Nicotine induces negative energy balance through hypothalamic AMP-activated protein kinase.
paper
Cited
Public
- Authors
- Martínez de Morentin, Pablo B; Whittle, Andrew J; Fernø, Johan; Nogueiras, Rubén; Diéguez, Carlos; Vidal-Puig, Antonio; López, Miguel
- Year
- 2012
- Journal
- Diabetes
- PMID
- 22315316
- DOI
- 10.2337/db11-1079
- PMCID
- PMC3314364
Smokers around the world commonly report increased body weight after smoking cessation as a major factor that interferes with their attempts to quit. Numerous controlled studies in both humans and rodents have reported that nicotine exerts a marked anorectic action. The effects of nicotine on energy homeostasis have been mostly pinpointed in the central nervous system, but the molecular mechanisms controlling its action are still not fully understood. The aim of this study was to investigate the effect of nicotine on hypothalamic AMP-activated protein kinase (AMPK) and its effect on energy balance. Here we demonstrate that nicotine-induced weight loss is associated with inactivation of hypothalamic AMPK, decreased orexigenic signaling in the hypothalamus, increased energy expenditure as a result of increased locomotor activity, increased thermogenesis in brown adipose tissue (BAT), and alterations in fuel substrate utilization. Conversely, nicotine withdrawal or genetic activation of hypothalamic AMPK in the ventromedial nucleus of the hypothalamus reversed nicotine-induced negative energy balance. Overall these data demonstrate that the effects of nicotine on energy balance involve specific modulation of the hypothalamic AMPK-BAT axis. These targets may be relevant for the development of new therapies for human obesity.
Effects of nicotine administration on energy balance. A: Body weight change. B: Food intake. C: RD. D: CTA. E: Body temperature change. F: EE (cumulative in left panel and total in right panel). G: LA (cumulative in left panel and total in right panel). H: RQ (cumulative in left panel and total in right panel) of vehicle (Veh) and nicotine-treated (Nic) rats for 48 h are shown. *P < 0.05, **P < 0.01, ***P < 0.001 vs. vehicle; ###P < 0.001 nicotine vs. LiCl. In the right panels of F and G, the asterisks above the lines refer to the daily (diurnal + nocturnal) EE or LA. All data are expressed as mean ± SEM.
Effects of nicotine administration on hypothalamic neuropeptides, AMPK, and BAT thermogenic program. In situ hybridization autoradiographic images (A) and AgRP, NPY, POMC, and CART mRNA levels in the ARC (B), FAS mRNA levels in the VMH (C), hypothalamic FAS activity (D), Western blot autoradiographic images (left panel) and hypothalamic protein levels of the different proteins of the AMPK pathway (right panel) (E), and infrared thermal images (left panel) with quantification of temperature (Temp; right panel) (F) and thermogenic markers (G) in the BAT of vehicle (Veh) and nicotine-treated (Nic) rats for 48 h are shown. *P < 0.05, **P < 0.01, ***P < 0.001 vs. vehicle. 3V, third ventricle. PGC1, peroxisome proliferator–activated receptor γ coactivator 1. All data are expressed as mean ± SEM. (A high-quality digital representation of this figure is available in the online issue.)
Effect of antagonism of α3β4-nicotinic acetylcholine receptors on nicotine-induced inhibition of hypothalamic AMPK. Body weight change (A), food intake (B), and Western blot autoradiographic images (left panel) and hypothalamic protein levels of the different proteins of the AMPK pathway (right panel) (C) of rats treated with vehicle (Veh), nicotine (Nic), and mecamylamine (Mec). Dividing lines show spliced bands. *P < 0.05, **P < 0.01, ***P < 0.001 vs. vehicle; #P < 0.05, ###P < 0.001 nicotine vehicle vs. nicotine mecamylamine. All data are expressed as mean ± SEM.
