Daily Rhythms in Metabolic Liver Enzymes and Plasma Glucose Require a Balance in the Autonomic Output to the Liver
Daily variations in plasma glucose concentrations are controlled by the biological clock, located in the suprachiasmatic nucleus. Our previous studies indicated an important role for the sympathetic innervation of the liver in the generation of the daily glucose rhythm. In the present study, we inve...
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description | Daily variations in plasma glucose concentrations are controlled by the biological clock, located in the suprachiasmatic nucleus. Our previous studies indicated an important role for the sympathetic innervation of the liver in the generation of the daily glucose rhythm. In the present study, we investigated further the role of the autonomic nervous system (ANS) in the genesis of the plasma glucose rhythm. First, we showed that complete removal of the autonomic inputs to the liver did not impair the plasma glucose rhythm or the daily expression of the glucoregulatory enzymes in the liver. Consequently, we studied whether the daily glucose rhythm is driven by the daily feeding activity in denervated animals. Surprisingly, complete denervation combined with a noncircadian feeding schedule also did not abolish the 24-h profile in plasma glucose or all daily rhythms in the gene expression of liver enzymes. These results demonstrate that the mechanisms used by the suprachiasmatic nucleus to control the rhythmic expression of glucose-metabolizing enzymes and the 24-h rhythm in plasma glucose concentrations are highly versatile and the glucose rhythm can be maintained in absence of hepatic ANS input and/or a day/night rhythm in feeding activity. Interestingly, a hepatic sympathectomy or parasympathectomy did abolish the plasma glucose rhythm, demonstrating that a unilateral denervation of the liver is more deleterious to maintaining the rhythmic liver metabolism than a complete removal of both branches. This observation supports the notion that an unbalanced ANS in obesity and diabetes accounts for the disturbed glucose balance in these disorders. |
doi_str_mv | 10.1210/en.2007-0816 |
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Our previous studies indicated an important role for the sympathetic innervation of the liver in the generation of the daily glucose rhythm. In the present study, we investigated further the role of the autonomic nervous system (ANS) in the genesis of the plasma glucose rhythm. First, we showed that complete removal of the autonomic inputs to the liver did not impair the plasma glucose rhythm or the daily expression of the glucoregulatory enzymes in the liver. Consequently, we studied whether the daily glucose rhythm is driven by the daily feeding activity in denervated animals. Surprisingly, complete denervation combined with a noncircadian feeding schedule also did not abolish the 24-h profile in plasma glucose or all daily rhythms in the gene expression of liver enzymes. These results demonstrate that the mechanisms used by the suprachiasmatic nucleus to control the rhythmic expression of glucose-metabolizing enzymes and the 24-h rhythm in plasma glucose concentrations are highly versatile and the glucose rhythm can be maintained in absence of hepatic ANS input and/or a day/night rhythm in feeding activity. Interestingly, a hepatic sympathectomy or parasympathectomy did abolish the plasma glucose rhythm, demonstrating that a unilateral denervation of the liver is more deleterious to maintaining the rhythmic liver metabolism than a complete removal of both branches. This observation supports the notion that an unbalanced ANS in obesity and diabetes accounts for the disturbed glucose balance in these disorders.