Cannabinoid receptor signaling in central regulation of feeding behavior: A mini-review

Frontiers in Neuroscience

Volumn 11, Issue MAY, 2017, Pages

  Koch, Marco ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

Anorexia; Cachexia; Cannabinoid receptor type 1; Endocannabinoids; Feeding behavior; Hypothalamus; Obesity; Overeating

Indexed keywords

CANNABINOID; CANNABINOID 1 RECEPTOR;

DRUG TARGETING; FEEDING BEHAVIOR; FOOD INTAKE; HOMEOSTASIS; HUMAN; NONHUMAN; PLEASURE; SHORT SURVEY; SIGNAL TRANSDUCTION;

EID: 85019609143     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2017.00293     Document Type: Short Survey

References (92)

1. Aigner, M., Treasure, J., Kaye, W., Kasper, S., and Disorders, W.T.F.O.E. (2011). World Federation of Societies of Biological Psychiatry (WFSBP) guidelines for the pharmacological treatment of eating disorders. World J. Biol. Psychiatry 12, 400-443. doi: 10.3109/15622975.2011.602720
2. Alonso-Alonso, M., Woods, S. C., Pelchat, M., Grigson, P. S., Stice, E., Farooqi, S., et al. (2015). Food reward system: current perspectives and future research needs. Nutr. Rev. 73, 296-307. doi: 10.1093/nutrit/nuv002
3. Alpar, A., and Harkany, T. (2013). Orexin neurons use endocannabinoids to break obesity-induced inhibition. Proc. Natl. Acad. Sci. U.S.A. 110, 9625-9626. doi: 10.1073/pnas.1307389110
4. Argente-Arizon, P., Guerra-Cantera, S., Garcia-Segura, L. M., Argente, J., and Chowen, J. A. (2017). Glial cells and energy balance. J. Mol. Endocrinol. 58, R59-R71. doi: 10.1530/JME-16-0182
5. Baufeld, C., Osterloh, A., Prokop, S., Miller, K. R., and Heppner, F. L. (2016). High-fat diet-induced brain region-specific phenotypic spectrum of CNS resident microglia. Acta Neuropathol. 132, 361-375. doi: 10.1007/s00401-016-1595-4
6. Bellocchio, L., Lafenetre, P., Cannich, A., Cota, D., Puente, N., Grandes, P., et al. (2010). Bimodal control of stimulated food intake by the endocannabinoid system. Nat. Neurosci. 13, 281-283. doi: 10.1038/nn.2494
7. Benard, G., Massa, F., Puente, N., Lourenco, J., Bellocchio, L., Soria-Gomez, E., et al. (2012). Mitochondrial CB(1) receptors regulate neuronal energy metabolism. Nat. Neurosci. 15, 558-564. doi: 10.1038/nn.3053
8. Bosier, B., Bellocchio, L., Metna-Laurent, M., Soria-Gomez, E., Matias, I., Hebert-Chatelain, E., et al. (2013). Astroglial CB1 cannabinoid receptors regulate leptin signaling in mouse brain astrocytes. Mol. Metab. 2, 393-404. doi: 10.1016/j.molmet.2013.08.001
9. Busquets Garcia, A., Soria-Gomez, E., Bellocchio, L., and Marsicano, G. (2016). Cannabinoid receptor type-1: breaking the dogmas. F1000Res 2016:5. doi: 10.12688/f1000research.8245.1
10. Campbell, J. N., Macosko, E. Z., Fenselau, H., Pers, T. H., Lyubetskaya, A., Tenen, D., et al. (2017). A molecular census of arcuate hypothalamus and median eminence cell types. Nat. Neurosci. 20, 484-496. doi: 10.1038/nn.4495
11. Cardinal, P., Bellocchio, L., Clark, S., Cannich, A., Klugmann, M., Lutz, B., et al. (2012). Hypothalamic CB1 cannabinoid receptors regulate energy balance in mice. Endocrinology 153, 4136-4143. doi: 10.1210/en.2012-1405
12. Castillo, P. E., Younts, T. J., Chavez, A. E., and Hashimotodani, Y. (2012). Endocannabinoid signaling and synaptic function. Neuron 76, 70-81. doi: 10.1016/j.neuron.2012.09.020
13. Chen, Y., Lin, Y. C., Kuo, T. W., and Knight, Z. A. (2015). Sensory detection of food rapidly modulates arcuate feeding circuits. Cell 160, 829-841. doi: 10.1016/j.cell.2015.01.033
