often harbor a spine apparatus organelle, composed of smooth endoplasmic reticulum, which is responsible for calcium sequestration and release into the spine head and neck. The spine apparatus has recently been linked to synaptic plasticity in adult human cortical neurons. While the morphological heterogeneity of spines and their intracellular organization has been extensively demonstrated in animal models, the influence of spine apparatus organelles on critical signaling pathways, such as calcium-mediated dynamics, is less well known in human dendritic spines. In this study we used serial transmission electron microscopy to anatomically reconstruct nine human cortical spines in detail as a basis for modeling and simulation of the calcium dynamics between spine and dendrite. The anatomical study of reconstructed human dendritic spines revealed that the size of the postsynaptic density correlates with spine head volume and that the spine apparatus volume is proportional to the spine volume. Using a newly developed simulation pipeline, we have linked these findings to spine-to-dendrite calcium communication. While the absence of a spine apparatus, or the presence of a purely passive spine apparatus did not enable any of the reconstructed spines to relay a calcium signal to the dendritic shaft, the calcium-induced calcium release from this intracellular organelle allowed for finely tuned “all-or-nothing” spine-to-dendrite calcium coupling; controlled by spine morphology, neck plasticity, and ryanodine receptors. Our results suggest that spine apparatus organelles are strategically positioned in the neck of human dendritic spines and demonstrate their potential relevance to the maintenance and regulation of spine-to-dendrite calcium communication. |
format | Online Article Text |
id | pubmed-9071165 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-90711652022-05-06 Calcium modeling of spine apparatus-containing human dendritic spines demonstrates an “all-or-nothing” communication switch between the spine head and dendrite Rosado, James Bui, Viet Duc Haas, Carola A. Beck, Jürgen Queisser, Gillian Vlachos, Andreas PLoS Comput Biol Research Article Dendritic spines are highly dynamic neuronal compartments that control the synaptic transmission between neurons. Spines form ultrastructural units, coupling synaptic contact sites to the dendritic shaft and often harbor a spine apparatus organelle, composed of smooth endoplasmic reticulum, which is responsible for calcium sequestration and release into the spine head and neck. The spine apparatus has recently been linked to synaptic plasticity in adult human cortical neurons. While the morphological heterogeneity of spines and their intracellular organization has been extensively demonstrated in animal models, the influence of spine apparatus organelles on critical signaling pathways, such as calcium-mediated dynamics, is less well known in human dendritic spines. In this study we used serial transmission electron microscopy to anatomically reconstruct nine human cortical spines in detail as a basis for modeling and simulation of the calcium dynamics between spine and dendrite. The anatomical study of reconstructed human dendritic spines revealed that the size of the postsynaptic density correlates with spine head volume and that the spine apparatus volume is proportional to the spine volume. Using a newly developed simulation pipeline, we have linked these findings to spine-to-dendrite calcium communication. While the absence of a spine apparatus, or the presence of a purely passive spine apparatus did not enable any of the reconstructed spines to relay a calcium signal to the dendritic shaft, the calcium-induced calcium release from this intracellular organelle allowed for finely tuned “all-or-nothing” spine-to-dendrite calcium coupling; controlled by spine morphology, neck plasticity, and ryanodine receptors. Our results suggest that spine apparatus organelles are strategically positioned in the neck of human dendritic spines and demonstrate their potential relevance to the maintenance and regulation of spine-to-dendrite calcium communication. Public Library of Science 2022-04-25 /pmc/articles/PMC9071165/ /pubmed/35468131 http://dx.doi.org/10.1371/journal.pcbi.1010069 Text en © 2022 Rosado et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. |
spellingShingle | Research Article Rosado, James Bui, Viet Duc Haas, Carola A. Beck, Jürgen Queisser, Gillian Vlachos, Andreas Calcium modeling of spine apparatus-containing human dendritic spines demonstrates an “all-or-nothing” communication switch between the spine head and dendrite |
title | Calcium modeling of spine apparatus-containing human dendritic spines demonstrates an “all-or-nothing” communication switch between the spine head and dendrite |
title_full | Calcium modeling of spine apparatus-containing human dendritic spines demonstrates an “all-or-nothing” communication switch between the spine head and dendrite |
title_fullStr | Calcium modeling of spine apparatus-containing human dendritic spines demonstrates an “all-or-nothing” communication switch between the spine head and dendrite |
title_full_unstemmed | Calcium modeling of spine apparatus-containing human dendritic spines demonstrates an “all-or-nothing” communication switch between the spine head and dendrite |
title_short | Calcium modeling of spine apparatus-containing human dendritic spines demonstrates an “all-or-nothing” communication switch between the spine head and dendrite |
title_sort | calcium modeling of spine apparatus-containing human dendritic spines demonstrates an “all-or-nothing” communication switch between the spine head and dendrite |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9071165/ https://www.ncbi.nlm.nih.gov/pubmed/35468131 http://dx.doi.org/10.1371/journal.pcbi.1010069 |
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