WIN55212-2 attenuates amyloid-beta-induced neuroinflammation in rats through activation of cannabinoid receptors and PPAR-γ pathway

Neuropharmacology

Volumn 63, Issue 4, 2012, Pages 653-666

  Fakhfouri, Gohar ^a   Ahmadiani, Abolhasan ^a   Rahimian, Reza ^b,c   Grolla, Ambra A ^d   Moradi, Fatemeh ^a   Haeri, Ali ^a  

^a SHAHID BEHESHTI UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^d UNIVERSITY OF EASTERN PIEDMONT   (Italy)

Author keywords

Beta amyloid; CB1; CB2; Neuroinflammation; PPAR ; WIN55212 2

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; 2 CHLORO 5 NITROBENZANILIDE; 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]; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; CASPASE 3; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; DEGENERATIVE DISEASE; DRUG MECHANISM; GENETIC TRANSCRIPTION; MALE; MEMORY; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; SIGNAL TRANSDUCTION;

ALZHEIMER DISEASE; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; BENZOXAZINES; CANNABINOID RECEPTOR AGONISTS; CANNABINOID RECEPTOR ANTAGONISTS; DISEASE MODELS, ANIMAL; HIPPOCAMPUS; INJECTIONS, INTRAVENTRICULAR; MALE; MORPHOLINES; NAPHTHALENES; NERVE TISSUE PROTEINS; NEUROGLIA; NEURONS; NOOTROPIC AGENTS; PPAR GAMMA; RANDOM ALLOCATION; RATS; RATS, WISTAR; RECEPTOR, CANNABINOID, CB1; RECEPTOR, CANNABINOID, CB2; RECEPTORS, CANNABINOID; SIGNAL TRANSDUCTION;

EID: 84863612316     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2012.05.013     Document Type: Article

References (65)

