Chronic oxytocin administration inhibits food intake, increases energy expenditure, and produces weight loss in fructose-fed obese rhesus monkeys.

Despite compelling evidence that oxytocin (OT) is effective in reducing body weight (BW) in diet-induced obese (DIO) rodents, studies of the effects of OT in humans and rhesus monkeys have primarily focused on noningestive behaviors. The goal of this study was to translate findings in DIO rodents to a preclinical translational model of DIO. We tested the hypothesis that increased OT signaling would reduce BW in DIO rhesus monkeys by inhibiting food intake and increasing energy expenditure (EE). Male DIO rhesus monkeys from the California National Primate Research Center were adapted to a 12-h fast and maintained on chow and a daily 15% fructose-sweetened beverage. Monkeys received 2× daily subcutaneous vehicle injections over 1 wk. We subsequently identified doses of OT (0.2 and 0.4 mg/kg) that reduced food intake and BW in the absence of nausea or diarrhea. Chronic administration of OT for 4 wk (0.2 mg/kg for 2 wk; 0.4 mg/kg for 2 wk) reduced BW relative to vehicle by 3.3 ± 0.4% (≈0.6 kg; P < 0.05). Moreover, the low dose of OT suppressed 12-h chow intake by 26 ± 7% (P < 0.05). The higher dose of OT reduced 12-h chow intake by 27 ± 5% (P < 0.05) and 8-h fructose-sweetened beverage intake by 18 ± 8% (P < 0.05). OT increased EE during the dark cycle by 14 ± 3% (P < 0.05) and was associated with elevations of free fatty acids and glycerol and reductions in triglycerides suggesting increased lipolysis. Together, these data suggest that OT reduces BW in DIO rhesus monkeys through decreased food intake as well as increased EE and lipolysis.

[1]  C. Billington,et al.  Oxytocin in the ventromedial hypothalamic nucleus reduces feeding and acutely increases energy expenditure. , 2014, American journal of physiology. Regulatory, integrative and comparative physiology.

[2]  J. Altirriba,et al.  Divergent effects of oxytocin treatment of obese diabetic mice on adiposity and diabetes. , 2014, Endocrinology.

[3]  J. Waas,et al.  Functional relationship between oxytocin and appetite for carbohydrates versus saccharin , 2014, Neuroreport.

[4]  L. Young,et al.  The neuroanatomical distribution of oxytocin receptor binding and mRNA in the male rhesus macaque (Macaca mulatta) , 2014, Psychoneuroendocrinology.

[5]  M. Althaus,et al.  Chronic enhancement of brain oxytocin levels causes enduring anti-aggressive and pro-social explorative behavioral effects in male rats , 2014, Hormones and Behavior.

[6]  K. Krskova,et al.  Hypooxytocinaemia in obese Zucker rats relates to oxytocin degradation in liver and adipose tissue. , 2014, The Journal of endocrinology.

[7]  J. Born,et al.  Oxytocin Reduces Reward-Driven Food Intake in Humans , 2013, Diabetes.

[8]  S. Roh,et al.  Oxytocin receptor in the hypothalamus is sufficient to rescue normal thermoregulatory function in male oxytocin receptor knockout mice. , 2013, Endocrinology.

[9]  Kristen E Kay,et al.  Oxytocin action in the ventral tegmental area affects sucrose intake , 2013, Brain Research.

[10]  D. Cai,et al.  Treatment of Obesity and Diabetes Using Oxytocin or Analogs in Patients and Mouse Models , 2013, PloS one.

[11]  A. Wong,et al.  Efficacy and safety of lorcaserin in obese adults: a meta‐analysis of 1‐year randomized controlled trials (RCTs) and narrative review on short‐term RCTs , 2013, Obesity reviews : an official journal of the International Association for the Study of Obesity.

[12]  M. Kusama,et al.  Involvement of Prolactin-Releasing Peptide in the Activation of Oxytocin Neurones in Response to Food Intake , 2013, Journal of neuroendocrinology.

[13]  Inês Barroso,et al.  Genome-wide SNP and CNV analysis identifies common and low-frequency variants associated with severe early-onset obesity , 2013, Nature Genetics.

[14]  D. Marks,et al.  Chronic Treatment With a Melanocortin-4 Receptor Agonist Causes Weight Loss, Reduces Insulin Resistance, and Improves Cardiovascular Function in Diet-Induced Obese Rhesus Macaques , 2013, Diabetes.

[15]  R Todd Constable,et al.  Effects of fructose vs glucose on regional cerebral blood flow in brain regions involved with appetite and reward pathways. , 2013, JAMA.

[16]  B. Lowell,et al.  An Obligate Role of Oxytocin Neurons in Diet Induced Energy Expenditure , 2012, PloS one.

[17]  Katherine A. Winters,et al.  Long-acting FGF21 has enhanced efficacy in diet-induced obese mice and in obese rhesus monkeys. , 2012, Endocrinology.

