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A Cre-driver rat model for anatomical and functional analysis of glucagon (Gcg)-expressing cells in the brain and periphery
The glucagon gene (Gcg) encodes preproglucagon, which is cleaved to form glucagon-like peptide 1 (GLP1) and other mature signaling molecules implicated in metabolic functions. To date there are no transgenic rat models available for precise manipulation of GLP1-expressing cells in the brain and peri...
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Published in: | Molecular metabolism (Germany) 2022-12, Vol.66, p.101631-101631, Article 101631 |
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creator | Zheng, Huiyuan López-Ferreras, Lorena Krieger, Jean-Phillipe Fasul, Stephen Cea Salazar, Valentina Valderrama Pena, Natalia Skibicka, Karolina P. Rinaman, Linda |
description | The glucagon gene (Gcg) encodes preproglucagon, which is cleaved to form glucagon-like peptide 1 (GLP1) and other mature signaling molecules implicated in metabolic functions. To date there are no transgenic rat models available for precise manipulation of GLP1-expressing cells in the brain and periphery.
To visualize and manipulate Gcg-expressing cells in rats, CRISPR/Cas9 was used to express iCre under control of the Gcg promoter. Gcg-Cre rats were bred with tdTomato reporter rats to tag Gcg-expressing cells. Cre-dependent AAVs and RNAscope in situ hybridization were used to evaluate the specificity of iCre expression by GLP1 neurons in the caudal nucleus of the solitary tract (cNTS) and intermediate reticular nucleus (IRt), and by intestinal and pancreatic secretory cells. Food intake was assessed in heterozygous (Het) Gcg-Cre rats after chemogenetic stimulation of cNTS GLP1 neurons expressing an excitatory DREADD.
While genotype has minimal effect on body weight or composition in chow-fed Gcg-Cre rats, homozygous (Homo) rats have lower plasma glucose levels. In neonatal and adult Gcg-Cre/tdTom rats, reporter-labeled cells are present in the cNTS and IRt, and in additional brain regions (e.g., basolateral amygdala, piriform cortex) that lack detectable Gcg mRNA in adults but display transient developmental or persistently low Gcg expression. Compared to wildtype (WT) rats, hindbrain Gcg mRNA and GLP1 protein in brain and plasma are markedly reduced in Homo Gcg-Cre rats. Chemogenetic stimulation of cNTS GLP1 neurons reduced overnight chow intake in males but not females, the effect in males was blocked by antagonism of central GLP1 receptors, and hypophagia was enhanced when combined with a subthreshold dose of cholecystokinin-8 to stimulate gastrointestinal vagal afferents.
Gcg-Cre rats are a novel and valuable experimental tool for analyzing the development, anatomy, and function of Gcg-expressing cells in the brain and periphery. In addition, Homo Gcg-Cre rats are a unique model for assessing the role of Gcg-encoded proteins in glucose homeostasis and energy metabolism.
•A transgenic Gcg-Cre rat model expresses iCre under control of the Gcg promoter.•iCre is expressed by GLP1-positive cells in the hindbrain, pancreas, and intestine.•Additional brain regions display transient and/or very low levels of Gcg expression.•+/+ Gcg-Cre rats display a marked knockdown of Gcg mRNA and GLP1 protein.•Chemogenetic activation of Gcg neurons suppresses food intake i |
doi_str_mv | 10.1016/j.molmet.2022.101631 |
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To visualize and manipulate Gcg-expressing cells in rats, CRISPR/Cas9 was used to express iCre under control of the Gcg promoter. Gcg-Cre rats were bred with tdTomato reporter rats to tag Gcg-expressing cells. Cre-dependent AAVs and RNAscope in situ hybridization were used to evaluate the specificity of iCre expression by GLP1 neurons in the caudal nucleus of the solitary tract (cNTS) and intermediate reticular nucleus (IRt), and by intestinal and pancreatic secretory cells. Food intake was assessed in heterozygous (Het) Gcg-Cre rats after chemogenetic stimulation of cNTS GLP1 neurons expressing an excitatory DREADD.
