Characterization of the effects of reuptake and hydrolysis inhibition on interstitial endocannabinoid levels in the brain: An in vivo microdialysis study

ACS Chemical Neuroscience

Volumn 3, Issue 5, 2012, Pages 407-417

  Wiskerke, Joost ^a,b   Irimia, Cristina ^a   Cravatt, Benjamin F ^a   De Vries, Taco J ^b   Schoffelmeer, Anton N M ^b   Pattij, Tommy ^b   Parsons, Loren H ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Endocannabinoid transporter; endogenous cannabinoid system; FAAH; in vivo microdialysis; MAGL; nucleus accumbens

Indexed keywords

ACYLGLYCEROL LIPASE; ANANDAMIDE; CARRIER PROTEIN; CYCLOHEXYLCARBAMIC ACID 3' CARBAMOYLBIPHENYL 3 YL ESTER; ENDOCANNABINOID; ENDOCANNABINOID TRANSPORTER; FATTY ACID AMIDASE; JZL 184; JZL 195; N (3 FURYLMETHYL)ARACHIDONAMIDE; N (4 HYDROXYPHENYL)ARACHIDONAMIDE; PF 3845; UNCLASSIFIED DRUG; URB 602;

ANIMAL EXPERIMENT; BRAIN LEVEL; COMPARATIVE STUDY; CONFERENCE PAPER; CONTROLLED STUDY; DEPOLARIZATION; DIALYSATE; DRUG EFFICACY; HYDROLYSIS KINETICS; IN VIVO STUDY; MALE; MICRODIALYSIS; MOUSE; NONHUMAN; NUCLEUS ACCUMBENS; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; RAT; SPECIES COMPARISON; SPECIES DIFFERENCE; TRANSPORT KINETICS;

ENDOCANNABINOID TRANSPORTER; ENDOGENOUS CANNABINOID SYSTEM; FAAH; IN VIVO MICRODIALYSIS; MAGL; NUCLEUS ACCUMBENS;

ANIMALS; BENZODIOXOLES; BIOLOGICAL TRANSPORT; BRAIN; ENDOCANNABINOIDS; EXTRACELLULAR FLUID; HYDROLYSIS; MALE; MICE; MICE, INBRED C57BL; MICRODIALYSIS; PIPERIDINES; RATS; RATS, WISTAR;

MUS; RATTUS;

EID: 84862092052     PISSN: None     EISSN: 19487193     Source Type: Journal    
DOI: 10.1021/cn300036b     Document Type: Conference Paper

References (64)

