Partial Inhibition of Adipose Tissue Lipolysis Improves Glucose Metabolism and Insulin Sensitivity Without Alteration of Fat Mass
When energy is needed, white adipose tissue (WAT) provides fatty acids (FAs) for use in peripheral tissues via stimulation of fat cell lipolysis. FAs have been postulated to play a critical role in the development of obesity-induced insulin resistance, a major risk factor for diabetes and cardiovasc...
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| Published in | PLoS biology Vol. 11; no. 2; p. e1001485 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
01.02.2013
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1545-7885 1544-9173 1545-7885 |
| DOI | 10.1371/journal.pbio.1001485 |
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| Abstract | When energy is needed, white adipose tissue (WAT) provides fatty acids (FAs) for use in peripheral tissues via stimulation of fat cell lipolysis. FAs have been postulated to play a critical role in the development of obesity-induced insulin resistance, a major risk factor for diabetes and cardiovascular disease. However, whether and how chronic inhibition of fat mobilization from WAT modulates insulin sensitivity remains elusive. Hormone-sensitive lipase (HSL) participates in the breakdown of WAT triacylglycerol into FAs. HSL haploinsufficiency and treatment with a HSL inhibitor resulted in improvement of insulin tolerance without impact on body weight, fat mass, and WAT inflammation in high-fat-diet-fed mice. In vivo palmitate turnover analysis revealed that blunted lipolytic capacity is associated with diminution in FA uptake and storage in peripheral tissues of obese HSL haploinsufficient mice. The reduction in FA turnover was accompanied by an improvement of glucose metabolism with a shift in respiratory quotient, increase of glucose uptake in WAT and skeletal muscle, and enhancement of de novo lipogenesis and insulin signalling in liver. In human adipocytes, HSL gene silencing led to improved insulin-stimulated glucose uptake, resulting in increased de novo lipogenesis and activation of cognate gene expression. In clinical studies, WAT lipolytic rate was positively and negatively correlated with indexes of insulin resistance and WAT de novo lipogenesis gene expression, respectively. In obese individuals, chronic inhibition of lipolysis resulted in induction of WAT de novo lipogenesis gene expression. Thus, reduction in WAT lipolysis reshapes FA fluxes without increase of fat mass and improves glucose metabolism through cell-autonomous induction of fat cell de novo lipogenesis, which contributes to improved insulin sensitivity. |
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| AbstractList | Partial inhibition of adipose tissue lipolysis does not increase fat mass but improves glucose metabolism and insulin sensitivity through modulation of fatty acid turnover and induction of fat cell de novo lipogenesis.
When energy is needed, white adipose tissue (WAT) provides fatty acids (FAs) for use in peripheral tissues via stimulation of fat cell lipolysis. FAs have been postulated to play a critical role in the development of obesity-induced insulin resistance, a major risk factor for diabetes and cardiovascular disease. However, whether and how chronic inhibition of fat mobilization from WAT modulates insulin sensitivity remains elusive. Hormone-sensitive lipase (HSL) participates in the breakdown of WAT triacylglycerol into FAs. HSL haploinsufficiency and treatment with a HSL inhibitor resulted in improvement of insulin tolerance without impact on body weight, fat mass, and WAT inflammation in high-fat-diet–fed mice. In vivo palmitate turnover analysis revealed that blunted lipolytic capacity is associated with diminution in FA uptake and storage in peripheral tissues of obese HSL haploinsufficient mice. The reduction in FA turnover was accompanied by an improvement of glucose metabolism with a shift in respiratory quotient, increase of glucose uptake in WAT and skeletal muscle, and enhancement of de novo lipogenesis and insulin signalling in liver. In human adipocytes, HSL gene silencing led to improved insulin-stimulated glucose uptake, resulting in increased de novo lipogenesis and activation of cognate gene expression. In clinical studies, WAT lipolytic rate was positively and negatively correlated with indexes of insulin resistance and WAT de novo lipogenesis gene expression, respectively. In obese individuals, chronic inhibition of lipolysis resulted in induction of WAT de novo lipogenesis gene expression. Thus, reduction in WAT lipolysis reshapes FA fluxes without increase of fat mass and improves glucose metabolism through cell-autonomous induction of fat cell de novo lipogenesis, which contributes to improved insulin sensitivity.
