PACAP Induces Light Aversion in Mice by an Inheritable Mechanism Independent of CGRP
The neuropeptides CGRP (calcitonin gene-related peptide) and PACAP (pituitary adenylate cyclase-activating polypeptide) have emerged as mediators of migraine, yet the potential overlap of their mechanisms remains unknown. Infusion of PACAP, like CGRP, can cause migraine in people, and both peptides...
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description | The neuropeptides CGRP (calcitonin gene-related peptide) and PACAP (pituitary adenylate cyclase-activating polypeptide) have emerged as mediators of migraine, yet the potential overlap of their mechanisms remains unknown. Infusion of PACAP, like CGRP, can cause migraine in people, and both peptides share similar vasodilatory and nociceptive functions. In this study, we have used light aversion in mice as a surrogate for migraine-like photophobia to compare CGRP and PACAP and ask whether CGRP or PACAP actions were dependent on each other. Similar to CGRP, PACAP induced light aversion in outbred CD-1 mice. The light aversion was accompanied by increased resting in the dark, but not anxiety in a light-independent open field assay. Unexpectedly, about one-third of the CD-1 mice did not respond to PACAP, which was not seen with CGRP. The responder and nonresponder phenotypes were stable, inheritable, and not sex linked, although there was a trend for greater responses among male mice. RNA-sequencing analysis of trigeminal ganglia yielded hierarchical clustering of responder and nonresponder mice and revealed a number of candidate genes, including greater expression of the
and
ion channels and glycoprotein hormones and receptors in a subset of male responder mice. Importantly, an anti-PACAP monoclonal antibody could block PACAP-induced light aversion but not CGRP-induced light aversion. Conversely, an anti-CGRP antibody could not block PACAP-induced light aversion. Thus, we propose that CGRP and PACAP act by independent convergent pathways that cause a migraine-like symptom in mice.
The relationship between the neuropeptides CGRP (calcitonin gene-related peptide) and PACAP (pituitary adenylate cyclase-activating polypeptide) in migraine is relevant given that both peptides can induce migraine in people, yet to date only drugs that target CGRP are available. Using an outbred strain of mice, we were able to show that most, but not all, mice respond to PACAP in a preclinical photophobia assay. Our finding that CGRP and PACAP monoclonal antibodies do not cross-inhibit the other peptide indicates that CGRP and PACAP actions are independent and suggests that PACAP-targeted drugs may be effective in patients who do not respond to CGRP-based therapeutics. |
doi_str_mv | 10.1523/JNEUROSCI.2200-20.2021 |
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and
ion channels and glycoprotein hormones and receptors in a subset of male responder mice. Importantly, an anti-PACAP monoclonal antibody could block PACAP-induced light aversion but not CGRP-induced light aversion. Conversely, an anti-CGRP antibody could not block PACAP-induced light aversion. Thus, we propose that CGRP and PACAP act by independent convergent pathways that cause a migraine-like symptom in mice.
The relationship between the neuropeptides CGRP (calcitonin gene-related peptide) and PACAP (pituitary adenylate cyclase-activating polypeptide) in migraine is relevant given that both peptides can induce migraine in people, yet to date only drugs that target CGRP are available. Using an outbred strain of mice, we were able to show that most, but not all, mice respond to PACAP in a preclinical photophobia assay. Our finding that CGRP and PACAP monoclonal antibodies do not cross-inhibit the other peptide indicates that CGRP and PACAP actions are independent and suggests that PACAP-targeted drugs may be effective in patients who do not respond to CGRP-based therapeutics.