1. Hohmann, A. G., Suplita, R. L., Bolton, N. M., Neely, M. H., Fegley, D., Mangieri, R., Krey, J. F., Walker, J. M., Holmes, P. V., Crystal, J. D., Duranti, A., Tontini, A., Mor, M., Tarzia, G., and Piomelli, D. (2005) An endocannabinoid mechanism for stress-induced analgesia Nature 435, 1108-1112 (Pubitemid 40910518)
2. Holt, S., Comelli, F., Costa, B., and Fowler, C. J. (2005) Inhibitors of fatty acid amide hydrolase reduce carrageenan-induced hind paw inflammation in pentobarbital-treated mice: comparison with indomethacin and possible involvement of cannabinoid receptors Br. J. Pharmacol. 146, 467-476 (Pubitemid 41486689)
3. Marsicano, G., Wotjak, C. T., Azad, S. C., Bisogno, T., Rammes, G., Cascio, M. G., Hermann, H., Tang, J., Hofmann, C., Zieglgansberger, W., Di Marzo, V., and Lutz, B. (2002) The endogenous cannabinoid system controls extinction of aversive memories Nature 418, 530-534 (Pubitemid 34851398)
4. Maccarrone, M., Gasperi, V., Catani, M. V., Diep, T. A., Dainese, E., Hansen, H. S., and Avigliano, L. (2010) The endocannabinoid system and its relevance for nutrition Annu. Rev. Nutr. 30, 423-440
5. Pattij, T., Wiskerke, J., and Schoffelmeer, A. N. (2008) Cannabinoid modulation of executive functions Eur. J. Pharmacol. 585, 458-463
6. Hill, M. N. and Gorzalka, B. B. (2009) The endocannabinoid system and the treatment of mood and anxiety disorders CNS Neurol. Disord.: Drug Targets 8, 451-458
7. Solinas, M., Goldberg, S. R., and Piomelli, D. (2008) The endocannabinoid system in brain reward processes Br. J. Pharmacol. 154, 369-383 (Pubitemid 351670594)
8. Kano, M., Ohno-Shosaku, T., Hashimotodani, Y., Uchigashima, M., and Watanabe, M. (2009) Endocannabinoid-mediated control of synaptic transmission Physiol. Rev. 89, 309-380
9. Iversen, L. (2003) Cannabis and the brain Brain 126, 1252-1270 (Pubitemid 36644373)
10. Di Marzo, V. (2009) The endocannabinoid system: its general strategy of action, tools for its pharmacological manipulation and potential therapeutic exploitation Pharmacol. Res. 60, 77-84
11. Astarita, G., Geaga, J., Ahmed, F., and Piomelli, D. (2009) Targeted lipidomics as a tool to investigate endocannabinoid function Int. Rev. Neurobiol. 85, 35-55
12. Di Marzo, V. (2010) Anandamide serves two masters in the brain Nat. Neurosci. 13, 1446-1448
13. Natarajan, V., Reddy, P. V., Schmid, P. C., and Schmid, H. H. (1982) N-Acylation of ethanolamine phospholipids in canine myocardium Biochim. Biophys. Acta 712, 342-355
14. Bisogno, T., Howell, F., Williams, G., Minassi, A., Cascio, M. G., Ligresti, A., Matias, I., Schiano-Moriello, A., Paul, P., Williams, E. J., Gangadharan, U., Hobbs, C., Di Marzo, V., and Doherty, P. (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 (Pubitemid 37429860)
15. Bisogno, T., Cascio, M. G., Saha, B., Mahadevan, A., Urbani, P., Minassi, A., Appendino, G., Saturnino, C., Martin, B., Razdan, R., and Di Marzo, V. (2006) Development of the first potent and specific inhibitors of endocannabinoid biosynthesis Biochim. Biophys. Acta 1761, 205-212
16. 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
17. McFarland, M. J. and Barker, E. L. (2004) Anandamide transport Pharmacol. Ther. 104, 117-135 (Pubitemid 39424256)
18. Glaser, S. T., Kaczocha, M., and Deutsch, D. G. (2005) Anandamide transport: a critical review Life Sci. 77, 1584-1604 (Pubitemid 41073654)
19. Fu, J., Bottegoni, G., Sasso, O., Bertorelli, R., Rocchia, W., Masetti, M., Guijarro, A., Lodola, A., Armirotti, A., Garau, G., Bandiera, T., Reggiani, A., Mor, M., Cavalli, A., and Piomelli, D. (2011) A catalytically silent FAAH-1 variant drives anandamide transport in neurons. Nat Neurosci., DOI: 10.1007/s13311-011-0100-y, PMID: 22270809.
