Serotonergic mechanisms of trigeminal meningeal nociception: Implications for migraine pain
Serotonergic mechanisms play a central role in migraine pathology. However, the region-specific effects of serotonin (5-HT) mediated via multiple types of receptors in the nociceptive system are poorly understood. Using extracellular and patch-clamp recordings, we studied the action of 5-HT on the e...
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| Veröffentlicht in: | Neuropharmacology 2017-04, Vol.116, p.160-173 |
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| creator | Kilinc, Erkan Guerrero-Toro, Cindy Zakharov, Andrey Vitale, Carmela Gubert-Olive, Max Koroleva, Ksenia Timonina, Arina Luz, Liliana L. Shelukhina, Irina Giniatullina, Raisa Tore, Fatma Safronov, Boris V. Giniatullin, Rashid |
| description | Serotonergic mechanisms play a central role in migraine pathology. However, the region-specific effects of serotonin (5-HT) mediated via multiple types of receptors in the nociceptive system are poorly understood. Using extracellular and patch-clamp recordings, we studied the action of 5-HT on the excitability of peripheral and central terminals of trigeminal afferents. 5-HT evoked long-lasting TTX-sensitive firing in the peripheral terminals of meningeal afferents, the origin site of migraine pain. Cluster analysis revealed that in majority of nociceptive fibers 5-HT induced either transient or persistent spiking activity with prevailing delta and theta rhythms. The 5-HT3-receptor antagonist MDL-72222 or 5-HT1B/D-receptor antagonist GR127935 largely reduced, but their combination completely prevented the excitatory pro-nociceptive action of 5-HT. The 5-HT3 agonist mCPBG activated spikes in MDL-72222-dependent manner but the 5HT-1 receptor agonist sumatriptan did not affect the nociceptive firing. 5-HT also triggered peripheral CGRP release in meninges, which was blocked by MDL-72222.5-HT evoked fast membrane currents and Ca2+ transients in a fraction of trigeminal neurons. Immunohistochemistry showed expression of 5-HT3A receptors in fibers innervating meninges. Endogenous release of 5-HT from degranulated mast cells increased nociceptive firing. Low pH but not histamine strongly activated firing. 5-HT reduced monosynaptic inputs from trigeminal Aδ- and C-afferents to the upper cervical lamina I neurons and this effect was blocked by MDL-72222. Consistent with central inhibitory effect, 5-HT reduced CGRP release in the brainstem slices. In conclusion, 5-HT evokes powerful pro-nociceptive peripheral and anti-nociceptive central effects in trigeminal system transmitting migraine pain.
•5-HT induced a robust nociceptive activity in peripheral nerve terminals in meninges.•5-HT3 receptors contributed to pro-nociceptive action 5-HT and CGRP release.•Cluster analysis revealed fibers with remarkably long-lasting firing activity.•In contrast to periphery, 5-HT inhibited central nerve terminals of nociceptors. |
| doi_str_mv | 10.1016/j.neuropharm.2016.12.024 |
| format | Article |
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•5-HT induced a robust nociceptive activity in peripheral nerve terminals in meninges.•5-HT3 receptors contributed to pro-nociceptive action 5-HT and CGRP release.•Cluster analysis revealed fibers with remarkably long-lasting firing activity.•In contrast to periphery, 5-HT inhibited central nerve terminals of nociceptors.