Fatty acid amide hydrolase blockade attenuates the development of collagen-induced arthritis and related thermal hyperalgesia in mice

Pharmacology Biochemistry and Behavior

Volumn 99, Issue 4, 2011, Pages 718-725

  Kinsey, Steven G ^a,b   Naidu, Pattipati S ^b   Cravatt, Benjamin F ^c   Dudley, David T ^d   Lichtman, Aron H ^b  

^a WEST VIRGINIA UNIVERSITY   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d PFIZER INC   (United States)

Author keywords

Anandamide; Chronic inflammation; Collagen induced arthritis; Endocannabinoid; Fatty acid amide hydrolase (FAAH); Inflammatory pain

Indexed keywords

ANANDAMIDE; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; CYCLOHEXYLCARBAMIC ACID 3' CARBAMOYLBIPHENYL 3 YL ESTER; FATTY ACID AMIDASE;

ANALGESIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANKLE; ARTHRITIS; ARTICLE; BONE EROSION; CELL INFILTRATION; CHONDROPATHY; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; GENE DELETION; HISTOPATHOLOGY; HYPERALGESIA; INFLAMMATORY CELL; JOINT INJURY; KNEE; MALE; MOUSE; NERVOUS SYSTEM; NONHUMAN; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPEATED DRUG DOSE; THERMAL HYPERALGESIA; TRANSGENIC MOUSE; WILD TYPE;

AMIDOHYDROLASES; ANIMALS; ARTHRITIS, EXPERIMENTAL; BENZAMIDES; BORNANES; CARBAMATES; FOOT; GENOTYPE; HOT TEMPERATURE; HYPERALGESIA; MALE; MICE; MICE, INBRED DBA; MICE, KNOCKOUT; PAIN MEASUREMENT; PHENOTYPE; PYRAZOLES; RECEPTOR, CANNABINOID, CB1; RECEPTOR, CANNABINOID, CB2;

MUS; RODENTIA;

EID: 79960892570     PISSN: 00913057     EISSN: 18735177     Source Type: Journal    
DOI: 10.1016/j.pbb.2011.06.022     Document Type: Article

References (76)

