Inhibitors of monoacylglycerol lipase, fatty-acid amide hydrolase and endocannabinoid transport differentially suppress capsaicin-induced behavioral sensitization through peripheral endocannabinoid mechanisms

Pharmacological Research

Volumn 62, Issue 3, 2010, Pages 249-258

  Spradley, Jessica M ^a   Guindon, Josée ^b   Hohmann, Andrea G ^a,b  

^a UNIVERSITY OF GEORGIA   (United States)

^b NONE   (United States)

Author keywords

Capsaicin; Endocannabinoid; Endocannabinoid transport; Fatty acid amide ydrolase; Monoacylglycerol lipase; Pain

Indexed keywords

2 ARACHIDONOYLGLYCEROL; 4 NITROPHENYL 4 [DIBENZO[D][1,3]DIOXOL 5 YL(HYDROXYL)METHYL]PIPERIDINE 1 CARBOXYLATE; ACYLGLYCEROL LIPASE; ANANDAMIDE; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; CAPSAICIN; CYCLOHEXYLCARBAMIC ACID 3' CARBAMOYLBIPHENYL 3 YL ESTER; ENDOCANNABINOID; ESTERASE INHIBITOR; FATTY ACID AMIDASE; JZL 184; N (4 HYDROXY 2 METHYLPHENYL)ARACHIDONAMIDE; UNCLASSIFIED DRUG; 1,3 BENZODIOXOLE DERIVATIVE; 4 [BIS(1,3 BENZODIOXOL 5 YL)HYDROXYMETHYL] 1 PIPERIDINECARBOXYLIC ACID 4 NITROPHENYL ESTER; AGENTS ACTING ON THE PERIPHERAL NERVOUS AND NEUROMUSCULAR SYSTEMS; AMIDASE; ARACHIDONIC ACID DERIVATIVE; BENZAMIDE DERIVATIVE; CANNABINOID RECEPTOR AFFECTING AGENT; CARBAMIC ACID DERIVATIVE; CYCLOHEXYL CARBAMIC ACID 3'-CARBAMOYLBIPHENYL-3-YL ESTER; FATTY-ACID AMIDE HYDROLASE; N-(2-METHYL-3-HYDROXYPHENYL)-5,8,11,14-EICOSATETRAENAMIDE; PIPERIDINE DERIVATIVE;

ALLODYNIA; ANALGESIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; DRUG DOSE COMPARISON; DRUG EFFICACY; DRUG MEGADOSE; DRUG SPECIFICITY; ENZYME INHIBITION; HYPERALGESIA; LOW DRUG DOSE; MALE; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; RAT; ANIMAL; ANIMAL BEHAVIOR; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; METABOLISM; SPRAGUE DAWLEY RAT; TRANSPORT AT THE CELLULAR LEVEL;

AMIDOHYDROLASES; ANIMALS; ARACHIDONIC ACIDS; BEHAVIOR, ANIMAL; BENZAMIDES; BENZODIOXOLES; BIOLOGICAL TRANSPORT; CAPSAICIN; CARBAMATES; ENDOCANNABINOIDS; MALE; MONOACYLGLYCEROL LIPASES; PIPERIDINES; RATS; RATS, SPRAGUE-DAWLEY; SENSORY SYSTEM AGENTS; CANNABINOID RECEPTOR MODULATORS;

EID: 77954145799     PISSN: 10436618     EISSN: 10961186     Source Type: Journal    
DOI: 10.1016/j.phrs.2010.03.007     Document Type: Article

References (68)

