PPAR-alpha dependent regulation of vanin-1 mediates hepatic lipid metabolism
Peroxisome proliferator-activated receptor alpha (PPARα) is a key regulator of hepatic fat oxidation that serves as an energy source during starvation. Vanin-1 has been described as a putative PPARα target gene in liver, but its function in hepatic lipid metabolism is unknown. We investigated the re...
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| Published in | Journal of hepatology Vol. 61; no. 2; pp. 366 - 372 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Netherlands
Elsevier B.V
01.08.2014
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| Subjects | |
| Online Access | Get full text |
| ISSN | 0168-8278 1600-0641 1600-0641 |
| DOI | 10.1016/j.jhep.2014.04.013 |
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| Abstract | Peroxisome proliferator-activated receptor alpha (PPARα) is a key regulator of hepatic fat oxidation that serves as an energy source during starvation. Vanin-1 has been described as a putative PPARα target gene in liver, but its function in hepatic lipid metabolism is unknown.
We investigated the regulation of vanin-1, and total vanin activity, by PPARα in mice and humans. Furthermore, the function of vanin-1 in the development of hepatic steatosis in response to starvation was examined in Vnn1 deficient mice, and in rats treated with an inhibitor of vanin activity.
Liver microarray analyses reveals that Vnn1 is the most prominently regulated gene after modulation of PPARα activity. In addition, activation of mouse PPARα regulates hepatic- and plasma vanin activity. In humans, consistent with regulation by PPARα, plasma vanin activity increases in all subjects after prolonged fasting, as well as after treatment with the PPARα agonist fenofibrate. In mice, absence of vanin-1 exacerbates the fasting-induced increase in hepatic triglyceride levels. Similarly, inhibition of vanin activity in rats induces accumulation of hepatic triglycerides upon fasting. Microarray analysis reveal that the absence of vanin-1 associates with gene sets involved in liver steatosis, and reduces pathways involved in oxidative stress and inflammation.
We show that hepatic vanin-1 is under extremely sensitive regulation by PPARα and that plasma vanin activity could serve as a readout of changes in PPARα activity in human subjects. In addition, our data propose a role for vanin-1 in regulation of hepatic TG levels during fasting. |
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| AbstractList | Background & Aims Peroxisome proliferator-activated receptor alpha (PPARα) is a key regulator of hepatic fat oxidation that serves as an energy source during starvation. Vanin-1 has been described as a putative PPARα target gene in liver, but its function in hepatic lipid metabolism is unknown. Methods We investigated the regulation of vanin-1, and total vanin activity, by PPARα in mice and humans. Furthermore, the function of vanin-1 in the development of hepatic steatosis in response to starvation was examined in Vnn1 deficient mice, and in rats treated with an inhibitor of vanin activity. Results Liver microarray analyses reveals that Vnn1 is the most prominently regulated gene after modulation of PPARα activity. In addition, activation of mouse PPARα regulates hepatic- and plasma vanin activity. In humans, consistent with regulation by PPARα, plasma vanin activity increases in all subjects after prolonged fasting, as well as after treatment with the PPARα agonist fenofibrate. In mice, absence of vanin-1 exacerbates the fasting-induced increase in hepatic triglyceride levels. Similarly, inhibition of vanin activity in rats induces accumulation of hepatic triglycerides upon fasting. Microarray analysis reveal that the absence of vanin-1 associates with gene sets involved in liver steatosis, and reduces pathways involved in oxidative stress and inflammation. Conclusions We show that hepatic vanin-1 is under extremely sensitive regulation by PPARα and that plasma vanin activity could serve as a readout of changes in PPARα activity in human subjects. In addition, our data propose a role for vanin-1 in regulation of hepatic TG levels during fasting. Background & Aims Peroxisome proliferator-activated receptor alpha (PPARa) is a key regulator of hepatic fat oxidation that serves as an energy source during starvation. Vanin-1 has been described as a putative PPARa target gene in liver, but its function in hepatic lipid metabolism is unknown. Methods We investigated