1. M. Abdelrahman, A. Sivarajah, and C. Thiemermann Beneficial effects of PPAR-g ligands in ischemia-reperfusion injury, inflammation and shock Cardiovasc. Res. 65 2005 772 781 (Pubitemid 40249723)
2. K.T. Akama, C. Albanese, R.G. Pestell, and L.J. Van Eldik Amyloid β-peptide stimulates nitric oxide production in astrocytes through an NF-κB-dependent mechanism Proc. Natl. Acad. Sci. USA 95 1998 5795 5800 (Pubitemid 28224176)
3. A.L. Ambrosio, S.M. Dias, I. Polikarpov, R.B. Zurier, S.H. Burstein, and R.C. Garratt Ajulemic acid, a synthetic nonpsychoactive cannabinoid acid, bound to the ligand binding domain of the human peroxisome proliferator-activated receptor γ J. Biol. Chem. 282 25 2007 18625 18633 (Pubitemid 47100214)
4. P.A. Bäuerle, and D. Baltimore NF-κB: ten years after Cell 87 1996 13 20
5. C. Benito, E. Núñez, M.R. Pazos, R.M. Tolón, and J. Romero The endocannabinoid system and Alzheimer's disease Mol. Neurobiol. 36 2007 75 81 (Pubitemid 351360357)
6. A.F. Bento, R. Marcon, R.C. Dutra, R.F. Claudino, M. Cola, D.F. Pereira Leite, and J.B. Calixto β-Caryophyllene inhibits dextran sulfate sodium-induced colitis in mice through CB2 receptor activation and PPARγ pathway Am. J. Pathol. 178 2011 1153 1166
7. M. Bradford A rapid and sensitive method for the quantitation of micro- gram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72 1976 248 254
8. S. Burstein PPAR-γ: a nuclear receptor with affinity for cannabinoids Life Sci. 77 2005 1674 1684 (Pubitemid 41073661)
9. V.A. Campbell, and A. Gowran Alzheimer's disease; taking the edge off with cannabinoids? Brit. J. Pharmacol. 152 2007 655 662 (Pubitemid 350034982)
10. M. Collino, M. Aragno, R. Mastrocola, M. Gallicchio, A.C. Rosa, C. Dianzani, O. Danni, C. Thiemermann, and R. Fantozzi Modulation of the oxidative stress and inflammatory response by PPAR-γ agonists in the hippocampus of rats exposed to cerebral ischemia/reperfusion Eur. J. Pharmacol. 530 2006 70 80 (Pubitemid 43037126)
11. C.K. Combs, J.C. Karlo, S.C. Kao, and G.E. Landreth Beta-Amyloid stimulation of microglia and monocytes results in TNFalpha-dependent expression of inducible nitric oxide synthase and neuronal apoptosis J. Neurosci. 21 2001 1179 1188 (Pubitemid 32128763)
12. S.N. Davies, R.G. Pertwee, and G. Riedel Functions of cannabinoid receptors in the hippocampus Neuropharmacology 42 2002 993 1007 (Pubitemid 34786553)
13. D. De Filippis, A. Russo, D. De Stefano, M.C. Maiuri, G. Esposito, M.P. Cinelli, C. Pietropaolo, R. Carnuccio, G. Russo, and T. Iuvone Local administration of WIN 55,212-2 reduces chronic granuloma-associated angiogenesis in rat by inhibiting NF-κB activation J. Mol. Med. 85 2007 635 645 (Pubitemid 46870895)
14. T. Dehmer, M.T. Heneka, M. Sastre, J. Dichgans, and J.B. Schulz Protection by pioglitazone in the MPTP model of Parkinson's disease correlates with I kappa B alpha induction and block of NF kappa B and iNOS activation J. Neurochem. 88 2004 494 501 (Pubitemid 38084565)
15. D.J. De Quervain, B. Roozendaal, and J.L. McGaugh Stress and glucocorticoids impair retrieval of long-term spatial memory Nature 394 1998 787 790 (Pubitemid 28391643)
16. M. Dragunow, R.L. Faull, P. Lawlor, E.J. Beilharz, K. Singleton, E.B. Walker, and E. Mee In situ evidence for DNA fragmentation in Huntington's disease striatum and Alzheimer's disease temporal lobes Neuroreport 6 1995 1053 1057
17. C. Drouet, A.N. Shakhov, and C.V. Jongeneel Enhancers and transcription factors controlling the inducibility of the tumor necrosis factor-a promotor in primary macrophages J. Immunol. 147 1991 1694 1700
