Cdkn2a deficiency promotes adipose tissue browning
Genome-wide association studies have reported that DNA polymorphisms at the CDKN2A locus modulate fasting glucose in human and contribute to type 2 diabetes (T2D) risk. Yet the causal relationship between this gene and defective energy homeostasis remains elusive. Here we sought to understand the co...
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| Published in | Molecular metabolism (Germany) Vol. 8; pp. 65 - 76 |
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| Main Authors | , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
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Elsevier GmbH
01.02.2018
Elsevier |
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| Abstract | Genome-wide association studies have reported that DNA polymorphisms at the CDKN2A locus modulate fasting glucose in human and contribute to type 2 diabetes (T2D) risk. Yet the causal relationship between this gene and defective energy homeostasis remains elusive. Here we sought to understand the contribution of Cdkn2a to metabolic homeostasis.
We first analyzed glucose and energy homeostasis from Cdkn2a-deficient mice subjected to normal or high fat diets. Subsequently Cdkn2a-deficient primary adipose cells and human-induced pluripotent stem differentiated into adipocytes were further characterized for their capacity to promote browning of adipose tissue. Finally CDKN2A levels were studied in adipocytes from lean and obese patients.
We report that Cdkn2a deficiency protects mice against high fat diet-induced obesity, increases energy expenditure and modulates adaptive thermogenesis, in addition to improving insulin sensitivity. Disruption of Cdkn2a associates with increased expression of brown-like/beige fat markers in inguinal adipose tissue and enhances respiration in primary adipose cells. Kinase activity profiling and RNA-sequencing analysis of primary adipose cells further demonstrate that Cdkn2a modulates gene networks involved in energy production and lipid metabolism, through the activation of the Protein Kinase A (PKA), PKG, PPARGC1A and PRDM16 signaling pathways, key regulators of adipocyte beiging. Importantly, CDKN2A expression is increased in adipocytes from obese compared to lean subjects. Moreover silencing CDKN2A expression during human-induced pluripotent stem cells adipogenic differentiation promoted UCP1 expression.
Our results offer novel insight into brown/beige adipocyte functions, which has recently emerged as an attractive therapeutic strategy for obesity and T2D. Modulating Cdkn2a-regulated signaling cascades may be of interest for the treatment of metabolic disorders.
•Cdkn2a deficiency protects mice against high fat diet-induced obesity.•Cdkn2a modulates brown-like/beige fat gene networks involved in energy production and lipid metabolism.•Increased CDKN2A expression in human obese adipocytes.•Increased UCP1 levels in adipocytes differentiated from CDKN2A-silenced hiPS cells. |
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| AbstractList | Objectives: Genome-wide association studies have reported that DNA polymorphisms at the CDKN2A locus modulate fasting glucose in human and contribute to type 2 diabetes (T2D) risk. Yet the causal relationship between this gene and defective energy homeostasis remains elusive. Here we sought to understand the contribution of Cdkn2a to metabolic homeostasis. Methods: We first analyzed glucose and energy homeostasis from Cdkn2a-deficient mice subjected to normal or high fat diets. Subsequently Cdkn2a-deficient primary adipose cells and human-induced pluripotent stem differentiated into adipocytes were further characterized for their capacity to promote browning of adipose tissue. Finally CDKN2A levels were studied in adipocytes from lean and obese patients. Results: We report that Cdkn2a deficiency protects mice against high fat diet-induced obesity, increases energy expenditure and modulates adaptive thermogenesis, in addition to improving insulin sensitivity. Disruption of Cdkn2a associates with increased expression of brown-like/beige fat markers in inguinal adipose tissue and enhances respiration in primary adipose cells. Kinase activity profiling