Effects of nicotine withdrawal on energy balance. Body weight (BW) change (A), food intake (B), fat and lean mass (C), EE (D; cumulative in left panel and total in right panel), LA (E; cumulative in left panel and total in right panel), and RQ (F; cumulative in left panel and total in right panel) of vehicle (Veh), nicotine (Nic), and nicotine withdrawal (With) rats are shown. EE, LA, and RQ data are from nicotine and nicotine withdrawal rats during the last 72 h of nicotine cessation. *P < 0.05, **P < 0.01, ***P < 0.001 vs. vehicle; #P < 0.05, ##P < 0.01, ###P < 0.001 nicotine vs. withdrawal; in the right panels of D and E, the symbols above the lines refer to the daily (diurnal + nocturnal) EE or LA. All data are expressed as mean ± SEM.
Effects of nicotine withdrawal hypothalamic AMPK pathway and BAT thermogenic program. Western blot autoradiographic images (left panel) and hypothalamic protein levels of the different proteins of the AMPK pathway (right panel) (A) and thermogenic markers (B) in the BAT of vehicle, nicotine, and nicotine withdrawal rats. Dividing lines show spliced bands. *P < 0.05, **P < 0.01, ***P < 0.001 vs. vehicle; ##P < 0.01, ###P < 0.001 nicotine vs. withdrawal. HPRT, hypoxanthine-guanine phosphoribosyltransferase; PGC1, peroxisome proliferator–activated receptor γ coactivator 1. All data are expressed as mean ± SEM.
Effects of hypothalamic AMPK activation on nicotine actions on energy balance, neuropeptides, and BAT thermogenic program. A: Food intake in rats treated with nicotine and the AMPK activator AICAR. Body weight change (B); daily food intake (C); in situ hybridization autoradiographic images (D); AgRP, NPY, and POMC mRNA levels in the ARC (E); and thermogenic markers (F) in the BAT of rats treated with vehicle or nicotine and stereotaxically treated with GFP-expressing adenoviruses or GFP plus AMPK constitutively active (AMPKα-CA) adenoviruses are shown. *P < 0.05, **P < 0.01, ***P < 0.001 vs. vehicle or vehicle GFP; #P < 0.05, ##P < 0.01, ###P < 0.001 nicotine vehicle vs. nicotine AICAR or nicotine GFP vs. nicotine AMPKα-CA. 3V, third ventricle; PGC1, peroxisome proliferator–activated receptor γ coactivator 1; HPRT, hypoxanthine-guanine phosphoribosyltransferase. All data are expressed as mean ± SEM.
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| 12-h feeding patterns local | phenotype |
| ACACA local | gene |
| ACCα local | gene |
| ACTB | gene |
| adipose tissue | phenotype |
| adult male local | phenotype |
| AgRP local | gene |
| AGRP local | gene |
| AICAR | drug |
| AMPK | gene |
| AMPK pathway local | gene |
| AMPKα local | gene |
| AMPKα1 local | gene |
| AMPKα2 local | gene |
| AMPKα-CA local | gene |
| AMPKα-CA local | variant |
| anorectic actions local | phenotype |
| anorexia nervosa | phenotype |
| ARC local | anatomy |
| aversive response | phenotype |
| BAT | phenotype |
| BAT activation local | phenotype |
| BAT thermogenesis local | phenotype |
| BAT thermogenic markers local | phenotype |
| body composition | phenotype |
| body temperature | phenotype |
| body weight | phenotype |
| Brown Adipose Tissue Activation local | phenotype |
| CAMKK1 local | gene |
| CAMKK2 | gene |
| CaMKKα local | gene |
| CART | gene |
| Chrna3 | gene |
| Chrnb4 | gene |
| conditioned taste aversion | phenotype |
| coronal brain sections local | anatomy |
| decreased food intake local | phenotype |
| Energy balance local | phenotype |
| energy expenditure | phenotype |
| energy homeostasis | phenotype |
| Experimental animals local | cohort |
| FASN | phenotype |
| feeding | phenotype |
| feeding behavior | phenotype |
| food intake | phenotype |
| GFP | drug |
| Hispanic | phenotype |
| HPRT1 | gene |
| Human obesity local | phenotype |
| hypophagia local | phenotype |
| Hypophagia local | phenotype |
| Hypophagic state local | phenotype |
| hypothalamic AMPK-BAT axis local | drug |
