Endocannabinoids and the immune system in health and disease

Handbook of Experimental Pharmacology

Volumn 231, Issue , 2015, Pages 185-211

  Cabral, Guy A ^a   Ferreira, Gabriela A ^a   Jamerson, Melissa J ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

2 Arachidonoylglycerol; Anandamide; Antigen presentation; Astrocyte; Basophil; Cannabinoid receptor; Chemokine; Cytokine; Dendritic cell; Endocannabinoid; Interferon; Interleukin; Lymphocyte; Macrophage; Mast cell; Microglia; Monocyte; Natural killer (NK) cell; Neutrophil; Nitric oxide

Indexed keywords

2 ARACHIDONOYLGLYCEROL; ANANDAMIDE; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; CHEMOKINE; CYTOKINE; ENDOCANNABINOID; NITRIC OXIDE;

ANTIGEN PRESENTATION; ASTROCYTE; ATHEROSCLEROSIS; AUTOCRINE EFFECT; BASOPHIL; CELL MIGRATION; CYTOKINE PRODUCTION; DELAYED HYPERSENSITIVITY; DENDRITIC CELL; EOSINOPHIL; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE SYSTEM; LYMPHOCYTE; MACROPHAGE; MAST CELL; MICROGLIA; MONOCYTE; MULTIPLE SCLEROSIS; NATURAL KILLER CELL; NEUTROPHIL; NONHUMAN; PARACRINE SIGNALING; PERIODONTITIS; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION;

EID: 84942511296     PISSN: 01712004     EISSN: 18650325     Source Type: Book Series    
DOI: 10.1007/978-3-319-20825-1_6     Document Type: Chapter

References (74)