and RNA-sequencing analysis of primary adipose cells further demonstrate that Cdkn2a modulates gene networks involved in energy production and lipid metabolism, through the activation of the Protein Kinase A (PKA), PKG, PPARGC1A and PRDM16 signaling pathways, key regulators of adipocyte beiging. Importantly, CDKN2A expression is increased in adipocytes from obese compared to lean subjects. Moreover silencing CDKN2A expression during human-induced pluripotent stem cells adipogenic differentiation promoted UCP1 expression. Conclusion: Our results offer novel insight into brown/beige adipocyte functions, which has recently emerged as an attractive therapeutic strategy for obesity and T2D. Modulating Cdkn2a-regulated signaling cascades may be of interest for the treatment of metabolic disorders. Keywords: Obesity, Type 2 diabetes, Insulin sensitivity, Energy expenditure, cdkn2a, Genome-wide association study, Adipose tissue browning • Cdkn2a deficiency protects mice against high fat diet-induced obesity. • Cdkn2a modulates brown-like/beige fat gene networks involved in energy production and lipid metabolism. • Increased CDKN2A expression in human obese adipocytes. • Increased UCP1 levels in adipocytes differentiated from CDKN2A- silenced hiPS cells. Objectives: Genome-wide association studies have reported that DNA polymorphisms at the CDKN2A locus modulate fasting glucose in human and contribute to type 2 diabetes (T2D) risk. Yet the causal relationship between this gene and defective energy homeostasis remains elusive. Here we sought to understand the contribution of Cdkn2a to metabolic homeostasis. Methods: We first analyzed glucose and energy homeostasis from Cdkn2a-deficient mice subjected to normal or high fat diets. Subsequently Cdkn2a-deficient primary adipose cells and human-induced pluripotent stem differentiated into adipocytes were further characterized for their capacity to promote browning of adipose tissue. Finally CDKN2A levels were studied in adipocytes from lean and obese patients. Results: We report that Cdkn2a deficiency protects mice against high fat diet-induced obesity, increases energy expenditure and modulates adaptive thermogenesis, in addition to improving insulin sensitivity. Disruption of Cdkn2a associates with increased expression of brown-like/ beige fat markers in inguinal adipose tissue and enhances respiration in primary adipose cells. Kinase activity profiling and RNA-sequencing analysis of primary adipose cells further demonstrate that Cdkn2a modulates gene networks involved in energy production and lipid metabolism, through the activation of the Protein Kinase A (PKA), PKG, PPARGC1A and PRDM16 signaling pathways, key regulators of adipocyte beiging. Importantly, CDKN2A expression is increased in adipocytes from obese compared to lean subjects. Moreover silencing CDKN2A expression during human-induced pluripotent stem cells adipogenic differentiation promoted UCP1 expression. Conclusion: Our results offer novel insight into brown/beige adipocyte functions, which has recently emerged as an attractive therapeutic strategy for obesity and T2D. Modulating Cdkn2a-regulated signaling cascades may be of interest for the treatment of metabolic disorders. Genome-wide association studies have reported that DNA polymorphisms at the CDKN2A locus modulate fasting glucose in human and contribute to type 2 diabetes (T2D) risk. Yet the causal relationship between this gene and defective energy homeostasis remains elusive. Here we sought to understand the contribution of Cdkn2a to metabolic homeostasis. We first analyzed glucose and energy homeostasis from Cdkn2a-deficient mice subjected to normal or high fat diets. Subsequently Cdkn2a-deficient primary adipose cells and human-induced pluripotent stem differentiated into adipocytes were further characterized for their capacity to promote browning of adipose tissue. Finally CDKN2A levels were studied in adipocytes from lean and obese patients. We report that Cdkn2a deficiency protects mice against high fat diet-induced obesity, increases energy expenditure and modulates adaptive thermogenesis, in addition to improving insulin sensitivity. Disruption of Cdkn2a associates with increased expression