Regulatory role of the cannabinoid CB2 receptor in stress-induced neuroinflammation in mice

British Journal of Pharmacology

Volumn 171, Issue 11, 2014, Pages 2814-2826

  Zoppi, S ^a,b,c   Madrigal, J L ^a,b,c   Caso, J R ^a,b,c   Garcia Gutierrez M S ^d,e   Manzanares, J ^d,e   Leza, J C ^a,b,c   Garcia Bueno B ^a,b,c  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE SALUD MENTAL CIBERSAM   (Spain)

^c Instituto de Investigaciõn Sanitaria Hospital 12 de Octubre ^*  (Spain)

^d CSIC   (Spain)

^e RETICS Red Temática de Investigación Cooperativa Sanitaria en Enfermedades Oculares Oftared   (Spain)

Author keywords

brain frontal cortex; CB2xP mice; excitotoxicity; JWH 133; neuroinflammation; stress

Indexed keywords

1 DEOXY 3 (1,1 DIMETHYLBUTYL) DELTA8 TETRAHYDROCANNABINOL; CANNABINOID 2 RECEPTOR; CORTICOSTERONE; CYCLOOXYGENASE 2; GLUTAMIC ACID; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA; 1,1-DIMETHYLBUTYL-1-DEOXY-DELTA(9)-THC; CANNABINOID; CCL2 PROTEIN, MOUSE; NITRITE; NOS2 PROTEIN, MOUSE; PROSTAGLANDIN E2; PTGS2 PROTEIN, MOUSE;

ACOUSTIC STRESS; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BLOOD SAMPLING; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG MECHANISM; ENZYME RELEASE; EXCITOTOXICITY; FRONTAL CORTEX; HORMONE BLOOD LEVEL; IMMOBILIZATION; LIPID PEROXIDATION; MALE; MOUSE; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SYNAPTOSOME; WESTERN BLOTTING; AGONISTS; ANIMAL; BLOOD; FRONTAL LOBE; GENETICS; INFLAMMATION; INSTITUTE FOR CANCER RESEARCH MOUSE; MENTAL STRESS; METABOLISM; TRANSGENIC MOUSE;

ANIMALS; CANNABINOIDS; CHEMOKINE CCL2; CORTICOSTERONE; CYCLOOXYGENASE 2; DINOPROSTONE; FRONTAL LOBE; GLUTAMIC ACID; INFLAMMATION; MALE; MICE, INBRED ICR; MICE, TRANSGENIC; NF-KAPPA B; NITRIC OXIDE SYNTHASE TYPE II; NITRITES; RECEPTOR, CANNABINOID, CB2; STRESS, PSYCHOLOGICAL; SYNAPTOSOMES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84900533302     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.12607     Document Type: Article

References (62)

