Chronic monoacylglycerol lipase blockade causes functional antagonism of the endocannabinoid system

Nature Neuroscience

Volumn 13, Issue 9, 2010, Pages 1113-1119

  Schlosburg, Joel E ^a   Blankman, Jacqueline L ^b   Long, Jonathan Z ^b   Nomura, Daniel K ^b   Pan, Bin ^c   Kinsey, Steven G ^a   Nguyen, Peter T ^a   Ramesh, Divya ^a   Booker, Lamont ^a   Burston, James J ^a   Thomas, Elizabeth A ^b   Selley, Dana E ^a   Sim Selley, Laura J ^a   Liu, Qing Song ^c   Lichtman, Aron H ^a   Cravatt, Benjamin F ^b  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANALGESIC AGENT; CANNABINOID 1 RECEPTOR; CANNABINOID 1 RECEPTOR AGONIST; ENDOCANNABINOID; ENDOCANNABINOID 2 ARACHIDONOYLGLYCEROL; ENZYME INHIBITOR; JZL 184; UNCLASSIFIED DRUG; 1,3 BENZODIOXOLE DERIVATIVE; 4 [BIS(1,3 BENZODIOXOL 5 YL)HYDROXYMETHYL] 1 PIPERIDINECARBOXYLIC ACID 4 NITROPHENYL ESTER; ACYLGLYCEROL LIPASE; AMIDASE; CANNABINOID RECEPTOR AFFECTING AGENT; FATTY-ACID AMIDE HYDROLASE; PIPERIDINE DERIVATIVE;

ANALGESIC ACTIVITY; ARTICLE; DRUG DEPENDENCE; DRUG EFFECT; DRUG MECHANISM; GENE DISRUPTION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PAIN THRESHOLD; PRIORITY JOURNAL; ANIMAL; ANIMAL MODEL; ANTAGONISTS AND INHIBITORS; BRAIN; C57BL MOUSE; DRUG EFFECTS; FEMALE; GENETICS; KNOCKOUT MOUSE; MALE; METABOLISM; PAIN; PHYSIOLOGY; SYNAPSE; TRANSGENIC MOUSE;

AMIDOHYDROLASES; ANALGESICS; ANIMALS; BENZODIOXOLES; BRAIN; ENDOCANNABINOIDS; ENZYME INHIBITORS; FEMALE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MODELS, ANIMAL; MONOACYLGLYCEROL LIPASES; NEURONAL PLASTICITY; PAIN; PIPERIDINES; RECEPTOR, CANNABINOID, CB1; SYNAPSES; CANNABINOID RECEPTOR MODULATORS;

EID: 77956181836     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn.2616     Document Type: Article

References (50)

