Peroxisome proliferator-activated receptor γ is expressed in hippocampal neurons and its activation prevents β-amyloid neurodegeneration: Role of Wnt signaling

Experimental Cell Research

Volumn 304, Issue 1, 2005, Pages 91-104

  Inestrosa, Nibaldo C ^a   Godoy, Juan A ^a   Quintanilla, Rodrigo A ^a   Koenig, Cecilia S ^a   Bronfman, Miguel ^a  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

Author keywords

Alzheimer's disease; Anti diabetic drugs; A peptide; Cell survival; PPAR ; Wnt signaling

Indexed keywords

AMYLOID BETA PROTEIN; ANTIBODY; BETA CATENIN; BROMINE DERIVATIVE; CALCIUM; CIGLITAZONE; GLYCOGEN SYNTHASE KINASE 3BETA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR AGONIST; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; ROSIGLITAZONE; TROGLITAZONE; WNT PROTEIN;

ALZHEIMER DISEASE; AMYLOID NEUROPATHY; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASSAY; CELL ACTIVATION; CELL CULTURE; CONTROLLED STUDY; CYTOPLASM; ELECTRON MICROSCOPY; EMBRYO; HIPPOCAMPUS; IMMUNOFLUORESCENCE; NERVE CELL; NERVE DEGENERATION; NEUROFILAMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; RAT; SIGNAL TRANSDUCTION;

EID: 13644271368     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2004.09.032     Document Type: Article

References (66)

