IL-1beta in the trigeminal subnucleus caudalis contributes to extra-territorial allodynia/hyperalgesia following a trigeminal nerve injury
Abstract It has been reported that the whisker pad (WP) area, which is innervated by the second branch of the trigeminal nerve, shows allodynia/hyperalgesia following transection of the mental nerve (MN: the third branch of the trigeminal nerve). However, the mechanisms of this extra-territorial pai...
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| Veröffentlicht in: | European journal of pain 2011-05, Vol.15 (5), p.467.e1-467.e14 |
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| creator | Takahashi, Kouji Watanabe, Mineo Suekawa, Yohei Ito, Goshi Inubushi, Toshihiro Hirose, Naoto Murasaki, Kyoko Hiyama, Shinji Uchida, Takashi Tanne, Kazuo |
| description | Abstract It has been reported that the whisker pad (WP) area, which is innervated by the second branch of the trigeminal nerve, shows allodynia/hyperalgesia following transection of the mental nerve (MN: the third branch of the trigeminal nerve). However, the mechanisms of this extra-territorial pain induction still remain unclear. Glia and cytokines are known to facilitate perception of noxious input, raising a possibility that these non-neuronal elements are involved in the induction and spread of allodynia/hyperalgesia at non-injured skin territory. One day after MN transection, tactile allodynia/hyperalgesia developed on the ipsilateral WP area, which is in the non-injured skin territory. The tactile allodynia/hyperalgesia lasted for more than 56 days. In response to MN transection, astrocytes and microglia appeared to be in an activated state, and interleukin (IL)-1beta was up-regulated in astrocytes in the trigeminal subnucleus caudalis (Vc). Allodynia/hyperalgesia at WP area induced by MN transection was attenuated dose-dependently by IL-1 receptor antagonist IL-1ra (i.t., 0.05, 0.5, and 5 pg/rat). Fos-like immunoreactive (Fos-Li) neurons were observed in the Vc after non-noxious mechanical stimulation of the WP area in the rats with MN transection. Administration of IL-1ra also attenuated the number of Fos-Li neurons dose-dependently. Administration of a noncompetitive antagonist of NMDA receptors MK-801 (i.t., 5 μg/rat) reversed allodynia/hyperalgesia. IL-1 receptor type I (IL-1RI) was localized in Fos- and phospho NR1-immunoreactive neurons. These results suggest that IL-1beta in the Vc plays an important role in the development of extra-territorial tactile allodynia/hyperalgesia after MN transection. |
| doi_str_mv | 10.1016/j.ejpain.2010.10.006 |
| format | Article |
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However, the mechanisms of this extra-territorial pain induction still remain unclear. Glia and cytokines are known to facilitate perception of noxious input, raising a possibility that these non-neuronal elements are involved in the induction and spread of allodynia/hyperalgesia at non-injured skin territory. One day after MN transection, tactile allodynia/hyperalgesia developed on the ipsilateral WP area, which is in the non-injured skin territory. The tactile allodynia/hyperalgesia lasted for more than 56 days. In response to MN transection, astrocytes and microglia appeared to be in an activated state, and interleukin (IL)-1beta was up-regulated in astrocytes in the trigeminal subnucleus caudalis (Vc). Allodynia/hyperalgesia at WP area induced by MN transection was attenuated dose-dependently by IL-1 receptor antagonist IL-1ra (i.t., 0.05, 0.5, and 5 pg/rat). Fos-like immunoreactive (Fos-Li) neurons were observed in the Vc after non-noxious mechanical stimulation of the WP area in the rats with MN transection. Administration of IL-1ra also attenuated the number of Fos-Li neurons dose-dependently. Administration of a noncompetitive antagonist of NMDA receptors MK-801 (i.t., 5 μg/rat) reversed allodynia/hyperalgesia. IL-1 receptor type I (IL-1RI) was localized in Fos- and phospho NR1-immunoreactive neurons. These results suggest that IL-1beta in the Vc plays an important role in the development of extra-territorial tactile allodynia/hyperalgesia after MN transection.