Opposite control of frontocortical 2-arachidonoylglycerol turnover rate by cannabinoid type-1 receptors located on glutamatergic neurons and on astrocytes

Journal of Neurochemistry

Volumn 133, Issue 1, 2015, Pages 26-37

  Belluomo, Ilaria ^a   Matias, Isabelle ^a   Pernègre, Camille ^a   Marsicano, Giovanni ^a   Chaouloff, Francis ^a  

^a INSTITUT FRANÇOIS MAGENDIE   (France)

Author keywords

2 arachidonoylglycerol; anandamide; CB1< inf> receptors; FAAH MAGL inhibition; fractional rate constant; turnover rate

Indexed keywords

2 ARACHIDONOYLGLYCEROL; ACYLGLYCEROL LIPASE; ANANDAMIDE; CANNABINOID 1 RECEPTOR; FATTY ACID AMIDASE; FATTY ACID AMIDASE INHIBITOR; JZL 195; PALMIDROL; PLACEBO; UNCLASSIFIED DRUG; 2-ARACHIDONYLGLYCEROL; ACYLGLYCEROL; AMIDASE; ARACHIDONIC ACID DERIVATIVE; CARBAMIC ACID DERIVATIVE; ENDOCANNABINOID; ENZYME INHIBITOR; FATTY-ACID AMIDE HYDROLASE; GLUTAMIC ACID; JZL195; PIPERAZINE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BIOACCUMULATION; BRAIN CELL; BRAIN REGION; CB1 GENE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CORPUS STRIATUM; DRUG TARGETING; ENZYME ACTIVITY; FRONTAL CORTEX; GENE; GENE DELETION; GENOTYPE; GLUTAMATERGIC NERVE CELL; HIPPOCAMPUS; KNOCKOUT MOUSE; LIPID METABOLISM; LIPOGENESIS; LIPOLYSIS; MALE; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; TISSUE DISTRIBUTION; TURNOVER TIME; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; KINETICS; METABOLISM; NERVE CELL; PHYSIOLOGY; PREFRONTAL CORTEX;

MUS;

AMIDOHYDROLASES; ANIMALS; ARACHIDONIC ACIDS; ASTROCYTES; CARBAMATES; ENDOCANNABINOIDS; ENZYME INHIBITORS; GLUTAMIC ACID; GLYCERIDES; HIPPOCAMPUS; KINETICS; MALE; MICE; MICE, KNOCKOUT; NEURONS; PIPERAZINES; PREFRONTAL CORTEX; RECEPTOR, CANNABINOID, CB1;

EID: 84924618466     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.13044     Document Type: Article

References (62)