1. D.P. Salmon, and M.W. Bondi Neuropsychology of Alzheimer disease R.D. Terry R. Katzman K.L. Bick S.S. Sisodia Alzheimer Disease 1999 Lippincott Williams and Wilkins Philadelphia 39 56
2. M.P. Mattson Pathways towards and away from Alzheimer's disease Nature 430 2004 631 639
3. B.A. Yanker Mechanism of neuronal degeneration in Alzheimer's disease Neuron 16 1996 921 923
4. S. Miranda, C. Opazo, L.F. Larrondo, F.J. Munoz, F. Ruiz, and Leighton.N.C. Inestrosa The role of oxidative stress in the toxicity induced by amyloid β-peptide in Alzheimer's disease Prog. Neurobiol. 62 2000 633 648
5. C. Opazo, X. Huang, R.A. Cherny, D. Moir, A.E. Roher, A.R. White, R. Cappai, C.L. Masters, R.E. Tanzi, N.C. Inestrosa, and A.I. Bush Metalloenzyme-like activity of Alzheimer's disease β-amyloid J. Biol. Chem. 277 2002 40302 40308
6. A. Takashima, T. Honda, K. Yasutake, G. Michel, O. Murayama, M. Murayama, K. Ishiguro, and H. Yamaguchi Activation of tau protein kinase I/glycogen synthase kinase-3β by amyloid β peptide (25-35) enhances phosphorylation of tau in hippocampal neurons Neurosci. Res. 31 1998 317 323
7. J. Busciglio, A. Lorenzo, J. Yeh, and B.A. Yanker β-Amyloid fibrils induce tau phosphorylation and loss of microtubule binding Neuron 14 1995 879 888
8. J.L. Garrido, J.A. Godoy, A. Alvarez, M. Bronfman, and N.C. Inestrosa Protein kinase C inhibits amyloid-β-peptide neurotoxicity by acting on members of the Wnt pathway FASEB J. 16 2002 1982 1984
9. G.V. De Ferrari, M.A. Chacón, M.I. Barría, J.L. Garrido, J.A. Godoy, G. Olivares, A.E. Reyes, A. Alvarez, M. Bronfman, and N.C. Inestrosa Activation of Wnt signaling rescue neurodegeneration and behavioral impairments induced by β-amyloid fibrils Mol. Psychiatry 8 2003 195 208
10. A. Caricasole, A. Copani, A. Caruso, F. Caraci, L. Iacovelli, M.A. Sortino, G.C. Terstappen, and F. Nicoletti The Wnt pathways, cell-cycle activation and β-amyloid: novel therapeutic strategies in Alzheimer's disease? Trends Pharmacol. Sci. 24 2003 233 239
11. Z. Zhang, H. Hartmann, V. DO, D. Abramowski, C. Sturchler-Pierrat, M. Staufenbiel, B. Sommer, M. van de Wetering, H. Clevers, P. Saftig, B. De Strooper, X. He, and B.A. Yankner Destabilization of β-catenin by mutations in presenilin-1 potentiates neuronal apoptosis Nature 395 1998 698 702
12. J.J. Pei, E. Braak, H. Braak, I. Grundke-Iqbal, K. Iqbal, B. Winblad, and R.F. Cowburn Distribution of active glycogen synthase kinase 3β (GSK-3β) in brains staged for Alzheimer disease neurofibrillary changes J. Neuropathol. Exp. Neurol. 58 1999 1010 1019
13. A. Patapoutian, and L.F. Reichardt Roles of Wnt proteins in neural development and maintenance Curr. Opin. Neurobiol. 10 2000 392 399
14. E.D. Rosen, and B.M. Spiegelman PPARγ: a nuclear regulator of metabolism, differentiation, and cell growth J. Biol. Chem. 276 2001 37731 37734
15. J. Berger, and D.E. Moller The mechanisms of action of PPARs Annu. Rev. Med. 53 2002 409 435
16. T.C. He, T.A. Chan, B. Vogelstein, and K.W. Kinzler PPARδ is an APC-regulated target of nonsteroidal anti-inflammatory drugs Cell 99 1999 335 345
17. S.E. Ross, N. Hemati, K.A. Longo, C.N. Bennett, P.C. Lucas, R.L. Erickson, and O.A. MacDougald Inhibition of adipogenesis by Wnt signalling Science 289 2000 950 953
18. J.M. Lehmann, I.B. Moore, T.A. Smith-Oliver, W.O. Wilkison, T.M. Willson, and S.A. Kliewer An antidiabetic thiazolidinedione is a high affinity ligand for peroxisome proliferator-activated receptor gamma (PPARγ) J. Biol. Chem. 270 1996 12953 12956
19. G.S. Watson, and S. Craft The role of insulin resistance in the pathogenesis of Alzheimer's disease: implications for treatment CNS Drugs 17 2003 27 45
20. Y. Zhu, K. Alvarez, M.S. Rao, and J.K. Reddy Cloning of a new member of the peroxisome proliferator-activated receptor gene family from mouse liver J. Biol. Chem. 268 1993 26817 26820
21. 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 2002 131 145
22. 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-γ in Alzheimer's disease brains Biochem. Biophys. Res. Commun. 254 1999 582 586
23. A. Cáceres, G. Banker, O. Steward, L. Binder, and M. Payne MAP2 is localized to the dendrites of hippocampal neurons, which develop in culture Brain Res. 13 1984 314 318