While genotype has minimal effect on body weight or composition in chow-fed Gcg-Cre rats, homozygous (Homo) rats have lower plasma glucose levels. In neonatal and adult Gcg-Cre/tdTom rats, reporter-labeled cells are present in the cNTS and IRt, and in additional brain regions (e.g., basolateral amygdala, piriform cortex) that lack detectable Gcg mRNA in adults but display transient developmental or persistently low Gcg expression. Compared to wildtype (WT) rats, hindbrain Gcg mRNA and GLP1 protein in brain and plasma are markedly reduced in Homo Gcg-Cre rats. Chemogenetic stimulation of cNTS GLP1 neurons reduced overnight chow intake in males but not females, the effect in males was blocked by antagonism of central GLP1 receptors, and hypophagia was enhanced when combined with a subthreshold dose of cholecystokinin-8 to stimulate gastrointestinal vagal afferents.
Gcg-Cre rats are a novel and valuable experimental tool for analyzing the development, anatomy, and function of Gcg-expressing cells in the brain and periphery. In addition, Homo Gcg-Cre rats are a unique model for assessing the role of Gcg-encoded proteins in glucose homeostasis and energy metabolism.
•A transgenic Gcg-Cre rat model expresses iCre under control of the Gcg promoter.•iCre is expressed by GLP1-positive cells in the hindbrain, pancreas, and intestine.•Additional brain regions display transient and/or very low levels of Gcg expression.•+/+ Gcg-Cre rats display a marked knockdown of Gcg mRNA and GLP1 protein.•Chemogenetic activation of Gcg neurons suppresses food intake in +/− Gcg-Cre rats.</description><identifier>ISSN: 2212-8778</identifier><identifier>EISSN: 2212-8778</identifier><identifier>DOI: 10.1016/j.molmet.2022.101631</identifier><identifier>PMID: 36368622</identifier><language>eng</language><publisher>Germany: Elsevier GmbH</publisher><subject>Animals ; Brain ; Food intake ; Glucagon - metabolism ; Glucagon-like peptide 1 ; Glucagon-Like Peptide 1 - genetics ; Glucagon-Like Peptide 1 - metabolism ; Glucagon-Secreting Cells - metabolism ; Intestine ; Male ; Neurosciences ; Neurovetenskaper ; Original ; Pancreas ; Rats ; RNA, Messenger - metabolism ; Solitary Nucleus - metabolism</subject><ispartof>Molecular metabolism (Germany), 2022-12, Vol.66, p.101631-101631, Article 101631</ispartof><rights>2022 The Author(s)</rights><rights>Copyright © 2022 The Author(s). Published by Elsevier GmbH.. All rights reserved.</rights><rights>2022 The Author(s) 2022</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c567t-300e41d4e9785950c1eaaf16a84c31b8943081627864345aa284a435896487d93</citedby><cites>FETCH-LOGICAL-c567t-300e41d4e9785950c1eaaf16a84c31b8943081627864345aa284a435896487d93</cites><orcidid>0000-0001-5999-8811</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/PMC9677222/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S2212877822002009$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,3549,27924,27925,45780,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36368622$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://gup.ub.gu.se/publication/323621$$DView record from Swedish Publication Index$$Hfree_for_read</backlink></links><search><creatorcontrib>Zheng, Huiyuan</creatorcontrib><creatorcontrib>López-Ferreras, Lorena</creatorcontrib><creatorcontrib>Krieger, Jean-Phillipe</creatorcontrib><creatorcontrib>Fasul, Stephen</creatorcontrib><creatorcontrib>Cea Salazar, Valentina</creatorcontrib><creatorcontrib>Valderrama Pena, Natalia</creatorcontrib><creatorcontrib>Skibicka, Karolina P.</creatorcontrib><creatorcontrib>Rinaman, Linda</creatorcontrib><title>A Cre-driver rat model for anatomical and functional analysis of glucagon (Gcg)-expressing cells in the brain and periphery</title><title>Molecular metabolism (Germany)</title><addtitle>Mol Metab</addtitle><description>The glucagon gene (Gcg) encodes preproglucagon, which is cleaved to form glucagon-like peptide 1 (GLP1) and other mature signaling molecules implicated in metabolic functions. To date there are no transgenic rat models available for precise manipulation of GLP1-expressing cells in the brain and periphery.
