Evaluation of the neuroprotective effect of cannabinoids in a rat model of Parkinson's disease: Importance of antioxidant and cannabinoid receptor-independent properties

Brain Research

Volumn 1134, Issue 1, 2007, Pages 162-170

  García Arencibia, Moisés ^a   González, Sara ^a   de Lago, Eva ^a   Ramos, José A ^a   Mechoulam, Raphael ^b   Fernández Ruiz, Javier ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

6 Hydroxydopamine; Antioxidant property; Basal ganglia; Cannabinoid; Neurodegeneration; Neuroprotection; Parkinson's disease

Indexed keywords

2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; 4 [4 (1,1 DIMETHYLHEPTYL) 2,6 DIMETHOXYPHENYL] 6,6 DIMETHYLBICYCLO[3.1.1] HEPT 2 EN 2 YLMETHANOL; 4 [4 (1,1 DIMETHYLHEPTYL) 2,6 DIMETHOXYPHENYL] 6,6 DIMETHYLBICYCLO[3.1.1]HEPT 2 EN 2 YLMETHANOL; ANTIOXIDANT; ARACHIDONYL 2 CHLOROETHYLAMIDE; CANNABIDIOL; CANNABINOID; CANNABINOID 2 RECEPTOR; CANNABINOID RECEPTOR; CANNABINOID RECEPTOR AGONIST; COPPER ZINC SUPEROXIDE DISMUTASE; DOPAMINE; MESSENGER RNA; N (3 FURYLMETHYL)ARACHIDONAMIDE; N (4 HYDROXYPHENYL)ARACHIDONAMIDE; OXIDOPAMINE; TETRAHYDROCANNABINOL; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN DAMAGE; BRAIN DEGENERATION; CONTROLLED STUDY; DOPAMINERGIC SYSTEM; DRUG MECHANISM; NEUROPROTECTION; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; PRIORITY JOURNAL; RAT; RECEPTOR BLOCKING; SIGNAL TRANSDUCTION;

ANIMALS; ANTIOXIDANTS; ARACHIDONIC ACIDS; BENZOXAZINES; CANNABINOIDS; DISEASE MODELS, ANIMAL; DOPAMINE; FURANS; MALE; MORPHOLINES; NAPHTHALENES; NERVE DEGENERATION; NEUROPROTECTIVE AGENTS; ORGAN CULTURE TECHNIQUES; OXIDATIVE STRESS; OXIDOPAMINE; PARKINSONIAN DISORDERS; POLYUNSATURATED ALKAMIDES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, CANNABINOID; SUPEROXIDE DISMUTASE; SYMPATHOLYTICS;

ANIMALIA; RATTUS;

EID: 33846401540     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2006.11.063     Document Type: Article

References (50)

