Cannabinoids and neuroprotection in Basal ganglia disorders

Molecular Neurobiology

Volumn 36, Issue 1, 2007, Pages 82-91

  Sagredo, Onintza ^a,b   García Arencibia, Moisés ^a,b   De Lago, Eva ^a,b   Finetti, Simone ^a   Decio, Alessandra ^a   Fernández Ruiz, Javier ^a,b  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

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

Author keywords

Basal ganglia; Cannabinoid signaling system; Cannabinoids; Huntington's disease; Neurodegeneration; Neuroprotection; Parkinson's disease

Indexed keywords

5 (4 CHLORO 3 METHYLPHENYL) 1 (4 METHYLBENZYL) N (1,3,3 TRIMETHYLBICYCLO[2.2.1]HEPTAN 2 YL) 3 PYRAZOLECARBOXAMIDE; ANANDAMIDE; CANNABINOID; CANNABINOID 1 RECEPTOR AGONIST; CANNABINOID 1 RECEPTOR ANTAGONIST; CANNABINOID 2 RECEPTOR; CANNABINOID RECEPTOR ANTAGONIST; DEXANABINOL; LEVODOPA; N (3 FURYLMETHYL)ARACHIDONAMIDE; N (4 HYDROXYPHENYL)ARACHIDONAMIDE; RIMONABANT; NEUROPROTECTIVE AGENT;

BRAIN BLOOD FLOW; CALCIUM TRANSPORT; CELL SURVIVAL; CONFERENCE PAPER; DISEASE COURSE; DRUG MECHANISM; HUMAN; HUNTINGTON CHOREA; NERVE CELL; NEUROPROTECTION; NONHUMAN; PARKINSON DISEASE; UPREGULATION; ANIMAL; DRUG EFFECT; EXTRAPYRAMIDAL SYNDROME; PATHOLOGY; REVIEW;

ANIMALS; BASAL GANGLIA DISEASES; CANNABINOIDS; HUMANS; HUNTINGTON DISEASE; NEURONS; NEUROPROTECTIVE AGENTS; PARKINSON DISEASE;

EID: 38449120611     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-007-0004-3     Document Type: Review

References (79)

