Natural cannabinoids improve dopamine neurotransmission and tau and amyloid pathology in a mouse model of tauopathy

Journal of Alzheimer's Disease

Volumn 35, Issue 3, 2013, Pages 525-539

  Casarejos, Maria J ^a,c   Perucho, Juan ^a,c   Gomez, Ana ^a,c   Muñoz, Maria P ^a,c   Fernandez Estevez, Marian ^a,c   Sagredo, Onintza ^b,c   Fernandez Ruiz, Javier ^b,c   Guzman, Manuel ^b,c   De Yebenes, Justo Garcia ^a,c   Mena, Maria A ^a,c  

^a HOSPITAL RAMÓN Y CAJAL   (Spain)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

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

Author keywords

Amyloid; autophagy; cannabinoids; dopamine; frontotemporal dementia; lower motor neuron disease; parkin; parkinsonism; reactive oxygen species; Sativex regd ; tau

Indexed keywords

CANNABINOID; DOPAMINE; NABIXIMOLS; TAU PROTEIN;

ABNORMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; BRAIN CORTEX; CONTROLLED STUDY; DOPAMINE METABOLISM; FRONTOTEMPORAL DEMENTIA; GLIOSIS; HIPPOCAMPUS; LIMBIC SYSTEM; MOTOR NEURON DISEASE; MOUSE; NEUROTRANSMISSION; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PARKINSONISM; PHENOTYPE; PRIORITY JOURNAL; PROTEIN METABOLISM; STEREOTYPY; TAUOPATHY;

EID: 84880208269     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-130050     Document Type: Article

References (57)

