Comprehensive amelioration of high-fat diet-induced metabolic dysfunctions through activation of the PGC-1α pathway by probiotics treatment in mice
Although the beneficial effects of probiotics in the prevention or treatment of metabolic disorders have been extensively researched, the precise mechanisms by which probiotics improve metabolic homeostasis are still not clear. Given that probiotics usually exert a comprehensive effect on multiple m...
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| description | Although the beneficial effects of probiotics in the prevention or treatment of metabolic disorders have been extensively researched, the precise mechanisms by which probiotics improve metabolic homeostasis are still not clear. Given that probiotics usually exert a comprehensive effect on multiple metabolic disorders, defining a concurrent mechanism underlying the multiple effects is critical to understand the function of probiotics. In this study, we identified the SIRT1-dependent or independent PGC-1α pathways in multiple organs that mediate the protective effects of a strain of Lactobacillus plantarum against high-fat diet-induced adiposity, glucose intolerance, and dyslipidemia. L. plantarum treatment significantly enhanced the expression of SIRT1, PPARα, and PGC-1α in the liver and adipose tissues under HFD-fed condition. L. plantarum treated mice also exhibited significantly increased expressions of genes involved in bile acid synthesis and reverse cholesterol transport in the liver, browning and thermogenesis of adipose tissue, and fatty acid oxidation in the liver and adipose tissue. Additionally, L. plantarum treatment significantly upregulated the expressions of adiponectin in adipose tissue, irisin in skeletal muscle and subcutaneous adipose tissue (SAT), and FGF21 in SAT. These beneficial changes were associated with a significantly improved HFD-induced alteration of gut microbiota. Our findings suggest that the PGC-1α-mediated pathway could be regarded as a potential target in the development of probiotics-based therapies for the prevention and treatment of metabolic disorders. |
| doi_str_mv | 10.1371/journal.pone.0228932 |
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Given that probiotics usually exert a comprehensive effect on multiple metabolic disorders, defining a concurrent mechanism underlying the multiple effects is critical to understand the function of probiotics. In this study, we identified the SIRT1-dependent or independent PGC-1α pathways in multiple organs that mediate the protective effects of a strain of Lactobacillus plantarum against high-fat diet-induced adiposity, glucose intolerance, and dyslipidemia. L. plantarum treatment significantly enhanced the expression of SIRT1, PPARα, and PGC-1α in the liver and adipose tissues under HFD-fed condition. L. plantarum treated mice also exhibited significantly increased expressions of genes involved in bile acid synthesis and reverse cholesterol transport in the liver, browning and thermogenesis of adipose tissue, and fatty acid oxidation in the liver and adipose tissue. Additionally, L. plantarum treatment significantly upregulated the expressions of adiponectin in adipose tissue, irisin in skeletal muscle and subcutaneous adipose tissue (SAT), and FGF21 in SAT. These beneficial changes were associated with a significantly improved HFD-induced alteration of gut microbiota. Our findings suggest that the PGC-1α-mediated pathway could be regarded as a potential target in the development of probiotics-based therapies for the prevention and treatment of metabolic disorders.