1. Marsicano G, Lutz B (2006) Neuromodulatory functions of the endocannabinoid system J Endocrinol Invest 29:27-46
2. Fernández-Ruiz J, González S (2005) Cannabinoid control of motor function at the basal ganglia. Handb Exp Pharmacol 168:479-507
3. van der Stelt M, Di Marzo V (2003) The endocannabinoid system in the basal ganglia and in the mesolimbic reward system: implications for neurological and psychiatric disorders. Eur J Pharmacol 480:133-150
4. Romero J, Lastres-Becker I, de Miguel R, Berrendero F, Ramos JA, Fernández-Ruiz JJ (2002) The endogenous cannabinoid system and the basal ganglia: biochemical, pharmacological and therapeutic aspects. Pharmacol Ther 95:137-152 (Pubitemid 35232132)
5. Giuffrida A, Piomelli D (2000) The endocannabinoid system: a physiological perspective on its role in psychomotor control. Chem Phys Lipids 108:151-158
6. Fernández-Ruiz J, González S, Romero J, Ramos JA (2005) Cannabinoids in neurodegeneration and neuroprotection. In:Mechoulam R (ed) Cannabinoids as therapeutics (MDT). Birkhaüser, Switzerland, pp79-109
7. Lastres-Becker I, Hansen HH, Berrendero F, de Miguel R, Pérez- Rosado A, Manzanares J, Ramos JA, Fernández-Ruiz J (2002) Loss of cannabinoid CB1 receptors and alleviation of motor hyperactivity and neurochemical deficits by endocannabinoid uptake inhibition in a rat model of Huntington's disease. Synapse 44:23-35 (Pubitemid 34174375)
8. Lastres-Becker I, de Miguel R, De Petrocellis L, Makriyannis A, Di Marzo V, Fernández-Ruiz J (2003) Compounds acting at the endocannabinoid and/or endovanilloid systems reduce hyperkinesia in a rat model of Huntington's disease. J Neurochem 84:1097-1109 (Pubitemid 36330662)
9. Fernández-Espejo E, Caraballo I, Rodríguez de Fonseca F, El Banoua F, Ferrer B, Flores JA, Galán-Rodríguez B (2005) Cannabinoid CB1 antagonists possess antiparkinsonian efficacy only in rats with very severe nigral lesion in experimental parkinsonism. Neurobiol Dis 18:591-601
10. González S, Scorticati C, García-Arencibia M, de Miguel R, Ramos JA, Fernández-Ruiz J (2006) Effects of rimonabant, a selective cannabinoid CB1 receptor antagonist, in a rat model of Parkinson's disease. Brain Res 1073-1074:209-219
11. Mechoulam R, Panikashivili A, Shohami E (2002) Cannabinoids and brain injury: therapeutic implications. Trends Mol Med 8:58-61 (Pubitemid 34094440)
12. Grundy RI (2002) The therapeutic potential of the cannabinoids in neuroprotection. Expert Opin Investig Drugs 11:1-10
13. Akwa Y, Allain H, Bentue-Ferrer D, Berr C, Bordet R, Geerts H, Nieoullon A, Onteniente B, Vercelletto M (2005) Neuroprotection and neurodegenerative diseases: from biology to clinical practice. Alzheimer Dis Assoc Disord 19:226-239 (Pubitemid 44366624)
14. Guzmán M, Sánchez C, Galve-Roperh I (2001) Control of the cell survival/death decision by cannabinoids. J Mol Med 78:613-625
15. Fernández-Ruiz J, Romero J, Velasco G, Tolón RM, Ramos JA, Guzmán M (2007) Cannabinoid CB2 receptor: a new target for the control of neural cell survival? Trends Pharmacol Sci 28:39-45
16. Hansen HS, Moesgaard B, Petersen G, Hansen HH (2002) Putative neuroprotective actions of N-acyl-ethanolamines. Pharmacol Ther 95:119-126 (Pubitemid 35232130)
17. van der Stelt M, Veldhuis WB, Maccarrone M, Bar PR, Nicolay K, Veldink GA, Di Marzo V, Vliegenthart JF (2002) Acute neuronal injury, excitotoxicity, and the endocannabinoid system. Mol Neurobiol 26:317-346 (Pubitemid 35239807)
18. Hansen HS, Moesgaard B, Hansen HH, Schousboe A, Petersen G (1999) Formation of N-acyl-phosphatidylethanolamine and N-acylethanolamine (including anandamide) during glutamateinduced neurotoxicity. Lipids 34:S327-S330
19. Hansen HH, Schmid PC, Bittigau P, Lastres-Becker I, Berrendero F, Manzanares J, Ikonomidou C, Schmid HH, Fernandez-Ruiz JJ, Hansen HS (2001) Anandamide, but not 2-arachidonoylglycerol, accumulates during in vivo neurodegeneration. J Neurochem 78:1415-1427 (Pubitemid 32899773)
20. Marsicano G, Goodenough S, Monory K, Hermann H, Eder M, Cannich A, Azad SC, Cascio MG, Gutierrez SO, van der Stelt M, Lopez-Rodriguez ML, Casanova E, Schutz G, Zieglgansberger W, Di Marzo V, Behl C, Lutz B (2003) CB1 cannabinoid receptors and on-demand defense against excitotoxicity. Science 302:84-88 (Pubitemid 37210691)