1. Arafah K, Croix D, Vizioli J, Desmons A, Fournier I, Salzet M (2013) Involvement of nitric oxide through endocannabinoids release in microglia activation during the course of CNS regeneration in the medicinal leech. Glia 61:636–649
2. Balenga NA, Aflaki E, Kargl J, Platzer W, Schroder R, Blättermann S et al (2011) GPR55 regulates cannabinoid 2 receptor-mediated responses in human neutrophils. Cell Res 21:1452–1469
3. Berdyshev EV, Boichot E, Germain N, Allain N, Anger JP, Lagente V (1997) Influence of fatty acid ethanolamides and delta9-tetrahydrocannabinol on cytokine and arachidonate release by mononuclear cells. Eur J Pharmacol 330:231–240
4. Bittner S, Meuth SG, Gobel K, Melzer N, Herrmann AM, Simon OJ et al (2009) TASK1 modulates inflammation and neurodegeneration in autoimmune inflammation of the central nervous system. Brain 132:2501–2516
5. Cabral GA, Toney DM, Fischer-Stenger K, Harrison MP, Marciano-Cabral F (1995) Anandamide inhibits macrophage-mediated killing of tumor necrosis factor-sensitive cells. Life Sci 56:2065–2072
6. Chang YH, Lee ST, Lin WW (2001) Effects of cannabinoids on LPS-stimulated inflammatory mediator release from macrophages: involvement of eicosanoids. J Cell Biochem 81:715–723
7. Chiurchiũ V, Cencioni MT, Bisicchia E, De Bardi M, Gasperini C, Borsellino G et al (2013) Distinct modulation of human myeloid and plasmacytoid dendritic cells by anandamide in multiple sclerosis. Ann Neurol 73:626–636
8. Chouinard F, Lefebvre JS, Navarro P, Bouchard L, Ferland C, Lalancette-Hébert M et al (2011) The endocannabinoid 2-arachidonoyl-glycerol activates human neutrophils: critical role of its hydrolysis and de novo leukotriene B4 biosynthesis. J Immunol 186:3188–3196
9. Chouinard F, Turcotte C, Guan X, Larose MC, Poirier S, Bouchard L et al (2013) 2-Arachidonoylglycerol- and arachidonic acid-stimulated neutrophils release antimicrobial effectors against E. coli, S. aureus, HSV-1, and RSV. J Leukoc Biol 93:267–276
10. Coopman K, Smith LD, Wright KL, Ward SG (2007) Temporal variation in CB2R levels following T lymphocyte activation: evidence that cannabinoids modulate CXCL12-induced chemotaxis. Int Immunopharmacol 7:360–371
11. Correa F, Docagne F, Mestre L, Clemente D, Hernangomez M, Loria F et al (2009) A role for CB2 receptors in anandamide signalling pathways involved in the regulation of IL-12 and IL-23 in microglial cells. Biochem Pharmacol 77:86–100
12. Correa F, Hernangomez M, Mestre L, Loria F, Spagnolo A, Docagne F et al (2010) Anandamide enhances IL-10 production in activated microglia by targeting CB(2) receptors: roles of ERK1/ 2, JNK, and NF-kappaB. Glia 58:135–147
13. Correa F, Hernangómez-Herrero M, Mestre L, Loriá F, Docagne F, Guaza C (2011) The endocannabinoid anandamide downregulates IL-23 and IL-12 subunits in a viral model of multiple sclerosis: evidence for a cross-talk between IL-12p70/IL-23 axis and IL-10 in microglial cells. Brain Behav Immun 25:736–749
14. Derocq JM, Bouaboula M, Marchand J, Rinaldi-Carmona M, Ségui M, Casellas P (1998) The endogenous cannabinoid anandamide is a lipid messenger activating cell growth via a cannabinoid receptor-independent pathway in hematopoietic cell lines. FEBS Lett 425:419–425
15. Devane WA, Hanus L, Breuer A, Pertwee RG, Stevenson LA, Griffin G et al (1992) Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 258:1946–1949
16. Do Y, McKallip RJ, Nagarkatti M, Nagarkatti PS (2004) Activation through cannabinoid receptors1 and 2 on dendritic cells triggers NF-kappaB-dependent apoptosis: novel role for endogenous and exogenous cannabinoids in immunoregulation. J Immunol 173:2373–2382
17. Donovan J, Grundy D (2012) Endocannabinoid modulation of jejunal afferent responses to LPS. Neurogastroenterol Motil 24:956–e465
18. Facci L, Dal TR, Romanello S, Buriani A, Skaper SD, Leon A (1995) Mast cells express a peripheral cannabinoid receptor with differential sensitivity to anandamide and palmitoylethanolamide. Proc Natl Acad Sci USA 92:3376–3380
