Effect of dietary fat on endocannabinoids and related mediators: Consequences on energy homeostasis, inflammation and mood

Molecular Nutrition and Food Research

Volumn 54, Issue 1, 2010, Pages 82-92

  Banni, Sebastiano ^a,b   di Marzo, Vincenzo ^c  

^a UNIVERSITY OF CAGLIARI   (Italy)

^b SARDEGNA RICERCHE   (Italy)

^c CNR   (Italy)

Author keywords

2 arachidonoylglycerol; Cannabinoid; N arachidonoyl ethanolamine; Omega 3 fatty acids; PUFA

Indexed keywords

2 ARACHIDONOYLGLYCEROL; 2-ARACHIDONYLGLYCEROL; ACYLGLYCEROL; AMIDE; ANANDAMIDE; ARACHIDONIC ACID DERIVATIVE; ENDOCANNABINOID; OMEGA 3 FATTY ACID;

ANIMAL; ENERGY METABOLISM; FAT INTAKE; HOMEOSTASIS; HUMAN; INFLAMMATION; METABOLIC DISORDER; METABOLISM; MOOD DISORDER; PHYSIOLOGICAL STRESS; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; ARACHIDONIC ACIDS; DIETARY FATS; ENDOCANNABINOIDS; ENERGY METABOLISM; FATTY ACIDS, OMEGA-3; GLYCERIDES; HOMEOSTASIS; HUMANS; INFLAMMATION; METABOLIC DISEASES; MOOD DISORDERS; POLYUNSATURATED ALKAMIDES; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL;

MAMMALIA;

EID: 74349103519     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.200900516     Document Type: Review

References (72)

