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Spine-to-Dendrite Calcium Modeling Discloses Relevance for Precise Positioning of Ryanodine Receptor-Containing Spine Endoplasmic Reticulum
The endoplasmic reticulum (ER) forms a complex endomembrane network that reaches into the cellular compartments of a neuron, including dendritic spines. Recent work discloses that the spine ER is a dynamic structure that enters and leaves spines. While evidence exists that ER Ca(2+) release is invol...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Nature Publishing Group UK
2018
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6199256/ https://www.ncbi.nlm.nih.gov/pubmed/30353066 http://dx.doi.org/10.1038/s41598-018-33343-9 |
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author | Breit, Markus Kessler, Marcus Stepniewski, Martin Vlachos, Andreas Queisser, Gillian |
author_facet | Breit, Markus Kessler, Marcus Stepniewski, Martin Vlachos, Andreas Queisser, Gillian |
author_sort | Breit, Markus |
collection | PubMed |
description | The endoplasmic reticulum (ER) forms a complex endomembrane network that reaches into the cellular compartments of a neuron, including dendritic spines. Recent work discloses that the spine ER is a dynamic structure that enters and leaves spines. While evidence exists that ER Ca(2+) release is involved in synaptic plasticity, the role of spine ER morphology remains unknown. Combining a new 3D spine generator with 3D Ca(2+) modeling, we addressed the relevance of ER positioning on spine-to-dendrite Ca(2+) signaling. Our simulations, which account for Ca(2+) exchange on the plasma membrane and ER, show that spine ER needs to be present in distinct morphological conformations in order to overcome a barrier between the spine and dendritic shaft. We demonstrate that RyR-carrying spine ER promotes spine-to-dendrite Ca(2+) signals in a position-dependent manner. Our simulations indicate that RyR-carrying ER can initiate time-delayed Ca(2+) reverberation, depending on the precise position of the spine ER. Upon spine growth, structural reorganization of the ER restores spine-to-dendrite Ca(2+) communication, while maintaining aspects of Ca(2+) homeostasis in the spine head. Our work emphasizes the relevance of precise positioning of RyR-containing spine ER in regulating the strength and timing of spine Ca(2+) signaling, which could play an important role in tuning spine-to-dendrite Ca(2+) communication and homeostasis. |
format | Online Article Text |
id | pubmed-6199256 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2018 |
publisher | Nature Publishing Group UK |
record_format | MEDLINE/PubMed |
spelling | pubmed-61992562018-10-25 Spine-to-Dendrite Calcium Modeling Discloses Relevance for Precise Positioning of Ryanodine Receptor-Containing Spine Endoplasmic Reticulum Breit, Markus Kessler, Marcus Stepniewski, Martin Vlachos, Andreas Queisser, Gillian Sci Rep Article The endoplasmic reticulum (ER) forms a complex endomembrane network that reaches into the cellular compartments of a neuron, including dendritic spines. Recent work discloses that the spine ER is a dynamic structure that enters and leaves spines. While evidence exists that ER Ca(2+) release is involved in synaptic plasticity, the role of spine ER morphology remains unknown. Combining a new 3D spine generator with 3D Ca(2+) modeling, we addressed the relevance of ER positioning on spine-to-dendrite Ca(2+) signaling. Our simulations, which account for Ca(2+) exchange on the plasma membrane and ER, show that spine ER needs to be present in distinct morphological conformations in order to overcome a barrier between the spine and dendritic shaft. We demonstrate that RyR-carrying spine ER promotes spine-to-dendrite Ca(2+) signals in a position-dependent manner. Our simulations indicate that RyR-carrying ER can initiate time-delayed Ca(2+) reverberation, depending on the precise position of the spine ER. Upon spine growth, structural reorganization of the ER restores spine-to-dendrite Ca(2+) communication, while maintaining aspects of Ca(2+) homeostasis in the spine head. Our work emphasizes the relevance of precise positioning of RyR-containing spine ER in regulating the strength and timing of spine Ca(2+) signaling, which could play an important role in tuning spine-to-dendrite Ca(2+) communication and homeostasis. Nature Publishing Group UK 2018-10-23 /pmc/articles/PMC6199256/ /pubmed/30353066 http://dx.doi.org/10.1038/s41598-018-33343-9 Text en © The Author(s) 2018 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 Breit, Markus Kessler, Marcus Stepniewski, Martin Vlachos, Andreas Queisser, Gillian Spine-to-Dendrite Calcium Modeling Discloses Relevance for Precise Positioning of Ryanodine Receptor-Containing Spine Endoplasmic Reticulum |
title | Spine-to-Dendrite Calcium Modeling Discloses Relevance for Precise Positioning of Ryanodine Receptor-Containing Spine Endoplasmic Reticulum |
title_full | Spine-to-Dendrite Calcium Modeling Discloses Relevance for Precise Positioning of Ryanodine Receptor-Containing Spine Endoplasmic Reticulum |
title_fullStr | Spine-to-Dendrite Calcium Modeling Discloses Relevance for Precise Positioning of Ryanodine Receptor-Containing Spine Endoplasmic Reticulum |
title_full_unstemmed | Spine-to-Dendrite Calcium Modeling Discloses Relevance for Precise Positioning of Ryanodine Receptor-Containing Spine Endoplasmic Reticulum |
title_short | Spine-to-Dendrite Calcium Modeling Discloses Relevance for Precise Positioning of Ryanodine Receptor-Containing Spine Endoplasmic Reticulum |
title_sort | spine-to-dendrite calcium modeling discloses relevance for precise positioning of ryanodine receptor-containing spine endoplasmic reticulum |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6199256/ https://www.ncbi.nlm.nih.gov/pubmed/30353066 http://dx.doi.org/10.1038/s41598-018-33343-9 |
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