Obesity remodels activity and transcriptional state of a lateral hypothalamic brake on feeding
The current obesity epidemic is a major worldwide health concern. Despite the consensus that the brain regulates energy homeostasis, the neural adaptations governing obesity are unknown. Using a combination of high-throughput single-cell RNA sequencing and longitudinal in vivo two-photon calcium ima...
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| Veröffentlicht in: | Science (American Association for the Advancement of Science) 2019-06, Vol.364 (6447), p.1271-1274 |
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| creator | Rossi, Mark A. Basiri, Marcus L. McHenry, Jenna A. Kosyk, Oksana Otis, James M. van den Munkhof, Hanna E. Bryois, Julien Hübel, Christopher Breen, Gerome Guo, Wilson Bulik, Cynthia M. Sullivan, Patrick F. Stuber, Garret D. |
| description | The current obesity epidemic is a major worldwide health concern. Despite the consensus that the brain regulates energy homeostasis, the neural adaptations governing obesity are unknown. Using a combination of high-throughput single-cell RNA sequencing and longitudinal in vivo two-photon calcium imaging, we surveyed functional alterations of the lateral hypothalamic area (LHA)–a highly conserved brain region that orchestrates feeding–in a mouse model of obesity. The transcriptional profile of LHA glutamatergic neurons was affected by obesity, exhibiting changes indicative of altered neuronal activity. Encoding properties of individual LHA glutamatergic neurons were then tracked throughout obesity, revealing greatly attenuated reward responses. These data demonstrate how diet disrupts the function of an endogenous feeding suppression system to promote overeating and obesity. |
| doi_str_mv | 10.1126/science.aax1184 |
| format | Article |
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Despite the consensus that the brain regulates energy homeostasis, the neural adaptations governing obesity are unknown. Using a combination of high-throughput single-cell RNA sequencing and longitudinal in vivo two-photon calcium imaging, we surveyed functional alterations of the lateral hypothalamic area (LHA)–a highly conserved brain region that orchestrates feeding–in a mouse model of obesity. The transcriptional profile of LHA glutamatergic neurons was affected by obesity, exhibiting changes indicative of altered neuronal activity. Encoding properties of individual LHA glutamatergic neurons were then tracked throughout obesity, revealing greatly attenuated reward responses. These data demonstrate how diet disrupts the function of an endogenous feeding suppression system to promote overeating and obesity.</description><identifier>ISSN: 0036-8075</identifier><identifier>EISSN: 1095-9203</identifier><identifier>DOI: 10.1126/science.aax1184</identifier><identifier>PMID: 31249056</identifier><language>eng</language><publisher>United States: American Association for the Advancement of Science</publisher><subject>Adaptation ; Animals ; Brain ; Brakes ; Calcium ; Calcium imaging ; Diet ; Diet, High-Fat ; Disease Models, Animal ; Eating disorders ; Eating Habits ; Energy balance ; Epidemics ; Feeding ; Feeding behavior ; Food intake ; Gene sequencing ; Glutamatergic transmission ; Glutamic Acid - metabolism ; Homeostasis ; Hypothalamic Area, Lateral - metabolism ; Hypothalamic Area, Lateral - physiopathology ; Hypothalamus ; Hypothalamus (lateral) ; Mice ; Neuroimaging ; Neurons ; Obesity ; Obesity - genetics ; Obesity - physiopathology ; Obesity - psychology ; Regulators ; Reinforcement ; Reward ; Ribonucleic acid ; RNA ; Transcription ; Transcriptome ; Vesicular Glutamate Transport Protein 2 - genetics</subject><ispartof>Science (American Association for the Advancement of Science), 2019-06, Vol.364 (6447), p.1271-1274</ispartof><rights>Copyright © 2019 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.