</description><identifier>ISSN: 0270-6474</identifier><identifier>EISSN: 1529-2401</identifier><identifier>DOI: 10.1523/JNEUROSCI.2200-20.2021</identifier><identifier>PMID: 33846231</identifier><language>eng</language><publisher>United States: Society for Neuroscience</publisher><subject>Animals ; Aversion ; Calcitonin ; Calcitonin gene-related peptide ; Calcitonin Gene-Related Peptide - metabolism ; Calcitonin Gene-Related Peptide - pharmacology ; Cluster analysis ; Clustering ; Female ; Ganglia ; Gene expression ; Gene sequencing ; Glycoproteins ; Headache ; Hormones ; Ion channels ; Light ; Male ; Males ; Mice ; Migraine ; Migraine Disorders - genetics ; Migraine Disorders - metabolism ; Monoclonal antibodies ; Neuropeptides ; Pain perception ; Peptides ; Phenotypes ; Photophobia - genetics ; Photophobia - metabolism ; Pituitary adenylate cyclase-activating polypeptide ; Pituitary Adenylate Cyclase-Activating Polypeptide - metabolism ; Pituitary Adenylate Cyclase-Activating Polypeptide - pharmacology ; Polypeptides ; Sequence analysis ; Trigeminal ganglion ; Trigeminal Ganglion - metabolism</subject><ispartof>The Journal of neuroscience, 2021-05, Vol.41 (21), p.4697-4715</ispartof><rights>Copyright © 2021 the authors.</rights><rights>Copyright Society for Neuroscience May 26, 2021</rights><rights>Copyright © 2021 the authors 2021</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c442t-619114a8039c58637b399b1790e886b26e012dea766f03cbd9823d0df3d207873</citedby><cites>FETCH-LOGICAL-c442t-619114a8039c58637b399b1790e886b26e012dea766f03cbd9823d0df3d207873</cites><orcidid>0000-0002-8156-5649</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/PMC8260237/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8260237/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33846231$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kuburas, Adisa</creatorcontrib><creatorcontrib>Mason, Bianca N</creatorcontrib><creatorcontrib>Hing, Benjamin</creatorcontrib><creatorcontrib>Wattiez, Anne-Sophie</creatorcontrib><creatorcontrib>Reis, Alyssa S</creatorcontrib><creatorcontrib>Sowers, Levi P</creatorcontrib><creatorcontrib>Moldovan Loomis, Cristina</creatorcontrib><creatorcontrib>Garcia-Martinez, Leon F</creatorcontrib><creatorcontrib>Russo, Andrew F</creatorcontrib><title>PACAP Induces Light Aversion in Mice by an Inheritable Mechanism Independent of CGRP</title><title>The Journal of neuroscience</title><addtitle>J Neurosci</addtitle><description>The neuropeptides CGRP (calcitonin gene-related peptide) and PACAP (pituitary adenylate cyclase-activating polypeptide) have emerged as mediators of migraine, yet the potential overlap of their mechanisms remains unknown. Infusion of PACAP, like CGRP, can cause migraine in people, and both peptides share similar vasodilatory and nociceptive functions. In this study, we have used light aversion in mice as a surrogate for migraine-like photophobia to compare CGRP and PACAP and ask whether CGRP or PACAP actions were dependent on each other. Similar to CGRP, PACAP induced light aversion in outbred CD-1 mice. The light aversion was accompanied by increased resting in the dark, but not anxiety in a light-independent open field assay. Unexpectedly, about one-third of the CD-1 mice did not respond to PACAP, which was not seen with CGRP. The responder and nonresponder phenotypes were stable, inheritable, and not sex linked, although there was a trend for greater responses among male mice. RNA-sequencing analysis of trigeminal ganglia yielded hierarchical clustering of responder and nonresponder mice and revealed a number of candidate genes, including greater expression of the
and
ion channels and glycoprotein hormones and receptors in a subset of male responder mice. Importantly, an anti-PACAP monoclonal antibody could block PACAP-induced light aversion but not CGRP-induced light aversion. Conversely, an anti-CGRP antibody could not block PACAP-induced light aversion. Thus, we propose that CGRP and PACAP act by independent convergent pathways that cause a migraine-like symptom in mice.
The relationship between the neuropeptides CGRP (calcitonin gene-related peptide) and PACAP (pituitary adenylate cyclase-activating polypeptide) in migraine is relevant given that both peptides can induce migraine in people, yet to date only drugs that target CGRP are available. Using an outbred strain of mice, we were able to show that most, but not all, mice respond to PACAP in a preclinical photophobia assay. Our finding that CGRP and PACAP monoclonal antibodies do not cross-inhibit the other peptide indicates that CGRP and PACAP actions are independent and suggests that PACAP-targeted drugs may be effective in patients who do not respond to CGRP-based therapeutics.