14. Colombo, G., Agabio, R., Diaz, G., Lobina, C., Reali, R., and Gessa, G. L. (1998). Appetite suppression and weight loss after the cannabinoid antagonist SR 141716. Life Sci. 63, PL113-PL117. doi: 10.1016/S0024-3205(98)00322-1
15. Cota, D., Marsicano, G., Tschop, M., Grubler, Y., Flachskamm, C., Schubert, M., et al. (2003). The endogenous cannabinoid system affects energy balance via central orexigenic drive and peripheral lipogenesis. J. Clin. Invest. 112, 423-431. doi: 10.1172/JCI17725
16. Cristino, L., Busetto, G., Imperatore, R., Ferrandino, I., Palomba, L., Silvestri, C., et al. (2013). Obesity-driven synaptic remodeling affects endocannabinoid control of orexinergic neurons. Proc. Natl. Acad. Sci. U.S.A. 110, E2229-E2238. doi: 10.1073/pnas.1219485110
17. Devane, W. A., Hanus, L., Breuer, A., Pertwee, R. G., Stevenson, L. A., Griffin, G., et al. (1992). Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 258, 1946-1949. doi: 10.1126/science.1470919
18. Di Marzo, V., Goparaju, S. K., Wang, L., Liu, J., Batkai, S., Jarai, Z., et al. (2001). Leptin-regulated endocannabinoids are involved in maintaining food intake. Nature 410, 822-825. doi: 10.1038/35071088
19. Di Marzo, V., Ligresti, A., and Cristino, L. (2009). The endocannabinoid system as a link between homoeostatic and hedonic pathways involved in energy balance regulation. Int. J. Obes. 33(Suppl. 2), S18-S24. doi: 10.1038/ijo.2009.67
20. Dietrich, M. O., and Horvath, T. L. (2012). Limitations in anti-obesity drug development: the critical role of hunger-promoting neurons. Nat. Rev. Drug Discov. 11, 675-691. doi: 10.1038/nrd3739
21. Dodd, G. T., Mancini, G., Lutz, B., and Luckman, S. M. (2010). The peptide hemopressin acts through CB1 cannabinoid receptors to reduce food intake in rats and mice. J. Neurosci. 30, 7369-7376. doi: 10.1523/JNEUROSCI.5455-09.2010
22. Dodd, G. T., Worth, A. A., Hodkinson, D. J., Srivastava, R. K., Lutz, B., Williams, S. R., et al. (2013). Central functional response to the novel peptide cannabinoid, hemopressin. Neuropharmacology 71, 27-36. doi: 10.1016/j.neuropharm.2013.03.007
23. Engeli, S. (2008). Dysregulation of the endocannabinoid system in obesity. J. Neuroendocrinol. 20(Suppl. 1), 110-115. doi: 10.1111/j.1365-2826.2008.01683.x
24. Fenselau, H., Campbell, J. N., Verstegen, A. M., Madara, J. C., Xu, J., Shah, B. P., et al. (2017). A rapidly acting glutamatergic ARC→PVH satiety circuit postsynaptically regulated by alpha-MSH. Nat. Neurosci. 20, 42-51. doi: 10.1038/nn.4442
25. Fisette, A., Tobin, S., Decarie-Spain, L., Bouyakdan, K., Peyot, M. L., Madiraju, S. R., et al. (2016). Alpha/beta-hydrolase domain 6 in the ventromedial hypothalamus controls energy metabolism flexibility. Cell Rep. 17, 1217-1226. doi: 10.1016/j.celrep.2016.10.004
26. Fu, J., Gaetani, S., Oveisi, F., Lo Verme, J., Serrano, A., Rodriguez De Fonseca, F., et al. (2003). Oleylethanolamide regulates feeding and body weight through activation of the nuclear receptor PPAR-alpha. Nature 425, 90-93. doi: 10.1038/nature01921
27. Gaetani, S., Fu, J., Cassano, T., Dipasquale, P., Romano, A., Righetti, L., et al. (2010). The fat-induced satiety factor oleoylethanolamide suppresses feeding through central release of oxytocin. J. Neurosci. 30, 8096-8101. doi: 10.1523/JNEUROSCI.0036-10.2010
28. Gao, X. B., and Horvath, T. L. (2016). Feeding behavior: hypocretin/orexin neurons act between food seeking and eating. Curr. Biol. 26, R845-R847. doi: 10.1016/j.cub.2016.07.069