of brown-like/beige fat markers in inguinal adipose tissue and enhances respiration in primary adipose cells. Kinase activity profiling and RNA-sequencing analysis of primary adipose cells further demonstrate that Cdkn2a modulates gene networks involved in energy production and lipid metabolism, through the activation of the Protein Kinase A (PKA), PKG, PPARGC1A and PRDM16 signaling pathways, key regulators of adipocyte beiging. Importantly, CDKN2A expression is increased in adipocytes from obese compared to lean subjects. Moreover silencing CDKN2A expression during human-induced pluripotent stem cells adipogenic differentiation promoted UCP1 expression. Our results offer novel insight into brown/beige adipocyte functions, which has recently emerged as an attractive therapeutic strategy for obesity and T2D. Modulating Cdkn2a-regulated signaling cascades may be of interest for the treatment of metabolic disorders. •Cdkn2a deficiency protects mice against high fat diet-induced obesity.•Cdkn2a modulates brown-like/beige fat gene networks involved in energy production and lipid metabolism.•Increased CDKN2A expression in human obese adipocytes.•Increased UCP1 levels in adipocytes differentiated from CDKN2A-silenced hiPS cells. Genome-wide association studies have reported that DNA polymorphisms at the CDKN2A locus modulate fasting glucose in human and contribute to type 2 diabetes (T2D) risk. Yet the causal relationship between this gene and defective energy homeostasis remains elusive. Here we sought to understand the contribution of Cdkn2a to metabolic homeostasis. We first analyzed glucose and energy homeostasis from Cdkn2a-deficient mice subjected to normal or high fat diets. Subsequently Cdkn2a-deficient primary adipose cells and human-induced pluripotent stem differentiated into adipocytes were further characterized for their capacity to promote browning of adipose tissue. Finally CDKN2A levels were studied in adipocytes from lean and obese patients. We report that Cdkn2a deficiency protects mice against high fat diet-induced obesity, increases energy expenditure and modulates adaptive thermogenesis, in addition to improving insulin sensitivity. Disruption of Cdkn2a associates with increased expression of brown-like/beige fat markers in inguinal adipose tissue and enhances respiration in primary adipose cells. Kinase activity profiling and RNA-sequencing analysis of primary adipose cells further demonstrate that Cdkn2a modulates gene networks involved in energy production and lipid metabolism, through the activation of the Protein Kinase A (PKA), PKG, PPARGC1A and PRDM16 signaling pathways, key regulators of adipocyte beiging. Importantly, CDKN2A expression is increased in adipocytes from obese compared to lean subjects. Moreover silencing CDKN2A expression during human-induced pluripotent stem cells adipogenic differentiation promoted UCP1 expression. Our results offer novel insight into brown/beige adipocyte functions, which has recently emerged as an attractive therapeutic strategy for obesity and T2D. Modulating Cdkn2a-regulated signaling cascades may be of interest for the treatment of metabolic disorders. Genome-wide association studies have reported that DNA polymorphisms at the CDKN2A locus modulate fasting glucose in human and contribute to type 2 diabetes (T2D) risk. Yet the causal relationship between this gene and defective energy homeostasis remains elusive. Here we sought to understand the contribution of Cdkn2a to metabolic homeostasis.OBJECTIVESGenome-wide association studies have reported that DNA polymorphisms at the CDKN2A locus modulate fasting glucose in human and contribute to type 2 diabetes (T2D) risk. Yet the causal relationship between this gene and defective energy homeostasis remains elusive. Here we sought to understand the contribution of Cdkn2a to metabolic homeostasis.We first analyzed glucose and energy homeostasis from Cdkn2a-deficient mice subjected to normal or high fat diets. Subsequently Cdkn2a-deficient primary adipose cells and human-induced pluripotent stem differentiated into adipocytes were further characterized for their capacity to promote browning of adipose tissue. Finally CDKN2A levels were studied in