CB1 receptor selective activation inhibits β-amyloid-induced iNOS protein expression in C6 cells and subsequently blunts tau protein hyperphosphorylation in co-cultured neurons

Neuroscience Letters

Volumn 404, Issue 3, 2006, Pages 342-346

  Esposito, Giuseppe ^a   De Filippis, Daniele ^b   Steardo, Luca ^a   Scuderi, Caterina ^a   Savani, Claudia ^a   Cuomo, Vincenzo ^a   Iuvone, Teresa ^b  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

Alzheimer's disease; Cannabinoids; CB1 receptors; Nitric oxide (NO); Tau protein hyperphosphorylation

Indexed keywords

2 METHYL 3 (1 NAPHTHOYL) 1 PROPYLINDOLE; 2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; 5 (4 CHLORO 3 METHYLPHENYL) 1 (4 METHYLBENZYL) N (1,3,3 TRIMETHYLBICYCLO[2.2.1]HEPTAN 2 YL) 3 PYRAZOLECARBOXAMIDE; AMYLOID BETA PROTEIN[1-42]; ARACHIDONOYL 2' CHLOROETHYLAMIDE; CANNABINOID 1 RECEPTOR; CANNABINOID RECEPTOR AGONIST; CANNABINOID RECEPTOR ANTAGONIST; INDUCIBLE NITRIC OXIDE SYNTHASE; NITRIC OXIDE; RIMONABANT; TAU PROTEIN; UNCLASSIFIED DRUG; AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN (1 42); AMYLOID BETA-PROTEIN (1-42); PEPTIDE FRAGMENT;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; COCULTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFECT; GLIOMA CELL; IN VITRO STUDY; MACROGLIA; NERVE CELL CULTURE; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; STATISTICAL SIGNIFICANCE; TAUOPATHY; ANIMAL; BIOSYNTHESIS; DRUG ANTAGONISM; DRUG POTENTIATION; GLIOMA; HUMAN; METABOLISM; NERVE CELL; PHEOCHROMOCYTOMA; PHOSPHORYLATION; PHYSIOLOGY; TUMOR CELL LINE;

AMYLOID BETA-PROTEIN; ANIMALS; CELL LINE, TUMOR; COCULTURE TECHNIQUES; GLIOMA; HUMANS; NEURONS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; PEPTIDE FRAGMENTS; PHEOCHROMOCYTOMA; PHOSPHORYLATION; RATS; RECEPTOR, CANNABINOID, CB1; TAU PROTEINS;

EID: 33746296471     PISSN: 03043940     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neulet.2006.06.012     Document Type: Article

References (27)