18. R.M. Friedlander Mechanisms of disease: apoptosis and caspases in neurodegenerative diseases N. Engl. J. Med. 348 2003 1365 1375 (Pubitemid 36384105)
19. B. García-Bueno, J.L. Madrigal, B.G. Pérez-Nievas, and J.C. Leza Stress mediators regulate brain prostaglandin synthesis and peroxisome proliferator-activated receptor-gamma activation after stress in rats Endocrinology 149 4 2008 1969 1978 (Pubitemid 351468348)
20. M.G. Giovannini, C. Scali, C. Prosperi, A. Bellucci, M.G. Vannucchi, S. Rosi, G. Pepeu, and F. Casamenti β-amyloid-induced inflammation and cholinergic hypofunction in the rat brain in vivo: Involvement of the p38MAPK pathway Neurobiol. Dis. 11 2002 257 274 (Pubitemid 36135690)
21. M.T. Heneka, D.L. Feinstein, E. Galea, M. Gleichmann, U. Wüllner, and T. Klockgether Peroxisome proliferator-activated receptor gamma agonists protect cerebellar granule cells from cytokineinduced apoptotic cell death by inhibition of inducible nitric oxide synthase J. Neuroimmunol. 100 1999 156 168 (Pubitemid 30038249)
22. D.Y. Hwang, K.R. Chae, T.S. Kang, J.H. Hwang, C.H. Lim, H.K. Kang, J.S. Goo, M.R. Lee, H.J. Lim, S.H. Min, J.Y. Cho, J.T. Hong, C.W. Song, S.G. Paik, J.S. Cho, and Y.K. Kim Alterations in behavior, amyloid beta-42, caspase-3, and Cox-2 in mutant PS2 transgenic mouse model of Alzheimer's disease FASEB J. 6 2002 805 813 (Pubitemid 34615129)
23. N.C. Inestrosa, J.A. Godoy, R.A. Quintanilla, C.S. Koenig, and M. Bronfman Peroxisome proliferator-activated receptor gamma is expressed in hippocampal neurons and its activation prevents beta-amyloid neurodegeneration: role of Wnt signaling Exp. Cell. Res. 304 2005 91 104 (Pubitemid 40227422)
24. S.J. Jackson, G. Pryce, L.T. Diemel, M.L. Cuzner, and D. Baker Cannabinoid-receptor 1 null mice are susceptible to neurofilament damage and caspase 3 activation Neuroscience 134 2005 261 268 (Pubitemid 40943652)
25. J.H. Jang, and Y.J. Surh β-Amyloid-induced apoptosis is associated with cyclooxygenase-2 up-regulation via the mitogen-activated protein kinase-NF-κB signaling pathway Free Rad. Bio. Med. 38 2005 1604 1613
26. R.U. Jänicke, M.L. Sprengart, M.R. Wati, and A.G. Porter Caspase-3 is required for DNA fragmentation and morphological changes associated with apoptosis J. Biol. Chem. 273 16 1998 9357 9360 (Pubitemid 28183012)
27. S.H. Jia, Y. Li, J. Parodo, A. Kapus, L. Fan, O.D. Rotstein, and J.C. Marshall Pre-B cell colony-enhancing factor inhibits neutrophil apoptosis in experimental inflammation and clinical sepsis J. Clin. Invest. 113 2004 1318 1327 (Pubitemid 39069931)
28. Q. Jiang, M. Heneka, and G.E. Landreth The role of peroxisome proliferator-activated receptor-γ (PPARγ) in Alzheimer's disease, therapeutic implications CNS Drugs 22 1 2008 1 14 (Pubitemid 350243363)
29. E. Jüttler, I. Potrovita, V. Tarabin, S. Prinz, T. Dong-Si, G. Fink, and M. Schwaninger The cannabinoid dexanabinol is an inhibitor of the nuclear factor-kappa B (NF-κB) Neuropharmacology 47 2004 580 592 (Pubitemid 39221780)
30. B. Kaltschmidt, M. Uherek, B. Volk, P.A. Baeuerle, and C. Kaltschmidt Transcription factor NF-kappaB is activated in primary neurons by amyloid beta peptides and in neurons surroundingearly plaques from patients with Alzheimer disease Proc. Natl. Acad. Sci. USA 94 6 1997 2642 2647 (Pubitemid 27136929)
31. R. Kapadia, J.H. Yi, and R. Vemuganti Mechanisms of anti-inflammatory and neuroprotective actions of PPAR-gamma agonists Front. Biosci. 13 2008 1813 1826 (Pubitemid 351599735)
32. E.M. Kawamoto, L.B. Lepsch, M.F. Boaventura, C.D. Munhoz, L.S. Lima, L.M. Yshii, M.C. Avellar, R. Curi, M.P. Mattson, and C. Scavone Amyloid β-peptide activates nuclear factor-κB through an N-Methyl-D Aspartate signaling pathway in cultured cerebellar cells J. Neurosci. Res. 86 2008 845 860 (Pubitemid 351357765)
