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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| Published in | PloS one Vol. 17; no. 7; p. e0267248 |
|---|---|
| Main Authors | , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
San Francisco
Public Library of Science
01.07.2022
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1932-6203 1932-6203 |
| DOI | 10.1371/journal.pone.0267248 |
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| 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. |
|---|---|
| AbstractList | 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. 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, Ca2+/calmodulin-dependent protein kinase kinase and Ca2+ 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.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, Ca2+/calmodulin-dependent protein kinase kinase and Ca2+ 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. 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, Ca2+/calmodulin-dependent protein kinase kinase and Ca2+ 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. 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. |
| Author | Takahashi, Haruya Goto, Tsuyoshi Suganuma, Hiroyuki Matsumura, Yasuki Waki, Naoko Sugawara, Tatsuya Shibata, Daisuke Mohri, Shinsuke Sakai, Maiko Kawada, Teruo Aizawa, Koichi Takahashi, Shingo Ara, Takeshi |
| AuthorAffiliation | 3 KAGOME Tomato Discoveries Laboratory, Graduate School of Agriculture, Kyoto University, Kyoto, Japan 2 Laboratory of Technology of Marine Bioproducts, Graduate School of Agriculture, Kyoto University, Kyoto, Japan 4 Innovation Division, KAGOME CO., LTD., Tochigi, Japan 7 Research Unit for Physiological Chemistry, Kyoto University, Kyoto, Japan 1 Laboratory of Molecular Function of Food, Graduate School of Agriculture, Kyoto University, Kyoto, Japan 6 Laboratory of Quality Analysis and Assessment, Graduate School of Agriculture, Kyoto University, Kyoto, Japan 5 Kazusa DNA Research Institutes, Kazusa-Kamatari, Chiba, Japan Foshan University, CHINA |
| AuthorAffiliation_xml | – name: 4 Innovation Division, KAGOME CO., LTD., Tochigi, Japan – name: 3 KAGOME Tomato Discoveries Laboratory, Graduate School of Agriculture, Kyoto University, Kyoto, Japan – name: 2 Laboratory of Technology of Marine Bioproducts, Graduate School of Agriculture, Kyoto University, Kyoto, Japan – name: 5 Kazusa DNA Research Institutes, Kazusa-Kamatari, Chiba, Japan – name: 1 Laboratory of Molecular Function of Food, Graduate School of Agriculture, Kyoto University, Kyoto, Japan – name: Foshan University, CHINA – name: 7 Research Unit for Physiological Chemistry, Kyoto University, Kyoto, Japan – name: 6 Laboratory of Quality Analysis and Assessment, Graduate School of Agriculture, Kyoto University, Kyoto, Japan |
| Author_xml | – sequence: 1 givenname: Shinsuke orcidid: 0000-0002-9083-2913 surname: Mohri fullname: Mohri, Shinsuke – sequence: 2 givenname: Haruya orcidid: 0000-0003-3182-2894 surname: Takahashi fullname: Takahashi, Haruya – sequence: 3 givenname: Maiko surname: Sakai fullname: Sakai, Maiko – sequence: 4 givenname: Naoko surname: Waki fullname: Waki, Naoko – sequence: 5 givenname: Shingo surname: Takahashi fullname: Takahashi, Shingo – sequence: 6 givenname: Koichi surname: Aizawa fullname: Aizawa, Koichi – sequence: 7 givenname: Hiroyuki surname: Suganuma fullname: Suganuma, Hiroyuki – sequence: 8 givenname: Takeshi surname: Ara fullname: Ara, Takeshi – sequence: 9 givenname: Tatsuya surname: Sugawara fullname: Sugawara, Tatsuya – sequence: 10 givenname: Daisuke surname: Shibata fullname: Shibata, Daisuke – sequence: 11 givenname: Yasuki surname: Matsumura fullname: Matsumura, Yasuki – sequence: 12 givenname: Tsuyoshi surname: Goto fullname: Goto, Tsuyoshi – sequence: 13 givenname: Teruo surname: Kawada fullname: Kawada, Teruo |
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| CitedBy_id | crossref_primary_10_3390_metabo13090979 crossref_primary_10_5995_jis_25_2_111 crossref_primary_10_3390_nu16193269 crossref_primary_10_1093_bbb_zbae182 crossref_primary_10_3390_nu17030411 crossref_primary_10_1016_j_plaphy_2024_108589 |
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| Copyright | 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. 2022 Mohri et al 2022 Mohri et al |
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| SubjectTerms | 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 |
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| 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 |
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