A Single Episode of Cortical Spreading Depolarization Increases mRNA Levels of Proinflammatory Cytokines, Calcitonin Gene-Related Peptide and Pannexin-1 Channels in the Cerebral Cortex
Cortical spreading depolarization (CSD) is the neuronal correlate of migraine aura and the reliable consequence of acute brain injury. The role of CSD in triggering headaches that follow migraine aura and brain injury remains to be uncertain. We examined whether a single CSD occurring in awake anima...
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description | Cortical spreading depolarization (CSD) is the neuronal correlate of migraine aura and the reliable consequence of acute brain injury. The role of CSD in triggering headaches that follow migraine aura and brain injury remains to be uncertain. We examined whether a single CSD occurring in awake animals modified the expression of proinflammatory cytokines (Il1b, TNF, and Il6) and endogenous mediators of nociception/neuroinflammation-pannexin 1 (Panx1) channel and calcitonin gene-related peptide (CGRP), transforming growth factor beta (TGFb) in the cortex. Unilateral microinjury of the somatosensory cortex triggering a single CSD was produced in awake Wistar rats. Three hours later, tissue samples from the lesioned cortex, intact ipsilesional cortex invaded by CSD, and homologous areas of the contralateral sham-treated cortex were harvested and analyzed using qPCR. Three hours post-injury, intact CSD-exposed cortexes increased TNF, Il1b, Panx1, and CGRP mRNA levels. The strongest upregulation of proinflammatory cytokines was observed at the injury site, while CGRP and Panx1 were upregulated more strongly in the intact cortexes invaded by CSD. A single CSD is sufficient to produce low-grade parenchymal neuroinflammation with simultaneous overexpression of Panx1 and CGRP. The CSD-induced molecular changes may contribute to pathogenic mechanisms of migraine pain and post-injury headache. |
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The role of CSD in triggering headaches that follow migraine aura and brain injury remains to be uncertain. We examined whether a single CSD occurring in awake animals modified the expression of proinflammatory cytokines (Il1b, TNF, and Il6) and endogenous mediators of nociception/neuroinflammation-pannexin 1 (Panx1) channel and calcitonin gene-related peptide (CGRP), transforming growth factor beta (TGFb) in the cortex. Unilateral microinjury of the somatosensory cortex triggering a single CSD was produced in awake Wistar rats. Three hours later, tissue samples from the lesioned cortex, intact ipsilesional cortex invaded by CSD, and homologous areas of the contralateral sham-treated cortex were harvested and analyzed using qPCR. Three hours post-injury, intact CSD-exposed cortexes increased TNF, Il1b, Panx1, and CGRP mRNA levels. The strongest upregulation of proinflammatory cytokines was observed at the injury site, while CGRP and Panx1 were upregulated more strongly in the intact cortexes invaded by CSD. A single CSD is sufficient to produce low-grade parenchymal neuroinflammation with simultaneous overexpression of Panx1 and CGRP. The CSD-induced molecular changes may contribute to pathogenic mechanisms of migraine pain and post-injury headache.</description><identifier>ISSN: 1422-0067</identifier><identifier>EISSN: 1422-0067</identifier><identifier>DOI: 10.3390/ijms24010085</identifier><identifier>PMID: 36613527</identifier><language>eng</language><publisher>Switzerland: MDPI</publisher><subject>Animals ; Brief Report ; Calcitonin Gene-Related Peptide - metabolism ; Cerebral Cortex - metabolism ; Cortical Spreading Depression - physiology ; Cytokines - genetics ; Cytokines - metabolism ; Epilepsy - metabolism ; Interleukin-1 - metabolism ; Migraine Disorders - metabolism ; Neuroinflammatory Diseases ; Rats ; Rats, Wistar ; RNA, Messenger - genetics ; RNA, Messenger - metabolism</subject><ispartof>International journal of molecular sciences, 2022-12, Vol.24 (1), p.85</ispartof><rights>2022 by the authors. 