29. Grygiel-Gorniak, B. (2014). Peroxisome proliferator-activated receptors and their ligands: nutritional and clinical implications-a review. Nutr. J. 13:17. doi: 10.1186/1475-2891-13-17
30. Han, J., Kesner, P., Metna-Laurent, M., Duan, T., Xu, L., Georges, F., et al. (2012). Acute cannabinoids impair working memory through astroglial CB1 receptor modulation of hippocampal LTD. Cell 148, 1039-1050. doi: 10.1016/j.cell.2012.01.037
31. Harkany, T., and Horvath, T. L. (2017). (S)Pot on mitochondria: cannabinoids disrupt cellular respiration to limit neuronal activity. Cell Metab. 25, 8-10. doi: 10.1016/j.cmet.2016.12.020
32. Hebert-Chatelain, E., Desprez, T., Serrat, R., Bellocchio, L., Soria-Gomez, E., Busquets-Garcia, A., et al. (2016). A cannabinoid link between mitochondria and memory. Nature 539, 555-559. doi: 10.1038/nature20127
33. Hebert-Chatelain, E., Reguero, L., Puente, N., Lutz, B., Chaouloff, F., Rossignol, R., et al. (2014). Cannabinoid control of brain bioenergetics: exploring the subcellular localization of the CB1 receptor. Mol. Metab. 3, 495-504. doi: 10.1016/j.molmet.2014.03.007
34. Heimann, A. S., Gomes, I., Dale, C. S., Pagano, R. L., Gupta, A., De Souza, L. L., et al. (2007). Hemopressin is an inverse agonist of CB1 cannabinoid receptors. Proc. Natl. Acad. Sci. U.S.A. 104, 20588-20593. doi: 10.1073/pnas.0706980105
35. Hentges, S. T., Low, M. J., and Williams, J. T. (2005). Differential regulation of synaptic inputs by constitutively released endocannabinoids and exogenous cannabinoids. J. Neurosci. 25, 9746-9751. doi: 10.1523/JNEUROSCI.2769-05.2005
36. Herkenham, M., Lynn, A. B., Little, M. D., Johnson, M. R., Melvin, L. S., De Costa, B. R., et al. (1990). Cannabinoid receptor localization in brain. Proc. Natl. Acad. Sci. U.S.A. 87, 1932-1936. doi: 10.1073/pnas.87.5.1932
37. Horvath, T. L. (2003). Endocannabinoids and the regulation of body fat: the smoke is clearing. J. Clin. Invest. 112, 323-326. doi: 10.1172/JCI19376
38. Hua, T., Vemuri, K., Pu, M., Qu, L., Han, G. W., Wu, Y., et al. (2016). Crystal structure of the human cannabinoid receptor CB1. Cell 167, 750 e714-762 e714. doi: 10.1016/j.cell.2016.10.004
39. Jamshidi, N., and Taylor, D. A. (2001). Anandamide administration into the ventromedial hypothalamus stimulates appetite in rats. Br. J. Pharmacol. 134, 1151-1154. doi: 10.1038/sj.bjp.0704379
40. Kim, J. G., Suyama, S., Koch, M., Jin, S., Argente-Arizon, P., Argente, J., et al. (2014). Leptin signaling in astrocytes regulates hypothalamic neuronal circuits and feeding. Nat. Neurosci. 17, 908-910. doi: 10.1038/nn.3725
41. Koch, M., and Horvath, T. L. (2014). Molecular and cellular regulation of hypothalamic melanocortin neurons controlling food intake and energy metabolism. Mol. Psychiatry 19, 752-761. doi: 10.1038/mp.2014.30
42. Koch, M., Varela, L., Kim, J. G., Kim, J. D., Hernandez-Nuno, F., Simonds, S. E., et al. (2015). Hypothalamic POMC neurons promote cannabinoid-induced feeding. Nature 519, 45-50. doi: 10.1038/nature14260
43. Kola, B., Farkas, I., Christ-Crain, M., Wittmann, G., Lolli, F., Amin, F., et al. (2008). The orexigenic effect of ghrelin is mediated through central activation of the endogenous cannabinoid system. PLoS ONE 3:e1797. doi: 10.1371/journal.pone.0001797
44. Kruger, R. P. (2016). Harvesting benefits from cannabinoids. Cell 167, 1663-1665. doi: 10.1016/j.cell.2016.12.001
