Blunted leptin sensitivity during hedonic overeating can be reinstated by activating galanin 2 receptors (Gal2R) in the lateral hypothalamus.


Journal

Acta physiologica (Oxford, England)
ISSN: 1748-1716
Titre abrégé: Acta Physiol (Oxf)
Pays: England
ID NLM: 101262545

Informations de publication

Date de publication:
02 2020
Historique:
received: 24 01 2019
revised: 08 07 2019
accepted: 11 07 2019
pubmed: 17 7 2019
medline: 29 6 2021
entrez: 17 7 2019
Statut: ppublish

Résumé

Since foods with high hedonic value are often consumed in excess of energetic needs, this study was designed to identify the mechanisms that may counter anorexigenic signalling in the presence of hedonic foods in lean animals. Mice, in different states of satiety (fed/fasted, or fed/fasted and treated with ghrelin or leptin, respectively), were allowed to choose between high-fat/high-sucrose and standard foods. Intake of each food type and the activity of hypothalamic neuropetidergic neurons that regulate appetite were monitored. In some cases, food choice was monitored in leptin-injected fasted mice that received microinjections of galanin receptor agonists into the lateral hypothalamus. Appetite-stimulating orexin neurons in the lateral hypothalamus are rapidly activated when lean, satiated mice consume a highly palatable food (PF); such activation (upregulated c-Fos expression) occurred even after administration of the anorexigenic hormone leptin and despite intact leptin signalling in the hypothalamus. The ability of leptin to restrain PF eating is restored when a galanin receptor 2 (Gal2R) agonist is injected into the lateral hypothalamus. Hedonically-loaded foods interrupt the inhibitory actions of leptin on orexin neurons and interfere with the homeostatic control of feeding. Overeating of palatable foods can be curtailed in lean animals by activating Gal2R in the lateral hypothalamus.

Identifiants

pubmed: 31310704
doi: 10.1111/apha.13345
doi:

Substances chimiques

Ghrelin 0
Leptin 0
Orexins 0
Receptor, Galanin, Type 2 0
Galanin 88813-36-9

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e13345

Informations de copyright

© 2019 The Authors. Acta Physiologica published by John Wiley & Sons Ltd on behalf of Scandinavian Physiological Society.