[18]  I. McGregor,et al.  The Nonpeptide Oxytocin Receptor Agonist WAY 267,464: Receptor‐Binding Profile, Prosocial Effects and Distribution of c‐Fos Expression in Adolescent Rats , 2012, Journal of neuroendocrinology.

[19]  T. Yada,et al.  Peripheral oxytocin treatment ameliorates obesity by reducing food intake and visceral fat mass , 2011, Aging.

[20]  P. Kwok,et al.  Replication and Extension of Association Between Common Genetic Variants in SIM1 and Human Adiposity , 2011, Obesity.

[21]  Kim-Anh Do,et al.  A Peptidomimetic Targeting White Fat Causes Weight Loss and Improved Insulin Resistance in Obese Monkeys , 2011, Science Translational Medicine.

[22]  D. Cai,et al.  Circadian intervention of obesity development via resting-stage feeding manipulation or oxytocin treatment. , 2011, American journal of physiology. Endocrinology and metabolism.

[23]  W. Wahli,et al.  Mechanisms of the Anti-Obesity Effects of Oxytocin in Diet-Induced Obese Rats , 2011, PloS one.

[24]  B. Cummings,et al.  Fructose‐Fed Rhesus Monkeys: A Nonhuman Primate Model of Insulin Resistance, Metabolic Syndrome, and Type 2 Diabetes , 2011, Clinical and translational science.

[25]  D. Cai,et al.  Neuropeptide Exocytosis Involving Synaptotagmin-4 and Oxytocin in Hypothalamic Programming of Body Weight and Energy Balance , 2011, Neuron.

[26]  H. Schiöth,et al.  Molecular, immunohistochemical, and pharmacological evidence of oxytocin's role as inhibitor of carbohydrate but not fat intake. , 2010, Endocrinology.

[27]  A. Guastella,et al.  Systemically administered oxytocin decreases methamphetamine activation of the subthalamic nucleus and accumbens core and stimulates oxytocinergic neurons in the hypothalamus , 2010, Addiction biology.

[28]  F. Hu,et al.  Contemporary Reviews in Cardiovascular Medicine Sugar-Sweetened Beverages, Obesity, Type 2 Diabetes Mellitus, and Cardiovascular Disease Risk , 2010 .

[29]  A. Butler,et al.  A Recurring Problem With the Analysis of Energy Expenditure in Genetic Models Expressing Lean and Obese Phenotypes , 2010, Diabetes.

[30]  M. Dietrich,et al.  Nesfatin-1-regulated oxytocinergic signaling in the paraventricular nucleus causes anorexia through a leptin-independent melanocortin pathway. , 2009, Cell metabolism.

[31]  Wei Zhang,et al.  Consuming fructose-sweetened, not glucose-sweetened, beverages increases visceral adiposity and lipids and decreases insulin sensitivity in overweight/obese humans. , 2009, The Journal of clinical investigation.

[32]  C. Camerino Low Sympathetic Tone and Obese Phenotype in Oxytocin‐deficient Mice , 2009, Obesity.

[33]  Tadashi Kimura,et al.  Evidence That Oxytocin Exerts Anxiolytic Effects via Oxytocin Receptor Expressed in Serotonergic Neurons in Mice , 2009, The Journal of Neuroscience.

[34]  A. Zinn,et al.  Oxytocin deficiency mediates hyperphagic obesity of Sim1 haploinsufficient mice. , 2008, Molecular endocrinology.

[35]  T. Kawada,et al.  Oxytocin receptor-deficient mice developed late-onset obesity , 2008, Neuroreport.

[36]  S. Grundy Metabolic Syndrome Pandemic , 2008, Arteriosclerosis, thrombosis, and vascular biology.

[37]  P. Havel,et al.  Fructose consumption: potential mechanisms for its effects to increase visceral adiposity and induce dyslipidemia and insulin resistance , 2008, Current opinion in lipidology.

[38]  Kenneth D Anderson,et al.  Peripherally administered non-peptide oxytocin antagonist, L368,899®, accumulates in limbic brain areas: A new pharmacological tool for the study of social motivation in non-human primates , 2007, Hormones and Behavior.

[39]  Yun-Fei Chen,et al.  The metabolic state of diabetic monkeys is regulated by fibroblast growth factor-21. , 2007, Endocrinology.

[40]  F. Hu,et al.  Intake of sugar-sweetened beverages and weight gain: a systematic review. , 2006, The American journal of clinical nutrition.

[41]  T. Yoshikawa,et al.  Microarray profiling of gene expression in human adipocytes in response to anthocyanins. , 2006, Biochemical pharmacology.

[42]  R. Vollmer,et al.  Enhanced initial and sustained intake of sucrose solution in mice with an oxytocin gene deletion. , 2005, American journal of physiology. Regulatory, integrative and comparative physiology.

