Adenylyl Cyclase Subtype 1 is Essential for Late-Phase Long Term Potentiation and Spatial Propagation of Synaptic Responses in the Anterior Cingulate Cortex of Adult Mice
Long-term potentiation (LTP) is a key cellular mechanism for pathological pain in the central nervous system. LTP contains at least two different phases: early-phase LTP (E-LTP) and late-phase LTP (L-LTP). Among several major cortical areas, the anterior cingulate cortex (ACC) is a critical brain re...
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| Veröffentlicht in: | Molecular pain 2014-10, Vol.10 (1), p.65-65 |
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| description | Long-term potentiation (LTP) is a key cellular mechanism for pathological pain in the central nervous system. LTP contains at least two different phases: early-phase LTP (E-LTP) and late-phase LTP (L-LTP). Among several major cortical areas, the anterior cingulate cortex (ACC) is a critical brain region for pain perception and its related emotional changes. Periphery tissue or nerve injuries cause LTP of excitatory synaptic transmission in the ACC. Our previous studies have demonstrated that genetic deletion of calcium-stimulated adenylyl cyclase 1 (AC1) or pharmacological application of a selective AC1 inhibitor NB001 blocked E-LTP in the ACC. However, the effect of AC1 on L-LTP, which requires new protein synthesis and is important for the process of chronic pain, has not been investigated. Here we tested the effects of NB001 on the ACC L-LTP and found that bath application of NB001 (0.1 μM) totally blocked the induction of L-LTP and recruitment of cortical circuitry without affecting basal excitatory transmission. In contrast, gabapentin, a widely used analgesic drug for neuropathic pain, did not block the induction of L-LTP and circuitry recruitment even at a high concentration (100 μM). Gabapentin non-selectively decreased basal synaptic transmission. Our results provide strong evidence that the selective AC1 inhibitor NB001 can be used to inhibit pain-related cortical L-LTP without affecting basal synaptic transmission. It also provides basic mechanisms for possible side effects of gabapentin in the central nervous system and its ineffectiveness in some patients with neuropathic pain. |
| doi_str_mv | 10.1186/1744-8069-10-65 |
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LTP contains at least two different phases: early-phase LTP (E-LTP) and late-phase LTP (L-LTP). Among several major cortical areas, the anterior cingulate cortex (ACC) is a critical brain region for pain perception and its related emotional changes. Periphery tissue or nerve injuries cause LTP of excitatory synaptic transmission in the ACC. Our previous studies have demonstrated that genetic deletion of calcium-stimulated adenylyl cyclase 1 (AC1) or pharmacological application of a selective AC1 inhibitor NB001 blocked E-LTP in the ACC. However, the effect of AC1 on L-LTP, which requires new protein synthesis and is important for the process of chronic pain, has not been investigated. Here we tested the effects of NB001 on the ACC L-LTP and found that bath application of NB001 (0.1 μM) totally blocked the induction of L-LTP and recruitment of cortical circuitry without affecting basal excitatory transmission. In contrast, gabapentin, a widely used analgesic drug for neuropathic pain, did not block the induction of L-LTP and circuitry recruitment even at a high concentration (100 μM). Gabapentin non-selectively decreased basal synaptic transmission. Our results provide strong evidence that the selective AC1 inhibitor NB001 can be used to inhibit pain-related cortical L-LTP without affecting basal synaptic transmission. It also provides basic mechanisms for possible side effects of gabapentin in the central nervous system and its ineffectiveness in some patients with neuropathic pain.</description><identifier>ISSN: 1744-8069</identifier><identifier>EISSN: 1744-8069</identifier><identifier>DOI: 10.1186/1744-8069-10-65</identifier><identifier>PMID: 25304256</identifier><language>eng</language><publisher>Los Angeles, CA: SAGE Publications</publisher><subject>Acids ; Adenosine Triphosphate - analogs & derivatives ; Adenosine Triphosphate - pharmacology ; Adenylate cyclase ; Adenylyl Cyclase Inhibitors ; Adenylyl Cyclases - metabolism ; Amines - pharmacology ; Analgesics ; Analysis ; Anatomy & physiology ; Animals ; Benzofurans ; Brain injury ; Central nervous system ; Chronic pain ; Cortex (cingulate) ; Cyclohexanecarboxylic Acids - pharmacology ; Dizocilpine Maleate - pharmacology ; Dose-Response Relationship, Drug ; Excitatory Amino Acid Antagonists - pharmacology ; Gabapentin ; gamma-Aminobutyric Acid - pharmacology ; Glutamic Acid - metabolism ; Gyrus Cinguli - drug effects ; Gyrus Cinguli - physiology ; In Vitro Techniques ; Long-term potentiation ; Long-Term Potentiation - physiology ; Male ; Medical research ; Mice ; N-Methylaspartate - pharmacology ; Nerve Net - drug effects ; Nerve Net - physiology ; Nervous system ; Neuralgia ; Pain ; Pain perception ; Physiological aspects ; Propagation ; Protein biosynthesis ; Quinolines ; Synaptic transmission ; Synaptic Transmission - drug effects ; Synaptic Transmission - physiology ; Time Factors</subject><ispartof>Molecular pain, 2014-10, Vol.10 (1), p.65-65</ispartof><rights>2014 Chen et al</rights><rights>COPYRIGHT 2014 BioMed Central Ltd.</rights><rights>2014 Chen et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. 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.</rights><rights>2014 Chen et al. This work is licensed under the Creative Commons Attribution License 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>Chen et al.; licensee BioMed Central Ltd. 2014</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c652t-4f52e4f7f0a741c69c359b4d896f5f0b3a6687ab4ab757fad30087555af3b9ab3</citedby><cites>FETCH-LOGICAL-c652t-4f52e4f7f0a741c69c359b4d896f5f0b3a6687ab4ab757fad30087555af3b9ab3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4198686/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4198686/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,21945,27830,27901,27902,44921,45309,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25304256$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Chen, Tao</creatorcontrib><creatorcontrib>O'Den, Gerile</creatorcontrib><creatorcontrib>Song, Qian</creatorcontrib><creatorcontrib>Koga, Kohei</creatorcontrib><creatorcontrib>Zhang, Ming-Ming</creatorcontrib><creatorcontrib>Zhuo, Min</creatorcontrib><title>Adenylyl Cyclase Subtype 1 is Essential for Late-Phase Long Term Potentiation and Spatial Propagation of Synaptic Responses in the Anterior Cingulate Cortex of Adult Mice</title><title>Molecular pain</title><addtitle>Mol Pain</addtitle><description>Long-term potentiation (LTP) is a key cellular mechanism for pathological pain in the central nervous system. LTP contains at least two different phases: early-phase LTP (E-LTP) and late-phase LTP (L-LTP). Among several major cortical areas, the anterior cingulate cortex (ACC) is a critical brain region for pain perception and its related emotional changes. Periphery tissue or nerve injuries cause LTP of excitatory synaptic transmission in the ACC. Our previous studies have demonstrated that genetic deletion of calcium-stimulated adenylyl cyclase 1 (AC1) or pharmacological application of a selective AC1 inhibitor NB001 blocked E-LTP in the ACC. However, the effect of AC1 on L-LTP, which requires new protein synthesis and is important for the process of chronic pain, has not been investigated. Here we tested the effects of NB001 on the ACC L-LTP and found that bath application of NB001 (0.1 μM) totally blocked the induction of L-LTP and recruitment of cortical circuitry without affecting basal excitatory transmission. In contrast, gabapentin, a widely used analgesic drug for neuropathic pain, did not block the induction of L-LTP and circuitry recruitment even at a high concentration (100 μM). Gabapentin non-selectively decreased basal synaptic transmission. Our results provide strong evidence that the selective AC1 inhibitor NB001 can be used to inhibit pain-related cortical L-LTP without affecting basal synaptic transmission. It also provides basic mechanisms for possible side effects of gabapentin in the central nervous system and its ineffectiveness in some patients with neuropathic pain.</description><subject>Acids</subject><subject>Adenosine Triphosphate - analogs & derivatives</subject><subject>Adenosine Triphosphate - pharmacology</subject><subject>Adenylate cyclase</subject><subject>Adenylyl Cyclase Inhibitors</subject><subject>Adenylyl Cyclases - metabolism</subject><subject>Amines - pharmacology</subject><subject>Analgesics</subject><subject>Analysis</subject><subject>Anatomy & physiology</subject><subject>Animals</subject><subject>Benzofurans</subject><subject>Brain injury</subject><subject>Central nervous system</subject><subject>Chronic pain</subject><subject>Cortex (cingulate)</subject><subject>Cyclohexanecarboxylic Acids - pharmacology</subject><subject>Dizocilpine Maleate - pharmacology</subject><subject>Dose-Response Relationship, Drug</subject><subject>Excitatory Amino Acid Antagonists - pharmacology</subject><subject>Gabapentin</subject><subject>gamma-Aminobutyric Acid - pharmacology</subject><subject>Glutamic Acid - metabolism</subject><subject>Gyrus Cinguli - drug effects</subject><subject>Gyrus Cinguli - physiology</subject><subject>In Vitro Techniques</subject><subject>Long-term potentiation</subject><subject>Long-Term Potentiation - physiology</subject><subject>Male</subject><subject>Medical research</subject><subject>Mice</subject><subject>N-Methylaspartate - pharmacology</subject><subject>Nerve Net - drug effects</subject><subject>Nerve Net - physiology</subject><subject>Nervous system</subject><subject>Neuralgia</subject><subject>Pain</subject><subject>Pain perception</subject><subject>Physiological aspects</subject><subject>Propagation</subject><subject>Protein biosynthesis</subject><subject>Quinolines</subject><subject>Synaptic transmission</subject><subject>Synaptic Transmission - drug effects</subject><subject>Synaptic Transmission - physiology</subject><subject>Time Factors</subject><issn>1744-8069</issn><issn>1744-8069</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>AFRWT</sourceid><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNqFksFu1DAQhiMEoqVw5oYsceHQtHYSO8kFabVqAWkRK7acLScZZ1157WA7iLwST4nTLcsWgZBl2Rp__z-e0STJS4IvCKnYJSmLIq0wq1OCU0YfJaeHyOOj-0nyzPtbjPMSM_I0OclojouMstPkx6IDM-lJo-XUauEBbcYmTAMggpRHV96DCUpoJK1DKxEgXW9namVNj27A7dDahjskKGuQMB3aDOJOsXZ2EP0-biXaTEYMQbXoM_jBGg8eKYPCFtDCBHAq-i-V6Ucdk6CldQG-z7JFN-qAPqoWnidPpNAeXtyfZ8mX66ub5ft09endh-VilbaMZiEtJM2gkKXEoixIy-o2p3VTdFXNJJW4yQVjVSmaQjQlLaXocoyrklIqZN7UosnPkrd732FsdtC1sTonNB-c2gk3cSsUf_hi1Jb39hsvSF2xikWDN_cGzn4dwQe-U74FrYUBO3pOGKnipnUV0dd_oLd2dCaWx7Ma05L-j4o-pKaEsPI31QsNXBlp4-_aOTVf0LxmVU4zHKmLv1BxdbBTrTUgVYw_EFzuBa2z3juQh04QzOch5POY8XnM5gijUfHquIEH_tfUReB8D3jRw1Et__D7Cdjk5M4</recordid><startdate>20141010</startdate><enddate>20141010</enddate><creator>Chen, Tao</creator><creator>O'Den, Gerile</creator><creator>Song, Qian</creator><creator>Koga, Kohei</creator><creator>Zhang, Ming-Ming</creator><creator>Zhuo, Min</creator><general>SAGE Publications</general><general>BioMed Central Ltd</general><general>Sage Publications Ltd</general><general>BioMed Central</general><scope>AFRWT</scope><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>3V.</scope><scope>7TK</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BENPR</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>K9.</scope><scope>M0S</scope><scope>M1P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>5PM</scope></search><sort><creationdate>20141010</creationdate><title>Adenylyl Cyclase Subtype 1 is Essential for Late-Phase Long Term Potentiation and Spatial Propagation of Synaptic Responses in the Anterior Cingulate Cortex of Adult Mice</title><author>Chen, Tao ; O'Den, Gerile ; Song, Qian ; Koga, Kohei ; Zhang, Ming-Ming ; Zhuo, Min</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c652t-4f52e4f7f0a741c69c359b4d896f5f0b3a6687ab4ab757fad30087555af3b9ab3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Acids</topic><topic>Adenosine Triphosphate - analogs & derivatives</topic><topic>Adenosine Triphosphate - pharmacology</topic><topic>Adenylate cyclase</topic><topic>Adenylyl Cyclase Inhibitors</topic><topic>Adenylyl Cyclases - metabolism</topic><topic>Amines - pharmacology</topic><topic>Analgesics</topic><topic>Analysis</topic><topic>Anatomy & physiology</topic><topic>Animals</topic><topic>Benzofurans</topic><topic>Brain injury</topic><topic>Central nervous system</topic><topic>Chronic pain</topic><topic>Cortex (cingulate)</topic><topic>Cyclohexanecarboxylic Acids - pharmacology</topic><topic>Dizocilpine Maleate - pharmacology</topic><topic>Dose-Response Relationship, Drug</topic><topic>Excitatory Amino Acid Antagonists - pharmacology</topic><topic>Gabapentin</topic><topic>gamma-Aminobutyric Acid - pharmacology</topic><topic>Glutamic Acid - metabolism</topic><topic>Gyrus Cinguli - drug effects</topic><topic>Gyrus Cinguli - physiology</topic><topic>In Vitro Techniques</topic><topic>Long-term potentiation</topic><topic>Long-Term Potentiation - physiology</topic><topic>Male</topic><topic>Medical research</topic><topic>Mice</topic><topic>N-Methylaspartate - pharmacology</topic><topic>Nerve Net - drug effects</topic><topic>Nerve Net - physiology</topic><topic>Nervous system</topic><topic>Neuralgia</topic><topic>Pain</topic><topic>Pain perception</topic><topic>Physiological aspects</topic><topic>Propagation</topic><topic>Protein