19. Fernandez-Suarez D, Celorrio M, Riezu-Boj JI, Ugarte A, Pacheco R, Gonzalez H, Oyarzabal J, Hillard CJ, Franco R, Aymerich MS (2014) The monoacylglycerol lipase inhibitor JZL184 is neuroprotective and alters glial cell phenotype in the chronic MPTP mouse model. Neurobiol Aging 35:2603–2616
20. Galiegue S, Mary S, Marchand J, Dussossoy D, Carriére D, Carayon P et al (1995) Expression of central and peripheral cannabinoid receptors in human immune tissues and leukocyte subpopulations. Eur J Biochem 232:54–61
21. Gasperi V, Evangelista D, Chiurchiũ V, Florenzano F, Savini I, Oddi S et al (2014) 2-Arachidonoylglycerol modulates human endothelial cell/leukocyte interactions by controlling selectin expression through CB1 and CB2 receptors. Int J Biochem Cell Biol 51:79–88
22. Gerard CM, Mollereau C, Vassart G, Parmentier M (1991) Molecular cloning of a human cannabinoid receptor which is also expressed in testis. Biochem J 279:129–134
23. Gokoh M, Kishimoto S, Oka S, Metani Y, Sugiura T (2005) 2-Arachidonoylglycerol, an endogenous cannabinoid receptor ligand, enhances the adhesion of HL-60 cells differentiated into macrophage-like cells and human peripheral blood monocytes. FEBS Lett 579:6473–6478
24. Gokoh M, Kishimoto S, Oka S, Sugiura T (2007) 2-Arachidonoylglycerol enhances the phagocytosis of opsonized zymosan by HL-60 cells differentiated into macrophage-like cells. Biol Pharm Bull 30:1199–1205
25. Herkenham M, Lynn AB, Little MD, Johnson MR, Melvin LS, De Costa BR et al (1990) Cannabinoid receptor localization in brain. Proc Natl Acad Sci USA 87:1932–1936
26. Hernangomez M, Mestre L, Correa FG, Loria F, Mecha M, Inigo PM et al (2012) CD200-CD200R1 interaction contributes to neuroprotective effects of anandamide on experimentally induced inflammation. Glia 60:1437–1450
27. Hu SS, Arnold A, Hutchens JM, Radicke J, Cravatt BF, Wager-Miller J et al (2010) Architecture of cannabinoid signaling in mouse retina. J Comp Neurol 518:3848–3866
28. Jackson AR, Hegde VL, Nagarkatti PS, Nagarkatti M (2014) Characterization of endocannabinoid-mediated induction of myeloid-derived suppressor cells involving mast cells and MCP-1. J Leukoc Biol 95:609–619
29. Katz PS, Sulzer JK, Impastato RA, Teng SX, Rogers EK, Molina P (2014) Endocannabinoid degradation inhibition improves neurobehavioral function, blood brain barrier integrity, and neuroinflammation following mild traumatic brain injury. J Neurotrauma 32:297–306
30. Kishimoto S, Gokoh M, Oka S, Muramatsu M, Kajiwara T, Waku K et al (2003) 2-arachidonoylglycerol induces the migration of HL-60 cells differentiated into macrophagelike cells and human peripheral blood monocytes through the cannabinoid CB2 receptordependent mechanism. J Biol Chem 278:24469–24475
31. Kishimoto S, Muramatsu M, Gokoh M, Oka S, Waku K, Sugiura T (2005) Endogenous cannabinoid receptor ligand induces the migration of human natural killer cells. J Biol Chem 137:217–223
32. Kishimoto S, Oka S, Gokoh M, Sugiura T (2006) Chemotaxis of human peripheral blood eosinophils to 2-arachidonoylglycerol: comparison with other eosinophil chemoattractants. Int Arch Allergy Immunol 140:3–7
33. Kraft B, Kress HG (2005) Indirect CB2 receptor and mediator-dependent stimulation of human whole-blood neutrophils by exogenous and endogenous cannabinoids. J Pharmacol Exp Ther 315:641–647
34. Kreutz S, Koch M, Bottger C, Ghadban C, Korf HW, Dehghani F (2009) 2-Arachidonoylglycerol elicits neuroprotective effects on excitotoxically lesioned dentate gyrus granule cells via abnormal-cannabidiol-sensitive receptors on microglial cells. Glia 57:286–294
35. Krishnan G, Chatterjee N (2014) Endocannabinoids affect innate immunity of Muller glia during HIV-1 Tat cytotoxicity. Mol Cell Neurosci 59:10–23
36. Kurihara R, Tohyama Y, Matsusaka S, Naruse H, Kinoshita E, Tsujioka T et al (2006) Effects of peripheral cannabinoid receptor ligands on motility and polarization in neutrophil-like HL60 cells and human neutrophils. J Biol Chem 281:12908–12918
37. Lau AH, Chow SS (2003) Effects of cannabinoid receptor agonists on immunologically induced histamine release from rat peritoneal mast cells. Eur J Pharmacol 464:229–235