1. Blazquez C, Chiarlone A, Sagredo O, Aguado T, Pazos MR, Resel E, Palazuelos J, Julien B, Salazar M, Borner C, Benito C, Carrasco C, Diez-Zaera M, Paoletti P, Diaz-Hernandez M, Ruiz C, Sendtner M, Lucas JJ, de Yebenes JG, Marsicano G, Monory K, Lutz B, Romero J, Alberch J, Gines S, Kraus J, Fernandez-Ruiz J, Galve-Roperh I, Guzman M (2011) Loss of striatal type 1 cannabinoid receptors is a key pathogenic factor in Huntington's disease. Brain 134, 119-136.
2. Chen B, Bromley-Brits K, He G, Cai F, Zhang X, Song W (2010) Effect of synthetic cannabinoid HU210 on memory deficits and neuropathology in Alzheimer's disease mouse model. Curr Alzheimer Res 7, 255-261.
3. Fernandez-Ruiz J, Hernandez M, Ramos JA (2010) Cannabinoid-dopamine interaction in the pathophysiology and treatment of CNS disorders. CNS Neurosci Ther 16, e72-e91.
4. Fernandez-Ruiz J, Moreno-Martet M, Rodriguez-Cueto C, Palomo-Garo C, Gomez-Canas M, Valdeolivas S, Guaza C, Romero J, Guzman M, Mechoulam R, Ramos JA (2011) Prospects for cannabinoid therapies in basal ganglia disorders. Br J Pharmacol 163, 1365-1378.
5. Kalifa S, Polston EK, Allard JS, Manaye KF (2010) Distribution patterns of cannabinoid CB1 receptors in the hippocampus of APPswe/PS1DeltaE9 double transgenic mice. Brain Res 1376, 94-100.
6. Koppel J, Bradshaw H, Goldberg TE, Khalili H, Marambaud P, Walker MJ, Pazos M, Gordon ML, Christen E, Davies P (2009) Endocannabinoids in Alzheimer's disease and their impact on normative cognitive performance: A case-control and cohort study. Lipids Health Dis 8, 2.
7. Koppel J, Davies P (2008) Targeting the endocannabinoid system in Alzheimer's disease. J Alzheimers Dis 15, 495-504.
8. Krishnan S, Cairns R, Howard R (2009) Cannabinoids for the treatment of dementia. Cochrane Database Syst Rev, CD007204.
9. Lee JH, Agacinski G, Williams JH, Wilcock GK, Esiri MM, Francis PT, Wong PT, Chen CP, Lai MK (2010) Intact cannabinoid CB1 receptors in the Alzheimer's disease cortex. Neurochem Int 57, 985-989.
10. Martin-Moreno AM, Reigada D, Ramirez BG, Mechoulam R, Innamorato N, Cuadrado A, de Ceballos ML (2011) Cannabidiol and other cannabinoids reduce microglial activation in vitro and in vivo: Relevance to Alzheimer's disease. Mol Pharmacol 79, 964-973.
11. Noonan J, Tanveer R, Klompas A, Gowran A, McKiernan J, Campbell VA (2010) Endocannabinoids prevent beta-amyloid-mediated lysosomal destabilization in cultured neurons. J Biol Chem 285, 38543-38554.
12. Marco EM, Laviola G (2011) The endocannabinoid system in the regulation of emotions throughout lifespan: A discussion on therapeutic perspectives. J Psychopharmacol 26, 150-163.
13. Pazos MR, Nunez E, Benito C, Tolon RM, Romero J (2004) Role of the endocannabinoid system in Alzheimer's disease: New perspectives. Life Sci 75, 1907-1915.
14. Ramirez BG, Blazquez C, Gomez del Pulgar T, Guzman M, de Ceballos ML (2005) Prevention of Alzheimer's disease pathology by cannabinoids: Neuroprotection mediated by blockade of microglial activation. J Neurosci 25, 1904-1913.
15. Ruiz-Valdepenas L, Benito C, Tolon RM, Martinez Orgado JA, Romero J (2010) The endocannabinoid system and amyloid-related diseases. Exp Neurol 224, 66-73.
16. Ruiz-Valdepenas L, Martinez-Orgado JA, Benito C, Millan A, Tolon RM, Romero J (2011) Cannabidiol reduces lipopolysaccharide-induced vascular changes and inflammation in the mouse brain: An intravital microscopy study. J Neuroinflammation 8, 5.
17. Sagredo O, Pazos MR, Satta V, Ramos JA, Pertwee RG, Fernandez-Ruiz J (2011) Neuroprotective effects of phytocannabinoid-based medicines in experimental models of Huntington's disease. J Neurosci Res 89, 1509-1518.
18. Tolon RM, Nunez E, Pazos MR, Benito C, Castillo AI, Martinez-Orgado JA, Romero J (2009) The activation of cannabinoid CB2 receptors stimulates in situ and in vitro betaamyloid removal by human macrophages. Brain Res 1283, 148-154.
19. Palazuelos J, Ortega Z, Diaz-Alonso J, Guzman M, Galve-Roperh I (2012) CB2 cannabinoid receptors promote neural progenitor cell proliferation via mTORC1 signaling. J Biol Chem 287, 1198-1209.