</description><identifier>ISSN: 1090-3801</identifier><identifier>EISSN: 1532-2149</identifier><identifier>DOI: 10.1016/j.ejpain.2010.10.006</identifier><identifier>PMID: 21093329</identifier><language>eng</language><publisher>Oxford, UK: Elsevier Ltd</publisher><subject>Allodynia/hyperalgesia ; Anesthesia & Perioperative Care ; Animals ; Antirheumatic Agents - pharmacology ; Astrocytes - metabolism ; Astrocytes - pathology ; Disease Models, Animal ; Dizocilpine Maleate - pharmacology ; Excitatory Amino Acid Antagonists - pharmacology ; Fos ; Hyperalgesia - drug therapy ; Hyperalgesia - metabolism ; Hyperalgesia - pathology ; Injections, Spinal ; Interleukin 1 Receptor Antagonist Protein - pharmacology ; Interleukin-1beta ; Interleukin-1beta - metabolism ; Mandible - innervation ; Mental nerve ; Microglia - metabolism ; Microglia - pathology ; Nerve injury ; Pain Medicine ; Rats ; Trigeminal Caudal Nucleus - metabolism ; Trigeminal Caudal Nucleus - pathology ; Trigeminal Nerve Injuries ; Up-Regulation - physiology ; Vibrissae - innervation</subject><ispartof>European journal of pain, 2011-05, Vol.15 (5), p.467.e1-467.e14</ispartof><rights>European Federation of International Association for the Study of Pain Chapters</rights><rights>2010 European Federation of International Association for the Study of Pain Chapters</rights><rights>2011 European Federation of Chapters of the International Association for the Study of Pain</rights><rights>Copyright © 2010 European Federation of International Association for the Study of Pain Chapters. Published by Elsevier Ltd. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5703-b9f32ee6f8e80ca3848de0264e762b378b406b92454d95ebd3dd7654bbf9249f3</citedby><cites>FETCH-LOGICAL-c5703-b9f32ee6f8e80ca3848de0264e762b378b406b92454d95ebd3dd7654bbf9249f3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1016%2Fj.ejpain.2010.10.006$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1016%2Fj.ejpain.2010.10.006$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,780,784,1416,27922,27923,45572,45573</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21093329$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Takahashi, Kouji</creatorcontrib><creatorcontrib>Watanabe, Mineo</creatorcontrib><creatorcontrib>Suekawa, Yohei</creatorcontrib><creatorcontrib>Ito, Goshi</creatorcontrib><creatorcontrib>Inubushi, Toshihiro</creatorcontrib><creatorcontrib>Hirose, Naoto</creatorcontrib><creatorcontrib>Murasaki, Kyoko</creatorcontrib><creatorcontrib>Hiyama, Shinji</creatorcontrib><creatorcontrib>Uchida, Takashi</creatorcontrib><creatorcontrib>Tanne, Kazuo</creatorcontrib><title>IL-1beta in the trigeminal subnucleus caudalis contributes to extra-territorial allodynia/hyperalgesia following a trigeminal nerve injury</title><title>European journal of pain</title><addtitle>Eur J Pain</addtitle><description>Abstract It has been reported that the whisker pad (WP) area, which is innervated by the second branch of the trigeminal nerve, shows allodynia/hyperalgesia following transection of the mental nerve (MN: the third branch of the trigeminal nerve). However, the mechanisms of this extra-territorial pain induction still remain unclear. Glia and cytokines are known to facilitate perception of noxious input, raising a possibility that these non-neuronal elements are involved in the induction and spread of allodynia/hyperalgesia at non-injured skin territory. One day after MN transection, tactile allodynia/hyperalgesia developed on the ipsilateral WP area, which is in the non-injured skin territory. The tactile allodynia/hyperalgesia lasted for more than 56 days. In response to MN transection, astrocytes and microglia appeared to be in an activated state, and interleukin (IL)-1beta was up-regulated in astrocytes in the trigeminal subnucleus caudalis (Vc). Allodynia/hyperalgesia at WP area induced by MN transection was attenuated dose-dependently by IL-1 receptor antagonist IL-1ra (i.t., 0.05, 0.5, and 5 pg/rat). Fos-like immunoreactive (Fos-Li) neurons were observed in the Vc after non-noxious mechanical stimulation of the WP area in the rats with MN transection. Administration of IL-1ra also attenuated the number of Fos-Li neurons dose-dependently. Administration of a noncompetitive antagonist of NMDA receptors MK-801 (i.t., 5 μg/rat) reversed allodynia/hyperalgesia. IL-1 receptor type I (IL-1RI) was localized in Fos- and phospho NR1-immunoreactive neurons. These results suggest that IL-1beta in the Vc plays an important role in the development of extra-territorial tactile allodynia/hyperalgesia after MN transection.