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Insulin and the Constituent Branches of the Hepatic Vagus Interact to Modulate Hypothalamic and Limbic Neuropeptide mRNA Expression Differentially
Insulin and signalling through the vagus nerve act in concert to regulate metabolic homeostasis and ingestive behaviour. Our previous studies using streptozotocin (STZ)‐diabetic rats have shown that hepatic branch vagotomy (HV), gastroduodenal branch vagotomy (GV) and capsaicin treatment of the comm...
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| Published in: | Journal of neuroendocrinology 2008-09, Vol.20 (9), p.1067-1077 |
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| creator | Warne, J. P. Horneman, H. F. Akana, S. F. Foster, M. T. Dallman, M. F. |
| description | Insulin and signalling through the vagus nerve act in concert to regulate metabolic homeostasis and ingestive behaviour. Our previous studies using streptozotocin (STZ)‐diabetic rats have shown that hepatic branch vagotomy (HV), gastroduodenal branch vagotomy (GV) and capsaicin treatment of the common hepatic branch that selectively destroys afferent fibres (CapV), all promote lard, but not total, caloric intake to levels similar to those achieved with insulin treatment. Because hypothalamic and limbic mRNA expression of neuropeptides linked to energy balance is altered by STZ‐diabetes and HV, we examined the role(s) of insulin and the common hepatic and gastroduodenal branches of the vagus nerve and hepatic afferent fibres in the regulation of these neuropeptides in rats with high, steady‐state corticosterone levels. STZ‐diabetic rats were prepared with osmotic minipumps containing either saline or insulin and were compared with nondiabetic counterparts: half of each group received a vagal manipulation, the other half were sham operated. Five days after surgery, rats were offered the choice of lard and chow to consume for another 5 days, when brains were collected and processed for in situ hybridisation. Paraventricular nucleus corticotrophin‐releasing factor (CRF) mRNA was elevated by STZ treatment, an effect prevented by either insulin treatment or GV. By contrast, CRF mRNA expression in the central nucleus of the amygdala and bed nuclei of the stria terminalis was unaffected by STZ treatment, but HV and CapV manipulations elevated expression in the nondiabetic, but not STZ‐diabetic groups. Arcuate nucleus neuropeptide Y, but not pro‐opiomelanocortin, mRNA expression was elevated by STZ treatment and all vagal manipulations; however, exogenous insulin treatment failed to prevent this, in keeping with their previously documented elevated caloric intake. These results strongly suggest that the gastroduodenal branch and hepatic branch proper, which merge to form the common hepatic branch, differentially interact with prevailing insulin levels to regulate hypothalamic and limbic neuropeptide mRNA expression. |
| doi_str_mv | 10.1111/j.1365-2826.2008.01766.x |
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P. ; Horneman, H. F. ; Akana, S. F. ; Foster, M. T. ; Dallman, M. F.</creator><creatorcontrib>Warne, J. P. ; Horneman, H. F. ; Akana, S. F. ; Foster, M. T. ; Dallman, M. F.</creatorcontrib><description>Insulin and signalling through the vagus nerve act in concert to regulate metabolic homeostasis and ingestive behaviour. Our previous studies using streptozotocin (STZ)‐diabetic rats have shown that hepatic branch vagotomy (HV), gastroduodenal branch vagotomy (GV) and capsaicin treatment of the common hepatic branch that selectively destroys afferent fibres (CapV), all promote lard, but not total, caloric intake to levels similar to those achieved with insulin treatment. Because hypothalamic and limbic mRNA expression of neuropeptides linked to energy balance is altered by STZ‐diabetes and HV, we examined the role(s) of insulin and the common hepatic and gastroduodenal branches of the vagus nerve and hepatic afferent fibres in the regulation of these neuropeptides in rats with high, steady‐state corticosterone levels. STZ‐diabetic rats were prepared with osmotic minipumps containing either saline or insulin and were compared with nondiabetic counterparts: half of each group received a vagal manipulation, the other half were sham operated. Five days after surgery, rats were offered the choice of lard and chow to consume for another 5 days, when brains were collected