In periods of energy demand, mobilization of fat stores in mammals (i.e., adipose tissue lipolysis) is essential to provide energy in the form of fatty acids. In excess, however, fatty acids induce resistance to the action of insulin, which serves to regulate glucose metabolism in skeletal muscle and liver. Insulin resistance (or low insulin sensitivity) is believed to be a cornerstone of the complications of obesity such as type 2 diabetes and cardiovascular diseases. In this study, our clinical observation of natural variation in fat cell lipolysis in individuals reveals that a high lipolytic rate is associated with low insulin sensitivity. Furthermore, partial genetic and pharmacologic inhibition of hormone-sensitive lipase, one of the enzymes involved in the breakdown of white adipose tissue lipids, results in improvement of insulin sensitivity in mice without gain in body weight and fat mass. We undertake a series of mechanistic studies in mice and in human fat cells to show that blunted lipolytic capacity increases the synthesis of new fatty acids from glucose in fat cells, a pathway that has recently been shown by others to be a major determinant of whole body insulin sensitivity. In conclusion, partial inhibition of adipose tissue lipolysis is a plausible strategy in the treatment of obesity-related insulin resistance. When energy is needed, white adipose tissue (WAT) provides fatty acids (FAs) for use in peripheral tissues via stimulation of fat cell lipolysis. FAs have been postulated to play a critical role in the development of obesity-induced insulin resistance, a major risk factor for diabetes and cardiovascular disease. However, whether and how chronic inhibition of fat mobilization from WAT modulates insulin sensitivity remains elusive. Hormone-sensitive lipase (HSL) participates in the breakdown of WAT triacylglycerol into FAs. HSL haploinsufficiency and treatment with a HSL inhibitor resulted in improvement of insulin tolerance without impact on body weight, fat mass, and WAT inflammation in high-fat-diet-fed mice. In vivo palmitate turnover analysis revealed that blunted lipolytic capacity is associated with diminution in FA uptake and storage in peripheral tissues of obese HSL haploinsufficient mice. The reduction in FA turnover was accompanied by an improvement of glucose metabolism with a shift in respiratory quotient, increase of glucose uptake in WAT and skeletal muscle, and enhancement of de novo lipogenesis and insulin signalling in liver. In human adipocytes, HSL gene silencing led to improved insulin-stimulated glucose uptake, resulting in increased de novo lipogenesis and activation of cognate gene expression. In clinical studies, WAT lipolytic rate was positively and negatively correlated with indexes of insulin resistance and WAT de novo lipogenesis gene expression, respectively. In obese individuals, chronic inhibition of lipolysis resulted in induction of WAT de novo lipogenesis gene expression. Thus, reduction in WAT lipolysis reshapes FA fluxes without increase of fat mass and improves glucose metabolism through cell-autonomous induction of fat cell de novo lipogenesis, which contributes to improved insulin sensitivity. When energy is needed, white adipose tissue (WAT) provides fatty acids (FAs) for use in peripheral tissues via stimulation of fat cell lipolysis. FAs have been postulated to play a critical role in the development of obesity-induced insulin resistance, a major risk factor for diabetes and cardiovascular disease. However, whether and how chronic inhibition of fat mobilization from WAT modulates insulin sensitivity remains elusive. Hormone-sensitive lipase (HSL) participates in the breakdown of WAT triacylglycerol into FAs. HSL