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      Synaptic neuron-astrocyte communication is supported by an order of magnitude analysis of inositol tris-phosphate diffusion at the nanoscale in a model of peri-synaptic astrocyte projection

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          Abstract

          Background

          Astrocytes were conceived for decades only as supporting cells of the brain. However, the observation of Ca2+ waves in astrocyte synctitia, their neurotransmitter receptor expression and gliotransmitter secretion suggested a role in information handling, conception that has some controversies. Synaptic Neuron-Astrocyte metabotropic communication mediated by Inositol tris-phosphate (SN-AmcIP3) is supported by different reports. However, some models contradict this idea and Ca2+ stores are 1000 ± 325 nm apart from the Postsynaptic Density in the Perisynaptic Astrocyte Projections (PAP’s), suggesting that SN-AmcIP3 is extrasynaptic. However, this assumption does not consider IP3 Diffusion Coefficient ( Dab), that activates IP3 Receptor (IP3R) releasing Ca2+ from intracellular stores.

          Results

          In this work we idealized a model of a PAP (PAPm) to perform an order of magnitude analysis of IP3 diffusion using a transient mass diffusion model. This model shows that IP3 forms a concentration gradient along the PAPm that reaches the steady state in milliseconds, three orders of magnitude before IP3 degradation. The model predicts that IP3 concentration near the Ca2+ stores may activate IP3R, depending upon Phospholipase C (PLC) number and activity. Moreover, the PAPm supports that IP3 and extracellular Ca2+ entry synergize to promote global Ca2+ transients.

          Conclusion

          The model presented here indicates that Ca2+ stores position in PAP’s does not limit SN-AmcIP3.

          Electronic supplementary material

          The online version of this article (10.1186/s13628-018-0043-3) contains supplementary material, which is available to authorized users.

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          Most cited references46

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          Diversity of astrocyte functions and phenotypes in neural circuits.

          Astrocytes tile the entire CNS. They are vital for neural circuit function, but have traditionally been viewed as simple, homogenous cells that serve the same essential supportive roles everywhere. Here, we summarize breakthroughs that instead indicate that astrocytes represent a population of complex and functionally diverse cells. Physiological diversity of astrocytes is apparent between different brain circuits and microcircuits, and individual astrocytes display diverse signaling in subcellular compartments. With respect to injury and disease, astrocytes undergo diverse phenotypic changes that may be protective or causative with regard to pathology in a context-dependent manner. These new insights herald the concept that astrocytes represent a diverse population of genetically tractable cells that mediate neural circuit-specific roles in health and disease.
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            Tripartite synapses: glia, the unacknowledged partner.

            According to the classical view of the nervous system, the numerically superior glial cells have inferior roles in that they provide an ideal environment for neuronal-cell function. However, there is a wave of new information suggesting that glia are intimately involved in the active control of neuronal activity and synaptic neurotransmission. Recent evidence shows that glia respond to neuronal activity with an elevation of their internal Ca2+ concentration, which triggers the release of chemical transmitters from glia themselves and, in turn, causes feedback regulation of neuronal activity and synaptic strength. In view of these new insights, this article suggests that perisynaptic Schwann cells and synaptically associated astrocytes should be viewed as integral modulatory elements of tripartite synapses.
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              Inositol trisphosphate receptor Ca2+ release channels.

              The inositol 1,4,5-trisphosphate (InsP3) receptors (InsP3Rs) are a family of Ca2+ release channels localized predominately in the endoplasmic reticulum of all cell types. They function to release Ca2+ into the cytoplasm in response to InsP3 produced by diverse stimuli, generating complex local and global Ca2+ signals that regulate numerous cell physiological processes ranging from gene transcription to secretion to learning and memory. The InsP3R is a calcium-selective cation channel whose gating is regulated not only by InsP3, but by other ligands as well, in particular cytoplasmic Ca2+. Over the last decade, detailed quantitative studies of InsP3R channel function and its regulation by ligands and interacting proteins have provided new insights into a remarkable richness of channel regulation and of the structural aspects that underlie signal transduction and permeation. Here, we focus on these developments and review and synthesize the literature regarding the structure and single-channel properties of the InsP3R.
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                Author and article information

                Contributors
                pavel73@hotmail.com
                horacio.montesdeoca77@gmail.com
                Journal
                BMC Biophys
                BMC Biophys
                BMC Biophysics
                BioMed Central (London )
                2046-1682
                12 February 2018
                12 February 2018
                2018
                : 11
                : 3
                Affiliations
                ISNI 0000 0000 8637 5954, GRID grid.419204.a, Unit of Dynamic Neurobiology, Neurochemistry Deprtment Instituto Nacional de Neurología y Neurocirugía, ; Insurgentes Sur #3877, Col. La Fama, C.P. 14269 Ciudad de México, Mexico
                Author information
                http://orcid.org/0000-0003-3537-4080
                Article
                43
                10.1186/s13628-018-0043-3
                5809920
                24b0f036-1dab-4f4d-96b2-7b33293c2e0a
                © The Author(s). 2018

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided 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 Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 14 August 2017
                : 30 January 2018
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2018

                Biophysics
                pap,neuron-astrocyte communication,tripartite synapse,astrocyte,ca2+ stores
                Biophysics
                pap, neuron-astrocyte communication, tripartite synapse, astrocyte, ca2+ stores

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