Reshaping circadian metabolism in the suprachiasmatic nucleus and prefrontal cortex by nutritional challenge
Food is a powerful entrainment cue for circadian clocks in peripheral tissues, and changes in the composition of nutrients have been demonstrated to metabolically reprogram peripheral clocks. However, how food challenges may influence circadian metabolism of the master clock in the suprachiasmatic n...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2020-11, Vol.117 (47), p.29904-29913 |
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| creator | Tognini, Paola Samad, Muntaha Kinouchi, Kenichiro Liu, Yu Helbling, Jean-Christophe Moisan, Marie-Pierre Eckel-Mahan, Kristin L. Baldi, Pierre Sassone-Corsi, Paolo |
| description | Food is a powerful entrainment cue for circadian clocks in peripheral tissues, and changes in the composition of nutrients have been demonstrated to metabolically reprogram peripheral clocks. However, how food challenges may influence circadian metabolism of the master clock in the suprachiasmatic nucleus (SCN) or in other brain areas is poorly understood. Using high-throughput metabolomics, we studied the circadian metabolome profiles of the SCN and medial prefrontal cortex (mPFC) in lean mice compared with mice challenged with a high-fat diet (HFD). Both the mPFC and the SCN displayed a robust cyclic metabolism, with a strikingly high sensitivity to HFD perturbation in an area-specific manner. The phase and amplitude of oscillations were drastically different between the SCN and mPFC, and the metabolic pathways impacted by HFD were remarkably region-dependent. Furthermore, HFD induced a significant increase in the number of cycling metabolites exclusively in the SCN, revealing an unsuspected susceptibility of the master clock to food stress. |
| doi_str_mv | 10.1073/pnas.2016589117 |
| format | Article |
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However, how food challenges may influence circadian metabolism of the master clock in the suprachiasmatic nucleus (SCN) or in other brain areas is poorly understood. Using high-throughput metabolomics, we studied the circadian metabolome profiles of the SCN and medial prefrontal cortex (mPFC) in lean mice compared with mice challenged with a high-fat diet (HFD). Both the mPFC and the SCN displayed a robust cyclic metabolism, with a strikingly high sensitivity to HFD perturbation in an area-specific manner. The phase and amplitude of oscillations were drastically different between the SCN and mPFC, and the metabolic pathways impacted by HFD were remarkably region-dependent. Furthermore, HFD induced a significant increase in the number of cycling metabolites exclusively in the SCN, revealing an unsuspected susceptibility of the master clock to food stress.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.2016589117</identifier><identifier>PMID: 33172990</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Animals ; Biological clocks ; Biological Sciences ; Circadian Clocks - physiology ; Circadian rhythm ; Circadian rhythms ; Diet, High-Fat - adverse effects ; Entrainment ; Food ; High fat diet ; Life Sciences ; Male ; Metabolic pathways ; Metabolism ; Metabolites ; Metabolome - physiology ; Metabolomics ; Mice ; Models, Animal ; Nutrients ; Oscillations ; Perturbation ; Photoperiod ; Prefrontal cortex ; Prefrontal Cortex - metabolism ; Suprachiasmatic nucleus ; Suprachiasmatic Nucleus - metabolism</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2020-11, Vol.117 (47), p.29904-29913</ispartof><rights>Copyright National Academy of Sciences Nov 24, 2020</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>2020</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c543t-d53330dc875dd772f6077cc4c7c795a2443b8e1334d11350ece517da47a4151d3</citedby><cites>FETCH-LOGICAL-c543t-d53330dc875dd772f6077cc4c7c795a2443b8e1334d11350ece517da47a4151d3</cites><orcidid>0000-0001-7407-0114 ; 0000-0001-8752-4664 ; 0000-0001-7315-5319</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26970844$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26970844$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,724,777,781,800,882,27905,27906,53772,53774,57998,58231</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33172990$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.inrae.fr/hal-03173039$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Tognini, Paola</creatorcontrib><creatorcontrib>Samad, Muntaha</creatorcontrib><creatorcontrib>Kinouchi, Kenichiro</creatorcontrib><creatorcontrib>Liu, Yu</creatorcontrib><creatorcontrib>Helbling, Jean-Christophe</creatorcontrib><creatorcontrib>Moisan, Marie-Pierre</creatorcontrib><creatorcontrib>Eckel-Mahan, Kristin L.