A role for CB2 receptors in anandamide signalling pathways involved in the regulation of IL-12 and IL-23 in microglial cells

Biochemical Pharmacology

Volumn 77, Issue 1, 2009, Pages 86-100

  Correa, Fernando ^a   Docagne, Fabian ^a   Mestre, Leyre ^a   Clemente, Diego ^a   Hernangómez, Miriam ^a   Loría, Frida ^a   Guaza, Carmen ^a  

^a INSTITUTO CAJAL   (Spain)

Author keywords

CB2 receptors; Endocannabinoids; IL 12 IL 23; Microglia; Signalling pathways

Indexed keywords

ANANDAMIDE; CANNABINOID 2 RECEPTOR; INTERLEUKIN 12P70; INTERLEUKIN 23; JANUS KINASE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME INHIBITION; HUMAN; HUMAN CELL; MICROGLIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ANIMALS; ARACHIDONIC ACIDS; CANNABINOIDS; CELLS, CULTURED; FETUS; HUMANS; INTERLEUKIN-12; INTERLEUKIN-23; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED BALB C; MICROGLIA; POLYUNSATURATED ALKAMIDES; RECEPTOR, CANNABINOID, CB2; SIGNAL TRANSDUCTION;

EID: 56649092813     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2008.09.014     Document Type: Article

References (53)