and processed for in situ hybridisation. Paraventricular nucleus corticotrophin‐releasing factor (CRF) mRNA was elevated by STZ treatment, an effect prevented by either insulin treatment or GV. By contrast, CRF mRNA expression in the central nucleus of the amygdala and bed nuclei of the stria terminalis was unaffected by STZ treatment, but HV and CapV manipulations elevated expression in the nondiabetic, but not STZ‐diabetic groups. Arcuate nucleus neuropeptide Y, but not pro‐opiomelanocortin, mRNA expression was elevated by STZ treatment and all vagal manipulations; however, exogenous insulin treatment failed to prevent this, in keeping with their previously documented elevated caloric intake. These results strongly suggest that the gastroduodenal branch and hepatic branch proper, which merge to form the common hepatic branch, differentially interact with prevailing insulin levels to regulate hypothalamic and limbic neuropeptide mRNA expression.</description><identifier>ISSN: 0953-8194</identifier><identifier>EISSN: 1365-2826</identifier><identifier>DOI: 10.1111/j.1365-2826.2008.01766.x</identifier><identifier>PMID: 18638024</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Publishing Ltd</publisher><subject>Animals ; Biological and medical sciences ; Corticosterone - blood ; corticotrophin-releasing factor ; Corticotropin-Releasing Hormone - genetics ; Corticotropin-Releasing Hormone - metabolism ; Diabetes Mellitus, Experimental - blood ; Diabetes Mellitus, Experimental - genetics ; Diabetes Mellitus, Experimental - metabolism ; Fundamental and applied biological sciences. Psychology ; Gene Expression Regulation - drug effects ; glucocorticoids ; Hypothalamus - drug effects ; Hypothalamus - metabolism ; insulin ; Insulin - pharmacology ; Limbic System - drug effects ; Limbic System - metabolism ; Liver - drug effects ; Liver - innervation ; Male ; Models, Biological ; neuropeptide Y ; Neuropeptide Y - genetics ; Neuropeptide Y - metabolism ; Neuropeptides - genetics ; Neuropeptides - metabolism ; pro-opiomelanocortin ; Pro-Opiomelanocortin - genetics ; Pro-Opiomelanocortin - metabolism ; Rats ; Rats, Sprague-Dawley ; RNA, Messenger - metabolism ; Streptozocin ; vagus nerve ; Vagus Nerve - physiology ; Vertebrates: endocrinology</subject><ispartof>Journal of neuroendocrinology, 2008-09, Vol.20 (9), p.1067-1077</ispartof><rights>2008 The Authors. 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P.</creatorcontrib><creatorcontrib>Horneman, H. F.</creatorcontrib><creatorcontrib>Akana, S. F.</creatorcontrib><creatorcontrib>Foster, M. T.</creatorcontrib><creatorcontrib>Dallman, M. F.</creatorcontrib><title>Insulin and the Constituent Branches of the Hepatic Vagus Interact to Modulate Hypothalamic and Limbic Neuropeptide mRNA Expression Differentially</title><title>Journal of neuroendocrinology</title><addtitle>J Neuroendocrinol</addtitle><description>Insulin and signalling through the vagus nerve act in concert to regulate metabolic homeostasis and ingestive behaviour. Our previous studies using streptozotocin (STZ)‐diabetic rats have shown that hepatic branch vagotomy (HV), gastroduodenal branch vagotomy (GV) and capsaicin treatment of the common hepatic branch that selectively destroys afferent fibres (CapV), all promote lard, but not total, caloric intake to levels similar to those achieved with insulin treatment. Because hypothalamic and limbic mRNA expression of neuropeptides linked to energy balance is altered by STZ‐diabetes and HV, we examined the role(s) of insulin and the common hepatic and gastroduodenal branches of the vagus nerve and hepatic afferent fibres in the regulation of these neuropeptides in rats with high, steady‐state corticosterone levels. STZ‐diabetic rats were prepared with osmotic minipumps containing either saline or insulin and were compared with nondiabetic counterparts: half of each group received a vagal manipulation, the other half were sham operated. Five days after surgery, rats were offered the choice of lard and chow to consume for another 5 days, when brains were collected and processed for in situ hybridisation. Paraventricular nucleus corticotrophin‐releasing factor (CRF) mRNA was elevated by STZ treatment, an effect prevented by either insulin treatment or GV. By contrast, CRF mRNA expression in the central nucleus of the amygdala and bed nuclei of the stria terminalis was unaffected by STZ treatment, but HV and CapV manipulations elevated expression in the nondiabetic, but not STZ‐diabetic groups. Arcuate nucleus neuropeptide Y, but not pro‐opiomelanocortin, mRNA expression was elevated by STZ treatment and all vagal manipulations; however, exogenous insulin treatment failed to prevent this, in keeping with their previously documented elevated caloric intake. These results strongly suggest that the gastroduodenal branch and hepatic branch proper, which merge to form the common hepatic branch, differentially interact with prevailing insulin levels to regulate hypothalamic and limbic neuropeptide mRNA expression.