20. 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 (Pubitemid 351796405)
21. 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 (Pubitemid 26374593)
22. 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. U.S.A. 99, 10819-10824
23. Blankman, J. L., Simon, G. M., and Cravatt, B. F. (2007) A Comprehensive Profile of Brain Enzymes that Hydrolyze the Endocannabinoid 2- Arachidonoylglycerol Chem. Biol. 14, 1347-1356 (Pubitemid 350257008)
24. Petrosino, S., Ligresti, A., and Di Marzo, V. (2009) Endocannabinoid chemical biology: a tool for the development of novel therapies Curr. Opin. Chem. Biol. 13, 309-320
25. Fowler, C. J. (2008) 'The tools of the trade'-An overview of the pharmacology of the endocannabinoid system Curr. Pharm. Des. 14, 2254-2265
26. Long, J. Z., Nomura, D. K., Vann, R. E., Walentiny, D. M., Booker, L., Jin, X., Burston, J. J., Sim-Selley, L. J., Lichtman, A. H., Wiley, J. L., and Cravatt, B. F. (2009) 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
27. Bortolato, M., Mangieri, R. A., Fu, J., Kim, J. H., Arguello, O., Duranti, A., Tontini, A., Mor, M., Tarzia, G., and Piomelli, D. (2007) Antidepressant-like activity of the fatty acid amide hydrolase inhibitor URB597 in a rat model of chronic mild stress Biol. Psychiatry 62, 1103-1110 (Pubitemid 350029716)
28. Ahn, K., Johnson, D. S., Mileni, M., Beidler, D., Long, J. Z., McKinney, M. K., Weerapana, E., Sadagopan, N., Liimatta, M., Smith, S. E., Lazerwith, S., Stiff, C., Kamtekar, S., Bhattacharya, K., Zhang, Y., Swaney, S., Van Becelaere, K., Stevens, R. C., and Cravatt, B. F. (2009) Discovery and Characterization of a Highly Selective FAAH Inhibitor that Reduces Inflammatory Pain Chem. Biol. 16, 411-420
29. Long, J. Z., Li, W., Booker, L., Burston, J. J., Kinsey, S. G., Schlosburg, J. E., Pavon, F. J., Serrano, A. M., Selley, D. E., Parsons, L. H., Lichtman, A. H., and Cravatt, B. F. (2009) Selective blockade of 2-arachidonoylglycerol hydrolysis produces cannabinoid behavioral effects Nat. Chem. Biol. 5, 37-44
30. Bortolato, M., Campolongo, P., Mangieri, R. A., Scattoni, M. L., Frau, R., Trezza, V., La Rana, G., Russo, R., Calignano, A., Gessa, G. L., Cuomo, V., and Piomelli, D. (2006) Anxiolytic-like properties of the anandamide transport inhibitor AM404 Neuropsychopharmacology 31, 2652-2659 (Pubitemid 44764162)
31. de Lago, E., Fernandez-Ruiz, J., Ortega-Gutierrez, S., Viso, A., Lopez-Rodriguez, M. L., and Ramos, J. A. (2002) UCM707, a potent and selective inhibitor of endocannabinoid uptake, potentiates hypokinetic and antinociceptive effects of anandamide Eur. J. Pharmacol. 449, 99-103
32. Alvarez-Jaimes, L., Stouffer, D. G., and Parsons, L. H. (2009) Chronic ethanol treatment potentiates ethanol-induced increases in interstitial nucleus accumbens endocannabinoid levels in rats J. Neurochem. 111, 37-48
33. Bequet, 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 (Pubitemid 350243513)
34. Buczynski, M. W. and Parsons, L. H. (2010) Quantification of brain endocannabinoid levels: methods, interpretations and pitfalls Br. J. Pharmacol. 160, 423-442
35. Long, J. Z., Nomura, D. K., and Cravatt, B. F. (2009) Characterization of monoacylglycerol lipase inhibition reveals differences in central and peripheral endocannabinoid metabolism Chem. Biol. 16, 744-753