haploinsufficiency and treatment with a HSL inhibitor resulted in improvement of insulin tolerance without impact on body weight, fat mass, and WAT inflammation in high-fat-diet-fed mice. In vivo palmitate turnover analysis revealed that blunted lipolytic capacity is associated with diminution in FA uptake and storage in peripheral tissues of obese HSL haploinsufficient mice. The reduction in FA turnover was accompanied by an improvement of glucose metabolism with a shift in respiratory quotient, increase of glucose uptake in WAT and skeletal muscle, and enhancement of de novo lipogenesis and insulin signalling in liver. In human adipocytes, HSL gene silencing led to improved insulin-stimulated glucose uptake, resulting in increased de novo lipogenesis and activation of cognate gene expression. In clinical studies, WAT lipolytic rate was positively and negatively correlated with indexes of insulin resistance and WAT de novo lipogenesis gene expression, respectively. In obese individuals, chronic inhibition of lipolysis resulted in induction of WAT de novo lipogenesis gene expression. Thus, reduction in WAT lipolysis reshapes FA fluxes without increase of fat mass and improves glucose metabolism through cell-autonomous induction of fat cell de novo lipogenesis, which contributes to improved insulin sensitivity. When energy is needed, white adipose tissue (WAT) provides fatty acids (FAs) for use in peripheral tissues via stimulation of fat cell lipolysis. FAs have been postulated to play a critical role in the development of obesity-induced insulin resistance, a major risk factor for diabetes and cardiovascular disease. However, whether and how chronic inhibition of fat mobilization from WAT modulates insulin sensitivity remains elusive. Hormone-sensitive lipase (HSL) participates in the breakdown of WAT triacylglycerol into FAs. HSL haploinsufficiency and treatment with a HSL inhibitor resulted in improvement of insulin tolerance without impact on body weight, fat mass, and WAT inflammation in high-fat-diet-fed mice. In vivo palmitate turnover analysis revealed that blunted lipolytic capacity is associated with diminution in FA uptake and storage in peripheral tissues of obese HSL haploinsufficient mice. The reduction in FA turnover was accompanied by an improvement of glucose metabolism with a shift in respiratory quotient, increase of glucose uptake in WAT and skeletal muscle, and enhancement of de novo lipogenesis and insulin signalling in liver. In human adipocytes, HSL gene silencing led to improved insulin-stimulated glucose uptake, resulting in increased de novo lipogenesis and activation of cognate gene expression. In clinical studies, WAT lipolytic rate was positively and negatively correlated with indexes of insulin resistance and WAT de novo lipogenesis gene expression, respectively. In obese individuals, chronic inhibition of lipolysis resulted in induction of WAT de novo lipogenesis gene expression. Thus, reduction in WAT lipolysis reshapes FA fluxes without increase of fat mass and improves glucose metabolism through cell-autonomous induction of fat cell de novo lipogenesis, which contributes to improved insulin sensitivity.When energy is needed, white adipose tissue (WAT) provides fatty acids (FAs) for use in peripheral tissues via stimulation of fat cell lipolysis. FAs have been postulated to play a critical role in the development of obesity-induced insulin resistance, a major risk factor for diabetes and cardiovascular disease. However, whether and how chronic inhibition of fat mobilization from WAT modulates insulin sensitivity remains elusive. Hormone-sensitive lipase (HSL) participates in the breakdown of WAT triacylglycerol into FAs. HSL haploinsufficiency and treatment