</description><subject>Animals</subject><subject>Aversion</subject><subject>Calcitonin</subject><subject>Calcitonin gene-related peptide</subject><subject>Calcitonin Gene-Related Peptide - metabolism</subject><subject>Calcitonin Gene-Related Peptide - pharmacology</subject><subject>Cluster analysis</subject><subject>Clustering</subject><subject>Female</subject><subject>Ganglia</subject><subject>Gene expression</subject><subject>Gene sequencing</subject><subject>Glycoproteins</subject><subject>Headache</subject><subject>Hormones</subject><subject>Ion channels</subject><subject>Light</subject><subject>Male</subject><subject>Males</subject><subject>Mice</subject><subject>Migraine</subject><subject>Migraine Disorders - genetics</subject><subject>Migraine Disorders - metabolism</subject><subject>Monoclonal antibodies</subject><subject>Neuropeptides</subject><subject>Pain perception</subject><subject>Peptides</subject><subject>Phenotypes</subject><subject>Photophobia - genetics</subject><subject>Photophobia - metabolism</subject><subject>Pituitary adenylate cyclase-activating polypeptide</subject><subject>Pituitary Adenylate Cyclase-Activating Polypeptide - metabolism</subject><subject>Pituitary Adenylate Cyclase-Activating Polypeptide - pharmacology</subject><subject>Polypeptides</subject><subject>Sequence analysis</subject><subject>Trigeminal ganglion</subject><subject>Trigeminal Ganglion - metabolism</subject><issn>0270-6474</issn><issn>1529-2401</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkUFr3DAQhUVpabbb_oUg6KUXb0cjWZIvhcWk6ZZNs6TJWci2nFXw2lvJDuTfVybp0haGmcN87zHDI-ScwYrlyD9__3Fxd3P9s9ysEAEyhBUCsldkkbZFhgLYa7IAVJBJocQZeRfjAwAoYOotOeNcC4mcLcjtbl2ud3TTN1PtIt36-_1I148uRD_01Pf0yteOVk_U9gnau-BHW3WOXrl6b3sfD7PUHV1q_UiHlpaXN7v35E1ru-g-vMwluft6cVt-y7bXl5tyvc1qIXDMJCsYE1YDL-pcS64qXhQVUwU4rWWF0gHDxlklZQu8rppCI2-gaXmDoLTiS_Ll2fc4VQfX1OmEYDtzDP5gw5MZrDf_bnq_N_fDo9EoAfls8OnFIAy_JhdHc_Cxdl1nezdM0WDOkAuWK5HQj_-hD8MU-vReoniuNYc0l0Q-U3UYYgyuPR3DwMzBmVNwZg7O4FzIkvD871dOsj9J8d8CUJKQ</recordid><startdate>20210526</startdate><enddate>20210526</enddate><creator>Kuburas, Adisa</creator><creator>Mason, Bianca N</creator><creator>Hing, Benjamin</creator><creator>Wattiez, Anne-Sophie</creator><creator>Reis, Alyssa S</creator><creator>Sowers, Levi P</creator><creator>Moldovan Loomis, Cristina</creator><creator>Garcia-Martinez, Leon F</creator><creator>Russo, Andrew F</creator><general>Society for Neuroscience</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>7QG</scope><scope>7QR</scope><scope>7TK</scope><scope>7U7</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>P64</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-8156-5649</orcidid></search><sort><creationdate>20210526</creationdate><title>PACAP Induces Light Aversion in Mice by an Inheritable Mechanism Independent of CGRP</title><author>Kuburas, Adisa ; Mason, Bianca N ; Hing, Benjamin ; Wattiez, Anne-Sophie ; Reis, Alyssa S ; Sowers, Levi P ; Moldovan Loomis, Cristina ; Garcia-Martinez, Leon F ; Russo, Andrew F</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c442t-619114a8039c58637b399b1790e886b26e012dea766f03cbd9823d0df3d207873</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Animals</topic><topic>Aversion</topic><topic>Calcitonin</topic><topic>Calcitonin gene-related peptide</topic><topic>Calcitonin Gene-Related Peptide - metabolism</topic><topic>Calcitonin Gene-Related Peptide - pharmacology</topic><topic>Cluster analysis</topic><topic>Clustering</topic><topic>Female</topic><topic>Ganglia</topic><topic>Gene expression</topic><topic>Gene sequencing</topic><topic>Glycoproteins</topic><topic>Headache</topic><topic>Hormones</topic><topic>Ion channels</topic><topic>Light</topic><topic>Male</topic><topic>Males</topic><topic>Mice</topic><topic>Migraine</topic><topic>Migraine Disorders - genetics</topic><topic>Migraine Disorders - metabolism</topic><topic>Monoclonal antibodies</topic><topic>Neuropeptides</topic><topic>Pain perception</topic><topic>Peptides</topic><topic>Phenotypes</topic><topic>Photophobia - genetics</topic><topic>Photophobia - metabolism</topic><topic>Pituitary adenylate cyclase-activating polypeptide</topic><topic>Pituitary Adenylate Cyclase-Activating Polypeptide - metabolism</topic><topic>Pituitary Adenylate Cyclase-Activating Polypeptide - pharmacology</topic><topic>Polypeptides</topic><topic>Sequence analysis</topic><topic>Trigeminal ganglion</topic><topic>Trigeminal Ganglion - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kuburas, Adisa</creatorcontrib><creatorcontrib>Mason, Bianca