Références

Swinburn BA, Sacks G, Hall KD, et al. The global obesity pandemic: shaped by global drivers and local environments. Lancet (London, England). 2011;378(9793):804-814.
Myers MG, Leibel RL, Seeley RJ, Schwartz MW. Obesity and leptin resistance: distinguishing cause from effect. Trends Endocrinol Metab. 2010;21(11):643-651.
Morton GJ, Meek TH, Schwartz MW. Neurobiology of food intake in health and disease. Nat Rev Neurosci. 2014;15(6):367-378.
Liu J-J, Bello NT, Pang ZP. Presynaptic regulation of leptin in a defined lateral hypothalamus-ventral tegmental area neurocircuitry depends on energy state. J Neurosci. 2017;37(49):11854-11866.
Berridge KC, Kringelbach ML. Neuroscience of affect: brain mechanisms of pleasure and displeasure. Curr Opin Neurobiol. 2013;23(3):294-303.
Kojima M, Hosoda H, Date Y, Nakazato M, Matsuo H, Kangawa K. Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature. 1999;402(6762):656-660.
Kojima M, Kangawa K. Ghrelin: structure and function. Physiol Rev. 2005;85(2):495-522.
Tschöp M, Weyer C, Tataranni PA, Devanarayan V, Ravussin E, Heiman ML. Circulating ghrelin levels are decreased in human obesity. Diabetes. 2001;50(4):707-709.
Greenman Y, Golani N, Gilad S, Yaron M, Limor R, Stern N. Ghrelin secretion is modulated in a nutrient- and gender-specific manner. Clin Endocrinol (Oxf). 2004;60(3):382-388.
Friedman J. 20 years of leptin: leptin at 20: an overview. J Endocrinol. 2014;223(1):T1-T8.
El-Haschimi K, Pierroz DD, Hileman SM, Bjørbaek C, Flier JS. Two defects contribute to hypothalamic leptin resistance in mice with diet-induced obesity. J Clin Invest. 2000;105(12):1827-1832.
Münzberg H, Flier JS, Bjørbaek C. Region-specific leptin resistance within the hypothalamus of diet-induced obese mice. Endocrinology. 2004;145(11):4880-4889.
Elmquist JK, Coppari R, Balthasar N, Ichinose M, Lowell BB. Identifying hypothalamic pathways controlling food intake, body weight, and glucose homeostasis. J Comp Neurol. 2005;493(1):63-71.
Laque A, Zhang Y, Gettys S, et al. Leptin receptor neurons in the mouse hypothalamus are colocalized with the neuropeptide galanin and mediate anorexigenic leptin action. Am J Physiol Endocrinol Metab. 2013;304(9):E999-E1011.
López-Ferreras L, Richard JE, Anderberg RH, et al. Ghrelin’s control of food reward and body weight in the lateral hypothalamic area is sexually dimorphic. Physiol Behav. 2017;176:40-49.
Shintani M, Ogawa Y, Ebihara K, et al. Ghrelin, an endogenous growth hormone secretagogue, is a novel orexigenic peptide that antagonizes leptin action through the activation of hypothalamic neuropeptide Y/Y1 receptor pathway. Diabetes. 2001;50(2):227-232.
Chen HY, Trumbauer ME, Chen AS, et al. Orexigenic action of peripheral ghrelin is mediated by neuropeptide Y and agouti-related protein. Endocrinology. 2004;145(6):2607-2612.
Diano S, Horvath B, Urbanski HF, Sotonyi P, Horvath TL. Fasting activates the nonhuman primate hypocretin (orexin) system and its postsynaptic targets. Endocrinology. 2003;144(9):3774-3778.
Yamanaka A, Beuckmann CT, Willie JT, et al. Hypothalamic orexin neurons regulate arousal according to energy balance in mice. Neuron. 2003;38(5):701-713.
Toshinai K, Date Y, Murakami N, et al. Ghrelin-induced food intake is mediated via the orexin pathway. Endocrinology. 2003;144(4):1506-1512.
Elias CF, Aschkenasi C, Lee C, et al. Leptin differentially regulates NPY and POMC neurons projecting to the lateral hypothalamic area. Neuron. 1999;23(4):775-786.
Nair SG, Golden SA, Shaham Y. Differential effects of the hypocretin 1 receptor antagonist SB 334867 on high-fat food self-administration and reinstatement of food seeking in rats. Br J Pharmacol. 2009;154(2):406-416.
Borgland SL, Chang S-J, Bowers MS, et al. Orexin A/hypocretin-1 selectively promotes motivation for positive reinforcers. J Neurosci. 2009;29(36):11215-11225.
Laque A, Yu S, Qualls-Creekmore E, et al. Leptin modulates nutrient reward via inhibitory galanin action on orexin neurons. Mol Metab. 2015;4(10):706-717.
Goforth PB, Leinninger GM, Patterson CM, Satin LS, Myers MG. Leptin acts via lateral hypothalamic area neurotensin neurons to inhibit orexin neurons by multiple GABA-independent mechanisms. J Neurosci. 2014;34(34):11405-11415.
Louis GW, Leinninger GM, Rhodes CJ, Myers MG. Direct innervation and modulation of orexin neurons by lateral hypothalamic LepRb neurons. J Neurosci. 2010;30(34):11278-11287.
Leinninger GM, Jo Y-H, Leshan RL, et al. Leptin acts via leptin receptor-expressing lateral hypothalamic neurons to modulate the mesolimbic dopamine system and suppress feeding. Cell Metab. 2009;10(2):89-98.
Leinninger G, Opland D, Jo Y-H, et al. Leptin action via neurotensin neurons controls orexin, the mesolimbic dopamine system and energy balance. Cell Metab. 2011;14(3):313-323.
