Functional interaction between Ghrelin and GLP-1 regulates feeding through the vagal afferent system
The gastrointestinal tract transmits feeding-regulatory signals to the brain via neuronal and hormonal pathways. Here we studied the interaction between the orexigenic gastric peptide, ghrelin, and the anorectic intestinal peptide, glucagon-like peptide 1 (GLP-1), in terms of feeding regulation via...
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| Veröffentlicht in: | Scientific reports 2020-10, Vol.10 (1), p.18415-18415, Article 18415 |
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| creator | Zhang, Weidong Waise, T. M. Zaved Toshinai, Koji Tsuchimochi, Wakaba Naznin, Farhana Islam, Md Nurul Tanida, Ryota Sakoda, Hideyuki Nakazato, Masamitsu |
| description | The gastrointestinal tract transmits feeding-regulatory signals to the brain via neuronal and hormonal pathways. Here we studied the interaction between the orexigenic gastric peptide, ghrelin, and the anorectic intestinal peptide, glucagon-like peptide 1 (GLP-1), in terms of feeding regulation via the vagal afferents. GLP-1 preadministration 30 min before ghrelin administration to rats and mice abolished ghrelin-induced food intake, while ghrelin preadministration abolished the anorectic effect of GLP-1. Ghrelin preadministration suppressed GLP-1-induced Fos expression in the nodose ganglia (NG). Electrophysiological assessment confirmed that the initially administered peptide abolished the vagal afferent electrical alteration induced by the subsequently administered peptide. Both the growth hormone secretagogue receptor (GHSR) and the GLP-1 receptor (GLP-1R) are co-localised in a major proportion of NG neurons that innervate the stomach. In these
Ghsr
+
Glp1r
+
neurons, ghrelin preadministration abolished the GLP-1-induced calcium response. Ghrelin generated a hyperpolarising current and GLP-1 generated a depolarising current in isolated NG neurons in a patch-clamp experiment. Ghrelin and GLP-1 potently influenced each other in terms of vagally mediated feeding regulation. This peptidergic interaction allows for fine control of the electrophysiological properties of NG neurons. |
| doi_str_mv | 10.1038/s41598-020-75621-5 |
| format | Article |
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Ghsr
+
Glp1r
+
neurons, ghrelin preadministration abolished the GLP-1-induced calcium response. Ghrelin generated a hyperpolarising current and GLP-1 generated a depolarising current in isolated NG neurons in a patch-clamp experiment. Ghrelin and GLP-1 potently influenced each other in terms of vagally mediated feeding regulation. This peptidergic interaction allows for fine control of the electrophysiological properties of NG neurons.</description><identifier>ISSN: 2045-2322</identifier><identifier>EISSN: 2045-2322</identifier><identifier>DOI: 10.1038/s41598-020-75621-5</identifier><identifier>PMID: 33116243</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>631/378 ; 631/443 ; 692/163 ; 692/4020 ; 692/617 ; Afferent Pathways - physiology ; Animals ; Appetite Regulation ; Calcium ; Calcium - metabolism ; Feeding ; Food intake ; Gastrointestinal tract ; Ghrelin ; Ghrelin - physiology ; Glucagon ; Glucagon-like peptide 1 ; Glucagon-Like Peptide 1 - physiology ; Glucagon-Like Peptide-1 Receptor - physiology ; Growth hormones ; Humanities and Social Sciences ; Intestine ; Male ; Mice, Inbred C57BL ; multidisciplinary ; Neurons ; Nodose ganglion ; Nodose Ganglion - physiology ; Peptides ; Rats, Wistar ; Receptors, Ghrelin - metabolism ; Science ; Science (multidisciplinary) ; Sensory neurons ; Vagus nerve</subject><ispartof>Scientific reports, 2020-10, Vol.10 (1), p.18415-18415, Article 18415</ispartof><rights>The Author(s) 2020</rights><rights>The Author(s) 2020. This work is published under 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><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c577t-5178e66b87f5ac85d00f57303783e55f658ab60096b8043a1dc3ff31336d70923</citedby><cites>FETCH-LOGICAL-c577t-5178e66b87f5ac85d00f57303783e55f658ab60096b8043a1dc3ff31336d70923</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/PMC7595212/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7595212/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,27924,27925,41120,42189,51576,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33116243$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhang, Weidong</creatorcontrib><creatorcontrib>Waise, T. M. Zaved</creatorcontrib><creatorcontrib>Toshinai, Koji</creatorcontrib><creatorcontrib>Tsuchimochi, Wakaba</creatorcontrib><creatorcontrib>Naznin, Farhana</creatorcontrib><creatorcontrib>Islam, Md Nurul</creatorcontrib><creatorcontrib>Tanida, Ryota</creatorcontrib><creatorcontrib>Sakoda, Hideyuki</creatorcontrib><creatorcontrib>Nakazato, Masamitsu</creatorcontrib><title>Functional interaction between Ghrelin and GLP-1 regulates feeding through the vagal afferent