1. Trinchieri G. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat Rev Immunol 3 (2003) 133-146
2. Belladonna M.L., Renaud J.C., Bianchi R., Vacca C., Fallarino F., and Orabona C. IL-23 and IL-12 have overlapping, but distinct, effects on murine dendritic cells. J Immunol 168 (2002) 5699-5708
3. Oppmann B., Lesley R., Blom B., Timans J.C., Xu Y., and Hunte B. Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 13 (2000) 715-725
4. Chen Y., Langrish C.L., McKenzie B., Joyce-Shaikh B., Stumhofer J.S., McClanahan T., et al. Anti-IL-23 therapy inhibits multiple inflammatory pathways and ameliorates autoimmune encephalomyelitis. J Clin Invest 116 (2006) 1317-1326 2006
5. Cua D.J., Sherlock J., Chen Y., Murphy C.A., Joyce B., Seymour B., et al. Interleukin-23 rather that interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 421 (2003) 744-748
6. Hanisch U., and Kettenmann H. Microglia: active sensor and versatile effector cells in the normal and pathological brain. Nat Neurosci 10 (2007) 1387-1394
7. Benito C., Romero J.P., Tolón R.M., Clemente D., Docagne F., Hillard C.J., et al. Cannabinoid CB1 and CB2 receptors and fatty acid amide hydrolase are specific markers of plaque cell subtypes in human multiple sclerosis. J Neurosci 27 (2007) 2396-2402
8. Cabral G.A., and Marciano-Cabral F. Cannabinoid receptors in microglia of the central nervous system: immune functional relevance. J Leukoc Biol 78 (2005) 1192-1197
9. Carlisle S.J., Marciano-Cabral F., Staab A., Ludwick C., and Cabral G.A. Differential expression of the CB2 cannabinoid receptor by rodent macrophages and macrophage-like cells in relation to cell activation. Int Inmunopharmacol 2 (2002) 69-82
10. Maresz K., Carrier E.J., Ponomarev E.D., Hillard C.J., and Dittel B.N. Modulation of the cannabinoid CB2 receptor in microglial cells in response to inflammatory stimuli. J Neurochem 95 (2005) 437-445
11. Walter L., Franklin A., Witting A., Wade C., Xie Y., Kunos G., et al. Non-psychotropic cannabinoid receptors regulate microglia cell migration. J Neurosci 23 (2003) 1398-1405
12. Eljaschewitsch E., Witting A., Mawrin C., Lee T., Schmidt P.M., Wolf S., et al. The endocannabinoid anandamide protects neurons during CNS inflammation by induction of MKP-1 in microglial cells. Neuron 49 (2006) 67-79
13. Arévalo-Martín A., García-Ovejero D., Gómez O., Rubio-Araiz A., Navarro-Galve B., Guaza C., et al. CB2 cannabinoid receptors as an emerging target for demyelinating diseases: from neuroimmune interactions to cell replacement strategies. Br J Pharmacol 153 (2008) 216-225
14. Lambert D.M., and Fowler C.J. The endocannabinoid system: drug targets, lead compounds and potential therapeutic applications. J Med Chem 48 (2005) 5059-5087
15. Arévalo-Martín A., Vela J.M., Molina-Holgado E., Borrell J., and Guaza C. Therapeutic action of cannabinoids in a murine model of multiple sclerosis. J Neurosci 23 (2003) 2511-2516
16. Croxford J.L., and Miller S.D. Immunoregulation of a viral model of multiple sclerosis using the synthetic cannabinoid R+WIN55,212. J Clin Invest 111 (2003) 1231-1240
17. Baker D., Pryce G., Croxford J.L., Brown P., Pertwee R.G., Makriyannis A., et al. Endocannabinoids control spasticity in a multiple sclerosis model. FASEB J 15 (2001) 300-302
18. Cabranes A., Venderoka K., de Lago E., Fezza F., Sanchez A., Mestre L., et al. Decreased endocannabinoid levels in the brain and beneficial effects of agents activating cannabinoid and/or vanilloid receptors in a rat model of multiple sclerosis. Neurobiol Dis 20 (2005) 207-217
19. Ligresti A., Cascio M.G., Pryce G., Kulasegram S., Beletskaya I., De Petrocellis L., et al. New potent and selective inhibitors of anandamide reuptake with antispastic activity in a mouse model of multiple sclerosis. Br J Pharmacol 147 (2006) 83-91
20. Mestre L., Correa F., Arévalo-Martín A., Molina-Holgado E., Valenti M., Ortar G., et al. Pharmacological modulation of the endocannabinoid system in a viral model of multiple sclerosis. J Neurochem 92 (2005) 1327-1339
21. Ortega-Gutiérrez S., Molina-Holgado E., Arévalo-Martín A., Correa F., Viso A., López-Rodríguez M.L., et al. Activation of the endocannabinoid system as therapeutic approach in a murine model of multiple sclerosis. FASEB J 19 (2005) 1338-1340
22. Carrier E.J., Kearn C.S., Barkmeier A.J., Breese N.M., YangW, Nithipatikom K., et al. Cultured rat microglial cells synthesize the endocannabinoid 2-arachidonylglycerol, which increases proliferation via a CB2 receptor-dependent mechanism. Mol Pharmacol 65 (2004) 999-1007
23. Correa F., Mestre L., Docagne F., and Guaza C. Activation of cannabinoid CB2 receptor negatively regulates IL-12p40 synthesis in murine macrophages: role of IL-10 and ERK1/2 kinase signaling. Br J Pharmacol 145 (2005) 441-448
24. Puffenbarger R.A., Boothe A.C., and Cabral G.A. Cannabinoids inhibit LPS-inducible cytokine mRNA expression in rat microglial cells. Glia 29 (2000) 58-69
25. Lipton H.L., and Dal Canto M.C. Chronic neurologic disease in Theiler's virus infection of SJL/J mice. J Neurol Sci 30 1 (1976) 201-207
26. Correa F., Docagne F., Clemente D., Mestre L., Becker C., and Guaza C. Anandamide inhibits IL-12p40 production by acting on the promoter repressor element GA-12: possible involvement of the COX-2 metabolite prostamide E(2). Biochem J 409 (2008) 761-770
27. Li Y., Chu N., Hu A., Gran B., Rostami A., and Zhang G. Increased IL-23 p19 expression in multiple sclerosis lesions and its induction in microglia. Brain 130 (2007) 490-501
28. Dong C., Davis R.J., and Flavell R.A. MAP kinases in the immune response. Annu Rev Immunol 20 (2002) 55-72