1. Gilchrist H.D., Allard B.L., Simone D.A. Enhanced withdrawal responses to heat and mechanical stimuli following intraplantar injection of capsaicin in rats. Pain 1996, 67:179-188.
2. Kenins P. Responses of single nerve fibres to capsaicin applied to the skin. Neurosci Lett 1982, 29:83-88.
3. Szolcsanyi J., Anton F., Reeh P.W., Handwerker H.O. Selective excitation by capsaicin of mechano-heat sensitive nociceptors in rat skin. Brain Res 1988, 446:262-268.
4. Baumann T.K., Simone D.A., Shain C.N., LaMotte R.H. Neurogenic hyperalgesia: the search for the primary cutaneous afferent fibers that contribute to capsaicin-induced pain and hyperalgesia. J Neurophysiol 1991, 66:212-227.
5. LaMotte R.H., Lundberg L.E., Torebjork H.E. Pain, hyperalgesia and activity in nociceptive C units in humans after intradermal injection of capsaicin. J Physiol 1992, 448:749-764.
6. Torebjork H.E., Lundberg L.E., LaMotte R.H. Central changes in processing of mechanoreceptive input in capsaicin-induced secondary hyperalgesia in humans. J Physiol 1992, 448:765-780.
7. Serra J., Campero M., Bostock H., Ochoa J. Two types of C nociceptors in human skin and their behavior in areas of capsaicin-induced secondary hyperalgesia. J Neurophysiol 2004, 91:2770-2781.
8. Caterina M.J., Schumacher M.A., Tominaga M., Rosen T.A., Levine J.D., Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 1997, 389:816-824.
9. Szallasi A., Blumberg P.M. Vanilloid (capsaicin) receptors and mechanisms. Pharmacol Rev 1991, 51:159-212.
10. Tominaga M., Caterina M.J., Malmberg A.B., Rosen T.A., Gilbert H., Skinner K., et al. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 1998, 21:531-543.
11. Davis J.B., Gray J., Gunthorpe M.J., Hatcher J.P., Davey P.T., Overend P., et al. Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 2000, 405:183-187.
12. Matsuda L.A., Lolait S.J., Brownstein M.J., Young A.C., Bonner T.I. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 1990, 346:561-564.
13. Ledent C., Valverde O., Cossu G., Petitet F., Aubert J.F., Beslot F., et al. Unresponsiveness to cannabinoids and reduced addictive effects of opiates in CB1 receptor knockout mice. Science 1999, 283:401-404.
14. Zimmer A., Zimmer A.M., Hohmann A.G., Herkenham M., Bonner T.I. Increased mortality, hypoactivity, and hypoalgesia in cannabinoid CB1 receptor knockout mice. Proc Natl Acad Sci USA 1999, 96:5780-5785.
15. Munro S., Thomas K.L., Abu-Shaar M. Molecular characterization of a peripheral receptor for cannabinoids. Nature 1993, 365:61-65.
16. Walker J.M., Hohmann A.G. Cannabinoid mechanisms of pain suppression. Handbook Exp Pharmacol 2005, 168:509-554.
17. Devane W.A., Hanus L., Breuer A., Pertwee R.G., Stevenson L.A., Griffin G., et al. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 1992, 258:1946-1949.
18. Piomelli D. The molecular logic of endocannabinoid signaling. Nat Rev Neurosci 2003, 4:873-884.
19. Cravatt B.F., Giang D.K., Mayfield S.P., Boger D.L., Lerner R.A., Gilula N.B. Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides. Nature 1996, 384:83-87.
20. Dinh T.P., Carpenter D., Leslie F.M., Freund T.F., Katona I., Sensi S.L., et al. Brain monoacylglyceride lipase participating in endocannabinoid inactivation. Proc Natl Acad Sci USA 2002, 99:10819-10824.
21. Zygmunt P.M., Petersson J., Andersson D.A., Chuang H., Sorgard M., Di Marzo V., et al. Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature 1999, 400:452-457.
22. Al-Hayani A., Wease K.N., Ross R.A., Pertwee R.G., Davis S.N. The endogenous cannabinoid anandamide activates vanilloid receptors in the rat hippocampal slice. Neuropharmacology 2001, 41:1000-1005.
23. Maione S., Bisogno T., de Novellis V., Palazzo E., Cristino L., Valenti M., et al. Elevation of endocannabinoid levels in the ventrolateral periaqueductal gray through inhibition of fatty acid amide hydrolase affects descending nociceptive pathways via both cannabinoid receptor type 1 and transient receptor potential vanilloid type-1 receptors. J Pharmacol Exp Ther 2006, 316:969-982.
24. Calignano A., La Rana G., Piomelli D. Antinociceptive activity of the endogenous fatty acid amide, palmitylethanolamide. Eur J Pharmacol 2001, 419:191-198.
25. Potenzieri C., Brink T.S., Simone D.A. Excitation of cutaneous C nociceptors by intraplantar administration of anandamide. Brain Res 2009, 1268:38-47.