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0228932</identifier><identifier>PMID: 32040532</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adiponectin ; Adipose tissue ; Adipose Tissue - metabolism ; Adiposity ; Animals ; Bile Acids and Salts - biosynthesis ; Biology and Life Sciences ; Browning ; Cholesterol ; Cholesterol - metabolism ; Diet ; Diet, High-Fat - adverse effects ; Disorders ; Dyslipidemia ; Dyslipidemias - metabolism ; Dyslipidemias - prevention & control ; Dyslipidemias - therapy ; Experiments ; Fatty acids ; Gastrointestinal Microbiome ; Glucose Intolerance - metabolism ; Glucose Intolerance - prevention & control ; Glucose Intolerance - therapy ; Glucose tolerance ; High fat diet ; Homeostasis ; Insulin resistance ; Intestinal microflora ; Intolerance ; Lactobacillus plantarum - physiology ; Life sciences ; Lipid Metabolism ; Lipids ; Liver ; Liver - metabolism ; Male ; Medicine and Health Sciences ; Metabolic Diseases - metabolism ; Metabolic Diseases - prevention & control ; Metabolic Diseases - therapy ; Metabolic disorders ; Metabolic rate ; Metabolites ; Mice ; Mice, Inbred C57BL ; Microbiota ; Muscles ; Musculoskeletal system ; Organs ; Oxidation ; Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha - metabolism ; Plant protection ; Plant tissues ; Prevention ; Probiotics ; Probiotics - therapeutic use ; Signal Transduction ; SIRT1 protein ; Sirtuin 1 - metabolism ; Skeletal muscle ; Studies ; Thermogenesis</subject><ispartof>PloS one, 2020-02, Vol.15 (2), p.e0228932-e0228932</ispartof><rights>2020 Kwon et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2020 Kwon et al 2020 Kwon et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c526t-e420d042467878514aea8e11510b17339f0149cc3e775e05d5c26e4ed1ac4fb3</citedby><cites>FETCH-LOGICAL-c526t-e420d042467878514aea8e11510b17339f0149cc3e775e05d5c26e4ed1ac4fb3</cites><orcidid>0000-0003-1862-8739</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/PMC7010303/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7010303/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79569,79570</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32040532$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kwon, Jeonghyeon</creatorcontrib><creatorcontrib>Kim, Bobae</creatorcontrib><creatorcontrib>Lee, Chungho</creatorcontrib><creatorcontrib>Joung, Hyunchae</creatorcontrib><creatorcontrib>Kim, Byoung-Kook</creatorcontrib><creatorcontrib>Choi, In Suk</creatorcontrib><creatorcontrib>Hyun, Chang-Kee</creatorcontrib><title>Comprehensive amelioration of high-fat diet-induced metabolic dysfunctions through activation of the PGC-1α pathway by probiotics treatment in mice</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Although the beneficial effects of probiotics in the prevention or treatment of metabolic disorders have been extensively researched, the precise mechanisms by which probiotics improve metabolic homeostasis are still not clear. Given that probiotics usually exert a comprehensive effect on multiple metabolic disorders, defining a concurrent mechanism underlying the multiple effects is critical to understand the function of probiotics. In this study, we identified the SIRT1-dependent or independent PGC-1α pathways in multiple organs that mediate the protective effects of a strain of Lactobacillus plantarum against high-fat diet-induced adiposity, glucose intolerance, and dyslipidemia. L. plantarum treatment significantly enhanced the expression of SIRT1, PPARα, and PGC-1α in the liver and adipose tissues under HFD-fed condition. L. plantarum treated mice also exhibited significantly increased expressions of genes involved in bile acid synthesis and reverse cholesterol transport in the liver, browning and thermogenesis of adipose tissue, and fatty acid oxidation in the liver and adipose tissue. Additionally, L. plantarum treatment significantly upregulated the expressions of adiponectin in adipose tissue, irisin in skeletal muscle and subcutaneous adipose tissue (SAT), and FGF21 in SAT. These beneficial changes were associated with a significantly improved HFD-induced alteration of gut microbiota. Our findings suggest that the PGC-1α-mediated pathway could be regarded as a potential target in the development of probiotics-based therapies for the prevention and treatment of metabolic disorders.