Anandamide suppresses pain initiation through a peripheral endocannabinoid mechanism

Nature Neuroscience

Volumn 13, Issue 10, 2010, Pages 1265-1270

  Clapper, Jason R ^a   Moreno Sanz, Guillermo ^a,b   Russo, Roberto ^c   Guijarro, Ana ^a   Vacondio, Federica ^d   Duranti, Andrea ^e   Tontini, Andrea ^e   Sanchini, Silvano ^e   Sciolino, Natale R ^f   Spradley, Jessica M ^g   Hohmann, Andrea G ^f,g   Calignano, Antonio ^c   Mor, Marco ^d   Tarzia, Giorgio ^e   Piomelli, Daniele ^a,h  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^c UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^d UNIVERSITY OF PARMA   (Italy)

^e UNIVERSITY OF URBINO   (Italy)

^f University of Georgia   (United States)

^g UNIVERSITY OF GEORGIA   (United States)

^h ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; 1,2,3,4,6,7,12,12A OCTAHYDRO 6 ISOBUTYL 9 METHOXY 1,4 DIOXOPYRAZINO[1',2':1,6]PYRIDO[3,4 B]INDOLE 3 PROPANOIC ACID TERT BUTYL ESTER; 2,6 DICHLORO 4 NITROPHENOL; 3 [3 TERT BUTYLTHIO 1 (4 CHLOROBENZYL) 5 ISOPROPYL 2 INDOLYL] 2,2 DIMETHYLPROPIONIC ACID; ANANDAMIDE; CANNABINOID 1 RECEPTOR; CANNABINOID RECEPTOR; CYCLOHEXYLCARBAMIC ACID 3' CARBAMOYLBIPHENYL 3 YL ESTER; ENDOCANNABINOID; FATTY ACID AMIDASE; FATTY ACID AMIDASE INHIBITOR; INDOMETACIN; PROBENECID; PROTEIN FOS; RIFAMPICIN; RIMONABANT; UNCLASSIFIED DRUG; URB 937; VERAPAMIL; ACYLGLYCEROL LIPASE; AMIDASE; AMIDE; ARACHIDONIC ACID DERIVATIVE; ARACHIDONOYLETHYLENE GLYCOL; CANNABINOID; CANNABINOID RECEPTOR AFFECTING AGENT; CARRAGEENAN; ENZYME INHIBITOR; ETHYLENE GLYCOL DERIVATIVE; FATTY-ACID AMIDE HYDROLASE; FORMALDEHYDE; INDOLE DERIVATIVE; IODOPRAVADOLINE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PIPERIDINE DERIVATIVE; PROTEIN V FOS; PYRAZOLE DERIVATIVE; TRITIUM; URB937;

ANALGESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINOCICEPTION; ARTICLE; BLOOD BRAIN BARRIER; CONTROLLED STUDY; DRUG TISSUE LEVEL; DRUG TRANSPORT; INFLAMMATION; LIPOPHILICITY; MALE; MOUSE; NOCICEPTION; NONHUMAN; PAIN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CHEMICALLY INDUCED; DEFICIENCY; DIAGNOSTIC USE; DISEASE MODEL; DRUG ADMINISTRATION; DRUG ADMINISTRATION ROUTE; DRUG EFFECTS; ESCAPE BEHAVIOR; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION; GENETICS; HYPERALGESIA; KNOCKOUT MOUSE; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLISM; MOTOR ACTIVITY; NONPARAMETRIC TEST; PAIN MEASUREMENT; PAIN THRESHOLD; PATHOLOGY; PERIPHERAL NEUROPATHY; PROCEDURES; RAT; SCIATICA; SPINAL CORD; SPRAGUE DAWLEY RAT; TIME; TISSUE DISTRIBUTION;

AMIDOHYDROLASES; ANIMALS; ARACHIDONIC ACIDS; CANNABINOIDS; CARRAGEENAN; CHROMATOGRAPHY, LIQUID; DISEASE MODELS, ANIMAL; DRUG ADMINISTRATION ROUTES; DRUG ADMINISTRATION SCHEDULE; ENDOCANNABINOIDS; ENZYME INHIBITORS; ESCAPE REACTION; ETHYLENE GLYCOLS; FEEDING BEHAVIOR; FORMALDEHYDE; GENE EXPRESSION REGULATION; HYPERALGESIA; INDOLES; MALE; MASS SPECTROMETRY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MONOACYLGLYCEROL LIPASES; MOTOR ACTIVITY; ONCOGENE PROTEINS V-FOS; PAIN; PAIN MEASUREMENT; PAIN THRESHOLD; PERIPHERAL NERVOUS SYSTEM DISEASES; PIPERIDINES; POLYUNSATURATED ALKAMIDES; PPAR ALPHA; PYRAZOLES; RATS; RATS, SPRAGUE-DAWLEY; SCIATICA; SPINAL CORD; STATISTICS, NONPARAMETRIC; TIME FACTORS; TISSUE DISTRIBUTION; TRITIUM; CANNABINOID RECEPTOR MODULATORS;