26. Agarwal N., Pacher P., Tegeder I., Amaya F., Constantin C.E., Brenner G.J., et al. Cannabinoids mediate analgesia largely via peripheral type I cannabinoid receptors in nociceptors. Nat Neurosci 2007, 10:870-879.
27. Calignano A., La Rana G., Giuffrida A., Piomelli D. Control of pain initiation by endogenous cannabinoids. Nature 1998, 394:277-281.
28. Richardson J.D., Kilo S., Hargreaves K.M. Cannabinoid reduce hyperalgesia and inflammation via interaction with peripheral CB1 receptors. Pain 1998, 75:111-119.
29. Guindon J., LoVerme J., De Lean A., Piomelli D., Beaulieu P. Synergistic antinociceptive effects of anandamide, an endocannabinoid, and nonsteroidal anti-inflammatory drugs in peripheral tissue: a role for endogenous fatty-acid ethanolamides?. Eur J Pharmacol 2006, 550:68-77.
30. Guindon J., De Lean A., Beaulieu P. Local interactions between anandamide, an endocannabinoid, and ibuprofen, a nonsteroidal anti-inflammatory drug, in acute and inflammatory pain. Pain 2006, 121:85-93.
31. Guindon J., Desroches J., Beaulieu P. The antinociceptive effects of intraplantar injections of 2-arachidonoyl glycerol are mediated by cannabinoid CB2 receptors. Br J Pharmacol 2007, 150:693-701.
32. Hohmann A.G., Farthing J.N., Zvonok A.M., Makriyannis A. Selective activation of cannabinoid CB2 receptors suppresses hyperalgesia evoked by intradermal capsaicin. J Pharmacol Exp Ther 2004, 308:446-453.
33. Quartilho A., Mata H.P., Ibrahim M.M., Vanderah T.W., Porreca F., Makriyannis A., et al. Inhibition of inflammatory hyperalgesia by activation of peripheral CB2 cannabinoid receptors. Anesthesiology 2003, 99:955-960.
34. Johanek L.M., Heitmiller D.R., Turner M., Nader N., Hodges J., Simone D.A. Cannabinoids attenuate capsaicin-evoked hyperalgesia through spinal and peripheral mechanisms. Pain 2001, 93:303-315.
35. Johanek L.M., Simone D.A. Activation of peripheral cannabinoid receptors attenuates cutaneous hyperalgesia produced by a heat injury. Pain 2004, 109:432-442.
36. Jhaveri M.D., Richardson D., Chapman V. Endocannabinoid metabolism and uptake: novel targets for neuropathic and inflammatory pain. Br J Pharmacol 2007, 152:624-632.
37. Costa B., Bettoni I., Petrosino S., Comelli F., Giagnoni G., Di Marzo V. The dual fatty acid amide hydrolase/TRPV1 blocker, N-arachidonoyl-serotonin, relieves carrageenan-induced inflammation and hyperalgesia in mice. Pharmacol Res 2010, [Epub ahead of print].
38. Maione S., De Petrocellis L., de Novellis V., Moriello A.S., Petrosino S., Palazzo E., et al. Analgesic actions of N-arachidonoyl-serotonin, a fatty acid amide hydrolase inhibitor with antagonistic activity at vanilloid TRPV1 receptors. Br J Pharmacol 2007, 150:766-781.
39. Jhaveri M.D., Richardson D., Robinson I., Garle M.J., Patel A., Sun Y., et al. Inhibition of fatty acid amide hydrolase and cyclooxygenase-2 increases levels of endocannabinoid related molecules and produces analgesia via peroxisome proliferator-activated receptor-alpha in a model of inflammatory pain. Neuropharmacology 2008, 55:85-93.
40. Long J.Z., Li W., Booker L., Burston J.J., Kinsey S.G., Schlosburg J.E., et al. Selective blockade of 2-arachidonoylglycerol hydrolysis produces cannabinoid behavioral effects. Nat Chem Biol 2009, 5:37-44.
41. Kinsey S.G., Long J.Z., O'Neal S.T., Abdullah R.A., Poklis J.L., Boger D.L., et al. Blockade of endocannabinoid-degrading enzymes attenuates neuropathic pain. J Pharmacol Exp Ther 2009, 330:902-910.
42. de Lago E., Petrosino S., Valenti M., Morera E., Ortega-Gutierrez S., Fernandez-Ruiz J., et al. Effect of repeated systemic administration of selective inhibitors of endocannabinoid inactivation on rat brain endocannabinoid levels. Biochem Pharmacol 2005, 70:446-452.
43. Calignano A., La Rana G., Giuffrida A., Piomelli D. Control of pain initiation by endogenous cannabinoids. Nature 1998, 394:227-281.
44. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 1983, 16:109-110.
45. Moezi L., Gaskari S.A., Liu H., Baik S.K., Dehpour A.R., Lee S.S. Anandamide mediates hyperdynamic circulation in cirrhotic rats via CB(1) and VR(1) receptors. Br J Pharmacol 2006, 149:898-908.
46. Hargreaves K., Dubner R., Brown F., Flores C., Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 1988, 32:77-88.