1. 9-tetrahydrocannabinol: studies on precipitated and abrupt withdrawal J Pharmacol Exp Ther 278 1996 1290 1295 (Pubitemid 27166981)
2. M.D. Aceto, S.M. Scates, and B.B. Martin Spontaneous and precipitated withdrawal with a synthetic cannabinoid, WIN 55212-2 Eur J Pharmacol 416 2001 75 81 (Pubitemid 32244437)
3. N. Agarwal, P. Pacher, I. Tegeder, F. Amaya, C.E. Constantin, and G.J. Brenner Cannabinoids mediate analgesia largely via peripheral type 1 cannabinoid receptors in nociceptors Nat Neurosci 10 2007 870 879 (Pubitemid 47013432)
4. K. Ahn, D.S. Johnson, M. Mileni, D. Beidler, J.Z. Long, and M.K. McKinney Discovery and characterization of a highly selective FAAH inhibitor that reduces inflammatory pain Chem Biol 16 2009 411 420
5. P. Beaulieu, T. Bisogno, S. Punwar, W.P. Farquhar-Smith, G. Ambrosino, and V. Di Marzo Role of the endogenous cannabinoid system in the formalin test of persistent pain in the rat Eur J Pharmacol 396 2000 85 92 (Pubitemid 30265563)
6. S. Bluml, M. Bonelli, B. Niederreiter, A. Puchner, G. Mayr, and S. Hayer Essential role for micro-RNA 155 in the pathogenesis of autoimmune arthritis Arthritis Rheum 2011
7. T. Bongartz, A.J. Sutton, M.J. Sweeting, I. Buchan, E.L. Matteson, and V. Montori Anti-TNF antibody therapy in rheumatoid arthritis and the risk of serious infections and malignancies: systematic review and meta-analysis of rare harmful effects in randomized controlled trials J Am Med Assoc 295 2006 2275 2285 (Pubitemid 43736578)
8. L. Booker, S.G. Kinsey, R.A. Abdullah, J.L. Blankman, J.Z. Long, and C. Ezzili The FAAH inhibitor PF-3845 acts in the nervous system to reverse lipopolysaccharide-induced tactile allodynia in mice Br J Pharmacol 2011
9. A. Calignano, G. La Rana, A. Giuffrida, and D. Piomelli Control of pain initiation by endogenous cannabinoids Nature 394 1998 277 281 (Pubitemid 28335039)
10. I.K. Campbell, M.J. Rich, R.J. Bischof, A.R. Dunn, D. Grail, and J.A. Hamilton Protection from collagen-induced arthritis in granulocyte-macrophage colony-stimulating factor-deficient mice J Immunol 161 1998 3639 3644
11. J.R. Clapper, G. Moreno-Sanz, R. Russo, A. Guijarro, F. Vacondio, and A. Duranti Anandamide suppresses pain initiation through a peripheral endocannabinoid mechanism Nat Neurosci 2010
12. A.F. Coburn, C.E. Graham, and J. Haninger The effect of egg yolk in diets on anaphylactic arthritis (passive Arthus phenomenon) in the guinea pig J Exp Med 100 1954 425 435
13. 9-tetrahydrocannabinol J Pharmacol Exp Ther 263 1992 1118 1126 (Pubitemid 23157189)
14. J.S. Courtenay, M.J. Dallman, A.D. Dayan, A. Martin, and B. Mosedale Immunisation against heterologous type II collagen induces arthritis in mice Nature 283 1980 666 668 (Pubitemid 10099994)
15. B.F. Cravatt, D.K. Giang, S.P. Mayfield, D.L. Boger, R.A. Lerner, and N.B. Gilula Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides Nature 384 1996 83 87 (Pubitemid 26374593)
16. B.F. Cravatt, K. Demarest, M.P. Patricelli, M.H. Bracey, D.K. Giang, and B.R. Martin Supersensitivity to anandamide and enhanced endogenous cannabinoid signaling in mice lacking fatty acid amide hydrolase Proc Natl Acad Sci USA 98 2001 9371 9376 (Pubitemid 32743923)
17. B.F. Cravatt, A. Saghatelian, E.G. Hawkins, A.B. Clement, M.H. Bracey, and A.H. Lichtman Functional disassociation of the central and peripheral fatty acid amide signaling systems Proc Natl Acad Sci USA 101 2004 10821 10826 (Pubitemid 38955826)
18. G. D'Agostino, G. La Rana, R. Russo, O. Sasso, A. Iacono, and E. Esposito Acute intracerebroventricular administration of palmitoylethanolamide, an endogenous peroxisome proliferator-activated receptor-alpha agonist, modulates carrageenan-induced paw edema in mice J Pharmacol Exp Ther 322 2007 1137 1143 (Pubitemid 47295805)