EID: 77957263726     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn.2632     Document Type: Article

References (42)

1. Stein, C., Schafer, M. & Machelska, H. Attacking pain at its source: new perspectives on opioids. Nat. Med. 9, 1003-1008 (2003).
2. Calignano, A., La Rana, G., Giuffrida, A. & Piomelli, D. Control of pain initiation by endogenous cannabinoids. Nature 394, 277-281 (1998).
3. Nackley, A.G., Suplita, R.L. II & Hohmann, A.G. A peripheral cannabinoid mechanism suppresses spinal fos protein expression and pain behavior in a rat model of infammation. Neuroscience 117, 659-670 (2003).
4. Dziadulewicz, E.K. et al. Naphthalen-1-yl-(4-pentyloxynaphthalen-1-yl) methanone: a potent, orally bioavailable human CB1/CB2 dual agonist with antihyperalgesic properties and restricted central nervous system penetration. J. Med. Chem. 50, 3851-3856 (2007).
5. Anand, P., Whiteside, G., Fowler, C.J. & Hohmann, A.G. Targeting CB2 receptors and the endocannabinoid system for the treatment of pain. Brain Res. Rev. 60, 255-266 (2009).
6. Agarwal, N. et al. Cannabinoids mediate analgesia largely via peripheral type 1 cannabinoid receptors in nociceptors. Nat. Neurosci. 10, 870-879 (2007).
7. Kaufmann, I. et al. Enhanced anandamide plasma levels in patients with complex regional pain syndrome following traumatic injury: a preliminary report. Eur. Surg. Res. 43, 325-329 (2009).
8. Richardson, D. et al. Characterization of the cannabinoid receptor system in synovial tissue and fuid in patients with osteoarthritis and rheumatoid arthritis. Arthritis Res. Ther. 10, R43 (2008).
9. Mitrirattanakul, S. et al. Site-specifc increases in peripheral cannabinoid receptors and their endogenous ligands in a model of neuropathic pain. Pain 126, 102-114 (2006).
10. Schlosburg, J.E., Kinsey, S.G. & Lichtman, A.H. Targeting fatty acid amide hydrolase (FAAH) to treat pain and infammation. AAPS J. 11, 39-44 (2009).
11. Kathuria, S. et al. Modulation of anxiety through blockade of anandamide hydrolysis. Nat. Med. 9, 76-81 (2003).
12. Piomelli, D. et al. Pharmacological profle of the selective FAAH inhibitor KDS-4103 (URB597). CNS Drug Rev. 12, 21-38 (2006).
13. Clapper, J.R. et al. A second generation of carbamate-based fatty acid amide hydrolase inhibitors with improved activity in vivo. ChemMedChem 4, 1505-1513 (2009).
14. Alexander, J.P. & Cravatt, B.F. Mechanism of carbamate inactivation of FAAH: implications for the design of covalent inhibitors and in vivo functional probes for enzymes. Chem. Biol. 12, 1179-1187 (2005).
15. Löscher, W. & Potschka, H. Blood-brain barrier active effux transporters: ATP-binding cassette gene family. NeuroRx 2, 86-98 (2005).
16. Imai, Y. et al. Breast cancer resistance protein exports sulfated estrogens, but not free estrogens. Mol. Pharmacol. 64, 610-618 (2003).
17. LoVerme, J., La Rana, G., Russo, R., Calignano, A. & Piomelli, D. The search for the palmitoylethanolamide receptor. Life Sci. 77, 1685-1698 (2005).
18. 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).
19. Starowicz, K., Nigam, S. & Di Marzo, V. Biochemistry and pharmacology of endovanilloids. Pharmacol. Ther. 114, 13-33 (2007).
20. LoVerme, J. et al. Rapid broad-spectrum analgesia through activation of peroxisome proliferator-activated receptor alpha. J. Pharmacol. Exp. Ther. 319, 1051-1061 (2006).
21. Russo, R. et al. Synergistic antinociception by the cannabinoid receptor agonist anandamide and the PPAR alpha receptor agonist GW7647. Eur. J. Pharmacol. 566, 117-119 (2007).
22. Bennett, G.J. & Xie, Y.K. A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33, 87-107 (1988).