38. Lee M, Yang KH, Kaminski NE (1995) Effects of putative cannabinoid receptor ligands, anandamide and 2-arachidonyl-glycerol, on immune function in B6C3F1 mouse splenocytes. J Pharmacol Exp Ther 275:529–536
39. Lenglet S, Thomas A, Soehnlein O, Montecucco F, Burger F, Pelli G et al (2013) Fatty acid amide hydrolase deficiency enhances intraplaque neutrophil recruitment in atherosclerotic mice. Arterioscler Thromb Vasc Biol 33:215–223
40. Lourbopoulos A, Grigoriadis N, Lagoudaki R, Touloumi O, Polyzoidou E, Mavromatis I et al (2011) Administration of 2-arachidonoylglycerol ameliorates both acute and chronic experimental autoimmune encephalomyelitis. Brain Res 16:126–141
41. Maestroni GJ (2004) The endogenous cannabinoid 2-arachidonoyl glycerol as in vivo chemoattractant for dendritic cells and adjuvant for Th1 response to a soluble protein. FASEB J 18:1914–1916
42. Matias I, Pochard P, Orlando P, Salzet M, Pestel J, Di MV (2002) Presence and regulation of the endocannabinoid system in human dendritic cells. Eur J Biochem 269:3771–3778
43. Matsuda LA, Lolait SJ, Brownstein MJ, Young AC, Bonner TI (1990) Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 346:561–564
44. McHugh D, Tanner C, Mechoulam R, Pertwee RG, Ross RA (2008) Inhibition of human neutrophil chemotaxis by endogenous cannabinoids and phytocannabinoids: evidence for a site distinct from CB1 and CB2. Mol Pharmacol 73:441–450
45. McHugh D, Hu SS, Rimmerman N, Juknat A, Vogel Z, Walker JM et al (2010) N-arachidonoyl glycine, an abundant endogenous lipid, potently drives directed cellular migration through GPR18, the putative abnormal cannabidiol receptor. BMC Neurosci 11:44
46. Mechoulam R, Ben-Shabat S, Hanus L, Ligumsky M, Kaminski NE, Schatz AR et al (1995) Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochem Pharmacol 50:83–90
47. Mestre L, I~nigo PM, Mecha M, Correa FG, Hernanǵomez-Herrero M, Loría F et al (2011) Anandamide inhibits Theiler’s virus induced VCAM-1 in brain endothelial cells and reduces leukocyte transmigration in a model of blood brain barrier by activation of CB(1) receptors. J Neuroinflammation 8:102
48. Metcalfe DD, Baram D, Mekori YA (1997) Mast cells. Physiol Rev 77:1033–1079
49. Mimura T, Oka S, Koshimoto H, Ueda Y, Watanabe Y, Sugiura T (2012) Involvement of the endogenous cannabinoid 2 ligand 2-arachidonyl glycerol in allergic inflammation. Int Arch Allergy Immunol 159:149–156
50. Molina-Holgado F, Lledó A, Guaza C (1997) Anandamide suppresses nitric oxide and TNF-alpha responses to Theiler’s virus or endotoxin in astrocytes. Neuroreport 8:1929–1933
51. Molina-Holgado F, Molina-Holgado E, Guaza C (1998) The endogenous cannabinoid anandamide potentiates interleukin-6 production by astrocytes infected with Theiler’s murine encephalomyelitis virus by a receptor-mediated pathway. FEBS Lett 433:139–142
52. Molina-Holgado F, Molina-Holgado E, Guaza C, Rothwell NJ (2002) Role of CB1 and CB2 receptors in the inhibitory effects of cannabinoids on lipopolysaccharide-induced nitric oxide release in astrocyte cultures. J Neurosci Res 67:829–836
53. Montecucco F, Matias I, Lenglet S, Petrosino S, Burger F, Pelli G et al (2009) Regulation and possible role of endocannabinoids and related mediators in hypercholesterolemic mice with atherosclerosis. Atherosclerosis 205:433–441
54. Navarrete CM, Fiebich BL, de Vinuesa AG, Hess S, de Oliveira AC, Candelario-Jalil E et al (2009) Opposite effects of anandamide and N-arachidonoyl dopamine in the regulation of prostaglandin E and 8-iso-PGF formation in primary glial cells. J Neurochem 109:452–464
55. Oka S, Ikeda S, Kishimoto S, Gokoh M, Yanagimoto S, Waku K et al (2004) 2-arachidonoylglycerol, an endogenous cannabinoid receptor ligand, induces the migration of EoL-1 human eosinophilic leukemia cells and human peripheral blood eosinophils. J Leukoc Biol 76:1002–1009
56. Oka S, Yanagimoto S, Ikeda S, Gokoh M, Kishimoto S, Waku K et al (2005) Evidence for the involvement of the cannabinoid CB2 receptor and its endogenous ligand 2-arachidonoylglycerol in 12-O-tetradecanoylphorbol-13-acetate-induced acute inflammation in mouse ear. J Biol Chem 280:18488–18497