20. Anavi-Goffer S, Baillie G, Irving AJ, Gertsch J, Greig IR, Pertwee RG, Ross RA (2012) Modulation of L-alphalysophosphatidylinositol/GPR55 mitogen-activated protein kinase (MAPK) signaling by cannabinoids. J Biol Chem 287, 91-104.
21. Giuliano M, Pellerito O, Portanova P, Calvaruso G, Santulli A, De Blasio A, Vento R, Tesoriere G (2009) Apoptosis induced in HepG2 cells by the synthetic cannabinoid WIN: Involvement of the transcription factor PPARgamma. Biochimie 91, 457-465.
22. Novotna A, Mares J, Ratcliffe S, Novakova I, Vachova M, Zapletalova O, Gasperini C, Pozzilli C, Cefaro L, Comi G, Rossi P, Ambler Z, Stelmasiak Z, Erdmann A, Montalban X, Klimek A, Davies P (2011) A randomized, double-blind, placebo-controlled, parallel-group, enriched-design study of nabiximols. (Sativex®), as add-on therapy, in subjects with refractory spasticity caused by multiple sclerosis. Eur J Neurol 18, 1122-1131.
23. Collin C, Davies P, Mutiboko IK, Ratcliffe S (2007) Randomized controlled trial of cannabis-based medicine in spasticity caused by multiple sclerosis. Eur J Neurol 14, 290-296.
24. Garcia-Arencibia M, Gonzalez S, de Lago E, Ramos JA, Mechoulam R, Fernandez-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.
25. Rodriguez-Navarro JA, Gomez A, Rodal I, Perucho J, Martinez A, Furio V, Ampuero I, Casarejos MJ, Solano RM, de Yebenes JG, Mena MA (2008) Parkin deletion causes cerebral and systemic amyloidosis in human mutated tau overexpressing mice. Hum Mol Genet 17, 3128-3143.
26. Menendez J, Rodriguez-Navarro JA, Solano RM, Casarejos MJ, Rodal I, Guerrero R, Sanchez MP, Avila J, Mena MA, de Yebenes JG (2006) Suppression of Parkin enhances nigrostriatal and motor neuron lesion in mice over-expressing human-mutated tau protein. Hum Mol Genet 15, 2045-2058.
27. Rodriguez-Navarro JA, Rodriguez L, Casarejos MJ, Solano RM, Gomez A, Perucho J, Cuervo AM, Garcia de Yebenes J, MenaMA(2010)Trehalose ameliorates dopaminergic and tau pathology in parkin deleted/tau overexpressing mice through autophagy activation. Neurobiol Dis 39, 423-438.
28. Mena MA, Rodriguez-Navarro JA, de Yebenes JG (2009) The multiple mechanisms of amyloid deposition: The role of parkin. Prion 3, 5-11.
29. Garcia-Arencibia M, Garcia C, Kurz A, Rodriguez-Navarro JA, Gispert-Sachez S, Mena MA, Auburger G, de Yebenes JG, Fernandez-Ruiz J (2009) Cannabinoid CB1 receptors are early downregulated followed by a further upregulation in the basal ganglia of mice with deletion of specific park genes. J Neural Transm Suppl 269-275.
30. Hilliard A, Stott C, Wright S, Guy G, Pryce G, Al-Izki S, Bolton C, Giovannoni G (2012) Evaluation of the efects of Sativex (THC BDS: CBD BDS) on Inhibition of spasticity in a chronic relapsing experimental allergic autoimmune encephalomyelitis: A model of multiple sclerosis. ISRN Neurol 2012, 802649.
31. Fentress JC (1988) Expressive contexts, fine structure, and central mediation of rodent grooming. Ann N Y Acad Sci 525, 18-26.
32. van den Broek FA, Omtzigt CM, Beynen AC (1993) Whisker trimming behaviour in A2G mice is not prevented by offering means of withdrawal from it. Lab Anim 27, 270-272.
33. Sarna JR, Dyck RH, Whishaw IQ (2000) The Dalila effect: C57BL6 mice barber whiskers by plucking. Behav Brain Res 108, 39-45.
34. Biala G, Kruk M, Budzynska B (2009) Effects of the cannabinoid receptor ligands on anxiety-related effects of damphetamine and nicotine in the mouse elevated plus maze test. J Physiol Pharmacol 60, 113-122.
35. Rey AA, Purrio M, Viveros MP, Lutz B (2012) Biphasic effects of cannabinoids in anxiety responses: CB1 and GABA(B) receptors in the balance of GABAergic and glutamatergic neurotransmission. Neuropsychopharmacology 37, 2624-2634.
36. Witkin JM, Tzavara ET, Nomikos GG (2005) A role for cannabinoid CB1 receptors in mood and anxiety disorders. Behav Pharmacol 16, 315-331.
37. Tietze F (1969) Enzymatic method for quantitative determination of nanogram amounts of total and oxidized glutathione: Application to mammalian blood and other tissue. Anal Biochem 27, 502-522.
38. Rodriguez-Navarro JA, Casarejos MJ, Menendez J, Solano RM, Rodal I, Gomez A, Yebenes JG, Mena MA (2007) Mortality, oxidative stress and tau accumulation during ageing in parkin null mice. J Neurochem 103, 98-114.
