Dietary challenges differentially affect activity and sleep/wake behavior in mus musculus: Isolating independent associations with diet/energy balance and body weight
Associated with numerous metabolic and behavioral abnormalities, obesity is classified by metrics reliant on body weight (such as body mass index). However, overnutrition is the common cause of obesity, and may independently contribute to these obesity-related abnormalities. Here, we use dietary cha...
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| description | Associated with numerous metabolic and behavioral abnormalities, obesity is classified by metrics reliant on body weight (such as body mass index). However, overnutrition is the common cause of obesity, and may independently contribute to these obesity-related abnormalities. Here, we use dietary challenges to parse apart the relative influence of diet and/or energy balance from body weight on various metabolic and behavioral outcomes.
Seventy male mice (mus musculus) were subjected to the diet switch feeding paradigm, generating groups with various body weights and energetic imbalances. Spontaneous activity patterns, blood metabolite levels, and unbiased gene expression of the nutrient-sensing ventral hypothalamus (using RNA-sequencing) were measured, and these metrics were compared using standardized multivariate linear regression models.
Spontaneous activity patterns were negatively related to body weight (p |
| doi_str_mv | 10.1371/journal.pone.0196743 |
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Seventy male mice (mus musculus) were subjected to the diet switch feeding paradigm, generating groups with various body weights and energetic imbalances. Spontaneous activity patterns, blood metabolite levels, and unbiased gene expression of the nutrient-sensing ventral hypothalamus (using RNA-sequencing) were measured, and these metrics were compared using standardized multivariate linear regression models.
Spontaneous activity patterns were negatively related to body weight (p<0.0001) but not diet/energy balance (p = 0.63). Both body weight and diet/energy balance predicted circulating glucose and insulin levels, while body weight alone predicted plasma leptin levels. Regarding gene expression within the ventral hypothalamus, only two genes responded to diet/energy balance (neuropeptide y [npy] and agouti-related peptide [agrp]), while others were related only to body weight.
Collectively, these results demonstrate that individual components of obesity-specifically obesogenic diets/energy imbalance and elevated body mass-can have independent effects on metabolic and behavioral outcomes. This work highlights the shortcomings of using body mass-based indices to assess metabolic health, and identifies novel associations between blood biomarkers, neural gene expression, and animal behavior following dietary challenges.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0196743</identifier><identifier>PMID: 29746501</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Abnormalities ; Activity patterns ; Agouti-Related Protein - metabolism ; Analysis ; Animal behavior ; Animal models ; Animals ; Behavior, Animal - physiology ; Biology and Life Sciences ; Biomarkers ; Biomarkers - blood ; Blood ; Body mass ; Body mass index ; Body size ; Body weight ; Body Weight - physiology ; Circadian Rhythm - physiology ; Diet ; Diet - methods ; Energy balance ; Energy Intake - physiology ; Energy Metabolism - physiology ; Gene expression ; Gene Expression - physiology ; Gene sequencing ; Health aspects ; Hormones ; Hypothalamus ; Hypothalamus - metabolism ; Hypothalamus - physiology ; Insulin ; Leptin ; Leptin - blood ; Male ; Medicine and Health Sciences ; Metabolites ; Mice ; Mice, Inbred C57BL ; Neuropeptide Y ; Neuropeptide Y - metabolism ; Obesity ; Obesity - blood ; Obesity - metabolism ; Obesity - physiopathology ; Occupational health ; Overnutrition ; Regression analysis ; Regression models ; Ribonucleic acid ; RNA ; Rodents ; Sleep ; Sleep - physiology ; Sleep and wakefulness ; Wakefulness - physiology</subject><ispartof>PloS one, 2018-05, Vol.13 (5), p.e0196743</ispartof><rights>COPYRIGHT 2018 Public Library of Science</rights><rights>This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication: https://creativecommons.org/publicdomain/zero/1.