1. Adhikary S, Li H, Heller J, Skarica M, Zhang M, Ganea D, et al. (2011). Modulation of inflammatory responses by a cannabinoid-2-selective agonist after spinal cord injury. J Neurotrauma 28: 2417-2427.
2. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013a). The Concise Guide to PHARMACOLOGY 2013/14: G Protein-Coupled Receptors. Br J Pharmacol 170: 1459-1581
3. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013b). The Concise Guide to PHARMACOLOGY 2013/14: Transporters. Br J Pharmacol 170: 1706-1796.
4. 2 receptors. Neuropsychopharmacology 7: 1749-1763.
5. Arévalo-Martín A, Vela JM, Molina-Holgado E, Borrell J, Guaza C, (2003). Therapeutic action of cannabinoids in a murine model of multiple sclerosis. J Neurosci 23: 2511-2516.
6. 2: a cannabinoid receptor with an identity crisis. Br J Pharmacol 160: 467-479.
7. Bambico FR, Duranti A, Tontini A, Tarzia G, Gobbi G, (2009). Endocannabinoids in the treatment of mood disorders: evidence from animal models. Curr Pharm Des 15: 1623-1646.
8. Bierhaus A, Wolf J, Andrassy M, Rohleder N, Humpert PM, Petrov D, et al. (2003). A mechanism converting psychosocial stress into mononuclear cell activation. Proc Natl Acad Sci U S A 100: 1920-1925.
9. Bisogno T, Di Marzo V, (2010). Cannabinoid receptors and endocannabinoids: role in neuroinflammatory and neurodegenerative disorders. CNS Neurol Disord Drug Targets 9: 564-573.
10. Bradford MM, (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
11. Bremner JD, Randall P, Scott TM, Bronen RA, Seibyl JP, Southwick SM, et al. (1995). MRI-based measurement of hippocampal volume in patients with combat-related posttraumatic stress disorder. Am J Psychiatry 152: 973-981.
12. Cabral GA, Griffin-Thomas L, (2009). Emerging role of the cannabinoid receptor CB2 in immune regulation: therapeutic prospects for neuroinflammation. Expert Rev Mol Med 11: e3.
13. Capuron L, Miller AH, (2011). Immune system to brain signaling: neuropsychopharmacological implications. Pharmacol Ther 130: 226-238.
14. Castillo A, Tolõn MR, Fernández-Ruiz J, Romero J, Martinez-Orgado J, (2010). The neuroprotective effect of cannabidiol in an in vitro model of newborn hypoxic-ischemic brain damage in mice is mediated by CB(2) and adenosine receptors. Neurobiol Dis 37: 434-440.
15. Conductier G, Blondeau N, Guyon A, Nahon JL, Rovère C, (2010). The role of monocyte chemoattractant protein MCP1/CCL2 in neuroinflammatory diseases. J Neuroimmunol 224: 93-100.
16. Correa F, Hernangõmez M, Mestre L, Loría 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.
17. Das NP, Ratty AK, (1987). Studies on the effects of the narcotic alkaloids, cocaine, morphine and codeine on nonenzymatic lipid peroxidation in rat brain mitochondria. Biochem Med Metab Biol 37: 256-264.
18. 2 receptor activation. Mol Cell Neurosci 34: 551-561.
19. Farooq RK, Isingrini E, Tanti A, Le Guisquet AM, Arlicot N, Minier F, et al. (2012). Is unpredictable chronic mild stress (UCMS) a reliable model to study depression-induced neuroinflammation? Behav Brain Res 231: 130-137.
20. Fernández-Ruiz J, (2009). The endocannabinoid system as a target for the treatment of motor dysfunction. Br J Pharmacol 156: 1029-1040.
21. García-Bueno B, Caso JR, Pérez-Nievas BG, Lorenzo P, Leza JC, (2007). Effects of peroxisome proliferator-activated receptor gamma agonists on brain glucose and glutamate transporters after stress in rats. Neuropsychopharmacology 32: 1251-1260.
22. García-Bueno B, Caso JR, Leza JC, (2008). Stress as a neuroinflammatory condition in brain: damaging and protective mechanisms. Neurosci Biobehav Rev 32: 1136-1151.
23. 2 cannabinoid receptors decreased vulnerability to anxiety and impaired anxiolytic action of alprazolam in mice. Psychopharmacol 25: 111-120.
24. García-Gutiérrez MS, Pérez-Ortiz JM, Gutiérrez-Adán A, Manzanares J, (2010). Depression-resistant endophenotype in mice overexpressing cannabinoid CB(2) receptors. Br J Pharmacol 160: 1773-1784.
25. Gong JP, Onaivi ES, Ishiguro H, Liu QR, Tagliaferro PA, Brusco A, et al. (2006). Cannabinoid CB2 receptors: immunohistochemical localization in rat brain. Brain Res 1071: 10-23.
26. Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR, (1982). Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Anal Biochem 126: 131-138.
27. Herbert TB, Cohen S, (1993). Stress and immunity in humans: a meta-analytic review. Psychosom Med 55: 364-379.
28. Huffman JW, Liddle J, Yu S, Aung MM, Abood ME, Wiley JL, et al. (1999). 3-(1′,1′-Dimethylbutyl)-1-deoxy-delta8-THC and related compounds: synthesis of selective ligands for the CB2 receptor. Bioorg Med Chem 7: 2905-2914.
29. Jean-Gilles L, Gran B, Constantinescu CS, (2010). Interaction between cytokines, cannabinoids and the nervous system. Immunobiology 215: 606-610.
30. Jeon YJ, Yang KH, Pulaski JT, Kaminski NE, (1996). Attenuation of inducible nitric oxide synthase gene expression by delta 9-tetrahydrocannabinol is mediated through the inhibition of nuclear factor-kappa B/Rel activation. Mol Pharmacol 50: 334-341.
31. Kiank C, Holtfreter B, Starke A, Mundt A, Wilke C, Schütt C, (2006). Stress susceptibility predicts the severity of immune depression and the failure to combat bacterial infections in chronically stressed mice. Brain Behav Immun 20: 359-368.
32. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG, (2010). Animal research: reporting in vivo experiments: the ARRIVE guidelines. Br J Pharmacol 160: 1577-1579.
