Activation of CB2 receptor is required for the therapeutic effect of ABHD6 inhibition in experimental autoimmune encephalomyelitis

Neuropharmacology

Volumn 99, Issue , 2015, Pages 196-209

  Wen, Jie ^a   Ribeiro, Rachel ^a   Tanaka, Mikiei ^a   Zhang, Yumin ^a  

^a UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

Author keywords

2 Arachidonoylglycerol; ABHD6; Cannabinoid receptors; Demyelination; Inflammation; Microglia

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N MORPHOLINO 1H PYRAZOLE 3 CARBOXAMIDE; 6 IODO 3 (4 METHOXYBENZOYL) 2 METHYL 1 (2 MORPHOLINOETHYL)INDOLE; ACTIVATED LEUKOCYTE CELL ADHESION MOLECULE; ALPHA BETA HYDROLASE DOMAIN 6; CANNABINOID 2 RECEPTOR; CYCLOOXYGENASE 2; ENZYME INHIBITOR; HYDROLASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; WWL 70; ABHD6 PROTEIN, MOUSE; ACYLGLYCEROL LIPASE; ANTIINFLAMMATORY AGENT; BIPHENYL DERIVATIVE; CANNABINOID 1 RECEPTOR; CARBAMIC ACID DERIVATIVE; CNR1 PROTEIN, MOUSE; CNR2 PROTEIN, MOUSE; N-METHYL-N-((3-(4-PYRIDINYL)PHENYL)METHYL)-4'-(AMINOCARBONYL)(1,1'-BIPHENYL)-4-YL ESTER, CARBAMIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL ACTIVATION; CELL LOSS; CELL SURVIVAL; CONTROLLED STUDY; DEMYELINATION; ENZYME INHIBITION; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FEMALE; LYMPHOCYTIC INFILTRATION; MACROPHAGE; MICROGLIA; MOUSE; NERVE FIBER; NEUROPROTECTION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; SPINAL CORD; T LYMPHOCYTE; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; DRUG EFFECTS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; ENZYMOLOGY; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; MYELIN SHEATH; PATHOLOGY;

ANIMALS; ANTI-INFLAMMATORY AGENTS; BIPHENYL COMPOUNDS; CARBAMATES; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; ENZYME INHIBITORS; FEMALE; MACROPHAGES; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROGLIA; MONOACYLGLYCEROL LIPASES; MYELIN SHEATH; OLIGODENDROGLIA; RECEPTOR, CANNABINOID, CB1; RECEPTOR, CANNABINOID, CB2; SPINAL CORD;

EID: 84938241935     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2015.07.010     Document Type: Article

References (70)