2022</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c450t-8334c6f42d033302eef4c49e93cdcda13f038b36831eb2d9acf2a73ae94e4cb43</citedby><cites>FETCH-LOGICAL-c450t-8334c6f42d033302eef4c49e93cdcda13f038b36831eb2d9acf2a73ae94e4cb43</cites><orcidid>0000-0002-6668-958X ; 0000-0003-0336-606X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9820231/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9820231/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36613527$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Volobueva, Maria N</creatorcontrib><creatorcontrib>Suleymanova, Elena M</creatorcontrib><creatorcontrib>Smirnova, Maria P</creatorcontrib><creatorcontrib>Bolshakov, Alexey P</creatorcontrib><creatorcontrib>Vinogradova, Lyudmila V</creatorcontrib><title>A Single Episode of Cortical Spreading Depolarization Increases mRNA Levels of Proinflammatory Cytokines, Calcitonin Gene-Related Peptide and Pannexin-1 Channels in the Cerebral Cortex</title><title>International journal of molecular sciences</title><addtitle>Int J Mol Sci</addtitle><description>Cortical spreading depolarization (CSD) is the neuronal correlate of migraine aura and the reliable consequence of acute brain injury. The role of CSD in triggering headaches that follow migraine aura and brain injury remains to be uncertain. We examined whether a single CSD occurring in awake animals modified the expression of proinflammatory cytokines (Il1b, TNF, and Il6) and endogenous mediators of nociception/neuroinflammation-pannexin 1 (Panx1) channel and calcitonin gene-related peptide (CGRP), transforming growth factor beta (TGFb) in the cortex. Unilateral microinjury of the somatosensory cortex triggering a single CSD was produced in awake Wistar rats. Three hours later, tissue samples from the lesioned cortex, intact ipsilesional cortex invaded by CSD, and homologous areas of the contralateral sham-treated cortex were harvested and analyzed using qPCR. Three hours post-injury, intact CSD-exposed cortexes increased TNF, Il1b, Panx1, and CGRP mRNA levels. The strongest upregulation of proinflammatory cytokines was observed at the injury site, while CGRP and Panx1 were upregulated more strongly in the intact cortexes invaded by CSD. A single CSD is sufficient to produce low-grade parenchymal neuroinflammation with simultaneous overexpression of Panx1 and CGRP. The CSD-induced molecular changes may contribute to pathogenic mechanisms of migraine pain and post-injury headache.</description><subject>Animals</subject><subject>Brief Report</subject><subject>Calcitonin Gene-Related Peptide - metabolism</subject><subject>Cerebral Cortex - metabolism</subject><subject>Cortical Spreading Depression - physiology</subject><subject>Cytokines - genetics</subject><subject>Cytokines - metabolism</subject><subject>Epilepsy - metabolism</subject><subject>Interleukin-1 - metabolism</subject><subject>Migraine Disorders - metabolism</subject><subject>Neuroinflammatory Diseases</subject><subject>Rats</subject><subject>Rats, Wistar</subject><subject>RNA, Messenger - genetics</subject><subject>RNA, Messenger - metabolism</subject><issn>1422-0067</issn><issn>1422-0067</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVUcFO3DAUjKpWhdLeeq587IFQ28-bTS6VVikFpFVB0J4tx3lhTR072F7E9sv4PLyCouX0Rpp580ZviuIzo0cADf1mbsbIBWWU1rM3xT4TnJeUVvO3O3iv-BDjDaUc-Kx5X-xBVTGY8fl-8bAgV8ZdWyTHk4m-R-IH0vqQjFaWXE0BVZ958gMnb1Uw_1Qy3pEzpzMTMZLx8teCLPEObdyuXgRv3GDVOKrkw4a0m-T_GofxkLTKapO8M46coMPyEq1K2JMLnJLJh5XLWDmH98aVjLSrLc6uWZ9WSFoM2IUcapsO7z8W7wZlI356ngfFn5_Hv9vTcnl-ctYulqUWM5rKGkDoahC8pwBAOeIgtGiwAd3rXjEYKNQdVDUw7HjfKD1wNQeFjUChOwEHxfcn32ndjdhrdCmHkFMwowob6ZWRrxlnVvLa38mm5vnfLBt8fTYI_naNMcnRRI3WKod-HSWfV6ypWVNBlh4-SXXwMQYcXs4wKrdly92ys_zLbrQX8f924RHJKaoA</recordid><startdate>20221221</startdate><enddate>20221221</enddate><creator>Volobueva, Maria N</creator><creator>Suleymanova, Elena M</creator><creator>Smirnova, Maria P</creator><creator>Bolshakov, Alexey P</creator><creator>Vinogradova, Lyudmila V</creator><general>MDPI</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-6668-958X</orcidid><orcidid>https://orcid.org/0000-0003-0336-606X</orcidid></search><sort><creationdate>20221221</creationdate><title>A Single Episode of Cortical Spreading Depolarization Increases mRNA Levels of Proinflammatory Cytokines, Calcitonin Gene-Related Peptide and Pannexin-1 Channels in the