Peripheral endocannabinoid signaling controls hyperphagia in western diet-induced obesity

Physiology and Behavior

Volumn 171, Issue , 2017, Pages 32-39

  Argueta, Donovan A ^a   DiPatrizio, Nicholas V ^a,b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Keck School of Medicine   (United States)

^c Biomedical Sciences   (United States)

Author keywords

2 AG; Anandamide; Endocannabinoid; Obesity; Peripheral; Western diet

Indexed keywords

2 ARACHIDONOYLGLYCEROL; ANANDAMIDE; CANNABINOID 1 RECEPTOR ANTAGONIST; ENDOCANNABINOID; ACYLGLYCEROL; AM6545; AMIDE; ARACHIDONIC ACID DERIVATIVE; CANNABINOID 1 RECEPTOR; GLYCERYL 2-ARACHIDONATE; LIPID; MORPHOLINE DERIVATIVE; PYRAZOLE DERIVATIVE; TRITIUM;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALORIC INTAKE; CONTROLLED STUDY; DRUG EFFECT; ENERGY CONSUMPTION; FAT INTAKE; FEEDING BEHAVIOR; GENE EXPRESSION; HYPERPHAGIA; INTESTINE BLOOD FLOW; LIQUID CHROMATOGRAPHY; MALE; MOUSE; NONHUMAN; OBESITY; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; SHAM FEEDING; SIGNAL TRANSDUCTION; SMALL INTESTINE MUCOSA; TANDEM MASS SPECTROMETRY; WEIGHT GAIN; WESTERN DIET; ADVERSE EFFECTS; ANALYSIS OF VARIANCE; ANIMAL; BLOOD; C57BL MOUSE; CHEMICALLY INDUCED; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY;

ANALYSIS OF VARIANCE; ANIMALS; ARACHIDONIC ACIDS; DIET, WESTERN; DISEASE MODELS, ANIMAL; ENDOCANNABINOIDS; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION; GLYCERIDES; HYPERPHAGIA; LIPIDS; MALE; MICE; MICE, INBRED C57BL; MORPHOLINES; OBESITY; POLYUNSATURATED ALKAMIDES; PYRAZOLES; RECEPTOR, CANNABINOID, CB1; SIGNAL TRANSDUCTION; TRITIUM;

EID: 85008506327     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2016.12.044     Document Type: Article

References (54)