</rights><rights>Copyright © 2019 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c547t-28247259f672572e38cf5069afe23d524096362bc6b87d77dd319a178303d8d13</citedby><cites>FETCH-LOGICAL-c547t-28247259f672572e38cf5069afe23d524096362bc6b87d77dd319a178303d8d13</cites><orcidid>0000-0002-5724-3615 ; 0000-0002-4747-2166 ; 0000-0002-4829-7187 ; 0000-0003-2053-1792 ; 0000-0001-7772-3264 ; 0000-0002-6619-873X ; 0000-0001-9770-9099 ; 0000-0001-7269-8856 ; 0000-0002-1267-8287 ; 0000-0003-1730-4855</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,550,776,780,881,2870,2871,27903,27904</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31249056$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttp://kipublications.ki.se/Default.aspx?queryparsed=id:141311989$$DView record from Swedish Publication Index$$Hfree_for_read</backlink></links><search><creatorcontrib>Rossi, Mark A.</creatorcontrib><creatorcontrib>Basiri, Marcus L.</creatorcontrib><creatorcontrib>McHenry, Jenna A.</creatorcontrib><creatorcontrib>Kosyk, Oksana</creatorcontrib><creatorcontrib>Otis, James M.</creatorcontrib><creatorcontrib>van den Munkhof, Hanna E.</creatorcontrib><creatorcontrib>Bryois, Julien</creatorcontrib><creatorcontrib>Hübel, Christopher</creatorcontrib><creatorcontrib>Breen, Gerome</creatorcontrib><creatorcontrib>Guo, Wilson</creatorcontrib><creatorcontrib>Bulik, Cynthia M.</creatorcontrib><creatorcontrib>Sullivan, Patrick F.</creatorcontrib><creatorcontrib>Stuber, Garret D.</creatorcontrib><title>Obesity remodels activity and transcriptional state of a lateral hypothalamic brake on feeding</title><title>Science (American Association for the Advancement of Science)</title><addtitle>Science</addtitle><description>The current obesity epidemic is a major worldwide health concern. Despite the consensus that the brain regulates energy homeostasis, the neural adaptations governing obesity are unknown. Using a combination of high-throughput single-cell RNA sequencing and longitudinal in vivo two-photon calcium imaging, we surveyed functional alterations of the lateral hypothalamic area (LHA)–a highly conserved brain region that orchestrates feeding–in a mouse model of obesity. The transcriptional profile of LHA glutamatergic neurons was affected by obesity, exhibiting changes indicative of altered neuronal activity. Encoding properties of individual LHA glutamatergic neurons were then tracked throughout obesity, revealing greatly attenuated reward responses. These data demonstrate how diet disrupts the function of an endogenous feeding suppression system to promote overeating and obesity.</description><subject>Adaptation</subject><subject>Animals</subject><subject>Brain</subject><subject>Brakes</subject><subject>Calcium</subject><subject>Calcium imaging</subject><subject>Diet</subject><subject>Diet, High-Fat</subject><subject>Disease Models, Animal</subject><subject>Eating disorders</subject><subject>Eating Habits</subject><subject>Energy balance</subject><subject>Epidemics</subject><subject>Feeding</subject><subject>Feeding behavior</subject><subject>Food intake</subject><subject>Gene sequencing</subject><subject>Glutamatergic transmission</subject><subject>Glutamic Acid - metabolism</subject><subject>Homeostasis</subject><subject>Hypothalamic Area, Lateral - metabolism</subject><subject>Hypothalamic Area, Lateral - physiopathology</subject><subject>Hypothalamus</subject><subject>Hypothalamus (lateral)</subject><subject>Mice</subject><subject>Neuroimaging</subject><subject>Neurons</subject><subject>Obesity</subject><subject>Obesity - genetics</subject><subject>Obesity - physiopathology</subject><subject>Obesity - psychology</subject><subject>Regulators</subject><subject>Reinforcement</subject><subject>Reward</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>Transcription</subject><subject>Transcriptome</subject><subject>Vesicular Glutamate Transport Protein 2 - genetics</subject><issn>0036-8075</issn><issn>1095-9203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>D8T</sourceid><recordid>eNpdkctv1DAQxi0EokvhzAkUiQuXtH7ErwsSqnhJlXqBK5ZjT7reJvFiewv73-Nlw4pysUfz_WY0Mx9CLwm-IISKy-wCzA4urP1FiOoeoRXBmreaYvYYrTBmolVY8jP0LOcNxlXT7Ck6Y4R2GnOxQt9vesih7JsEU_Qw5sa6Eu4PGTv7piQ7Z5fCtoQ427HJxRZo4tDYZqxRqqn1fhvL2o52Cq7pk72r-twMAD7Mt8_Rk8GOGV4s_zn69vHD16vP7fXNpy9X769bxztZWqpoJynXg6ivpMCUGzgW2g5Amee0w1owQXsneiW9lN4zoi2RimHmlSfsHLXHvvknbHe92aYw2bQ30QazpO5qBKaTSkpd-XdHvioTeAdz3XR8UPZQmcPa3MZ7IxlRSvDa4O3SIMUfO8jFTCE7GEc7Q9xlQ2mdv27AREXf_Idu4i7Va_6hJKVK8sNEl0fKpZhzguE0DMHm4LVZvDaL17Xi9b87nPi_5lbg1RHY5BLTSadCdrxenP0GXKSydQ</recordid><startdate>20190628</startdate><enddate>20190628</enddate><creator>Rossi, Mark A.