Cerebral Cortex</title><author>Volobueva, Maria N ; Suleymanova, Elena M ; Smirnova, Maria P ; Bolshakov, Alexey P ; Vinogradova, Lyudmila V</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c450t-8334c6f42d033302eef4c49e93cdcda13f038b36831eb2d9acf2a73ae94e4cb43</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Animals</topic><topic>Brief Report</topic><topic>Calcitonin Gene-Related Peptide - metabolism</topic><topic>Cerebral Cortex - metabolism</topic><topic>Cortical Spreading Depression - physiology</topic><topic>Cytokines - genetics</topic><topic>Cytokines - metabolism</topic><topic>Epilepsy - metabolism</topic><topic>Interleukin-1 - metabolism</topic><topic>Migraine Disorders - metabolism</topic><topic>Neuroinflammatory Diseases</topic><topic>Rats</topic><topic>Rats, Wistar</topic><topic>RNA, Messenger - genetics</topic><topic>RNA, Messenger - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Volobueva, Maria N</creatorcontrib><creatorcontrib>Suleymanova, Elena M</creatorcontrib><creatorcontrib>Smirnova, Maria P</creatorcontrib><creatorcontrib>Bolshakov, Alexey P</creatorcontrib><creatorcontrib>Vinogradova, Lyudmila V</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>International journal of molecular sciences</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Volobueva, Maria N</au><au>Suleymanova, Elena M</au><au>Smirnova, Maria P</au><au>Bolshakov, Alexey P</au><au>Vinogradova, Lyudmila V</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A Single Episode of Cortical Spreading Depolarization Increases mRNA Levels of Proinflammatory Cytokines, Calcitonin Gene-Related Peptide and Pannexin-1 Channels in the Cerebral Cortex</atitle><jtitle>International journal of molecular sciences</jtitle><addtitle>Int J Mol Sci</addtitle><date>2022-12-21</date><risdate>2022</risdate><volume>24</volume><issue>1</issue><spage>85</spage><pages>85-</pages><issn>1422-0067</issn><eissn>1422-0067</eissn><abstract>Cortical spreading depolarization (CSD) is the neuronal correlate of migraine aura and the reliable consequence of acute brain injury. The role of CSD in triggering headaches that follow migraine aura and brain injury remains to be uncertain. We examined whether a single CSD occurring in awake animals modified the expression of proinflammatory cytokines (Il1b, TNF, and Il6) and endogenous mediators of nociception/neuroinflammation-pannexin 1 (Panx1) channel and calcitonin gene-related peptide (CGRP), transforming growth factor beta (TGFb) in the cortex. Unilateral microinjury of the somatosensory cortex triggering a single CSD was produced in awake Wistar rats. Three hours later, tissue samples from the lesioned cortex, intact ipsilesional cortex invaded by CSD, and homologous areas of the contralateral sham-treated cortex were harvested and analyzed using qPCR. Three hours post-injury, intact CSD-exposed cortexes increased TNF, Il1b, Panx1, and CGRP mRNA levels. The strongest upregulation of proinflammatory cytokines was observed at the injury site, while CGRP and Panx1 were upregulated more strongly in the intact cortexes invaded by CSD. A single CSD is sufficient to produce low-grade parenchymal neuroinflammation with simultaneous overexpression of Panx1 and CGRP. The CSD-induced molecular changes may contribute to pathogenic mechanisms of migraine pain and post-injury headache.</abstract><cop>Switzerland</cop><pub>MDPI</pub><pmid>36613527</pmid><doi>10.3390/ijms24010085</doi><orcidid>https://orcid.org/0000-0002-6668-958X</orcidid><orcidid>https://orcid.org/0000-0003-0336-606X</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Brief Report Calcitonin Gene-Related Peptide - metabolism Cerebral Cortex - metabolism Cortical Spreading Depression - physiology Cytokines - genetics Cytokines - metabolism Epilepsy - metabolism Interleukin-1 - metabolism Migraine Disorders - metabolism Neuroinflammatory Diseases Rats Rats, Wistar RNA, Messenger - genetics RNA, Messenger - metabolism |
title | A Single Episode of Cortical Spreading Depolarization Increases mRNA Levels of Proinflammatory Cytokines, Calcitonin Gene-Related Peptide and Pannexin-1 Channels in the Cerebral Cortex |
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