33. E.J. Kim, K.J. Kwon, J.Y. Park, S.H. Lee, C.H. Moona, and E.J. Baik Effects of peroxisome proliferator-activated receptor agonists on LPS-induced neuronal death in mixed cortical neurons: associated with iNOS and COX-2 Brain Res. 941 2002 1 10 (Pubitemid 34603279)
34. Y. Kitamura, S. Shimohama, H. Koike, J. Kakimura, Y. Matsuoka, Y. Nomura, P.J. Gebicke-Haerter, and T. Taniguchi Increased expression of cyclooxygenases and peroxisome proliferator-activated receptor-gamma in Alzheimer's disease brains Biochem. Biophys. Res. Commun. 254 1999 582 586 (Pubitemid 29290509)
35. J. Liu, H. Li, S.H. Burstein, R.B. Zurier, and J.D. Chen Activation and binding of peroxisome proliferator-activated receptor by synthetic cannabinoid ajulemic acid Mol. Pharmacol. 63 5 2003 983 992 (Pubitemid 36529916)
36. R. Luna-Medina, M. Cortes-Canteli, M. Alonso, A. Santos, A. Martínez, and A. Perez-Castillo Regulation of inflammatory response in neural cells in vitro by thiadiazolidinones derivatives through peroxisome proliferator-activated receptor gamma activation J. Biol. Chem. 280 2005 21453 21462 (Pubitemid 40805710)
37. Y. Marchalant, F. Cerbai, H.M. Brothers, and G.L. Wenk Cannabinoid receptor stimulation is anti-inflammatory and improves memory in old rats Neurobiol. Aging 29 2008 1894 1901
38. J. Martínez-Orgado, D. Fernández-López, I. Lizasoain, and J. Romero The seek of neuroprotection: introducing cannabinoids Recent Pat. CNS Drug Discov. 2 2 2007 131 139 (Pubitemid 46952450)
39. J. Martínez-Orgado, B. Fernández-Frutos, R. González, E. Romero, L. Urigüen, J. Romero, and M.P. Viveros Neuroprotection by the cannabinoid agonist WIN-55212 in an in vivo newborn rat model of acute severe asphyxia Mol. Brain Res. 114 2003 132 139 (Pubitemid 36773554)
40. 1 receptor blockade Eur. J. Pharmacol. 477 2003 219 225 (Pubitemid 38366394)
41. R.J. McDonald, and N.M. White Parallel information processing in the water maze: evidence for independent memory systems involving dorsal striatum and hippocampus Behav. Neural Biol. 61 1994 260 270
42. R.K. McNamara, and R.W. Skelton The neuropharmacological and neurochemical basis of place learning in the Morris Water Maze Brain Res. Rev. 18 1993 33 49 (Pubitemid 23090010)
43. L. Mestre, F. Docagne, F. Correa, F. Loría, M. Hernangómez, J. Borrell, and C. Guaza A cannabinoid agonist interferes with the progression of a chronic model of multiple sclerosis by downregulating adhesion molecules Mol. Cell. Neurosci. 40 2009 258 266
44. S. Moreno, S. Farioli-Vecchioli, and M.P. Ceru Immunolocalization of peroxisome proliferator-activated receptors and retinoid X receptors in the adult rat CNS Neuroscience 123 2004 131 145 (Pubitemid 37518482)
45. J. Morgenweck, O.S. Abdel-aleem, K.C. McNamara, R.R. Donahue, M.Z. Badr, and B.K. Taylor Activation of peroxisome proliferator activated receptor γ in brain inhibits inflammatory pain, dorsal horn expression of Fos, and local edema Neuropharmacology 58 2 2010 337 345
46. S.E. O'Sullivan Cannabinoids go nuclear: evidence for activation of peroxisome proliferator-activated receptors Brit. J. Pharmacol. 152 2007 576 582 (Pubitemid 350034977)
47. S.E. O'Sullivan, and D.A. Kendall Cannabinoid activation of peroxisome proliferator-activated receptors: potential for modulation of inflammatory disease Immunobiology 215 2010 611 616
48. C. Pagano, C. Pilon, A. Calcagno, R. Urbanet, M. Rossato, G. Milan, K. Bianchi, R. Rizzuto, P. Bernante, G. Federspil, and R. Vettor The endogenous cannabinoid system stimulates glucose uptake in human fat cells via PI3-kinase and calcium-dependent mechanisms J. Clin. Endocrin. Metab. 92 12 2007 4810 4819 (Pubitemid 350223464)