adipocytes from lean and obese patients.METHODSWe first analyzed glucose and energy homeostasis from Cdkn2a-deficient mice subjected to normal or high fat diets. Subsequently Cdkn2a-deficient primary adipose cells and human-induced pluripotent stem differentiated into adipocytes were further characterized for their capacity to promote browning of adipose tissue. Finally CDKN2A levels were studied in adipocytes from lean and obese patients.We report that Cdkn2a deficiency protects mice against high fat diet-induced obesity, increases energy expenditure and modulates adaptive thermogenesis, in addition to improving insulin sensitivity. Disruption of Cdkn2a associates with increased expression of brown-like/beige fat markers in inguinal adipose tissue and enhances respiration in primary adipose cells. Kinase activity profiling and RNA-sequencing analysis of primary adipose cells further demonstrate that Cdkn2a modulates gene networks involved in energy production and lipid metabolism, through the activation of the Protein Kinase A (PKA), PKG, PPARGC1A and PRDM16 signaling pathways, key regulators of adipocyte beiging. Importantly, CDKN2A expression is increased in adipocytes from obese compared to lean subjects. Moreover silencing CDKN2A expression during human-induced pluripotent stem cells adipogenic differentiation promoted UCP1 expression.RESULTSWe report that Cdkn2a deficiency protects mice against high fat diet-induced obesity, increases energy expenditure and modulates adaptive thermogenesis, in addition to improving insulin sensitivity. Disruption of Cdkn2a associates with increased expression of brown-like/beige fat markers in inguinal adipose tissue and enhances respiration in primary adipose cells. Kinase activity profiling and RNA-sequencing analysis of primary adipose cells further demonstrate that Cdkn2a modulates gene networks involved in energy production and lipid metabolism, through the activation of the Protein Kinase A (PKA), PKG, PPARGC1A and PRDM16 signaling pathways, key regulators of adipocyte beiging. Importantly, CDKN2A expression is increased in adipocytes from obese compared to lean subjects. Moreover silencing CDKN2A expression during human-induced pluripotent stem cells adipogenic differentiation promoted UCP1 expression.Our results offer novel insight into brown/beige adipocyte functions, which has recently emerged as an attractive therapeutic strategy for obesity and T2D. Modulating Cdkn2a-regulated signaling cascades may be of interest for the treatment of metabolic disorders.CONCLUSIONOur results offer novel insight into brown/beige adipocyte functions, which has recently emerged as an attractive therapeutic strategy for obesity and T2D. Modulating Cdkn2a-regulated signaling cascades may be of interest for the treatment of metabolic disorders. |
| Author | Fajas, Lluis Annicotte, Jean-Sébastien Lopez-Mejia, Isabel C. Salas, Elisabet Oger, Frédérik Bonnefond, Amélie Yao, Xi Rabearivelo, Iandry Rabhi, Nabil Caron, Emilie Dani, Christian Hannou, Sarah Anissa Durand, Emmanuelle Gromada, Xavier Froguel, Philippe Carney, Charlène |
| AuthorAffiliation | 4 Université Côte d'Azur, CNRS, INSERM, iBV, Faculté de Médecine, F-06107 Nice Cedex 2, France 6 INSERM, UMR S-1172, Development and Plasticity of Postnatal Brain, F-59000 Lille, France 1 Lille University, UMR 8199 – EGID, F-59000 Lille, France 3 Institut Pasteur de Lille, F-59000 Lille, France 5 Center for Integrative Genomics, Université de Lausanne, CH-1015 Lausanne, Switzerland 2 CNRS, UMR 8199, F-59000 Lille, France 7 Department of Genomics of Common Disease, School of Public Health, Imperial College London, Hammersmith Hospital, London W12 0NN, UK |
| AuthorAffiliation_xml | – name: 1 Lille University, UMR 8199 – EGID, F-59000 Lille, France – name: 4 Université Côte d'Azur, CNRS, INSERM, iBV, Faculté de Médecine, F-06107 Nice Cedex 2, France – name: 5 Center for Integrative Genomics, Université de Lausanne, CH-1015 Lausanne, Switzerland – name: 3 Institut Pasteur de Lille, F-59000 Lille, France – name: 2 CNRS, UMR 8199, F-59000 Lille, France – name: 6 INSERM, UMR S-1172, Development and Plasticity of Postnatal Brain, F-59000 Lille, France – name: 7 Department of Genomics of Common Disease, School of Public Health, Imperial College London, Hammersmith Hospital, London W12 0NN, UK |