33. Kim JJ, Yoon KS, (1998). Stress: metaplastic effects in the hippocampus. Trends Neurosci 21: 505-509.
34. Klein TW, Newton C, Larsen K, Lu L, Perkins I, Nong L, et al. (2003). The cannabinoid system and immune modulation. Leukoc Biol 74: 486-496.
35. Licinio J, Wong ML, (1999). The role of inflammatory mediators in the biology of major depression: central nervous system cytokines modulate the biological substrate of depressive symptoms, regulate stress-responsive systems, and contribute to neurotoxicity and neuroprotection. Mol Psychiatry 4: 317-327.
36. Loría F, Petrosino S, Hernangõmez M, Mestre L, Spagnolo A, Correa F, et al. (2010). An endocannabinoid tone limits excitotoxicity in vitro and in a model of multiple sclerosis. Neurobiol Dis 37: 166-176.
37. Madrigal JL, Hurtado O, Moro MA, Lizasoain I, Lorenzo P, Castrillo A, et al. (2002). The increase in TNF-alpha levels is involved in NF-kappaB activation and inducible nitric oxide synthase expression in brain cortex after immobilization stress. Neuropsychopharmacology 26: 155-163.
38. Madrigal JL, García-Bueno B, Caso JR, Pérez-Nievas BG, Leza JC, (2006). Stress-induced oxidative changes in brain. CNS Neurol Disord Drug Targets 5: 561-568.
39. Marchetti L, Klein M, Schlett K, Pfizenmaier K, Eisel UL, (2004). Tumor necrosis factor (TNF)-mediated neuroprotection against glutamate-induced excitotoxicity is enhanced by N-methyl-D-aspartate receptor activation. Essential role of a TNF receptor 2-mediated phosphatidylinositol 3-kinase-dependent NF-kappa B pathway. J Biol Chem 279: 32869-32881.
40. Martín-Moreno AM, Brera B, Spuch C, Carro E, García- García L, Delgado M, et al. (2012). Prolonged oral cannabinoid administration prevents neuroinflammation, lowers β-amyloid levels and improves cognitive performance in Tg APP 2576 mice. J Neuroinflammation 9: 8.
41. McGrath J, Drummond G, McLachlan E, Kilkenny C, Wainwright C, (2010). Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol 160: 1573-1576.
42. Mechoulam R, Parker LA, (2013). The endocannabinoid system and the brain. Annu Rev Psychol 64: 21-47.
43. Mechoulam R, Shohami E, (2007). Endocannabinoids and traumatic brain injury. Mol Neurobiol 36: 68-74.
44. 2 receptor-mediated migration of immune cells: it can go either way. Br J Pharmacol 153: 299-308.
45. Moghaddam B, (1993). Stress preferentially increases extraneuronal levels of excitatory amino acids in the prefrontal cortex: comparison to hippocampus and basal ganglia. J Neurochem 60: 1650-1657.
46. 2 cannabinoid receptors: beyond neuro-immuno-cannabinoid activity. J Psychopharmacol 26: 92-103.
47. 2 cannabinoid receptor induces schizophrenia-related behaviors in mice. Neuropsychopharmacology 36: 1489-1504.
48. Palazuelos J, Davoust N, Julien B, Hatterer E, Aguado T, Mechoulam R, et al. (2008). The CB(2) cannabinoid receptor controls myeloid progenitor trafficking: involvement in the pathogenesis of an animal model of multiple sclerosis. J Biol Chem 83: 13320-13329.
49. 2 cannabinoid receptors are neuroprotective in Huntington's disease excitotoxicity. Brain 132 (Pt 11): 3152-3164.
50. 2 receptors. Pharmacol Ther 74: 129-180.
51. Racz I, Nadal X, Alferink J, Baños JE, Rehnelt J, Martín M, et al. (2008). Crucial role of CB(2) cannabinoid receptor in the regulation of central immune responses during neuropathic pain. J Neurosci 28: 12125-12135.
52. Radley JJ, Arias CM, Sawchenko PE, (2006). Regional differentiation of the medial prefrontal cortex in regulating adaptive responses to acute emotional stress. J Neurosci 26: 12967-12976.
53. Roche M, Diamond M, Kelly JP, Finn DP, (2006). In vivo modulation of LPS-induced alterations in brain and peripheral cytokines and HPA axis activity by cannabinoids. J Neuroimmunol 181: 57-67.
54. 2 receptor in the brain induces hyperglycaemia and a lean phenotype in adult mice. J Neuroendocrinol 24: 1106-1119.
55. Schreiber E, Matthias P, Müller MM, Schaffner W, (1989). Rapid detection of octamer binding proteins with 'mini-extracts', prepared from a small number of cells. Nucleic Acid Res 17: 6419.
56. Sorrells SF, Caso JR, Munhoz CD, Sapolsky RM, (2009). The stressed CNS: when glucocorticoids aggravate inflammation. Neuron 64: 33-39.
57. 2 cannabinoid receptors results in neuroprotection against behavioral and neurochemical alterations induced by intracaudate administration of 6-hydroxydopamine. Neurobiol Aging 33: 421.e1-421.e16.
58. Wager-Smith K, Markou A, (2011). Depression: a repair response to stress-induced neuronal microdamage that can grade into a chronic neuroinflammatory condition? Neurosci Biobehav Rev 35: 742-764.
59. Wolf SA, Tauber S, Ullrich O, (2008). CNS immune surveillance and neuroinflammation: endocannabinoids keep control. Curr Pharm Des 14: 2266-2278.
60. Yamagata K, Andreasson KI, Kaufmann WE, Barnes CA, Worley PF, (1993). Expression of a mitogen-inducible cyclooxygenase in brain neurons: regulation by synaptic activity and glucocorticoids. Neuron 11: 371-386.
61. Zarruk JG, Fernández-Lõpez D, García-Yébenes I, García-Gutiérrez MS, Vivancos J, Nombela F, et al. (2012). Cannabinoid type 2 receptor activation downregulates stroke-induced classic and alternative brain macrophage/microglial activation concomitant to neuroprotection. Stroke 43: 211-219.
62. Zoppi S, Pérez Nievas BG, Madrigal JL, Manzanares J, Leza JC, García-Bueno B, (2011). Regulatory role of cannabinoid receptor 1 in stress-induced excitotoxicity and neuroinflammation. Neuropsychopharmacology 236: 805-818.