Bullitt E. Expression ofC-fos-like protein as a marker for neuronal activity following noxious stimulation in the rat. J Comp Neurol. 1990;296(4):517-530. https://doi.org/10.1002/cne.902960402.
Perrin-Terrin A-S, Jeton F, Pichon A, et al. The c-FOS protein immunohistological detection: a useful tool as a marker of central pathways involved in specific physiological responses in vivo and ex vivo. J Vis Exp. 2016;110:e53613.
Sakurai T, Amemiya A, Ishii M, et al. Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell. 1998;92(4):573-585.
López M, Seoane L, del Carmen García M, et al. Leptin regulation of prepro-orexin and orexin receptor mRNA levels in the hypothalamus. Biochem Biophys Res Commun. 2000;269(1):41-45.
Schwartz MW, Seeley RJ, Campfield LA, Burn P, Baskin DG. Identification of targets of leptin action in rat hypothalamus. J Clin Invest. 1996;98(5):1101-1106.
Elias CF, Lee C, Kelly J, et al. Leptin activates hypothalamic CART neurons projecting to the spinal cord. Neuron. 1998;21(6):1375-1385.
Kleinridders A, Schenten D, Könner AC, et al. MyD88 signaling in the CNS is required for development of fatty acid-induced leptin resistance and diet-induced obesity. Cell Metab. 2009;10(4):249-259.
Sohn J-W, Elmquist JK, Williams KW. Neuronal circuits that regulate feeding behavior and metabolism. Trends Neurosci. 2013;36(9):504-512.
Magnan C, Levin BE, Luquet S. Brain lipid sensing and the neural control of energy balance. Mol Cell Endocrinol. 2015;418:3-8.
Lee M-J, Fried SK. Integration of hormonal and nutrient signals that regulate leptin synthesis and secretion. Am J Physiol Metab. 2009;296(6):E1230-E1238.
Webling K, Runesson J, Bartfai T, Langel Ü. Galanin receptors and ligands. Front Endocrinol (Lausanne). 2012;3:146.
Egecioglu E, Jerlhag E, Salomé N, et al. Ghrelin increases intake of rewarding food in rodents. Addict Biol. 2010;15(3):304-311.
Perello M, Sakata I, Birnbaum S, et al. Ghrelin increases the rewarding value of high-fat diet in an orexin-dependent manner. Biol Psychiatry. 2010;67(9):880-886.
Cone JJ, McCutcheon JE, Roitman MF. Ghrelin acts as an interface between physiological state and phasic dopamine signaling. J Neurosci. 2014;34(14):4905-4913.
Berthoud H-R, Münzberg H. The lateral hypothalamus as integrator of metabolic and environmental needs: from electrical self-stimulation to opto-genetics. Physiol Behav. 2011;104(1):29-39.
Shizgal P, Bielajew C, Corbett D, Skelton R, Yeomans J. Behavioral methods for inferring anatomical linkage between rewarding brain stimulation sites. J Comp Physiol Psychol. 1980;94(2):227-237.
Nieh E, Matthews G, Allsop S, et al. Decoding neural circuits that control compulsive sucrose seeking. Cell. 2015;160(3):528-541.
Tyree SM, de Lecea L. Lateral hypothalamic control of the ventral tegmental area: reward evaluation and the driving of motivated behavior. Front Syst Neurosci. 2017;11:50.
Wortley KE, Chang G-Q, Davydova Z, Leibowitz SF. Peptides that regulate food intake: orexin gene expression is increased during states of hypertriglyceridemia. Am J Physiol Regul Integr Comp Physiol. 2003;284(6):R1454-R1465.
Harris GC, Wimmer M, Aston-Jones G. A role for lateral hypothalamic orexin neurons in reward seeking. Nature. 2005;437(7058):556-559.
Valdivia S, Patrone A, Reynaldo M, Perello M. Acute high fat diet consumption activates the mesolimbic circuit and requires orexin signaling in a mouse model. Chowen JA, ed. PLoS ONE. 2014;9(1):e87478.
Valdivia S, Cornejo MP, Reynaldo M, De Francesco PN, Perello M. Escalation in high fat intake in a binge eating model differentially engages dopamine neurons of the ventral tegmental area and requires ghrelin signaling. Psychoneuroendocrinology. 2015;60:206-216.
Ossewaarde L, Qin S, Van Marle H, van Wingen GA, Fernández G, Hermans EJ. Stress-induced reduction in reward-related prefrontal cortex function. NeuroImage. 2011;55(1):345-352.
Graf EN, Wheeler RA, Baker DA, et al. Corticosterone Acts in the Nucleus Accumbens to Enhance Dopamine Signaling and Potentiate Reinstatement of Cocaine Seeking. J Neurosci. 2013;33(29):11800-11810.
Bonnavion P, Jackson AC, Carter ME, de Lecea L. Antagonistic interplay between hypocretin and leptin in the lateral hypothalamus regulates stress responses. Nat Commun. 2015;6(1):6266.
Leibowitz SF. Regulation and effects of hypothalamic galanin: relation to dietary fat, alcohol ingestion, circulating lipids and energy homeostasis. Neuropeptides. 2005;39(3):327-332. https://doi.org/10.1016/j.npep.2004.12.022.
Qualls-Creekmore E, Yu S, Francois M, et al. Galanin-Expressing GABA Neurons in the Lateral Hypothalamus Modulate Food Reward and Noncompulsive Locomotion. J Neurosci. 2017;37(25):6053-6065.