</creatorcontrib><creatorcontrib>Baldi, Pierre</creatorcontrib><creatorcontrib>Sassone-Corsi, Paolo</creatorcontrib><title>Reshaping circadian metabolism in the suprachiasmatic nucleus and prefrontal cortex by nutritional challenge</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Food is a powerful entrainment cue for circadian clocks in peripheral tissues, and changes in the composition of nutrients have been demonstrated to metabolically reprogram peripheral clocks. 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Furthermore, HFD induced a significant increase in the number of cycling metabolites exclusively in the SCN, revealing an unsuspected susceptibility of the master clock to food stress.</description><subject>Animals</subject><subject>Biological clocks</subject><subject>Biological Sciences</subject><subject>Circadian Clocks - physiology</subject><subject>Circadian rhythm</subject><subject>Circadian rhythms</subject><subject>Diet, High-Fat - adverse effects</subject><subject>Entrainment</subject><subject>Food</subject><subject>High fat diet</subject><subject>Life Sciences</subject><subject>Male</subject><subject>Metabolic pathways</subject><subject>Metabolism</subject><subject>Metabolites</subject><subject>Metabolome - physiology</subject><subject>Metabolomics</subject><subject>Mice</subject><subject>Models, Animal</subject><subject>Nutrients</subject><subject>Oscillations</subject><subject>Perturbation</subject><subject>Photoperiod</subject><subject>Prefrontal cortex</subject><subject>Prefrontal Cortex - metabolism</subject><subject>Suprachiasmatic nucleus</subject><subject>Suprachiasmatic Nucleus - metabolism</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkc2LFDEQxYMo7rh69qQEvOhhditfne7LwrKoKwwIoueQSWemM6STNkkv7n9vmllH3VNB1a9eJe8h9JrABQHJLqeg8wUF0oi2I0Q-QSsCHVk3vIOnaAVA5brllJ-hFzkfAKATLTxHZ4wRSbsOVsh_s3nQkwt7bFwyunc64NEWvY3e5RG7gMtgcZ6npM3gdB51cQaH2Xg7Z6xDj6dkdymGoj02MRX7C2_vK1CSKy6GpTto723Y25fo2U77bF891HP049PH7ze3683Xz19urjdrIzgr614wxqA3rRR9LyXdNSClMdxIIzuhKeds21rCGO8JYQKssYLIXnOpORGkZ-fo6qg7zdvR9saGkrRXU3KjTvcqaqf-nwQ3qH28U1ICa6ioAh-OAsOjtdvrjVp6UA1kwLo7Utn3D8dS_DnbXNTosrHe62DjnBXlomtowxuo6LtH6CHOqVq0UA1vF4hW6vJImRRzruaeXkBALamrJXX1N_W68fbf_574PzFX4M0ROOQS02lOm05CW-38DYn4s54</recordid><startdate>20201124</startdate><enddate>20201124</enddate><creator>Tognini, Paola</creator><creator>Samad, Muntaha</creator><creator>Kinouchi, Kenichiro</creator><creator>Liu, Yu</creator><creator>Helbling, Jean-Christophe</creator><creator>Moisan, Marie-Pierre</creator><creator>Eckel-Mahan, Kristin L.</creator><creator>Baldi, Pierre</creator><creator>Sassone-Corsi, Paolo</creator><general>National Academy of Sciences</general><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>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>1XC</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-7407-0114</orcidid><orcidid>https://orcid.org/0000-0001-8752-4664</orcidid><orcidid>https://orcid.org/0000-0001-7315-5319</orcidid></search><sort><creationdate>20201124</creationdate><title>Reshaping circadian metabolism in the suprachiasmatic nucleus and prefrontal cortex by nutritional challenge</title><author>Tognini, Paola ; Samad, Muntaha ; Kinouchi, Kenichiro ; Liu, Yu ; Helbling, Jean-Christophe ; Moisan, Marie-Pierre ; Eckel-Mahan, Kristin L. ; Baldi, Pierre ; Sassone-Corsi, Paolo</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c543t-d53330dc875dd772f6077cc4c7c795a2443b8e1334d11350ece517da47a4151d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Animals</topic><topic>Biological