Selective blockade of the hydrolysis of the endocannabinoid 2-arachidonoylglycerol impairs learning and memory performance while producing antinociceptive activity in rodents

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Griebel, Guy ^a   Pichat, Philippe ^a   Beeske, Sandra ^a   Leroy, Thibaud ^a   Redon, Nicolas ^a   Jacquet, Agnes ^a   Françon, Dominique ^a   Bert, Lionel ^b   Even, Luc ^a   Lopez Grancha, Mati ^c   Tolstykh, Tatiana ^d   Sun, Fangxian ^d   Yu, Qunyan ^d   Brittain, Scott ^d   Arlt, Heike ^d   He, Timothy ^d   Zhang, Bailin ^d   Wiederschain, Dmitri ^d   Bertrand, Thomas ^e   Houtmann, Jacques ^e   Rak, Alexey ^e   Vallee, François ^e   Michot, Nadine ^e   Auge, Franck ^a   Menet, Veronique ^f   Bergis, Olivier E ^a   George, Pascal ^c   Avenet, Patrick ^a   Mikol, Vincent ^e   Didier, Michel ^b   Escoubet, Johanna ^b   more..

^a SANOFI   (France)

^b Exploratory Unit   (France)

^c Therapeutic Strategic Unit Aging Alzheimer/Parkinson/Stroke   (France)

^d Sanofi Aventis   (United States)

^e Lead Generation to Candidate Realization Sanofi Research and Development   (France)

^f Therapeutic Strategic Unit Aging   (France)

Author keywords

[No Author keywords available]

Indexed keywords

2-ARACHIDONYLGLYCEROL; ACETYLCHOLINE; ACYLGLYCEROL; ACYLGLYCEROL LIPASE; ANALGESIC AGENT; ARACHIDONIC ACID DERIVATIVE; CANNABINOID RECEPTOR ANTAGONIST; CARBAMIC ACID DERIVATIVE; ENDOCANNABINOID; ENZYME INHIBITOR; PIPERIDINE DERIVATIVE; PYRAZOLE DERIVATIVE; RIMONABANT; SAR127303; SULFONAMIDE;

ANIMAL; ANTAGONISTS AND INHIBITORS; BINDING SITE; BRAIN; C57BL MOUSE; CHEMISTRY; DISEASE MODEL; DRUG EFFECTS; ELECTROSTIMULATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HIPPOCAMPUS; HUMAN; HYDROLYSIS; IN VITRO STUDY; LEARNING; LONG TERM POTENTIATION; MASS SPECTROMETRY; METABOLISM; MOUSE; ORAL DRUG ADMINISTRATION; PAIN; PATHOLOGY; PROTEIN TERTIARY STRUCTURE; SCID MOUSE; SEIZURES; SHORT TERM MEMORY; X RAY CRYSTALLOGRAPHY;

ACETYLCHOLINE; ADMINISTRATION, ORAL; ANALGESICS; ANIMALS; ARACHIDONIC ACIDS; BINDING SITES; BRAIN; CANNABINOID RECEPTOR ANTAGONISTS; CARBAMATES; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CRYSTALLOGRAPHY, X-RAY; DISEASE MODELS, ANIMAL; ELECTRIC STIMULATION; ENDOCANNABINOIDS; ENZYME INHIBITORS; GLYCERIDES; HIPPOCAMPUS; HUMANS; HYDROLYSIS; IN VITRO TECHNIQUES; LEARNING; LONG-TERM POTENTIATION; MASS SPECTROMETRY; MEMORY, SHORT-TERM; MICE; MICE, INBRED C57BL; MICE, SCID; MONOACYLGLYCEROL LIPASES; PAIN; PIPERIDINES; PROTEIN STRUCTURE, TERTIARY; PYRAZOLES; SEIZURES; SULFONAMIDES;

EID: 84930274673     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep07642     Document Type: Article

References (74)

