The endocannabinoid arachidonylethanolamide attenuates aspects of lipopolysaccharide-induced changes in energy intake, energy expenditure and hypothalamic Fos expression

Journal of Neuroimmunology

Volumn 233, Issue 1-2, 2011, Pages 127-134

  Hollis, Jacob H ^a   Jonaidi, Hossein ^a,b   Lemus, Moyra ^a   Oldfield, Brian J ^a  

^a MONASH UNIVERSITY   (Australia)

^b SHAHID BAHONAR UNIVERSITY OF KERMAN   (Iran)

Author keywords

Appetite; Arcuate nucleus; Fever; Sickness

Indexed keywords

ANANDAMIDE; PROTEIN FOS;

ANIMAL CELL; ANIMAL EXPERIMENT; APPETITE; ARCUATE NUCLEUS; ARTICLE; CALORIC INTAKE; CALORIMETRY; CONTROLLED STUDY; CORE TEMPERATURE; ENERGY EXPENDITURE; HYPOTHALAMUS; HYPOTHALAMUS VENTROMEDIAL NUCLEUS; LIMBIC CORTEX; MALE; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ANIMALS; APPETITE REGULATION; ARACHIDONIC ACIDS; DISEASE MODELS, ANIMAL; ENDOCANNABINOIDS; ENERGY METABOLISM; FEVER; HYPOTHALAMUS; ILLNESS BEHAVIOR; MALE; POLYUNSATURATED ALKAMIDES; RATS; RATS, SPRAGUE-DAWLEY;

EID: 79953325301     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2010.12.009     Document Type: Article

References (67)