1. Beltramo M., Stella N., Calignano A., Lin S.Y., Makriyannis A., and Piomelli D. Functional role of high-affinity anandamide transport, as revealed by selective inhibition. Science 277 (1997) 1094-1097
2. 2 receptors and fatty acid amide hydrolase are selectively overexpressed in neuritic plaque-associated glia in Alzheimer's disease brains. J. Neurosci. 23 (2003) 11136-11141
3. Bisogno T., Hanus L., De Petrocellis L., Tchilibon S., Ponde D.E., Brandi I., Moriello A.S., Davis J.B., Mechoulam R., and Di Marzo V. Molecular targets for cannabidiol and its synthetic analogues: effects on vanilloid VR1 receptors and on the cellular uptake and enzymatic hydrolysis of anandamide. Br. J. Pharmacol. 134 (2001) 845-852
4. Blum D., Torch S., Lamberg N., Nisson M.-F., Benabid A.-L., Sadou L.R., and Verna J.-M. Molecular pathways involved in the neurotoxicity of 6-OHDA, dopamine and MPTP: contribution to the apoptotic theory in Parkinson's disease. Prog. Neurobiol. 65 (2001) 135-172
5. Chen Y., and Buck J. Cannabinoids protect cells from oxidative cell death: a receptor-independent mechanism. J. Pharmacol. Exp. Ther. 293 (2000) 807-812
6. Clow A., Hussain T., Glover V., Sandler M., Walker M., and Dexter D. Pergolide can induce soluble superoxide dismutase in rat striata. J. Neural Transm. 90 (1992) 27-31
7. de Lago E., Fernández-Ruiz J., Ortega-Gutiérrez S., Viso A., López-Rodríguez M.L., and Ramos J.A. UCM707, a potent and selective inhibitor of endocannabinoid uptake, potentiates hypokinetic and antinociceptive effects of anandamide. Eur. J. Pharmacol. 449 (2002) 99-103
8. de Lago E., Fernández-Ruiz J., Ortega-Gutierrez S., Cabranes A., Pryce G., Baker D., Lopez-Rodriguez M., and Ramos J.A. UCM707, an inhibitor of the anandamide uptake, behaves as a symptom control agent in models of Huntington's disease and multiple sclerosis, but fails to delay/arrest the progression of different motor-related disorders. Eur. Neuropsychopharmacol. 16 (2006) 7-18
9. De Petrocellis L., Bisogno T., Davis J.B., Pertwee R.G., and Di Marzo V. Overlap between the ligand recognition properties of the anandamide transporter and the VR1 vanilloid receptor: inhibitors of anandamide uptake with negligible capsaicin-like activity. FEBS Lett. 483 (2000) 52-56
10. Fernández-Ruiz J., González S., Romero J., and Ramos J.A. Cannabinoids in neurodegeneration and neuroprotection. In: Mechoulam R. (Ed). Cannabinoids as Therapeutics (MDT) (2005), Birkhaüser Verlag, Switzerland 79-109
11. Fernández-Ruiz J., Romero J., Velasco G., Tolón R.M., Ramos J.A., and Guzmán M. Cannabinoid CB2 receptor: a new target for the control of neural cell survival?. Trends Pharmacol. Sci. (2007) doi:10.1016/j.tips.2006.11.001
12. 1-tetrahydrocannabinol and other neutral cannabinoids from hashish. J. Am. Chem. Soc. 93 (1971) 217-224
13. 9-tetrahydrocannabinol exposure did not alter dopamine transporter and tyrosine hydroxylase mRNA levels in midbrain dopaminergic neurons of adult male and female rats. Neurotoxicol. Teratol. 20 (1998) 549-553
14. González S., Romero J., de Miguel R., Lastres-Becker I., Villanua M.A., Makriyannis A., Ramos J.A., and Fernández-Ruiz J.J. Extrapyramidal and neuroendocrine effects of AM404, an inhibitor of the carrier-mediated transport of anandamide. Life Sci. 65 (1999) 327-336
15. 1 receptors in the basal ganglia and motor response to activation or blockade of these receptors in parkin-null mice. Brain Res. 1046 (2005) 195-206
16. Grundy R.I. The therapeutic potential of the cannabinoids in neuroprotection. Expert Opin. Invest. Drugs 11 (2002) 1-10
17. 9-tetrahydrocannabinol are neuroprotective antioxidants. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 8268-8273
18. Hampson A.J., Grimaldi M., Lolic M., Wink D., Rosenthal R., and Axelrod J. Neuroprotective antioxidants from marijuana. Ann. N. Y. Acad. Sci. 899 (2000) 274-282
19. Hanus L., Breuer A., Tchilibon S., Shiloah S., Goldenberg D., Horowitz M., Pertwee R.G., Ross R.A., Mechoulam R., and Fride E. HU-308: a specific agonist for CB(2), a peripheral cannabinoid receptor. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 1433-14228
20. 1). J. Pharmacol. Exp. Ther. 289 (1999) 1427-1433
21. Hogestatt E.D., Jonsson B.A., Ermund A., Andersson D.A., Bjork H., Alexander J.P., Cravatt B.F., Basbaum A.I., and Zygmunt P.M. Conversion of acetaminophen to the bioactive N-acylphenolamine AM404 via fatty acid amide hydrolase-dependent arachidonic acid conjugation in the nervous system. J. Biol. Chem. 280 (2005) 31405-31412
22. Ihara Y., Chuda M., Kuroda S., and Hayabara T. Hydroxyl radical and superoxide dismutase in blood of patients with Parkinson's disease: relationship to clinical data. J. Neurol. Sci. 170 (1999) 90-95
23. Kunikowska G., and Jenner P. 6-Hydroxydopamine-lesioning of the nigrostriatal pathway in rats alters basal ganglia mRNA for copper, zinc- and manganese-superoxide dismutase, but not glutathione peroxidase. Brain Res. 922 (2001) 51-64