1. Pertwee, R. G. The pharmacology of cannabinoid receptors and their ligands: an overview. Int. J. Obes. (Lond) 30 Suppl 1, , S13-S18 (2006).
2. Di Marzo, V., Petrosino, S. Endocannabinoids and the regulation of their levels in health and disease. Curr. Opin. Lipidol. 18, 129-140 (2007).
3. Hohmann, A. G., Suplita, R. L. Endocannabinoid mechanisms of pain modulation. AAPS. J. 8, E693-E708 (2006).
4. Jhaveri, M. D., Richardson, D., Chapman, V. Endocannabinoid metabolism and uptake: novel targets for neuropathic and inflammatory pain. Br. J. Pharmacol. 152, 624-632 (2007).
5. Lambert, D. M. Allergic contact dermatitis and the endocannabinoid system: from mechanisms to skin care. ChemMedChem. 2, 1701-1702 (2007).
6. Bisogno, T., Di Marzo, V. Short-and long-term plasticity of the endocannabinoid system in neuropsychiatric and neurological disorders. Pharmacol. Res. 56, 428-442 (2007).
7. Matias, I., Di Marzo, V. Endocannabinoids and the control of energy balance. Trends Endocrinol. Metab 18, 27-37 (2007).
8. Pagotto, U.,Marsicano, G., Cota, D., Lutz, B., Pasquali, R. The emerging role of the endocannabinoid system in endocrine regulation and energy balance. Endocr. Rev. 27, 73-100 (2006).
9. Bifulco, M., Laezza, C., Gazzerro, P., Pentimalli, F. Endocannabinoids as emerging suppressors of angiogenesis and tumor invasion (review). Oncol. Rep. 17, 813-816 (2007).
10. Di Marzo, V., Bifulco, M., De, P. L. The endocannabinoid system and its therapeutic exploitation. Nat. Rev. Drug Discov. 3, 771-784 (2004).
11. Di Marzo, V. Targeting the endocannabinoid system: to enhance or reduce Nat. Rev. Drug Discov. 7, 438-455 (2008).
12. Piomelli, D. The endocannabinoid system: a drug discovery perspective. Curr. Opin. Investig. Drugs 6, 672-679 (2005).
13. Despres, J. P., Golay, A., Sjostrom, L. Effects of rimonabant on metabolic risk factors in overweight patients with dyslipidemia. N. Engl. J. Med. 353, 2121-2134 (2005).
14. Pi-Sunyer, F. X.,Aronne, L. J., Heshmati, H. M.,Devin, J. Rosenstock, J. Effect of rimonabant, a cannabinoid-1 receptor blocker, on weight and cardiometabolic risk factors in overweight or obese patients: RIO-North America: a randomized controlled trial. JAMA 295, 761-775 (2006).
15. Scheen, A J., Finer, N., Hollander, P., Jensen, M. D., Van Gaal, L. F. Efficacy and tolerability of rimonabant in overweight or obese patients with type 2 diabetes: a randomised controlled study. Lancet 368, 1660-1672 (2006).
16. Van Gaal, L. F., Rissanen, A. M., Scheen, A. J., Ziegler, O., Rossner, S. Effects of the cannabinoid-1 receptor blocker rimonabant on weight reduction and cardiovascular risk factors in overweight patients: 1-year experience from the RIO-Europe study. Lancet 365, 1389-1397 (2005).
17. Van Gaal, L. F. et al. Long-term effect of CB1 blockade with rimonabant on cardiometabolic risk factors: two year results from the RIO-Europe Study. Eur. Heart J. 29, 1761-1771 (2008).
18. Moreira, F. A., Grieb, M., Lutz, B. Central side-effects of therapies based on CB1 cannabinoid receptor agonists and antagonists: focus on anxiety and depression. Best. Pract. Res. Clin. Endocrinol. Metab 23, 133-144 (2009).
19. Fowler, C. J. Monoacylglycerol lipase-a target for drug development Br. J. Pharmacol. 166, 1568-1585 (2012).
20. Gaetani, S., Cuomo, V., Piomelli, D. Anandamide hydrolysis: a new target for anti-anxiety drugs Trends Mol. Med. 9, 474-478 (2003).
21. Gaetani, S. et al. The endocannabinoid system as a target for novel anxiolytic and antidepressant drugs. Int. Rev. Neurobiol. 85, 57-72 (2009).
22. Mulvihill, M. M., Nomura, D. K. Therapeutic potential of monoacylglycerol lipase inhibitors. Life Sci. 92, 492-497 (2013).
23. 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. 272, 27218-27223 (1997).
24. Cravatt, B. F. et al. Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides. Nature 384, 83-87 (1996).
25. Bisogno, T.,Maccarrone, M. Latest advances in the discovery of fatty acid amide hydrolase inhibitors. Expert. Opin. Drug Discov. 8, 509-522 (2013).
26. Hansen, H. S. Palmitoylethanolamide and other anandamide congeners. Proposed role in the diseased brain. Exp. Neurol. 224, 48-55 (2010).
