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Upregulation of Gene Expression in Reward-Modulatory Striatal Opioid Systems by Sleep Loss
Epidemiological studies have shown a link between sleep loss and the obesity 'epidemic,' and several observations indicate that sleep curtailment engenders positive energy balance via increased palatable-food 'snacking.' These effects suggest alterations in reward-modulatory brai...
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| Published in: | Neuropsychopharmacology (New York, N.Y.) N.Y.), 2013-12, Vol.38 (13), p.2578-2587 |
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| creator | BALDO, Brian A HANLON, Erin C OBERMEYER, William BREMER, Quentin PALETZ, Elliott BENCA, Ruth M |
| description | Epidemiological studies have shown a link between sleep loss and the obesity 'epidemic,' and several observations indicate that sleep curtailment engenders positive energy balance via increased palatable-food 'snacking.' These effects suggest alterations in reward-modulatory brain systems. We explored the effects of 10 days of sleep deprivation in rats on the expression of striatal opioid peptide (OP) genes that subserve food motivation and hedonic reward, and compared effects with those seen in hypothalamic energy balance-regulatory systems. Sleep-deprived (Sleep-Dep) rats were compared with yoked forced-locomotion apparatus controls (App-Controls), food-restricted rats (Food-Restrict), and unmanipulated controls (Home-Cage). Detection of mRNA levels with in situ hybridization revealed a subregion-specific upregulation of striatal preproenkephalin and prodynorhin gene expression in the Sleep-Dep group relative to all other groups. Neuropeptide Y (NPY) gene expression in the hippocampal dentate gyrus and throughout neocortex was also robustly upregulated selectively in the Sleep-Dep group. In contrast, parallel gene expression changes were observed in the Sleep-Dep and Food-Restrict groups in hypothalamic energy-sensing systems (arcuate nucleus NPY was upregulated, and cocaine- and amphetamine-regulated transcript was downregulated), in alignment with leptin suppression in both groups. Together, these results reveal a novel set of sleep deprivation-induced transcriptional changes in reward-modulatory peptide systems, which are dissociable from the energy-balance perturbations of sleep loss or the potentially stressful effects of the forced-locomotion procedure. The recruitment of telencephalic food-reward systems may provide a feeding drive highly resistant to feedback control, which could engender obesity through the enhancement of palatable feeding. |
| doi_str_mv | 10.1038/npp.2013.174 |
| format | article |
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These effects suggest alterations in reward-modulatory brain systems. We explored the effects of 10 days of sleep deprivation in rats on the expression of striatal opioid peptide (OP) genes that subserve food motivation and hedonic reward, and compared effects with those seen in hypothalamic energy balance-regulatory systems. Sleep-deprived (Sleep-Dep) rats were compared with yoked forced-locomotion apparatus controls (App-Controls), food-restricted rats (Food-Restrict), and unmanipulated controls (Home-Cage). Detection of mRNA levels with in situ hybridization revealed a subregion-specific upregulation of striatal preproenkephalin and prodynorhin gene expression in the Sleep-Dep group relative to all other groups. Neuropeptide Y (NPY) gene expression in the hippocampal dentate gyrus and throughout neocortex was also robustly upregulated selectively in the Sleep-Dep group. In contrast, parallel gene expression changes were observed in the Sleep-Dep and Food-Restrict groups in hypothalamic energy-sensing systems (arcuate nucleus NPY was upregulated, and cocaine- and amphetamine-regulated transcript was downregulated), in alignment with leptin suppression in both groups. Together, these results reveal a novel set of sleep deprivation-induced transcriptional changes in reward-modulatory peptide systems, which are dissociable from the energy-balance perturbations of sleep loss or the potentially stressful effects of the forced-locomotion procedure. The recruitment of telencephalic food-reward systems may provide a feeding drive highly resistant to feedback control, which could engender obesity through the enhancement of palatable feeding.