1. M. Alhouayek, J. Masquelier, P.D. Cani, D.M. Lambert, and G.G. Muccioli Implication of the anti-inflammatory bioactive lipid prostaglandin D2-glycerol ester in the control of macrophage activation and inflammation by ABHD6 Proc. Natl. Acad. Sci. U. S. A. 110 2013 17558 17563
2. A. Arevalo-Martin, D. Garcia-Ovejero, O. Gomez, A. Rubio-Araiz, B. Navarro-Galve, C. Guaza, E. Molina-Holgado, and F. Molina-Holgado CB2 cannabinoid receptors as an emerging target for demyelinating diseases: from neuroimmune interactions to cell replacement strategies Br. J. Pharmacol. 153 2008 216 225
3. J.L. Berard, B.J. Kerr, H.M. Johnson, and S. David Differential expression of SOCS1 in macrophages in relapsing-remitting and chronic EAE and its role in disease severity Glia 58 2010 1816 1826
4. J.L. Berard, K. Wolak, S. Fournier, and S. David Characterization of relapsing-remitting and chronic forms of experimental autoimmune encephalomyelitis in C57BL/6 mice Glia 58 2010 434 445
5. M. Bhasin, M. Wu, and S.E. Tsirka Modulation of microglial/macrophage activation by macrophage inhibitory factor (TKP) or tuftsin (TKPR) attenuates the disease course of experimental autoimmune encephalomyelitis BMC Immunol. 8 2007 10
6. J.L. Blankman, and B.F. Cravatt Chemical probes of endocannabinoid metabolism Pharmacol. Rev. 65 2013 849 871
7. J.L. Blankman, G.M. Simon, and B.F. Cravatt A comprehensive profile of brain enzymes that hydrolyze the endocannabinoid 2-arachidonoylglycerol Chem. Biol. 14 2007 1347 1356
8. M.A. Bowen, D.D. Patel, X. Li, B. Modrell, A.R. Malacko, W.C. Wang, H. Marquardt, M. Neubauer, J.M. Pesando, U. Francke, and et al. Cloning, mapping, and characterization of activated leukocyte-cell adhesion molecule (ALCAM), a CD6 ligand J. Exp. Med. 181 1995 2213 2220
9. G.A. Cabral, E.S. Raborn, L. Griffin, J. Dennis, and F. Marciano-Cabral CB2 receptors in the brain: role in central immune function Br. J. Pharmacol. 153 2008 240 251
10. E.J. Carrier, C.S. Kearn, A.J. Barkmeier, N.M. Breese, W. Yang, K. Nithipatikom, S.L. Pfister, W.B. Campbell, and C.J. Hillard Cultured rat microglial cells synthesize the endocannabinoid 2-arachidonylglycerol, which increases proliferation via a CB2 receptor-dependent mechanism Mol. Pharmacol. 65 2004 999 1007
11. E.J. Carrier, S. Patel, and C.J. Hillard Endocannabinoids in neuroimmunology and stress Curr. Drug Targets CNS Neurol. Disord. 4 2005 657 665
12. B.D. Carter, C. Kaltschmidt, B. Kaltschmidt, N. Offenhauser, R. Bohm-Matthaei, P.A. Baeuerle, and Y.A. Barde Selective activation of NF-kappa B by nerve growth factor through the neurotrophin receptor p75 Science 272 1996 542 545
13. R. Cayrol, K. Wosik, J.L. Berard, A. Dodelet-Devillers, I. Ifergan, H. Kebir, A.S. Haqqani, K. Kreymborg, S. Krug, R. Moumdjian, A. Bouthillier, B. Becher, N. Arbour, S. David, D. Stanimirovic, and A. Prat Activated leukocyte cell adhesion molecule promotes leukocyte trafficking into the central nervous system Nat. Immunol. 9 2008 137 145
14. D. Centonze, M. Bari, S. Rossi, C. Prosperetti, R. Furlan, F. Fezza, V. De Chiara, L. Battistini, G. Bernardi, S. Bernardini, G. Martino, and M. Maccarrone The endocannabinoid system is dysregulated in multiple sclerosis and in experimental autoimmune encephalomyelitis Brain 130 2007 2543 2553
