The neuroprotective effect of cannabidiol in an in vitro model of newborn hypoxic-ischemic brain damage in mice is mediated by CB2 and adenosine receptors

Neurobiology of Disease

Volumn 37, Issue 2, 2010, Pages 434-440

  Castillo, A ^a   Tolon M R ^a,b   Fernandez Ruiz J ^b,c   Romero, J ^a,b   Martinez Orgado, J ^a,b,d  

^a HOSPITAL UNIVERSITARIO FUNDACIÓN ALCORCÓN   (Spain)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

^c UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^d HOSPITAL UNIVERSITARIO PUERTA DE HIERRO   (Spain)

Author keywords

Adenosine; Cannabidiol; Hypoxia ischemia; Mice; Neuroprotection; Newborn

Indexed keywords

5 AMINO 2 (2 FURYL) 7 (2 PHENYLETHYL)PYRAZOLO[4,3 E][1,2,4]TRIAZOLO[1,5 C]PYRIMIDINE; 6 IODO 3 (4 METHOXYBENZOYL) 2 METHYL 1 (2 MORPHOLINOETHYL)INDOLE; 8 CYCLOPENTYL 1,3 DIPROPYLXANTHINE; ADENOSINE A1 RECEPTOR; ADENOSINE A2 RECEPTOR; ADENOSINE RECEPTOR; ADENOSINE RECEPTOR BLOCKING AGENT; CANNABIDIOL; CANNABINOID 1 RECEPTOR ANTAGONIST; CANNABINOID 2 RECEPTOR; CASPASE 9; CYCLOOXYGENASE 2; GLUCOSE; GLUTAMIC ACID; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 6; LACTATE DEHYDROGENASE; OXYGEN; RIMONABANT; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN DAMAGE; BRAIN HYPOXIA; BRAIN ISCHEMIA; BRAIN MATURATION; BRAIN SLICE; CONTROLLED STUDY; CULTURE MEDIUM; FOREBRAIN; IN VITRO STUDY; MOUSE; NERVE CELL NECROSIS; NEUROPROTECTION; NEWBORN; NONHUMAN; PRIORITY JOURNAL;

AGING; ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; BRAIN; CANNABIDIOL; CASPASES; CYTOPROTECTION; DISEASE MODELS, ANIMAL; DOWN-REGULATION; GLUTAMIC ACID; HYPOXIA-ISCHEMIA, BRAIN; INFLAMMATION MEDIATORS; INTERLEUKIN-6; MICE; MICE, INBRED C57BL; NERVE DEGENERATION; NEUROPROTECTIVE AGENTS; ORGAN CULTURE TECHNIQUES; RECEPTOR, ADENOSINE A1; RECEPTOR, ADENOSINE A2A; RECEPTOR, CANNABINOID, CB1; RECEPTOR, CANNABINOID, CB2; RECEPTORS, PURINERGIC P1;

EID: 72749107868     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2009.10.023     Document Type: Article

References (39)