</description><subject>Allodynia/hyperalgesia</subject><subject>Anesthesia & Perioperative Care</subject><subject>Animals</subject><subject>Antirheumatic Agents - pharmacology</subject><subject>Astrocytes - metabolism</subject><subject>Astrocytes - pathology</subject><subject>Disease Models, Animal</subject><subject>Dizocilpine Maleate - pharmacology</subject><subject>Excitatory Amino Acid Antagonists - pharmacology</subject><subject>Fos</subject><subject>Hyperalgesia - drug therapy</subject><subject>Hyperalgesia - metabolism</subject><subject>Hyperalgesia - pathology</subject><subject>Injections, Spinal</subject><subject>Interleukin 1 Receptor Antagonist Protein - pharmacology</subject><subject>Interleukin-1beta</subject><subject>Interleukin-1beta - metabolism</subject><subject>Mandible - innervation</subject><subject>Mental nerve</subject><subject>Microglia - metabolism</subject><subject>Microglia - pathology</subject><subject>Nerve injury</subject><subject>Pain Medicine</subject><subject>Rats</subject><subject>Trigeminal Caudal Nucleus - metabolism</subject><subject>Trigeminal Caudal Nucleus - pathology</subject><subject>Trigeminal Nerve Injuries</subject><subject>Up-Regulation - physiology</subject><subject>Vibrissae - innervation</subject><issn>1090-3801</issn><issn>1532-2149</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNUk1v1DAQjRCIlsI_QCg3Ttn6I3GcCxJaldJqBUgUwc2yncnWqddZbKdt_kJ_dR1SKsQFTh69eW9mPG-y7DVGK4wwO-5X0O-lcSuCfkErhNiT7BBXlBQEl83TFKMGFZQjfJC9CKFHCJU1os-zA5IylJLmMLs72xRYQZS5cXm8hDx6s4WdcdLmYVRu1BbGkGs5ttKaFAwuMdQYIeRxyOE2ellE8N7EwZskktYO7eSMPL6c9uCl3UIwMu-GhN8Yt83lny0c-GtIrfvRTy-zZ520AV49vEfZtw8nF-uPxebz6dn6_abQVZq-UE1HCQDrOHCkJeUlbwERVkLNiKI1VyViqiFlVbZNBaqlbVuzqlSqS2ASH2Vvl7p7P_wcIUSxM0GDtdLBMAbBWU0JqViVmOXC1H4IwUMn9t7spJ8ERmI2QfRiMUHMJsxoMiHJ3jw0GNUO2kfR760nQrMQboyF6b-KipPzL5RzmrTFojUhwu2jVvorkeauK_H906k452v2gxMsLhL_3cKHtNJrA14EbcBpaI0HHUU7mH_95u8C2hpntLRXMEHoh9EnJ4PAIhCBxNf56Oabw-ncCCMlvQdgY9Md</recordid><startdate>201105</startdate><enddate>201105</enddate><creator>Takahashi, Kouji</creator><creator>Watanabe, Mineo</creator><creator>Suekawa, Yohei</creator><creator>Ito, Goshi</creator><creator>Inubushi, Toshihiro</creator><creator>Hirose, Naoto</creator><creator>Murasaki, Kyoko</creator><creator>Hiyama, Shinji</creator><creator>Uchida, Takashi</creator><creator>Tanne, Kazuo</creator><general>Elsevier Ltd</general><general>Blackwell Publishing Ltd</general><scope>BSCLL</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>7X8</scope></search><sort><creationdate>201105</creationdate><title>IL-1beta in the trigeminal subnucleus caudalis contributes to extra-territorial allodynia/hyperalgesia following a trigeminal nerve injury</title><author>Takahashi, Kouji ; Watanabe, Mineo ; Suekawa, Yohei ; Ito, Goshi ; Inubushi, Toshihiro ; Hirose, Naoto ; Murasaki, Kyoko ; Hiyama, Shinji ; Uchida, Takashi ; Tanne, Kazuo</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5703-b9f32ee6f8e80ca3848de0264e762b378b406b92454d95ebd3dd7654bbf9249f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Allodynia/hyperalgesia</topic><topic>Anesthesia & Perioperative Care</topic><topic>Animals</topic><topic>Antirheumatic Agents - pharmacology</topic><topic>Astrocytes - metabolism</topic><topic>Astrocytes - pathology</topic><topic>Disease Models, Animal</topic><topic>Dizocilpine Maleate - pharmacology</topic><topic>Excitatory Amino Acid Antagonists - pharmacology</topic><topic>Fos</topic><topic>Hyperalgesia - drug therapy</topic><topic>Hyperalgesia - metabolism</topic><topic>Hyperalgesia - pathology</topic><topic>Injections, Spinal</topic><topic>Interleukin 1 Receptor Antagonist Protein - pharmacology</topic><topic>Interleukin-1beta</topic><topic>Interleukin-1beta - metabolism</topic><topic>Mandible - innervation</topic><topic>Mental nerve</topic><topic>Microglia - metabolism</topic><topic>Microglia - pathology</topic><topic>Nerve injury</topic><topic>Pain Medicine</topic><topic>Rats</topic><topic>Trigeminal Caudal Nucleus - metabolism</topic><topic>Trigeminal Caudal Nucleus - pathology</topic><topic>Trigeminal Nerve Injuries</topic><topic>Up-Regulation - physiology</topic><topic>Vibrissae - innervation</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Takahashi, Kouji</creatorcontrib><creatorcontrib>Watanabe, Mineo</creatorcontrib><creatorcontrib>Suekawa, Yohei</creatorcontrib><creatorcontrib>Ito, Goshi</creatorcontrib><creatorcontrib>Inubushi, Toshihiro</creatorcontrib><creatorcontrib>Hirose, Naoto</creatorcontrib><creatorcontrib>Murasaki, Kyoko</creatorcontrib><creatorcontrib>Hiyama, Shinji</creatorcontrib><creatorcontrib>Uchida, Takashi</creatorcontrib><creatorcontrib>Tanne, Kazuo</creatorcontrib><collection>Istex</collection><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>European journal of pain</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Takahashi, Kouji</au><au>Watanabe, Mineo</au><au>Suekawa, Yohei</au><au>Ito, Goshi</au><au>Inubushi, Toshihiro</au><au>Hirose, Naoto</au><au>Murasaki, Kyoko</au><au>Hiyama, Shinji</au><au>Uchida, Takashi</au><au>Tanne, Kazuo</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>IL-1beta in the trigeminal subnucleus caudalis contributes to extra-territorial allodynia/hyperalgesia following a trigeminal nerve injury</atitle><jtitle>European journal of pain</jtitle><addtitle>Eur J Pain</addtitle><date>2011-05</date><risdate>2011</risdate><volume>15</volume><issue>5</issue><spage>467.e1</spage><epage>467.e14</epage><pages>467.e1-467.e14</pages><issn>1090-3801</issn><eissn>1532-2149</eissn><abstract>Abstract It has been reported that the whisker pad (WP) area, which is innervated by the second branch of the trigeminal nerve, shows allodynia/hyperalgesia following transection of the mental nerve (MN: the third branch of the trigeminal nerve). However, the mechanisms of this extra-territorial pain induction still remain unclear. Glia and cytokines are known to facilitate perception of noxious input, raising a possibility that these non-neuronal elements are involved in the induction and spread of allodynia/hyperalgesia at non-injured skin territory. One day after MN transection, tactile allodynia/hyperalgesia developed on the ipsilateral WP area, which is in the non-injured skin territory. The tactile allodynia/hyperalgesia lasted for more than 56 days. In response to MN transection, astrocytes and microglia appeared to be in an activated state, and interleukin (IL)-1beta was up-regulated in astrocytes in the trigeminal subnucleus caudalis (Vc). Allodynia/hyperalgesia at WP area induced by MN transection was attenuated dose-dependently by IL-1 receptor antagonist IL-1ra (i.t., 0.05, 0.5, and 5 pg/rat). Fos-like immunoreactive (Fos-Li) neurons were observed in the Vc after non-noxious mechanical stimulation of the WP area in the rats with MN transection. Administration of IL-1ra also attenuated the number of Fos-Li neurons dose-dependently. Administration of a noncompetitive antagonist of NMDA receptors MK-801 (i.t., 5 μg/rat) reversed allodynia/hyperalgesia. IL-1 receptor type I (IL-1RI) was localized in Fos- and phospho NR1-immunoreactive neurons. These results suggest that IL-1beta in the Vc plays an important role in the development of extra-territorial tactile allodynia/hyperalgesia after MN transection.</abstract><cop>Oxford, UK</cop><pub>Elsevier Ltd</pub><pmid>21093329</pmid><doi>10.1016/j.ejpain.2010.10.006</doi><tpages>14</tpages></addata></record> |
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| subjects | Allodynia/hyperalgesia Anesthesia & Perioperative Care Animals Antirheumatic Agents - pharmacology Astrocytes - metabolism Astrocytes - pathology Disease Models, Animal Dizocilpine Maleate - pharmacology Excitatory Amino Acid Antagonists - pharmacology Fos Hyperalgesia - drug therapy Hyperalgesia - metabolism Hyperalgesia - pathology Injections, Spinal Interleukin 1 Receptor Antagonist Protein - pharmacology Interleukin-1beta Interleukin-1beta - metabolism Mandible - innervation Mental nerve Microglia - metabolism Microglia - pathology Nerve injury Pain Medicine Rats Trigeminal Caudal Nucleus - metabolism Trigeminal Caudal Nucleus - pathology Trigeminal Nerve Injuries Up-Regulation - physiology Vibrissae - innervation |
| title | IL-1beta in the trigeminal subnucleus caudalis contributes to extra-territorial allodynia/hyperalgesia following a trigeminal nerve injury |
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