with a HSL inhibitor resulted in improvement of insulin tolerance without impact on body weight, fat mass, and WAT inflammation in high-fat-diet-fed mice. In vivo palmitate turnover analysis revealed that blunted lipolytic capacity is associated with diminution in FA uptake and storage in peripheral tissues of obese HSL haploinsufficient mice. The reduction in FA turnover was accompanied by an improvement of glucose metabolism with a shift in respiratory quotient, increase of glucose uptake in WAT and skeletal muscle, and enhancement of de novo lipogenesis and insulin signalling in liver. In human adipocytes, HSL gene silencing led to improved insulin-stimulated glucose uptake, resulting in increased de novo lipogenesis and activation of cognate gene expression. In clinical studies, WAT lipolytic rate was positively and negatively correlated with indexes of insulin resistance and WAT de novo lipogenesis gene expression, respectively. In obese individuals, chronic inhibition of lipolysis resulted in induction of WAT de novo lipogenesis gene expression. Thus, reduction in WAT lipolysis reshapes FA fluxes without increase of fat mass and improves glucose metabolism through cell-autonomous induction of fat cell de novo lipogenesis, which contributes to improved insulin sensitivity. |
| Audience | Academic |
| Author | Louche, Katie Besse-Patin, Aurèle Vila, Isabelle Marques, Marie-Adeline Dinel, Anne-Laure Arner, Peter Girousse, Amandine Monbrun, Laurent Holm, Cecilia Waget, Aurélie Caspar-Bauguil, Sylvie Galitzky, Jean Sulpice, Thierry Houssier, Marianne Burcelin, Rémy Moro, Cedric Roussel, Balbine Bézaire, Véronic Mir, Lucile Combes, Marion Mairal, Aline Mouisel, Etienne Tavernier, Geneviève Langin, Dominique Thalamas, Claire Mejhert, Niklas Renoud, Marie-Laure Viguerie, Nathalie Valle, Carine Prunet-Marcassus, Bénédicte |
| AuthorAffiliation | 7 INSERM, UMR1048, Team 1, I2MC, Institute of Metabolic and Cardiovascular Diseases, Toulouse, France 5 INSERM, UMR1048,Team 2, I2MC, Institute of Metabolic and Cardiovascular Diseases, Toulouse, France 4 Physiogenex, Prologue Biotech, Labège-Innopole, France 8 Department of Experimental Medical Science, Lund University, Lund, Sweden 9 Toulouse University Hospitals, INSERM, Clinical Investigation Center, Toulouse, France University of Cambridge, United Kingdom 3 Department of Medicine, Karolinska Institute at Karolinska Hospital, Huddinge, Stockholm, Sweden 6 Toulouse University Hospitals, Laboratory of Clinical Biochemistry, Toulouse, France 1 INSERM, UMR1048, Obesity Research Laboratory, Institute of Metabolic and Cardiovascular Diseases, Toulouse, France 2 University of Toulouse, UMR1048, Paul Sabatier University, France |
| AuthorAffiliation_xml | – name: 3 Department of Medicine, Karolinska Institute at Karolinska Hospital, Huddinge, Stockholm, Sweden – name: 5 INSERM, UMR1048,Team 2, I2MC, Institute of Metabolic and Cardiovascular Diseases, Toulouse, France – name: University of Cambridge, United Kingdom – name: 8 Department of Experimental Medical Science, Lund University, Lund, Sweden – name: 4 Physiogenex, Prologue Biotech, Labège-Innopole, France – name: 1 INSERM, UMR1048, Obesity Research Laboratory, Institute of Metabolic and Cardiovascular Diseases, Toulouse, France – name: 7 INSERM, UMR1048, Team 1, I2MC, Institute of Metabolic and Cardiovascular Diseases, Toulouse, France – name: 9 Toulouse University Hospitals, INSERM, Clinical Investigation Center, Toulouse, France – name: 2 University of Toulouse, UMR1048, Paul Sabatier University, France – name: 6 Toulouse University Hospitals, Laboratory of Clinical Biochemistry, Toulouse, France |