24. A. Alvarez, R. Alarcon, C. Opazo, E.O. Campos, F.J. Munoz, F.H. Calderon, F. Dajas, M.K. Gentry, B.P. Doctor, F.G. De Mello, and N.C. Inestrosa Stable complexes involving acetylcholinesterase and amyloid-β peptide change the biochemical properties of the enzyme and increase the neurotoxicity of Alzheimer's fibrils J. Neurosci. 18 1998 3213 3223
25. F.J. Muñoz, C. Opazo, G. Gil-Gomez, G. Tapia, V. Fernandez, M.A. Valverde, and N.C. Inestrosa Vitamin E but not 17-β estradiol protects against vascular toxicity induced by β-amyloid wild-type and the Dutch amyloid variant J. Neurosci. 22 2002 3081 3089
26. A.E. Reyes, M.A. Chacón, M.C. Dinamarca, W.F. Cerpa, C. Morgan, and N.C. Inestrosa Acetylcholinesterase-Aβ complexes are more toxic than Aβ fibrils in rat hippocampus: effect on rat β-amyloid aggregation, laminin expression, reactive astrocytosis and neuronal cell loss Am. J. Pathol. 16 2004 2163 2174
27. R.P. Doornbos, M. Theelen, P.C. van der Hoeven, W.J. van Blitterswijk, A.J. Verkleij, and P.M. van Bergen en Henegouwen Protein kinase Cζ is a negative regulator of protein kinase B activity Eur. J. Biochem. 274 1999 8589 8596
28. A.D. Roth, A.V. Leisewitz, J.E. Jung, P. Cassina, L. Barbeito, N.C. Inestrosa, and M. Bronfman PPARγ activators induce growth arrest and process extension in B12 oligodendrocyte-like cells and terminal differentiation of cultured oligodendrocytes J. Neurosci. Res. 72 2003 425 435
29. 2+ modulates basal GLUT1 activity and plays a permissive role in its activation by metabolic stress and insulin in rat epithelial cells Cell Calcium 28 2000 97 106
30. E.A. Newman, and K.R. Zahs Calcium waves in retinal glial cells Science 275 1997 844 847
31. K.W. Svoboda, D. Denk, D. Kleinfeld, and D.W. Tank In vivo dendritic calcium dynamics in neocortical pyramidal neurons Nature 385 1997 161 165
32. T.M. Willson, P.J. Brown, D.D. Sternbach, and B.R. Henke The PPARs: from orphan receptors to drug discovery J. Med. Chem. 43 2000 527 550
33. K.S. Park, R.D. Lee, Kang.S.Y. Han, K.L. Park, K.H. Yang, Y.S. Song, H.J. Park, Y.M. Lee, Y.P. Yun, K.W. Oh, D.J. Kim, Y.W. Yun, S.J. Hwang, S.E. Lee, and J.T. Hong Neuronal differentiation of embryonic midbrain cells by upregulation of peroxisome proliferator-activated receptor-gamma via the JNK-dependent pathway Exp. Cell Res. 297 2004 424 433
34. N.C. Inestrosa, G.V. De Ferrari, J.L. Garrido, A. Alvarez, G.H. Olivares, M.I. Barria, M. Bronfman, and M.A. Chacón Wnt signaling involvement in β-amyloid-dependent neurodegeneration Neurochem. Int. 41 2002 341 344
35. K. Willert, and R. Nusse β-Catenin: a key mediator of Wnt signaling Curr. Opin. Genet. Dev. 8 1998 95 102
36. R.H. Chen, W.V. Ding, and F. McCormick Wnt signaling to β-catenin involves two interactive components. Glycogen synthase kinase 3β inhibition and activation of protein kinase C J. Biol. Chem. 275 2000 17894 17899
37. A. Alvarez, J.A. Godoy, K. Mullendorf, G.H. Olivares, M. Bronfman, and N.C. Inestrosa Wnt-3a prevents β-amyloid toxicity in rat hippocampal neurons Exp. Cell Res. 297 2004 186 196
38. A. Mudher, and S. Lovestone Alzheimer's disease-Do Tautis and Baptists finally shake hands? Trends Neurosci. 25 2002 22 26
39. J.J. Lucas, F. Hernandez, P. Gomez-Ramos, M.A. Moran, and J. Avila Decreased nuclear β-catenin, tau hyperphosphorylation and neurodegeneration in GSK-3β conditional transgenic mice EMBO J. 20 2002 27 39
40. R.A. Fuentealba, G. Farias, J. Scheu, M. Bronfman, M.P. Marzolo, and N.C. Inestrosa Signal transduction during amyloid-β-peptide neurotoxicity: role in Alzheimer's disease Brain Res., Brain Res. Rev. 2004 [in press]
41. A. Hecht, K. Vleminckx, M.P. Stemmler, F. van Roy, and R. Kemler The p300/CBP acetyltransferases function as transcriptional coactivators of β-catenin in vertebrates EMBO J. 19 2000 1839 1850
42. M. Bienz, and H. Clevers Linking colorectal cancer to Wnt signaling Cell 103 2000 311 320
43. S. Uryu, J. Harada, M. Hisamoto, and T. Oda Troglitazone inhibits both post-glutamate neurotoxicity and low-potassium-induced apoptosis in cerebellar granule neurons Brain Res. 924 2002 229 236