</creator><creator>Basiri, Marcus L.</creator><creator>McHenry, Jenna A.</creator><creator>Kosyk, Oksana</creator><creator>Otis, James M.</creator><creator>van den Munkhof, Hanna E.</creator><creator>Bryois, Julien</creator><creator>Hübel, Christopher</creator><creator>Breen, Gerome</creator><creator>Guo, Wilson</creator><creator>Bulik, Cynthia M.</creator><creator>Sullivan, Patrick F.</creator><creator>Stuber, Garret D.</creator><general>American Association for the Advancement of Science</general><general>The American Association for the Advancement of Science</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>7QF</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QQ</scope><scope>7QR</scope><scope>7SC</scope><scope>7SE</scope><scope>7SN</scope><scope>7SP</scope><scope>7SR</scope><scope>7SS</scope><scope>7T7</scope><scope>7TA</scope><scope>7TB</scope><scope>7TK</scope><scope>7TM</scope><scope>7U5</scope><scope>7U9</scope><scope>8BQ</scope><scope>8FD</scope><scope>C1K</scope><scope>F28</scope><scope>FR3</scope><scope>H8D</scope><scope>H8G</scope><scope>H94</scope><scope>JG9</scope><scope>JQ2</scope><scope>K9.</scope><scope>KR7</scope><scope>L7M</scope><scope>L~C</scope><scope>L~D</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>ADTPV</scope><scope>AOWAS</scope><scope>D8T</scope><scope>ZZAVC</scope><orcidid>https://orcid.org/0000-0002-5724-3615</orcidid><orcidid>https://orcid.org/0000-0002-4747-2166</orcidid><orcidid>https://orcid.org/0000-0002-4829-7187</orcidid><orcidid>https://orcid.org/0000-0003-2053-1792</orcidid><orcidid>https://orcid.org/0000-0001-7772-3264</orcidid><orcidid>https://orcid.org/0000-0002-6619-873X</orcidid><orcidid>https://orcid.org/0000-0001-9770-9099</orcidid><orcidid>https://orcid.org/0000-0001-7269-8856</orcidid><orcidid>https://orcid.org/0000-0002-1267-8287</orcidid><orcidid>https://orcid.org/0000-0003-1730-4855</orcidid></search><sort><creationdate>20190628</creationdate><title>Obesity remodels activity and transcriptional state of a lateral hypothalamic brake on feeding</title><author>Rossi, Mark A. ; Basiri, Marcus L. ; McHenry, Jenna A. ; Kosyk, Oksana ; Otis, James M. ; van den Munkhof, Hanna E. ; Bryois, Julien ; Hübel, Christopher ; Breen, Gerome ; Guo, Wilson ; Bulik, Cynthia M. ; Sullivan, Patrick F. ; Stuber, Garret D.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c547t-28247259f672572e38cf5069afe23d524096362bc6b87d77dd319a178303d8d13</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Adaptation</topic><topic>Animals</topic><topic>Brain</topic><topic>Brakes</topic><topic>Calcium</topic><topic>Calcium imaging</topic><topic>Diet</topic><topic>Diet, High-Fat</topic><topic>Disease Models, Animal</topic><topic>Eating disorders</topic><topic>Eating Habits</topic><topic>Energy balance</topic><topic>Epidemics</topic><topic>Feeding</topic><topic>Feeding behavior</topic><topic>Food intake</topic><topic>Gene sequencing</topic><topic>Glutamatergic transmission</topic><topic>Glutamic Acid - 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| source | MEDLINE; SWEPUB Freely available online; American Association for the Advancement of Science |
| subjects | Adaptation Animals Brain Brakes Calcium Calcium imaging Diet Diet, High-Fat Disease Models, Animal Eating disorders Eating Habits Energy balance Epidemics Feeding Feeding behavior Food intake Gene sequencing Glutamatergic transmission Glutamic Acid - metabolism Homeostasis Hypothalamic Area, Lateral - metabolism Hypothalamic Area, Lateral - physiopathology Hypothalamus Hypothalamus (lateral) Mice Neuroimaging Neurons Obesity Obesity - genetics Obesity - physiopathology Obesity - psychology Regulators Reinforcement Reward Ribonucleic acid RNA Transcription Transcriptome Vesicular Glutamate Transport Protein 2 - genetics |
| title | Obesity remodels activity and transcriptional state of a lateral hypothalamic brake on feeding |
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