</description><identifier>ISSN: 0028-3908</identifier><identifier>EISSN: 1873-7064</identifier><identifier>DOI: 10.1016/j.neuropharm.2016.12.024</identifier><identifier>PMID: 28025094</identifier><language>eng</language><publisher>England: Elsevier Ltd</publisher><subject>5-HT3 receptor ; Action Potentials - drug effects ; Action Potentials - physiology ; Animals ; Calcitonin Gene-Related Peptide - metabolism ; Calcium - metabolism ; Cations, Divalent - metabolism ; Female ; Male ; Meninges ; Migraine ; Migraine Disorders - metabolism ; Neurons, Afferent - cytology ; Neurons, Afferent - drug effects ; Neurons, Afferent - metabolism ; Nociception - drug effects ; Nociception - physiology ; Patch-Clamp Techniques ; Rats, Wistar ; Receptors, Serotonin - metabolism ; Serotonin ; Serotonin - metabolism ; Serotonin Agents - pharmacology ; Spike ; Tissue Culture Techniques ; Trigeminal nerve ; Trigeminal Nerve - cytology ; Trigeminal Nerve - drug effects ; Trigeminal Nerve - metabolism ; TRPV Cation Channels - metabolism ; Voltage-Sensitive Dye Imaging</subject><ispartof>Neuropharmacology, 2017-04, Vol.116, p.160-173</ispartof><rights>2016 Elsevier Ltd</rights><rights>Copyright © 2016 Elsevier Ltd. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c517t-91a1a75aed926501cf690b907a2fba5abca59bfef8c9a343eac89be16b7c06fe3</citedby><cites>FETCH-LOGICAL-c517t-91a1a75aed926501cf690b907a2fba5abca59bfef8c9a343eac89be16b7c06fe3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0028390816305895$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,776,780,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28025094$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kilinc, Erkan</creatorcontrib><creatorcontrib>Guerrero-Toro, Cindy</creatorcontrib><creatorcontrib>Zakharov, Andrey</creatorcontrib><creatorcontrib>Vitale, Carmela</creatorcontrib><creatorcontrib>Gubert-Olive, Max</creatorcontrib><creatorcontrib>Koroleva, Ksenia</creatorcontrib><creatorcontrib>Timonina, Arina</creatorcontrib><creatorcontrib>Luz, Liliana L.</creatorcontrib><creatorcontrib>Shelukhina, Irina</creatorcontrib><creatorcontrib>Giniatullina, Raisa</creatorcontrib><creatorcontrib>Tore, Fatma</creatorcontrib><creatorcontrib>Safronov, Boris V.</creatorcontrib><creatorcontrib>Giniatullin, Rashid</creatorcontrib><title>Serotonergic mechanisms of trigeminal meningeal nociception: Implications for migraine pain</title><title>Neuropharmacology</title><addtitle>Neuropharmacology</addtitle><description>Serotonergic mechanisms play a central role in migraine pathology. However, the region-specific effects of serotonin (5-HT) mediated via multiple types of receptors in the nociceptive system are poorly understood. Using extracellular and patch-clamp recordings, we studied the action of 5-HT on the excitability of peripheral and central terminals of trigeminal afferents. 5-HT evoked long-lasting TTX-sensitive firing in the peripheral terminals of meningeal afferents, the origin site of migraine pain. Cluster analysis revealed that in majority of nociceptive fibers 5-HT induced either transient or persistent spiking activity with prevailing delta and theta rhythms. The 5-HT3-receptor antagonist MDL-72222 or 5-HT1B/D-receptor antagonist GR127935 largely reduced, but their combination completely prevented the excitatory pro-nociceptive action of 5-HT. The 5-HT3 agonist mCPBG activated spikes in MDL-72222-dependent manner but the 5HT-1 receptor agonist sumatriptan did not affect the nociceptive firing. 5-HT also triggered peripheral CGRP release in meninges, which was blocked by MDL-72222.5-HT evoked fast membrane currents and Ca2+ transients in a fraction of trigeminal neurons. Immunohistochemistry showed expression of 5-HT3A receptors in fibers innervating meninges. Endogenous release of 5-HT from degranulated mast cells increased nociceptive firing. Low pH but not histamine strongly activated firing. 5-HT reduced monosynaptic inputs from trigeminal Aδ- and C-afferents to the upper cervical lamina I neurons and this effect was blocked by MDL-72222. Consistent with central inhibitory effect, 5-HT reduced CGRP release in the brainstem slices. In conclusion, 5-HT evokes powerful pro-nociceptive peripheral and anti-nociceptive central effects in trigeminal system transmitting migraine pain.
