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Modeling the heterogeneity of sodium and calcium homeostasis between cortical and hippocampal astrocytes and its impact on bioenergetics
Emerging evidence indicates that neuronal activity-evoked changes in sodium concentration in astrocytes Na represent a special form of excitability, which is tightly linked to all other major ions in the astrocyte and extracellular space, as well as to bioenergetics, neurotransmitter uptake, and neu...
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Published in: | Frontiers in cellular neuroscience 2023-01, Vol.17, p.1035553-1035553 |
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description | Emerging evidence indicates that neuronal activity-evoked changes in sodium concentration in astrocytes Na
represent a special form of excitability, which is tightly linked to all other major ions in the astrocyte and extracellular space, as well as to bioenergetics, neurotransmitter uptake, and neurovascular coupling. Recently, one of us reported that Na
transients in the neocortex have a significantly higher amplitude than those in the hippocampus. Based on the extensive data from that study, here we develop a detailed biophysical model to further understand the origin of this heterogeneity and how it affects bioenergetics in the astrocytes. In addition to closely fitting the observed experimental Na
changes under different conditions, our model shows that the heterogeneity in Na
signaling leads to substantial differences in the dynamics of astrocytic Ca
signals in the two brain regions, and leaves cortical astrocytes more susceptible to Na
and Ca
overload under metabolic stress. The model also predicts that activity-evoked Na
transients result in significantly larger ATP consumption in cortical astrocytes than in the hippocampus. The difference in ATP consumption is mainly due to the different expression levels of NMDA receptors in the two regions. We confirm predictions from our model experimentally by fluorescence-based measurement of glutamate-induced changes in ATP levels in neocortical and hippocampal astrocytes in the absence and presence of the NMDA receptor's antagonist (2R)-amino-5-phosphonovaleric acid. |
doi_str_mv | 10.3389/fncel.2023.1035553 |
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represent a special form of excitability, which is tightly linked to all other major ions in the astrocyte and extracellular space, as well as to bioenergetics, neurotransmitter uptake, and neurovascular coupling. Recently, one of us reported that Na
transients in the neocortex have a significantly higher amplitude than those in the hippocampus. Based on the extensive data from that study, here we develop a detailed biophysical model to further understand the origin of this heterogeneity and how it affects bioenergetics in the astrocytes. In addition to closely fitting the observed experimental Na
changes under different conditions, our model shows that the heterogeneity in Na
signaling leads to substantial differences in the dynamics of astrocytic Ca
signals in the two brain regions, and leaves cortical astrocytes more susceptible to Na
and Ca
overload under metabolic stress. The model also predicts that activity-evoked Na
transients result in significantly larger ATP consumption in cortical astrocytes than in the hippocampus. The difference in ATP consumption is mainly due to the different expression levels of NMDA receptors in the two regions. We confirm predictions from our model experimentally by fluorescence-based measurement of glutamate-induced changes in ATP levels in neocortical and hippocampal astrocytes in the absence and presence of the NMDA receptor's antagonist (2R)-amino-5-phosphonovaleric acid.</description><identifier>ISSN: 1662-5102</identifier><identifier>EISSN: 1662-5102</identifier><identifier>DOI: 10.3389/fncel.2023.1035553</identifier><identifier>PMID: 36794264</identifier><language>eng</language><publisher>Switzerland: Frontiers Research Foundation</publisher><subject>Astrocytes ; astrocytic Ca2+ signaling ; astrocytic Na+ signaling ; ATP ; Bioenergetics ; Brain ; Calcium homeostasis ; Calcium signalling ; Cellular Neuroscience ; Excitability ; Exports ; Glutamic acid receptors (ionotropic) ; heterogeneity in astrocytic Na+ ; Hippocampus ; Homeostasis ; Iontophoresis ; Ligands ; N-Methyl-D-aspartic acid receptors ; Neocortex</subject><ispartof>Frontiers in cellular neuroscience, 2023-01, Vol.17, p.1035553-1035553</ispartof><rights>Copyright © 2023 Thapaliya, Pape, Rose and Ullah.