Serotonin 2C receptors in pro-opiomelanocortin neurons regulate energy and glucose homeostasis.

Energy and glucose homeostasis are regulated by central serotonin 2C receptors. These receptors are attractive pharmacological targets for the treatment of obesity; however, the identity of the serotonin 2C receptor-expressing neurons that mediate the effects of serotonin and serotonin 2C receptor agonists on energy and glucose homeostasis are unknown. Here, we show that mice lacking serotonin 2C receptors (Htr2c) specifically in pro-opiomelanocortin (POMC) neurons had normal body weight but developed glucoregulatory defects including hyperinsulinemia, hyperglucagonemia, hyperglycemia, and insulin resistance. Moreover, these mice did not show anorectic responses to serotonergic agents that suppress appetite and developed hyperphagia and obesity when they were fed a high-fat/high-sugar diet. A requirement of serotonin 2C receptors in POMC neurons for the maintenance of normal energy and glucose homeostasis was further demonstrated when Htr2c loss was induced in POMC neurons in adult mice using a tamoxifen-inducible POMC-cre system. These data demonstrate that serotonin 2C receptor-expressing POMC neurons are required to control energy and glucose homeostasis and implicate POMC neurons as the target for the effect of serotonin 2C receptor agonists on weight-loss induction and improved glycemic control.

[1]  D. Burrin,et al.  Central GLP-2 enhances hepatic insulin sensitivity via activating PI3K signaling in POMC neurons. , 2013, Cell metabolism.

[2]  E. Colman,et al.  The FDA's assessment of two drugs for chronic weight management. , 2012, The New England journal of medicine.

[3]  J. Gosden,et al.  What is the prognosis for new centrally-acting anti-obesity drugs? , 2012, Neuropharmacology.

[4]  R. Coppari,et al.  Direct leptin action on POMC neurons regulates glucose homeostasis and hepatic insulin sensitivity in mice. , 2012, The Journal of clinical investigation.

[5]  J. D. do Carmo,et al.  Activation of the central melanocortin system contributes to the increased arterial pressure in obese Zucker rats. , 2012, American journal of physiology. Regulatory, integrative and comparative physiology.

[6]  A. Cherrington,et al.  Glucagonocentric restructuring of diabetes: a pathophysiologic and therapeutic makeover. , 2012, The Journal of clinical investigation.

[7]  J. Elmquist,et al.  Serotonin 2C Receptor Activates a Distinct Population of Arcuate Pro-opiomelanocortin Neurons via TRPC Channels , 2011, Neuron.

[8]  A. Garfield,et al.  Role of central serotonin and melanocortin systems in the control of energy balance. , 2011, European journal of pharmacology.

[9]  Nu-Chu Liang,et al.  The use of serotonergic drugs to treat obesity – is there any hope? , 2011, Drug design, development and therapy.

[10]  A. Zinn,et al.  A Serotonin and Melanocortin Circuit Mediates d-Fenfluramine Anorexia , 2010, The Journal of Neuroscience.

[11]  Philipp E. Scherer,et al.  5-HT2CRs Expressed by Pro-opiomelanocortin Neurons Regulate Insulin Sensitivity in Liver , 2010, Nature Neuroscience.

[12]  Arya M. Sharma,et al.  Effect of sibutramine on cardiovascular outcomes in overweight and obese subjects. , 2010, The New England journal of medicine.

[13]  B. Lowell,et al.  Direct insulin and leptin action on pro-opiomelanocortin neurons is required for normal glucose homeostasis and fertility. , 2010, Cell metabolism.

[14]  Kevin W. Williams,et al.  Segregation of Acute Leptin and Insulin Effects in Distinct Populations of Arcuate Proopiomelanocortin Neurons , 2010, The Journal of Neuroscience.

[15]  A. Garfield,et al.  Pharmacological targeting of the serotonergic system for the treatment of obesity , 2009, The Journal of physiology.

[16]  Kevin W. Williams,et al.  5-HT2CRs Expressed by Pro-Opiomelanocortin Neurons Regulate Energy Homeostasis , 2008, Neuron.

[17]  K. Nishikura,et al.  Dysregulated Editing of Serotonin 2C Receptor mRNAs Results in Energy Dissipation and Loss of Fat Mass , 2008, The Journal of Neuroscience.