system</title><title>Scientific reports</title><addtitle>Sci Rep</addtitle><addtitle>Sci Rep</addtitle><description>The gastrointestinal tract transmits feeding-regulatory signals to the brain via neuronal and hormonal pathways. Here we studied the interaction between the orexigenic gastric peptide, ghrelin, and the anorectic intestinal peptide, glucagon-like peptide 1 (GLP-1), in terms of feeding regulation via the vagal afferents. GLP-1 preadministration 30 min before ghrelin administration to rats and mice abolished ghrelin-induced food intake, while ghrelin preadministration abolished the anorectic effect of GLP-1. Ghrelin preadministration suppressed GLP-1-induced Fos expression in the nodose ganglia (NG). Electrophysiological assessment confirmed that the initially administered peptide abolished the vagal afferent electrical alteration induced by the subsequently administered peptide. Both the growth hormone secretagogue receptor (GHSR) and the GLP-1 receptor (GLP-1R) are co-localised in a major proportion of NG neurons that innervate the stomach. In these
Ghsr
+
Glp1r
+
neurons, ghrelin preadministration abolished the GLP-1-induced calcium response. Ghrelin generated a hyperpolarising current and GLP-1 generated a depolarising current in isolated NG neurons in a patch-clamp experiment. Ghrelin and GLP-1 potently influenced each other in terms of vagally mediated feeding regulation. This peptidergic interaction allows for fine control of the electrophysiological properties of NG neurons.</description><subject>631/378</subject><subject>631/443</subject><subject>692/163</subject><subject>692/4020</subject><subject>692/617</subject><subject>Afferent Pathways - physiology</subject><subject>Animals</subject><subject>Appetite Regulation</subject><subject>Calcium</subject><subject>Calcium - metabolism</subject><subject>Feeding</subject><subject>Food intake</subject><subject>Gastrointestinal tract</subject><subject>Ghrelin</subject><subject>Ghrelin - physiology</subject><subject>Glucagon</subject><subject>Glucagon-like peptide 1</subject><subject>Glucagon-Like Peptide 1 - physiology</subject><subject>Glucagon-Like Peptide-1 Receptor - physiology</subject><subject>Growth hormones</subject><subject>Humanities and Social Sciences</subject><subject>Intestine</subject><subject>Male</subject><subject>Mice, Inbred C57BL</subject><subject>multidisciplinary</subject><subject>Neurons</subject><subject>Nodose ganglion</subject><subject>Nodose Ganglion - physiology</subject><subject>Peptides</subject><subject>Rats, Wistar</subject><subject>Receptors, Ghrelin - metabolism</subject><subject>Science</subject><subject>Science (multidisciplinary)</subject><subject>Sensory neurons</subject><subject>Vagus nerve</subject><issn>2045-2322</issn><issn>2045-2322</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>C6C</sourceid><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp9kU1P3DAQhq2qqKwW_kAPlaVeegn1R8ZOLpUqVBakleAAZ8ubjLNBWWdrO1T8e7y7QGkP-DK25pnXM_MS8pmzM85k9T2WHOqqYIIVGpTgBXwgM8FKKIQU4uOb-zE5jfGe5QOiLnn9iRxLybkSpZyR9mLyTepHbwfa-4TB7l90hekPoqeLdcCh99T6li6WNwWnAbtpsAkjdYht7zua1mGcunWOSB9sl5WscxjQJxofY8LNCTlydoh4-hzn5O7i1-35ZbG8Xlyd_1wWDWidCuC6QqVWlXZgmwpaxhxoyaSuJAI4BZVdKcbqjLBSWt420jnJpVStZrWQc_LjoLudVhtsm9xBsIPZhn5jw6MZbW_-zfh-bbrxwWioQfCdwLdngTD-njAms-ljg8NgPY5TNKIEqGStSp3Rr_-h9-MU8hp3lOZQMlAsU-JANWGMMaB7bYYzs_PRHHw02Uez99FALvrydozXkhfXMiAPQMwp32H4-_c7sk8W_6hY</recordid><startdate>20201028</startdate><enddate>20201028</enddate><creator>Zhang, Weidong</creator><creator>Waise, T. 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Zaved</creator><creator>Toshinai, Koji</creator><creator>Tsuchimochi, Wakaba</creator><creator>Naznin, Farhana</creator><creator>Islam, Md Nurul</creator><creator>Tanida, Ryota</creator><creator>Sakoda, Hideyuki</creator><creator>Nakazato, Masamitsu</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</general><scope>C6C</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>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88I</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20201028</creationdate><title>Functional interaction between Ghrelin and GLP-1 regulates feeding through the vagal afferent system</title><author>Zhang, Weidong ; Waise, T. 