the regulation of vanin-1, and total vanin activity, by PPARa in mice and humans. Furthermore, the function of vanin-1 in the development of hepatic steatosis in response to starvation was examined in Vnn1 deficient mice, and in rats treated with an inhibitor of vanin activity. Results Liver microarray analyses reveals that Vnn1 is the most prominently regulated gene after modulation of PPARa activity. In addition, activation of mouse PPARa regulates hepatic- and plasma vanin activity. In humans, consistent with regulation by PPARa, plasma vanin activity increases in all subjects after prolonged fasting, as well as after treatment with the PPARa agonist fenofibrate. In mice, absence of vanin-1 exacerbates the fasting-induced increase in hepatic triglyceride levels. Similarly, inhibition of vanin activity in rats induces accumulation of hepatic triglycerides upon fasting. Microarray analysis reveal that the absence of vanin-1 associates with gene sets involved in liver steatosis, and reduces pathways involved in oxidative stress and inflammation. Conclusions We show that hepatic vanin-1 is under extremely sensitive regulation by PPARa and that plasma vanin activity could serve as a readout of changes in PPARa activity in human subjects. In addition, our data propose a role for vanin-1 in regulation of hepatic TG levels during fasting. Abbreviations PPAR, Peroxisome proliferator-activated receptor; RXR, Retinoid X Receptor; VNN1, vanin-1; VNN2, vanin-2; VNN3, vanin-3; WT, wild-type; BMI, body mass index; Pan-AMC, pantothenate-7-amino-4-methylcoumarin; TG, Triglycerides; TC, total cholesterol; FFA, free fatty acids; KLF15, Kruppel-like factor 15; STAT3, signal transducer and activator of transcription 3; SP1, trans-acting transcription factor 1; CBFB, core binding factor beta; XBP1, x-box binding protein 1; NAFLD, non-alcoholic fatty liver disease; Pan-PNa, pantothenate-4-nitroanilide; Abcd2, chemokine (C-C motif) ligand 17; Acadm, acyl-CoA dehydrogenase, medium chain; Acot1, acyl-CoA thioesterase 1; Acot2, acyl-CoA thioesterase 2; Acsl5, acyl-CoA synthetase long-chain family member 5; Ehhadh, enoyl-CoA hydratase/3-hydroxylacyl CoA dehydrogenase; NASH, non-alcoholic steatohepatitis (NASH) Peroxisome proliferator-activated receptor alpha (PPARα) is a key regulator of hepatic fat oxidation that serves as an energy source during starvation. Vanin-1 has been described as a putative PPARα target gene in liver, but its function in hepatic lipid metabolism is unknown. We investigated the regulation of vanin-1, and total vanin activity, by PPARα in mice and humans. Furthermore, the function of vanin-1 in the development of hepatic steatosis in response to starvation was examined in Vnn1 deficient mice, and in rats treated with an inhibitor of vanin activity. Liver microarray analyses reveals that Vnn1 is the most prominently regulated gene after modulation of PPARα activity. In addition, activation of mouse PPARα regulates hepatic- and plasma vanin activity. In humans, consistent with regulation by PPARα, plasma vanin activity increases in all subjects after prolonged fasting, as well as after treatment with the PPARα agonist fenofibrate. In mice, absence of vanin-1 exacerbates the fasting-induced increase in hepatic triglyceride levels. Similarly, inhibition of vanin activity in rats induces accumulation of hepatic triglycerides upon fasting. Microarray analysis reveal that the absence of vanin-1 associates with gene sets involved in liver steatosis, and reduces pathways involved in oxidative stress and inflammation. We show that hepatic vanin-1 is under extremely sensitive regulation by PPARα and that plasma vanin activity could serve as a readout of changes in PPARα activity in human subjects. In addition, our data propose a role for vanin-1 in regulation of hepatic TG levels during fasting. Peroxisome proliferator-activated receptor alpha (PPARα) is a key regulator of hepatic fat oxidation that serves as an energy source during starvation. Vanin-1 has been described as a putative PPARα target gene in liver, but its function in hepatic lipid metabolism is unknown.BACKGROUND & AIMSPeroxisome proliferator-activated receptor alpha (PPARα) is a key regulator of hepatic fat oxidation that serves as an energy source during starvation. Vanin-1 has been described as a putative PPARα target gene in liver, but its function in hepatic lipid metabolism is unknown.We investigated the regulation of vanin-1, and total vanin activity, by PPARα in mice and humans. Furthermore, the