•5-HT induced a robust nociceptive activity in peripheral nerve terminals in meninges.•5-HT3 receptors contributed to pro-nociceptive action 5-HT and CGRP release.•Cluster analysis revealed fibers with remarkably long-lasting firing activity.•In contrast to periphery, 5-HT inhibited central nerve terminals of nociceptors.</description><subject>5-HT3 receptor</subject><subject>Action Potentials - drug effects</subject><subject>Action Potentials - physiology</subject><subject>Animals</subject><subject>Calcitonin Gene-Related Peptide - metabolism</subject><subject>Calcium - metabolism</subject><subject>Cations, Divalent - metabolism</subject><subject>Female</subject><subject>Male</subject><subject>Meninges</subject><subject>Migraine</subject><subject>Migraine Disorders - metabolism</subject><subject>Neurons, Afferent - cytology</subject><subject>Neurons, Afferent - drug effects</subject><subject>Neurons, Afferent - metabolism</subject><subject>Nociception - drug effects</subject><subject>Nociception - physiology</subject><subject>Patch-Clamp Techniques</subject><subject>Rats, Wistar</subject><subject>Receptors, Serotonin - metabolism</subject><subject>Serotonin</subject><subject>Serotonin - metabolism</subject><subject>Serotonin Agents - pharmacology</subject><subject>Spike</subject><subject>Tissue Culture Techniques</subject><subject>Trigeminal nerve</subject><subject>Trigeminal Nerve - cytology</subject><subject>Trigeminal Nerve - drug effects</subject><subject>Trigeminal Nerve - metabolism</subject><subject>TRPV Cation Channels - metabolism</subject><subject>Voltage-Sensitive Dye Imaging</subject><issn>0028-3908</issn><issn>1873-7064</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkE1vFDEMhiNURLeFv4DmyGWmTuYr4UYroJUqcQBOHCJP1tlmNUmmySwS_56strRHLv58bcsPYxWHhgMfrvZNoEOKywMm34hSabhoQHSv2IbLsa1HGLoztgEQsm4VyHN2kfMeADrJ5Rt2LiSIHlS3Yb--U4prDJR2zlSezAMGl32uoq3W5HbkXcC5NIILOypRiMYZWlYXw8fqzi-zM3hMcmVjqrzbJXSBqqXYt-y1xTnTuyd_yX5--fzj5ra-__b17ubTfW16Pq614shx7JG2Sgw9cGMHBZOCEYWdsMfJYK8mS1YahW3XEhqpJuLDNBoYLLWX7MNp75Li44Hyqr3LhuYZA8VD1lz2bTu0PYcilSepSTHnRFYvyXlMfzQHfUSr9_oFrT6i1VzograMvn-6cpg8bZ8H_7EsguuTgMqvvx0lnY2jYGjrEplVb6P7_5W_d8iSvQ</recordid><startdate>20170401</startdate><enddate>20170401</enddate><creator>Kilinc, Erkan</creator><creator>Guerrero-Toro, Cindy</creator><creator>Zakharov, Andrey</creator><creator>Vitale, Carmela</creator><creator>Gubert-Olive, Max</creator><creator>Koroleva, Ksenia</creator><creator>Timonina, Arina</creator><creator>Luz, Liliana L.</creator><creator>Shelukhina, Irina</creator><creator>Giniatullina, Raisa</creator><creator>Tore, Fatma</creator><creator>Safronov, Boris V.</creator><creator>Giniatullin, Rashid</creator><general>Elsevier Ltd</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></search><sort><creationdate>20170401</creationdate><title>Serotonergic mechanisms of trigeminal meningeal nociception: Implications for migraine pain</title><author>Kilinc, Erkan ; Guerrero-Toro, Cindy ; Zakharov, Andrey ; Vitale, Carmela ; Gubert-Olive, Max ; Koroleva, Ksenia ; Timonina, Arina ; Luz, Liliana L. ; Shelukhina, Irina ; Giniatullina, Raisa ; Tore, Fatma ; Safronov, Boris V. ; Giniatullin, Rashid</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c517t-91a1a75aed926501cf690b907a2fba5abca59bfef8c9a343eac89be16b7c06fe3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>5-HT3 receptor</topic><topic>Action Potentials - drug effects</topic><topic>Action Potentials - physiology</topic><topic>Animals</topic><topic>Calcitonin Gene-Related Peptide - metabolism</topic><topic>Calcium - metabolism</topic><topic>Cations, Divalent - metabolism</topic><topic>Female</topic><topic>Male</topic><topic>Meninges</topic><topic>Migraine</topic><topic>Migraine Disorders - metabolism</topic><topic>Neurons, Afferent - cytology</topic><topic>Neurons, Afferent - drug effects</topic><topic>Neurons, Afferent - metabolism</topic><topic>Nociception - drug effects</topic><topic>Nociception - physiology</topic><topic>Patch-Clamp Techniques</topic><topic>Rats, Wistar</topic><topic>Receptors, Serotonin - metabolism</topic><topic>Serotonin</topic><topic>Serotonin - metabolism</topic><topic>Serotonin Agents - pharmacology</topic><topic>Spike</topic><topic>Tissue Culture Techniques</topic><topic>Trigeminal nerve</topic><topic>Trigeminal Nerve - cytology</topic><topic>Trigeminal Nerve - drug effects</topic><topic>Trigeminal Nerve - metabolism</topic><topic>TRPV Cation Channels - metabolism</topic><topic>Voltage-Sensitive Dye Imaging</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kilinc, Erkan</creatorcontrib><creatorcontrib>Guerrero-Toro, Cindy</creatorcontrib><creatorcontrib>Zakharov, Andrey</creatorcontrib><creatorcontrib>Vitale, Carmela</creatorcontrib><creatorcontrib>Gubert-Olive, Max</creatorcontrib><creatorcontrib>Koroleva, Ksenia</creatorcontrib><creatorcontrib>Timonina, Arina</creatorcontrib><creatorcontrib>Luz, Liliana L.