N</creatorcontrib><creatorcontrib>Hing, Benjamin</creatorcontrib><creatorcontrib>Wattiez, Anne-Sophie</creatorcontrib><creatorcontrib>Reis, Alyssa S</creatorcontrib><creatorcontrib>Sowers, Levi P</creatorcontrib><creatorcontrib>Moldovan Loomis, Cristina</creatorcontrib><creatorcontrib>Garcia-Martinez, Leon F</creatorcontrib><creatorcontrib>Russo, Andrew F</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kuburas, Adisa</au><au>Mason, Bianca N</au><au>Hing, Benjamin</au><au>Wattiez, Anne-Sophie</au><au>Reis, Alyssa S</au><au>Sowers, Levi P</au><au>Moldovan Loomis, Cristina</au><au>Garcia-Martinez, Leon F</au><au>Russo, Andrew F</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>PACAP Induces Light Aversion in Mice by an Inheritable Mechanism Independent of CGRP</atitle><jtitle>The Journal of neuroscience</jtitle><addtitle>J Neurosci</addtitle><date>2021-05-26</date><risdate>2021</risdate><volume>41</volume><issue>21</issue><spage>4697</spage><epage>4715</epage><pages>4697-4715</pages><issn>0270-6474</issn><eissn>1529-2401</eissn><abstract>The neuropeptides CGRP (calcitonin gene-related peptide) and PACAP (pituitary adenylate cyclase-activating polypeptide) have emerged as mediators of migraine, yet the potential overlap of their mechanisms remains unknown. Infusion of PACAP, like CGRP, can cause migraine in people, and both peptides share similar vasodilatory and nociceptive functions. In this study, we have used light aversion in mice as a surrogate for migraine-like photophobia to compare CGRP and PACAP and ask whether CGRP or PACAP actions were dependent on each other. Similar to CGRP, PACAP induced light aversion in outbred CD-1 mice. The light aversion was accompanied by increased resting in the dark, but not anxiety in a light-independent open field assay. Unexpectedly, about one-third of the CD-1 mice did not respond to PACAP, which was not seen with CGRP. The responder and nonresponder phenotypes were stable, inheritable, and not sex linked, although there was a trend for greater responses among male mice. RNA-sequencing analysis of trigeminal ganglia yielded hierarchical clustering of responder and nonresponder mice and revealed a number of candidate genes, including greater expression of the
and
ion channels and glycoprotein hormones and receptors in a subset of male responder mice. Importantly, an anti-PACAP monoclonal antibody could block PACAP-induced light aversion but not CGRP-induced light aversion. Conversely, an anti-CGRP antibody could not block PACAP-induced light aversion. Thus, we propose that CGRP and PACAP act by independent convergent pathways that cause a migraine-like symptom in mice.
The relationship between the neuropeptides CGRP (calcitonin gene-related peptide) and PACAP (pituitary adenylate cyclase-activating polypeptide) in migraine is relevant given that both peptides can induce migraine in people, yet to date only drugs that target CGRP are available. Using an outbred strain of mice, we were able to show that most, but not all, mice respond to PACAP in a preclinical photophobia assay. Our finding that CGRP and PACAP monoclonal antibodies do not cross-inhibit the other peptide indicates that CGRP and PACAP actions are independent and suggests that PACAP-targeted drugs may be effective in patients who do not respond to CGRP-based therapeutics.</abstract><cop>United States</cop><pub>Society for Neuroscience</pub><pmid>33846231</pmid><doi>10.1523/JNEUROSCI.2200-20.2021</doi><tpages>19</tpages><orcidid>https://orcid.org/0000-0002-8156-5649</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Aversion Calcitonin Calcitonin gene-related peptide Calcitonin Gene-Related Peptide - metabolism Calcitonin Gene-Related Peptide - pharmacology Cluster analysis Clustering Female Ganglia Gene expression Gene sequencing Glycoproteins Headache Hormones Ion channels Light Male Males Mice Migraine Migraine Disorders - genetics Migraine Disorders - metabolism Monoclonal antibodies Neuropeptides Pain perception Peptides Phenotypes Photophobia - genetics Photophobia - metabolism Pituitary adenylate cyclase-activating polypeptide Pituitary Adenylate Cyclase-Activating Polypeptide - metabolism Pituitary Adenylate Cyclase-Activating Polypeptide - pharmacology Polypeptides Sequence analysis Trigeminal ganglion Trigeminal Ganglion - metabolism |
title | PACAP Induces Light Aversion in Mice by an Inheritable Mechanism Independent of CGRP |
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