15. D. Centonze, A. Finazzi-Agro, G. Bernardi, and M. Maccarrone The endocannabinoid system in targeting inflammatory neurodegenerative diseases Trends Pharmacol. Sci. 28 2007 180 187
16. P.K. Chanda, Y. Gao, L. Mark, J. Btesh, B.W. Strassle, P. Lu, M.J. Piesla, M.Y. Zhang, B. Bingham, A. Uveges, D. Kowal, D. Garbe, E.V. Kouranova, R.H. Ring, B. Bates, M.N. Pangalos, J.D. Kennedy, G.T. Whiteside, and T.A. Samad Monoacylglycerol lipase activity is a critical modulator of the tone and integrity of the endocannabinoid system Mol. Pharmacol. 78 2010 996 1003
17. R. Chen, J. Zhang, Y. Wu, D. Wang, G. Feng, Y.P. Tang, Z. Teng, and C. Chen Monoacylglycerol lipase is a therapeutic target for Alzheimer's disease Cell Rep. 2 2012 1329 1339
18. B.F. Cravatt, A.T. Wright, and J.W. Kozarich Activity-based protein profiling: from enzyme chemistry to proteomic chemistry Annu. Rev. Biochem. 77 2008 383 414
19. C.J. De Groot, S.R. Ruuls, J.W. Theeuwes, C.D. Dijkstra, and P. Van der Valk Immunocytochemical characterization of the expression of inducible and constitutive isoforms of nitric oxide synthase in demyelinating multiple sclerosis lesions J. Neuropathol. Exp. Neurol. 56 1997 10 20
20. E. de Lago, M. Moreno-Martet, A. Cabranes, J.A. Ramos, and J. Fernandez-Ruiz Cannabinoids ameliorate disease progression in a model of multiple sclerosis in mice, acting preferentially through CB1 receptor-mediated anti-inflammatory effects Neuropharmacology 62 2012 2299 2308
21. A. Dhopeshwarkar, and K. Mackie CB2 Cannabinoid receptors as a therapeutic target-what does the future hold? Mol. Pharmacol. 86 2014 430 437
22. F. Docagne, L. Mestre, F. Loria, M. Hernangomez, F. Correa, and C. Guaza Therapeutic potential of CB2 targeting in multiple sclerosis Expert Opin. Ther. Targets 12 2008 185 195
23. B. Engelhardt Regulation of immune cell entry into the central nervous system Results Probl. Cell Differ. 43 2006 259 280
24. Y. Esaki, Y. Li, D. Sakata, C. Yao, E. Segi-Nishida, T. Matsuoka, K. Fukuda, and S. Narumiya Dual roles of PGE2-EP4 signaling in mouse experimental autoimmune encephalomyelitis Proc. Natl. Acad. Sci. U. S. A. 107 2010 12233 12238
25. R. Gallily, A. Breuer, and R. Mechoulam 2-Arachidonylglycerol, an endogenous cannabinoid, inhibits tumor necrosis factor-alpha production in murine macrophages, and in mice Eur. J. Pharmacol. 406 2000 R5 R7
26. A. Gentile, S. Rossi, V. Studer, C. Motta, V. De Chiara, A. Musella, H. Sepman, D. Fresegna, G. Musumeci, G. Grasselli, N. Haji, S. Weiss, L. Hayardeny, G. Mandolesi, and D. Centonze Glatiramer acetate protects against inflammatory synaptopathy in experimental autoimmune encephalomyelitis J. Neuroimmune Pharmacol. 8 2013 651 663
27. I. Gimferrer, M. Calvo, M. Mittelbrunn, M. Farnos, M.R. Sarrias, C. Enrich, J. Vives, F. Sanchez-Madrid, and F. Lozano Relevance of CD6-mediated interactions in T cell activation and proliferation J. Immunol. 173 2004 2262 2270
28. J.P. Gong, E.S. Onaivi, H. Ishiguro, Q.R. Liu, P.A. Tagliaferro, A. Brusco, and G.R. Uhl Cannabinoid CB2 receptors: immunohistochemical localization in rat brain Brain Res. 1071 2006 10 23