1. Benito C., Nunez E., Tolon R.M., Carrier E.J., Rabano A., Hillard C.J., and Romero J. Cannabinoid CB2 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
2. Coma M., Guix F.X., Uribesalgo I., Espuna G., Sole M., Andreu D., and Munoz F.J. Lack of oestrogen protection in amyloid-mediated endothelial damage due to protein nitrotyrosination. Brain 128 (2005) 1613-1621
3. Di Rosa M., Radomski M., Carnuccio R., and Moncada S. Glucocorticoids inhibit the induction of nitric oxide synthase in macrophages. Biochem. Biophys. Res. Commun. 172 (1990) 1246-1252
4. Esposito G., De Filippis D., Carnuccio R., Izzo A.A., and Iuvone T. The marijuana component cannabidiol inhibits beta-amyloid-induced tau protein hyperphosphorylation through Wnt/beta-catenin pathway rescue in PC12 cells. J. Mol. Med. 84 (2006) 253-258
5. 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 β-amyloid stimulated PC12 neurons through p38 MAP kinase and NF-κB involvement. Neurosci. Lett. (2006) Epub ahead of print
6. Esposito G., Izzo A.A., Di Rosa M., and Iuvone T. Selective cannabinoid CB1 receptor-mediated inhibition of inducible nitric oxide synthase protein expression in C6 rat glioma cells. J. Neurochem. 78 (2001) 835-841
7. Esposito G., Ligresti A., Izzo A.A., Bisogno T., Ruvo M., Di Rosa M., Di Marzo V., and Iuvone T. The endocannabinoid system protects rat glioma cells against HIV-1 Tat protein-induced cytotoxicity. Mechanism and regulation. J. Biol. Chem. 27 (2002) 50348-50354
8. Grundke-Iqbal I., Iqbal K., Quinlan M., Tung Y.C., Zaidi M.S., and Wisniewski H.M. Microtubule-associated protein tau. A component of Alzheimer paired helical filaments. J. Biol. Chem. 261 (1986) 6084-6089
9. Hillard C.J., Manna S., Greenberg M.J., DiCamelli R., Ross R.A., Stevenson L.A., Murphy V., Pertwee R.G., and Campbell W.B. Synthesis and characterization of potent and selective agonists of the neuronal cannabinoid receptor (CB1). CJ J. Pharmacol. Exp. Ther. 289 (1999) 1427-1433
10. Iuvone T., Esposito G., Esposito R., Santamaria R., Di Rosa M., and Izzo A.A. Neuroprotective effect of cannabidiol, a non-psychoactive component from Cannabis sativa, on beta-amyloid-induced toxicity in PC12 cells. J. Neurochem. 89 (2004) 134-141
11. Kim S.U., and de Vellis J. Microglia in health and disease. J. Neurosci. Res. 81 (2005) 302-313
12. Marsicano G., Goodenough S., Monory K., Hermann H., Eder M., Cannich A., Azad S.C., Cascio M.G., Gutierrez S.O., van der Stelt M., Lopez-Rodriguez M.L., Casanova E., Schutz G., Zieglgansberger W., Di Marzo V., Behl C., and Lutz B. CB1 cannabinoid receptors and on-demand defense against excitotoxicity. Science 302 (2003) 84-88
13. McGeer P.L., and McGeer E.G. Inflammation, autotoxicity and Alzheimer disease. Neurobiol. Aging 6 (2001) 799-809
14. Molderings G.J., Bonisch H., Hammermann R., Gothert M., and Bruss M. Noradrenaline release-inhibiting receptors on PC12 cells devoid of alpha(2(-)) and CB(1) receptors: similarities to presynaptic imidazoline and edg receptors. Neurochem. Int. 40 (2002) 157-167
15. Moncada S., and Higgs E.A. Endogenous nitric oxide: physiology, pathology and clinical relevance. Eur. J. Clin. Invest. 21 (1991) 361-374
16. Nagayama T., Sinor A.D., Simon R.P., Chen J., Graham S.H., Jin K., and Greenberg D.A. Cannabinoids and neuroprotection in global and focal cerebral ischemia and in neuronal cultures. J. Neurosci. 19 (1999) 2987-2995
17. Nathan C., Calingasan N., Nezezon J., Ding A., Lucia M.S., La Perle K., Fuortes M., Lin M., Ehrt S., Kwon N.S., Chen J., Vodovotz Y., Kipiani K., and Beal M.F. Protection from Alzheimer's-like disease in the mouse by genetic ablation of inducible nitric oxide synthase. J. Exp. Med. 202 (2005) 1163-1169
18. Panikashvili D., Mechoulam R., Beni S.M., Alexandrovich A., and Shohami E. CB1 cannabinoid receptors are involved in neuroprotection via NF-kappa B inhibition. J. Cereb. Blood Flow Metab. 25 (2005) 477-484
19. Parmentier-Batteur S., Jin K., Mao X.O., Xie L., and Greenberg D.A. Increased severity of stroke in CB1 cannabinoid receptor knock-out mice. J. Neurosci. 22 (2002) 9771-9775
20. Ramirez B.G., Blazquez C., Gomez del Pulgar T., Guzman M., and de Ceballos M.L. Prevention of Alzheimer's disease pathology by cannabinoids: neuroprotection mediated by blockade of microglial activation. J. Neurosci. 25 (2005) 1904-1913
21. Saez T.E., Pehar M., Vargas M., Barbeito L., and Maccioni R.B. Astrocytic nitric oxide triggers tau hyperphosphorylation in hippocampal neurons. In Vivo 18 (2004) 275-280
22. Smith M.A., Vasak M., Knipp M., Castellani R.J., and Perry G. Dimethylargininase, a nitric oxide regulatory protein, in Alzheimer disease. Free Radic. Biol. Med. 25 (1998) 898-902
23. Togo T., Katsuse O., and Iseki E. Nitric oxide pathways in Alzheimer's disease and other neurodegenerative dementias. Neurol. Res. 26 (2004) 563-566
24. van der Stelt M., and Di Marzo V. Cannabinoid receptors and their role in neuroprotection. Neuromol. Med. 7 (2005) 37-50
25. van der Stelt M., Veldhuis W.B., Bar P.R., Veldink G.A., Vliegenthart J.F., and Nicolay K. Neuroprotection by Delta9-tetrahydrocannabinol, the main active compound in marijuana, against ouabain-induced in vivo excitotoxicity. J. Neurosci. 21 (2001) 6475-6479
26. Vincent B., and Smith J.D. Astrocytes down-regulate neuronal beta-amyloid precursor protein expression and modify its processing in an apolipoprotein E isoform-specific manner. Eur. J. Neurosci. 14 (2001) 256-266
27. Walker D.G., and Lue L.F. Investigations with cultured human microglia on pathogenic mechanisms of Alzheimer's disease and other neurodegenerative diseases. J. Neurosci. Res. 81 (2005) 81412-81425