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-6a8ec1f7ce5250055f49a8b09a490e1bfd937506c637b37d8a2792cb8e8ef863</citedby><cites>FETCH-LOGICAL-c692t-6a8ec1f7ce5250055f49a8b09a490e1bfd937506c637b37d8a2792cb8e8ef863</cites><orcidid>0000-0002-2080-6189</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5945034/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5945034/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29746501$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Perron, Isaac J</creatorcontrib><creatorcontrib>Keenan, Brendan T</creatorcontrib><creatorcontrib>Chellappa, Karthikeyani</creatorcontrib><creatorcontrib>Lahens, Nicholas F</creatorcontrib><creatorcontrib>Yohn, Nicole L</creatorcontrib><creatorcontrib>Shockley, Keith R</creatorcontrib><creatorcontrib>Pack, Allan I</creatorcontrib><creatorcontrib>Veasey, Sigrid C</creatorcontrib><title>Dietary challenges differentially affect activity and sleep/wake behavior in mus musculus: Isolating independent associations with diet/energy balance and body weight</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Associated with numerous metabolic and behavioral abnormalities, obesity is classified by metrics reliant on body weight (such as body mass index). However, overnutrition is the common cause of obesity, and may independently contribute to these obesity-related abnormalities. Here, we use dietary challenges to parse apart the relative influence of diet and/or energy balance from body weight on various metabolic and behavioral outcomes.
Seventy male mice (mus musculus) were subjected to the diet switch feeding paradigm, generating groups with various body weights and energetic imbalances. Spontaneous activity patterns, blood metabolite levels, and unbiased gene expression of the nutrient-sensing ventral hypothalamus (using RNA-sequencing) were measured, and these metrics were compared using standardized multivariate linear regression models.
Spontaneous activity patterns were negatively related to body weight (p<0.0001) but not diet/energy balance (p = 0.63). Both body weight and diet/energy balance predicted circulating glucose and insulin levels, while body weight alone predicted plasma leptin levels. Regarding gene expression within the ventral hypothalamus, only two genes responded to diet/energy balance (neuropeptide y [npy] and agouti-related peptide [agrp]), while others were related only to body weight.
Collectively, these results demonstrate that individual components of obesity-specifically obesogenic diets/energy imbalance and elevated body mass-can have independent effects on metabolic and behavioral outcomes. This work highlights the shortcomings of using body mass-based indices to assess metabolic health, and identifies novel associations between blood biomarkers, neural gene expression, and animal behavior following dietary challenges.</description><subject>Abnormalities</subject><subject>Activity patterns</subject><subject>Agouti-Related Protein - metabolism</subject><subject>Analysis</subject><subject>Animal behavior</subject><subject>Animal models</subject><subject>Animals</subject><subject>Behavior, Animal - physiology</subject><subject>Biology and Life Sciences</subject><subject>Biomarkers</subject><subject>Biomarkers - blood</subject><subject>Blood</subject><subject>Body mass</subject><subject>Body mass index</subject><subject>Body size</subject><subject>Body weight</subject><subject>Body Weight - physiology</subject><subject>Circadian Rhythm - physiology</subject><subject>Diet</subject><subject>Diet - methods</subject><subject>Energy balance</subject><subject>Energy Intake - physiology</subject><subject>Energy Metabolism - physiology</subject><subject>Gene expression</subject><subject>Gene Expression - physiology</subject><subject>Gene sequencing</subject><subject>Health aspects</subject><subject>Hormones</subject><subject>Hypothalamus</subject><subject>Hypothalamus - metabolism</subject><subject>Hypothalamus - physiology</subject><subject>Insulin</subject><subject>Leptin</subject><subject>Leptin - blood</subject><subject>Male</subject><subject>Medicine and Health Sciences</subject><subject>Metabolites</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Neuropeptide Y</subject><subject>Neuropeptide Y - metabolism</subject><subject>Obesity</subject><subject>Obesity - blood</subject><subject>Obesity - metabolism</subject><subject>Obesity - physiopathology</subject><subject>Occupational health</subject><subject>Overnutrition</subject><subject>Regression analysis</subject><subject>Regression models</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>Rodents</subject><subject>Sleep</subject><subject>Sleep - 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However, overnutrition is the common cause of obesity, and may independently contribute to these obesity-related abnormalities. Here, we use dietary challenges to parse apart the relative influence of diet and/or energy balance from body weight on various metabolic and behavioral outcomes.