1. Pacher, P., Bátkai, S. & Kunos, G. The endocannabinoid system as an emerging target of pharmacotherapy. Pharm col. Rev. 58, 389-462 (2006).
2. Devane, W.A. et al. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 258, 1946-1949 (1992).
3. Mechoulam, R. et al. Identification of an endogenous 2-monoglyceride, present in canine gut, that binds cannabinoid receptors. Biochem. Pharmacol. 50, 83-90 (1995).
4. Sugiura, T. et al. 2-Arachidonylglycerol: a possible endogenous cannabinoid receptor ligand in brain. Biochem. Biophys. Res. Commun. 215, 89-97 (1995).
5. Mackie, K. Cannabinoid receptors as therapeutic targets. Annu. Rev. Pharmacol. Toxicol. 46, 101-122 (2006).
6. Marsicano, G. et al. CB1 cannabinoid receptors and on-demand defense against excitotoxicity. Science 302, 84-88 (2003).
7. Fowler, C.J. The cannabinoid system and its pharmacological manipulation-a review, with emphasis upon the uptake and hydrolysis of anandamide. Fundam. Clin. Pharmacol. 20, 549-562 (2006).
8. Ahn, K., McKinney, M.K. & Cravatt, B.F. Enzymatic pathways that regulate endocannabinoid signaling in the nervous system. Chem. Rev. 108, 1687-1707 (2008).
9. Deutsch, D.G. & Chin, S.A. Enzymatic synthesis and degradation of anandamide, a cannabinoid receptor agonist. Biochem. Pharmacol. 46, 791-796 (1993).
10. Cravatt, B.F. et al. Supersensitivity to anandamide and enhanced endogenous cannabinoid signaling in mice lacking fatty acid amide hydrolase. Proc. Natl. Acad. Sci. USA 98, 9371-9376 (2001).
11. Lichtman, A.H., Shelton, C.C., Advani, T. & Cravatt, B.F. Mice lacking fatty acid amide hydrolase exhibit a cannabinoid receptor-mediated phenotypic hypoalgesia. Pain 109, 319-327 (2004).
12. Kathuria, S. et al. Modulation of anxiety through blockade of anandamide hydrolysis. Nat. Med. 9, 76-81 (2003).
13. Lichtman, A.H. et al. Reversible inhibitors of fatty acid amide hydrolase that promote analgesia: evidence for an unprecedented combination of potency and selectivity. J. Pharmacol. Exp. Ther. 311, 441-448 (2004).
14. Jhaveri, M.D., Richardson, D., Kendall, D.A., Barrett, D.A. & Chapman, V. Analgesic effects of fatty acid amide hydrolase inhibition in a rat model of neuropathic pain. J. Neurosci. 26, 13318-13327 (2006).
15. Ahn, K. et al. Discovery and characterization of a highly selective FAAH inhibitor that reduces inflammatory pain. Chem. Biol. 16, 411-420 (2009).
16. Cravatt, B.F. et al. Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides. Nature 384, 83-87 (1996).
17. Long, J.Z. et al. Selective blockade of 2-arachidonoylglycerol hydrolysis produces cannabinoid behavioral effects. Nat. Chem. Biol. 5, 37-44 (2009).
18. Kinsey, S.G. et al. Blockade of endocannabinoid-degrading enzymes attenuates neuropathic pain. J. Pharmacol. Exp. Ther. 330, 902-910 (2009).
19. Long, J.Z. et al. Dual blockade of FAAH and MAGL identifies behavioral processes regulated by endocannabinoid crosstalk in vivo. Proc. Natl. Acad. Sci. USA 106, 20270-20275 (2009).
20. Pan, B. et al. Blockade of 2-arachidonoylglycerol hydrolysis by selective monoacylglycerol lipase inhibitor 4-nitrophenyl 4-(dibenzo[d][1,3]dioxol-5- yl(hydroxy)methyl)piperidine-1-carboxylate (JZL184) enhances retrograde endocannabinoid signaling. J. Pharmacol. Exp. Ther. 331, 591-597 (2009).
21. Straiker, A. et al. Monoacylglycerol lipase limits the duration of endocannabinoid-mediated depolarization-induced suppression of excitation in autaptic hippocampal neurons. Mol. Pharmacol. 76, 1220-1227 (2009).
22. Wilson, R.I. & Nicoll, R.A. Endocannabinoid signaling in the brain. Science 296, 678-682 (2002).
23. Tanimura, A. et al. The endocannabinoid 2-arachidonoylglycerol produced by diacylglycerol lipase alpha mediates retrograde suppression of synaptic transmission. Neuron 65, 320-327 (2010).
24. Gao, Y. et al. Loss of retrograde endocannabinoid signaling and reduced adult neurogenesis in diacylglycerol lipase knock-out mice. J. Neurosci. 30, 2017-2024 (2010).
25. Haller, J. et al. Interactions between environmental aversiveness and the anxiolytic effects of enhanced cannabinoid signaling by FAAH inhibition in rats. Psychopharmacology (Berl.) 204, 607-616 (2009).
26. Liu, Y., Patricelli, M.P. & Cravatt, B.F. Activity-based protein profiling: the serine hydrolases. Proc. Natl. Acad. Sci. USA 96, 14694-14699 (1999).
27. Blankman, J.L., Simon, G.M. & Cravatt, B.F. A comprehensive profile of brain enzymes that hydrolyze the endocannabinoid 2-arachidonoylglycerol. Chem. Biol. 14, 1347-1356 (2007).