45. Leishman, E., Cornett, B., Spork, K., Straiker, A., Mackie, K., and Bradshaw, H. B. (2016a). Broad impact of deleting endogenous cannabinoid hydrolyzing enzymes and the CB1 cannabinoid receptor on the endogenous cannabinoid-related lipidome in eight regions of the mouse brain. Pharmacol. Res. 110, 159-172. doi: 10.1016/j.phrs.2016.04.020
46. Leishman, E., Mackie, K., Luquet, S., and Bradshaw, H. B. (2016b). Lipidomics profile of a NAPE-PLD KO mouse provides evidence of a broader role of this enzyme in lipid metabolism in the brain. Biochim. Biophys. Acta 1861, 491-500. doi: 10.1016/j.bbalip.2016.03.003
47. Liu, B., Song, S., Jones, P. M., and Persaud, S. J. (2015). GPR55: from orphan to metabolic regulator? Pharmacol. Ther. 145, 35-42. doi: 10.1016/j.pharmthera.2014.06.007
48. Lo Verme, J., Fu, J., Astarita, G., La Rana, G., Russo, R., Calignano, A., et al. (2005). The nuclear receptor peroxisome proliferator-activated receptor-alpha mediates the anti-inflammatory actions of palmitoylethanolamide. Mol. Pharmacol. 67, 15-19. doi: 10.1124/mol.104.006353
49. Lutz, B., Marsicano, G., Maldonado, R., and Hillard, C. J. (2015). The endocannabinoid system in guarding against fear, anxiety and stress. Nat. Rev. Neurosci. 16, 705-718. doi: 10.1038/nrn4036
50. Matsuda, L. A., Lolait, S. J., Brownstein, M. J., Young, A. C., and Bonner, T. I. (1990). Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 346, 561-564. doi: 10.1038/346561a0
51. Mazier, W., Saucisse, N., Gatta-Cherifi, B., and Cota, D. (2015). The endocannabinoid system: pivotal orchestrator of obesity and metabolic disease. Trends Endocrinol. Metab. 26, 524-537. doi: 10.1016/j.tem.2015.07.007
52. Melis, T., Succu, S., Sanna, F., Boi, A., Argiolas, A., and Melis, M. R. (2007). The cannabinoid antagonist SR 141716A (Rimonabant) reduces the increase of extra-cellular dopamine release in the rat nucleus accumbens induced by a novel high palatable food. Neurosci. Lett. 419, 231-235. doi: 10.1016/j.neulet.2007.04.012
53. Metna-Laurent, M., and Marsicano, G. (2015). Rising stars: modulation of brain functions by astroglial type-1 cannabinoid receptors. Glia 63, 353-364. doi: 10.1002/glia.22773
54. Morello, G., Imperatore, R., Palomba, L., Finelli, C., Labruna, G., Pasanisi, F., et al. (2016). Orexin-A represses satiety-inducing POMC neurons and contributes to obesity via stimulation of endocannabinoid signaling. Proc. Natl. Acad. Sci. U.S.A. 113, 4759-4764. doi: 10.1073/pnas.1521304113
55. Morozov, Y. M., Koch, M., Rakic, P., and Horvath, T. L. (2017). Cannabinoid type 1 receptor-containing axons innervate NPY/AgRP neurons in the mouse arcuate nucleus. Mol. Metab. 6, 374-381. doi: 10.1016/j.molmet.2017.01.004
56. Muller, T. D., Nogueiras, R., Andermann, M. L., Andrews, Z. B., Anker, S. D., Argente, J., et al. (2015). Ghrelin. Mol. Metab. 4, 437-460. doi: 10.1016/j.molmet.2015.03.005
57. Munzberg, H., Qualls-Creekmore, E., Yu, S., Morrison, C. D., and Berthoud, H. R. (2016). Hedonics act in unison with the homeostatic system to unconsciously control body weight. Front Nutr 3:6. doi: 10.3389/fnut.2016.00006
58. Navarrete, M., and Araque, A. (2010). Endocannabinoids potentiate synaptic transmission through stimulation of astrocytes. Neuron 68, 113-126. doi: 10.1016/j.neuron.2010.08.043
59. Nogueiras, R., Veyrat-Durebex, C., Suchanek, P. M., Klein, M., Tschop, J., Caldwell, C., et al. (2008). Peripheral, but not central, CB1 antagonism provides food intake-independent metabolic benefits in diet-induced obese rats. Diabetes 57, 2977-2991. doi: 10.2337/db08-0161
