CB2 cannabinoid receptor agonist ameliorates alzheimer-like phenotype in AβPP/PS1 mice

Journal of Alzheimer's Disease

Volumn 35, Issue 4, 2013, Pages 847-858

  Aso, Ester ^a   Juvés, Salvador ^a,b   Maldonado, Rafael ^c   Ferrer, Isidro ^a,b  

^a HOSPITAL UNIVERSITARI DE BELLVITGE   (Spain)

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

^c UNIVERSITAT POMPEU FABRA   (Spain)

Author keywords

Alzheimer's disease; CB 2 cannabinoid receptor; cognition; neuroinflammation; oxidative stress; tau kinases

Indexed keywords

1 DEOXY 3 (1,1 DIMETHYLBUTYL) DELTA8 TETRAHYDROCANNABINOL; GAMMA INTERFERON; INTERLEUKIN 1BETA; INTERLEUKIN 6; STRESS ACTIVATED PROTEIN KINASE; 1,1-DIMETHYLBUTYL-1-DEOXY-DELTA(9)-THC; AMYLOID PRECURSOR PROTEIN; CANNABINOID; CANNABINOID 2 RECEPTOR; CANNABINOID RECEPTOR AGONIST; CYTOKINE; GLYCOGEN SYNTHASE KINASE 3; PRESENILIN 1; RNA; SYNAPTOPHYSIN; TAU PROTEIN; TAU-PROTEIN KINASE; 1,1 DIMETHYLBUTYL 1 DEOXY DELTA(9) THC; TAU PROTEIN KINASE;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; DISEASE COURSE; HIPPOCAMPUS; LONG TERM CARE; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; AGONISTS; AMYLOID PLAQUE; ANIMAL; AVOIDANCE BEHAVIOR; BIOSYNTHESIS; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; HUMAN; IMMUNOHISTOCHEMISTRY; METABOLISM; PATHOLOGY; PHYSIOLOGY; PSYCHOMOTOR PERFORMANCE; RECOGNITION; TRANSGENIC MOUSE; DRUG POTENTIATION;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; AVOIDANCE LEARNING; CANNABINOID RECEPTOR AGONISTS; CANNABINOIDS; CYTOKINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLUORESCENT ANTIBODY TECHNIQUE; GLYCOGEN SYNTHASE KINASE 3; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MICE, TRANSGENIC; OXIDATIVE STRESS; PLAQUE, AMYLOID; PRESENILIN-1; PSYCHOMOTOR PERFORMANCE; RECEPTOR, CANNABINOID, CB2; RECOGNITION (PSYCHOLOGY); RNA; SYNAPTOPHYSIN; TAU PROTEINS;

EID: 84878863032     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-130137     Document Type: Article

References (41)