29. J. Guindon, Y. Lai, S.M. Takacs, H.B. Bradshaw, and A.G. Hohmann Alterations in endocannabinoid tone following chemotherapy-induced peripheral neuropathy: effects of endocannabinoid deactivation inhibitors targeting fatty-acid amide hydrolase and monoacylglycerol lipase in comparison to reference analgesics following cisplatin treatment Pharmacol. Res. 67 2013 94 109
30. K.L. Hsu, K. Tsuboi, J.W. Chang, L.R. Whitby, A.E. Speers, H. Pugh, and B.F. Cravatt Discovery and optimization of piperidyl-1,2,3-triazole ureas as potent, selective, and in vivo-active inhibitors of alpha/beta-hydrolase domain containing 6 (ABHD6) J. Med. Chem. 56 2013 8270 8279
31. J. Hwang, C. Adamson, D. Butler, D.R. Janero, A. Makriyannis, and B.A. Bahr Enhancement of endocannabinoid signaling by fatty acid amide hydrolase inhibition: a neuroprotective therapeutic modality Life Sci. 86 2010 615 623
32. P.S. Katz, J.K. Sulzer, R.A. Impastato, S.X. Teng, E.K. Rogers, and P.E. Molina Endocannabinoid degradation inhibition improves neurobehavioral function, blood-brain barrier integrity, and neuroinflammation following mild traumatic brain injury J. Neurotrauma 32 2015 297 306
33. H. Kebir, K. Kreymborg, I. Ifergan, A. Dodelet-Devillers, R. Cayrol, M. Bernard, F. Giuliani, N. Arbour, B. Becher, and A. Prat Human TH17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation Nat. Med. 13 2007 1173 1175
34. S.G. Kinsey, L.E. Wise, D. Ramesh, R. Abdullah, D.E. Selley, B.F. Cravatt, and A.H. Lichtman 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 2013 492 501
35. W. Kong, H. Li, R.F. Tuma, and D. Ganea Selective CB2 receptor activation ameliorates EAE by reducing Th17 differentiation and immune cell accumulation in the CNS Cell Immunol. 287 2014 1 17
36. I. Kubajewska, and C.S. Constantinescu Cannabinoids and experimental models of multiple sclerosis Immunobiology 215 2010 647 657
37. A. Lourbopoulos, N. Grigoriadis, R. Lagoudaki, O. Touloumi, E. Polyzoidou, I. Mavromatis, N. Tascos, A. Breuer, H. Ovadia, D. Karussis, E. Shohami, R. Mechoulam, and C. Simeonidou Administration of 2-arachidonoylglycerol ameliorates both acute and chronic experimental autoimmune encephalomyelitis Brain Res. 1390 2011 126 141
38. C. Lucchinetti, W. Bruck, J. Parisi, B. Scheithauer, M. Rodriguez, and H. Lassmann Heterogeneity of multiple sclerosis lesions: implications for the pathogenesis of demyelination Ann. Neurol. 47 2000 707 717
39. K. Mackie Cannabinoid receptors: where they are and what they do J. Neuroendocrinol. 20 Suppl. 1 2008 10 14
40. K. Maresz, E.J. Carrier, E.D. Ponomarev, C.J. Hillard, and B.N. Dittel Modulation of the cannabinoid CB2 receptor in microglial cells in response to inflammatory stimuli J. Neurochem. 95 2005 437 445
41. K. Maresz, G. Pryce, E.D. Ponomarev, G. Marsicano, J.L. Croxford, L.P. Shriver, C. Ledent, X. Cheng, E.J. Carrier, M.K. Mann, G. Giovannoni, R.G. Pertwee, T. Yamamura, N.E. Buckley, C.J. Hillard, B. Lutz, D. Baker, and B.N. Dittel Direct suppression of CNS autoimmune inflammation via the cannabinoid receptor CB1 on neurons and CB2 on autoreactive T cells Nat. Med. 13 2007 492 497
