Endocannabinoid signaling in the gut mediates preference for dietary unsaturated fats

FASEB Journal

Volumn 27, Issue 6, 2013, Pages 2513-2520

  DiPatrizio, Nicholas V ^a   Joslin, Alexandra ^a   Jung, Kwang Mook ^a   Piomelli, Daniele ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

Author keywords

2 arachidonoyl sn glycerol; Anandamide; Lipids; Taste

Indexed keywords

AM 6546; CANNABINOID 1 RECEPTOR ANTAGONIST; CORN OIL; ENDOCANNABINOID; L 156602; LINOLEIC ACID; MINERAL OIL; OLEIC ACID; STEARIC ACID; UNCLASSIFIED DRUG; UNSATURATED FATTY ACID; URB 447;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMULSION; FEEDING; INTESTINE; JEJUNUM; LIPID DIET; MALE; NONHUMAN; PRIORITY JOURNAL; RAT;

2-ARACHIDONOYL-SN-GLYCEROL; ANANDAMIDE; LIPIDS; TASTE;

ADMINISTRATION, ORAL; ANIMALS; ARACHIDONIC ACIDS; BENZYL COMPOUNDS; DIETARY FATS, UNSATURATED; EMULSIONS; ENDOCANNABINOIDS; FOOD PREFERENCES; GLYCERIDES; JEJUNUM; MALE; PYRROLES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, CANNABINOID, CB1; SIGNAL TRANSDUCTION; TASTE;

ANIMALIA; RATTUS; ZEA MAYS;

EID: 84878755494     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-227587     Document Type: Article

References (49)