</description><subject>Adiponectin</subject><subject>Adipose tissue</subject><subject>Adipose Tissue - metabolism</subject><subject>Adiposity</subject><subject>Animals</subject><subject>Bile Acids and Salts - biosynthesis</subject><subject>Biology and Life Sciences</subject><subject>Browning</subject><subject>Cholesterol</subject><subject>Cholesterol - metabolism</subject><subject>Diet</subject><subject>Diet, High-Fat - adverse effects</subject><subject>Disorders</subject><subject>Dyslipidemia</subject><subject>Dyslipidemias - metabolism</subject><subject>Dyslipidemias - prevention & control</subject><subject>Dyslipidemias - therapy</subject><subject>Experiments</subject><subject>Fatty acids</subject><subject>Gastrointestinal Microbiome</subject><subject>Glucose Intolerance - metabolism</subject><subject>Glucose Intolerance - 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metabolism</subject><subject>Plant protection</subject><subject>Plant tissues</subject><subject>Prevention</subject><subject>Probiotics</subject><subject>Probiotics - therapeutic use</subject><subject>Signal Transduction</subject><subject>SIRT1 protein</subject><subject>Sirtuin 1 - metabolism</subject><subject>Skeletal muscle</subject><subject>Studies</subject><subject>Thermogenesis</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNptUstu1DAUjRCIlsIfILDEhk0GP_PYIKFRKZUqwaJ7y7FvJh4lcbCdQfMf_Ag_wjfV00lHLWJ1fe1zju-xT5a9JXhFWEk-bd3sR9WvJjfCClNa1Yw-y85JKnlBMXv-aH2WvQphi7FgVVG8zM4YxTw19Dz7vXbD5KGDMdgdIDVAb51X0boRuRZ1dtPlrYrIWIi5Hc2swaABompcbzUy-9DOoz7AA4qdd_OmQyr1u5NE7AD9uFrn5O8fNKnY_VJ71OzR5F1jXbQ68TyoOMAYkR3RYDW8zl60qg_wZqkX2e3Xy9v1t_zm-9X1-stNrgUtYg6cYoM55UVZlZUgXIGqgBBBcENKxuoWE15rzaAsBWBhhKYFcDBEad427CJ7f5Sdehfk8p5BUiZoXfNSFAlxfUQYp7Zy8nZQfi-dsvJ-w_mNVD556EHWSpCCCV4VRnDTpt_QhRaK1BVlTVmzpPV5uW1uBjA6-fWqfyL69GS0ndy4nSwxwQwfBD4uAt79nCFEOdigoe_VCG6-n5uJMlklCfrhH-j_3fEjSnsXgof2NAzB8pCxB5Y8ZEwuGUu0d4-NnEgPoWJ3wpDSYw</recordid><startdate>20200210</startdate><enddate>20200210</enddate><creator>Kwon, Jeonghyeon</creator><creator>Kim, Bobae</creator><creator>Lee, Chungho</creator><creator>Joung, Hyunchae</creator><creator>Kim, Byoung-Kook</creator><creator>Choi, In Suk</creator><creator>Hyun, Chang-Kee</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0003-1862-8739</orcidid></search><sort><creationdate>20200210</creationdate><title>Comprehensive amelioration of high-fat diet-induced metabolic dysfunctions through activation of the PGC-1α pathway by probiotics treatment in mice</title><author>Kwon, Jeonghyeon ; Kim, Bobae ; Lee, Chungho ; Joung, Hyunchae ; Kim, Byoung-Kook ; Choi, In Suk ; Hyun, Chang-Kee</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c526t-e420d042467878514aea8e11510b17339f0149cc3e775e05d5c26e4ed1ac4fb3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Adiponectin</topic><topic>Adipose tissue</topic><topic>Adipose Tissue - metabolism</topic><topic>Adiposity</topic><topic>Animals</topic><topic>Bile Acids and Salts - biosynthesis</topic><topic>Biology and Life Sciences</topic><topic>Browning</topic><topic>Cholesterol</topic><topic>Cholesterol - metabolism</topic><topic>Diet</topic><topic>Diet, High-Fat - adverse effects</topic><topic>Disorders</topic><topic>Dyslipidemia</topic><topic>Dyslipidemias - metabolism</topic><topic>Dyslipidemias - prevention & control</topic><topic>Dyslipidemias - therapy</topic><topic>Experiments</topic><topic>Fatty acids</topic><topic>Gastrointestinal Microbiome</topic><topic>Glucose Intolerance - metabolism</topic><topic>Glucose Intolerance - prevention & control</topic><topic>Glucose Intolerance - therapy</topic><topic>Glucose tolerance</topic><topic>High fat diet</topic><topic>Homeostasis</topic><topic>Insulin resistance</topic><topic>Intestinal microflora</topic><topic>Intolerance</topic><topic>Lactobacillus plantarum - physiology</topic><topic>Life sciences</topic><topic>Lipid Metabolism</topic><topic>Lipids</topic><topic>Liver</topic><topic>Liver - 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Given that probiotics usually exert a comprehensive effect on multiple metabolic disorders, defining a concurrent mechanism underlying the multiple effects is critical to understand the function of probiotics. In this study, we identified the SIRT1-dependent or independent PGC-1α pathways in multiple organs that mediate the protective effects of a strain of Lactobacillus plantarum against high-fat diet-induced adiposity, glucose intolerance, and dyslipidemia. L. plantarum treatment significantly enhanced the expression of SIRT1, PPARα, and PGC-1α in the liver and adipose tissues under HFD-fed condition. L. plantarum treated mice also exhibited significantly increased expressions of genes involved in bile acid synthesis and reverse cholesterol transport in the liver, browning and thermogenesis of adipose tissue, and fatty acid oxidation in the liver and adipose tissue. Additionally, L. plantarum treatment significantly upregulated the expressions of adiponectin in adipose tissue, irisin in skeletal muscle and subcutaneous adipose tissue (SAT), and FGF21 in SAT. These beneficial changes were associated with a significantly improved HFD-induced alteration of gut microbiota. Our findings suggest that the PGC-1α-mediated pathway could be regarded as a potential target in the development of probiotics-based therapies for the prevention and treatment of metabolic disorders.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>32040532</pmid><doi>10.1371/journal.pone.0228932</doi><orcidid>https://orcid.org/0000-0003-1862-8739</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | PloS one, 2020-02, Vol.15 (2), p.e0228932-e0228932 |
| issn | 1932-6203 1932-6203 |
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| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS) |
| subjects | Adiponectin Adipose tissue Adipose Tissue - metabolism Adiposity Animals Bile Acids and Salts - biosynthesis Biology and Life Sciences Browning Cholesterol Cholesterol - metabolism Diet Diet, High-Fat - adverse effects Disorders Dyslipidemia Dyslipidemias - metabolism Dyslipidemias - prevention & control Dyslipidemias - therapy Experiments Fatty acids Gastrointestinal Microbiome Glucose Intolerance - metabolism Glucose Intolerance - prevention & control Glucose Intolerance - therapy Glucose tolerance High fat diet Homeostasis Insulin resistance Intestinal microflora Intolerance Lactobacillus plantarum - physiology Life sciences Lipid Metabolism Lipids Liver Liver - metabolism Male Medicine and Health Sciences Metabolic Diseases - metabolism Metabolic Diseases - prevention & control Metabolic Diseases - therapy Metabolic disorders Metabolic rate Metabolites Mice Mice, Inbred C57BL Microbiota Muscles Musculoskeletal system Organs Oxidation Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha - metabolism Plant protection Plant tissues Prevention Probiotics Probiotics - therapeutic use Signal Transduction SIRT1 protein Sirtuin 1 - metabolism Skeletal muscle Studies Thermogenesis |
| title | Comprehensive amelioration of high-fat diet-induced metabolic dysfunctions through activation of the PGC-1α pathway by probiotics treatment in mice |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-15T19%3A14%3A40IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Comprehensive%20amelioration%20of%20high-fat%20diet-induced%20metabolic%20dysfunctions%20through%20activation%20of%20the%20PGC-1%CE%B1%20pathway%20by%20probiotics%20treatment%20in%20mice&rft.jtitle=PloS%20one&rft.au=Kwon,%20Jeonghyeon&rft.date=2020-02-10&rft.volume=15&rft.issue=2&rft.spage=e0228932&rft.epage=e0228932&rft.pages=e0228932-e0228932&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0228932&rft_dat=%3Cproquest_plos_%3E2353577751%3C/proquest_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2352994756&rft_id=info:pmid/32040532&rft_doaj_id=oai_doaj_org_article_9a51635486d54df893c6c5a19823b793&rfr_iscdi=true |