| Author_xml | – sequence: 1 givenname: Amandine surname: Girousse fullname: Girousse, Amandine – sequence: 2 givenname: Geneviève surname: Tavernier fullname: Tavernier, Geneviève – sequence: 3 givenname: Carine surname: Valle fullname: Valle, Carine – sequence: 4 givenname: Cedric surname: Moro fullname: Moro, Cedric – sequence: 5 givenname: Niklas surname: Mejhert fullname: Mejhert, Niklas – sequence: 6 givenname: Anne-Laure surname: Dinel fullname: Dinel, Anne-Laure – sequence: 7 givenname: Marianne surname: Houssier fullname: Houssier, Marianne – sequence: 8 givenname: Balbine surname: Roussel fullname: Roussel, Balbine – sequence: 9 givenname: Aurèle surname: Besse-Patin fullname: Besse-Patin, Aurèle – sequence: 10 givenname: Marion surname: Combes fullname: Combes, Marion – sequence: 11 givenname: Lucile surname: Mir fullname: Mir, Lucile – sequence: 12 givenname: Laurent surname: Monbrun fullname: Monbrun, Laurent – sequence: 13 givenname: Véronic surname: Bézaire fullname: Bézaire, Véronic – sequence: 14 givenname: Bénédicte surname: Prunet-Marcassus fullname: Prunet-Marcassus, Bénédicte – sequence: 15 givenname: Aurélie surname: Waget fullname: Waget, Aurélie – sequence: 16 givenname: Isabelle surname: Vila fullname: Vila, Isabelle – sequence: 17 givenname: Sylvie surname: Caspar-Bauguil fullname: Caspar-Bauguil, Sylvie – sequence: 18 givenname: Katie surname: Louche fullname: Louche, Katie – sequence: 19 givenname: Marie-Adeline surname: Marques fullname: Marques, Marie-Adeline – sequence: 20 givenname: Aline surname: Mairal fullname: Mairal, Aline – sequence: 21 givenname: Marie-Laure surname: Renoud fullname: Renoud, Marie-Laure – sequence: 22 givenname: Jean surname: Galitzky fullname: Galitzky, Jean – sequence: 23 givenname: Cecilia surname: Holm fullname: Holm, Cecilia – sequence: 24 givenname: Etienne surname: Mouisel fullname: Mouisel, Etienne – sequence: 25 givenname: Claire surname: Thalamas fullname: Thalamas, Claire – sequence: 26 givenname: Nathalie surname: Viguerie fullname: Viguerie, Nathalie – sequence: 27 givenname: Thierry surname: Sulpice fullname: Sulpice, Thierry – sequence: 28 givenname: Rémy surname: Burcelin fullname: Burcelin, Rémy – sequence: 29 givenname: Peter surname: Arner fullname: Arner, Peter – sequence: 30 givenname: Dominique surname: Langin fullname: Langin, Dominique |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/23431266$$D View this record in MEDLINE/PubMed https://inserm.hal.science/inserm-00841328$$DView record in HAL https://lup.lub.lu.se/record/3674672$$DView record from Swedish Publication Index oai:portal.research.lu.se:publications/e9d88119-b1e3-4dd3-8fc3-c541d330beac$$DView record from Swedish Publication Index http://kipublications.ki.se/Default.aspx?queryparsed=id:126238584$$DView record from Swedish Publication Index |
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| Keywords | Sterol Esterase Humans Middle Aged Lipid Metabolism Male Glucose Niacin Lipolysis Young Adult Adipose Tissue, White Animals Adolescent Adult Aged Mice Adipose Tissue |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 ObjectType-Undefined-3 The author(s) have made the following declarations about their contributions: Conceived and designed the experiments: AG GT CT NV TS RB PA DL. Performed the experiments: AG GT CV CM NM ALD MH ABP MC LMir LMonbrun VB BPM AW IV KL MAM AM MLR JG. Analyzed the data: AG GT CV CM NM BR BPM SCB TS CH EM RB PA DL. Contributed reagents/materials/analysis tools: CH. Wrote the paper: AG DL. The authors have declared that no competing interests exist. |
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| Title | Partial Inhibition of Adipose Tissue Lipolysis Improves Glucose Metabolism and Insulin Sensitivity Without Alteration of Fat Mass |
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