44. C.K. Combs, D.E. Johnson, J.C. Karlo, S.B. Cannady, and G.E. Landreth Inflammatory mechanisms in Alzheimer's disease: inhibition of β-amyloid-stimulated proinflammatory responses and neurotoxicity by PPARγ agonists J. Neurosci. 20 2000 558 567
45. C. Nishijima, K. Kimoto, and Y. Arakawa Survival activity of troglitazone in rat motoneurones J. Neurochem. 76 2001 383 390
46. L. Ciani, O. Krylova, M.J. Smalley, T.C. Dale, and P.C. Salinas Divergent canonical WNT-signaling pathway regulates microtubule dynamics: Dishevelled signals locally to stabilize microtubules J. Cell Biol. 164 2004 243 253
47. D.J. Adam, J. Barakesh, R. Laskey, and C. Van Breemen Ion channels and regulation of intracellular calcium in vascular endothelial cells FASEB J. 3 1989 2380 2400
48. 2+ currents and not endothelial nitric oxide production Diabetes 46 1997 659 664
49. 2+ signal and tube formation induced by vascular endothelial growth factor in bovine aortic endothelial cells Eur. J. Pharmacol. 98 2000 19 29
50. +ATP channel activity and depolarises tolbutamide-sensitive neurones in the rat ventromedial hypothalamus Brain Res. 751 1997 165 168
51. +ATP channel activity by troglitazone in CRI-G1 insulin-secreting cells Eur. J. Pharmacol. 313 1996 163 167
52. J.G. Begley, W. Duan, S. Chan, K. Duff, and M.P. Mattson Altered calcium homeostasis and mitochondrial dysfunction in cortical synaptic compartments of presenilin-1 mutant mice J. Neurochem. 72 1999 1030 1039
53. F.M. LaFerla Calcium dyshomeostasis and intracellular signalling in Alzheimer's disease Nat. Rev., Neurosci. 3 2002 862 872
54. T. Kielian, and P.D. Drew Effects of peroxisome proliferators activated-receptor-γ agonists on central nervous system inflammation J. Neurosci. Res. 71 2003 315 325
55. B. Viviani, S. Bartesaghi, F. Gardoni, A. Vezzani, M.M. Behrens, T. Bartfai, M. Binaglia, E. Corsini, M. Di Luca, C.L. Galli, and M. Marinovich Interleukin-1β enhances NMDA receptor-mediated intracellular calcium increase through activation of the Src family of kinases J. Neurosci. 23 2003 8692 8700
56. C.A. Singer, X.A. Figueroa-Masot, R.H. Batchelor, and D.M. Dorsa The mitogen-activated protein kinase pathway mediates estrogen neuroprotection after glutamate toxicity in primary cortical neurons J. Neurosci. 19 1999 2455 2463
57. R. Bi, G. Broutman, M.R. Foy, R.F. Thompson, and M. Baudry The tyrosine kinase and mitogen-activated protein kinase pathways mediate multiple effects of estrogen in hippocampus Proc. Natl. Acad. Sci. U. S. A. 97 2000 3602 3607
58. J. Nilsen, S. Chen, and R.D. Brinton Dual action of estrogen on glutamate-induced calcium signaling: mechanisms requiring interaction between estrogen receptors and src/mitogen activated protein kinase pathway Brain Res. 930 2002 216 234
59. R. Steward, and D. Liolitsa Type 2 Diabetes mellitus, cognitive impairment and dementia Diabetes Med. 16 1999 93 112
60. J. Kuusisto, K. Koivisto, L. Mykkanen, E.L. Helkala, M. Vanhanen, T. Hanninen, K. Kervinen, Y.A. Kesaniemi, P.J. Riekkinen, and M. Laakso Association between features of the insulin resistance syndrome and Alzheimer's disease independently of apolipoprotein E ε4 phenotype: cross sectional population based study Br. Med. J. 315 1997 1045 1049
61. A. Ott, R.P. Stolk, F. van Harskamp, H.A. Pols, A. Hofman, and M.M. Breteler Diabetes mellitus and the risk of dementia: the Rotterdam study Neurology 53 1999 1937 1942
62. a 344)
63. T. Dale Signal transduction by the Wnt family of ligands Biochem. J. 329 1998 209 223
64. R. Scatena, P. Bottoni, G.E. Martorana, F. Ferrari, P. De Sole, C. Rossi, and B. Giardina Mitochondrial respiratory chain dysfunction, a non-receptor-mediated effect of synthetic PPAR-ligands: biochemical and pharmacological implications Biochem. Biophys. Res. Commun. 319 2004 967 973
65. M. Citron Strategies for disease modification in Alzheimer's disease Nat. Rev., Neurosci. 5 2004 677 685
66. D.L. Gerhold, F. Liu, G. Jiang, Z. Li, J. Xu, M. Lu, J.R. Sachs, A. Bagchi, A. Fridman, D.J. Holder, T.W. Doebber, J. Berger, A. Elbrecht, D.E. Moller, and B.B. Zhang Gene expression profile of adipocyte differentiation and its regulation by peroxisome proliferator-activated receptor-γ agonists Endocrinology 143 2002 2106 2118