1. Aden U., Leverin A.L., Hagberg H., and Fredholm B.B. Adenosine A(1) receptor agonism in the immature rat brain and heart. Eur. J. Pharmacol. 426 (2001) 185-192
2. 2A knockout mice. Stroke 34 (2003) 739-744
3. Alvarez F.J., Lafuente H., Rey-Santano M.C., Mielgo V.E., Gastiasoro E., Rueda M., Pertwee R.G., Castillo A.I., Romero J., and Martinez-Orgado J. Neuroprotective effects of the non-psychoactive cannabinoid cannabidiol in hypoxic-ischemic newbornpiglets. Pediatr. Res. 64 (2008) 653-658
4. 2 receptor as a target for inflammation-dependent neurodegeneration. Curr. Neuropharmacol. 5 (2007) 73-80
5. 2 receptor in the brain. Neurosci. Lett. 412 (2007) 114-117
6. Bona E., Aden U., Gilland E., Fredholm B.B., and Hagberg H. Neonatal cerebral hypoxia-ischemia: the effect of adenosine receptor antagonists. Neuropharmacology 36 (1997) 1327-1338
7. 3 adenosine receptor: pharmacology and role in disease. Handb. Exp. Pharmacol. 193 (2009) 297-327
8. Braida D., Pegorini S., Arcidiacono M.V., Consalez G.G., Croci L., and Sala M. Post-ischemic treatment with cannabidiol prevents electroencephalographic flattening, hyperlocomotion and neuronal injury in gerbils. Neurosci. Lett. 346 (2003) 61-64
9. Carrier E.J., Auchampach J.A., and Hillard C.J. Inhibition of an equilibrative nucleoside transporter by cannabidiol: a mechanism of cannabinoid immunosuppression. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 7895-7900
10. 2A receptors and brain injury: broad spectrum of neuroprotection, multifaceted actions and "fine tuning" modulation. Prog. Neurobiol. 83 (2007) 310-331
11. de Mendonca A., Sebastiao A.M., and Ribeiro J.A. Adenosine: does it have a neuroprotective effect after all?. Brain Res. Brain Res. Rev. 33 (2000) 258-274
12. Esposito G., De Filippis D., Maiuri M.C., De Stefano D., Carnuccio R., and Iuvone T. Cannabidiol inhibits inducible nitric oxide synthase protein expression and nitric oxide production in beta-amyloid stimulated PC12 neurons through p38 MAP kinase and NF-kappaB involvement. Neurosci. Lett. 399 (2006) 91-95
13. Fernandez-Lopez D., Martinez-Orgado J., Casanova I., Bonet B., Leza J.C., Lorenzo P., Moro M.A., and Lizasoain I. Immature rat brain slices exposed to oxygen-glucose deprivation as an in vitro model of neonatal hypoxic-ischemic encephalopathy. J. Neurosci. Methods 145 (2005) 205-212
14. Fernandez-Lopez D., Martinez-Orgado J., Nunez E., Romero J., Lorenzo P., Moro M.A., and Lizasoain I. Characterization of the neuroprotective effect of the cannabinoid agonist WIN-55212 in an in vitro model of hypoxic-ischemic brain damage in newborn rats. Pediatr. Res. 60 (2006) 169-173
15. Fernandez-Lopez D., Pazos M.R., Tolon R.M., Moro M.A., Romero J., Lizasoain I., and Martinez-Orgado J. The cannabinoid agonist WIN55212 reduces brain damage in an in vivo model of hypoxic-ischemic encephalopathy in newborn rats. Pediatr. Res. 62 (2007) 255-260
16. Ferriero D.M. Neonatal brain injury. N. Engl. J. Med. 351 (2004) 1985-1995
17. Hampson A.J., Grimaldi M., Axelrod J., and Wink D. Cannabidiol and (-)Delta9-tetrahydrocannabinol are neuroprotective antioxidants. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 8268-8273
18. 2a receptor-dependent and independent mechanisms. FASEB J. 14 (2000) 2065-2074
19. Hayakawa K., Mishima K., Nozako M., Hazekawa M., Irie K., Fujioka M., Orito K., Abe K., Hasebe N., Egashira N., Iwasaki K., and Fujiwara M. Delayed treatment with cannabidiol has a cerebroprotective action via a cannabinoid receptor-independent myeloperoxidase-inhibiting mechanism. J. Neurochem. 102 (2007) 1488-1496