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Zaved ; Toshinai, Koji ; Tsuchimochi, Wakaba ; Naznin, Farhana ; Islam, Md Nurul ; Tanida, Ryota ; Sakoda, Hideyuki ; Nakazato, Masamitsu</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c577t-5178e66b87f5ac85d00f57303783e55f658ab60096b8043a1dc3ff31336d70923</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>631/378</topic><topic>631/443</topic><topic>692/163</topic><topic>692/4020</topic><topic>692/617</topic><topic>Afferent Pathways - physiology</topic><topic>Animals</topic><topic>Appetite Regulation</topic><topic>Calcium</topic><topic>Calcium - metabolism</topic><topic>Feeding</topic><topic>Food intake</topic><topic>Gastrointestinal tract</topic><topic>Ghrelin</topic><topic>Ghrelin - physiology</topic><topic>Glucagon</topic><topic>Glucagon-like peptide 1</topic><topic>Glucagon-Like Peptide 1 - physiology</topic><topic>Glucagon-Like Peptide-1 Receptor - physiology</topic><topic>Growth hormones</topic><topic>Humanities and Social Sciences</topic><topic>Intestine</topic><topic>Male</topic><topic>Mice, Inbred C57BL</topic><topic>multidisciplinary</topic><topic>Neurons</topic><topic>Nodose ganglion</topic><topic>Nodose Ganglion - physiology</topic><topic>Peptides</topic><topic>Rats, Wistar</topic><topic>Receptors, Ghrelin - metabolism</topic><topic>Science</topic><topic>Science (multidisciplinary)</topic><topic>Sensory neurons</topic><topic>Vagus nerve</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zhang, Weidong</creatorcontrib><creatorcontrib>Waise, T. 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Zaved</creatorcontrib><creatorcontrib>Toshinai, Koji</creatorcontrib><creatorcontrib>Tsuchimochi, Wakaba</creatorcontrib><creatorcontrib>Naznin, Farhana</creatorcontrib><creatorcontrib>Islam, Md Nurul</creatorcontrib><creatorcontrib>Tanida, Ryota</creatorcontrib><creatorcontrib>Sakoda, Hideyuki</creatorcontrib><creatorcontrib>Nakazato, Masamitsu</creatorcontrib><collection>Springer Nature OA Free Journals</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>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Science Database (Alumni Edition)</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</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>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</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 Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Science Database</collection><collection>Biological Science 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>ProQuest Central Basic</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Scientific reports</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhang, Weidong</au><au>Waise, T. M. Zaved</au><au>Toshinai, Koji</au><au>Tsuchimochi, Wakaba</au><au>Naznin, Farhana</au><au>Islam, Md Nurul</au><au>Tanida, Ryota</au><au>Sakoda, Hideyuki</au><au>Nakazato, Masamitsu</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Functional interaction between Ghrelin and GLP-1 regulates feeding through the vagal afferent system</atitle><jtitle>Scientific reports</jtitle><stitle>Sci Rep</stitle><addtitle>Sci Rep</addtitle><date>2020-10-28</date><risdate>2020</risdate><volume>10</volume><issue>1</issue><spage>18415</spage><epage>18415</epage><pages>18415-18415</pages><artnum>18415</artnum><issn>2045-2322</issn><eissn>2045-2322</eissn><abstract>The gastrointestinal tract transmits feeding-regulatory signals to the brain via neuronal and hormonal pathways. Here we studied the interaction between the orexigenic gastric peptide, ghrelin, and the anorectic intestinal peptide, glucagon-like peptide 1 (GLP-1), in terms of feeding regulation via the vagal afferents. GLP-1 preadministration 30 min before ghrelin administration to rats and mice abolished ghrelin-induced food intake, while ghrelin preadministration abolished the anorectic effect of GLP-1. Ghrelin preadministration suppressed GLP-1-induced Fos expression in the nodose ganglia (NG). Electrophysiological assessment confirmed that the initially administered peptide abolished the vagal afferent electrical alteration induced by the subsequently administered peptide. Both the growth hormone secretagogue receptor (GHSR) and the GLP-1 receptor (GLP-1R) are co-localised in a major proportion of NG neurons that innervate the stomach. In these
Ghsr
+
Glp1r
+
neurons, ghrelin preadministration abolished the GLP-1-induced calcium response. Ghrelin generated a hyperpolarising current and GLP-1 generated a depolarising current in isolated NG neurons in a patch-clamp experiment. Ghrelin and GLP-1 potently influenced each other in terms of vagally mediated feeding regulation. This peptidergic interaction allows for fine control of the electrophysiological properties of NG neurons.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>33116243</pmid><doi>10.1038/s41598-020-75621-5</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | 631/378 631/443 692/163 692/4020 692/617 Afferent Pathways - physiology Animals Appetite Regulation Calcium Calcium - metabolism Feeding Food intake Gastrointestinal tract Ghrelin Ghrelin - physiology Glucagon Glucagon-like peptide 1 Glucagon-Like Peptide 1 - physiology Glucagon-Like Peptide-1 Receptor - physiology Growth hormones Humanities and Social Sciences Intestine Male Mice, Inbred C57BL multidisciplinary Neurons Nodose ganglion Nodose Ganglion - physiology Peptides Rats, Wistar Receptors, Ghrelin - metabolism Science Science (multidisciplinary) Sensory neurons Vagus nerve |
| title | Functional interaction between Ghrelin and GLP-1 regulates feeding through the vagal afferent system |
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