biosynthesis</topic><topic>Quinolines</topic><topic>Synaptic transmission</topic><topic>Synaptic Transmission - drug effects</topic><topic>Synaptic Transmission - physiology</topic><topic>Time Factors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Chen, Tao</creatorcontrib><creatorcontrib>O'Den, Gerile</creatorcontrib><creatorcontrib>Song, Qian</creatorcontrib><creatorcontrib>Koga, Kohei</creatorcontrib><creatorcontrib>Zhang, Ming-Ming</creatorcontrib><creatorcontrib>Zhuo, Min</creatorcontrib><collection>Sage Journals GOLD Open Access 2024</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Neurosciences Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>ProQuest Central</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Publicly Available Content Database</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>PubMed Central (Full Participant titles)</collection><jtitle>Molecular pain</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Chen, Tao</au><au>O'Den, Gerile</au><au>Song, Qian</au><au>Koga, Kohei</au><au>Zhang, Ming-Ming</au><au>Zhuo, Min</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Adenylyl Cyclase Subtype 1 is Essential for Late-Phase Long Term Potentiation and Spatial Propagation of Synaptic Responses in the Anterior Cingulate Cortex of Adult Mice</atitle><jtitle>Molecular pain</jtitle><addtitle>Mol Pain</addtitle><date>2014-10-10</date><risdate>2014</risdate><volume>10</volume><issue>1</issue><spage>65</spage><epage>65</epage><pages>65-65</pages><issn>1744-8069</issn><eissn>1744-8069</eissn><abstract>Long-term potentiation (LTP) is a key cellular mechanism for pathological pain in the central nervous system. LTP contains at least two different phases: early-phase LTP (E-LTP) and late-phase LTP (L-LTP). Among several major cortical areas, the anterior cingulate cortex (ACC) is a critical brain region for pain perception and its related emotional changes. Periphery tissue or nerve injuries cause LTP of excitatory synaptic transmission in the ACC. Our previous studies have demonstrated that genetic deletion of calcium-stimulated adenylyl cyclase 1 (AC1) or pharmacological application of a selective AC1 inhibitor NB001 blocked E-LTP in the ACC. However, the effect of AC1 on L-LTP, which requires new protein synthesis and is important for the process of chronic pain, has not been investigated. Here we tested the effects of NB001 on the ACC L-LTP and found that bath application of NB001 (0.1 μM) totally blocked the induction of L-LTP and recruitment of cortical circuitry without affecting basal excitatory transmission. In contrast, gabapentin, a widely used analgesic drug for neuropathic pain, did not block the induction of L-LTP and circuitry recruitment even at a high concentration (100 μM). Gabapentin non-selectively decreased basal synaptic transmission. Our results provide strong evidence that the selective AC1 inhibitor NB001 can be used to inhibit pain-related cortical L-LTP without affecting basal synaptic transmission. It also provides basic mechanisms for possible side effects of gabapentin in the central nervous system and its ineffectiveness in some patients with neuropathic pain.</abstract><cop>Los Angeles, CA</cop><pub>SAGE Publications</pub><pmid>25304256</pmid><doi>10.1186/1744-8069-10-65</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Acids Adenosine Triphosphate - analogs & derivatives Adenosine Triphosphate - pharmacology Adenylate cyclase Adenylyl Cyclase Inhibitors Adenylyl Cyclases - metabolism Amines - pharmacology Analgesics Analysis Anatomy & physiology Animals Benzofurans Brain injury Central nervous system Chronic pain Cortex (cingulate) Cyclohexanecarboxylic Acids - pharmacology Dizocilpine Maleate - pharmacology Dose-Response Relationship, Drug Excitatory Amino Acid Antagonists - pharmacology Gabapentin gamma-Aminobutyric Acid - pharmacology Glutamic Acid - metabolism Gyrus Cinguli - drug effects Gyrus Cinguli - physiology In Vitro Techniques Long-term potentiation Long-Term Potentiation - physiology Male Medical research Mice N-Methylaspartate - pharmacology Nerve Net - drug effects Nerve Net - physiology Nervous system Neuralgia Pain Pain perception Physiological aspects Propagation Protein biosynthesis Quinolines Synaptic transmission Synaptic Transmission - drug effects Synaptic Transmission - physiology Time Factors |
| title | Adenylyl Cyclase Subtype 1 is Essential for Late-Phase Long Term Potentiation and Spatial Propagation of Synaptic Responses in the Anterior Cingulate Cortex of Adult Mice |
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