23. Russo, R. et al. The fatty acid amide hydrolase inhibitor URB597 (cyclohexylcarbamic acid 3′-carbamoylbiphenyl-3-yl ester) reduces neuropathic pain after oral administration in mice. J. Pharmacol. Exp. Ther. 322, 236-242 (2007).
24. Coderre, T.J. & Melzack, R. The contribution of excitatory amino acids to central sensitization and persistent nociception after formalin-induced tissue injury. J. Neurosci. 12, 3665-3670 (1992).
25. Puig, S. & Sorkin, L.S. Formalin-evoked activity in identifed primary afferent fbers: systemic lidocaine suppresses phase-2 activity. Pain 64, 345-355 (1996).
26. Kunos, G., Osei-Hyiaman, D., Batkai, S., Sharkey, K.A. & Makriyannis, A. Should peripheral CB(1) cannabinoid receptors be selectively targeted for therapeutic gain? Trends Pharmacol. Sci. 30, 1-7 (2009).
27. Ahluwalia, J., Yaqoob, M., Urban, L., Bevan, S. & Nagy, I. Activation of capsaicin-sensitive primary sensory neurones induces anandamide production and release. J. Neurochem. 84, 585-591 (2003).
28. Liu, J. et al. A biosynthetic pathway for anandamide. Proc. Natl. Acad. Sci. USA 103, 13345-13350 (2006).
29. Hohmann, A.G. & Herkenham, M. Localization of central cannabinoid CB1 receptor messenger RNA in neuronal subpopulations of rat dorsal root ganglia: a double-label in situ hybridization study. Neuroscience 90, 923-931 (1999).
30. Hohmann, A.G. & Herkenham, M. Cannabinoid receptors undergo axonal fow in sensory nerves. Neuroscience 92, 1171-1175 (1999).
31. Richardson, J.D., Kilo, S. & Hargreaves, K.M. Cannabinoids reduce hyperalgesia and infammation via interaction with peripheral CB1 receptors. Pain 75, 111-119 (1998).
32. Guindon, J. & Hohmann, A.G. Cannabinoid CB2 receptors: a therapeutic target for the treatment of infammatory and neuropathic pain. Br. J. Pharmacol. 153, 319-334 (2008).
33. Sagar, D.R., Kendall, D.A. & Chapman, V. Inhibition of fatty acid amide hydrolase produces PPAR alpha-mediated analgesia in a rat model of infammatory pain. Br. J. Pharmacol. 155, 1297-1306 (2008).
34. Cravatt, B.F. et al. Functional disassociation of the central and peripheral fatty acid amide signaling systems. Proc. Natl. Acad. Sci. USA 101, 10821-10826 (2004).
35. Lever, I.J. et al. Localization of the endocannabinoid-degrading enzyme fatty acid amide hydrolase in rat dorsal root ganglion cells and its regulation after peripheral nerve injury. J. Neurosci. 29, 3766-3780 (2009).
36. Stein, C. & Zollner, C. Opioids and sensory nerves. Handb. Exp. Pharmacol. 194, 495-518 (2009).
37. Tegeder, I. et al. Peripheral opioid analgesia in experimental human pain models. Brain 126, 1092-1102 (2003).
38. Mor, M. et al. Cyclohexylcarbamic acid 3′-or 4′-substituted biphenyl-3-yl esters as fatty acid amide hydrolase inhibitors: synthesis, quantitative structure-activity relationships, and molecular modeling studies. J. Med. Chem. 47, 4998-5008 (2004).
39. King, A.R. et al. URB602 inhibits monoacylglycerol lipase and selectively blocks 2-arachidonoylglycerol degradation in intact brain slices. Chem. Biol. 14, 1357-1365 (2007).
40. Astarita, G., Ahmed, F. & Piomelli, D. Identifcation of biosynthetic precursors for the endocannabinoid anandamide in the rat brain. J. Lipid Res. 49, 48-57 (2008).
41. Calignano, A., La Rana, G. & Piomelli, D. Antinociceptive activity of the endogenous fatty acid amide, palmitylethanolamide. Eur. J. Pharmacol. 419, 191-198 (2001).
42. Tjølsen, A., Berge, O.G., Hunskaar, S., Rosland, J.H. & Hole, K. The formalin test: an evaluation of the method. Pain 51, 5-17 (1992).