24. Lastres-Becker I., Molina-Holgado F., Ramos J.A., Mechoulam R., and Fernández-Ruiz J. Cannabinoids provide neuroprotection against 6-hydroxydopamine toxicity in vivo and in vitro: relevance to Parkinson's disease. Neurobiol. Dis. 19 (2005) 96-107
25. López-Rodríguez M.L., Viso A., Ortega-Gutiérrez S., Fowler C.J., Tiger G., de Lago E., Fernández-Ruiz J., and Ramos J.A. Design, synthesis, and biological evaluation of new inhibitors of the endocannabinoid uptake: comparison with effects on fatty acid amidohydrolase. J. Med. Chem. 46 (2003) 1512-1522
26. 1. J. Neurochem. 80 (2002) 448-456
27. McGeer P.L., Yasojima K., and McGeer E.G. Inflammation in Parkinson's disease. Adv. Neurol. 86 (2001) 83-89
28. Mechoulam R., and Hanus L. Cannabidiol: an overview of some chemical and pharmacological aspects: Part I. Chemical aspects. Chem. Phys. Lipids 121 (2002) 35-43
29. Mechoulam R., Panikashvili A., and Shohami E. Cannabinoids and brain injury: therapeutic implications. Trends Mol. Med. 8 (2002) 58-61
30. Mezey E., Toth Z.E., Cortright D.N., Arzubi M.K., Krause J.E., Elde R., Guo A., Blumberg P.M., and Szallasi A. Distribution of mRNA for vanilloid receptor subtype 1 (VR1), and VR1-like immunoreactivity, in the central nervous system of the rat and human. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 3360-3655
31. Nagatsu T., Oka K., and Kato T. Highly sensitive assay for tyrosine-hydroxylase activity by high-performance liquid chromatography. J. Chromatogr. 163 (1979) 247-252
32. Nishibayashi S., Asanuma M., Kohno M., Gomez-Vargas M., and Ogawa N. Scavenging effects of dopamine agonists on nitric oxide radicals. J. Neurochem. 67 (1996) 2208-2211
33. Noor R., Mittal S., and Iqbal J. Superoxide dismutase-Applications and relevance to human diseases. Med. Sci. Monit. 8 (2002) RA210-RA215
34. Okuno T., Nakatsuji Y., Kumanogoh A., Moriya M., Ichinose H., Sumi H., Fujimura H., Kikutani H., and Sakoda S. Loss of dopaminergic neurons by the induction of inducible nitric oxide synthase and cyclooxygenase-2 via CD 40: relevance to Parkinson's disease. J. Neurosci. Res. 81 (2005) 874-882
35. Palkovits M., and Brownstein J. Maps and Guide to Microdissection of the Rat Brain (1988), Elsevier, New York
36. Patel Y., Collaco Moraes Y., Latchman D., Coffin R., and de Belleroche J. Neuroprotective effects of copper/zinc-dependent superoxide dismutase against a wide variety of death-inducing stimuli and proapoptotic effect of familial amyotrophic lateral sclerosis mutations. Mol. Brain Res. 109 (2002) 189-197
37. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates (1986), Academic Press, London
38. Pegorini S., Braida D., Verzoni C., Guerini-Rocco C., Consalez G.G., Croci L., and Sala M. Capsaicin exhibits neuroprotective effects in a model of transient global cerebral ischemia in Mongolian gerbils. Br. J. Pharmacol. 144 (2005) 727-735
39. Pegorini S., Zani A., Braida D., Guerini-Rocco C., and Sala M. Vanilloid VR1 receptor is involved in rimonabant-induced neuroprotection. Br. J. Pharmacol. 147 (2006) 552-559
40. 2 receptors. Pharmacol. Ther. 74 (1997) 129-180
41. Przedborski S. Pathogenesis of nigral cell death in Parkinson's disease. Parkinsonism Relat. Disord. 11 (2005) S3-S7
42. Ross R.A., Gibson T.M., Brockie H.C., Leslie M., Pashmi G., Craib S.J., Di Marzo V., and Pertwee R.G. Structure-activity relationship for the endogenous cannabinoid, anandamide, and certain of its analogues at vanilloid receptors in transfected cells and vas deferens. Br. J. Pharmacol. 132 (2001) 631-640
43. Schober A. Classic toxin-induced animal models of Parkinson's disease: 6-OHDA and MPTP. Cell Tissue Res. 318 (2004) 215-224
44. Sethi K.D. Clinical aspects of Parkinson disease. Curr. Opin. Neurol. 15 (2002) 457-460
45. Sherer T.B., Betarbet R., and Greenamyre J.T. Pathogenesis of Parkinson's disease. Curr. Opin. Invest. Drugs 2 (2001) 657-662
46. Teismann P., Tieu K., Choi D.K., Wu D.C., Naini A., Hunot S., Vila M., Jackson-Lewis V., and Przedborski S. Cyclooxygenase-2 is instrumental in Parkinson's disease neurodegeneration. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 5473-5478
47. Vajda F.J. Neuroprotection and neurodegenerative disease. J. Clin. Neurosci. 9 (2002) 4-8
48. Veldhuis W.B., van der Stelt M., Wadman M.W., van Zadelhoff G., Maccarrone M., Fezza F., Veldink G.A., Vliegenthart J.F., Bar P.R., Nicolay K., and Di Marzo V. Neuroprotection by the endogenous cannabinoid anandamide and arvanil against in vivo excitotoxicity in the rat: role of vanilloid receptors and lipoxygenases. J. Neurosci. 23 (2003) 4127-4133
49. Walter L., Franklin A., Witting A., Wade C., Xie Y., Kunos G., Mackie K., and Stella N. Nonpsychotropic cannabinoid receptors regulate microglial cell migration. J. Neurosci. 23 (2003) 1398-1405
50. Zygmunt P.M., Chuang H., Movahed P., Julius D., and Hogestatt E.D. The anandamide transport inhibitor AM404 activates vanilloid receptors. Eur. J. Pharmacol. 396 (2000) 39-42