</rights><rights>2023. This work is licensed under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Copyright © 2023 Thapaliya, Pape, Rose and Ullah. 2023 Thapaliya, Pape, Rose and Ullah</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c496t-3abed959191f5c6c7812ce0104c827cbd6ee9260418e75353bdb2affad1b46873</citedby><cites>FETCH-LOGICAL-c496t-3abed959191f5c6c7812ce0104c827cbd6ee9260418e75353bdb2affad1b46873</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/2770806803/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2770806803?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36794264$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Thapaliya, Pawan</creatorcontrib><creatorcontrib>Pape, Nils</creatorcontrib><creatorcontrib>Rose, Christine R</creatorcontrib><creatorcontrib>Ullah, Ghanim</creatorcontrib><title>Modeling the heterogeneity of sodium and calcium homeostasis between cortical and hippocampal astrocytes and its impact on bioenergetics</title><title>Frontiers in cellular neuroscience</title><addtitle>Front Cell Neurosci</addtitle><description>Emerging evidence indicates that neuronal activity-evoked changes in sodium concentration in astrocytes Na
represent a special form of excitability, which is tightly linked to all other major ions in the astrocyte and extracellular space, as well as to bioenergetics, neurotransmitter uptake, and neurovascular coupling. Recently, one of us reported that Na
transients in the neocortex have a significantly higher amplitude than those in the hippocampus. Based on the extensive data from that study, here we develop a detailed biophysical model to further understand the origin of this heterogeneity and how it affects bioenergetics in the astrocytes. In addition to closely fitting the observed experimental Na
changes under different conditions, our model shows that the heterogeneity in Na
signaling leads to substantial differences in the dynamics of astrocytic Ca
signals in the two brain regions, and leaves cortical astrocytes more susceptible to Na
and Ca
overload under metabolic stress. The model also predicts that activity-evoked Na
transients result in significantly larger ATP consumption in cortical astrocytes than in the hippocampus. The difference in ATP consumption is mainly due to the different expression levels of NMDA receptors in the two regions. We confirm predictions from our model experimentally by fluorescence-based measurement of glutamate-induced changes in ATP levels in neocortical and hippocampal astrocytes in the absence and presence of the NMDA receptor's antagonist (2R)-amino-5-phosphonovaleric acid.</description><subject>Astrocytes</subject><subject>astrocytic Ca2+ signaling</subject><subject>astrocytic Na+ signaling</subject><subject>ATP</subject><subject>Bioenergetics</subject><subject>Brain</subject><subject>Calcium homeostasis</subject><subject>Calcium signalling</subject><subject>Cellular Neuroscience</subject><subject>Excitability</subject><subject>Exports</subject><subject>Glutamic acid receptors (ionotropic)</subject><subject>heterogeneity in astrocytic Na+</subject><subject>Hippocampus</subject><subject>Homeostasis</subject><subject>Iontophoresis</subject><subject>Ligands</subject><subject>N-Methyl-D-aspartic acid receptors</subject><subject>Neocortex</subject><issn>1662-5102</issn><issn>1662-5102</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNpdkk1v1DAQhiMEoqXwBzggS1y47OKvOPYFCVV8VCriAmfLsScbr5I42E7R_gN-Ns7uUrWcPPa884zHfqvqNcFbxqR6300Whi3FlG0JZnVdsyfVJRGCbmqC6dMH8UX1IqU9xoIKLp9XF0w0ipf4svrzLTgY_LRDuQfUQ4YYdjCBzwcUOpSC88uIzOSQNYNd4z6MEFI2ySfUQv4NMCEbYvZFcBT2fp6DNeO87lOOwR4ypGPK54R8SdiMwoRaH0qnuINSm15WzzozJHh1Xq-qn58__bj-urn9_uXm-uPtxnIl8oaZFpyqFVGkq62wjSTUAiaYW0kb2zoBoKjAnEhoalaz1rXUdJ1xpOVCNuyqujlxXTB7PUc_mnjQwXh9PAhxp806zABayc7VluOVzyUQ2fCOC-qc4lLWVhbWhxNrXtoRnIUpRzM8gj7OTL7Xu3CnlaJUNrgA3p0BMfxaIGU9-lQ-dTAThCVp2jQNx0zStdfb_6T7sMSpPNWqwhILiVlR0ZPKxpBShO7-MgTr1TT6aBq9mkafTVOK3jwc477kn0vYXyuWwdM</recordid><startdate>20230130</startdate><enddate>20230130</enddate><creator>Thapaliya, Pawan</creator><creator>Pape, Nils</creator><creator>Rose, Christine R</creator><creator>Ullah, Ghanim</creator><general>Frontiers Research Foundation</general><general>Frontiers Media S.A</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7XB</scope><scope>88I</scope><scope>8FE</scope><scope>8FH</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>LK8</scope><scope>M2P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20230130</creationdate><title>Modeling the heterogeneity of sodium and calcium