</description><identifier>ISSN: 0013-7227</identifier><identifier>EISSN: 1945-7170</identifier><identifier>DOI: 10.1210/en.2007-0816</identifier><identifier>PMID: 18162516</identifier><identifier>CODEN: ENDOAO</identifier><language>eng</language><publisher>Bethesda, MD: Endocrine Society</publisher><subject>Animals ; Autonomic nervous system ; Autonomic Nervous System - physiology ; Biodiversity ; Biodiversity and Ecology ; Biological and medical sciences ; Biological clocks ; Blood Glucose - analysis ; Circadian Rhythm - physiology ; Corticosterone - blood ; Denervation ; Diabetes mellitus ; Environmental Sciences ; Enzymes ; Feeding ; Fundamental and applied biological sciences. Psychology ; Gene expression ; Glucose ; Glucose - metabolism ; Innervation ; Insulin - blood ; Life Sciences ; Liver ; Liver - enzymology ; Liver - innervation ; Liver diseases ; Liver Glycogen - analysis ; Male ; Plasma ; Populations and Evolution ; Rats ; Rats, Wistar ; Rhythm ; Rhythms ; RNA, Messenger - analysis ; Suprachiasmatic nucleus ; Suprachiasmatic Nucleus - physiology ; Sympathetic nervous system ; Vertebrates: endocrinology</subject><ispartof>Endocrinology (Philadelphia), 2008-04, Vol.149 (4), p.1914-1925</ispartof><rights>Copyright © 2008 by the Endocrine Society 2008</rights><rights>2008 INIST-CNRS</rights><rights>Copyright © 2008 by the Endocrine Society</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c592t-a45c168c87e3aaa33131922d14a6261ae64ae5561620c93d843a7c9e6d929da3</citedby><orcidid>0000-0001-9606-8453 ; 0000-0002-6881-6546</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=20193227$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/18162516$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-00202153$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Cailotto, Cathy</creatorcontrib><creatorcontrib>van Heijningen, Caroline</creatorcontrib><creatorcontrib>van der Vliet, Jan</creatorcontrib><creatorcontrib>van der Plasse, Geoffrey</creatorcontrib><creatorcontrib>Habold, Caroline</creatorcontrib><creatorcontrib>Kalsbeek, Andries</creatorcontrib><creatorcontrib>Pévet, Paul</creatorcontrib><creatorcontrib>Buijs, Ruud M</creatorcontrib><title>Daily Rhythms in Metabolic Liver Enzymes and Plasma Glucose Require a Balance in the Autonomic Output to the Liver</title><title>Endocrinology (Philadelphia)</title><addtitle>Endocrinology</addtitle><description>Daily variations in plasma glucose concentrations are controlled by the biological clock, located in the suprachiasmatic nucleus. Our previous studies indicated an important role for the sympathetic innervation of the liver in the generation of the daily glucose rhythm. In the present study, we investigated further the role of the autonomic nervous system (ANS) in the genesis of the plasma glucose rhythm. First, we showed that complete removal of the autonomic inputs to the liver did not impair the plasma glucose rhythm or the daily expression of the glucoregulatory enzymes in the liver. Consequently, we studied whether the daily glucose rhythm is driven by the daily feeding activity in denervated animals. Surprisingly, complete denervation combined with a noncircadian feeding schedule also did not abolish the 24-h profile in plasma glucose or all daily rhythms in the gene expression of liver enzymes. These results demonstrate that the mechanisms used by the suprachiasmatic nucleus to control the rhythmic expression of glucose-metabolizing enzymes and the 24-h rhythm in plasma glucose concentrations are highly versatile and the glucose rhythm can be maintained in absence of hepatic ANS input and/or a day/night rhythm in feeding activity. Interestingly, a hepatic sympathectomy or parasympathectomy did abolish the plasma glucose rhythm, demonstrating that a unilateral denervation of the liver is more deleterious to maintaining the rhythmic liver metabolism than a complete removal of both branches. This observation supports the notion that an unbalanced ANS in obesity and diabetes accounts for the disturbed glucose balance in these disorders.</description><subject>Animals</subject><subject>Autonomic nervous system</subject><subject>Autonomic Nervous System - physiology</subject><subject>Biodiversity</subject><subject>Biodiversity and Ecology</subject><subject>Biological and medical sciences</subject><subject>Biological clocks</subject><subject>Blood Glucose - analysis</subject><subject>Circadian Rhythm - physiology</subject><subject>Corticosterone - blood</subject><subject>Denervation</subject><subject>Diabetes mellitus</subject><subject>Environmental Sciences</subject><subject>Enzymes</subject><subject>Feeding</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Gene expression</subject><subject>Glucose</subject><subject>Glucose - metabolism</subject><subject>Innervation</subject><subject>Insulin - blood</subject><subject>Life Sciences</subject><subject>Liver</subject><subject>Liver - enzymology</subject><subject>Liver - innervation</subject><subject>Liver diseases</subject><subject>Liver Glycogen - analysis</subject><subject>Male</subject><subject>Plasma</subject><subject>Populations and Evolution</subject><subject>Rats</subject><subject>Rats, Wistar</subject><subject>Rhythm</subject><subject>Rhythms</subject><subject>RNA, Messenger - analysis</subject><subject>Suprachiasmatic nucleus</subject><subject>Suprachiasmatic Nucleus - physiology</subject><subject>Sympathetic nervous system</subject><subject>Vertebrates: endocrinology</subject><issn>0013-7227</issn><issn>1945-7170</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2008</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFklFrFDEUhYModlt981kCoiI4NTeZTHYe11pbYaVS-h5uM3fZKTOTbTJTWH99M52hBVF8Crl8OeceThh7A-IYJIgv1B1LIUwmllA8Ywsoc50ZMOI5WwgBKjNSmgN2GONNuuZ5rl6yA0is1FAsWPiGdbPnl9t9v20jrzv-k3q89k3t-Lq-o8BPu9_7liLHruK_Gowt8rNmcD4Sv6TboQ7EkX_FBjtH4_t-S3w19L7zbdK4GPrd0PPeP8wfFF-xFxtsIr2ezyN29f306uQ8W1-c_ThZrTOnS9lnmGsHxdItDSlEVAoUlFJWkGMhC0AqciSti5REuFJVy1yhcSUVVSnLCtUR-zTJbrGxu1C3GPbWY23PV2s7zoSQQoJWd5DYDxO7C_52oNjbto6OmhSK_BCtETmYotD_BaXQBsCUCXz3B3jjh9ClvDYFEboEoUffzxPlgo8x0OZxURB2bNdSZ8d27dhuwt_OosN1S9UTPNeZgPczgNFhswmplDo-clJAqdJ3SNzHifPD7l-W2WypJpK6yrtQd7QLFONTmr8ueg-w4san</recordid><startdate>20080401</startdate><enddate>20080401</enddate><creator>Cailotto, Cathy</creator><creator>van Heijningen, Caroline</creator><creator>van der Vliet, Jan</creator><creator>van der Plasse, Geoffrey</creator><creator>Habold, Caroline</creator><creator>Kalsbeek, Andries</creator><creator>Pévet, Paul</creator><creator>Buijs, Ruud M</creator><general>Endocrine Society</general><general>Oxford University Press</general><scope>IQODW</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>7QG</scope><scope>7QP</scope><scope>7QR</scope><scope>7T5</scope><scope>7TM</scope><scope>7TO</scope><scope>7U7</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>K9.</scope><scope>P64</scope><scope>7TK</scope><scope>7X8</scope><scope>1XC</scope><orcidid>https://orcid.org/0000-0001-9606-8453</orcidid><orcidid>https://orcid.org/0000-0002-6881-6546</orcidid></search><sort><creationdate>20080401</creationdate><title>Daily Rhythms in Metabolic Liver Enzymes and Plasma Glucose Require a Balance in the Autonomic Output to the Liver</title><author>Cailotto, Cathy ; van Heijningen, Caroline ; van der Vliet, Jan ; van der Plasse, Geoffrey ; Habold, Caroline ; Kalsbeek, Andries ; Pévet, Paul ; Buijs, Ruud M</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c592t-a45c168c87e3aaa33131922d14a6261ae64ae5561620c93d843a7c9e6d929da3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2008</creationdate><topic>Animals</topic><topic>Autonomic nervous system</topic><topic>Autonomic Nervous System - physiology</topic><topic>Biodiversity</topic><topic>Biodiversity and Ecology</topic><topic>Biological and medical sciences</topic><topic>Biological clocks</topic><topic>Blood Glucose - analysis</topic><topic>Circadian Rhythm - physiology</topic><topic>Corticosterone - blood</topic><topic>Denervation</topic><topic>Diabetes mellitus</topic><topic>Environmental Sciences</topic><topic>Enzymes</topic><topic>Feeding</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Gene expression</topic><topic>Glucose</topic><topic>Glucose - metabolism</topic><topic>Innervation</topic><topic>Insulin - blood</topic><topic>Life Sciences</topic><topic>Liver</topic><topic>Liver - enzymology</topic><topic>Liver - innervation</topic><topic>Liver diseases</topic><topic>Liver Glycogen - analysis</topic><topic>Male</topic><topic>Plasma</topic><topic>Populations and Evolution</topic><topic>Rats</topic><topic>Rats, Wistar</topic><topic>Rhythm</topic><topic>Rhythms</topic><topic>RNA, Messenger - analysis</topic><topic>Suprachiasmatic nucleus</topic><topic>Suprachiasmatic Nucleus - physiology</topic><topic>Sympathetic nervous system</topic><topic>Vertebrates: endocrinology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Cailotto, Cathy</creatorcontrib><creatorcontrib>van Heijningen, Caroline</creatorcontrib><creatorcontrib>van