60. Oliveira Da Cruz, J. F., Robin, L. M., Drago, F., Marsicano, G., and Metna-Laurent, M. (2016). Astroglial type-1 cannabinoid receptor (CB1): a new player in the tripartite synapse. Neuroscience 323, 35-42. doi: 10.1016/j.neuroscience.2015.05.002
61. Palomba, L., Silvestri, C., Imperatore, R., Morello, G., Piscitelli, F., Martella, A., et al. (2015). Negative regulation of leptin-induced Reactive Oxygen Species (ROS) formation by cannabinoid CB1 receptor activation in hypothalamic neurons. J. Biol. Chem. 290, 13669-13677. doi: 10.1074/jbc.M115.646885
62. Pandurangan, M., and Hwang, I. (2015). Systemic mechanism of taste, flavour and palatability in brain. Appl. Biochem. Biotechnol. 175, 3133-3147. doi: 10.1007/s12010-015-1488-3
63. Park, R. J., Godier, L. R., and Cowdrey, F. A. (2014). Hungry for reward: how can neuroscience inform the development of treatment for Anorexia Nervosa? Behav. Res. Ther. 62, 47-59. doi: 10.1016/j.brat.2014.07.007
64. Patel, S., and Cone, R. D. (2015). Neuroscience: a cellular basis for the munchies. Nature 519, 38-40. doi: 10.1038/nature14206
65. Pertwee, R. G. (2010). Receptors and channels targeted by synthetic cannabinoid receptor agonists and antagonists. Curr. Med. Chem. 17, 1360-1381. doi: 10.2174/092986710790980050
66. Pertwee, R. G. (2014). Elevating endocannabinoid levels: pharmacological strategies and potential therapeutic applications. Proc. Nutr. Soc. 73, 96-105. doi: 10.1017/S0029665113003649
67. Pinto, S., Roseberry, A. G., Liu, H., Diano, S., Shanabrough, M., Cai, X., et al. (2004). Rapid rewiring of arcuate nucleus feeding circuits by leptin. Science 304, 110-115. doi: 10.1126/science.1089459
68. Piomelli, D. (2003). The molecular logic of endocannabinoid signalling. Nat. Rev. Neurosci. 4, 873-884. doi: 10.1038/nrn1247
69. Rajaraman, G., Simcocks, A., Hryciw, D. H., Hutchinson, D. S., and Mcainch, A. J. (2016). G protein coupled receptor 18: a potential role for endocannabinoid signaling in metabolic dysfunction. Mol. Nutr. Food Res. 60, 92-102. doi: 10.1002/mnfr.201500449
70. Reuter, S. E., and Martin, J. H. (2016). Pharmacokinetics of cannabis in cancer cachexia-anorexia syndrome. Clin. Pharmacokinet. 55, 807-812. doi: 10.1007/s40262-015-0363-2
71. Romanov, R. A., Zeisel, A., Bakker, J., Girach, F., Hellysaz, A., Tomer, R., et al. (2017). Molecular interrogation of hypothalamic organization reveals distinct dopamine neuronal subtypes. Nat. Neurosci. 20, 176-188. doi: 10.1038/nn.4462
72. Rouzer, C. A., and Marnett, L. J. (2011). Endocannabinoid oxygenation by cyclooxygenases, lipoxygenases, and cytochromes P450: cross-talk between the eicosanoid and endocannabinoid signaling pathways. Chem. Rev. 111, 5899-5921. doi: 10.1021/cr2002799
73. Savinainen, J. R., Saario, S. M., and Laitinen, J. T. (2012). The serine hydrolases MAGL, ABHD6 and ABHD12 as guardians of 2-arachidonoylglycerol signalling through cannabinoid receptors. Acta Physiol. 204, 267-276. doi: 10.1111/j.1748-1716.2011.02280.x
74. Scarlett, J. M., and Marks, D. L. (2005). The use of melanocortin antagonists in cachexia of chronic disease. Expert Opin. Investig. Drugs 14, 1233-1239. doi: 10.1517/13543784.14.10.1233
75. Seeley, R. J., and Berridge, K. C. (2015). The hunger games. Cell 160, 805-806. doi: 10.1016/j.cell.2015.02.028
76. Shao, Z., Yin, J., Chapman, K., Grzemska, M., Clark, L., Wang, J., et al. (2016). High-resolution crystal structure of the human CB1 cannabinoid receptor. Nature 540, 602-606. doi: 10.1038/nature20613