1. Ferrer I (2012) Defining Alzheimer as a common age-related neurodegenerative process not inevitably leading to dementia. Prog Neurobiol 97, 38-51.
2. Selkoe DJ (2012) Preventing Alzheimer's disease. Science 337, 1488-1492.
3. Campbell VA, Gowran A (2007) Alzheimer's disease; taking the edge off with cannabinoids? Br J Pharmacol 152, 655-662.
4. Koppel J, Davies P (2008) Targeting the endocannabinoid system in Alzheimer's disease. J Alzheimers Dis 15, 495-504.
5. Piomelli D (2003) The molecular logic of endocannabinoid signalling. Nat Rev Neurosci 4, 873-884.
6. Herkenham M, Lynn AB, Johnson MR, Melvin LS, de Costa BR, Rice KC (1991) Characterization and localization of cannabinoid receptors in rat brain: A quantitative in vitro autoradiographic study. J Neurosci 11, 563-583.
7. Wilson RI, Nicoll RA (2002) Endocannabinoid signaling in the brain. Science 296, 678-682.
8. Aso E, Palomer E, Juvés S, Maldonado R, Muñoz FJ, Ferrer I (2012) CB1 agonist ACEA protects neurons and reduces the cognitive impairment of A-PP/PS1 mice. J Alzheimers Dis 30, 439-459.
9. Núñez E, Benito C, Pazos MR, Barbachano A, Fajardo O, González S, Tolón RM, Romero J (2004) Cannabinoid CB2 receptors are expressed by perivascular microglial cells in the human brain: An immunohistochemical study. Synapse 53, 208-213.
10. Cabral GA, Raborn ES, Griffin L, Dennis J, Marciano-Cabral F (2008) CB2 receptors in the brain: Role in central immune function. Br J Pharmacol 153, 240-251.
11. Van Sickle MD, Duncan M, Kingsley PJ, Mouihate A, Urbani P, Mackie K, Stella N, Makriyannis A, Piomelli D, Davison JS, Marnett LJ, Di Marzo V, Pittman QJ, Patel KD, Sharkey KA (2005) Identification and functional characterization of brainstem cannabinoid CB2 receptors. Science 310, 329-332.
12. Brusco A, Tagliaferro PA, Saez T, Onaivi ES (2008) Ultrastructural localization of neuronal brain CB2 cannabinoid receptors. Ann N Y Acad Sci 1139, 450-457.
13. Onaivi ES, Ishiguro H, Gong JP, Patel S, Meozzi PA, Myers L, Perchuk A, Mora Z, Tagliaferro PA, Gardner E, Brusco A, Akinshola BE, Liu QR, Chirwa SS, Hope B, Lujilde J, Inada T, Iwasaki S, Macharia D, Teasenfitz L, Arinami T, Uhl GR (2008) Functional expression of brain neuronal CB2 cannabinoid receptors are involved in the effects of drugs of abuse and in depression. Ann N Y Acad Sci 1139, 434-449.
14. Callén L, Moreno E, Barroso-Chinea P, Moreno-Delgado D, Cortés A, Mallol J, Casadó V, Lanciego JL, Franco R, Lluis C, Canela EI, McCormick PJ (2012) Cannabinoid receptors CB1 and CB2 form functional heteromers in brain. J Biol Chem 287, 20851-20865.
15. Benito C, Núñez E, Tolón RM, Carrier EJ, Rábano A, Hillard CJ, Romero J (2003) Cannabinoid CB2 receptors and fatty acid amide hydrolase are selectively overexpressed in neuritic plaque-associated glia in Alzheimer's disease brains. J Neurosci 23, 11136-11141.
16. Benito C, Tolón RM, Pazos MR, Núñez E, Castillo AI, Romero J (2010) Cannabinoid CB2 receptors in human brain inflammation. Br J Pharmacol 153, 277-285.
17. Fernández-Ruiz J, Romero J, Velasco G, Tolón RM, Ramos JA, Guzmán M (2007) Cannabinoid CB2 receptor: A new target for controlling neural cell survival? Trends Pharmacol Sci 28, 39-45.
18. Ramírez BG, Blázquez C, Gómez del Pulgar T, Guzmán 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.
19. Martín-Moreno AM, Reigada D, Ramírez 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.
20. Martín-Moreno AM, Brera B, Spuch C, Carro E, García- García L, Delgado M, Pozo MA, Innamorato NG, Cuadrado A, de Ceballos ML(2012) Prolonged oral cannabinoid administration prevents neuroinflammation, lowers-amyloid levels and improves cognitive performance in Tg APP 2576 mice. J Neuroinflammation 9, 8.
21. Wu J, Bie B, Yang H, Xu JJ, Brown DL, Naguib M (2013) Activation of the CB(2) receptor system reverses amyloidinduced memory deficiency. Neurobiol Aging 34, 791-804.
22. Tolón RM, Núñez E, Pazos MR, Benito C, Castillo AI, Martínez-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.
23. Esposito G, De Filippis D, Carnuccio R, Izzo AA, Iuvone T (2006) The marijuana component cannabidiol inhibits betaamyloid-induced tau protein hyperphosphorylation through Wnt/beta-catenin pathway rescue in PC12 cells. J Mol Med 84, 253-258.