49. D. Panikashvili, R. Mechoulam, S.M. Beni, A. Alexandrovich, and E. Shohami CB1 cannabinoid receptors are involved in neuroprotection via NF-κB inhibition J. Cereb. Blood Flow Metab. 25 2005 477 484
50. G. Paxinos, and G. Watson The Rat Brain in Stereotaxic Coordinates 1982 Academic Press New York
51. M. Ramin, P. Azizi, F. Motamedi, A. Haghparast, and F. Khodagholi Inhibition of JNK phosphorylation reverses memory deficit induced by β-amyloid (1-42) associated with decrease of apoptotic factors Behav. Brain Res. 217 2 2011 424 431
52. B.G. Ramírez, C. Blázquez, T. Gómez del Pulgar, M. Guzmán, and M.L. de Ceballos Prevention of Alzheimer's disease pathology by cannabinoids: neuroprotection mediated by blocked of microglial activation J. Neurosci. 25 8 2005 1904 1913 (Pubitemid 40289395)
53. G. Rizzo, and S. Fiorucci PPARs and other nuclear receptors in inflammation Curr. Opin. Pharmacol. 6 2006 421 427
54. A. Schneider, A. Martin-Villalba, F. Weih, J. Vogel, T. Weirth, and M. Schwaninger NF-kB is activated and promoted cell death in focal cerebral ischemia Nat. Med. 5 1999 554 559 (Pubitemid 29220215)
55. K.S. Sink, K.N. Segovia, E.J. Nunes, L.E. Collins, V.K. Vemuri, G. Thakur, A. Makriyannis, and J.D. Salamone Intracerebroventricular administration of cannabinoid CB1 receptor antagonists AM251 and AM4113 fails to alter food-reinforced behavior in rats Psychopharmacology 206 2009 223 232
56. Y.S. Song, H.J. Park, S.Y. Kima, S.H. Lee, H.S. Yoo, H.S. Lee, M.K. Lee, K.W. Oh, S.K. Kang, S.E. Lee, and J.T. Hong Protective role of Bcl-2 on β-amyloid-induced cell death of differentiated PC12 cells: reduction of NF-κB and p38 MAP kinase activation Neurosci. Res. 49 2004 69 80 (Pubitemid 38501703)
57. Y. Sun, and A. Bennett Cannabinoids: a new group of agonists of PPARs PPAR Res. 2007 2007 23513
58. S. Sundararajan, Q. Jiang, M. Heneka, and G. Landreth PPARγ as a therapeutic target in central nervous system diseases Neurochem. Int. 49 2006 136 144 (Pubitemid 43867071)
59. S. Sundararajan, and G.E. Landreth Antiinflammatory properties of PPARgamma agonists following ischemia Drug News Perspect. 17 2004 229 236 (Pubitemid 38987364)
60. M. van der Stelt, and V. Di Marzo Cannabinoid receptors and their role in neuroprotection Neuromolecular Med. 7 2005 37 50 (Pubitemid 41278188)
61. M. van der Stelt, C. Mazzola, G. Esposito, I. Matias, S. Petrosino, D. De Filippis, V. Micale, L. Steardo, F. Drago, T. Iuvone, and V. Di Marzo Endocannabinoids and β-amyloid-induced neurotoxicity in vivo: effect of pharmacological elevation of endocannabinoid levels Cell. Mol. Life Sci. 63 2006 1410 1424 (Pubitemid 43939021)
62. R.E. Watson, N.M. Craven, S. Kang, C.J. Jones, C.M. Kielty, and C.E. Griffiths A short-term screening protocol, using fibrillin-1 as a reporter molecule, for photoaging repair agents J. Invest. Dermatol. 116 2001 672 678 (Pubitemid 32467644)
63. X.Q. Xiao, H.Y. Zhang, and X.C. Tang Huperzine A attenuates amyloid β-peptide fragment 25-35-induced apoptosis in rat cortical neurons via inhibiting reactive oxygen species formation and caspase-3 activation J. Neurosci. Res. 67 2002 30 36
64. J. Yuan, and B.A. Yankner Apoptosis in the nervous system Nature 7 2000 802 809
65. C.Z. Zhu, J.P. Mikusa, Y. Fan, P.R. Hollingsworth, M. Pai, P. Chandran, A.V. Daza, B.B. Yao, M.J. Dart, M.D. Meyer, M.W. Decker, G.C. Hsieh, and P. Honore Peripheral and central sites of action for the non-selective cannabinoid agonist WIN 55, 212-2 in a rat model of post-operative pain Brit. J. Pharmacol. 157 2009 645 655