Seventy male mice (mus musculus) were subjected to the diet switch feeding paradigm, generating groups with various body weights and energetic imbalances. Spontaneous activity patterns, blood metabolite levels, and unbiased gene expression of the nutrient-sensing ventral hypothalamus (using RNA-sequencing) were measured, and these metrics were compared using standardized multivariate linear regression models.
Spontaneous activity patterns were negatively related to body weight (p<0.0001) but not diet/energy balance (p = 0.63). Both body weight and diet/energy balance predicted circulating glucose and insulin levels, while body weight alone predicted plasma leptin levels. Regarding gene expression within the ventral hypothalamus, only two genes responded to diet/energy balance (neuropeptide y [npy] and agouti-related peptide [agrp]), while others were related only to body weight.
Collectively, these results demonstrate that individual components of obesity-specifically obesogenic diets/energy imbalance and elevated body mass-can have independent effects on metabolic and behavioral outcomes. This work highlights the shortcomings of using body mass-based indices to assess metabolic health, and identifies novel associations between blood biomarkers, neural gene expression, and animal behavior following dietary challenges.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>29746501</pmid><doi>10.1371/journal.pone.0196743</doi><tpages>e0196743</tpages><orcidid>https://orcid.org/0000-0002-2080-6189</orcidid><oa>free_for_read</oa></addata></record> |
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| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2018-05, Vol.13 (5), p.e0196743 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_2037055564 |
| source | Public Library of Science (PLoS) Journals Open Access; MEDLINE; DOAJ Directory of Open Access Journals; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Abnormalities Activity patterns Agouti-Related Protein - metabolism Analysis Animal behavior Animal models Animals Behavior, Animal - physiology Biology and Life Sciences Biomarkers Biomarkers - blood Blood Body mass Body mass index Body size Body weight Body Weight - physiology Circadian Rhythm - physiology Diet Diet - methods Energy balance Energy Intake - physiology Energy Metabolism - physiology Gene expression Gene Expression - physiology Gene sequencing Health aspects Hormones Hypothalamus Hypothalamus - metabolism Hypothalamus - physiology Insulin Leptin Leptin - blood Male Medicine and Health Sciences Metabolites Mice Mice, Inbred C57BL Neuropeptide Y Neuropeptide Y - metabolism Obesity Obesity - blood Obesity - metabolism Obesity - physiopathology Occupational health Overnutrition Regression analysis Regression models Ribonucleic acid RNA Rodents Sleep Sleep - physiology Sleep and wakefulness Wakefulness - physiology |
| title | Dietary challenges differentially affect activity and sleep/wake behavior in mus musculus: Isolating independent associations with diet/energy balance and body weight |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-05T15%3A31%3A54IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Dietary%20challenges%20differentially%20affect%20activity%20and%20sleep/wake%20behavior%20in%20mus%20musculus:%20Isolating%20independent%20associations%20with%20diet/energy%20balance%20and%20body%20weight&rft.jtitle=PloS%20one&rft.au=Perron,%20Isaac%20J&rft.date=2018-05-10&rft.volume=13&rft.issue=5&rft.spage=e0196743&rft.pages=e0196743-&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0196743&rft_dat=%3Cgale_plos_%3EA538070122%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2037055564&rft_id=info:pmid/29746501&rft_galeid=A538070122&rft_doaj_id=oai_doaj_org_article_cc8a41288d2543959c96f7cae511ac33&rfr_iscdi=true |