1. Abel E.L. Cannabis: effects on hunger and thirst. Behav Biol 1975, 15:255-281.
2. Adamantidis A., de Lecea L. Physiological arousal: a role for hypothalamic systems. Cell Mol Life Sci 2008, 65:1475-1488.
3. Agudo J., Martin M., Roca C., Molas M., Bura A.S., Zimmer A., Bosch F., Maldonado R. Deficiency of CB2 cannabinoid receptor in mice improves insulin sensitivity but increases food intake and obesity with age. Diabetologia 2010.
4. Akbas F., Gasteyger C., Sjodin A., Astrup A., Larsen T.M. A critical review of the cannabinoid receptor as a drug target for obesity management. Obes Rev 2009, 10:58-67.
5. Arnold J.C., Topple A.N., Mallet P.E., Hunt G.E., McGregor I.S. The distribution of cannabinoid-induced Fos expression in rat brain: differences between the Lewis and Wistar strain. Brain Res 2001, 921:240-255.
6. Baldo B.A., Gual-Bonilla L., Sijapati K., Daniel R.A., Landry C.F., Kelley A.E. Activation of a subpopulation of orexin/hypocretin-containing hypothalamic neurons by GABAA receptor-mediated inhibition of the nucleus accumbens shell, but not by exposure to a novel environment. Eur J Neurosci 2004, 19:376-386.
7. Becskei C., Riediger T., Hernadfalvy N., Arsenijevic D., Lutz T.A., Langhans W. Inhibitory effects of lipopolysaccharide on hypothalamic nuclei implicated in the control of food intake. Brain Behav Immun 2008, 22:56-64.
8. Benamar K., Yondorf M., Meissler J.J., Geller E.B., Tallarida R.J., Eisenstein T.K., Adler M.W. A novel role of cannabinoids: implication in the fever induced by bacterial lipopolysaccharide. J Pharmacol Exp Ther 2007, 320:1127-1133.
9. Berdyshev E.V. Cannabinoid receptors and the regulation of immune response. Chem Phys Lipids 2000, 108:169-190.
10. Cabral G.A., Griffin-Thomas L. Cannabinoids as therapeutic agents for ablating neuroinflammatory disease. Endocr Metab Immune Disord Drug Targets 2008, 8:159-172.
11. Cabral G.A., Marciano-Cabral F. Cannabinoid receptors in microglia of the central nervous system: immune functional relevance. J Leukoc Biol 2005, 78:1192-1197.
12. Cabral G.A., Raborn E.S., Griffin L., Dennis J., Marciano-Cabral F. CB2 receptors in the brain: role in central immune function. Br J Pharmacol 2008, 153:240-251.
13. Cao D.X., Wu G.H., Zhang B., Quan Y.J., Wei J., Jin H., Jiang Y., Yang Z.A. Resting energy expenditure and body composition in patients with newly detected cancer. Clin Nutr 2010, 29:72-77.
14. Carlezon W.A., Thomas M.J. Biological substrates of reward and aversion: a nucleus accumbens activity hypothesis. Neuropharmacology 2009, 56(Suppl 1):122-132.
15. Chang Y.H., Lee S.T., Lin W.W. Effects of cannabinoids on LPS-stimulated inflammatory mediator release from macrophages: involvement of eicosanoids. J Cell Biochem 2001, 81:715-723.
16. Correa F., Mestre L., Docagne F., Guaza C. Activation of cannabinoid CB2 receptor negatively regulates IL-12p40 production in murine macrophages: role of IL-10 and ERK1/2 kinase signaling. Br J Pharmacol 2005, 145:441-448.
17. Correa F., Docagne F., Clemente D., Mestre L., Becker C., Guaza C. Anandamide inhibits IL-12p40 production by acting on the promoter repressor element GA-12: possible involvement of the COX-2 metabolite prostamide E(2). Biochem J 2008, 409:761-770.
18. Correa F., Hernangomez M., Mestre L., Loria F., Spagnolo A., Docagne F., Di Marzo V., Guaza C. Anandamide enhances IL-10 production in activated microglia by targeting CB(2) receptors: roles of ERK1/2, JNK, and NF-kappaB. Glia 2010, 58:135-147.
19. Cota D., Marsicano G., Tschop M., Grubler Y., Flachskamm C., Schubert M., Auer D., Yassouridis A., Thone-Reineke C., Ortmann S., Tomassoni F., Cervino C., Nisoli E., Linthorst A.C., Pasquali R., Lutz B., Stalla G.K., Pagotto U. The endogenous cannabinoid system affects energy balance via central orexigenic drive and peripheral lipogenesis. J Clin Invest 2003, 112:423-431.
20. Cristino L., de Petrocellis L., Pryce G., Baker D., Guglielmotti V., Di Marzo V. Immunohistochemical localization of cannabinoid type 1 and vanilloid transient receptor potential vanilloid type 1 receptors in the mouse brain. Neuroscience 2006, 139:1405-1415.
21. De Filippis D., D'Amico A., Iuvone T. Cannabinomimetic control of mast cell mediator release: new perspective in chronic inflammation. J Neuroendocrinol 2008, 20(Suppl 1):20-25.
22. De Petrocellis L., Melck D., Bisogno T., Di Marzo V. Endocannabinoids and fatty acid amides in cancer, inflammation and related disorders. Chem Phys Lipids 2000, 108:191-209.