</description><subject>Animals</subject><subject>Biological and medical sciences</subject><subject>Corticosterone - blood</subject><subject>corticotrophin-releasing factor</subject><subject>Corticotropin-Releasing Hormone - genetics</subject><subject>Corticotropin-Releasing Hormone - metabolism</subject><subject>Diabetes Mellitus, Experimental - blood</subject><subject>Diabetes Mellitus, Experimental - genetics</subject><subject>Diabetes Mellitus, Experimental - metabolism</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Gene Expression Regulation - drug effects</subject><subject>glucocorticoids</subject><subject>Hypothalamus - drug effects</subject><subject>Hypothalamus - metabolism</subject><subject>insulin</subject><subject>Insulin - pharmacology</subject><subject>Limbic System - drug effects</subject><subject>Limbic System - metabolism</subject><subject>Liver - drug effects</subject><subject>Liver - innervation</subject><subject>Male</subject><subject>Models, Biological</subject><subject>neuropeptide Y</subject><subject>Neuropeptide Y - genetics</subject><subject>Neuropeptide Y - metabolism</subject><subject>Neuropeptides - genetics</subject><subject>Neuropeptides - metabolism</subject><subject>pro-opiomelanocortin</subject><subject>Pro-Opiomelanocortin - genetics</subject><subject>Pro-Opiomelanocortin - metabolism</subject><subject>Rats</subject><subject>Rats, Sprague-Dawley</subject><subject>RNA, Messenger - metabolism</subject><subject>Streptozocin</subject><subject>vagus nerve</subject><subject>Vagus Nerve - physiology</subject><subject>Vertebrates: endocrinology</subject><issn>0953-8194</issn><issn>1365-2826</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2008</creationdate><recordtype>article</recordtype><recordid>eNqNkc2O0zAUhS0EYsrAKyBvYJfgn8RxFixmSmemqBQJVbC0XOeGuuRvbEe0r8ET40yrssUbX-l-596rcxDClKQ0vg_7lHKRJ0wykTJCZEpoIUR6eIZml8ZzNCNlzhNJy-wKvfJ-TyKVc_ISXVEpuCQsm6E_y86Pje2w7iocdoDnfeeDDSN0Ad863ZkdeNzXT70HGHSwBn_XP0ePl10Ap03Aocdf-mpsdIjIcejDTje6jdw0c2XbbSzXMLp-gCHYCnD7bX2DF4fBgfe27_AnW9fg4karm-b4Gr2odePhzfm_Rpu7xWb-kKy-3i_nN6vEZEKIBAg3LNvKWkpSMU0kKQUThovoBytgS42kVNakiI5ATvOMcgK6ZqUuQXPKr9H709jB9Y8j-KBa6w00je6gH72iZUFpLvIIyhNoXO-9g1oNzrbaHRUlaopD7dXkuppcV1Mc6ikOdYjSt-cd47aF6p_w7H8E3p0B7Y1u6slw6y8cI7mUohSR-3jiftsGjv99gPq8XkxV1CcnvfUBDhe9dr-UKHiRqx_re7WSgm028lbd8b-P4rYC</recordid><startdate>200809</startdate><enddate>200809</enddate><creator>Warne, J. 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Psychology</topic><topic>Gene Expression Regulation - drug effects</topic><topic>glucocorticoids</topic><topic>Hypothalamus - drug effects</topic><topic>Hypothalamus - metabolism</topic><topic>insulin</topic><topic>Insulin - pharmacology</topic><topic>Limbic System - drug effects</topic><topic>Limbic System - metabolism</topic><topic>Liver - drug effects</topic><topic>Liver - innervation</topic><topic>Male</topic><topic>Models, Biological</topic><topic>neuropeptide Y</topic><topic>Neuropeptide Y - genetics</topic><topic>Neuropeptide Y - metabolism</topic><topic>Neuropeptides - genetics</topic><topic>Neuropeptides - metabolism</topic><topic>pro-opiomelanocortin</topic><topic>Pro-Opiomelanocortin - genetics</topic><topic>Pro-Opiomelanocortin - metabolism</topic><topic>Rats</topic><topic>Rats, Sprague-Dawley</topic><topic>RNA, Messenger - metabolism</topic><topic>Streptozocin</topic><topic>vagus nerve</topic><topic>Vagus Nerve - physiology</topic><topic>Vertebrates: endocrinology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Warne, J. P.</creatorcontrib><creatorcontrib>Horneman, H. F.</creatorcontrib><creatorcontrib>Akana, S. F.</creatorcontrib><creatorcontrib>Foster, M. T.</creatorcontrib><creatorcontrib>Dallman, M. F.</creatorcontrib><collection>Istex</collection><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><jtitle>Journal of neuroendocrinology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Warne, J. P.