[18]  S. O’Rahilly,et al.  Serotonin 5-HT2C receptor agonist promotes hypophagia via downstream activation of melanocortin 4 receptors. , 2008, Endocrinology.

[19]  E. H. Goulding,et al.  Synergistic impairment of glucose homeostasis in ob/ob mice lacking functional serotonin 2C receptors. , 2008, Endocrinology.

[20]  J. Elmquist,et al.  Serotonin 2C Receptor Agonists Improve Type 2 Diabetes via Melanocortin-4 Receptor Signaling Pathways , 2007, Cell metabolism.

[21]  L. Heisler,et al.  Serotonin and energy balance: molecular mechanisms and implications for type 2 diabetes , 2007, Expert Reviews in Molecular Medicine.

[22]  Olivier Boss,et al.  Serotonin Reciprocally Regulates Melanocortin Neurons to Modulate Food Intake , 2006, Neuron.

[23]  R. Palmiter,et al.  NPY/AgRP Neurons Are Essential for Feeding in Adult Mice but Can Be Ablated in Neonates , 2005, Science.

[24]  B. Lowell,et al.  Leptin Receptor Signaling in POMC Neurons Is Required for Normal Body Weight Homeostasis , 2004, Neuron.

[25]  Bei B. Zhang,et al.  Glucagon and regulation of glucose metabolism. , 2003, American journal of physiology. Endocrinology and metabolism.

[26]  M. Low,et al.  Activation of Central Melanocortin Pathways by Fenfluramine , 2002, Science.

[27]  R. Rizza,et al.  Lack of suppression of glucagon contributes to postprandial hyperglycemia in subjects with type 2 diabetes mellitus. , 2000, The Journal of clinical endocrinology and metabolism.

[28]  R. Cone,et al.  The central melanocortin system can directly regulate serum insulin levels. , 2000, Endocrinology.

[29]  J. Dean,et al.  Expression of Cre recombinase in mouse oocytes: A means to study maternal effect genes , 2000, Genesis.

[30]  R. Rizza,et al.  Impact of lack of suppression of glucagon on glucose tolerance in humans. , 1999, American journal of physiology. Endocrinology and metabolism.

[31]  L. Tecott,et al.  Reduced satiating effect of d-fenfluramine in serotonin 5-HT2C receptor mutant mice , 1999, Psychopharmacology.

[32]  L. Tecott,et al.  Leptin-independent hyperphagia and type 2 diabetes in mice with a mutated serotonin 5-HT2C receptor gene , 1998, Nature Medicine.

[33]  B. Corya,et al.  Valvular heart disease associated with fenfluramine-phentermine. , 1997, The New England journal of medicine.

[34]  P Chambon,et al.  Ligand-activated site-specific recombination in mice. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[35]  David Julius,et al.  Eating disorder and epilepsy in mice lacking 5-HT2C serotonin receptors , 1995, Nature.

[36]  M. Linnoila,et al.  Hyperglycemic properties of serotonin receptor antagonists. , 1991, Life sciences.

[37]  B. Hoebel,et al.  Serotonin release in lateral and medial hypothalamus during feeding and its anticipation , 1990, Brain Research Bulletin.

[38]  T. Jessell,et al.  5-HT1c receptor is a prominent serotonin receptor subtype in the central nervous system. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[39]  E. Kraegen,et al.  Effect of d-Fenfluramine on Basal Glucose Turnover and Fat-Feeding-Induced Insulin Resistance in Rats , 1989, Diabetes.

[40]  C. Léránth,et al.  Serotoninergic endings on VIP-neurons in the suprachiasmatic nucleus and on ACTH-neurons in the arcuate nucleus of the rat hypothalamus. A combination of high resolution autoradiography and electron microscopic immunocytochemistry , 1984, Neuroscience Letters.

[41]  R. Steele,et al.  Measurement of size and turnover rate of body glucose pool by the isotope dilution method. , 1956, The American journal of physiology.

[42]  S. Padilla,et al.  Pomc-expressing progenitors give rise to antagonistic neuronal populations in hypothalamic feeding circuits , 2022 .