1. Laugerette, F., Passilly-Degrace, P., Patris, B., Niot, I., Febbraio, M., Montmayeur, J. P., and Besnard, P. (2005) CD36 involvement in orosensory detection of dietary lipids, spontaneous fat preference, and digestive secretions. J. Clin. Invest. 115, 3177-31844
2. Cartoni, C., Yasumatsu, K., Ohkuri, T., Shigemura, N., Yoshida, R., Godinot, N., le Coutre, J., Ninomiya, Y., and Damak, S. (2010) Taste preference for fatty acids is mediated by GPR40 and GPR120. J. Neurosci. 30, 8376-83822
3. Liu, P., Shah, B. P., Croasdell, S., and Gilbertson, T. A. (2011) Transient receptor potential channel type M5 is essential for fat taste. J. Neurosci. 31, 8634-86422
4. Liang, N. C., Hajnal, A., and Norgren, R. (2006) Sham feeding corn oil increases accumbens dopamine in the rat. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291, R1236-R12399
5. Kelley, A. E. (2004) Ventral striatal control of appetitive motivation: role in ingestive behavior and reward-related learning. Neurosci. Biobehav. Rev. 27, 765-7766
6. Smith, K. S., Berridge, K. C., and Aldridge, J. W. (2011) Disentangling pleasure from incentive salience and learning signals in brain reward circuitry. Proc. Natl. Acad. Sci. U. S. A. 108, E255-E2644
7. Greenberg, D., and Smith, G. P. (1996) The controls of fat intake. Psychosom. Med. 58, 559-5699
8. DiPatrizio, N. V., and Piomelli, D. (2012) The thrifty lipids: endocannabinoids and the neural control of energy conservation. Trends Neurosci. 35, 403-4111
9. Matias, I., and Di Marzo, V. (2007) Endocannabinoids and the control of energy balance. Trends Endocrin. Metab. 18, 27-377
10. Jarbe, T. U., and DiPatrizio, N. V. (2005) Delta9-THC induced hyperphagia and tolerance assessment: interactions between the CB1 receptor agonist delta9-THC and the CB1 receptor antagonist SR-141716 (rimonabant) in rats. Behav. Pharmacol. 16, 373-3800
11. Hamilton, R. B., and Norgren, R. (1984) Central projections of gustatory nerves in the rat. J. Compar. Neurol. 222, 560-5777
12. Grill, H. J. (2006) Distributed neural control of energy balance: contributions from hindbrain and hypothalamus. Obesity 14(Suppl. 5), 216S-221SS
13. Wu, Q., Clark, M. S., and Palmiter, R. D. (2012) Deciphering a neuronal circuit that mediates appetite. Nature 483, 594-5977
14. DiPatrizio, N. V., and Simansky, K. J. (2008) Activating parabrachial cannabinoid CB1 receptors selectively stimulates feeding of palatable foods in rats. J. Neurosci. 28, 9702-97099
15. DiPatrizio, N. V., and Simansky, K. J. (2008) Inhibiting parabrachial fatty acid amide hydrolase activity selectively increases the intake of palatable food via cannabinoid CB1 receptors. Am. J. Physiol. Regul. Integr. Comp. Physiol. 295, R1409-R14144
16. Mahler, S. V., Smith, K. S., and Berridge, K. C. (2007) Endocannabinoid hedonic hotspot for sensory pleasure: anandamide in nucleus accumbens shell enhances 'liking' of a sweet reward. Neuropsychopharmacology 32, 2267-22788
17. Yoshida, R., Ohkuri, T., Jyotaki, M., Yasuo, T., Horio, N., Yasumatsu, K., Sanematsu, K., Shigemura, N., Yamamoto, T., Margolskee, R. F., and Ninomiya, Y. (2010) Endocannabinoids selectively enhance sweet taste. Proc. Natl. Acad. Sci. U. S. A. 107, 935-9399
18. DiPatrizio, N. V., Astarita, G., Schwartz, G., Li, X., and Piomelli, D. (2011) Endocannabinoid signal in the gut controls dietary fat intake. Proc. Natl. Acad. Sci. U. S. A. 108, 12904-129088
19. Hamosh, M., and Scow, R. O. (1973) Lingual lipase and its role in the digestion of dietary lipid. J. Clin. Invest. 52, 88-955
20. Hamosh, M., and Burns, W. A. (1977) Lipolytic activity of human lingual glands (Ebner). Lab. Invest. 37, 603-6088
21. Hamosh, M. (1990) Lingual and gastric lipases. Nutrition 6, 421-4288
22. Smith, G. P. (2001) Sham feeding in rats with chronic, reversible gastric fistulas. Curr. Protoc. Neurosci. Chapter 8, Unit 8.6D, doi: 10.1002/0471142301.ns0806ds044
23. Yu, W. Z., Sclafani, A., Delamater, A. R., and Bodnar, R. J. (1999) Pharmacology of flavor preference conditioning in sham-feeding rats: effects of naltrexone. Pharmacol. Biochem. Behav. 64, 573-5844
24. Mindell, S., Smith, G. P., and Greenberg, D. (1990) Corn oil and mineral oil stimulate sham feeding in rats. Physiol. Behav. 48, 283-2877
25. Astarita, G., and Piomelli, D. (2009) Lipidomic analysis of endocannabinoid metabolism in biological samples. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 877, 2755-27677
26. Giuffrida, A., Rodriguez de Fonseca, F., and Piomelli, D. (2000) Quantification of bioactive acylethanolamides in rat plasma by electrospray mass spectrometry. Anal. Biochem. 280, 87-933
27. Piomelli, D. (2003) The molecular logic of endocannabinoid signalling. Nat. Rev. Neurosci. 4, 873-8844
28. Moreau, R. A. (2011) Corn oil. In: Vegetable Oils in Food Technology: Composition, Properties and Uses, 2nd Ed. (Gunstone, F., ed) pp. 273-289, Wiley-Blackwell, New Yorkk