1. Di Marzo, V., Endocannabinoids' and other fatty acid derivatives with cannabimimetic properties: biochemistry and possible physiopathological relevance. Biochim. Biophys. Acta 1998, 1392, 153-175.
2. Matsuda, L.-A., Lolait, S.-J., Brownstein, M.-J., Young, A.-C., Bonner, T.-I., Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 1990, 346, 561-564.
3. Munro, S., Thomas, K.-L., Abu-Shaar, M., Molecular characterization of a peripheral receptor for cannabinoids. Nature 1993, 365, 61-65.
4. Devane, W.-A., Hanus, L., Breuer, A., Pertwee, R.-G. et al. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 1992, 258, 1946-1949.
5. Mechoulam, R., Ben-Shabat, S., Hanus, L., Ligumsky, M. et al. Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochem. Pharmacol. 1995, 50, 83-90.
6. Sugiura, T., Kondo, S., Sukagawa, A., Nakane, S. et al. 2-Arachidonoylglycerol: a possible endogenous cannabinoid receptor ligand in brain. Biochem. Biophys. Res. Commun. 1995, 215, 89-97.
7. Thabuis, C., Tissot-Favre, D., Bezelgues, J.-B., Martin, J.-C. et al. Biological functions and metabolism of oleoylethanolamide. Lipids 2008, 43,887-894.
8. LoVerme, J., La Rana, G., Russo, R., Calignano, A., Piomelli, D., The search for the palmitoylethanolamide receptor. Life Sci. 2005,77,1685-1698.
9. Costa, B., Comelli, F., Bettoni, I., Colleoni, M., Giagnoni, G., The endogenous fatty acid amide, palmitoylethanolamide, www.mnf-journal.com has anti-allodynic and anti-hyperalgesic effects in a murine model of neuropathic pain: involvement of CB(1), TRPV1 and PPARgamma receptors and neurotrophic factors. Pain 2008, 139, 541-550.
10. Oz, M., Receptor-independent effects of endocannabinoids on ion channels. Curr. Pharm. Des. 2006, 12: 227-239.
11. Starowicz, K., Nigam, S., Di Marzo, V., Biochemistry and pharmacology of endovanilloids. Pharmacol. Ther. 2007, 114,13-33.
12. Sugiura, T., Kodaka, T., Kondo, S., Tonegawa, T. et al. 2-Arachidonoylglycerol, a putative endogenous cannabinoid receptor ligand, induces rapid, transient elevation of intracellular free Ca21in neuroblastoma glioma hybrid NG108-15 cells. Biochem. Biophys. Res. Commun. 1996, 229,58-64.
13. Ben-Shabat, S., Fride, E., Sheskin, T., Tamiri, T. et al. An entourage effect: inactive endogenous fatty acid glycerol esters enhance 2-arachidonoyl-glycerol cannabinoid activ- ity. Eur. J. Pharmacol. 1998, 353, 23-31.
14. Panikashvili, D., Simeonidou, C., Ben-Shabat, S., Hanus, L. et al. An endogenous cannabinoid(2-AG) is neuroprotective after brain injury. Nature 2001, 413, 527-531.
15. Schmid, H.-H., Pathways and mechanisms of N-acylethanolamine biosynthesis: can anandamide be generated selectively? Chem. Phys. Lipids 2000, 108, 71-87.
16. Sugiura, T., Kondo, S., Sukagawa, A., Tonegawa, T. et al. Transacylase-mediated and phosphodiesterase-mediated synthesis of Narachidonoylethanolamine, an endogenous cannabinoidreceptor ligand, in rat brain microsomes. Comparison with synthesis from free arachidonic acid and ethanolamine. Eur. J. Biochem. 1996, 240, 53-62.
17. Okamoto, Y., Morishita, J., Tsuboi, K., Tonai, T., Ueda, N., Molecular characterization of a phospholipase D generating anandamide and its congeners. J. Biol. Chem. 2004, 279, 5298-5305.
18. Leung, D., Saghatelian, A., Simon, G.-M., Cravatt, B.-F., Inactivation of Nacyl phosphatidylethanolamine phospholipase D reveals multiple mechanisms for the biosynthesis of endocannabinoids. Biochemistry 2006, 45, 4720-4726.
19. Liu, J., Wang, L., Harvey-White, J., Huang, B.-X. et al. Multiple pathways involved in the biosynthesis of anandamide. Neuropharmacology 2008, 54, 1-7.
