Integration of bioassay and non-target metabolite analysis of tomato reveals that β-carotene and lycopene activate the adiponectin signaling pathway, including AMPK phosphorylation
Adiponectin, an adipokine, regulates glucose metabolism and insulin sensitivity through the adiponectin receptor (AdipoR). In this study, we searched for metabolites that activate the adiponectin signaling pathway from tomato ( Solanum lycopersicu ). Metabolites of mature tomato were separated into...
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| creator | Mohri, Shinsuke Takahashi, Haruya Sakai, Maiko Waki, Naoko Takahashi, Shingo Aizawa, Koichi Suganuma, Hiroyuki Ara, Takeshi Sugawara, Tatsuya Shibata, Daisuke Matsumura, Yasuki Goto, Tsuyoshi Kawada, Teruo |
| description | Adiponectin, an adipokine, regulates glucose metabolism and insulin sensitivity through the adiponectin receptor (AdipoR). In this study, we searched for metabolites that activate the adiponectin signaling pathway from tomato (
Solanum lycopersicu
). Metabolites of mature tomato were separated into 55 fractions by liquid chromatography, and then each fraction was examined using the phosphorylation assay of AMP-protein kinase (AMPK) in C2C12 myotubes and in AdipoR-knockdown cells by small interfering RNA (siRNA). Several fractions showed AMPK phosphorylation in C2C12 myotubes and siRNA-mediated abrogation of the effect. Non-targeted metabolite analysis revealed the presence of 721 diverse metabolites in tomato. By integrating the activity of fractions on AMPK phosphorylation and the 721 metabolites based on their retention times of liquid chromatography, we performed a comprehensive screen for metabolites that possess adiponectin-like activity. As the screening suggested that the active fractions contained four carotenoids, we further analyzed β-carotene and lycopene, the major carotenoids of food. They induced AMPK phosphorylation via the AdipoR, Ca
2+
/calmodulin-dependent protein kinase kinase and Ca
2+
influx, in addition to activating glucose uptake via AdipoR in C2C12 myotubes. All these events were characteristic adiponectin actions. These results indicated that the food-derived carotenoids, β-carotene and lycopene, activate the adiponectin signaling pathway, including AMPK phosphorylation. |
| doi_str_mv | 10.1371/journal.pone.0267248 |
| format | Article |
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Solanum lycopersicu
). Metabolites of mature tomato were separated into 55 fractions by liquid chromatography, and then each fraction was examined using the phosphorylation assay of AMP-protein kinase (AMPK) in C2C12 myotubes and in AdipoR-knockdown cells by small interfering RNA (siRNA). Several fractions showed AMPK phosphorylation in C2C12 myotubes and siRNA-mediated abrogation of the effect. Non-targeted metabolite analysis revealed the presence of 721 diverse metabolites in tomato. By integrating the activity of fractions on AMPK phosphorylation and the 721 metabolites based on their retention times of liquid chromatography, we performed a comprehensive screen for metabolites that possess adiponectin-like activity. As the screening suggested that the active fractions contained four carotenoids, we further analyzed β-carotene and lycopene, the major carotenoids of food. They induced AMPK phosphorylation via the AdipoR, Ca
2+
/calmodulin-dependent protein kinase kinase and Ca
2+
influx, in addition to activating glucose uptake via AdipoR in C2C12 myotubes. All these events were characteristic adiponectin actions. These results indicated that the food-derived carotenoids, β-carotene and lycopene, activate the adiponectin signaling pathway, including AMPK phosphorylation.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0267248</identifier><identifier>PMID: 35776737</identifier><language>eng</language><publisher>San Francisco: Public Library of Science</publisher><subject>Adiponectin ; Bioassays ; Biology and Life Sciences ; Ca2+/calmodulin-dependent protein kinase ; Calcium influx ; Calcium ions ; Calcium-binding protein ; Calmodulin ; Carotene ; Carotenoids ; Chromatography ; Diabetes ; Food ; Fractions ; Glucose ; Glucose metabolism ; Insulin ; Kinases ; Liquid chromatography ; Lycopene ; Medicine and Health Sciences ; Metabolic disorders ; Metabolism ; Metabolites ; Molecular weight ; Myotubes ; Obesity ; Penicillin ; Phosphorylation ; Physical Sciences ; Proteins ; Research and Analysis Methods ; Signal transduction ; Signaling ; siRNA ; Solanum lycopersicum ; Solvents ; Tomatoes ; β-Carotene</subject><ispartof>PloS one, 2022-07, Vol.17 (7), p.e0267248-e0267248</ispartof><rights>2022 Mohri 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>2022 Mohri et al 2022 Mohri et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c613t-23c9ba3e09de39b06361a8643f8e1d8ebeb981401ca2242c350b5eb6a174777f3</citedby><cites>FETCH-LOGICAL-c613t-23c9ba3e09de39b06361a8643f8e1d8ebeb981401ca2242c350b5eb6a174777f3</cites><orcidid>0000-0002-9083-2913 ; 