19. G. D'Agostino, G. La Rana, R. Russo, O. Sasso, A. Iacono, and E. Esposito Central administration of palmitoylethanolamide reduces hyperalgesia in mice via inhibition of NF-kappaB nuclear signalling in dorsal root ganglia Eur J Pharmacol 613 2009 54 59
20. W.A. Devane, L. Hanus, A. Breuer, R.G. Pertwee, L.A. Stevenson, and G. Griffin Isolation and structure of a brain constituent that binds to the cannabinoid receptor Sci. 258 1992 1946 1949 (Pubitemid 23026736)
21. V. Di Marzo, and L. De Petrocellis Endocannabinoids as regulators of transient receptor potential (TRP) channels: a further opportunity to develop new endocannabinoid-based therapeutic drugs Curr Med Chem 17 2010 1430 1449
22. A. Dray, and S. Bevan Inflammation and hyperalgesia: highlighting the team effort Trends Pharmacol Sci 14 1993 287 290 (Pubitemid 23242577)
23. M.R. Elphick, and M. Egertova The phylogenetic distribution and evolutionary origins of endocannabinoid signalling Handb Exp Pharmacol 2005 283 297
24. C. Ezzili, M. Mileni, N. McGlinchey, J.Z. Long, S.G. Kinsey, and D.G. Hochstatter Reversible competitive alpha-ketoheterocycle inhibitors of fatty acid amide hydrolase containing additional conformational constraints in the acyl side chain: orally active, long-acting analgesics J Med Chem 54 2011 2805 2822
25. T. Genovese, E. Esposito, E. Mazzon, R. Di Paola, R. Meli, and P. Bramanti Effects of palmitoylethanolamide on signaling pathways implicated in the development of spinal cord injury J Pharmacol Exp Ther 326 2008 12 23 (Pubitemid 351872139)
26. C.M. Gerard, C. Mollereau, G. Vassart, and M. Parmentier Molecular cloning of a human cannabinoid receptor which is also expressed in testis Biochem J 279 Pt 1 1991 129 134
27. G. Gobbi, F.R. Bambico, R. Mangieri, M. Bortolato, P. Campolongo, and M. Solinas Antidepressant-like activity and modulation of brain monoaminergic transmission by blockade of anandamide hydrolysis Proc Natl Acad Sci USA 102 2005 18620 18625 (Pubitemid 43011275)
28. J. Guindon, and A.G. Hohmann Cannabinoid CB2 receptors: a therapeutic target for the treatment of inflammatory and neuropathic pain Br J Pharmacol 153 2008 319 334
29. M. Herkenham, A.B. Lynn, M.R. Johnson, L.S. Melvin, B.R. de Costa, and K.C. Rice Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study J Neurosci 11 1991 563 583
30. A.G. Hohmann, R.L. Suplita, N.M. Bolton, M.H. Neely, D. Fegley, and R. Mangieri An endocannabinoid mechanism for stress-induced analgesia Nature 435 2005 1108 1112 (Pubitemid 40910518)
31. S. Holt, F. Comelli, B. Costa, and C.J. Fowler 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 2005 467 476 (Pubitemid 41486689)
32. G. Horvath, G. Kekesi, E. Nagy, and G. Benedek The role of TRPV1 receptors in the antinociceptive effect of anandamide at spinal level Pain 134 2008 277 284
33. A. Jayamanne, R. Greenwood, V.A. Mitchell, S. Aslan, D. Piomelli, and C.W. Vaughan Actions of the FAAH inhibitor URB597 in neuropathic and inflammatory chronic pain models Br J Pharmacol 147 2006 281 288 (Pubitemid 43214685)
34. Z. Justinova, G. Tanda, G.H. Redhi, and S.R. Goldberg Self-administration of delta9-tetrahydrocannabinol (THC) by drug naive squirrel monkeys Psychopharmacology (Berl) 169 2003 135 140 (Pubitemid 37129964)
35. Z. Justinova, R.A. Mangieri, M. Bortolato, S.I. Chefer, A.G. Mukhin, and J.R. Clapper Fatty acid amide hydrolase inhibition heightens anandamide signaling without producing reinforcing effects in primates Biol Psychiatry 64 2008 930 937
36. M. Karsak, E. Gaffal, R. Date, L. Wang-Eckhardt, J. Rehnelt, and S. Petrosino Attenuation of allergic contact dermatitis through the endocannabinoid system Sci. 316 2007 1494 1497 (Pubitemid 46906619)