</creatorcontrib><creatorcontrib>Shelukhina, Irina</creatorcontrib><creatorcontrib>Giniatullina, Raisa</creatorcontrib><creatorcontrib>Tore, Fatma</creatorcontrib><creatorcontrib>Safronov, Boris V.</creatorcontrib><creatorcontrib>Giniatullin, Rashid</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><jtitle>Neuropharmacology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kilinc, Erkan</au><au>Guerrero-Toro, Cindy</au><au>Zakharov, Andrey</au><au>Vitale, Carmela</au><au>Gubert-Olive, Max</au><au>Koroleva, Ksenia</au><au>Timonina, Arina</au><au>Luz, Liliana L.</au><au>Shelukhina, Irina</au><au>Giniatullina, Raisa</au><au>Tore, Fatma</au><au>Safronov, Boris V.</au><au>Giniatullin, Rashid</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Serotonergic mechanisms of trigeminal meningeal nociception: Implications for migraine pain</atitle><jtitle>Neuropharmacology</jtitle><addtitle>Neuropharmacology</addtitle><date>2017-04-01</date><risdate>2017</risdate><volume>116</volume><spage>160</spage><epage>173</epage><pages>160-173</pages><issn>0028-3908</issn><eissn>1873-7064</eissn><abstract>Serotonergic mechanisms play a central role in migraine pathology. However, the region-specific effects of serotonin (5-HT) mediated via multiple types of receptors in the nociceptive system are poorly understood. Using extracellular and patch-clamp recordings, we studied the action of 5-HT on the excitability of peripheral and central terminals of trigeminal afferents. 5-HT evoked long-lasting TTX-sensitive firing in the peripheral terminals of meningeal afferents, the origin site of migraine pain. Cluster analysis revealed that in majority of nociceptive fibers 5-HT induced either transient or persistent spiking activity with prevailing delta and theta rhythms. The 5-HT3-receptor antagonist MDL-72222 or 5-HT1B/D-receptor antagonist GR127935 largely reduced, but their combination completely prevented the excitatory pro-nociceptive action of 5-HT. The 5-HT3 agonist mCPBG activated spikes in MDL-72222-dependent manner but the 5HT-1 receptor agonist sumatriptan did not affect the nociceptive firing. 5-HT also triggered peripheral CGRP release in meninges, which was blocked by MDL-72222.5-HT evoked fast membrane currents and Ca2+ transients in a fraction of trigeminal neurons. Immunohistochemistry showed expression of 5-HT3A receptors in fibers innervating meninges. Endogenous release of 5-HT from degranulated mast cells increased nociceptive firing. Low pH but not histamine strongly activated firing. 5-HT reduced monosynaptic inputs from trigeminal Aδ- and C-afferents to the upper cervical lamina I neurons and this effect was blocked by MDL-72222. Consistent with central inhibitory effect, 5-HT reduced CGRP release in the brainstem slices. In conclusion, 5-HT evokes powerful pro-nociceptive peripheral and anti-nociceptive central effects in trigeminal system transmitting migraine pain.
•5-HT induced a robust nociceptive activity in peripheral nerve terminals in meninges.•5-HT3 receptors contributed to pro-nociceptive action 5-HT and CGRP release.•Cluster analysis revealed fibers with remarkably long-lasting firing activity.•In contrast to periphery, 5-HT inhibited central nerve terminals of nociceptors.</abstract><cop>England</cop><pub>Elsevier Ltd</pub><pmid>28025094</pmid><doi>10.1016/j.neuropharm.2016.12.024</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | 5-HT3 receptor Action Potentials - drug effects Action Potentials - physiology Animals Calcitonin Gene-Related Peptide - metabolism Calcium - metabolism Cations, Divalent - metabolism Female Male Meninges Migraine Migraine Disorders - metabolism Neurons, Afferent - cytology Neurons, Afferent - drug effects Neurons, Afferent - metabolism Nociception - drug effects Nociception - physiology Patch-Clamp Techniques Rats, Wistar Receptors, Serotonin - metabolism Serotonin Serotonin - metabolism Serotonin Agents - pharmacology Spike Tissue Culture Techniques Trigeminal nerve Trigeminal Nerve - cytology Trigeminal Nerve - drug effects Trigeminal Nerve - metabolism TRPV Cation Channels - metabolism Voltage-Sensitive Dye Imaging |
| title | Serotonergic mechanisms of trigeminal meningeal nociception: Implications for migraine pain |
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