To visualize and manipulate Gcg-expressing cells in rats, CRISPR/Cas9 was used to express iCre under control of the Gcg promoter. Gcg-Cre rats were bred with tdTomato reporter rats to tag Gcg-expressing cells. Cre-dependent AAVs and RNAscope in situ hybridization were used to evaluate the specificity of iCre expression by GLP1 neurons in the caudal nucleus of the solitary tract (cNTS) and intermediate reticular nucleus (IRt), and by intestinal and pancreatic secretory cells. Food intake was assessed in heterozygous (Het) Gcg-Cre rats after chemogenetic stimulation of cNTS GLP1 neurons expressing an excitatory DREADD.
While genotype has minimal effect on body weight or composition in chow-fed Gcg-Cre rats, homozygous (Homo) rats have lower plasma glucose levels. In neonatal and adult Gcg-Cre/tdTom rats, reporter-labeled cells are present in the cNTS and IRt, and in additional brain regions (e.g., basolateral amygdala, piriform cortex) that lack detectable Gcg mRNA in adults but display transient developmental or persistently low Gcg expression. Compared to wildtype (WT) rats, hindbrain Gcg mRNA and GLP1 protein in brain and plasma are markedly reduced in Homo Gcg-Cre rats. Chemogenetic stimulation of cNTS GLP1 neurons reduced overnight chow intake in males but not females, the effect in males was blocked by antagonism of central GLP1 receptors, and hypophagia was enhanced when combined with a subthreshold dose of cholecystokinin-8 to stimulate gastrointestinal vagal afferents.
Gcg-Cre rats are a novel and valuable experimental tool for analyzing the development, anatomy, and function of Gcg-expressing cells in the brain and periphery. In addition, Homo Gcg-Cre rats are a unique model for assessing the role of Gcg-encoded proteins in glucose homeostasis and energy metabolism.
•A transgenic Gcg-Cre rat model expresses iCre under control of the Gcg promoter.•iCre is expressed by GLP1-positive cells in the hindbrain, pancreas, and intestine.•Additional brain regions display transient and/or very low levels of Gcg expression.•+/+ Gcg-Cre rats display a marked knockdown of Gcg mRNA and GLP1 protein.•Chemogenetic activation of Gcg neurons suppresses food intake in +/− Gcg-Cre rats.</description><subject>Animals</subject><subject>Brain</subject><subject>Food intake</subject><subject>Glucagon - metabolism</subject><subject>Glucagon-like peptide 1</subject><subject>Glucagon-Like Peptide 1 - genetics</subject><subject>Glucagon-Like Peptide 1 - metabolism</subject><subject>Glucagon-Secreting Cells - metabolism</subject><subject>Intestine</subject><subject>Male</subject><subject>Neurosciences</subject><subject>Neurovetenskaper</subject><subject>Original</subject><subject>Pancreas</subject><subject>Rats</subject><subject>RNA, Messenger - metabolism</subject><subject>Solitary Nucleus - metabolism</subject><issn>2212-8778</issn><issn>2212-8778</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>DOA</sourceid><recordid>eNp9Uk1v1DAQjRCIVqX_ACEfyyFL_BHbuSBVKyiVKnGBszXrTLJeJXGwk4UVfx7vppTuBV88Hr_3xjN-WfaWFitaUPlht-p91-O0YgVjpxSnL7JLxijLtVL65bP4IruOcVekpaWUJX2dXXDJpZaMXWa_b8k6YF4Ht8dAAkyk9zV2pPGBwACT752FLoU1aebBTs4PpyN0h-gi8Q1pu9lC6wdyc2fb9zn-GgPG6IaWWOy6SNxApi2STYAUHXVGDG7cYji8yV410EW8ftyvsu-fP31bf8kfvt7dr28fcltKNeW8KFDQWmCldFmVhaUI0FAJWlhON7oSvNBUMqWl4KIEYFqA4KWupNCqrvhVdr_o1h52Zgyuh3AwHpw5JXxoDYTJ2Q4NayzWFAWoRolGNKApMF5sQNm6QY1JK1-04k8c582ZWjuPJqXa2UQ0nHHJaMJ_XPAJ3GNtcZgCdGe085vBbU3r96aSSjHGksDNo0DwP2aMk-ldPE4WBvRzNEylTpWSmieoWKA2-BgDNk9laGGOHjE7s9jGHG1jFtsk2rvnT3wi_TXJvx4wfdLeYTDROhzSpFxAO6Upuv9X-AO1pNbu</recordid><startdate>20221201</startdate><enddate>20221201</enddate><creator>Zheng, Huiyuan</creator><creator>López-Ferreras, Lorena</creator><creator>Krieger, Jean-Phillipe</creator><creator>Fasul, Stephen</creator><creator>Cea Salazar, Valentina</creator><creator>Valderrama Pena, Natalia</creator><creator>Skibicka, Karolina P.