1. [1] Poti, J.M., Duffey, K.J., Popkin, B.M., The association of fast food consumption with poor dietary outcomes and obesity among children: is it the fast food or the remainder of the diet?. Am. J. Clin. Nutr. 99 (2014), 162–171.
2. [2] Medina-RemOn, A., Kirwan, R., Lamuela-Raventos, R.M., Estruch, R., Dietary patterns and the risk of obesity, type 2 diabetes mellitus, cardiovascular diseases, asthma, and mental health problems. Crit. Rev. Food Sci. Nutr., 0, 2016.
3. [3] Laugerette, F., Passilly-Degrace, P., Patris, B., Niot, I., Febbraio, M., Montmayeur, J.P., et al. CD36 involvement in orosensory detection of dietary lipids, spontaneous fat preference, and digestive secretions. J. Clin. Invest. 115 (2005), 3177–3184.
4. [4] Cartoni, C., Yasumatsu, K., Ohkuri, T., Shigemura, N., Yoshida, R., Godinot, N., et al. Taste preference for fatty acids is mediated by GPR40 and GPR120. J. Neurosci. 30 (2010), 8376–8382.
5. [5] Liu, P., Shah, B.P., Croasdell, S., Gilbertson, T.A., Transient receptor potential channel type M5 is essential for fat taste. J. Neurosci. 31 (2011), 8634–8642.
6. [6] DiPatrizio, N.V., Is fat taste ready for primetime?. Physiol. Behav. 136 (2014), 145–154.
7. [7] Running, C.A., Craig, B.A., Mattes, R.D., Oleogustus: the unique taste of fat. Chem. Senses 40 (2015), 507–516.
8. [8] Mennella, J.A., Bobowski, N.K., Reed, D.R., The development of sweet taste: from biology to hedonics. Rev. Endocr. Metab. Disord. 17 (2016), 171–178.
9. [9] DiPatrizio, N.V., Piomelli, D., The thrifty lipids: endocannabinoids and the neural control of energy conservation. Trends Neurosci. 35 (2012), 403–411.
10. [10] Sclafani, A., Ackroff, K., Role of gut nutrient sensing in stimulating appetite and conditioning food preferences. Am. J. Phys. Regul. Integr. Comp. Phys. 302 (2012), R1119–R1133.
11. [11] Gatta-Cherifi, B., Cota, D., New insights on the role of the endocannabinoid system in the regulation of energy balance. Int. J. Obes. 40:2005 (2016), 210–219.
12. [12] Cota, D., Marsicano, G., Tschop, M., Grubler, Y., Flachskamm, C., Schubert, M., et al. The endogenous cannabinoid system affects energy balance via central orexigenic drive and peripheral lipogenesis. J. Clin. Invest. 112 (2003), 423–431.
13. [13] DiPatrizio, N.V., Simansky, K.J., Inhibiting parabrachial fatty acid amide hydrolase activity selectively increases the intake of palatable food via cannabinoid CB1 receptors. Am. J. Phys. Regul. Integr. Comp. Phys. 295 (2008), R1409–R1414.
14. [14] DiPatrizio, N.V., Simansky, K.J., Activating parabrachial cannabinoid CB1 receptors selectively stimulates feeding of palatable foods in rats. J. Neurosci. 28 (2008), 9702–9709.
15. [15] Di Marzo, V., Goparaju, S.K., Wang, L., Liu, J., Batkai, S., Jarai, Z., et al. Leptin-regulated endocannabinoids are involved in maintaining food intake. Nature 410 (2001), 822–825.
16. [16] Kirkham, T.C., Williams, C.M., Fezza, F., Di Marzo, V., Endocannabinoid levels in rat limbic forebrain and hypothalamus in relation to fasting, feeding and satiation: stimulation of eating by 2-arachidonoyl glycerol. Br. J. Pharmacol. 136 (2002), 550–557.
17. [17] Soria-Gomez, E., Bellocchio, L., Reguero, L., Lepousez, G., Martin, C., Bendahmane, M., et al. The endocannabinoid system controls food intake via olfactory processes. Nat. Neurosci., 2014.
18. [18] Soria-Gomez, E., Massa, F., Bellocchio, L., Rueda-Orozco, P.E., Ciofi, P., Cota, D., et al. Cannabinoid type-1 receptors in the paraventricular nucleus of the hypothalamus inhibit stimulated food intake. Neuroscience, 2014.
19. [19] Soria-Gomez, E., Matias, I., Rueda-Orozco, P.E., Cisneros, M., Petrosino, S., Navarro, L., et al. Pharmacological enhancement of the endocannabinoid system in the nucleus accumbens shell stimulates food intake and increases c-Fos expression in the hypothalamus. Br. J. Pharmacol. 151 (2007), 1109–1116.