0000-0003-3182-2894</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/PMC9249195/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9249195/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids></links><search><contributor>Wang, Chun-Hua</contributor><creatorcontrib>Mohri, Shinsuke</creatorcontrib><creatorcontrib>Takahashi, Haruya</creatorcontrib><creatorcontrib>Sakai, Maiko</creatorcontrib><creatorcontrib>Waki, Naoko</creatorcontrib><creatorcontrib>Takahashi, Shingo</creatorcontrib><creatorcontrib>Aizawa, Koichi</creatorcontrib><creatorcontrib>Suganuma, Hiroyuki</creatorcontrib><creatorcontrib>Ara, Takeshi</creatorcontrib><creatorcontrib>Sugawara, Tatsuya</creatorcontrib><creatorcontrib>Shibata, Daisuke</creatorcontrib><creatorcontrib>Matsumura, Yasuki</creatorcontrib><creatorcontrib>Goto, Tsuyoshi</creatorcontrib><creatorcontrib>Kawada, Teruo</creatorcontrib><title>Integration of bioassay and non-target metabolite analysis of tomato reveals that β-carotene and lycopene activate the adiponectin signaling pathway, including AMPK phosphorylation</title><title>PloS one</title><description>Adiponectin, an adipokine, regulates glucose metabolism and insulin sensitivity through the adiponectin receptor (AdipoR). In this study, we searched for metabolites that activate the adiponectin signaling pathway from tomato (
Solanum lycopersicu
). Metabolites of mature tomato were separated into 55 fractions by liquid chromatography, and then each fraction was examined using the phosphorylation assay of AMP-protein kinase (AMPK) in C2C12 myotubes and in AdipoR-knockdown cells by small interfering RNA (siRNA). Several fractions showed AMPK phosphorylation in C2C12 myotubes and siRNA-mediated abrogation of the effect. Non-targeted metabolite analysis revealed the presence of 721 diverse metabolites in tomato. By integrating the activity of fractions on AMPK phosphorylation and the 721 metabolites based on their retention times of liquid chromatography, we performed a comprehensive screen for metabolites that possess adiponectin-like activity. As the screening suggested that the active fractions contained four carotenoids, we further analyzed β-carotene and lycopene, the major carotenoids of food. They induced AMPK phosphorylation via the AdipoR, Ca
2+
/calmodulin-dependent protein kinase kinase and Ca
2+
influx, in addition to activating glucose uptake via AdipoR in C2C12 myotubes. All these events were characteristic adiponectin actions. These results indicated that the food-derived carotenoids, β-carotene and lycopene, activate the adiponectin signaling pathway, including AMPK phosphorylation.</description><subject>Adiponectin</subject><subject>Bioassays</subject><subject>Biology and Life Sciences</subject><subject>Ca2+/calmodulin-dependent protein kinase</subject><subject>Calcium influx</subject><subject>Calcium ions</subject><subject>Calcium-binding protein</subject><subject>Calmodulin</subject><subject>Carotene</subject><subject>Carotenoids</subject><subject>Chromatography</subject><subject>Diabetes</subject><subject>Food</subject><subject>Fractions</subject><subject>Glucose</subject><subject>Glucose metabolism</subject><subject>Insulin</subject><subject>Kinases</subject><subject>Liquid chromatography</subject><subject>Lycopene</subject><subject>Medicine and Health Sciences</subject><subject>Metabolic disorders</subject><subject>Metabolism</subject><subject>Metabolites</subject><subject>Molecular weight</subject><subject>Myotubes</subject><subject>Obesity</subject><subject>Penicillin</subject><subject>Phosphorylation</subject><subject>Physical Sciences</subject><subject>Proteins</subject><subject>Research and Analysis Methods</subject><subject>Signal transduction</subject><subject>Signaling</subject><subject>siRNA</subject><subject>Solanum 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of bioassay and non-target metabolite analysis of tomato reveals that β-carotene and lycopene activate the adiponectin signaling pathway, including AMPK phosphorylation</title><author>Mohri, Shinsuke ; Takahashi, Haruya ; Sakai, Maiko ; Waki, Naoko ; Takahashi, Shingo ; Aizawa, Koichi ; Suganuma, Hiroyuki ; Ara, Takeshi ; Sugawara, Tatsuya ; Shibata, Daisuke ; Matsumura, Yasuki ; Goto, Tsuyoshi ; Kawada, Teruo</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c613t-23c9ba3e09de39b06361a8643f8e1d8ebeb981401ca2242c350b5eb6a174777f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Adiponectin</topic><topic>Bioassays</topic><topic>Biology and Life Sciences</topic><topic>Ca2+/calmodulin-dependent protein kinase</topic><topic>Calcium influx</topic><topic>Calcium ions</topic><topic>Calcium-binding protein</topic><topic>Calmodulin</topic><topic>Carotene</topic><topic>Carotenoids</topic><topic>Chromatography</topic><topic>Diabetes</topic><topic>Food</topic><topic>Fractions</topic><topic>Glucose</topic><topic>Glucose metabolism</topic><topic>Insulin</topic><topic>Kinases</topic><topic>Liquid chromatography</topic><topic>Lycopene</topic><topic>Medicine and Health Sciences</topic><topic>Metabolic