</creator><creator>Rinaman, Linda</creator><general>Elsevier GmbH</general><general>Elsevier</general><scope>6I.</scope><scope>AAFTH</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><scope>5PM</scope><scope>ADTPV</scope><scope>AOWAS</scope><scope>F1U</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0001-5999-8811</orcidid></search><sort><creationdate>20221201</creationdate><title>A Cre-driver rat model for anatomical and functional analysis of glucagon (Gcg)-expressing cells in the brain and periphery</title><author>Zheng, Huiyuan ; López-Ferreras, Lorena ; Krieger, Jean-Phillipe ; Fasul, Stephen ; Cea Salazar, Valentina ; Valderrama Pena, Natalia ; Skibicka, Karolina P. ; Rinaman, Linda</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c567t-300e41d4e9785950c1eaaf16a84c31b8943081627864345aa284a435896487d93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Animals</topic><topic>Brain</topic><topic>Food intake</topic><topic>Glucagon - metabolism</topic><topic>Glucagon-like peptide 1</topic><topic>Glucagon-Like Peptide 1 - genetics</topic><topic>Glucagon-Like Peptide 1 - metabolism</topic><topic>Glucagon-Secreting Cells - metabolism</topic><topic>Intestine</topic><topic>Male</topic><topic>Neurosciences</topic><topic>Neurovetenskaper</topic><topic>Original</topic><topic>Pancreas</topic><topic>Rats</topic><topic>RNA, Messenger - metabolism</topic><topic>Solitary Nucleus - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zheng, Huiyuan</creatorcontrib><creatorcontrib>López-Ferreras, Lorena</creatorcontrib><creatorcontrib>Krieger, Jean-Phillipe</creatorcontrib><creatorcontrib>Fasul, Stephen</creatorcontrib><creatorcontrib>Cea Salazar, Valentina</creatorcontrib><creatorcontrib>Valderrama Pena, Natalia</creatorcontrib><creatorcontrib>Skibicka, Karolina P.</creatorcontrib><creatorcontrib>Rinaman, Linda</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</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><collection>PubMed Central (Full Participant titles)</collection><collection>SwePub</collection><collection>SwePub Articles</collection><collection>SWEPUB Göteborgs universitet</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>Molecular metabolism (Germany)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zheng, Huiyuan</au><au>López-Ferreras, Lorena</au><au>Krieger, Jean-Phillipe</au><au>Fasul, Stephen</au><au>Cea Salazar, Valentina</au><au>Valderrama Pena, Natalia</au><au>Skibicka, Karolina P.</au><au>Rinaman, Linda</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A Cre-driver rat model for anatomical and functional analysis of glucagon (Gcg)-expressing cells in the brain and periphery</atitle><jtitle>Molecular metabolism (Germany)</jtitle><addtitle>Mol Metab</addtitle><date>2022-12-01</date><risdate>2022</risdate><volume>66</volume><spage>101631</spage><epage>101631</epage><pages>101631-101631</pages><artnum>101631</artnum><issn>2212-8778</issn><eissn>2212-8778</eissn><abstract>The glucagon gene (Gcg) encodes preproglucagon, which is cleaved to form glucagon-like peptide 1 (GLP1) and other mature signaling molecules implicated in metabolic functions. To date there are no transgenic rat models available for precise manipulation of GLP1-expressing cells in the brain and periphery.