1. Ahn K., McKinney M. K., and, Cravatt B. F., (2008) Enzymatic pathways that regulate endocannabinoid signaling in the nervous system. Chem. Rev. 108, 1687-1707.
2. Bacci A., Huguenard J. R., and, Prince D. A., (2004) Long-lasting self-inhibition of neocortical interneurons mediated by endocannabinoids. Nature 431, 312-316.
3. Bellocchio L., Lafenêtre P., Cannich A., Cota D., Puente N., Grandes P., Chaouloff F., Piazza P. V., and, Marsicano G., (2010) Bimodal control of stimulated food intake by the endocannabinoid system. Nat. Neurosci. 13, 281-283.
4. Béquet F., Uzabiaga F., Desbazeille M., Ludwiczak P., Maftouh M., Picard C., Scatton B., and, Le Fur G., (2007) CB1 receptor-mediated control of the release of endocannabinoids (as assessed by microdialysis coupled with LC/MS) in the rat hypothalamus. Eur. J. Neurosci. 26, 3458-3464.
5. Bisogno T., Howell F., Williams G., et al,. (2003) Cloning of the first sn1-DAG lipases points to the spatial and temporal regulation of endocannabinoid signaling in the brain. J. Cell Biol. 163, 463-468.
6. Bosier B., Bellocchio L., Metna-Laurent M., et al,. (2013) Astroglial CB1 cannabinoid receptors regulate leptin signaling in mouse brain astrocytes. Mol. Metab. 2, 393-404.
7. Buczynski M. W., and, Parsons L. H., (2010) Quantification of brain endocannabinoid levels: methods, interpretations and pitfalls. Br. J. Pharmacol. 160, 423-442.
8. Chaouloff F., Laude D., Mignot E., Kamoun P., and, Elghozi J. L., (1985) Tryptophan and serotonin turnover rate in the brain of genetically hyperammonemic mice. Neurochem. Int. 7, 143-153.
9. Chevaleyre V., Takahashi K. A., and, Castillo P. E., (2006) Endocannabinoid-mediated synaptic plasticity in the CNS. Annu. Rev. Neurosci. 29, 37-76.
10. Cravatt B. F., Giang D. K., Mayfield S. P., Boger D. L., Lerner R. A., and, Gilula N. B., (1996) Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides. Nature 384, 83-87.
11. Di Marzo V., Berrendero F., Bisogno T., Gonzalez S., Cavaliere P., Romero J., Cebeira M., Ramos J. A., and, Fernandez-Ruiz J. J., (2000a) Enhancement of anandamide formation in the limbic forebrain and reduction of endocannabinoid contents in the striatum of Δ9-tetrahydrocannabinol-tolerant rats. J. Neurochem. 74, 1627-1635.
12. Di Marzo V., Breivogel C. S., Tao Q., Bridgen D. T., Razdan R. K., Zimmer A. M., Zimmer A., and, Martin B. R., (2000b) Levels, metabolism, and pharmacological activity of anandamide in CB1 cannabinoid receptor knockout mice: evidence for non-CB1, non-CB2 receptor-mediated actions of anandamide in mouse brain. J. Neurochem. 75, 2434-2444.
13. Dinh T. P., Carpenter D., Leslie F. M., Freund T. F., Katona I., Sensi S. L., Kathuria S., and, Piomelli D., (2002) Brain monoglyceride lipase participating in endocannabinoid inactivation. Proc. Natl Acad. Sci. USA 99, 10819-10824.
14. Dubreucq S., Matias I., Cardinal P., Häring M., Lutz B., Marsicano M., and, Chaouloff F., (2012) Genetic dissection of the role of cannabinoid type-1 receptors in the emotional consequences of repeated social stress in mice. Neuropsychopharmacology 37, 1885-1900.
15. Dubreucq S., Durand A., Matias I., et al,. (2013) Ventral tegmental area cannabinoid type-1 receptors control voluntary exercise performance. Biol. Psychiatry 73, 895-903.
16. Gao Y., Vasilyev D. V., Goncalves M. B., et al,. (2010) Loss of retrograde endocannabinoid signaling and reduced adult neurogenesis in diacylglycerol lipase knock-out mice. J. Neurosci. 30, 2017-2024.
17. Gatta-Cherifi B., Matias I., Vallée M., Tabarin A., Marsicano G., Piazza P. V., and, Cota D., (2012) Simultaneous postprandial deregulation of the orexigenic endocannabinoid anandamide and the anorexigenic peptide YY in obesity. Int. J. Obes. 36, 880-885.
18. Gregg L. C., Jung K. M., Spradley J. M., et al,. (2012) Activation of type 5 metabotropic glutamate receptors and diacylglycerol lipase-α initiates 2-arachidonoylglycerol formation and endocannabinoid-mediated analgesia. J. Neurosci. 32, 9457-9468.
19. Hadjiconstantinou M., and, Neff N. H., (1989) Determination of monoamine turnover by blockade of their synthesis or metabolism, in Neuromethods: Drugs as Tools in Neurotransmitter Research (, Boulton A. A., Baker G. B., and, Juorio A. V., eds), Vol. 12, pp 249-260, Humana Press, New York.