</au><au>Horneman, H. F.</au><au>Akana, S. F.</au><au>Foster, M. T.</au><au>Dallman, M. F.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Insulin and the Constituent Branches of the Hepatic Vagus Interact to Modulate Hypothalamic and Limbic Neuropeptide mRNA Expression Differentially</atitle><jtitle>Journal of neuroendocrinology</jtitle><addtitle>J Neuroendocrinol</addtitle><date>2008-09</date><risdate>2008</risdate><volume>20</volume><issue>9</issue><spage>1067</spage><epage>1077</epage><pages>1067-1077</pages><issn>0953-8194</issn><eissn>1365-2826</eissn><notes>ArticleID:JNE1766</notes><notes>istex:5CDB943E001E8AB73B7E76C570A7FCADD4DC162F</notes><notes>ark:/67375/WNG-L862TT8B-F</notes><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><abstract>Insulin and signalling through the vagus nerve act in concert to regulate metabolic homeostasis and ingestive behaviour. Our previous studies using streptozotocin (STZ)‐diabetic rats have shown that hepatic branch vagotomy (HV), gastroduodenal branch vagotomy (GV) and capsaicin treatment of the common hepatic branch that selectively destroys afferent fibres (CapV), all promote lard, but not total, caloric intake to levels similar to those achieved with insulin treatment. Because hypothalamic and limbic mRNA expression of neuropeptides linked to energy balance is altered by STZ‐diabetes and HV, we examined the role(s) of insulin and the common hepatic and gastroduodenal branches of the vagus nerve and hepatic afferent fibres in the regulation of these neuropeptides in rats with high, steady‐state corticosterone levels. STZ‐diabetic rats were prepared with osmotic minipumps containing either saline or insulin and were compared with nondiabetic counterparts: half of each group received a vagal manipulation, the other half were sham operated. Five days after surgery, rats were offered the choice of lard and chow to consume for another 5 days, when brains were collected and processed for in situ hybridisation. Paraventricular nucleus corticotrophin‐releasing factor (CRF) mRNA was elevated by STZ treatment, an effect prevented by either insulin treatment or GV. By contrast, CRF mRNA expression in the central nucleus of the amygdala and bed nuclei of the stria terminalis was unaffected by STZ treatment, but HV and CapV manipulations elevated expression in the nondiabetic, but not STZ‐diabetic groups. Arcuate nucleus neuropeptide Y, but not pro‐opiomelanocortin, mRNA expression was elevated by STZ treatment and all vagal manipulations; however, exogenous insulin treatment failed to prevent this, in keeping with their previously documented elevated caloric intake. These results strongly suggest that the gastroduodenal branch and hepatic branch proper, which merge to form the common hepatic branch, differentially interact with prevailing insulin levels to regulate hypothalamic and limbic neuropeptide mRNA expression.</abstract><cop>Oxford, UK</cop><pub>Blackwell Publishing Ltd</pub><pmid>18638024</pmid><doi>10.1111/j.1365-2826.2008.01766.x</doi><tpages>11</tpages></addata></record> |
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| subjects | Animals Biological and medical sciences Corticosterone - blood corticotrophin-releasing factor Corticotropin-Releasing Hormone - genetics Corticotropin-Releasing Hormone - metabolism Diabetes Mellitus, Experimental - blood Diabetes Mellitus, Experimental - genetics Diabetes Mellitus, Experimental - metabolism Fundamental and applied biological sciences. Psychology Gene Expression Regulation - drug effects glucocorticoids Hypothalamus - drug effects Hypothalamus - metabolism insulin Insulin - pharmacology Limbic System - drug effects Limbic System - metabolism Liver - drug effects Liver - innervation Male Models, Biological neuropeptide Y Neuropeptide Y - genetics Neuropeptide Y - metabolism Neuropeptides - genetics Neuropeptides - metabolism pro-opiomelanocortin Pro-Opiomelanocortin - genetics Pro-Opiomelanocortin - metabolism Rats Rats, Sprague-Dawley RNA, Messenger - metabolism Streptozocin vagus nerve Vagus Nerve - physiology Vertebrates: endocrinology |
| title | Insulin and the Constituent Branches of the Hepatic Vagus Interact to Modulate Hypothalamic and Limbic Neuropeptide mRNA Expression Differentially |
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