der Vliet, Jan</creatorcontrib><creatorcontrib>van der Plasse, Geoffrey</creatorcontrib><creatorcontrib>Habold, Caroline</creatorcontrib><creatorcontrib>Kalsbeek, Andries</creatorcontrib><creatorcontrib>Pévet, Paul</creatorcontrib><creatorcontrib>Buijs, Ruud M</creatorcontrib><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>Animal Behavior Abstracts</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Immunology Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Toxicology 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>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><jtitle>Endocrinology (Philadelphia)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Cailotto, Cathy</au><au>van Heijningen, Caroline</au><au>van der Vliet, Jan</au><au>van der Plasse, Geoffrey</au><au>Habold, Caroline</au><au>Kalsbeek, Andries</au><au>Pévet, Paul</au><au>Buijs, Ruud M</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Daily Rhythms in Metabolic Liver Enzymes and Plasma Glucose Require a Balance in the Autonomic Output to the Liver</atitle><jtitle>Endocrinology (Philadelphia)</jtitle><addtitle>Endocrinology</addtitle><date>2008-04-01</date><risdate>2008</risdate><volume>149</volume><issue>4</issue><spage>1914</spage><epage>1925</epage><pages>1914-1925</pages><issn>0013-7227</issn><eissn>1945-7170</eissn><coden>ENDOAO</coden><abstract>Daily variations in plasma glucose concentrations are controlled by the biological clock, located in the suprachiasmatic nucleus. Our previous studies indicated an important role for the sympathetic innervation of the liver in the generation of the daily glucose rhythm. In the present study, we investigated further the role of the autonomic nervous system (ANS) in the genesis of the plasma glucose rhythm. First, we showed that complete removal of the autonomic inputs to the liver did not impair the plasma glucose rhythm or the daily expression of the glucoregulatory enzymes in the liver. Consequently, we studied whether the daily glucose rhythm is driven by the daily feeding activity in denervated animals. Surprisingly, complete denervation combined with a noncircadian feeding schedule also did not abolish the 24-h profile in plasma glucose or all daily rhythms in the gene expression of liver enzymes. These results demonstrate that the mechanisms used by the suprachiasmatic nucleus to control the rhythmic expression of glucose-metabolizing enzymes and the 24-h rhythm in plasma glucose concentrations are highly versatile and the glucose rhythm can be maintained in absence of hepatic ANS input and/or a day/night rhythm in feeding activity. Interestingly, a hepatic sympathectomy or parasympathectomy did abolish the plasma glucose rhythm, demonstrating that a unilateral denervation of the liver is more deleterious to maintaining the rhythmic liver metabolism than a complete removal of both branches. This observation supports the notion that an unbalanced ANS in obesity and diabetes accounts for the disturbed glucose balance in these disorders.</abstract><cop>Bethesda, MD</cop><pub>Endocrine Society</pub><pmid>18162516</pmid><doi>10.1210/en.2007-0816</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0001-9606-8453</orcidid><orcidid>https://orcid.org/0000-0002-6881-6546</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Autonomic nervous system Autonomic Nervous System - physiology Biodiversity Biodiversity and Ecology Biological and medical sciences Biological clocks Blood Glucose - analysis Circadian Rhythm - physiology Corticosterone - blood Denervation Diabetes mellitus Environmental Sciences Enzymes Feeding Fundamental and applied biological sciences. Psychology Gene expression Glucose Glucose - metabolism Innervation Insulin - blood Life Sciences Liver Liver - enzymology Liver - innervation Liver diseases Liver Glycogen - analysis Male Plasma Populations and Evolution Rats Rats, Wistar Rhythm Rhythms RNA, Messenger - analysis Suprachiasmatic nucleus Suprachiasmatic Nucleus - physiology Sympathetic nervous system Vertebrates: endocrinology |
title | Daily Rhythms in Metabolic Liver Enzymes and Plasma Glucose Require a Balance in the Autonomic Output to the Liver |
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