42. W.R. Marrs, J.L. Blankman, E.A. Horne, A. Thomazeau, Y.H. Lin, J. Coy, A.L. Bodor, G.G. Muccioli, S.S. Hu, G. Woodruff, S. Fung, M. Lafourcade, J.P. Alexander, J.Z. Long, W. Li, C. Xu, T. Moller, K. Mackie, O.J. Manzoni, B.F. Cravatt, and N. Stella The serine hydrolase ABHD6 controls the accumulation and efficacy of 2-AG at cannabinoid receptors Nat. Neurosci. 13 2010 951 957
43. P.N. Moynagh, D.C. Williams, and L.A. O'Neill Interleukin-1 activates transcription factor NF kappa B in glial cells Biochem. J. 294 Pt 2 1993 343 347
44. N. Murataeva, A. Straiker, and K. Mackie Parsing the players: 2-arachidonoylglycerol synthesis and degradation in the CNS Br. J. Pharmacol. 171 2014 1379 1391
45. A.V. Naydenov, E.A. Horne, C.S. Cheah, K. Swinney, K.L. Hsu, J.K. Cao, W.R. Marrs, J.L. Blankman, S. Tu, A.E. Cherry, S. Fung, A. Wen, W. Li, M.S. Saporito, D.E. Selley, B.F. Cravatt, J.C. Oakley, and N. Stella ABHD6 blockade exerts antiepileptic activity in PTZ-induced seizures and in spontaneous seizures in R6/2 mice Neuron 83 2014 361 371
46. D.K. Nomura, B.E. Morrison, J.L. Blankman, J.Z. Long, S.G. Kinsey, M.C. Marcondes, A.M. Ward, Y.K. Hahn, A.H. Lichtman, B. Conti, and B.F. Cravatt Endocannabinoid hydrolysis generates brain prostaglandins that promote neuroinflammation Science 334 2011 809 813
47. J.H. Noseworthy, C. Lucchinetti, M. Rodriguez, and B.G. Weinshenker Multiple sclerosis N. Engl. J. Med. 343 2000 938 952
48. J. Palazuelos, N. Davoust, B. Julien, E. Hatterer, T. Aguado, R. Mechoulam, C. Benito, J. Romero, A. Silva, M. Guzman, S. Nataf, and I. Galve-Roperh The CB(2) cannabinoid receptor controls myeloid progenitor trafficking: involvement in the pathogenesis of an animal model of multiple sclerosis J. Biol. Chem. 283 2008 13320 13329
49. D. Panikashvili, C. Simeonidou, S. Ben-Shabat, L. Hanus, A. Breuer, R. Mechoulam, and E. Shohami An endogenous cannabinoid (2-AG) is neuroprotective after brain injury Nature 413 2001 527 531
50. R.G. Pertwee Elevating endocannabinoid levels: pharmacological strategies and potential therapeutic applications Proc. Nutr. Soc. 73 2014 96 105
51. J.R. Piro, D.I. Benjamin, J.M. Duerr, Y. Pi, C. Gonzales, K.M. Wood, J.W. Schwartz, D.K. Nomura, and T.A. Samad A dysregulated endocannabinoid-eicosanoid network supports pathogenesis in a mouse model of Alzheimer's disease Cell Rep. 1 2012 617 623
52. D. Pitt, P. Werner, and C.S. Raine Glutamate excitotoxicity in a model of multiple sclerosis Nat. Med. 6 2000 67 70
53. G. Pryce, and D. Baker Control of spasticity in a multiple sclerosis model is mediated by CB1, not CB2, cannabinoid receptors Br. J. Pharmacol. 150 2007 519 525
54. R. Ribeiro, F. Yu, J. Wen, A. Vana, and Y. Zhang Therapeutic potential of a novel cannabinoid agent CB52 in the mouse model of experimental autoimmune encephalomyelitis Neuroscience 254 2013 427 442
55. S. Rom, and Y. Persidsky Cannabinoid receptor 2: potential role in immunomodulation and neuroinflammation J. Neuroimmune Pharmacol. 8 2013 608 620
56. J.R. Savinainen, S.M. Saario, and J.T. Laitinen The serine hydrolases MAGL, ABHD6 and ABHD12 as guardians of 2-arachidonoylglycerol signalling through cannabinoid receptors Acta Physiol. (Oxf.) 204 2012 267 276
57. J.E. Schlosburg, J.L. Blankman, J.Z. Long, D.K. Nomura, B. Pan, S.G. Kinsey, P.T. Nguyen, D. Ramesh, L. Booker, J.J. Burston, E.A. Thomas, D.E. Selley, L.J. Sim-Selley, Q.S. Liu, A.H. Lichtman, and B.F. Cravatt Chronic monoacylglycerol lipase blockade causes functional antagonism of the endocannabinoid system Nat. Neurosci. 13 2010 1113 1119
