Cargando…

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...

Descripción completa

Detalles Bibliográficos
Autores principales: Breit, Markus, Kessler, Marcus, Stepniewski, Martin, Vlachos, Andreas, Queisser, Gillian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2018
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
_version_ 1783365104741384192
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
work_keys_str_mv AT breitmarkus spinetodendritecalciummodelingdisclosesrelevanceforprecisepositioningofryanodinereceptorcontainingspineendoplasmicreticulum
AT kesslermarcus spinetodendritecalciummodelingdisclosesrelevanceforprecisepositioningofryanodinereceptorcontainingspineendoplasmicreticulum
AT stepniewskimartin spinetodendritecalciummodelingdisclosesrelevanceforprecisepositioningofryanodinereceptorcontainingspineendoplasmicreticulum
AT vlachosandreas spinetodendritecalciummodelingdisclosesrelevanceforprecisepositioningofryanodinereceptorcontainingspineendoplasmicreticulum
AT queissergillian spinetodendritecalciummodelingdisclosesrelevanceforprecisepositioningofryanodinereceptorcontainingspineendoplasmicreticulum