homeostasis between cortical and hippocampal astrocytes and its impact on bioenergetics</title><author>Thapaliya, Pawan ; Pape, Nils ; Rose, Christine R ; Ullah, Ghanim</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c496t-3abed959191f5c6c7812ce0104c827cbd6ee9260418e75353bdb2affad1b46873</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Astrocytes</topic><topic>astrocytic Ca2+ signaling</topic><topic>astrocytic Na+ signaling</topic><topic>ATP</topic><topic>Bioenergetics</topic><topic>Brain</topic><topic>Calcium homeostasis</topic><topic>Calcium signalling</topic><topic>Cellular Neuroscience</topic><topic>Excitability</topic><topic>Exports</topic><topic>Glutamic acid receptors (ionotropic)</topic><topic>heterogeneity in astrocytic Na+</topic><topic>Hippocampus</topic><topic>Homeostasis</topic><topic>Iontophoresis</topic><topic>Ligands</topic><topic>N-Methyl-D-aspartic acid receptors</topic><topic>Neocortex</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Thapaliya, Pawan</creatorcontrib><creatorcontrib>Pape, Nils</creatorcontrib><creatorcontrib>Rose, Christine R</creatorcontrib><creatorcontrib>Ullah, Ghanim</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Science Database (Alumni Edition)</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>AUTh Library subscriptions: ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>Biological Sciences</collection><collection>ProQuest Science Journals</collection><collection>Biological Science Database</collection><collection>Publicly Available Content (ProQuest)</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>ProQuest Central Basic</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>Frontiers in cellular neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Thapaliya, Pawan</au><au>Pape, Nils</au><au>Rose, Christine R</au><au>Ullah, Ghanim</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Modeling the heterogeneity of sodium and calcium homeostasis between cortical and hippocampal astrocytes and its impact on bioenergetics</atitle><jtitle>Frontiers in cellular neuroscience</jtitle><addtitle>Front Cell Neurosci</addtitle><date>2023-01-30</date><risdate>2023</risdate><volume>17</volume><spage>1035553</spage><epage>1035553</epage><pages>1035553-1035553</pages><issn>1662-5102</issn><eissn>1662-5102</eissn><abstract>Emerging evidence indicates that neuronal activity-evoked changes in sodium concentration in astrocytes Na
represent a special form of excitability, which is tightly linked to all other major ions in the astrocyte and extracellular space, as well as to bioenergetics, neurotransmitter uptake, and neurovascular coupling. Recently, one of us reported that Na
transients in the neocortex have a significantly higher amplitude than those in the hippocampus. Based on the extensive data from that study, here we develop a detailed biophysical model to further understand the origin of this heterogeneity and how it affects bioenergetics in the astrocytes. In addition to closely fitting the observed experimental Na
changes under different conditions, our model shows that the heterogeneity in Na
signaling leads to substantial differences in the dynamics of astrocytic Ca
signals in the two brain regions, and leaves cortical astrocytes more susceptible to Na
and Ca
overload under metabolic stress. The model also predicts that activity-evoked Na
transients result in significantly larger ATP consumption in cortical astrocytes than in the hippocampus. The difference in ATP consumption is mainly due to the different expression levels of NMDA receptors in the two regions. We confirm predictions from our model experimentally by fluorescence-based measurement of glutamate-induced changes in ATP levels in neocortical and hippocampal astrocytes in the absence and presence of the NMDA receptor's antagonist (2R)-amino-5-phosphonovaleric acid.</abstract><cop>Switzerland</cop><pub>Frontiers Research Foundation</pub><pmid>36794264</pmid><doi>10.3389/fncel.2023.1035553</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Astrocytes astrocytic Ca2+ signaling astrocytic Na+ signaling ATP Bioenergetics Brain Calcium homeostasis Calcium signalling Cellular Neuroscience Excitability Exports Glutamic acid receptors (ionotropic) heterogeneity in astrocytic Na+ Hippocampus Homeostasis Iontophoresis Ligands N-Methyl-D-aspartic acid receptors Neocortex |
title | Modeling the heterogeneity of sodium and calcium homeostasis between cortical and hippocampal astrocytes and its impact on bioenergetics |
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