20. Simon, G.-M., Cravatt, B.-F., Endocannabinoid biosynthesis proceeding through glycerophospho-N-acyl ethanolamine and a role for alpha/beta-hydrolase 4 in this pathway. J. Biol. Chem. 2006, 281, 26465-26472.
21. Sun, Y.-X., Tsuboi, K., Okamoto, Y., Tonai, T. et al. Biosynthesis of anandamide and Npalmitoylethanolamine by sequential actions of phospholipase A2 and lysophospholipase D. Biochem. J. 2004, 380, 749-756.
22. Cadas, H., di Tomaso, E., Piomelli, D., Occurrence and biosynthesis of endogenous cannabinoid precursor, N-arachidonoyl phosphatidylethanolamine, in rat brain. J. Neurosci. 1997, 17, 1226-1242.
23. Di Marzo, V., De Petrocellis, L., Sugiura, T., Waku, K., Potential biosynthetic connections between the two cannabimimetic eicosanoids, anandamide and 2-arachido- noyl-glycerol, in mouse neuroblastoma cells. Biochem. Biophys. Res. Commun. 1996, 227, 281-288.
24. Sugiura, T., Kondo, S., Sukagawa, A., Tonegawa, T. et al. Enzymatic synthesis of anandamide, an endogenous cannabinoid receptor ligand, through N-acylphosphatidylethanolamine pathway in testis: involvement of Ca(21)-dependent transacylase and phosphodiesterase activities. Biochem. Biophys. Res. Commun. 1996, 218, 113-117.
25. Astarita, G., Ahmed, F., Piomelli, D., Identification of biosynthetic precursors for the endocannabinoid ananda- mide in the rat brain. J. Lipid Res. 2008, 49, 48-57.
26. Bisogno, T., Howell, F., Williams, G., Minassi, A. et al. Cloning of the first sn1-DAG lipases points to the spatial and temporal regulation of endocannabinoid signaling in the brain. J. Cell Biol. 2003, 163, 463-468.
27. Stella, N., Schweitzer, P., Piomelli, D., A second endogen- ous cannabinoid that modulates long-term potentiation. Nature 1997, 388, 773-778.
28. Bisogno, T., Melck, D., De Petrocellis, L., Di Marzo, V., Phosphatidic acid as the biosynthetic precursor of the endocannabinoid 2- arachidonoylglycerol in intact mouse neuroblastoma cells stimulated with ionomycin. J. Neurochem. 1999, 72, 2113-2119.
29. Bracey, M.-H., Hanson, M.-A., Masuda, K.-R., Stevens, R.-C., Cravatt, B.-F., Structural adaptations in a membrane enzyme that terminates endocannabinoid signaling. Science 2002, 298, 1793-1796.
30. McKinney, M.-K., Cravatt, B.-F., Structure and function of fatty acid amide hydrolase. Annu. Rev. Biochem. 2005, 74, 411-432.
31. Karlsson, M., Contreras, J.-A., Hellman, U., Tornqvist, H., Holm, C., cDNA cloning, tissue distribution, and identification of the catalytic triad of monoglyceride lipase. Evolutionary relationship to esterases, lysophospholipases, and haloperoxidases. J. Biol. Chem. 1997, 272, 27218-27223.
32. Dinh, T.-P., Carpenter, D., Leslie, F.-M., Freund, T.-F. et al. Brain monoglyceride lipase participating in endocannabi- noid inactivation. Proc. Natl. Acad. Sci. USA 2002, 99, 10819-10824.
33. Saario, S.-M., Salo, O.-M., Nevalainen, T., Poso, A. et al. Characterization of the sulfhydryl-sensitive site in the enzyme responsible for hydrolysis of 2-arachidonoyl- glycerol in rat cerebellar membranes. Chem. Biol. 2005, 12, 649-656.
34. Blankman, J.-L., Simon, G.-M., Cravatt, B.-F., A comprehensive profile of brain enzymes that hydrolyze the endo- cannabinoid 2- arachidonoylglycerol. Chem. Biol. 2007, 14, 1347-1356.
35. Di Marzo, V., Fontana, A., Cadas, H., Schinelli, S. et al. Formation and inactivation of endogenous cannabinoid anandamide in central neurons. Nature 1994, 372, 686-691.
36. Di Marzo, V., Bisogno, T., Sugiura, T., Melck, D., De Petrocellis, L., The novel endogenous cannabinoid 2-arachidonoylglycerol is inactivated by neuronal- and basophil-like cells: connections with anandamide. Biochem. J. 1998, 331, 15-19.