28. Nomura, D.K. et al. Activation of the endocannabinoid system by organophosphorus nerve agents. Nat. Chem. Biol. 4, 373-378 (2008).
29. Long, J.Z., Nomura, D.K. & Cravatt, B.F. Characterization of monoacylglycerol lipase inhibition reveals differences in central and peripheral endocannabinoid metabolism. Chem. Biol. 16, 744-753 (2009).
30. Aceto, M.D., Scates, S.M., Lowe, J.A. & Martin, B.R. Cannabinoid precipitated withdrawal by the selective cannabinoid receptor antagonist, SR 141716A. Eur. J. Pharmacol. 282, R1-R2 (1995).
31. Falenski, K.W. et al. Faah-/- mice display differential tolerance, dependence and cannabinoid receptor adaptation following .9-tetrahydrocannabinol and anandamide administration. Neuropsychopharmacology 35, 1775-1787 (2010).
32. Lichtman, A.H., Hawkins, E.G., Griffin, G. & Cravatt, B.F. Pharmacological activity of fatty acid amides is regulated, but not mediated, by fatty acid amide hydrolase in vivo. J. Pharmacol. Exp. Ther. 302, 73-79 (2002).
33. Wilson, R.I., Kunos, G. & Nicoll, R.A. Presynaptic specificity of endocannabinoid signaling in the hippocampus. Neuron 31, 453-462 (2001).
34. Kreitzer, A.C. & Regehr, W.G. Retrograde signaling by endocannabinoids. Curr. Opin. Neurobiol. 12, 324-330 (2002).
35. Monory, K. et al. Genetic dissection of behavioural and autonomic effects of .9-tetrahydrocannabinol in mice. PLoS Biol. 5, e269 (2007).
36. Lichtman, A.H. & Martin, B.R. Cannabinoid tolerance and dependence. Handb. Exp. Pharmacol. 168, 691-717 (2005).
37. Sim, L.J., Hampson, R.E., Deadwyler, S.A. & Childers, S.R. Effects of chronic treatment with .9-tetrahydrocannabinol on cannabinoid-stimulated [35S]GTP.S autoradiography in rat brain. J. Neurosci. 16, 8057-8066 (1996).
38. Romero, J. et al. Effects of chronic exposure to .9-tetrahydrocannabinol on cannabinoid receptor binding and mRNA levels in several rat brain regions. Brain Res. Mol. Brain Res. 46, 100-108 (1997).
39. Sun, M., Lee, C.J. & Shin, H.S. Reduced nicotinic receptor function in sympathetic ganglia is responsible for the hypothermia in the acetylcholinesterase knockout mouse. J. Physiol. (Lond.) 578, 751-764 (2007).
40. Lanoir, J., Hilaire, G. & Seif, I. Reduced density of functional 5-HT1A receptors in the brain, medulla and spinal cord of monoamine oxidase-A knockout mouse neonates. J. Comp. Neurol. 495, 607-623 (2006).
41. Luk, T. et al. Identification of a potent and highly efficacious, yet slowly desensitizing CB1 cannabinoid receptor agonist. Br. J. Pharmacol. 142, 495-500 (2004).
42. Hillard, C.J. Biochemistry and pharmacology of the endocannabinoids arachidonylethanolamide and 2-arachidonylglycerol. Prostaglandins Other Lipid Mediat. 61, 3-18 (2000).
43. Sim-Selley, L.J. & Martin, B.R. Effect of chronic administration of R-(+)- [2,3-dihydro-5-methyl-3-[(morpholinyl)methyl]pyrrolo[1,2,3-de]-1,4-b enzoxazinyl]- (1-naphthalenyl)methanone mesylate (WIN55,212-2) or .9-tetrahydrocannabinol on cannabinoid receptor adaptation in mice. J. Pharmacol. Exp. Ther. 303, 36-44 (2002).
44. Caillé, S., Alvarez-Jaimes, L., Polis, I., Stouffer, D.G. & Parsons, L.H. Specific alterations of extracellular endocannabinoid levels in the nucleus accumbens by ethanol, heroin and cocaine self-administration. J. Neurosci. 27, 3695-3702 (2007).
45. Ohno-Shosaku, T., Maejima, T. & Kano, M. Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals. Neuron 29, 729-738 (2001).
46. Fan, F., Compton, D.R., Ward, S., Melvin, L. & Martin, B.R. Development of cross-tolerance between .9-tetrahydrocannabinol, CP 55,940 and WIN 55,212. J. Pharmacol. Exp. Ther. 271, 1383-1390 (1994).
47. Pertwee, R.G. & Wickens, A.P. Enhancement by chlordiazepoxide of catalepsy induced in rats by intravenous or intrapallidal injections of enantiomeric cannabinoids. Neuropharmacology 30, 237-244 (1991).
48. Lichtman, A.H., Cook, S.A. & Martin, B.R. Investigation of brain sites mediating cannabinoid-induced antinociception in rats: evidence supporting periaqueductal gray involvement. J. Pharmacol. Exp. Ther. 276, 585-593 (1996).
49. Thomas, E.A. et al. Clozapine increases apolipoprotein D expression in rodent brain: towards a mechanism for neuroleptic pharmacotherapy. J. Neurochem. 76, 789-796 (2001).
50. Schlosburg, J.E. et al. Inhibitors of endocannabinoid-metabolizing enzymes reduce precipitated withdrawal responses in THC-dependent mice. AAPS J. 11, 342-352 (2009).