</description><identifier>ISSN: 0893-133X</identifier><identifier>EISSN: 1740-634X</identifier><identifier>DOI: 10.1038/npp.2013.174</identifier><identifier>PMID: 23864029</identifier><identifier>CODEN: NEROEW</identifier><language>eng</language><publisher>Basingstoke: Nature Publishing Group</publisher><subject>Animals ; Biological and medical sciences ; Body Weight ; Eating ; Energy ; Enkephalins - genetics ; Enkephalins - metabolism ; Fasting - physiology ; Food ; Gene expression ; Insulin - blood ; Leptin - blood ; Male ; Medical sciences ; Medicine ; Metabolism ; Narcotics ; Neostriatum - metabolism ; Nerve Tissue Proteins - genetics ; Nerve Tissue Proteins - metabolism ; Neuroimaging ; Neuropeptide Y - genetics ; Neuropeptide Y - metabolism ; Obesity ; Opioid Peptides - genetics ; Opioid Peptides - metabolism ; Original ; Peptides ; Protein Precursors - genetics ; Protein Precursors - metabolism ; Public health ; Rats ; Rats, Sprague-Dawley ; Research parks ; Reward ; Rodents ; Sleep deprivation ; Sleep Deprivation - pathology ; Up-Regulation - physiology ; Weight control</subject><ispartof>Neuropsychopharmacology (New York, N.Y.), 2013-12, Vol.38 (13), p.2578-2587</ispartof><rights>2015 INIST-CNRS</rights><rights>Copyright Nature Publishing Group Dec 2013</rights><rights>Copyright © 2013 American College of Neuropsychopharmacology 2013 American College of Neuropsychopharmacology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c475t-8ef8ce13cdb8e44b5c883e247cfd1a4bbefd33abf1f21352f0d6f7ef824d19d33</citedby><cites>FETCH-LOGICAL-c475t-8ef8ce13cdb8e44b5c883e247cfd1a4bbefd33abf1f21352f0d6f7ef824d19d33</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/PMC3828536/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3828536/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,315,730,783,787,888,27936,27937,53804,53806</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=28010430$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23864029$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>BALDO, Brian A</creatorcontrib><creatorcontrib>HANLON, Erin C</creatorcontrib><creatorcontrib>OBERMEYER, William</creatorcontrib><creatorcontrib>BREMER, Quentin</creatorcontrib><creatorcontrib>PALETZ, Elliott</creatorcontrib><creatorcontrib>BENCA, Ruth M</creatorcontrib><title>Upregulation of Gene Expression in Reward-Modulatory Striatal Opioid Systems by Sleep Loss</title><title>Neuropsychopharmacology (New York, N.Y.)</title><addtitle>Neuropsychopharmacology</addtitle><description>Epidemiological studies have shown a link between sleep loss and the obesity 'epidemic,' and several observations indicate that sleep curtailment engenders positive energy balance via increased palatable-food 'snacking.' These effects suggest alterations in reward-modulatory brain systems. We explored the effects of 10 days of sleep deprivation in rats on the expression of striatal opioid peptide (OP) genes that subserve food motivation and hedonic reward, and compared effects with those seen in hypothalamic energy balance-regulatory systems. Sleep-deprived (Sleep-Dep) rats were compared with yoked forced-locomotion apparatus controls (App-Controls), food-restricted rats (Food-Restrict), and unmanipulated controls (Home-Cage). Detection of mRNA levels with in situ hybridization revealed a subregion-specific upregulation of striatal preproenkephalin and prodynorhin gene expression in the Sleep-Dep group relative to all other groups. Neuropeptide Y (NPY) gene expression in the hippocampal dentate gyrus and throughout neocortex was also robustly upregulated selectively in the Sleep-Dep group. In contrast, parallel gene expression changes were observed in the Sleep-Dep and Food-Restrict groups in hypothalamic energy-sensing systems (arcuate nucleus NPY was upregulated, and cocaine- and amphetamine-regulated transcript was downregulated), in alignment with leptin suppression in both groups. Together, these results reveal a novel set of sleep deprivation-induced transcriptional changes in reward-modulatory peptide systems, which are dissociable from the energy-balance perturbations of sleep loss or the potentially stressful effects of the forced-locomotion procedure. 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genetics</topic><topic>Enkephalins - metabolism</topic><topic>Fasting - physiology</topic><topic>Food</topic><topic>Gene expression</topic><topic>Insulin - blood</topic><topic>Leptin - blood</topic><topic>Male</topic><topic>Medical sciences</topic><topic>Medicine</topic><topic>Metabolism</topic><topic>Narcotics</topic><topic>Neostriatum - metabolism</topic><topic>Nerve Tissue Proteins - genetics</topic><topic>Nerve Tissue Proteins - metabolism</topic><topic>Neuroimaging</topic><topic>Neuropeptide Y - genetics</topic><topic>Neuropeptide Y - metabolism</topic><topic>Obesity</topic><topic>Opioid Peptides - genetics</topic><topic>Opioid Peptides - metabolism</topic><topic>Original</topic><topic>Peptides</topic><topic>Protein Precursors - genetics</topic><topic>Protein Precursors - metabolism</topic><topic>Public health</topic><topic>Rats</topic><topic>Rats, Sprague-Dawley</topic><topic>Research parks</topic><topic>Reward</topic><topic>Rodents</topic><topic>Sleep deprivation</topic><topic>Sleep Deprivation - pathology</topic><topic>Up-Regulation - physiology</topic><topic>Weight control</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>BALDO, Brian A</creatorcontrib><creatorcontrib>HANLON, Erin C</creatorcontrib><creatorcontrib>OBERMEYER, William</creatorcontrib><creatorcontrib>BREMER, Quentin</creatorcontrib><creatorcontrib>PALETZ, Elliott</creatorcontrib><creatorcontrib>BENCA, Ruth 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>ProQuest Central (Corporate)</collection><collection>Neurosciences Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Psychology Database (Alumni)</collection><collection>ProQuest Pharma Collection</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)</collection><collection>ProQuest Central</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>PML(ProQuest Medical Library)</collection><collection>Psychology Database</collection><collection>Biological Science 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 One Psychology</collection><collection>ProQuest Central Basic</collection><collection>MEDLINE - Academic</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Neuropsychopharmacology (New York, N.Y.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>BALDO, Brian A</au><au>HANLON, Erin C</au><au>OBERMEYER, William</au><au>BREMER, Quentin</au><au>PALETZ, Elliott</au><au>BENCA, Ruth M</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Upregulation of Gene Expression in Reward-Modulatory Striatal Opioid Systems by Sleep Loss</atitle><jtitle>Neuropsychopharmacology (New York, N.Y.)</jtitle><addtitle>Neuropsychopharmacology</addtitle><date>2013-12-01</date><risdate>2013</risdate><volume>38</volume><issue>13</issue><spage>2578</spage><epage>2587</epage><pages>2578-2587</pages><issn>0893-133X</issn><eissn>1740-634X</eissn><coden>NEROEW</coden><abstract>Epidemiological studies have shown a link between sleep loss and the obesity 'epidemic,' and several observations indicate that sleep curtailment engenders positive energy balance via increased palatable-food 'snacking.' These effects suggest alterations in reward-modulatory brain systems. We explored the effects of 10 days of sleep deprivation in rats on the expression of striatal opioid peptide (OP) genes that subserve food motivation and hedonic reward, and compared effects with those seen in hypothalamic energy balance-regulatory systems. Sleep-deprived (Sleep-Dep) rats were compared with yoked forced-locomotion apparatus controls (App-Controls), food-restricted rats (Food-Restrict), and unmanipulated controls (Home-Cage). Detection of mRNA levels with in situ hybridization revealed a subregion-specific upregulation of striatal preproenkephalin and prodynorhin gene expression in the Sleep-Dep group relative to all other groups. Neuropeptide Y (NPY) gene expression in the hippocampal dentate gyrus and throughout neocortex was also robustly upregulated selectively in the Sleep-Dep group. In contrast, parallel gene expression changes were observed in the Sleep-Dep and Food-Restrict groups in hypothalamic energy-sensing systems (arcuate nucleus NPY was upregulated, and cocaine- and amphetamine-regulated transcript was downregulated), in alignment with leptin suppression in both groups. Together, these results reveal a novel set of sleep deprivation-induced transcriptional changes in reward-modulatory peptide systems, which are dissociable from the energy-balance perturbations of sleep loss or the potentially stressful effects of the forced-locomotion procedure. The recruitment of telencephalic food-reward systems may provide a feeding drive highly resistant to feedback control, which could engender obesity through the enhancement of palatable feeding.</abstract><cop>Basingstoke</cop><pub>Nature Publishing Group</pub><pmid>23864029</pmid><doi>10.1038/npp.2013.174</doi><tpages>10</tpages><oa>free_for_read</oa></addata></record> |
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| source | PubMed Central |
| subjects | Animals Biological and medical sciences Body Weight Eating Energy Enkephalins - genetics Enkephalins - metabolism Fasting - physiology Food Gene expression Insulin - blood Leptin - blood Male Medical sciences Medicine Metabolism Narcotics Neostriatum - metabolism Nerve Tissue Proteins - genetics Nerve Tissue Proteins - metabolism Neuroimaging Neuropeptide Y - genetics Neuropeptide Y - metabolism Obesity Opioid Peptides - genetics Opioid Peptides - metabolism Original Peptides Protein Precursors - genetics Protein Precursors - metabolism Public health Rats Rats, Sprague-Dawley Research parks Reward Rodents Sleep deprivation Sleep Deprivation - pathology Up-Regulation - physiology Weight control |
| title | Upregulation of Gene Expression in Reward-Modulatory Striatal Opioid Systems by Sleep Loss |
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