20. [20] Anderson-Baker, W.C., McLaughlin, C.L., Baile, C.A., Oral and hypothalamic injections of barbiturates, benzodiazepines and cannabinoids and food intake in rats. Pharmacol. Biochem. Behav. 11 (1979), 487–491.
21. [21] Jamshidi, N., Taylor, D.A., Anandamide administration into the ventromedial hypothalamus stimulates appetite in rats. Br. J. Pharmacol. 134 (2001), 1151–1154.
22. [22] Verty, A.N., McGregor, I.S., Mallet, P.E., Paraventricular hypothalamic CB(1) cannabinoid receptors are involved in the feeding stimulatory effects of Delta(9)-tetrahydrocannabinol. Neuropharmacology 49 (2005), 1101–1109.
23. [23] Cristino, L., Busetto, G., Imperatore, R., Ferrandino, I., Palomba, L., Silvestri, C., et al. Obesity-driven synaptic remodeling affects endocannabinoid control of orexinergic neurons. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), E2229–E2238.
24. [24] Randall, P.A., Vemuri, V.K., Segovia, K.N., Torres, E.F., Hosmer, S., Nunes, E.J., et al. The novel cannabinoid CB1 antagonist AM6545 suppresses food intake and food-reinforced behavior. Pharmacol. Biochem. Behav. 97 (2010), 179–184.
25. [25] Cluny, N.L., Vemuri, V.K., Chambers, A.P., Limebeer, C.L., Bedard, H., Wood, J.T., et al. A novel peripherally restricted cannabinoid receptor antagonist, AM6545, reduces food intake and body weight, but does not cause malaise, in rodents. Br. J. Pharmacol. 161 (2011), 629–642.
26. [26] LoVerme, J., Duranti, A., Tontini, A., Spadoni, G., Mor, M., Rivara, S., et al. Synthesis and characterization of a peripherally restricted CB1 cannabinoid antagonist, URB447, that reduces feeding and body-weight gain in mice. Bioorg. Med. Chem. Lett. 19 (2009), 639–643.
27. [27] DiPatrizio, N.V., Astarita, G., Schwartz, G., Li, X., Piomelli, D., Endocannabinoid signal in the gut controls dietary fat intake. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 12904–12908.
28. [28] DiPatrizio, N.V., Igarashi, M., Narayanaswami, V., Murray, C., Gancayco, J., Russell, A., et al. Fasting stimulates 2-AG biosynthesis in the small intestine: role of cholinergic pathways. Am. J. Phys. Regul. Integr. Comp. Phys. 309 (2015), R805–R813.
29. [29] DiPatrizio, N.V., Joslin, A., Jung, K.M., Piomelli, D., Endocannabinoid signaling in the gut mediates preference for dietary unsaturated fats. FASEB J. 27 (2013), 2513–2520.
30. [30] Tam, J., Vemuri, V.K., Liu, J., Batkai, S., Mukhopadhyay, B., Godlewski, G., et al. Peripheral CB1 cannabinoid receptor blockade improves cardiometabolic risk in mouse models of obesity. J. Clin. Invest. 120 (2010), 2953–2966.
31. [31] Gomez, R., Navarro, M., Ferrer, B., Trigo, J.M., Bilbao, A., Del Arco, I., et al. A peripheral mechanism for CB1 cannabinoid receptor-dependent modulation of feeding. J. Neurosci. 22 (2002), 9612–9617.
32. [32] Tam, J., Cinar, R., Liu, J., Godlewski, G., Wesley, D., Jourdan, T., et al. Peripheral cannabinoid-1 receptor inverse agonism reduces obesity by reversing leptin resistance. Cell Metab. 16 (2012), 167–179.
33. [33] Bellocchio, L., Soria-Gomez, E., Quarta, C., Metna-Laurent, M., Cardinal, P., Binder, E., et al. Activation of the sympathetic nervous system mediates hypophagic and anxiety-like effects of CB1 receptor blockade. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 4786–4791.
34. [34] DiPatrizio, N.V., Endocannabinoids in the Gut. Cannabis Cannabinoid Res. 1 (2016), 67–77.
35. [35] Greenberg, D., Smith, G.P., The controls of fat intake. Psychosom. Med. 58 (1996), 559–569.
36. [36] Matias, I., Gatta-Cherifi, B., Tabarin, A., Clark, S., Leste-Lasserre, T., Marsicano, G., et al. Endocannabinoids measurement in human saliva as potential biomarker of obesity. PLoS One, 7, 2012, e42399.