21. Gubellini P, Picconi B, Bari M, Battista N, Calabresi P, Centonze D, Bernardi G, Finazzi-Agrò A, Maccarrone M (2002) Experimental parkinsonism alters endocannabinoid degradation: implications for striatal glutamatergic transmission. J Neurosci 22:6900-6907 (Pubitemid 35379148)
22. Panikashvili D, Simeonidou C, Ben-Shabat S, Hanus L, Breuer A, Mechoulam R, Shohami E (2001) An endogenous cannabinoid (2-AG) is neuroprotective after brain injury. Nature 413:527-531 (Pubitemid 32938751)
23. Schabitz WR, Giuffrida A, Berger C, Aschoff A, Schwaninger M, Schwab S, Piomelli D (2002) Release of fatty acid amides in a patient with hemispheric stroke: a microdialysis study. Stroke 33:2112-2124
24. van der Stelt M, VeldhuisWB, van Haaften GW, Fezza F, Bisogno T, Bär PR, Veldink GA, Vliegenthart JF, Di Marzo V, Nicolay K (2001) Exogenous anandamide protects rat brain against acute neuronal injury in vivo. J Neurosci 21:8765-8771 (Pubitemid 33054840)
25. Jin KL, Mao XO, Goldsmith PC, Greenberg DA (2000) CB1 cannabinoid receptor induction in experimental stroke. Ann Neurol 48:257-261 (Pubitemid 30617047)
26. Benito C, Nuñez E, Tolon RM, Carrier EJ, Rabano A, Hillard CJ, Romero J. (2003) Cannabinoid CB2 receptors and fatty acid amide hydrolase are selectively overexpressed in neuritic plaqueassociated glia in Alzheimer's disease brains. J Neurosci 23:11136-11141 (Pubitemid 37548949)
27. Veldhuis WB, van der Stelt M, Wadman MW, van Zadelhoff G, Maccarrone M, Fezza F, Veldink GA, Vliegenthart JF, Bar PR, Nicolay K, Di Marzo V (2003) Neuroprotection by the endogenous cannabinoid anandamide and arvanil against in vivo excitotoxicity in the rat: role of vanilloid receptors and lipoxygenases. J Neurosci 23:4127-4133 (Pubitemid 36958432)
28. Shen M, Thayer SA (1998) Cannabinoid receptor agonists protect cultured rat hippocampal neurons from excitotoxicity. Mol Pharmacol 54:459-462 (Pubitemid 28442938)
29. AboodME, Rizvi G, Sallapudi N, McAllister SD (2001) Activation of the CB1 cannabinoid receptor protects cultured mouse spinal neurons against excitotoxicity. Neurosci Lett 309:197-201 (Pubitemid 32763173)
30. Nagayama T, Sinor AD, Simon RP, Chen J, Graham SH, Jin KL, Greenberg DA (1999) Cannabinoids and neuroprotection in global and focal cerebral ischemia and in neuronal cultures. J Neurosci 19:2987-2995 (Pubitemid 29173995)
31. Schlicker E, KathmannM(2001) Modulation of transmitter release via presynaptic cannabinoid receptors. Trends Pharmacol Sci 22:565-572 (Pubitemid 33042646)
32. Lastres-Becker I, Bizat N, Boyer F, Hantraye P, Brouillet E, Fernández-Ruiz J (2003) Effects of cannabinoids in the rat model of Huntington's disease generated by an intrastriatal injection of malonate. Neuroreport 14:813-816 (Pubitemid 36667917)
33. Hansen HH, Azcoitia I, Pons S, Romero J, Garcia-Segura LM, Ramos JA, Hansen HS, Fernandez-Ruiz J (2002) Blockade of cannabinoid CB1 receptor function protects against in vivo disseminating brain damage following NMDA-induced excitotoxicity. J Neurochem 82:154-158 (Pubitemid 34755260)
34. Shohami E, Mechoulam R (2000) A non-psychotropic cannabinoid with neuroprotective properties. Drug Dev Res 50:211-215
35. Hampson AJ, Bornheim LM, Scanziani M, Yost CS, Gray AT, Hansen BM, Leonoudakis DJ, Bickler PE (1998) Dual effects of anandamide on NMDA receptor-mediated responses and neurotransmission. J Neurochem 70:671-676 (Pubitemid 28079356)
36. Demuth DG, Molleman A (2006) Cannabinoid signalling. Life Sci 78:549-563 (Pubitemid 41785760)
37. Fowler CJ (2003) Plant-derived, synthetic and endogenous cannabinoids as neuroprotective agents. Non-psychoactive cannabinoids, 'entourage' compounds and inhibitors of N-acyl ethanolamine breakdown as therapeutic strategies to avoid pyschotropic effects. Brain Res Rev 41:26-43
38. Wagner JA, Varga K, Kunos G (1998) Cardiovascular actions of cannabinoids and their generation during shock. J Mol Med 76:824-836 (Pubitemid 28518708)