29. Feng G.J., Goodridge H.S., Harnett M.M., Wei X.Q., Nikolaev A.V., Higson A.P., et al. Extracellular signal-related kinase (ERK) and p38 mitogen-activated protein (MAP) kinases differentially regulate the lipopolysaccharide-mediated induction of inducible nitric oxide synthase and IL-12 in macrophages: Leishmania phosphoglycans subvert macrophage Il-12 production by targeting ERKMAP kinase. J Immunol 163 (1999) 6403-6412
30. Utsugi M., Dobashi K., Koga Y., Shimizu Y., Ishizuka T., Iizuka K., et al. Glutathione redox regulates lipopolysaccharide-induced IL-12 production through p38 mitogen-activated protein kinase activation in human monocytes: role of glutathione redox in IFN-gamma priming of IL-12 production. J Leukoc Biol 71 2 (2002) 339-347
31. Bouaboula M., Hilairet S., Marchand J., Fajas L., Le Fur G., and Casellas P. Anandamide induced PPAR gamma transcriptional activation and 3T3-L1 preadipocyte differentiation. Eur J Pharmacol 517 (2005) 174-181
32. Rockwell C.E., and Kaminski N.E. A cyclooxygenase metabolite of anandamide causes inhibition of interleukin-2 secretion in murine splenocytes. J Pharmacol Exp Ther 311 (2004) 683-690
33. Snider N.T., Kornilov A.M., Kent U.M., and Hollenberg P.F. Anandamide metabolism by human liver and kidney microsomal cytochrome p450 enzymes to form hydroxyeicosatetraenoic and epoxyeicosatrienoic acid ethanolamides. J Pharmacol Exp Ther 321 (2007) 590-597
34. Berdyshev E.V., Schmid P.C., Krebsbach R.J., Hillard C.J., Huang C., Chen N., et al. Cannabinoid-receptor-independent cell signalling by N-acylethanolamines. Biochem J 360 (2001) 67-75
35. Hidding U., Mielke K., Waetzig V., Brecht S., Hanisch U., Behrens A., et al. The c-Jun N-terminal kinases in cerebral microglia: immunological functions in the brain. Biochem Pharmacol 64 (2002) 781-788
36. Utsugi M., Dobashi K., Ishizuka T., Endou K., Hamuro J., Murata Y., et al. c-Jun N-terminal kinase negatively regulates lipopolysaccharide-induced IL-12 production in human macrophages: role of mitogen-activated protein kinase in glutathione redox regulation of IL-12 production. J Immunol 171 (2003) 628-635
37. Goodridge H.S., Harnett W., Liew F.Y., and Harnett M.M. Differential regulation of interleukin-12 p40 and p35 induction via Erk mitogen-activated protein kinase-dependent and independent mechanisms and the implications for bioactive IL-12 and IL-23 responses. Immunology 109 (2003) 415-425
38. Matias I., Pochard P., Orlando P., Salzet M., Pestel J., and Di Marzo V. Presence and regulation of the endocannabinoid system in human dendritic cells. Eur J Biochem 269 (2002) 3771-3778
39. Stella N. Canabinoid signalling in glial cells. Glia 48 (2004) 267-277
40. Centonze D., Bari M., Rossi S., Prosperetti C., Furlan R., Fezza F., et al. The endocannabinoid system is dysregulated in multiple sclerosis and in experimental autoimmune encephalomyelitis. Brain 1093 (2007) 1-11
41. Docagne F., Mestre L., Loría F., Hernangómez M., Correa F., and Guaza C. Therapeutic potential of CB2 targeting in multiple sclerosis. Expert Opin Ther Targets 12 (2008) 185-195
42. Chang J.T., Shevach E.M., and Segal B.M. Regulation of interleukin (IL)-12 receptor beta2 subunit expression by endogenous IL-12: a critical step in the differentiation of pathogenic autoreactive T cells. J Exp Med 189 (1999) 969-978
43. Windhagen A., Newcombe J., Dangond F., Strand C., Woodrofe M.N., and Cuzner M.L. Expression of costimulatory molecules B7-1 (CD80) B7-2 (CD86), and interleukin-12 cytokine in multiple sclerosis. J Exp Med 182 (1995) 1985-1996
44. Becher B., Durell B.G., and Noelle R.J. IL-23 produced by CNS-resident cells controls T cell encephalitogenicity during the effector phase of experimental autoimmune encephalomyelitis. J Clin Invest 112 (2003) 1186-1191
45. Nakahara T., Uchi H., Urabe K., Chen Q., Furue M., and Moroi Y. Role of c-Jun N-terminal kinase on lipopolysaccharide induced maturation of human monocyte-derived dendritic cells. Int Immunol 16 (2004) 1701-1709
46. Tomczak M.F., Gadjeva M., Wang Y.Y., Brown K., Maroulakou I., Tsichlis P.N., et al. Defective activation of ERK in macrophages lacking the p50/p105 subunit of NF-kappaB is responsible for elevated expression of IL-12 p40 observed after challenge with Helicobacter hepaticus. J Immunol 176 (2006) 1244-1251
47. Li Y., Chu N., Hu A., Gran B., Rostami A., and Zhang G. Inducible IL-23p19 expression in human microglia via p38 MAPK and NF-kappaB signal pathways. Exp Mol Pathol 84 (2008) 1-8
48. Daigle T.L., Kearn C.S., and Mackie K. Rapid CB1 cannabinoid receptor desensitization defines the time course of ERK1/2 MAP kinase signalling. Neuropharmacology 54 (2008) 36-44
49. Liu J., Gao B., Mirshahi F., Sanyal A.J., Khanolkar A.D., Makriyannis A., et al. Functional CB1 cannabinoid receptors in human vascular endothelial cells. Biochem J 346 (2000) 835-840
50. Rueda D., Galve-Roperh I., Haro A., and Guzmán M. The CB(1) cannabinoid receptor is coupled to the activation of c-Jun N-terminal kinase. Mol Pharmacol 58 (2000) 814-820
51. Molina-Holgado E., Vela J.M., Arévalo-Martín A., Almazán G., Molina-Holgado F., Borrell J., et al. Cannabinoids promote oligodendrocyte progenitor survival: involvement of cannabinoid receptors and phosphatidylinositol-3 kinase/Akt signaling. J Neurosci 22 (2002) 9742-9753
52. Bettelli E., Carrier Y., Gao W., Korn T., Strom T.B., Oukka M., et al. Reciprocal developmental pathways for the generation of pathogenic effector Th17 and regulatory T cells. Nature 441 (2006) 235-238
53. McKenzie B.S., Kastelein R.A., and Cua D.J. Understanding the IL-23-IL-17 immune pathway. Trends Immunol 27 (2006) 17-23