| hypothalamus | anatomy |
| illness | phenotype |
| ImageJ-1.33 local | drug |
| increased BAT-mediated energy dissipation local | phenotype |
| increased energy expenditure local | phenotype |
| insulin sensitivity | phenotype |
| ketamine | drug |
| lateral ventricle | anatomy |
| lean body mass | phenotype |
| lipid mobilization local | phenotype |
| Lipid mobilization local | phenotype |
| lipid oxidation local | phenotype |
| Lipid oxidation local | phenotype |
| Lithium chloride | drug |
| locomotor activity | phenotype |
| malaise local | phenotype |
| Malonyl-CoA local | drug |
| mecamylamine | drug |
| Metformin | drug |
| methylene blue | drug |
| mood disorders | phenotype |
| negative energy balance local | phenotype |
| Negative energy balance local | phenotype |
| Neonatal rats | cohort |
| nicotine | drug |
| nicotine gum | drug |
| nicotine replacement therapy | drug |
| nicotine withdrawal | phenotype |
| Nicotinic acetylcholine receptors local | gene |
| NPY | gene |
| obesity | phenotype |
| pACCα local | drug |
| Pomc | gene |
| postcessation weight gain local | phenotype |
| PP2Cα local | gene |
| PPARGC1A | gene |
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| rats | cohort |
| respiratory depression | phenotype |
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| RQ local | phenotype |
| saccharin | drug |
| Saccharin preference ratio local | phenotype |
| saline | drug |
| Skin temperature surrounding BAT local | phenotype |
| Skin temperature surrounding interscapular BAT local | phenotype |
| smoking | phenotype |
| smoking cessation | phenotype |
| Sodium saccharin local | drug |
| Sprague-Dawley rats | cohort |
| STK11 | gene |
| stress | phenotype |
| thermogenesis | phenotype |
| Thermogenic effect local | phenotype |
| thermogenic program local | phenotype |
| thiazolidinediones | drug |
| UCP1 | gene |
| UCP1 expression local | phenotype |
| vehicle-treated rats local | cohort |
| ventromedial nucleus of the hypothalamus local | anatomy |
| VMH | anatomy |
| weight gain | phenotype |
| weight loss | phenotype |
| xylazine | drug |
| α3β4 nicotinic acetylcholine receptors local | drug |
| α3β4-nicotinic acetylcholine receptors local | drug |
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| Estradiol Regulates Energy Balance by Ameliorating Hypothalamic Ceramide-Induced ER Stress. | González-García I et al. | — | 2018 | → |
| Genetic Targeting of GRP78 in the VMH Improves Obesity Independently of Food Intake. | Liñares-Pose L et al. | — | 2018 | → |
| Hypothalamic AMPK and energy balance. | López M | — | 2018 | → |
| Nicotinic Cholinergic System in the Hypothalamus Modulates the Activity of the Hypothalamic Neuropeptides During the Stress Response. | Balkan B et al. | — | 2018 | → |
| Pharmacological Effects and Regulatory Mechanisms of Tobacco Smoking Effects on Food Intake and Weight Control. | Hu T et al. | — | 2018 | → |
| Self-administered nicotine increases fat metabolism and suppresses weight gain in male rats. | Rupprecht LE et al. | — | 2018 | → |
| SF1-Specific AMPKα1 Deletion Protects Against Diet-Induced Obesity. | Seoane-Collazo P et al. | — | 2018 | → |
| A brain-sparing diphtheria toxin for chemical genetic ablation of peripheral cell lineages. | Pereira MM et al. | — | 2017 | → |
| Access to nicotine in drinking water reduces weight gain without changing caloric intake on high fat diet in male C57BL/6J mice. | Calarco CA et al. | — | 2017 | → |
| Brain Ceramide Metabolism in the Control of Energy Balance. | Cruciani-Guglielmacci C et al. | — | 2017 | → |
| Effects of nicotine on homeostatic and hedonic components of food intake. | Stojakovic A et al. | — | 2017 | → |
| EJE PRIZE 2017: Hypothalamic AMPK: a golden target against obesity? | López M | — | 2017 | → |
| Estradiol effects on hypothalamic AMPK and BAT thermogenesis: A gateway for obesity treatment? | López M et al. | — | 2017 | → |