Root DH, Melendez RI, Zaborszky L, Napier TC. The ventral pallidum: Subregion-specific functional anatomy and roles in motivated behaviors. Prog Neurogibol. 2015;130:29-70.
Woods SC, Begg DP. Food for Thought: Revisiting the Complexity of Food Intake. Cell Metab. 2015;22(3):348-351.
Koch M, Varela L, Kim JG, et al. Hypothalamic POMC neurons promote cannabinoid-induced feeding. Nature. 2015;519(7541):45-50.
Fenselau H, Campbell JN, Verstegen A, et al. A rapidly acting glutamatergic ARC→PVH satiety circuit postsynaptically regulated by α-MSH. Nat Neurosci. 2017;20(1):42-51.
Campbell JN, Macosko EZ, Fenselau H, et al. A molecular census of arcuate hypothalamus and median eminence cell types. Nat Neurosci. 2017;20(3):484-496.
Castro DC, Berridge KC. Opioid and orexin hedonic hotspots in rat orbitofrontal cortex and insula. Proc Natl Acad Sci U S A. 2017;114(43):E9125-E9134.
Hommel JD, Trinko R, Sears RM, et al. Leptin Receptor Signaling in Midbrain Dopamine Neurons Regulates Feeding. Neuron. 2006;51(6):801-810.
Domingos AI, Vaynshteyn J, Voss HU, et al. Leptin regulates the reward value of nutrient. Nat Neurosci. 2011;14(12):1562-1568.
Castro DC, Cole SL, Berridge KC. Lateral hypothalamus, nucleus accumbens, and ventral pallidum roles in eating and hunger: interactions between homeostatic and reward circuitry. Front Syst Neurosci. 2015;9:90.
Risco S, Mediavilla C. Orexin-1 receptor antagonist in central nucleus of the amygdala attenuates the acquisition of flavor-taste preference in rats. Pharmacol Biochem Behav. 2014;126:7-12.
Terrill SJ, Hyde KM, Kay KE, et al. Ventral tegmental area orexin 1 receptors promote palatable food intake and oppose postingestive negative feedback. Am J Physiol Integr Comp Physiol. 2016;311(3):R592-R599.
Wang L, Saint-Pierre DH, Taché Y. Peripheral ghrelin selectively increases Fos expression in neuropeptide Y - synthesizing neurons in mouse hypothalamic arcuate nucleus. Neurosci Lett. 2002;325(1):47-51.
Yannielli PC, Molyneux PC, Harrington ME, Golombek DA. Ghrelin effects on the circadian system of mice. J Neurosci. 2007;27(11):2890-2895.
Jerlhag E. Systemic administration of ghrelin induces conditioned place preference and stimulates accumbal dopamine. Addict Biol. 2008;13(3-4):358-363.
Vaisse C, Halaas JL, Horvath CM, Darnell JE, Stoffel M, Friedman JM. Leptin activation of Stat3 in the hypothalamus of wild-type and ob/ob mice but not db/db mice. Nat Genet. 1996;14(1):95-97.
Margetic S, Gazzola C, Pegg G, Hill R. Leptin: a review of its peripheral actions and interactions. Int J Obes. 2002;26(11):1407-1433.
Franklin K, Paxinos G. The Mouse Brain in Stereotaxic Coordinates. Boston: Elsevier Academic Press; 2008.
Lundstrӧm L, Sollenberg U, Brewer A, et al. A Galanin Receptor Subtype 1 Specific Agonist. Int J Pept Res Ther. 2005;11(1):17-27.
Blackshear A, Yamamoto M, Anderson BJ, et al. Intracerebroventricular administration of galanin or galanin receptor subtype 1 agonist M617 induces c-Fos activation in central amygdala and dorsomedial hypothalamus. Peptides. 2007;28(5):1120-1124.
Runesson J, Saar I, Lundström L, Järv J, Langel U. A novel GalR2-specific peptide agonist. Neuropeptides. 2009;43(3):187-192.
Saar I, Runesson J, McNamara I, Järv J, Robinson JK, Langel U. Novel galanin receptor subtype specific ligands in feeding regulation. Neurochem Int. 2011;58(6):714-720.
Murgatroyd C, Patchev AV, Wu Y, et al. Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nat Neurosci. 2009;12(12):1559-1566.
Liposits Z, Sétáló G, Flerkó B. Application of the silver-gold intensified 3,3’-diaminobenzidine chromogen to the light and electron microscopic detection of the luteinizing hormone-releasing hormone system of the rat brain. Neuroscience. 1984;13(2):513-525.

Auteurs

Este Leidmaa (E)

Max Planck Institute of Psychiatry, Munich, Germany.
Graduate School of Systems Neuroscience, Munich University, Planegg-Martinsried, Germany.
Institute of Molecular Psychiatry, Bonn, Germany.

Mary Gazea (M)

Max Planck Institute of Psychiatry, Munich, Germany.

Alexandre V Patchev (AV)

Max Planck Institute of Psychiatry, Munich, Germany.

Anna Pissioti (A)

Max Planck Institute of Psychiatry, Munich, Germany.

Nils Christian Gassen (N)

Max Planck Institute of Psychiatry, Munich, Germany.

Mayumi Kimura (M)

Max Planck Institute of Psychiatry, Munich, Germany.

Zsolt Liposits (Z)

Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, Hungary.

Imre Kallo (I)

Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, Hungary.

Osborne F X Almeida (OFX)

Max Planck Institute of Psychiatry, Munich, Germany.

Articles similaires

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male
Humans Meals Time Factors Female Adult

Classifications MeSH