57. Ortega-Gutiérrez S, Molina-Holgado E, Guaza C (2005) Effect of anandamide uptake inhibition in the production of nitric oxide and in the release of cytokines in astrocyte cultures. Glia 52:163–168
58. Parolaro D, Massi P, Rubino T, Monti E (2002) Endocannabinoids in the immune system and cancer. Prostaglandins Leukot Essent Fatty Acids 66:319–332
59. Piro JR, Benjamin DI, Duerr JM, Pi Y, Gonzales C, Wood KM, Schwartz JW et al (2012) A dysregulated endocannabinoid-eicosanoid network supports pathogenesis in a mouse model of Alzheimer’s disease. Cell Rep 28:617–623
60. Rettori E, De Laurentiis A, Zorrilla Zubilete M, Rettori V, Elverdin JC (2012) Anti-inflammatory effect of the endocannabinoid anandamide in experimental periodontitis and stress in the rat. Neuroimmunomodulation 19:293–303
61. Ribeiro A, Ferraz-de-Paula V, Pinheiro ML, Sakai M, Costa-Pinto FA, Palermo-Neto J (2010) Anandamide prior to sensitization increases cell-mediated immunity in mice. Int Immunopharmacol 10:431–439
62. Rockwell CE, Raman P, Kaplan BL, Kaminski NE (2008) A COX-2 metabolite of the endogenous cannabinoid, 2-arachidonyl glycerol, mediates suppression of IL-2 secretion in activated Jurkat T cells. Biochem Pharmacol 76:353–361
63. Rossi S, Furlan R, De Chiara V, Muzio L, Musella A, Motta C et al (2011) Cannabinoid CB1 receptors regulate neuronal TNF-a effects in experimental autoimmune encephalomyelitis. Brain Behav Immun 25:1242–1248
64. Sanchez Lopez AJ, Roman-Vega L, Ramil TE, Giuffrida A, Garcia-Merino A (2014) Regulation of cannabinoid receptor gene expression and endocannabinoid levels in lymphocyte subsets by IFN-beta: a longitudinal study in multiple sclerosis patients. Clin Exp Immunol 179:119–27
65. Schatz AR, Lee M, Condie RB, Pulaski JT, Kaminski NE (1997) Cannabinoid receptors CB1 and CB2: a characterization of expression and adenylate cyclase modulation within the immune system. Toxicol Appl Pharmacol 142:278–287
66. Schwarz H, Blanco FJ, Lotz M (1994) Anandamide, an endogenous cannabinoid receptor agonist inhibits lymphocyte proliferation and induces apoptosis. J Neuroimmunol 55:107–115
67. Stefano GB, Bilfinger TV, Rialas CM, Deutsch DG (2000) 2-arachidonyl-glycerol stimulates nitric oxide release from human immune and vascular tissues and invertebrate immunocytes by cannabinoid receptor 1. Pharmacol Res 42:317–322
68. Suárez J, Romero-Zerbo SY, Rivera P, Bermúdez-Silva FJ, Pérez J, De Fonseca FR et al (2010) Endocannabinoid system in the adult rat circumventricular areas: an immunohistochemical study. J Comp Neurol 518:3065–3085
69. Sugamura K, Sugiyama S, Nozaki T, Matsuzawa Y, Izumiya Y, Miyata K et al (2009) Activated endocannabinoid system in coronary artery disease and anti-inflammatory effects of cannabinoid 1 receptor blockade on macrophages. Circulation 119:28–36
70. Sugawara K, Biro T, Tsuruta D, Toth BI, Kromminga A, Zakany N et al (2012) Endocannabinoids limit excessive mast cell maturation and activation in human skin. J Allergy Clin Immunol 129:726–738
71. Sugiura T, Kondo S, Kishimoto S, Miyashita T, Nakane S, Kodaka T et al (2000) Evidence that 2-arachidonoylglycerol but not N-palmitoylethanolamine or anandamide is the physiological ligand for the cannabinoid CB2 receptor. Comparison of the agonistic activities of various cannabinoid receptor ligands in HL-60 cells. J Biol Chem 275:605–612
72. Valk P, Verbakel S, Vankan Y, Hol S, Mancham S, Ploemacher R et al (1997) Anandamide, a natural ligand for the peripheral cannabinoid receptor is a novel synergistic growth factor for hematopoietic cells. Blood 90:1448–1457
73. Vannacci A, Zagli G, Marzocca C, Pierpaoli S, Passani MB, Mannaioni PF, Masini E (2002) Down-regulation by cannabinoids of the immunological activation of human basophils and guinea pig mast cells. Inflamm Res 51:S09–S10
74. Vannacci A, Giannini L, Passani MB, Di FA, Pierpaoli S, Zagli G et al (2004) The endocannabinoid 2-arachidonylglycerol decreases the immunological activation of Guinea pig mast cells: involvement of nitric oxide and eicosanoids. J Pharmacol Exp Ther 311:256–264