23. Devane W.A., Hanus L., Breuer A., Pertwee R.G., Stevenson L.A., Griffin G., Gibson D., Mandelbaum A., Etinger A., Mechoulam R. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 1992, 258:1946-1949.
24. Deveaux V., Cadoudal T., Ichigotani Y., Teixeira-Clerc F., Louvet A., Manin S., Nhieu J.T., Belot M.P., Zimmer A., Even P., Cani P.D., Knauf C., Burcelin R., Bertola A., Le Marchand-Brustel Y., Gual P., Mallat A., Lotersztajn S. Cannabinoid CB2 receptor potentiates obesity-associated inflammation, insulin resistance and hepatic steatosis. PLoS ONE 2009, 4:e5844.
25. Di Marzo V., Bisogno T., De Petrocellis L. Endocannabinoids: new targets for drug development. Curr Pharm Des 2000, 6:1361-1380.
26. Di Marzo V., Melck D., De Petrocellis L., Bisogno T. Cannabimimetic fatty acid derivatives in cancer and inflammation. Prostaglandins Other Lipid Mediat 2000, 61:43-61.
27. Engeli S. Dysregulation of the endocannabinoid system in obesity. J Neuroendocrinol 2008, 20(Suppl 1):110-115.
28. Facchinetti F., Del Giudice E., Furegato S., Passarotto M., Leon A. Cannabinoids ablate release of TNFalpha in rat microglial cells stimulated with lypopolysaccharide. Glia 2003, 41:161-168.
29. Felder C.C., Joyce K.E., Briley E.M., Mansouri J., Mackie K., Blond O., Lai Y., Ma A.L., Mitchell R.L. Comparison of the pharmacology and signal transduction of the human cannabinoid CB1 and CB2 receptors. Mol Pharmacol 1995, 48:443-450.
30. Fusco F.R., Martorana A., Giampa C., De March Z., Farini D., D'Angelo V., Sancesario G., Bernardi G. Immunolocalization of CB1 receptor in rat striatal neurons: a confocal microscopy study. Synapse 2004, 53:159-167.
31. Gautron L., Mingam R., Moranis A., Combe C., Laye S. Influence of feeding status on neuronal activity in the hypothalamus during lipopolysaccharide-induced anorexia in rats. Neuroscience 2005, 134:933-946.
32. Gomez R., Navarro M., Ferrer B., Trigo J.M., Bilbao A., Del Arco I., Cippitelli A., Nava F., Piomelli D., Rodriguez de Fonseca F. A peripheral mechanism for CB1 cannabinoid receptor-dependent modulation of feeding. J Neurosci 2002, 22:9612-9617.
33. Hollis J.H., Evans A.K., Bruce K.P., Lightman S.L., Lowry C.A. Lipopolysaccharide has indomethacin-sensitive actions on Fos expression in topographically organized subpopulations of serotonergic neurons. Brain Behav Immun 2006, 20:569-577.
34. Hollis J.H., Lemus M., Evetts M.J., Oldfield B.J. Central interleukin-10 attenuates lipopolysaccharide-induced changes in food intake, energy expenditure and hypothalamic Fos expression. Neuropharmacology 2010, 58:730-738.
35. Jamshidi N., Taylor D.A. Anandamide administration into the ventromedial hypothalamus stimulates appetite in rats. Br J Pharmacol 2001, 134:1151-1154.
36. Jelsing J., Larsen P.J., Vrang N. Identification of cannabinoid type 1 receptor expressing cocaine amphetamine-regulated transcript neurons in the rat hypothalamus and brainstem using in situ hybridization and immunohistochemistry. Neuroscience 2008, 154:641-652.
37. Kentner A.C., Takeuchi A., James J.S., Miki T., Seino S., Hayley S., Bielajew C. The effects of rewarding ventral tegmental area stimulation and environmental enrichment on lipopolysaccharide-induced sickness behavior and cytokine expression in female rats. Brain Res 2008, 1217:50-61.
38. 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 2002, 136:550-557.
39. Klein T.W., Newton C.A. Therapeutic potential of cannabinoid-based drugs. Adv Exp Med Biol 2007, 601:395-413.
40. Maresz K., Carrier E.J., Ponomarev E.D., Hillard C.J., Dittel B.N. Modulation of the cannabinoid CB2 receptor in microglial cells in response to inflammatory stimuli. J Neurochem 2005, 95:437-445.
41. Marsicano G., Lutz B. Expression of the cannabinoid receptor CB1 in distinct neuronal subpopulations in the adult mouse forebrain. Eur J Neurosci 1999, 11:4213-4225.
42. Mathias S., Schiffelholz T., Linthorst A.C., Pollmacher T., Lancel M. Diurnal variations in lipopolysaccharide-induced sleep, sickness behavior and changes in corticosterone levels in the rat. Neuroendocrinology 2000, 71:375-385.
43. 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.
44. Matyas F., Yanovsky Y., Mackie K., Kelsch W., Misgeld U., Freund T.F. Subcellular localization of type 1 cannabinoid receptors in the rat basal ganglia. Neuroscience 2006, 137:337-361.