37. S.G. Kinsey, J.Z. Long, S.T. O'Neal, R.A. Abdullah, J.L. Poklis, and D.L. Boger Blockade of endocannabinoid-degrading enzymes attenuates neuropathic pain J Pharmacol Exp Ther 330 2009 902 910
38. S.G. Kinsey, J.Z. Long, B.F. Cravatt, and A.H. Lichtman Fatty acid amide hydrolase and monoacylglycerol lipase inhibitors produce anti-allodynic effects in mice through distinct cannabinoid receptor mechanisms J Pain 2010
39. S.G. Kinsey, A. Mahadevan, B. Zhao, H. Sun, P.S. Naidu, and R.K. Razdan The CB(2) cannabinoid receptor-selective agonist O-3223 reduces pain and inflammation without apparent cannabinoid behavioral effects Neuropharmacology 60 2011 244 251
40. S.G. Kinsey, S.T. O'Neal, J.Z. Long, B.F. Cravatt, and A.H. Lichtman Inhibition of endocannabinoid catabolic enzymes elicits anxiolytic-like effects in the marble burying assay Pharmacol Biochem Behav 98 2011 21 27
41. 9-tetrahydrocannabinol: behavioral effects and tolerance development J Pharm Exp Ther 159 1974 61 65
42. D.M. Lee, and M.E. Weinblatt Rheumatoid arthritis Lancet 358 2001 903 911 (Pubitemid 32900579)
43. A.H. Lichtman, S.A. Cook, and B.R. Martin Investigation of brain sites mediating cannabinoid -induced antinociception in rats: evidence supporting periaqueductal gray involvement J Pharmacol Exp Ther 276 1996 585 593
44. A.H. Lichtman, C.C. Shelton, T. Advani, and B.F. Cravatt Mice lacking fatty acid amide hydrolase exhibit a cannabinoid receptor-mediated phenotypic hypoalgesia Pain 109 2004 319 327 (Pubitemid 38638709)
45. A.H. Lichtman, D. Leung, C. Shelton, A. Saghatelian, C. Hardouin, and D. Boger Reversible inhibitors of fatty acid amide hydrolase that promote analgesia: evidence for an unprecedented combination of potency and selectivity J Pharmacol Exp Ther 2004
46. J. Lo Verme, J. Fu, G. Astarita, G. La Rana, R. Russo, and A. Calignano The nuclear receptor PPAR-{alpha} mediates the antiinflammatory actions of palmitoylethanolamide Mol Pharmacol 2004
47. J. Lo Verme, J. Fu, G. Astarita, G. La Rana, R. Russo, and A. Calignano The nuclear receptor peroxisome proliferator-activated receptor-alpha mediates the anti-inflammatory actions of palmitoylethanolamide Mol Pharmacol 67 2005 15 19 (Pubitemid 40069962)
48. J. LoVerme, R. Russo, G. La Rana, J. Fu, J. Farthing, and G. Mattace-Raso Rapid broad-spectrum analgesia through activation of peroxisome proliferator-activated receptor-alpha J Pharmacol Exp Ther 319 2006 1051 1061
49. A.M. Malfait, R. Gallily, P.F. Sumariwalla, A.S. Malik, E. Andreakos, and R. Mechoulam The nonpsychoactive cannabis constituent cannabidiol is an oral anti-arthritic therapeutic in murine collagen-induced arthritis Proc Natl Acad Sci USA 97 2000 9561 9566 (Pubitemid 30650815)
50. W.J. Martin, S.L. Patrick, P.O. Coffin, K. Tsou, and J.M. Walker An examination of the central sites of action of cannabinoid-induced antinociception in the rat Life Sci 56 1995 2103 2109
51. F. Massa, G. Marsicano, H. Hermann, A. Cannich, K. Monory, and B.F. Cravatt The endogenous cannabinoid system protects against colonic inflammation J Clin Invest 113 2004 1202 1209 (Pubitemid 38544105)
52. L.A. Matsuda, S.J. Lolait, M.J. Brownstein, A.C. Young, and T.I. Bonner Structure of a cannabinoid receptor and functional expression of the cloned cDNA Nature 346 1990 561 564
53. S. Maurelli, T. Bisogno, L. De Petrocellis, A. Di Luccia, G. Marino, and V. Di Marzo Two novel classes of neuroactive fatty acid amides are substrates for mouse neuroblastoma 'anandamide amidohydrolase' FEBS Lett 377 1995 82 86 (Pubitemid 26009779)
54. R. Mechoulam, S. Ben-Shabat, L. Hanus, M. Ligumsky, N. Kaminski, and A. Schatz Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors Biochem Pharmacol 50 1995 83 90