39. Randall MD, Harris D, Kendall DA, Ralevic V (2002) Cardiovascular effects of cannabinoids. Pharmacol Ther 95:191-202 (Pubitemid 35232137)
40. Chen Y, McCarron RM, Ohara Y, Bembry J, Azzam N, Lenz FA, Shohami E, Mechoulam R, Spatz M (2000) Human brain capillary endothelium: 2-arachidonoglycerol (endocannabinoid) interacts with endothelin-1. Circ Res 87:323-327 (Pubitemid 30655974)
41. Begg M, Pacher P, Batkai S, Osei-Hyiaman D, Offertaler L, Mo FM, Liu J, Kunos G (2005) Evidence for novel cannabinoid receptors. Pharmacol Ther 106:133-145 (Pubitemid 40613055)
42. Stella N (2004) Cannabinoid signaling in glial cells. Glia 48:267-277
43. Walter L, Stella N (2004) Cannabinoids and neuroinflammation. Br J Pharmacol 141:775-785 (Pubitemid 38446178)
44. Smith SR, Terminelli C, Denhardt G (2000) Effects of cannabinoid receptor agonist and antagonist ligands on production of inflammatory cytokines and anti-inflammatory interleukin-10 in endotoxemic mice. J Pharmacol Exp Ther 293:136-150 (Pubitemid 30180933)
45. Molina-Holgado F, Pinteaux E,Moore JD,Molina-Holgado E,Guaza C, Gibson RM, Rothwell NJ (2003) Endogenous interleukin-1 receptor antagonist mediates anti-inflammatory and neuroprotective actions of cannabinoids in neurons and glia. J Neurosci 23:6470-6474 (Pubitemid 36909872)
46. Guzman M, Sanchez C (1999) Effects of cannabinoids on energy metabolism. Life Sci 65:657-664 (Pubitemid 29362771)
47. Marsicano G, Moosmann B, Hermann H, Lutz B, Behl C (2002) Neuroprotective properties of cannabinoids against oxidative stress: role of the cannabinoid receptor CB1. J Neurochem 80:448-456 (Pubitemid 36383028)
48. Eshhar N, Striem S, Kohen R, Tirosh O, Biegon A (1995) Neuroprotective and antioxidant activities of HU-211, a novel NMDA receptor antagonist. Eur J Pharmacol 283:19-29
49. 9-tetrahydrocannabinol are neuroprotective antioxidants. Proc Natl Acad Sci U S A 95:8268-8273
50. Chen Y, Buck J (2000) Cannabinoids protect cells from oxidative cell death: a receptor-independent mechanism. J Pharmacol Exp Ther 293:807-812 (Pubitemid 30417845)
51. García-ArencibiaM, González S, de Lago E, Ramos JA, Mechoulam R, Fernández-Ruiz J (2007) Evaluation of the neuroprotective effect of cannabinoids in a rat model of Parkinson's disease: importance of antioxidant and cannabinoid receptor-independent properties. Brain Res 1134:162-170
52. Sagredo O, Ramos JA, Decio A, Mechoulam R, Fernández-Ruiz J (2007) Cannabidiol reduced the striatal atrophy caused 3-nitropropionic acid in vivo by mechanisms independent of the activation of cannabinoid receptors. Eur J Neurosci (in press)
53. Borrell-Pages M, Zala D, Humbert S, Saudou F (2006) Huntington's disease: from huntingtin function and dysfunction to therapeutic strategies. Cell Mol Life Sci 63:2642-2660 (Pubitemid 44800717)
54. Herkenham M, Lynn AB, Little MD, Melvin LS, Johnson MR, de Costa DR, Rice KC (1991) Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J Neurosci 11:563-583
55. Lastres-Becker I, De Miguel R, Fernández-Ruiz J (2003) The endocannabinoid system and Huntington's disease. Curr Drug Target CNS Neurol Disord 2:335-347
56. Lastres-Becker I, Bizat N, Boyer F, Hantraye P, Fernández-Ruiz JJ, Brouillet E (2004) Potential involvement of cannabinoid receptors in 3-nitropropionic acid toxicity in vivo: implication for Huntington's disease. Neuroreport 15:2375-2379 (Pubitemid 39488923)
57. Pintor A, Tebano MT, Martire A, Grieco R, Galluzzo M, Scattoni ML, Pezzola A, Coccurello R, Felici F, Cuomo V, Piomelli D, Calamandrei G, Popoli P (2006) The cannabinoid receptor agonist WIN 55,212-2 attenuates the effects induced by quinolinic acid in the rat striatum. Neuropharmacology 51:1004-1012 (Pubitemid 44528606)
58. Glass M, Dragunow M, Faull RLM (2000) The pattern of neurodegeneration in Huntington's disease: a comparative study of cannabinoid, dopamine, adenosine and GABA-A receptor alterations in the human basal ganglia in Huntington's disease. Neuroscience 97:505-519 (Pubitemid 30320757)
59. Lastres-Becker I, Berrendero F, Lucas JJ, Martin E, Yamamoto A, Ramos JA, Fernández-Ruiz J (2002) Loss of mRNA levels, binding and activation of GTP-binding proteins for cannabinoid CB1 receptors in the basal ganglia of a transgenic model of Huntington's disease. Brain Res 929:236-242 (Pubitemid 34178339)