36. Caille, S., Alvarez-Jaimes, L., Polis, I., Stouffer, D. G., and Parsons, L. H. (2007) Specific alterations of extracellular endocannabinoid levels in the nucleus accumbens by ethanol, heroin, and cocaine self-administration J. Neurosci. 27, 3695-3702 (Pubitemid 46557675)
37. Orio, L., Edwards, S., George, O., Parsons, L. H., and Koob, G. F. (2009) A role for the endocannabinoid system in the increased motivation for cocaine in extended-access conditions J. Neurosci. 29, 4846-4857
38. Ferrer, B., Bermudez-silva, F. J., Bilbao, A., Alvarez-jaimes, L., Sanchez-vera, I., Giuffrida, A., Serrano, A., Baixeras, E., Khaturia, S., Navarro, M., Parsons, L. H., Piomelli, D., and Rodriguez de Fonseca, F. (2007) Regulation of brain anandamide by acute administration of ethanol Biochem. J. 404, 97-104 (Pubitemid 46788089)
39. Giuffrida, A., Parsons, L. H., Kerr, T. M., Rodriguez de Fonseca, F., Navarro, M., and Piomelli, D. (1999) Dopamine activation of endogenous cannabinoid signaling in dorsal striatum Nat. Neurosci. 2, 358-363 (Pubitemid 30491279)
40. Di, S., Boudaba, C., Popescu, I. R., Weng, F. J., Harris, C., Marcheselli, V. L., Bazan, N. G., and Tasker, J. G. (2005) Activity-dependent release and actions of endocannabinoids in the rat hypothalamic supraoptic nucleus J. Physiol. 569, 751-760 (Pubitemid 41830220)
41. Jung, K.-M., Mangieri, R., Stapleton, C., Kim, J., Fegley, D., Wallace, M., Mackie, K., and Piomelli, D. (2005) Stimulation of Endocannabinoid Formation in Brain Slice Cultures through Activation of Group I Metabotropic Glutamate Receptors Mol. Pharmacol. 68, 1196-1202 (Pubitemid 41539977)
42. Hermann, A., Kaczocha, M., and Deutsch, D. G. (2006) 2- Arachidonoylglycerol (2-AG) membrane transport: history and outlook AAPS J. 8, E409-412
43. Yates, M. L. and Barker, E. L. (2009) Organized trafficking of anandamide and related lipids Vitam. Horm. 81, 25-53
44. de Lago, E., Petrosino, S., Valenti, M., Morera, E., Ortega-Gutierrez, S., Fernandez-Ruiz, J., and Di Marzo, V. (2005) Effect of repeated systemic administration of selective inhibitors of endocannabinoid inactivation on rat brain endocannabinoid levels Biochem. Pharmacol. 70, 446-452 (Pubitemid 40905116)
45. Beltramo, M., Stella, N., Calignano, A., Lin, S. Y., Makriyannis, A., and Piomelli, D. (1997) Functional role of high-affinity anandamide transport, as revealed by selective inhibition Science 277, 1094-1097 (Pubitemid 27371630)
46. Adamczyki, P., Golda, A., Mccreary, A. C., Filip, M., and Przegalnski, E. (2008) Activation of endocannabinoid transmission induces antidepressant-like effects in rats J. Physiol. Pharmacol. 59, 217-228 (Pubitemid 351955748)
47. De Lago, E., Gustafsson, S. B., Fernandez-Ruiz, J., Nilsson, J., Jacobsson, S. O., and Fowler, C. J. (2006) Acyl-based anandamide uptake inhibitors cause rapid toxicity to C6 glioma cells at pharmacologically relevant concentrations J. Neurochem. 99, 677-688 (Pubitemid 44477221)
48. Ronesi, J., Gerdeman, G. L., and Lovinger, D. M. (2004) Disruption of endocannabinoid release and striatal long-term depression by postsynaptic blockade of endocannabinoid membrane transport J. Neurosci. 24, 1673-1679 (Pubitemid 38240964)
49. Adermark, L. and Lovinger, D. M. (2007) Retrograde endocannabinoid signaling at striatal synapses requires a regulated postsynaptic release step Proc. Natl. Acad. Sci. U.S.A. 104, 20564-20569
50. Fu, J., Bottegoni, G., Sasso, O., Bertorelli, R., Rocchia, W., Masetti, M., Guijarro, A., Lodola, A., Armirotti, A., Garau, G., Bandiera, T., Reggiani, A., Mor, M., Cavalli, A., and Piomelli, D. (2012) A catalytically silent FAAH-1 variant drives anandamide transport in neurons Nat. Neurosci. 15, 64-69