29. Tam, J., Vemuri, V. K., Liu, J., Batkai, S., Mukhopadhyay, B., Godlewski, G., Osei-Hyiaman, D., Ohnuma, S., Ambudkar, S. V., Pickel, J., Makriyannis, A., and Kunos, G. (2010) Peripheral CB1 cannabinoid receptor blockade improves cardiometabolic risk in mouse models of obesity. J. Clin. Invest. 120, 2953-29666
30. LoVerme, J., Duranti, A., Tontini, A., Spadoni, G., Mor, M., Rivara, S., Stella, N., Xu, C., Tarzia, G., and Piomelli, D. (2009) 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, 639-6433
31. Yoneda, T., Saitou, K., Mizushige, T., Matsumura, S., Manabe, Y., Tsuzuki, S., Inoue, K., and Fushiki, T. (2007) The palatability of corn oil and linoleic acid to mice as measured by short-term two-bottle choice and licking tests. Physiol. Behav. 91, 304-3099
32. Saitou, K., Yoneda, T., Mizushige, T., Asano, H., Okamura, M., Matsumura, S., Eguchi, A., Manabe, Y., Tsuzuki, S., Inoue, K., and Fushiki, T. (2009) Contribution of gustation to the palatability of linoleic acid. Physiol. Behav. 96, 142-1488
33. Sclafani, A., Ackroff, K., and Abumrad, N. A. (2007) CD36 gene deletion reduces fat preference and intake but not post-oral fat conditioning in mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293, R1823-R18322
34. Martin, C., Chevrot, M., Poirier, H., Passilly-Degrace, P., Niot, I., and Besnard, P. (2011) CD36 as a lipid sensor. Physiol. Behav. 105, 36-422
35. Kawai, T., and Fushiki, T. (2003) Importance of lipolysis in oral cavity for orosensory detection of fat. Am. J. Physiol. Regul. Integr. Comp. Physiol. 285, R447-R4544
36. Smith, G. P., and Greenberg, D. (1991) Orosensory stimulation of feeding by oils in preweanling and adult rats. Brain Res. Bull. 27, 379-3822
37. Yoneda, T., Saitou, K., Asano, H., Mizushige, T., Matsumura, S., Eguchi, A., Manabe, Y., Tsuzuki, S., Inoue, K., and Fushiki, T. (2009) Assessing palatability of long-chain fatty acids from the licking behavior of BALB/c mice. Physiol. Behav. 96, 735-7411
38. Alvheim, A. R., Malde, M. K., Osei-Hyiaman, D., Hong Lin, Y., Pawlosky, R., Madsen, L., Kristiansen, K., Froyland, L., and Hibbeln, J. R. (2012) Dietary linoleic acid elevates endogenous 2-AG and anandamide and induces obesity. Obesity 20, 1984-19944
39. Dayton, S., Hashimoto, S., Dixon, W., and Pearce, M. L. (1966) Composition of lipids in human serum and adipose tissue during prolonged feeding of a diet high in unsaturated fat. J. Lipid Res. 7, 103-1111
40. Izzo, A. A., Piscitelli, F., Capasso, R., Aviello, G., Romano, B., Borrelli, F., Petrosino, S., and Di Marzo, V. (2009) Peripheral endocannabinoid dysregulation in obesity: relation to intestinal motility and energy processing induced by food deprivation and re-feeding. Br. J. Pharmacol. 158, 451-4611
41. Engeli, S., Bohnke, J., Feldpausch, M., Gorzelniak, K., Janke, J., Batkai, S., Pacher, P., Harvey-White, J., Luft, F. C., Sharma, A. M., and Jordan, J. (2005) Activation of the peripheral endocannabinoid system in human obesity. Diabetes 54, 2838-28433
42. Bluher, M., Engeli, S., Kloting, N., Berndt, J., Fasshauer, M., Batkai, S., Pacher, P., Schon, M. R., Jordan, J., and Stumvoll, M. (2006) Dysregulation of the peripheral and adipose tissue endocannabinoid system in human abdominal obesity. Diabetes 55, 3053-30600
43. Cote, M., Matias, I., Lemieux, I., Petrosino, S., Almeras, N., Despres, J. P., and Di Marzo, V. (2007) Circulating endocannabinoid levels, abdominal adiposity and related cardiometabolic risk factors in obese men. Int. J. Obes. 31, 692-6999
44. Matias, I., Gatta-Cherifi, B., Tabarin, A., Clark, S., Leste- Lasserre, T., Marsicano, G., Piazza, P. V., and Cota, D. (2012) Endocannabinoids measurement in human saliva as potential biomarker of obesity. PLoS ONE 7, e423999
45. Stratford, J. M., Curtis, K. S., and Contreras, R. J. (2006) Chorda tympani nerve transection alters linoleic acid taste discrimination by male and female rats. Physiol. Behav. 89, 311-3199
46. Pittman, D., Crawley, M. E., Corbin, C. H., and Smith, K. R. (2007) Chorda tympani nerve transection impairs the gustatory detection of free fatty acids in male and female rats. Brain Res. 1151, 74-833
47. Gaillard, D., Laugerette, F., Darcel, N., El-Yassimi, A., Passilly- Degrace, P., Hichami, A., Khan, N. A., Montmayeur, J. P., and Besnard, P. (2008) The gustatory pathway is involved in CD36- mediated orosensory perception of long-chain fatty acids in the mouse. FASEB J. 22, 1458-14688
48. Treesukosol, Y., Blonde, G. D., Jiang, E., Gonzalez, D., Smith, J. C., and Spector, A. C. (2010) Necessity of the glossopharyngeal nerve in the maintenance of normal intake and ingestive bout size of corn oil by rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 299, R1050-R10588
49. Sykaras, A. G., Demenis, C., Case, R. M., McLaughlin, J. T., and Smith, C. P. (2012) Duodenal enteroendocrine I-cells contain mRNA transcripts encoding key endocannabinoid and fatty acid receptors. PLoS ONE 7, e423733