disorders</topic><topic>Metabolism</topic><topic>Metabolites</topic><topic>Molecular weight</topic><topic>Myotubes</topic><topic>Obesity</topic><topic>Penicillin</topic><topic>Phosphorylation</topic><topic>Physical Sciences</topic><topic>Proteins</topic><topic>Research and Analysis Methods</topic><topic>Signal transduction</topic><topic>Signaling</topic><topic>siRNA</topic><topic>Solanum lycopersicum</topic><topic>Solvents</topic><topic>Tomatoes</topic><topic>β-Carotene</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Mohri, 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Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Mohri, Shinsuke</au><au>Takahashi, Haruya</au><au>Sakai, Maiko</au><au>Waki, Naoko</au><au>Takahashi, Shingo</au><au>Aizawa, Koichi</au><au>Suganuma, Hiroyuki</au><au>Ara, Takeshi</au><au>Sugawara, Tatsuya</au><au>Shibata, Daisuke</au><au>Matsumura, Yasuki</au><au>Goto, Tsuyoshi</au><au>Kawada, Teruo</au><au>Wang, Chun-Hua</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Integration of bioassay and non-target metabolite analysis of tomato reveals that β-carotene and lycopene activate the adiponectin signaling pathway, including AMPK phosphorylation</atitle><jtitle>PloS one</jtitle><date>2022-07-01</date><risdate>2022</risdate><volume>17</volume><issue>7</issue><spage>e0267248</spage><epage>e0267248</epage><pages>e0267248-e0267248</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Adiponectin, an adipokine, regulates glucose metabolism and insulin sensitivity through the adiponectin receptor (AdipoR). In this study, we searched for metabolites that activate the adiponectin signaling pathway from tomato (
Solanum lycopersicu
). Metabolites of mature tomato were separated into 55 fractions by liquid chromatography, and then each fraction was examined using the phosphorylation assay of AMP-protein kinase (AMPK) in C2C12 myotubes and in AdipoR-knockdown cells by small interfering RNA (siRNA). Several fractions showed AMPK phosphorylation in C2C12 myotubes and siRNA-mediated abrogation of the effect. Non-targeted metabolite analysis revealed the presence of 721 diverse metabolites in tomato. By integrating the activity of fractions on AMPK phosphorylation and the 721 metabolites based on their retention times of liquid chromatography, we performed a comprehensive screen for metabolites that possess adiponectin-like activity. As the screening suggested that the active fractions contained four carotenoids, we further analyzed β-carotene and lycopene, the major carotenoids of food. They induced AMPK phosphorylation via the AdipoR, Ca
2+
/calmodulin-dependent protein kinase kinase and Ca
2+
influx, in addition to activating glucose uptake via AdipoR in C2C12 myotubes. All these events were characteristic adiponectin actions. These results indicated that the food-derived carotenoids, β-carotene and lycopene, activate the adiponectin signaling pathway, including AMPK phosphorylation.</abstract><cop>San Francisco</cop><pub>Public Library of Science</pub><pmid>35776737</pmid><doi>10.1371/journal.pone.0267248</doi><orcidid>https://orcid.org/0000-0002-9083-2913</orcidid><orcidid>https://orcid.org/0000-0003-3182-2894</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | PloS one, 2022-07, Vol.17 (7), p.e0267248-e0267248 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_2686271700 |
| source | DOAJ Directory of Open Access Journals; Public Library of Science (PLoS); EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Adiponectin Bioassays Biology and Life Sciences Ca2+/calmodulin-dependent protein kinase Calcium influx Calcium ions Calcium-binding protein Calmodulin Carotene Carotenoids Chromatography Diabetes Food Fractions Glucose Glucose metabolism Insulin Kinases Liquid chromatography Lycopene Medicine and Health Sciences Metabolic disorders Metabolism Metabolites Molecular weight Myotubes Obesity Penicillin Phosphorylation Physical Sciences Proteins Research and Analysis Methods Signal transduction Signaling siRNA Solanum lycopersicum Solvents Tomatoes β-Carotene |
| title | Integration of bioassay and non-target metabolite analysis of tomato reveals that β-carotene and lycopene activate the adiponectin signaling pathway, including AMPK phosphorylation |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-06T06%3A39%3A44IST&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=Integration%20of%20bioassay%20and%20non-target%20metabolite%20analysis%20of%20tomato%20reveals%20that%20%CE%B2-carotene%20and%20lycopene%20activate%20the%20adiponectin%20signaling%20pathway,%20including%20AMPK%20phosphorylation&rft.jtitle=PloS%20one&rft.au=Mohri,%20Shinsuke&rft.date=2022-07-01&rft.volume=17&rft.issue=7&rft.spage=e0267248&rft.epage=e0267248&rft.pages=e0267248-e0267248&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0267248&rft_dat=%3Cproquest_plos_%3E2684099001%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=2686271700&rft_id=info:pmid/35776737&rft_doaj_id=oai_doaj_org_article_25bed657e5ae4bbe9427179e1958fe54&rfr_iscdi=true |