51. Jayamanne, A., Greenwood, R., Mitchell, V. A., Aslan, S., Piomelli, D., and Vaughan, C. W. (2006) Actions of the FAAH inhibitor URB597 in neuropathic and inflammatory chronic pain models Br. J. Pharmacol. 147, 281-288 (Pubitemid 43214685)
52. Rock, E. M., Limebeer, C. L., Mechoulam, R., Piomelli, D., and Parker, L. A. (2008) The effect of cannabidiol and URB597 on conditioned gaping (a model of nausea) elicited by a lithium-paired context in the rat Psychopharmacology 196, 389-395
53. Hasanein, P., Shahidi, S., Komaki, A., and Mirazi, N. (2008) Effects of URB597 as an inhibitor of fatty acid amide hydrolase on modulation of nociception in a rat model of cholestasis Eur. J. Pharmacol. 591, 132-135
54. Cippitelli, A., Astarita, G., Duranti, A., Caprioli, G., Ubaldi, M., Stopponi, S., Kallupi, M., Sagratini, G., Rodriguez de Fonseca, F., Piomelli, D., and Ciccocioppo, R. (2011) Endocannabinoid regulation of acute and protracted nicotine withdrawal: effect of FAAH inhibition PloS One 6, e28142
55. Kathuria, S., Gaetani, S., Fegley, D., Valino, F., Duranti, A., Tontini, A., Mor, M., Tarzia, G., Rana, G. L., Calignano, A., Giustino, A., Tattoli, M., Palmery, M., Cuomo, V., and Piomelli, D. (2003) Modulation of anxiety through blockade of anandamide hydrolysis Nat. Med. 9, 76-81 (Pubitemid 36098263)
56. King, A. R., Duranti, A., Tontini, A., Rivara, S., Rosengarth, A., Clapper, J. R., Astarita, G., Geaga, J. A., Luecke, H., Mor, M., Tarzia, G., and Piomelli, D. (2007) URB602 inhibits monoacylglycerol lipase and selectively blocks 2-arachidonoylglycerol degradation in intact brain slices Chem. Biol. 14, 1357-1365 (Pubitemid 350257009)
57. Comelli, F., Giagnoni, G., Bettoni, I., Colleoni, M., and Costa, B. (2007) The inhibition of monoacylglycerol lipase by URB602 showed an anti-inflammatory and anti-nociceptive effect in a murine model of acute inflammation Br. J. Pharmacol. 152, 787-794 (Pubitemid 350034978)
58. Vandevoorde, S., Jonsson, K. O., Labar, G., Persson, E., Lambert, D. M., and Fowler, C. J. (2007) Lack of selectivity of URB602 for 2-oleoylglycerol compared to anandamide hydrolysis in vitro Br. J. Pharmacol. 150, 186-191 (Pubitemid 46160608)
59. Sciolino, N. R., Zhou, W. Y., and Hohmann, A. G. (2011) 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
60. Oleson, E. B., Beckert, M. V., Morra, J. T., Lansink, C. S., Cachope, R., Abdullah, R. A., Loriaux, A. L., Schetters, D., Pattij, T., Roitman, M. F., Lichtman, A. H., and Cheer, J. F. (2012) Endocannabinoids Shape Accumbal Encoding of Cue-Motivated Behavior via CB1 Receptor Activation in the Ventral Tegmentum Neuron 73, 360-373
61. Naidoo, V., Karanian, D. A., Vadivel, S. K., Locklear, J. R., Wood, J. T., Nasr, M., Quizon, P. M., Graves, E. E., Shukla, V., Makriyannis, A., and Bahr, B. A. Equipotent Inhibition of Fatty Acid Amide Hydrolase and Monoacylglycerol Lipase-Dual Targets of the Endocannabinoid System to Protect against Seizure Pathology. Neurotherapeutics 2012, not supplied.
62. Cisneros, J. A., Bjorklund, E., Gonzalez-Gil, I., Hu, Y., Canales, A., Medrano, F. J., Romero, A., Ortega-Gutierrez, S., Fowler, C. J., and Lopez-Rodriguez, M. L. (2012) Structure-activity relationship of a new series of reversible dual monoacylglycerol lipase/fatty Acid amide hydrolase inhibitors J. Med. Chem. 55, 824-836
63. Paxinos, G. and Watson, C. (1998) The rat brain in stereotaxic coordinates, 4 th ed., Academic Press, San Diego.
64. Paxinos, G. and Franklin, K. B. J. (2001) The mouse brain in stereotaxic coordinates, 2 nd ed., Academic Press, San Diego.