47. Desroches J., Guindon J., Lambert C., Beaulieu P. Modulation of the anti-nociceptive effects of 2-arachidonoyl glycerol by peripherally administered FAAH and MGL inhibitors in a neuropathic pain model. Br J Pharmacol 2008, 155:913-924.
48. Nackley A.G., Suplita R.L., Hohmann A.G. A peripheral cannabinoid mechanism suppresses spinal Fos protein expression and pain behavior in a rat model of inflammation. Neuroscience 2003, 117:659-670.
49. Nackley A.G., Zvonok A.M., Makriyannis A., Hohmann A.G. Activation of cannabinoid CB2 receptors suppresses C-fiber responses and windup in spinal wide dynamic range neurons in the absence and presence of inflammation. J Neurophysiol 2004, 92:3562-3574.
50. Lim G., Sung B., Ji R.R., Mao J. Upregulation of spinal cannabinoid-1 receptors following nerve injury enhances the effects of Win55,212-2 on neuropathic pain behaviors in rats. Pain 2003, 105:275-283.
51. Mitrirattanakul S., Ramakul N., Guerrero A.V., Matsuka Y., Ono T., Iwase H., et al. Site-specific increases in peripheral cannabinoid receptors and their endogenous ligands in a model of neuropathic pain. Pain 2006, 126:102-114.
52. Lever I.J., Robinson M., Cibelli M., Paule C., Santa P., Yee L., 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 2009, 29:3766-3780.
53. Gulyas A.I., Cravatt B.F., Bracey M.H., Dinh T.P., Piomelli D., Boscia F., et al. Segregation of two endocannabinoid-hydrolyzing enzymes into pre- and postsynaptic compartments in the rat hippocampus, cerebellum and amygdala. Eur J Neurosci 2004, 20:441-458.
54. Muccioli G.G., Xu C., Odah E., Cudaback E., Cisneros J.A., Lambert D.M., et al. Identification of a novel endocannabinoid-hydrolyzing enzyme expressed by microglial cells. J Neurosci 2007, 27:2883-2889.
55. Gonsiorek W., Lunn C., Fan X., Narula S., Lundell D., Hipkin R.W. Endocannabinoid 2-arachidonoyl glycerol is a full agonist through human type 2 cannabinoid receptor: antagonism by anandamide. Mol Pharmacol 2000, 57:1045-1050.
56. Ahluwalia J., Urban L., Bevan S., Nagy I. Anandamide regulates neuropeptide release from capsaicin-sensitive primary sensory neurons by activating both the cannabinoid 1 receptor and the vanilloid receptor 1 in vitro. Eur J Neurosci 2003, 17:2611-2618.
57. 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 2006, 26:13318-13327.
58. 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 1999, 90:923-931.
59. Bridges D., Rice A.S., Egertova M., Elphick M.R., Winter J., Michael G.J. Localisation of cannabinoid receptor 1 in rat dorsal root ganglion using in situ hybridisation and immunohistochemistry. Neuroscience 2003, 119:803-812.
60. Hohmann A.G., Herkenham M. Cannabinoid receptors undergo axonal flow in sensory nerves. Neuroscience 1999, 92:1171-1175.
61. Anand U., Otto W.R., Sanchez-Herrera D., Facer D., Yiangou Y., Korchev Y., et al. Cannabinoid receptor CB2 localisation and agonist-mediated inhibition of capsaicin responses in human sensory neurons. Pain 2008, 138:667-680.
62. Holzer P. Acid-sensitive ion channels and receptors. Handbook Exp Pharmacol 2009, 194:283-332.
63. Glaser S.T., Abumrad N.A., Fatade F., Kaczocha M., Studholme K.M., Deutsch D.G. Evidence against the presence of an anandamide transporter. Proc Natl Acad Sci USA 2003, 100:4269-4274.
64. Fegley D., Kathuria S., Mercier R., Li C., Goutopoulos A., Makriyannis A., et al. Anandamide transport is independent of fatty-acid amide hydrolase activity and is blocked by the hydrolysis-resistant inhibitor AM1172. Proc Natl Acad Sci USA 2004, 101:8756-8761.
65. Kaczocha M., Glaser S.T., Deutsch D.G. Identification of intracellular carriers for the endocannabinoid anandamide. Proc Natl Acad Sci USA 2009, 106:6375-6380.
66. De Petrocellis L., Bisogno T., Davis J.B., Pertwee R.G., Di Marzo V. Overlap between the ligand recognition properties of the anandamide transporter and the VR1 vanilloid receptor: inhibitors of anandamide transport with negligible capsaicin-like activity. FEBS Lett 2000, 483:52-56.
67. Zygmunt P.M., Chuang H., Movahed P., Julius D., Hogestatt E.D. The anandamide transport inhibitor AM404 activates vanilloid receptors. Eur J Pharmacol 2000, 396:39-42.
68. De Petrocellis L., Bisogno T., Maccarrone M., Davis J.B., Finazzi-Agro A., Di Marzo V. The activity of anandamide at vanilloid VR1 receptors requires facilitated transport across the cell membrane and is limited by intracellular metabolism. J Biol Chem 2001, 276:12856-12863.