24. Esposito G, De Filippis D, Steardo L, Scuderi C, Savani C, Cuomo V, Iuvone T (2006b) CB1 receptor selective activation inhibits beta-amyloid-induced iNOS protein expression in C6 cells and subsequently blunts tau protein hyperphosphorylation in co-cultured neurons. Neurosci Lett 404, 342-346.
25. Borchelt DR, Ratovitski T, van Lare J, Lee MK, Gonzales V, Jenkins NA, Copeland NG, Price DL, Sisodia SS (1997) Accelerated amyloid deposition in the brains of transgenic mice coexpressing mutant presenilin 1 and amyloid precursor proteins. Neuron 19, 939-945.
26. Aso E, Lomoio S, López-González I, Joda L, Carmona M, Fernández-Yagüe N, Moreno J, Juvés S, Pujol A, Pamplona R, Portero-Otín M, Martín V, Díaz M, Ferrer I (2012) Amyloid generation and dysfunctional immunoproteasome activation with disease progression in animal model of familial Alzheimer's disease. Brain Pathol 22, 636-653.
27. Huffman JW, Liddle J, Yu S, Aung MM, Abood ME, Wiley JL, Martin BR(1999) 3-(1,1-Dimethylbutyl)-1-deoxy-delta-8-THC and related compounds: Synthesis of selective ligands for the CB2 receptor. Bioorg Med Chem Lett 7, 2905-2914.
28. Huestis MA (2005) Pharmacokinetics and metabolism of the plant cannabinoids, delta9-tetrahydrocannabinol, cannabidiol and cannabinol. Handb Exp Pharmacol 168, 657-690.
29. Jin M, Shepardson N, Yang T, Chen G, Walsh D, Selkoe DJ (2011) Soluble amyloid beta-protein dimers isolated from Alzheimer cortex directly induce tau hyperphosphorylation and neuritic degeneration. Proc Natl Acad Sci U S A 108, 5819-5824.
30. Zhu X, Raina AK, Lee HG, Chao M, Nunomura A, Tabaton M, Petersen RB, Perry G, Smith MA (2003) Oxidative stress and neuronal adaptation in Alzheimer disease: The role of SAPK pathways. Antioxid Redox Signal 5, 571-576.
31. Puig B, Gómez-Isla T, Ribé E, Cuadrado M, Torrejón-Escribano B, Dalfó E, Ferrer I (2004) Expression of stress-activated kinases c-Jun N-terminal kinase (SAPK/JNKP) and p38 kinase (p38-P), and tau hyperphosphorylation in neurites surrounding betaA plaques in APP Tg2576 mice. Neuropathol Appl Neurobiol 30, 491-502.
32. van der Stelt M, Mazzola C, Esposito G, Matias I, Petrosino S, De Filippis D, Micale V, Steardo L, Drago F, Iuvone T, Di Marzo V (2006) Endocannabinoids and beta-amyloidinduced neurotoxicity in vivo: Effect of pharmacological elevation of endocannabinoid levels. Cell Mol Life Sci 63, 1410-1424.
33. Esposito G, Iuvone T, Savani C, Scuderi C, De Filippis D, Papa M, Di Marzo V, Steardo L (2007) Opposing control of cannabinoid receptor stimulation on amyloid-beta-induced reactive gliosis: In vitro and in vivo evidence. J Pharmacol Exp Ther 322, 1144-1152.
34. Ferrer I, Gómez-Isla T, Puig B, Freixes M, Ribé E, Dalfó E, Ávila J (2005) Current advances on different kinases involved in tau phosphorylation, and implications in Alzheimer's disease and tauopathies. Curr Alzheimer Res 2, 3-18.
35. Hooper C, Killick R, Lovestone S (2008) The GSK3 hypothesis of Alzheimer's disease. J Neurochem 104, 1433-1439.
36. Rajesh M, Mukhopadhyay P, Haskó G, Huffman JW, Mackie K, Pacher P (2008) CB2 cannabinoid receptor agonists attenuate TNF-alpha-induced human vascular smooth muscle cell proliferation and migration. Br J Pharmacol 153, 347-357.
37. Ferrer I (2004) Stress kinases involved in tau phosphorylation in Alzheimer's disease, tauopathies and APP transgenic mice. Neurotox Res 6, 469-475.
38. Molina-Holgado F, Molina-Holgado E, Guaza C, Rothwell NJ (2002) Role ofCB1 andCB2 receptors in the inhibitory effects of cannabinoids on lipopolysaccharide-induced nitric oxide release in astrocyte cultures. J Neurosci Res 67, 829-836.
39. García-Arencibia M, 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.
40. Pacher P, Mackie K (2012) Interplay of cannabinoid 2 (CB2) receptors with nitric oxide synthases, oxidative and nitrative stress, and cell death during remote neurodegeneration. J Mol Med (Berl) 90, 347-351.
41. Franklin A, Stella N (2003) Arachidonylcyclopropylamide increases microglial cell migration through cannabinoid CB2 and abnormal-cannabidiol- sensitive receptors. Eur J Pharmacol 474, 195-198.