| Estradiol Regulation of Brown Adipose Tissue Thermogenesis. | González-García I et al. | — | 2017 | → |
| Hypothalamic Regulation of Liver and Muscle Nutrient Partitioning by Brain-Specific Carnitine Palmitoyltransferase 1C in Male Mice. | Pozo M et al. | — | 2017 | → |
| Oral nicotine aggravates endothelial dysfunction and vascular inflammation in diet-induced obese rats: Role of macrophage TNFα. | Liu C et al. | — | 2017 | → |
| Reduction of Hypothalamic Endoplasmic Reticulum Stress Activates Browning of White Fat and Ameliorates Obesity. | Contreras C et al. | — | 2017 | → |
| The Obesity-Impulsivity Axis: Potential Metabolic Interventions in Chronic Psychiatric Patients. | Sfera A et al. | — | 2017 | → |
| Thyroid hormones induce browning of white fat. | Martínez-Sánchez N et al. | — | 2017 | → |
| A Functional Link between AMPK and Orexin Mediates the Effect of BMP8B on Energy Balance. | Martins L et al. | — | 2016 | → |
| Classification of Therapeutic and Experimental Drugs for Brown Adipose Tissue Activation: Potential Treatment Strategies for Diabetes and Obesity. | Mukherjee J et al. | — | 2016 | → |
| Contribution of adaptive thermogenesis to the hypothalamic regulation of energy balance. | Lage R et al. | — | 2016 | → |
| Essential role of UCP1 modulating the central effects of thyroid hormones on energy balance. | Alvarez-Crespo M et al. | — | 2016 | → |
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| Hypothalamic AMPK: a canonical regulator of whole-body energy balance. | López M et al. | — | 2016 | → |
| Hypothalamus and thermogenesis: Heating the BAT, browning the WAT. | Contreras C et al. | — | 2016 | → |
| Metabolic effects of smoking cessation. | Harris KK et al. | — | 2016 | → |
| Molecular mechanisms of appetite and obesity: a role for brain AMPK. | Martínez de Morentin PB et al. | — | 2016 | → |
| Nighttime Administration of Nicotine Improves Hepatic Glucose Metabolism via the Hypothalamic Orexin System in Mice. | Tsuneki H et al. | — | 2016 | → |
| Self-Administered Nicotine Suppresses Body Weight Gain Independent of Food Intake in Male Rats. | Rupprecht LE et al. | — | 2016 | → |
| Activation of AMPKα2 in adipocytes is essential for nicotine-induced insulin resistance in vivo. | Wu Y et al. | — | 2015 | → |
| Cholinergic neurons in the dorsomedial hypothalamus regulate mouse brown adipose tissue metabolism. | Jeong JH et al. | — | 2015 | → |
| Come to Where Insulin Resistance Is, Come to AMPK Country. | Nogueiras R et al. | — | 2015 | → |
| Evidence for the contribution of multiple mechanisms in the feeding pattern of rats exposed to p-chloro-diphenyl diselenide-supplemented diets. | Bortolatto CF et al. | — | 2015 | → |
| Genome-wide association study of nicotine dependence in American populations: identification of novel risk loci in both African-Americans and European-Americans. | Gelernter J et al. | — | 2015 | → |
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| Hypothalamic CaMKKβ mediates glucagon anorectic effect and its diet-induced resistance. | Quiñones M et al. | — | 2015 | → |
| Hypothalamic control of brown adipose tissue thermogenesis. | Labbé SM et al. | — | 2015 | → |
| Hypothalamic GLP-1: the control of BAT thermogenesis and browning of white fat. | López M et al. | — | 2015 | → |
| Interaction of smoking and obesity susceptibility loci on adolescent BMI: The National Longitudinal Study of Adolescent to Adult Health. | Young KL et al. | — | 2015 | → |
| Neuronal Control of Brown Fat Activity. | Kooijman S et al. | — | 2015 | → |
| Orexins (hypocretins) and energy balance: More than feeding. | Fernø J et al. | — | 2015 | → |
| Possible role of afferent autonomic signals in abdominal organs in anorexic and cardiovascular responses to nicotine injection in rats. | Yagi S et al. | — | 2015 | → |