To visualize and manipulate Gcg-expressing cells in rats, CRISPR/Cas9 was used to express iCre under control of the Gcg promoter. Gcg-Cre rats were bred with tdTomato reporter rats to tag Gcg-expressing cells. Cre-dependent AAVs and RNAscope in situ hybridization were used to evaluate the specificity of iCre expression by GLP1 neurons in the caudal nucleus of the solitary tract (cNTS) and intermediate reticular nucleus (IRt), and by intestinal and pancreatic secretory cells. Food intake was assessed in heterozygous (Het) Gcg-Cre rats after chemogenetic stimulation of cNTS GLP1 neurons expressing an excitatory DREADD.
While genotype has minimal effect on body weight or composition in chow-fed Gcg-Cre rats, homozygous (Homo) rats have lower plasma glucose levels. In neonatal and adult Gcg-Cre/tdTom rats, reporter-labeled cells are present in the cNTS and IRt, and in additional brain regions (e.g., basolateral amygdala, piriform cortex) that lack detectable Gcg mRNA in adults but display transient developmental or persistently low Gcg expression. Compared to wildtype (WT) rats, hindbrain Gcg mRNA and GLP1 protein in brain and plasma are markedly reduced in Homo Gcg-Cre rats. Chemogenetic stimulation of cNTS GLP1 neurons reduced overnight chow intake in males but not females, the effect in males was blocked by antagonism of central GLP1 receptors, and hypophagia was enhanced when combined with a subthreshold dose of cholecystokinin-8 to stimulate gastrointestinal vagal afferents.
Gcg-Cre rats are a novel and valuable experimental tool for analyzing the development, anatomy, and function of Gcg-expressing cells in the brain and periphery. In addition, Homo Gcg-Cre rats are a unique model for assessing the role of Gcg-encoded proteins in glucose homeostasis and energy metabolism.
•A transgenic Gcg-Cre rat model expresses iCre under control of the Gcg promoter.•iCre is expressed by GLP1-positive cells in the hindbrain, pancreas, and intestine.•Additional brain regions display transient and/or very low levels of Gcg expression.•+/+ Gcg-Cre rats display a marked knockdown of Gcg mRNA and GLP1 protein.•Chemogenetic activation of Gcg neurons suppresses food intake in +/− Gcg-Cre rats.</abstract><cop>Germany</cop><pub>Elsevier GmbH</pub><pmid>36368622</pmid><doi>10.1016/j.molmet.2022.101631</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0001-5999-8811</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Brain Food intake Glucagon - metabolism Glucagon-like peptide 1 Glucagon-Like Peptide 1 - genetics Glucagon-Like Peptide 1 - metabolism Glucagon-Secreting Cells - metabolism Intestine Male Neurosciences Neurovetenskaper Original Pancreas Rats RNA, Messenger - metabolism Solitary Nucleus - metabolism |
title | A Cre-driver rat model for anatomical and functional analysis of glucagon (Gcg)-expressing cells in the brain and periphery |
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