45. McGregor I.S., Arnold J.C., Weber M.F., Topple A.N., Hunt G.E. A comparison of delta 9-THC and anandamide induced c-fos expression in the rat forebrain. Brain Res 1998, 802:19-26.
46. Meister B. Neurotransmitters in key neurons of the hypothalamus that regulate feeding behavior and body weight. Physiol Behav 2007, 92:263-271.
47. Morrow J.D., Opp M.R. Diurnal variation of lipopolysaccharide-induced alterations in sleep and body temperature of interleukin-6-deficient mice. Brain Behav Immun 2005, 19:40.
48. Munro S., Thomas K.L., Abu-Shaar M. Molecular characterization of a peripheral receptor for cannabinoids. Nature 1993, 365:61-65.
49. Ortega-Gutierrez S., Molina-Holgado E., Guaza C. Effect of anandamide uptake inhibition in the production of nitric oxide and in the release of cytokines in astrocyte cultures. Glia 2005, 52:163-168.
50. Osei-Hyiaman D., DePetrillo M., Pacher P., Liu J., Radaeva S., Batkai S., Harvey-White J., Mackie K., Offertaler L., Wang L., Kunos G. Endocannabinoid activation at hepatic CB1 receptors stimulates fatty acid synthesis and contributes to diet-induced obesity. J Clin Invest 2005, 115:1298-1305.
51. Park S.M., Gaykema R.P., Goehler L.E. How Does Immune Challenge Inhibit Ingestion of Palatable Food? 2008, Evidence that Systemic Lipopolysaccharide Treatment Modulates Key Nodal Points of Feeding Neurocircuitry, Brain Behav Immun.
52. Poirier B., Bidouard J.P., Cadrouvele C., Marniquet X., Staels B., O'Connor S.E., Janiak P., Herbert J.M. The anti-obesity effect of rimonabant is associated with an improved serum lipid profile. Diab Obes Metab 2005, 7:65-72.
53. Puffenbarger R.A., Boothe A.C., Cabral G.A. Cannabinoids inhibit LPS-inducible cytokine mRNA expression in rat microglial cells. Glia 2000, 29:58-69.
54. Ravinet Trillou C., Arnone M., Delgorge C., Gonalons N., Keane P., Maffrand J.P., Soubrie P. Anti-obesity effect of SR141716, a CB1 receptor antagonist, in diet-induced obese mice. Am J Physiol Regul Integr Comp Physiol 2003, 284:R345-R353.
55. Roche M., Kelly J.P., O'Driscoll M., Finn D.P. Augmentation of endogenous cannabinoid tone modulates lipopolysaccharide-induced alterations in circulating cytokine levels in rats. Immunology 2008, 125:263-271.
56. Sagar S.M., Price K.J., Kasting N.W., Sharp F.R. Anatomic patterns of Fos immunostaining in rat brain following systemic endotoxin administration. Brain Res Bull 1995, 36:381-392.
57. Soria-Gomez E., Matias I., Rueda-Orozco P.E., Cisneros M., Petrosino S., Navarro L., Di Marzo V., Prospero-Garcia O. 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 2007, 151:1109-1116.
58. Sugiura T., Kondo S., Sukagawa A., Nakane S., Shinoda A., Itoh K., Yamashita A., Waku K. 2-Arachidonoylglycerol: a possible endogenous cannabinoid receptor ligand in brain. Biochem Biophys Res Commun 1995, 215:89-97.
59. Sulcova E., Mechoulam R., Fride E. Biphasic effects of anandamide. Pharmacol Biochem Behav 1998, 59:347-352.
60. Sutcliffe J.G., de Lecea L. The hypocretins: setting the arousal threshold. Nat Rev Neurosci 2002, 3:339-349.
61. Takacs G., Papp S., Lukats B., Szalay C., Nagy B., Fotakos D., Karadi Z. Homeostatic alterations after IL-1beta microinjection into the nucleus accumbens of the rat. Appetite 2010, 54:354-362.
62. Van Der Stelt M., Di Marzo V. Endovanilloids. Putative endogenous ligands of transient receptor potential vanilloid 1 channels. Eur J Biochem 2004, 271:1827-1834.
63. Weidenfeld J., Feldman S., Mechoulam R. Effect of the brain constituent anandamide, a cannabinoid receptor agonist, on the hypothalamo-pituitary-adrenal axis in the rat. Neuroendocrinology 1994, 59:110-112.
64. Wenger T., Ledent C., Tramu G. The endogenous cannabinoid, anandamide, activates the hypothalamo-pituitary-adrenal axis in CB1 cannabinoid receptor knockout mice. Neuroendocrinology 2003, 78:294-300.
65. Williams C.M., Kirkham T.C. Anandamide induces overeating: mediation by central cannabinoid (CB1) receptors. Psychopharmacol (Berl) 1999, 143:315-317.
66. Wolf S.A., Tauber S., Ullrich O. CNS immune surveillance and neuroinflammation: endocannabinoids keep control. Curr Pharm Des 2008, 14:2266-2278.
67. Zheng H., Corkern M., Stoyanova I., Patterson L.M., Tian R., Berthoud H.R. Peptides that regulate food intake: appetite-inducing accumbens manipulation activates hypothalamic orexin neurons and inhibits POMC neurons. Am J Physiol Regul Integr Comp Physiol 2003, 284:R1436-R1444.