[43]  J. Schölmerich,et al.  Hypothesis paper Brain talks with fat – evidence for a hypothalamic–pituitary–adipose axis? , 2005, Neuropeptides.

[44]  P. Havel Dietary fructose: implications for dysregulation of energy homeostasis and lipid/carbohydrate metabolism. , 2005, Nutrition reviews.

[45]  M. Schwartz,et al.  Evidence that paraventricular nucleus oxytocin neurons link hypothalamic leptin action to caudal brain stem nuclei controlling meal size. , 2004, American journal of physiology. Regulatory, integrative and comparative physiology.

[46]  G. Bray,et al.  Consumption of high-fructose corn syrup in beverages may play a role in the epidemic of obesity. , 2004, The American journal of clinical nutrition.

[47]  H. Zingg,et al.  Mapping oxytocin receptor gene expression in the mouse brain and mammary gland using an oxytocin receptor–LacZ reporter mouse , 2003, Neuroscience.

[48]  B. Oldfield,et al.  The neurochemical characterisation of hypothalamic pathways projecting polysynaptically to brown adipose tissue in the rat , 2002, Neuroscience.

[49]  M. Morris,et al.  Baroreflex control of heart rate by oxytocin in the solitary-vagal complex. , 2002, American journal of physiology. Regulatory, integrative and comparative physiology.

[50]  G. Gimpl,et al.  The oxytocin receptor system: structure, function, and regulation. , 2001, Physiological reviews.

[51]  K. Kendrick,et al.  Oxytocin, motherhood and bonding , 2000, Experimental physiology.

[52]  R. Ritter,et al.  High fat maintenance diet attenuates hindbrain neuronal response to CCK , 2000, Regulatory Peptides.

[53]  Mihai Covasa,et al.  Reduced sensitivity to the satiation effect of intestinal oleate in rats adapted to high-fat diet. , 1999, American journal of physiology. Regulatory, integrative and comparative physiology.

[54]  R. Ritter,et al.  Rats maintained on high-fat diets exhibit reduced satiety in response to CCK and bombesin , 1998, Peptides.

[55]  A. Loewy,et al.  Transneuronal labeling of CNS neuropeptide and monoamine neurons after pseudorabies virus injections into the stellate ganglion , 1995, Brain Research.

[56]  D. Swaab,et al.  Alterations in the hypothalamic paraventricular nucleus and its oxytocin neurons (putative satiety cells) in Prader-Willi syndrome: a study of five cases. , 1995, The Journal of clinical endocrinology and metabolism.

[57]  E. Stricker,et al.  Brain oxytocin receptor antagonism blunts the effects of anorexigenic treatments in rats: evidence for central oxytocin inhibition of food intake. , 1991, Endocrinology.

[58]  A. Benelli,et al.  Oxytocin inhibits food and fluid intake in rats , 1990, Physiology & Behavior.

[59]  G. Klassen,et al.  Oxytocin modulation of intrathoracic sympathetic ganglionic neurons regulating the canine heart , 1990, Peptides.

[60]  A. Benelli,et al.  Influence of oxytocin on feeding behavior in the rat , 1989, Peptides.

[61]  S. Backman,et al.  Effects of oxytocin and vasopressin on thoracic sympathetic preganglionic neurones in the cat , 1984, Brain Research Bulletin.

[62]  L. Swanson,et al.  Immunohistochemical identification of neurons in the paraventricular nucleus of the hypothalamus that project to the medulla or to the spinal cord in the rat , 1982, The Journal of comparative neurology.

[63]  D. Muchmore,et al.  A dual mechanism of action of ocytocin in rat epididymal fat cells. , 1981, The Journal of biological chemistry.

[64]  J. B. Weir New methods for calculating metabolic rate with special reference to protein metabolism , 1949, The Journal of physiology.

[65]  B. Cummings,et al.  Fish oil supplementation ameliorates fructose-induced hypertriglyceridemia and insulin resistance in adult male rhesus macaques. , 2014, The Journal of nutrition.

[66]  S. Yanovski,et al.  Long-term drug treatment for obesity: a systematic and clinical review. , 2014, JAMA.

[67]  K. Flegal,et al.  Prevalence of obesity in the United States, 2009-2010. , 2012, NCHS data brief.

[68]  Brendan S. Thatcher,et al.  Peripheral oxytocin suppresses food intake and causes weight loss in diet-induced obese rats. , 2012, American journal of physiology. Endocrinology and metabolism.

[69]  Simon Smyth,et al.  Diabetes and obesity: the twin epidemics , 2006, Nature Medicine.

[70]  H. Minuk,et al.  Metabolic syndrome. , 2005, Journal of insurance medicine.

[71]  A. Zinn,et al.  Profound obesity associated with a balanced translocation that disrupts the SIM1 gene. , 2000, Human molecular genetics.