37. [37] Matias, I., Petrosino, S., Racioppi, A., Capasso, R., Izzo, A.A., Di Marzo, V., Dysregulation of peripheral endocannabinoid levels in hyperglycemia and obesity: effect of high fat diets. Mol. Cell. Endocrinol. 286 (2008), S66–S78.
38. [38] Engeli, S., Bohnke, J., Feldpausch, M., Gorzelniak, K., Janke, J., Batkai, S., et al. Activation of the peripheral endocannabinoid system in human obesity. Diabetes 54 (2005), 2838–2843.
39. [39] Izzo, A.A., Piscitelli, F., Capasso, R., Aviello, G., Romano, B., Borrelli, F., et al. Peripheral endocannabinoid dysregulation in obesity: relation to intestinal motility and energy processing induced by food deprivation and re-feeding. Br. J. Pharmacol. 158 (2009), 451–461.
40. [40] Alvheim, A.R., Malde, M.K., Osei-Hyiaman, D., Lin, Y.H., Pawlosky, R.J., Madsen, L., et al. Dietary linoleic acid elevates endogenous 2-AG and anandamide and induces obesity. Obesity (Silver Spring) 20 (2012), 1984–1994.
41. [41] Alvheim, A.R., Torstensen, B.E., Lin, Y.H., Lillefosse, H.H., Lock, E.J., Madsen, L., et al. Dietary linoleic acid elevates the endocannabinoids 2-AG and anandamide and promotes weight gain in mice fed a low fat diet. Lipids 49 (2014), 59–69.
42. [42] Iannotti, F.A., Piscitelli, F., Martella, A., Mazzarella, E., Allara, M., Palmieri, V., et al. Analysis of the “endocannabinoidome” in peripheral tissues of obese Zucker rats. Prostaglandins Leukot. Essent. Fat. Acids 89 (2013), 127–135.
43. [43] Stella, N., Schweitzer, P., Piomelli, D., A second endogenous cannabinoid that modulates long-term potentiation. Nature 388 (1997), 773–778.
44. 2) and mortality: a pooled analysis of 20 prospective studies. PLoS Med., 11, 2014, e1001673.
45. [45] Liang, N.C., Hajnal, A., Norgren, R., Sham feeding corn oil increases accumbens dopamine in the rat. Am. J. Phys. Regul. Integr. Comp. Phys. 291 (2006), R1236–R1239.
46. [46] Smith, G.P., Accumbens dopamine mediates the rewarding effect of orosensory stimulation by sucrose. Appetite 43 (2004), 11–13.
47. [47] Izzo, A.A., Sharkey, K.A., Cannabinoids and the gut: new developments and emerging concepts. Pharmacol. Ther. 126 (2010), 21–38.
48. [48] Alvheim, A.R., Torstensen, B.E., Lin, Y.H., Lillefosse, H.H., Lock, E.J., Madsen, L., et al. Dietary linoleic acid elevates the endocannabinoids 2-AG and anandamide and promotes weight gain in mice fed a low fat diet. Lipids, 2013.
49. [49] Jung, K.M., Astarita, G., Zhu, C., Wallace, M., Mackie, K., Piomelli, D., A key role for diacylglycerol lipase-alpha in metabotropic glutamate receptor-dependent endocannabinoid mobilization. Mol. Pharmacol. 72 (2007), 612–621.
50. [50] Berthoud, H.R., Vagal and hormonal gut-brain communication: from satiation to satisfaction. Neurogastroenterol. Motil. 20:Suppl. 1 (2008), 64–72.
51. [51] Sykaras, A.G., Demenis, C., Case, R.M., McLaughlin, J.T., Smith, C.P., Duodenal enteroendocrine I-cells contain mRNA transcripts encoding key endocannabinoid and fatty acid receptors. PLoS ONE, 7, 2012, e42373.
52. [52] Monteleone, A.M., Di Marzo, V., Monteleone, P., Dalle Grave, R., Aveta, T., Ghoch, M.E., et al. Responses of peripheral endocannabinoids and endocannabinoid-related compounds to hedonic eating in obesity. Eur. J. Nutr. 55 (2016), 1799–1805.
53. [53] Monteleone, P., Piscitelli, F., Scognamiglio, P., Monteleone, A.M., Canestrelli, B., Di Marzo, V., et al. Hedonic eating is associated with increased peripheral levels of ghrelin and the endocannabinoid 2-arachidonoyl-glycerol in healthy humans: a pilot study. J. Clin. Endocrinol. Metab. 97 (2012), E917–E924.
54. [54] Sam, A.H., Salem, V., Ghatei, M.A., Rimonabant: from RIO to Ban. J. Obes., 2011, 2011, 432607.