27. De Petrocellis, L. DiMarzo, V. An introduction to the endocannabinoid system: from the early to the latest concepts. Best. Pract. Res. Clin. Endocrinol. Metab 23, 1-15 (2009).
28. King, A. R. et al. Discovery of potent and reversible monoacylglycerol lipase inhibitors. Chem. Biol. 16, 1045-1052 (2009).
29. Long, J. Z. et al. Selective blockade of 2-arachidonoylglycerol hydrolysis produces cannabinoid behavioral effects. Nat. Chem. Biol. 5, 37-44 (2009).
30. Chang, J.W. et al. Highly selective inhibitors of monoacylglycerol lipase bearing a reactive group that is bioisosteric with endocannabinoid substrates. Chem. Biol. 19, 579-588 (2012).
31. 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).
32. Schlosburg, J. E. et al. Chronic monoacylglycerol lipase blockade causes functional antagonism of the endocannabinoid system. Nat. Neurosci. 13, 1113-1119 (2010).
33. Busquets-Garcia, A. et al. Differential role of anandamide and 2-arachidonoylglycerol in memory and anxiety-like responses. Biol. Psychiatry 70, 479-486 (2011).
34. Sciolino, N. R., Zhou, W., Hohmann, A. G. Enhancement of endocannabinoid signaling with JZL184, an inhibitor of the 2-arachidonoylglycerol hydrolyzing enzyme monoacylglycerol lipase, produces anxiolytic effects under conditions of high environmental aversiveness in rats. Pharmacol. Res. 64, 226-234 (2011).
35. Kinsey, S. G. et al. Blockade of endocannabinoid-degrading enzymes attenuates neuropathic pain. J. Pharmacol. Exp. Ther. 330, 902-910 (2009).
36. Kinsey, S. G., Naidu, P. S., Cravatt, B. F., Dudley, D. T., Lichtman, A. H. Fatty acid amide hydrolase blockade attenuates the development of collagen-induced arthritis and related thermal hyperalgesia in mice. Pharmacol. Biochem. Behav. 99, 718-725 (2011).
37. Kinsey, S. G. et al. Repeated low-dose administration of the monoacylglycerol lipase inhibitor JZL184 retains cannabinoid receptor type 1-mediated antinociceptive and gastroprotective effects. J. Pharmacol. Exp. Ther. 345, 492-501 (2013).
38. Ignatowska-Jankowska, B. M. et al. In vivo characterization of the highly selective monoacylglycerol lipase inhibitor KML29: Antinociceptive activity without cannabimimetic side effects. Br. J. Pharmacol. 229, 591-601 (2013).
39. Bertrand, T. et al. Structural basis for human monoglyceride lipase inhibition. J. Mol. Biol. 396, 663-673 (2010).
40. Paxinos, G., Watson, C. The rat brain: In stereotaxic coordinates (New York Academic Press, San Diego, 1998).
41. Bert, L. et al. Rapid and precise method to locate microdialysis probe implantation in the rodent brain. J. Neurosci. Methods 140, 53-57 (2004).
42. Damsma, G., Bueren, D. L., Westerink, B. H. C., Horn, A. S. Determination of acetylcholine and choline in the femtomole range by means of HPLC, a postcolumn enzyme reactor, and electrochemical detection. Chromatographia 24, 827-831 (1987).
43. Ennaceur, A., Delacour, J. A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data. Behav. Brain Res. 31, 47-59 (1988).
44. Griebel, G. et al. SAR110894, a potent histamine H3-receptor antagonist, displays procognitive effects in rodents. Pharmacol. Biochem. Behav. 102, 203-214 (2012).
45. Racine, R. J. Modification of seizure activity by electrical stimulation. I. Afterdischarge threshold. Electroencephalogr. Clin. Neurophysiol. 32, 269-279 (1972).
46. Marrs, W. R. et al. The serine hydrolase ABHD6 controls the accumulation and efficacy of 2-AG at cannabinoid receptors. Nat. Neurosci. 13, 951-957 (2010).
47. Long, J. Z. et al. Dual blockade of FAAH and MAGL identifies behavioral processes regulated by endocannabinoid crosstalk in vivo. Proc. Natl. Acad. Sci. U. S. A 106, 20270-20275 (2009).
48. Ligresti, A., Petrosino, S., Di, M. V From endocannabinoid profiling to 'endocannabinoid therapeutics'. Curr. Opin. Chem. Biol. 13, 321-331 (2009).
49. Piscitelli, F., Di Marzo, V. "Redundancy" of endocannabinoid inactivation: new challenges and opportunities for pain control. ACS Chem. Neurosci. 3, 356-363 (2012).
50. Roques, B. P., Fournie-Zaluski, M. C., Wurm, M. Inhibiting the breakdown of endogenous opioids and cannabinoids to alleviate pain. Nat. Rev. Drug Discov. 11, 292-310 (2012).
51. Salaga, M., Sobczak, M., Fichna, J. Inhibition of fatty acid amide hydrolase (FAAH) as a novel therapeutic strategy in the treatment of pain and inflammatory diseases in the gastrointestinal tract. Eur. J. Pharm. Sci. 52, 173-179 (2014).