function of vanin-1 in the development of hepatic steatosis in response to starvation was examined in Vnn1 deficient mice, and in rats treated with an inhibitor of vanin activity.METHODSWe investigated the regulation of vanin-1, and total vanin activity, by PPARα in mice and humans. Furthermore, the function of vanin-1 in the development of hepatic steatosis in response to starvation was examined in Vnn1 deficient mice, and in rats treated with an inhibitor of vanin activity.Liver microarray analyses reveals that Vnn1 is the most prominently regulated gene after modulation of PPARα activity. In addition, activation of mouse PPARα regulates hepatic- and plasma vanin activity. In humans, consistent with regulation by PPARα, plasma vanin activity increases in all subjects after prolonged fasting, as well as after treatment with the PPARα agonist fenofibrate. In mice, absence of vanin-1 exacerbates the fasting-induced increase in hepatic triglyceride levels. Similarly, inhibition of vanin activity in rats induces accumulation of hepatic triglycerides upon fasting. Microarray analysis reveal that the absence of vanin-1 associates with gene sets involved in liver steatosis, and reduces pathways involved in oxidative stress and inflammation.RESULTSLiver microarray analyses reveals that Vnn1 is the most prominently regulated gene after modulation of PPARα activity. In addition, activation of mouse PPARα regulates hepatic- and plasma vanin activity. In humans, consistent with regulation by PPARα, plasma vanin activity increases in all subjects after prolonged fasting, as well as after treatment with the PPARα agonist fenofibrate. In mice, absence of vanin-1 exacerbates the fasting-induced increase in hepatic triglyceride levels. Similarly, inhibition of vanin activity in rats induces accumulation of hepatic triglycerides upon fasting. Microarray analysis reveal that the absence of vanin-1 associates with gene sets involved in liver steatosis, and reduces pathways involved in oxidative stress and inflammation.We show that hepatic vanin-1 is under extremely sensitive regulation by PPARα and that plasma vanin activity could serve as a readout of changes in PPARα activity in human subjects. In addition, our data propose a role for vanin-1 in regulation of hepatic TG levels during fasting.CONCLUSIONSWe show that hepatic vanin-1 is under extremely sensitive regulation by PPARα and that plasma vanin activity could serve as a readout of changes in PPARα activity in human subjects. In addition, our data propose a role for vanin-1 in regulation of hepatic TG levels during fasting. |
| Author | Hooiveld, Guido J. van Diepen, Janna A. Galland, Franck Naquet, Philippe Schrauwen, Patrick Netea, Mihai G. Rutjes, Floris P.J.T. Tack, Cees J. Jansen, Patrick A. Hijmans, Anneke Schalkwijk, Joost Rommelaere, Samuel Stienstra, Rinke Ballak, Dov B. Mensink, Ronald P. Kersten, Sander |
| Author_xml | – sequence: 1 givenname: Janna A. surname: van Diepen fullname: van Diepen, Janna A. email: Janna.vanDiepen@radboudumc.nl organization: Department of Medicine, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands – sequence: 2 givenname: Patrick A. surname: Jansen fullname: Jansen, Patrick A. organization: Nijmegen Center for Molecular Life Sciences, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands – sequence: 3 givenname: Dov B. surname: Ballak fullname: Ballak, Dov B. organization: Department of Medicine, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands – sequence: 4 givenname: Anneke surname: Hijmans fullname: Hijmans, Anneke organization: Department of Medicine, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands – sequence: 5 givenname: Guido J. surname: Hooiveld fullname: Hooiveld, Guido J. organization: Nutrition, Metabolism and Genomics Group, Division of Human Nutrition, Wageningen University, Wageningen, The Netherlands – sequence: 6 givenname: Samuel surname: Rommelaere fullname: Rommelaere, Samuel organization: Centre d’Immunologie de Marseille-Luminy (CIML), Aix-Marseille University, UM2, Marseille, France – sequence: 7 givenname: Franck surname: Galland fullname: Galland, Franck organization: Centre d’Immunologie de Marseille-Luminy (CIML), Aix-Marseille University, UM2, Marseille, France – sequence: 8 givenname: Philippe surname: Naquet fullname: Naquet, Philippe organization: Centre d’Immunologie de Marseille-Luminy (CIML), Aix-Marseille University, UM2, Marseille, France – sequence: 9 givenname: Floris P.J.T. surname: Rutjes fullname: Rutjes, Floris P.J.T. organization: Department of Synthetic Organic Chemistry, Institute for Molecules and Materials, Radboud University Nijmegen, The Netherlands – sequence: 10 givenname: Ronald P. surname: Mensink fullname: Mensink, Ronald P. organization: Department of Human Biology, NUTRIM School for Nutrition, Toxicology and Metabolism, Maastricht University Medical Center, Maastricht, The Netherlands – sequence: 11 givenname: Patrick surname: Schrauwen fullname: Schrauwen, Patrick organization: Department of Human Biology, NUTRIM School for Nutrition, Toxicology and Metabolism, Maastricht University Medical Center, Maastricht, The Netherlands – sequence: 12 givenname: Cees J. surname: Tack fullname: Tack, Cees J. organization: Department of Medicine, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands – sequence: 13 givenname: Mihai G. surname: Netea fullname: Netea, Mihai G. organization: Department of Medicine, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands – sequence: 14 givenname: Sander surname: Kersten fullname: Kersten, Sander organization: Nutrition, Metabolism and Genomics Group, Division of Human Nutrition, Wageningen University, Wageningen, The Netherlands – sequence: 15 givenname: Joost surname: Schalkwijk fullname: Schalkwijk, Joost organization: Nijmegen Center for Molecular Life Sciences, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands – sequence: 16 givenname: Rinke surname: Stienstra fullname: Stienstra, Rinke organization: Department of Medicine, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24751833$$D View this record in MEDLINE/PubMed |
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| Copyright | 2014 European Association for the Study of the Liver European Association for the Study of the Liver Copyright © 2014 European Association for the Study of the Liver. Published by Elsevier B.V. All rights reserved. Wageningen University & Research |
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| Keywords | FFA Vanin NAFLD CBFB RXR Pan-PNa Abcd2 PPAR Pan-AMC WT BMI XBP1 Fasting STAT3 Acot1 Ehhadh Acot2 Acadm NASH Triglyceride KLF15 Lipid TC Steatosis Fenofibrate Peroxisome proliferator-activated receptor alpha α VNN1 TG VNN2 VNN3 SP1 Acsl5 Pantetheinase non-alcoholic steatohepatitis (NASH) total cholesterol x-box binding protein 1 Peroxisome proliferator-activated receptor enoyl-CoA hydratase/3-hydroxylacyl CoA dehydrogenase body mass index Retinoid X Receptor Kruppel-like factor 15 core binding factor beta non-alcoholic fatty liver disease chemokine (C-C motif) ligand 17 vanin-1 vanin-2 vanin-3 free fatty acids acyl-CoA thioesterase 1 acyl-CoA synthetase long-chain family member 5 acyl-CoA thioesterase 2 trans-acting transcription factor 1 pantothenate-7-amino-4-methylcoumarin Triglycerides signal transducer and activator of transcription 3 acyl-CoA dehydrogenase, medium chain pantothenate-4-nitroanilide wild-type |
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| Snippet | Peroxisome proliferator-activated receptor alpha (PPARα) is a key regulator of hepatic fat oxidation that serves as an energy source during starvation. Vanin-1... Background & Aims Peroxisome proliferator-activated receptor alpha (PPARα) is a key regulator of hepatic fat oxidation that serves as an energy source during... Background & Aims Peroxisome proliferator-activated receptor alpha (PPARa) is a key regulator of hepatic fat oxidation that serves as an energy source during... |
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| SubjectTerms | acids Amidohydrolases - physiology Animals cysteamine Fasting Fatty Liver - etiology Fenofibrate Gastroenterology and Hepatology gene-expression GPI-Linked Proteins - physiology hepatocytes high-fat diet Humans insulin-resistance Lipid Lipid Metabolism liver Liver - metabolism Male Mice Mice, Inbred C57BL null mice Pantetheinase Peroxisome proliferator-activated receptor alpha α PPAR PPAR alpha - physiology Rats Rats, Wistar Starvation - metabolism Steatosis tissue Triglyceride Vanin |
| Title | PPAR-alpha dependent regulation of vanin-1 mediates hepatic lipid metabolism |
| URI | https://www.clinicalkey.com/#!/content/1-s2.0-S0168827814002669 https://www.clinicalkey.es/playcontent/1-s2.0-S0168827814002669 https://dx.doi.org/10.1016/j.jhep.2014.04.013 https://www.ncbi.nlm.nih.gov/pubmed/24751833 https://www.proquest.com/docview/1546217123 http://www.narcis.nl/publication/RecordID/oai:library.wur.nl:wurpubs%2F478628 |
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