55. I.D. Meng, B.H. Manning, W.J. Martin, and H.L. Fields An analgesia circuit activated by cannabinoids Nature 395 1998 381 383 (Pubitemid 28450687)
56. A.R. Moore Collagen-induced arthritis Methods Mol Biol 225 2003 175 179
57. P.S. Naidu, L. Booker, B.F. Cravatt, and A.H. Lichtman Synergy between enzyme inhibitors of fatty acid amide hydrolase and cyclooxygenase in visceral nociception J Pharmacol Exp Ther 329 2009 48 56
58. P.S. Naidu, S.G. Kinsey, T.L. Guo, B.F. Cravatt, and A.H. Lichtman Regulation of inflammatory pain by inhibition of fatty acid amide hydrolase J Pharmacol Exp Ther 334 2010 182 190
59. E.J. Rahn, and A.G. Hohmann Cannabinoids as pharmacotherapies for neuropathic pain: from the bench to the bedside Neurotherapeutics 6 2009 713 737
60. J.R. Reynolds On the therapeutical uses and toxic effects of Cannabis indica Lancet 22 1890 637 638 March
61. J.D. Richardson, L. Aanonsen, and K.M. Hargreaves SR 141716A, a cannabinoid receptor antagonist, produces hyperalgesia in untreated mice Eur J Pharmacol 319 1997 R3 R4
62. D. Richardson, R.G. Pearson, N. Kurian, M.L. Latif, M.J. Garle, and D.A. Barrett Characterisation of the cannabinoid receptor system in synovial tissue and fluid in patients with osteoarthritis and rheumatoid arthritis Arthritis Res Ther 10 2008 R43
63. R. Russo, J. Loverme, G. La Rana, T.R. Compton, J. Parrott, and A. Duranti 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 2007 236 242 (Pubitemid 46956375)
64. A. Saghatelian, M.K. McKinney, M. Bandell, A. Patapoutian, and B.F. Cravatt A FAAH-regulated class of N-acyl taurines that activates TRP ion channels Biochemistry 45 2006 9007 9015 (Pubitemid 44156362)
65. M. Scherma, L.V. Panlilio, P. Fadda, L. Fattore, I. Gamaleddin, and B. Le Foll Inhibition of anandamide hydrolysis by cyclohexyl carbamic acid 3′-carbamoyl-3-yl ester (URB597) reverses abuse-related behavioral and neurochemical effects of nicotine in rats J Pharmacol Exp Ther 327 2008 482 490
66. J.E. Schlosburg, B.L. Carlson, D. Ramesh, R.A. Abdullah, J.Z. Long, and B.F. Cravatt Inhibitors of endocannabinoid-metabolizing enzymes reduce precipitated withdrawal responses in THC-dependent mice AAPS J 11 2009 342 352
67. J.E. Schlosburg, S.G. Kinsey, and A.H. Lichtman Targeting fatty acid amide hydrolase (FAAH) to treat pain and inflammation AAPS J 2009
68. R.D. Sofia, S.D. Nalepa, J.J. Harakal, and H.B. Vassar Anti-edema and analgesic properties of delta9-tetrahydrocannabinol (THC) J Pharmacol Exp Ther 186 1973 646 655
69. T. Sugiura, S. Kondo, A. Sukagawa, S. Nakane, A. Shinoda, and K. Itoh 2-Arachidonoyglycerol: a possible endogenous cannabinoid receptor ligand in brain Biochem Biophys Res Comm 215 1995 89 97
70. G. Tanda, P. Munzar, and S.R. Goldberg Self-administration behavior is maintained by the psychoactive ingredient of marijuana in squirrel monkeys Nat Neurosci 3 2000 1073 1074
71. D.E. Trentham Collagen arthritis as a relevant model for rheumatoid arthritis Arthritis Rheum 25 1982 911 916 (Pubitemid 12047017)
72. 9-tetrahydrocannabinol precipated by a cannabinoid receptor antagonist Eur J Pharmacol 280 1995 R13 R15
73. N. Ueda, Y. Kurahashi, S. Yamamoto, and T. Tokunaga Partial purifaction and characterization of the porcine brain enzyme hydrolyzing and synthesizing anandamide J Biol Chem 270 1995 23823 23827
74. R.O. Williams Rodent models of arthritis: relevance for human disease Clin Exp Immunol 114 1998 330 332 (Pubitemid 28539589)
75. L.E. Wise, R. Cannavacciulo, B.F. Cravatt, B.F. Martin, and A.H. Lichtman Evaluation of fatty acid amides in the carrageenan-induced paw edema model Neuropharmacology 54 2008 181 188 (Pubitemid 350299403)
76. T.L. Yaksh The antinociceptive effects of intrathecally-administered levonantradol and desacetyllevonantradol in the rat J Clin Pharmacol 21 1981 3345 3405