77. Silvestri, C., and Di Marzo, V. (2013). The endocannabinoid system in energy homeostasis and the etiopathology of metabolic disorders. Cell Metab. 17, 475-490. doi: 10.1016/j.cmet.2013.03.001
78. Simiand, J., Keane, M., Keane, P. E., and Soubrie, P. (1998). SR 141716, a CB1 cannabinoid receptor antagonist, selectively reduces sweet food intake in marmoset. Behav. Pharmacol. 9, 179-181
79. Soria-Gomez, E., Bellocchio, L., Reguero, L., Lepousez, G., Martin, C., Bendahmane, M., et al. (2014a). The endocannabinoid system controls food intake via olfactory processes. Nat. Neurosci. 17, 407-415. doi: 10.1038/nn.3647
80. Soria-Gomez, E., Massa, F., Bellocchio, L., Rueda-Orozco, P. E., Ciofi, P., Cota, D., et al. (2014b). Cannabinoid type-1 receptors in the paraventricular nucleus of the hypothalamus inhibit stimulated food intake. Neuroscience 263C, 46-53. doi: 10.1016/j.neuroscience.2014.01.005
81. Tam, J., Cinar, R., Liu, J., Godlewski, G., Wesley, D., Jourdan, T., et al. (2012). Peripheral cannabinoid-1 receptor inverse agonism reduces obesity by reversing leptin resistance. Cell Metab. 16, 167-179. doi: 10.1016/j.cmet.2012.07.002
82. Thibault, K., Carrel, D., Bonnard, D., Gallatz, K., Simon, A., Biard, M., et al. (2013). Activation-dependent subcellular distribution patterns of CB1 cannabinoid receptors in the rat forebrain. Cereb. Cortex 23, 2581-2591. doi: 10.1093/cercor/bhs240
83. Urquhart, P., Nicolaou, A., and Woodward, D. F. (2015). Endocannabinoids and their oxygenation by cyclo-oxygenases, lipoxygenases and other oxygenases. Biochim. Biophys. Acta 1851, 366-376. doi: 10.1016/j.bbalip.2014.12.015
84. Vallee, M., Vitiello, S., Bellocchio, L., Hebert-Chatelain, E., Monlezun, S., Martin-Garcia, E., et al. (2014). Pregnenolone can protect the brain from cannabis intoxication. Science 343, 94-98. doi: 10.1126/science.1243985
85. Varela, L., and Horvath, T. L. (2012). Leptin and insulin pathways in POMC and AgRP neurons that modulate energy balance and glucose homeostasis. EMBO Rep. 13, 1079-1086. doi: 10.1038/embor.2012.174
86. Verty, A. N., Boon, W. M., Mallet, P. E., Mcgregor, I. S., and Oldfield, B. J. (2009). Involvement of hypothalamic peptides in the anorectic action of the CB receptor antagonist rimonabant (SR 141716). Eur. J. Neurosci. 29, 2207-2216. doi: 10.1111/j.1460-9568.2009.06750.x
87. Vogt, M. C., and Bruning, J. C. (2013). CNS insulin signaling in the control of energy homeostasis and glucose metabolism-from embryo to old age. Trends Endocrinol. Metab. 24, 76-84. doi: 10.1016/j.tem.2012.11.004
88. Volkow, N. D., Wang, G. J., and Baler, R. D. (2011). Reward, dopamine and the control of food intake: implications for obesity. Trends Cogn. Sci. 15, 37-46. doi: 10.1016/j.tics.2010.11.001
89. Walter, L., and Stella, N. (2004). Cannabinoids and neuroinflammation. Br. J. Pharmacol. 141, 775-785. doi: 10.1038/sj.bjp.0705667
90. Whiting, P. F., Wolff, R. F., Deshpande, S., Di Nisio, M., Duffy, S., Hernandez, A. V., et al. (2015). Cannabinoids for medical use: a systematic review and meta-analysis. JAMA 313, 2456-2473. doi: 10.1001/jama.2015.6358
91. Williams, C. M., and Kirkham, T. C. (1999). Anandamide induces overeating: mediation by central cannabinoid (CB1) receptors. Psychopharmacology 143, 315-317. doi: 10.1007/s002130050953
92. Zhang, X., and van den Pol, A. N. (2016). Hypothalamic arcuate nucleus tyrosine hydroxylase neurons play orexigenic role in energy homeostasis. Nat. Neurosci. 19, 1341-1347. doi: 10.1038/nn.4372