20. Han J., Kesner P., Metna-Laurent M., et al,. (2012) Acute cannabinoids impair working memory through astroglial CB1 receptor modulation of hippocampal LTD. Cell 148, 1039-1050.
21. Hashimotodani Y., Ohno-Shosaku T., Maejima T., Kukami K., and, Kano M., (2008) Pharmacological evidence for the involvement of diacylglycerol lipase in depolarization-induced endocannabinoid release. Neuropharmacology 54, 58-67.
22. Herkenham M., Lynn A. B., Little M. D., Johnson M. R., Melvin L. S., de Costa B. R., and, Rice K. C., (1990) Cannabinoid receptor localization in brain. Proc. Natl Acad. Sci. USA 87, 1932-1936.
23. Hermanson D. J., Gamble-George J. C., Marnett L. J., and, Patel S., (2014) Substrate-selective COX-2 inhibition as a novel strategy for therapeutic endocannabinoid augmentation. Trends Pharmacol. Sci. 35, 358-367.
24. Hoover H. S., Blankman J. L., Niessen S., and, Cravatt B. F., (2008) Selectivity of inhibitors of endocannabinoid biosynthesis evaluated by activity-based protein profiling. Bioorg. Med. Chem. Lett. 18, 5838-5841.
25. Imai T., Chambon P., and, Metzger D., (2000) Inducible site-specific somatic mutagenesis in mouse hepatocytes. Genesis 26, 147-148.
26. Jonsson K. O., Vandevoorde S., Lambert D. M., Tiger G., and, Fowler C. J., (2001) Effects of homologues and analogues of palmitoylethanolamide upon the inactivation of the endocannabinoid anandamide. Br. J. Pharmacol. 133, 1263-1275.
27. Kamprath K., Plendl W., Marsicano G., Deussing J. M., Wurst W., Lutz B., and, Wotjak C. T., (2009) Endocannabinoids mediate acute fear adaptation via glutamatergic neurons independently of corticotropin-releasing hormone signaling. Genes Brain Behav. 8, 203-211.
28. Kano M., Ohno-Shosaku T., Hashimotodani Y., Uchigashima M., and, Watanabe M., (2009) Endocannabinoid-mediated control of synaptic transmission. Physiol. Rev. 89, 309-380.
29. Kathuria S., Gaetani S., Fegley D., et al,. (2003) Modulation of anxiety through blockade of anandamide hydrolysis. Nat. Med. 9, 76-81.
30. Kreitzer A. C., and, Regehr W. G., (2002) Retrograde signaling by endocannabinoids. Curr. Opin. Neurobiol. 12, 324-330.
31. Langer S. Z., (1997) 25 years since the discovery of presynaptic receptors: present knowledge and future perspectives. Trends Pharmacol. Sci. 18, 95-99.
32. Liedhegner E. S., Sasman A., and, Hillard C. J., (2014) Brain-region specific changes in N-acylethanolamine contents with time of day. J. Neurochem. 128, 491-506.
33. Long J. Z., Nomura D. K., Vann R. E., et al,. (2009) Dual blockade of FAAH and MAGL identifies behavioral processes regulated by endocannabinoid cross-talk in vivo. Proc. Natl Acad. Sci. USA 106, 20270-20275.
34. Maccarrone M., Attina M., Bari M., Cartoni A., Ledent C., and, Finazzi-Agro A., (2001) Anandamide degradation and N-acylethanolamines level in wild-type and CB1 cannabinoid receptor knockout mice of different ages. J. Neurochem. 78, 339-348.
35. Maccarrone M., Valverde O., Barbaccia M. L., Castané A., Maldonado R., Ledent C., Parmentier M., and, Finazzi-Agro A., (2002) Age-related changes of anandamide metabolism CB1 cannabinoid receptor knockout mice: correlation with behaviour. Eur. J. Neurosci. 15, 1178-1186.
36. Marrs W. R., Blankman J. L., Horne E. A., et al,. (2010) The serine hydrolase ABHD6 controls the accumulation and efficacy of 2-AG at cannabinoid receptors. Nat. Neurosci. 8, 951-959.
37. Marsicano G., and, Lutz B., (1999) Expression of the cannabinoid receptor CB1 in distinct neuronal subpopulations in the adult mouse forebrain. Eur. J. Neurosci. 11, 4213-4225.
38. Marsicano G., Goodenough S., Monory K., et al,. (2003) CB1 cannabinoid receptors and on-demand defense against excitotoxicity. Science 302, 84-88.
39. Melis M., Perra S., Muntoni A. L., Pillolla G., Lutz B., Marsicano G., Di Marzo V., Gessa G. L., and, Pistis M., (2004) Prefrontal cortex stimulation induces 2-arachidonoyl-glycerol-mediated suppression of excitation in dopamine neurons. J. Neurosci. 24, 10707-10715.
40. Metna-Laurent M., Soria-Gomez E., Verrier D., Conforzi M., Jego P., Lafenêtre P., and, Marsicano G., (2012) Bimodal control of fear-coping strategies by CB1 cannabinoid receptors. J. Neurosci. 32, 7109-7118.