39. Premi E, Padovani A, BorroniB(2012) Frontotemporal Lobar Degeneration. Adv Exp Med Biol 724, 114-127.
40. Akirav I (2011) The role of cannabinoids in modulating emotional and non-emotional memory processes in the hippocampus. Front Behav Neurosci 5, 34.
41. Benito C, Tolon RM, Pazos MR, Nunez E, Castillo AI, Romero J (2008) Cannabinoid CB2 receptors in human brain inflammation. Br J Pharmacol 153, 277-285.
42. Ehrhart J, Obregon D, Mori T, Hou H, Sun N, Bai Y, Klein T, Fernandez F, Tan J, Shytle RD (2005) Stimulation of cannabinoid receptor 2 (CB2) suppresses microglial activation. J Neuroinflammation 2, 29.
43. Canals S, Casarejos MJ, de Bernardo S, Solano RM, Mena MA (2003) Selective and persistent activation of extracellular signal-regulated protein kinase by nitric oxide in glial cells induces neuronal degeneration in glutathione-depleted midbrain cultures. Mol Cell Neurosci 24, 1012-1026.
44. Bosier B, Muccioli GG, Mertens B, Sarre S, Michotte Y, Lambert DM, Hermans E (2012) Differential modulations of striatal tyrosine hydroxylase and dopamine metabolism by cannabinoid agonists as evidence for functional selectivity in vivo. Neuropharmacology 62, 2327-2335.
45. Fisar Z (2010) Inhibition of monoamine oxidase activity by cannabinoids. Naunyn Schmiedebergs Arch Pharmacol 381, 563-572.
46. Liu B, Hong JS (2003) Role of microglia in inflammationmediated neurodegenerative diseases: Mechanisms and strategies for therapeutic intervention. J Pharmacol Exp Ther 304, 1-7.
47. Stamer K, Vogel R, Thies E, Mandelkow E, Mandelkow EM (2002) Tau blocks traffic of organelles, neurofilaments, and APP vesicles in neurons and enhances oxidative stress. J Cell Biol 156, 1051-1063.
48. Stoothoff W, Jones PB, Spires-Jones TL, Joyner D, Chhabra E, Bercury K, Fan Z, Xie H, Bacskai B, Edd J, Irimia D, Hyman BT (2009) Differential effect of three-repeat and fourrepeat tau on mitochondrial axonal transport. J Neurochem 111, 417-427.
49. Zhang Y, Champagne N, Beitel LK, Goodyer CG, Trifiro M, LeBlanc A (2004) Estrogen and androgen protection of human neurons against intracellular amyloid beta1-42 toxicity through heat shock protein 70. J Neurosci 24, 5315-5321.
50. Boland B, Kumar A, Lee S, Platt FM, Wegiel J, Yu WH, Nixon RA (2008) Autophagy induction and autophagosome clearance in neurons: Relationship to autophagic pathology in Alzheimer's disease. J Neurosci 28, 6926-6937.
51. Webb JL, Ravikumar B, Rubinsztein DC (2004) Microtubule disruption inhibits autophagosome-lysosome fusion: Implications for studying the roles of aggresomes in polyglutamine diseases. Int J Biochem Cell Biol 36, 2541-2550.
52. Klein RL, Dayton RD, Henderson KM, Petrucelli L (2006) Parkin is protective for substantia nigra dopamine neurons in a tau gene transfer neurodegeneration model. Neurosci Lett 401, 130-135.
53. Ren Y, Jiang H, Yang F, Nakaso K, Feng J (2009) Parkin protects dopaminergic neurons against microtubuledepolymerizing toxins by attenuating microtubule-associated protein kinase activation. J Biol Chem 284, 4009-4017.
54. Petrucelli L, Dickson D, Kehoe K, Taylor J, Snyder H, Grover A, De Lucia M, McGowan E, Lewis J, Prihar G, Kim J, Dillmann WH, Browne SE, Hall A,Voellmy R, TsuboiY, Dawson TM, Wolozin B, Hardy J, Hutton M (2004) CHIP and Hsp70 regulate tau ubiquitination, degradation and aggregation.Hum Mol Genet 13, 703-714.
55. Hatakeyama S, Matsumoto M, Kamura T, Murayama M, Chui DH, Planel E, Takahashi R, Nakayama KI, Takashima A (2004) U-box protein carboxyl terminus of Hsc70-interacting protein (CHIP) mediates poly-ubiquitylation preferentially on four-repeat Tau and is involved in neurodegeneration of tauopathy. J Neurochem 91, 299-307.
56. Shimura H, Schwartz D, Gygi SP, Kosik KS (2004) CHIP-Hsc70 complex ubiquitinates phosphorylated tau and enhances cell survival. J Biol Chem 279, 4869-4876.
57. Casarejos MJ, Solano RM, Rodriguez-Navarro JA, Gomez A, Perucho J, Castano JG, Garcia de Yebenes J, Mena MA (2009) Parkin deficiency increases the resistance of midbrain neurons and glia to mild proteasome inhibition: The role of autophagy and glutathione homeostasis. J Neurochem 110, 1523-1537.