clocks</topic><topic>Biological Sciences</topic><topic>Circadian Clocks - physiology</topic><topic>Circadian rhythm</topic><topic>Circadian rhythms</topic><topic>Diet, High-Fat - adverse effects</topic><topic>Entrainment</topic><topic>Food</topic><topic>High fat diet</topic><topic>Life Sciences</topic><topic>Male</topic><topic>Metabolic pathways</topic><topic>Metabolism</topic><topic>Metabolites</topic><topic>Metabolome - physiology</topic><topic>Metabolomics</topic><topic>Mice</topic><topic>Models, Animal</topic><topic>Nutrients</topic><topic>Oscillations</topic><topic>Perturbation</topic><topic>Photoperiod</topic><topic>Prefrontal cortex</topic><topic>Prefrontal Cortex - metabolism</topic><topic>Suprachiasmatic nucleus</topic><topic>Suprachiasmatic Nucleus - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Tognini, Paola</creatorcontrib><creatorcontrib>Samad, Muntaha</creatorcontrib><creatorcontrib>Kinouchi, Kenichiro</creatorcontrib><creatorcontrib>Liu, Yu</creatorcontrib><creatorcontrib>Helbling, Jean-Christophe</creatorcontrib><creatorcontrib>Moisan, Marie-Pierre</creatorcontrib><creatorcontrib>Eckel-Mahan, Kristin L.</creatorcontrib><creatorcontrib>Baldi, Pierre</creatorcontrib><creatorcontrib>Sassone-Corsi, Paolo</creatorcontrib><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>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS 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>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Tognini, Paola</au><au>Samad, Muntaha</au><au>Kinouchi, Kenichiro</au><au>Liu, Yu</au><au>Helbling, Jean-Christophe</au><au>Moisan, Marie-Pierre</au><au>Eckel-Mahan, Kristin L.</au><au>Baldi, Pierre</au><au>Sassone-Corsi, Paolo</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Reshaping circadian metabolism in the suprachiasmatic nucleus and prefrontal cortex by nutritional challenge</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2020-11-24</date><risdate>2020</risdate><volume>117</volume><issue>47</issue><spage>29904</spage><epage>29913</epage><pages>29904-29913</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>Food is a powerful entrainment cue for circadian clocks in peripheral tissues, and changes in the composition of nutrients have been demonstrated to metabolically reprogram peripheral clocks. However, how food challenges may influence circadian metabolism of the master clock in the suprachiasmatic nucleus (SCN) or in other brain areas is poorly understood. Using high-throughput metabolomics, we studied the circadian metabolome profiles of the SCN and medial prefrontal cortex (mPFC) in lean mice compared with mice challenged with a high-fat diet (HFD). Both the mPFC and the SCN displayed a robust cyclic metabolism, with a strikingly high sensitivity to HFD perturbation in an area-specific manner. The phase and amplitude of oscillations were drastically different between the SCN and mPFC, and the metabolic pathways impacted by HFD were remarkably region-dependent. Furthermore, HFD induced a significant increase in the number of cycling metabolites exclusively in the SCN, revealing an unsuspected susceptibility of the master clock to food stress.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>33172990</pmid><doi>10.1073/pnas.2016589117</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0001-7407-0114</orcidid><orcidid>https://orcid.org/0000-0001-8752-4664</orcidid><orcidid>https://orcid.org/0000-0001-7315-5319</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Biological clocks Biological Sciences Circadian Clocks - physiology Circadian rhythm Circadian rhythms Diet, High-Fat - adverse effects Entrainment Food High fat diet Life Sciences Male Metabolic pathways Metabolism Metabolites Metabolome - physiology Metabolomics Mice Models, Animal Nutrients Oscillations Perturbation Photoperiod Prefrontal cortex Prefrontal Cortex - metabolism Suprachiasmatic nucleus Suprachiasmatic Nucleus - metabolism |
| title | Reshaping circadian metabolism in the suprachiasmatic nucleus and prefrontal cortex by nutritional challenge |
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