| Author_xml | – sequence: 1 givenname: Nabil surname: Rabhi fullname: Rabhi, Nabil organization: Lille University, UMR 8199 – EGID, F-59000 Lille, France – sequence: 2 givenname: Sarah Anissa surname: Hannou fullname: Hannou, Sarah Anissa organization: Lille University, UMR 8199 – EGID, F-59000 Lille, France – sequence: 3 givenname: Xavier surname: Gromada fullname: Gromada, Xavier organization: Lille University, UMR 8199 – EGID, F-59000 Lille, France – sequence: 4 givenname: Elisabet surname: Salas fullname: Salas, Elisabet organization: Lille University, UMR 8199 – EGID, F-59000 Lille, France – sequence: 5 givenname: Xi surname: Yao fullname: Yao, Xi organization: Université Côte d'Azur, CNRS, INSERM, iBV, Faculté de Médecine, F-06107 Nice Cedex 2, France – sequence: 6 givenname: Frédérik surname: Oger fullname: Oger, Frédérik organization: Lille University, UMR 8199 – EGID, F-59000 Lille, France – sequence: 7 givenname: Charlène surname: Carney fullname: Carney, Charlène organization: Lille University, UMR 8199 – EGID, F-59000 Lille, France – sequence: 8 givenname: Isabel C. surname: Lopez-Mejia fullname: Lopez-Mejia, Isabel C. organization: Center for Integrative Genomics, Université de Lausanne, CH-1015 Lausanne, Switzerland – sequence: 9 givenname: Emmanuelle surname: Durand fullname: Durand, Emmanuelle organization: Lille University, UMR 8199 – EGID, F-59000 Lille, France – sequence: 10 givenname: Iandry surname: Rabearivelo fullname: Rabearivelo, Iandry organization: Lille University, UMR 8199 – EGID, F-59000 Lille, France – sequence: 11 givenname: Amélie surname: Bonnefond fullname: Bonnefond, Amélie organization: Lille University, UMR 8199 – EGID, F-59000 Lille, France – sequence: 12 givenname: Emilie surname: Caron fullname: Caron, Emilie organization: INSERM, UMR S-1172, Development and Plasticity of Postnatal Brain, F-59000 Lille, France – sequence: 13 givenname: Lluis surname: Fajas fullname: Fajas, Lluis organization: Center for Integrative Genomics, Université de Lausanne, CH-1015 Lausanne, Switzerland – sequence: 14 givenname: Christian surname: Dani fullname: Dani, Christian organization: Université Côte d'Azur, CNRS, INSERM, iBV, Faculté de Médecine, F-06107 Nice Cedex 2, France – sequence: 15 givenname: Philippe surname: Froguel fullname: Froguel, Philippe email: p.froguel@imperial.ac.uk organization: Lille University, UMR 8199 – EGID, F-59000 Lille, France – sequence: 16 givenname: Jean-Sébastien surname: Annicotte fullname: Annicotte, Jean-Sébastien email: jean-sebastien.annicotte@inserm.fr organization: Lille University, UMR 8199 – EGID, F-59000 Lille, France |
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| Keywords | Type 2 diabetes cdkn2a Obesity Genome-wide association study Insulin sensitivity Energy expenditure Adipose tissue browning |
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| Snippet | Genome-wide association studies have reported that DNA polymorphisms at the CDKN2A locus modulate fasting glucose in human and contribute to type 2 diabetes... Objectives: Genome-wide association studies have reported that DNA polymorphisms at the CDKN2A locus modulate fasting glucose in human and contribute to type 2... • Cdkn2a deficiency protects mice against high fat diet-induced obesity. • Cdkn2a modulates brown-like/beige fat gene networks involved in energy production... |
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| SubjectTerms | Adipocytes, Brown - cytology Adipocytes, Brown - metabolism Adipogenesis Adipose tissue browning Animals cdkn2a Cells, Cultured Cyclin-Dependent Kinase Inhibitor p16 - genetics Cyclin-Dependent Kinase Inhibitor p16 - metabolism Energy expenditure Gene Regulatory Networks Genome-wide association study Glucose - metabolism Humans Induced Pluripotent Stem Cells - cytology Induced Pluripotent Stem Cells - metabolism Insulin sensitivity Life Sciences Mice Obesity Obesity - metabolism Original Thermogenesis Type 2 diabetes |
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| Title | Cdkn2a deficiency promotes adipose tissue browning |
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