60. Denovan-Wright EM, Robertson HA (2000) Cannabinoid receptor messenger RNA levels decrease in subset neurons of the lateral striatum, cortex and hippocampus of transgenic Huntington's disease mice. Neuroscience 98:705-713 (Pubitemid 30417587)
61. Aiken CT, Tobin AJ, Schweitzer ES (2004) A cell-based screen for drugs to treat Huntington's disease. Neurobiol Dis 16:546-555 (Pubitemid 38942987)
62. Wang W, Duan W, Igarashi S, Morita H, Nakamura M, Ross CA (2005) Compounds blocking mutant huntingtin toxicity identified using a Huntington's disease neuronal cell model. Neurobiol Dis 20:500-508 (Pubitemid 41476276)
63. Gu M, Gash MT, Mann VM, Javoy-Agid F, Cooper JM, Schapira AH (1996) Mitochondrial defect in Huntington's disease caudate nucleus. Ann Neurol 39:385-389 (Pubitemid 26100764)
64. Bizat N, Hermel JM, Humbert S, Jacquard C, Creminon C, Escartin C, Saudou F, Krajewski S, Hantraye P, Brouillet E (2003) Invivocalpain/caspasecross- talkduring3-nitropropionicacid-induced striatal degeneration: implication of a calpain-mediated cleavage of activecaspase-3.JBiolChem278:43245-43253 (Pubitemid 37345944)
65. Galas MC, Bizat N, Cuvelier L, Bantubungi K, Brouillet E, Schiffmann SN, Blum D (2004) Death of cortical and striatal neurons induced by mitochondrial defect involves differential molecular mechanisms. Neurobiol Dis 15:152-159 (Pubitemid 38134390)
66. Toulmond S, Tang K, BureauY, Ashdown H,Degen S,O'Donnell R, Tam J, Han Y, Colucci J, Giroux A, Zhu Y, Boucher M, Pikounis B, Xanthoudakis S, Roy S, Rigby M, Zamboni R, Robertson GS, Ng GY, Nicholson DW, Fluckiger JP (2004) Neuroprotective effects of M826, a reversible caspase-3 inhibitor, in the rat malonate model of Huntington's disease. Br J Pharmacol 141:689-697 (Pubitemid 38453261)
67. Sapp E, Kegel KB, Aronin N, Hashikawa T, Uchiyama Y, Tohyama K, Bhide PG, Vonsattel JP, DiFiglia M (2001) Early and progressive accumulation of reactive microglia in the Huntington disease brain. J Neuropathol Exp Neurol 60:161-172 (Pubitemid 32172419)
68. Rajkowska G, Selemon LD, Goldman-Rakic PS (1998) Neuronal and glial somal size in the prefrontal cortex: a postmortem morphometric study of schizophrenia and Huntington disease. Arch Gen Psychiatry 55:215-224
69. Blandini F, Nappi G, Tassorelli C, Martignoni E (2000) Functional changes in the basal ganglia circuitry in Parkinson's disease. Prog Neurobiol 62:63-88 (Pubitemid 30252017)
70. McGeer PL, Yasojima K, McGeer EG (2001) Inflammation in Parkinson's disease. Adv Neurol 86:83-89
71. Sherer TB, Betarbet R, Greenamyre JT (2001) Pathogenesis of Parkinson's disease. Curr Opin Investig Drugs 2:657-662 (Pubitemid 32509687)
72. Sethi KD (2002) Clinical aspects of Parkinson disease. Curr Opin Neurol 15:457-460
73. Carlsson A (2002) Treatment of Parkinson's with L-DOPA. The early discovery phase, and a comment on current problems. J Neural Transm 109:777-787
74. Consroe P (1998) Brain cannabinoid systems as targets for the therapy of neurological disorders. Neurobiol Dis 5:534-551
75. Müller-Vahl KR, Kolbe H, Schneider U, Emrich HM (1999). Cannabis in movement disorders. Forsch Komplementmed 6:23-27
76. Lastres-Becker I, Molina-Holgado F, Ramos JA, Mechoulam R, Fernández-Ruiz J (2005) Cannabinoids provide neuroprotection against 6-hydroxydopamine toxicity in vivo and in vitro: relevance to Parkinson's disease. Neurobiol Dis 19:96-107 (Pubitemid 40544727)
77. Gao HM, Jiang J, Wilson B, Zhang W, Hong JS, Liu B (2002) Microglial activation-mediated delayed and progressive degeneration of rat nigral dopaminergic neurons: relevance to Parkinson's disease. J Neurochem 81:1285-1297 (Pubitemid 34809262)
78. Kim WG, Mohney RP, Wilson B, Jeohn GH, Liu B, Hong JS (2000) Regional difference in susceptibility to lipopolysaccharideinduced neurotoxicity in the rat brain: role of microglia. J Neurosci 20:6309-6316 (Pubitemid 30658427)
79. Nagatsu T, Mogi M, Ichinose H, Togari A (2000) Changes in cytokines and neurotrophins in Parkinson's disease. J Neural Transm 60:277-290 (Pubitemid 32037200)