37. Berger, A., Crozier, G., Bisogno, T., Cavaliere, P. et al. Anandamide and diet: inclusion of dietary arachidonate and docosahexaenoate leads to increased brain levels of the corresponding N-acylethanolamines in piglets. Proc. Natl. Acad. Sci. USA 2001, 98, 6402-6406.
38. Berger, A., Roberts, M.-A., (Eds.), Dietary Effects of Arachidonate-Rich Fungal Oil and Fish Oil on Murine Hippo-campal Gene Expression, Marcel Dekker, NY 2005 pp. 69-100.
39. Berger, A., Mutch, D.-M., German, J.-B., Roberts, M.-A., Dietary effects of arachidonate-rich fungal oil and fish oil on murine hepatic and hippocampal gene expression. Lipids Health Dis. 2002, 1, 2.
40. Berger, A., Roberts, M.-A., Hoff, B., How dietary arachidonic- and docosahexaenoic-acid rich oils differentially affect the murine hepatic transcriptome. Lipids Health Dis 2006,5,10.
41. Wood, J.-T., Williams, J.-S., Pandarinathan, L., Vouros, P. et al. Plasma and brain endocannabinoid level correlation studies after increasing DHA dietary intake. FASEB J. 2007, 21,836.10.
42. Watanabe, S., Doshi, M., Hamazaki, T., n-3 Polyunsaturated fatty acid (PUFA) deficiency elevates and n-3 PUFA enrichment reduces brain 2-arachidonoylglycerol level in mice. Prostaglandins Leukot. Essent. Fatty Acids 2003, 69, 51-59.
43. Tsuyama, S., Oikawa, D., Tsuji, Y., Akimoto, Y., et al., Dietary conjugated linoleic acid modifies the brain endocannabinoid system in mice. Nutr. Neurosci. 2009, 12, 155-159.
44. Belury, M., Dietary conjugated linoleic acid in health: physiological effects and mechanisms of action. Annu. Rev. Nutr. 2002, 22, 505-531.
45. Artmann, A., Petersen, G., Hellgren, L.-I., Boberg, J. et al. Influence of dietary fatty acids on endocannabinoid and N-acylethanolamine levels in rat brain, liver and small intestine. Biochim. Biophys. Acta 2008, 1781, 200-212.
46. Fu, J., Oveisi, F., Gaetani, S., Lin, E., Piomelli, D., Oleoylethanolamide, an endogenous PPAR-alpha agonist, lowers body weight and hyperlipidemia in obese rats. Neuropharmacology 2005, 48, 1147-1153.
47. Matias, I., Carta, G., Murru, E., Petrosino, S. et al. Effect of polyunsaturated fatty acids on endocannabinoid and N-acyl-ethanolamine levels in mouse adipocytes. Biochim. Biophys. Acta 2008, 1781, 52-60.
48. Matias, I., Gonthier, M.-P., Petrosino, S., Docimo, L. et al. Role and regulation of acylethanolamides in energy balance: focus on adipocytes and beta-cells. Br. J. Pharmacol. 2007, 152, 676-690.
49. Matias, I., Petrosino, S., Racioppi, A., Capasso, R. et al. Dysregulation of peripheral endocannabinoid levels in hyperglycemia and obesity: effect of high fat diets. Mol. Cell. Endocrinol. 2008, 286, S66-S78.
50. Matias, I., Vergoni, A.-V., Petrosino, S., Ottani, A. et al. Regulation of hypothalamic endocannabinoid levels by neuropeptides and hormones involved in food intake and metabolism: insulin and melanocortins. Neuropharmacology 2008, 54, 206-212.
51. Hansen, S. L., Nielsen, A. H., Knudsen, K. E., Artmann, A. et al., Ketogenic diet is antiepileptogenic in pentylenete- trazole kindled mice and decrease levels of N-acylethano- lamines in hippocampus. Neurochem. Int. 2009, 54, 199-204.
52. Aviello, G., Matias, I., Capasso, R., Petrosino, S. et al. Inhibitory effect of the anorexic compound oleoylethanolamide on gastric emptying in control and overweight mice. J. Mol. Med. 2008, 86, 413-422.
53. Di Marzo, V., Capasso, R., Matias, I., Aviello, G. et al. The role of endocannabinoids in the regulation of gastric emptying: alterations in mice fed a high-fat diet. Br. J. Pharmacol. 2008, 153, 1272-1280.
54. Starowicz, K. M., Cristino, L., Matias, I., Capasso, R. et al., Endocannabinoid dysregulation in the pancreas and adipose tissue of mice fed with a high-fat diet. Obesity (Silver Spring) 2008, 16, 553-565.
