Cargando…

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...

Descripción completa

Detalles Bibliográficos
Autores principales: Rosado, James, Bui, Viet Duc, Haas, Carola A., Beck, Jürgen, Queisser, Gillian, Vlachos, Andreas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
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
_version_ 1784700792791367680
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
work_keys_str_mv AT rosadojames calciummodelingofspineapparatuscontaininghumandendriticspinesdemonstratesanallornothingcommunicationswitchbetweenthespineheadanddendrite
AT buivietduc calciummodelingofspineapparatuscontaininghumandendriticspinesdemonstratesanallornothingcommunicationswitchbetweenthespineheadanddendrite
AT haascarolaa calciummodelingofspineapparatuscontaininghumandendriticspinesdemonstratesanallornothingcommunicationswitchbetweenthespineheadanddendrite
AT beckjurgen calciummodelingofspineapparatuscontaininghumandendriticspinesdemonstratesanallornothingcommunicationswitchbetweenthespineheadanddendrite
AT queissergillian calciummodelingofspineapparatuscontaininghumandendriticspinesdemonstratesanallornothingcommunicationswitchbetweenthespineheadanddendrite
AT vlachosandreas calciummodelingofspineapparatuscontaininghumandendriticspinesdemonstratesanallornothingcommunicationswitchbetweenthespineheadanddendrite