20. Hayakawa K., Mishima K., Irie K., Hazekawa M., Mishima S., Fujioka M., Orito K., Egashira N., Katsurabayashi S., Takasaki K., Iwasaki K., and Fujiwara M. Cannabidiol prevents a post-ischemic injury progressively induced by cerebral ischemia via a high-mobility group box 1-inhibiting mechanism. Neuropharmacology 55 (2008) 1280-1286
21. Lee J.K., Won J.S., Singh A.K., and Singh I. Adenosine kinase inhibitor attenuates the expression of inducible nitric oxide synthase in glial cells. Neuropharmacology 48 (2005) 151-160
22. Ligresti A., Moriello A.S., Starowicz K., Matias I., Pisanti S., De Petrocellis L., Laezza C., Portella G., Bifulco M., and Di Marzo V. Antitumor activity of plant cannabinoids with emphasis on the effect of cannabidiol on human breast carcinoma. J. Pharmacol. Exp. Ther. 318 (2006) 1375-1387
23. Martinez-Orgado J., Fernandez-Lopez D., Moro M.A., and Lizasoain I. Nitric oxide synthase as a target for the prevention of hypoxic-ischemic newborn brain damage. Curr. Enzym. Inhib 2 (2006) 219-229
24. Martinez-Orgado J., Fernandez-Lopez D., Lizasoain I., and Romero J. The seek of neuroprotection: introducing cannabinoids. Recent Patents CNS Drug Discov. 2 (2007) 131-139
25. Mechoulam R., Peters M., Murillo-Rodriguez E., and Hanus L.O. Cannabidiol-recent advances. Chem. Biodivers. 4 (2007) 1678-1692
26. Mereu G., Fa M., Ferraro L., Cagiano R., Antonelli T., Tattoli M., Ghiglieri V., Tanganelli S., Gessa G.L., and Cuomo V. Prenatal exposure to a cannabinoid agonist produces memory deficits linked to dysfunction in hippocampal long-term potentiation and glutamate release. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 4915-4920
27. 2A receptor antagonist SCH 58621 on cyclooxygenase-2 expression, glial activation, and brain-derived neurotrophic factor availability in a rat model of striatal neurodegeneration. J. Neuropathol. Exp. Neurol. 66 (2007) 363-371
28. 1A receptor-dependent mechanism. Stroke 36 (2005) 1077-1082
29. 2 receptors in the inhibitory effects of cannabinoids on lipopolysaccharide-induced nitric oxide release in astrocyte cultures. J. Neurosci. Res. 67 (2002) 829-836
30. Pertwee R.G. The pharmacology and therapeutic potential of cannabidiol. In: Di Marzo V. (Ed). Cannbinoids (2004), Kluwer AcademicPlenum Publishers 32-83
31. 2 receptor pharmacology of three plant cannabinoids: delta9-tetrahydrocannabinol, cannabidiol and delta9-tetrahydrocannabivarin. Br. J. Pharmacol. 153 (2008) 199-215
32. Rudolphi K.A., Schubert P., Parkinson F.E., and Fredholm B.B. Adenosine and brain ischemia. Cerebrovasc. Brain Metab Rev. 4 (1992) 346-369
33. Sacerdote P., Martucci C., Vaccani A., Bariselli F., Panerai A.E., Colombo A., Parolaro D., and Massi P. The nonpsychoactive component of marijuana cannabidiol modulates chemotaxis and IL-10 and IL-12 production of murine macrophages both in vivo and in vitro. J. Neuroimmunol. 159 (2005) 97-105
34. 2A receptors. Eur. J. Neurosci. 26 (2007) 843-851
35. Tian J., Kim S.F., Hester L., and Snyder S.H. S-nitrosylation/activation of COX-2 mediates NMDA neurotoxicity. Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 10537-10540
36. Troy C.M., and Salvesen G.S. Caspases on the brain. J. Neurosci. Res. 69 (2002) 145-150
37. Turkanis S.A., and Karler R. Changes in neurotrasmitter release at a neuromuscular junction of the lobster caused by cannabinoids. Neuropharmacology 27 (1988) 737-742
38. Vesce S., Rossi D., Brambilla L., and Volterra A. Glutamate release from astrocytes in physiological conditions and in neurodegenerative disorders characterized by neuroinflammation. Int. Rev. Neurobiol. 82 (2007) 57-71
39. Zhang M., Martin B.R., Adler M.W., Razdan R.K., Jallo J.I., and Tuma R.F. Cannabinoid CB(2) receptor activation decreases cerebral infarction in a mouse focal ischemia/reperfusion model. J. Cereb. Blood Flow Metab. 27 (2007) 1387-1396