| Pregnancy induces resistance to the anorectic effect of hypothalamic malonyl-CoA and the thermogenic effect of hypothalamic AMPK inhibition in female rats. | Martínez de Morentin PB et al. | — | 2015 | → |
| Regulation of brown fat by AMP-activated protein kinase. | van Dam AD et al. | — | 2015 | → |
| Smoking is associated with increased resting energy expenditure in the general population: The NEO study. | Blauw LL et al. | — | 2015 | → |
| The brain and brown fat. | Contreras C et al. | — | 2015 | → |
| Toxicological evaluation of smokeless tobacco: 2-year chronic toxicity and carcinogenicity feeding study in Wistar Han rats. | Theophilus EH et al. | — | 2015 | → |
| Uric Acid Produces an Inflammatory Response through Activation of NF-κB in the Hypothalamus: Implications for the Pathogenesis of Metabolic Disorders. | Lu W et al. | — | 2015 | → |
| Cellular energy sensors: AMPK and beyond. | López M et al. | — | 2014 | → |
| Central ceramide-induced hypothalamic lipotoxicity and ER stress regulate energy balance. | Contreras C et al. | — | 2014 | → |
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| Concomitant alpha7 and beta2 nicotinic AChR subunit deficiency leads to impaired energy homeostasis and increased physical activity in mice. | Somm E et al. | — | 2014 | → |
| Estradiol regulates brown adipose tissue thermogenesis via hypothalamic AMPK. | Martínez de Morentin PB et al. | — | 2014 | → |
| Fatty acid sensing in the gut and the hypothalamus: in vivo and in vitro perspectives. | Duca FA et al. | — | 2014 | → |
| GLP-1 agonism stimulates brown adipose tissue thermogenesis and browning through hypothalamic AMPK. | Beiroa D et al. | — | 2014 | → |
| Hypothalamic and brainstem neuronal circuits controlling homeostatic energy balance. | Schneeberger M et al. | — | 2014 | → |
| Hypothalamic effects of thyroid hormones on metabolism. | Martínez-Sánchez N et al. | — | 2014 | → |
| Long-term increased carnitine palmitoyltransferase 1A expression in ventromedial hypotalamus causes hyperphagia and alters the hypothalamic lipidomic profile. | Mera P et al. | — | 2014 | → |
| Metformin and berberine prevent olanzapine-induced weight gain in rats. | Hu Y et al. | — | 2014 | → |
| Nicotine improves obesity and hepatic steatosis and ER stress in diet-induced obese male rats. | Seoane-Collazo P et al. | — | 2014 | → |
| Nicotinic cholinergic signaling in adipose tissue and pancreatic islets biology: revisited function and therapeutic perspectives. | Somm E | — | 2014 | → |
| Olanzapine depot formulation in rat: a step forward in modelling antipsychotic-induced metabolic adverse effects. | Skrede S et al. | — | 2014 | → |
| Analysis of factors that determine weight gain during smoking cessation therapy. | Komiyama M et al. | — | 2013 | → |
| Assessment of brown adipose tissue function. | Virtue S et al. | — | 2013 | → |
| Energy balance regulation by thyroid hormones at central level. | López M et al. | — | 2013 | → |
| Hypothalamic ceramide levels regulated by CPT1C mediate the orexigenic effect of ghrelin. | Ramírez S et al. | — | 2013 | → |
| Leptin and thyrotropin relationship is modulated by smoking status in euthyroid subjects. | Lucas A et al. | — | 2013 | → |
| Smoking status, snus use, and variation at the CHRNA5-CHRNA3-CHRNB4 locus in relation to obesity: the GLACIER study. | Varga TV et al. | — | 2013 | → |
| BMP8B increases brown adipose tissue thermogenesis through both central and peripheral actions. | Whittle AJ et al. | — | 2012 | → |
| Cigarette smoking and brain regulation of energy homeostasis. | Chen H et al. | — | 2012 | → |
| Hypothalamic mTOR signaling mediates the orexigenic action of ghrelin. | Martins L et al. | — | 2012 | → |
| Nicotine and insulin resistance: when the smoke clears. | Bajaj M | — | 2012 | → |
| Recent Insights into the Role of Hypothalamic AMPK Signaling Cascade upon Metabolic Control. | Schneeberger M et al. | — | 2012 | → |
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