52. Savinainen, J. R., Saario, S. M., Laitinen, J. T. The serine hydrolases MAGL, ABHD6 and ABHD12 as guardians of 2-arachidonoylglycerol signalling through cannabinoid receptors. Acta Physiol (Oxf) 204, 267-276 (2012).
53. Alhouayek, M., Masquelier, J., Muccioli, G. G. Controlling 2-arachidonoylglycerol metabolism as an anti-inflammatory strategy. Drug Discov. Today 19, 295-304 (2013).
54. Morena, M., Campolongo, P. The endocannabinoid system: An emotional buffer in the modulation of memory function. Neurobiol. Learn.Mem. 112, 30-43 (2013).
55. Wise, L. E. et al. Dual fatty acid amide hydrolase and monoacylglycerol lipase blockade produces THC-like Morris water maze deficits in mice. ACS Chem. Neurosci. 3, 369-378 (2012).
56. Chanda, P. K. et al. Monoacylglycerol lipase activity is a critical modulator of the tone and integrity of the endocannabinoid system. Mol. Pharmacol. 78, 996-1003 (2010).
57. Herkenham,M. et al.Cannabinoid receptor localization in brain. Proc. Natl. Acad. Sci. U. S. A 87, 1932-1936 (1990).
58. Herkenham, M. et al. Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J. Neurosci. 11, 563-583 (1991).
59. Stella, N., Schweitzer, P., Piomelli, D. A second endogenous cannabinoid that modulates long-term potentiation. Nature 388, 773-778 (1997).
60. Sullivan, J. M. Cellular and molecular mechanisms underlying learning and memory impairments produced by cannabinoids. Learn. Mem. 7, 132-139 (2000).
61. Marsicano, G. et al. CB1 cannabinoid receptors and on-demand defense against excitotoxicity. Science 302, 84-88 (2003).
62. Wallace, M. J., Martin, B. R., DeLorenzo, R. J. Evidence for a physiological role of endocannabinoids in the modulation of seizure threshold and severity. Eur. J. Pharmacol. 452, 295-301 (2002).
63. Wallace, M. J., Blair, R. E., Falenski, K. W., Martin, B. R., DeLorenzo, R. J. The endogenous cannabinoid system regulates seizure frequency and duration in a model of temporal lobe epilepsy. J. Pharmacol. Exp. Ther. 307, 129-137 (2003).
64. Solbrig, M. V., Adrian, R., Baratta, J., Piomelli, D., Giuffrida, A. A role for endocannabinoids in viral-induced dyskinetic and convulsive phenomena. Exp. Neurol. 194, 355-362 (2005).
65. Naderi, N., Aziz, A. F., Shafaghi, B., Najarkolaei, A. H.,Motamedi, F. Evaluation of interactions between cannabinoid compounds and diazepam in electroshockinduced seizure model in mice. J. Neural Transm. 115, 1501-1511 (2008).
66. Naderi, N., Ahmad-Molaei, L., Aziz, A. F., Motamedi, F. Modulation of anticonvulsant effects of cannabinoid compounds by GABA-A receptor agonist in acute pentylenetetrazole model of seizure in rat. Neurochem. Res. 36, 1520-1525 (2011).
67. Wendt, H., Soerensen, J., Wotjak, C. T., Potschka, H. Targeting the endocannabinoid system in the amygdala kindling model of temporal lobe epilepsy in mice. Epilepsia 52, e62-e65 (2011).
68. Karanian, D. A. et al. Endocannabinoid enhancement protects against kainic acidinduced seizures and associated brain damage. J. Pharmacol. Exp. Ther. 322, 1059-1066 (2007).
69. Vilela, L. R. et al. Effects of cannabinoids and endocannabinoid hydrolysis inhibition on pentylenetetrazole-induced seizure and electroencephalographic activity in rats. Epilepsy Res. 104, 195-202 (2013).
70. Citraro, R. et al. Antiepileptic action of N-palmitoylethanolamine through CB1 and PPAR-alpha receptor activation in a genetic model of absence epilepsy. Neuropharmacology 69, 115-126 (2013).
71. Locher, W. Critical review of current animal models of seizures and epilepsy used in the discovery and development of new antiepileptic drugs. Seizure. 20, 359-368 (2011).
72. Matagne, A., Klitgaard, H. Validation of corneally kindled mice: a sensitive screening model for partial epilepsy in man. Epilepsy Res. 31, 59-71 (1998).
73. Sugiura, T., Yoshinaga, N., Kondo, S., Waku, K., Ishima, Y. Generation of 2-arachidonoylglycerol, an endogenous cannabinoid receptor ligand, in picrotoxinin-administered rat brain. Biochem. Biophys. Res. Commun. 271, 654-658 (2000).
74. Derkinderen, P. et al. Regulation of extracellular signal-regulated kinase by cannabinoids in hippocampus. J. Neurosci. 23, 2371-2382 (2003).