41. Min R., Di Marzo V., and, Mansvelder H. D., (2010) DAG lipase involvement in depolarization-induced suppression of inhibition: does endocannabinoid biosynthesis always meet demand? Neuroscientist 16, 608-613.
42. Moise A. M., Eisenstein S. A., Astarita G., Piomelli D., and, Hohmann A. G., (2008) An endocannabinoid signaling system modulates anxiety-like behavior in male Syrian hamsters. Psychopharmacology 200, 333-346.
43. Monory K., Massa F., Egertová M., et al,. (2006) The endocannabinoid system controls key epileptogenic circuits in the hippocampus. Neuron 51, 455-466.
44. Monory K., Blaudzun H., Massa F., Kaiser N., Lemberger T., Schütz G., Wotjak C. T., Lutz B., and, Marsicano G., (2007) Genetic dissection of behavioural and autonomic effects of delta9-tetrahydrocannabinol in mice. PLoS Biol. 5, e269.
45. Morot-Gaudry Y., Hamon M., Bourgoin S., Ley J. P., and, Glowinski J., (1974) Estimation of the rate of 5-HT synthesis in the mouse brain by various methods. Naunyn Schmiedebergs Arch. Pharmacol. 282, 233-238.
46. Navarrete M., and, Araque A., (2008) Endocannabinoids mediate neuron-astrocyte communication. Neuron 57, 883-893.
47. Nomura D. K., Morrison B. E., Blankman J. L., et al,. (2011) Endocannabinoid hydrolysis generates brain prostaglandins that promote neuroinflammation. Science 334, 809-813.
48. Ohno-Shosaku T., Tanimura A., Hashimotodani Y., and, Kano M., (2012) Endocannabinoids and retrograde modulation of synaptic transmission. Neuroscientist 18, 119-132.
49. Patel S., Carrier E. J., Ho W. S., Rademacher D. J., Cunningham S., Reddy D. S., Falck J. R., Cravatt B. F., and, Hillard C. J., (2005) The postmortal accumulation of brain N-arachidonylethanolamine (anandamide) is dependent upon fatty acid amide hydrolase activity. J. Lipid Res. 46, 342-349.
50. Piomelli D., (2003) The molecular logic of endocannabinoid signalling. Nat. Rev. Neurosci. 4, 873-884.
51. Puighermanet al., Marsicano G., Busquets-Garcia A., Lutz B., Maldonado R., and, Ozaita A., (2009) Cannabinoid modulation of hippocampal long-term memory is mediated by mTOR signaling. Nat. Neurosci. 12, 1152-1158.
52. Rahman I. A., Tsuboi K., Uyama T., and, Ueda N., (2014) New players in the fatty acyl ethanolamide metabolism. Pharmacol. Res. 86, 1-10.
53. Safo P. K., and, Regehr W. G., (2005) Endocannabinoids control the induction of cerebellar LTD. Neuron 48, 647-659.
54. Seillier A., Dominguez Aguilar D., and, Giuffrida A., (2014) The dual FAAH/MAGL inhibitor JZL195 has enhanced effects on endocannabinoid transmission and motor behavior in rats as compared to those of the MAGL inhibitor JZL184. Pharmacol. Biochem. Behav. 124, 153-159.
55. Starke K., Göthert M., and, Kilbinger H., (1989) Modulation of neurotransmitter release by presynaptic autoreceptors. Physiol. Rev. 69, 864-989.
56. Steindel F., Lerner R., Häring M., Ruehle S., Marsicano G., Lutz B., and, Monory K., (2013) Neuron-type specific cannabinoid-mediated G protein signalling in mouse hippocampus. J. Neurochem. 124, 795-807.
57. Stella N., (2010) Cannabinoid and cannabinoid-like receptors in microglia, astrocytes, and astrocytomas. Glia 58, 1017-1030.
58. Stella N., Schweitzer P., and, Piomelli D., (1997) A second endogenous cannabinoid that modulates long-term potentiation. Nature 388, 773-777.
59. Tanimura A., Yamazaki M., Hashimotodani Y., et al,. (2010) The endocannabinoid 2-arachidonoylglycerol produced by diacylglycerol lipase alpha mediates retrograde suppression of synaptic transmission. Neuron 65, 320-327.
60. Tanimura A., Uchigashima M., Yamazaki M., Uesaka N., Mikuni T., Abe M., Hashimoto K., Watanabe M., Sakimura K., and, Kano M., (2012) Synapse-type independent degradation of the endocannabinoid 2-arachidonoylglycerol after retrograde synaptic suppression. Proc. Natl Acad. Sci. USA 109, 12195-12200.
61. Ueda N., Kurahashi Y., Yamamoto S., and, Tokunaga T., (1995) Partial purification and characterization of the porcine brain enzyme hydrolyzing and synthesizing anandamide. J. Biol. Chem. 270, 23823-23827.
62. Wiskerke J., Irimia C., Cravatt B. F., De Vries T. J., Schoffelmeer A. N. M., Pattij T., and, Parsons L. H., (2012) Characterization of the effects of reuptake and hydrolysis inhibition on interstitial endocannabinoid levels in the brain: an in vivo microdialysis study. ACS Chem. Neurosci. 3, 407-417.