55. Di Marzo, V., The endocannabinoid system in obesity and type 2 diabetes. Diabetologia 2008, 51, 1356-1367.
56. Bluher, M., Engeli, S., Klöting, N., Berndt, J., Dysregulation of the peripheral and adipose tissue endocannabinoid system in human abdominal obesity. Diabetes 2006, 55, 3053-3060.
57. Côé, M., Matias, I., Lemieux, I., Petrosino, S. et al. Circulating endocannabinoid levels, abdominal adiposity and related cardiometabolic risk factors in obese men. Int. J. Obes. (Lond). 2007, 31, 692-699.
58. Di Marzo, V., Côé, M., Matias, I., Lemieux, I. et al. Changes in plasma endocannabinoid levels in viscerally obese men following a 1 year lifestyle modification programme and waist circumference reduction: associations with changes in metabolic risk factors. Diabetologia 2009,52,213-217.
59. Di Marzo, V, Verrijken, A., Hakkarainen, A., Petrosino, S. et al. Role of insulin as a negative regulator of plasma endocannabinoid levels in obese and nonobese subjects. Eur. J. Endocrinol. 2009, 161, 715-722.
60. Di Marzo, V., CB(1) receptor antagonism: biological basis for metabolic effects. Drug Discov. Today 2008, 13, 1026-1041.
61. Matias, I., Léonhardt, M., Lesage, J., De Petrocellis, L. et al. Effect of maternal under-nutrition on pup body weight and hypothalamic endocannabinoid levels. Cell. Mol. Life Sci. 2003,60,382-389.
62. Batetta, B., Griinari, M., Carta, G., Murru, E. et al. Endocannabinoids may mediate the ability of (n-3) fatty acids to reduce ectopic fat and inflammatory mediators in obese Zucker rats. J. Nutr. 2009, 139, 1495-1501.
63. Izzo, A.-A., Piscitelli, F., Capasso, R., Aviello, G. et al. Peripheral endocannabinoid dysregulation in obesity: relation to intestinal motility and energy processing induced by food deprivation and re-feeding. Br. J. Pharmacol. 2009, 158,451-461.
64. Schafer, A., Pfrang, J., Neumuller, J., Fiedler, S. et al. The cannabinoid receptor-1 antagonist rimonabant inhibits platelet activation and reduces pro-inflammatory chemokines and leukocytes in Zucker rats. Br. J. Pharmacol. 2008, 154,1047-1054.
65. Koolman, A. H., Bloks, V. W., Oosterveer, M. H., Jonas, I. et al., Metabolic responses to long-term pharmacological inhibition of CB(1)-receptor activity in mice in relation to dietary fat composition. Int. J. Obes. (Lond.) 2009, DOI: 10.1038/ijo.2009.219.
66. Judge, M. K., Zhang, Y., Scarpace, P. J., Responses to the cannabinoid receptor-1 antagonist, AM251, are more robust with age and with high-fat feeding. J. Endocrinol. 2009, 203, 281-290.
67. Di Marzo, V., Griinari, M., Carta, G., Murru, E. et al. Dietary krill oil increases DHA and reduces 2-arachidonoylglycerol but not N-acylethanolamine levels in the brain of obese Zucker rats. Int. Dairy J., in press.
68. Lutz, B., Endocannabinoid signals in the control of emotion. Curr. Opin. Pharmacol. 2009, 9, 46-52.
69. Berger, A., Di Marzo, V., in: Després, J.-P., Di Marzo, V. (Eds.), Abdominal Obesity and the Endocannabinoid System, Informa Healthcare, New York, London 2009, pp. 191-201.
70. Hill, M.-N., Gorzalka, B.-B., Pharmacological enhancement of cannabinoid CB1 receptor activity elicits an antidepressant-like response in the rat forced swim test. Eur. Neuropsychopharmacol. 2005, 15, 593-599.
71. D'Asti, E., Long, H., Tremblay-Mercier, J., Grazier, M. et al., Maternal dietary fat determines metabolic profile and the magnitude of endocannabinoid inhibition of the stress response in neonatal rat offspring. Endocrinology, in press.
72. Di Marzo, V., Targeting the endocannabinoid system: to enhance or reduce? Nat. Rev. Drug Discov. 2008, 7, 438-455.