58. N.R. Sciolino, W. Zhou, and A.G. Hohmann 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 2011 226 234
59. E. Sigel, R. Baur, I. Racz, J. Marazzi, T.G. Smart, A. Zimmer, and J. Gertsch The major central endocannabinoid directly acts at GABA(A) receptors Proc. Natl. Acad. Sci. U. S. A. 108 2011 18150 18155
60. S.M. Sparacio, Y. Zhang, J. Vilcek, and E.N. Benveniste Cytokine regulation of interleukin-6 gene expression in astrocytes involves activation of an NF-kappa B-like nuclear protein J. Neuroimmunol. 39 1992 231 242
61. M.L. Spencer, M. Theodosiou, and D.J. Noonan NPDC-1, a novel regulator of neuronal proliferation, is degraded by the ubiquitin/proteasome system through a PEST degradation motif J. Biol. Chem. 279 2004 37069 37078
62. S.C. Starossom, I.D. Mascanfroni, J. Imitola, L. Cao, K. Raddassi, S.F. Hernandez, R. Bassil, D.O. Croci, J.P. Cerliani, D. Delacour, Y. Wang, W. Elyaman, S.J. Khoury, and G.A. Rabinovich Galectin-1 deactivates classically activated microglia and protects from inflammation-induced neurodegeneration Immunity 37 2012 249 263
63. F. Tchantchou, and Y. Zhang Selective inhibition of alpha/beta-hydrolase domain 6 attenuates neurodegeneration, alleviates blood brain barrier breakdown, and improves functional recovery in a mouse model of traumatic brain injury J. Neurotrauma 30 2013 565 579
64. E.H. Tran, K. Hoekstra, N. van Rooijen, C.D. Dijkstra, and T. Owens Immune invasion of the central nervous system parenchyma and experimental allergic encephalomyelitis, but not leukocyte extravasation from blood, are prevented in macrophage-depleted mice J. Immunol. 161 1998 3767 3775
65. N. Ueda, K. Tsuboi, T. Uyama, and T. Ohnishi Biosynthesis and degradation of the endocannabinoid 2-arachidonoylglycerol Biofactors 37 2011 1 7
66. A.C. Vana, S. Li, R. Ribeiro, F. Tchantchou, and Y. Zhang Arachidonyl trifluoromethyl ketone ameliorates experimental autoimmune encephalomyelitis via blocking peroxynitrite formation in mouse spinal cord white matter Exp. Neurol. 231 2011 45 55
67. A. Witting, L. Chen, E. Cudaback, A. Straiker, L. Walter, B. Rickman, T. Moller, C. Brosnan, and N. Stella Experimental autoimmune encephalomyelitis disrupts endocannabinoid-mediated neuroprotection Proc. Natl. Acad. Sci. U. S. A. 103 2006 6362 6367
68. W.F. Wu, X.J. Tan, Y.B. Dai, V. Krishnan, M. Warner, and J.A. Gustafsson Targeting estrogen receptor beta in microglia and T cells to treat experimental autoimmune encephalomyelitis Proc. Natl. Acad. Sci. U. S. A. 110 2013 3543 3548
69. M.Y. Zhang, Y. Gao, J. Btesh, N. Kagan, E. Kerns, T.A. Samad, and P.K. Chanda Simultaneous determination of 2-arachidonoylglycerol, 1-arachidonoylglycerol and arachidonic acid in mouse brain tissue using liquid chromatography/tandem mass spectrometry J. Mass Spectrom. 45 2010 167 177
70. J. Zhang, Z. Teng, Y. Song, M. Hu, and C. Chen Inhibition of monoacylglycerol lipase prevents chronic traumatic encephalopathy-like neuropathology in a mouse model of repetitive mild closed head injury J. Cereb. Blood Flow. Metab. 35 2015 443 453