Activation of glycogen synthase kinase-3 beta mediates β-amyloid induced neuritic damage in Alzheimer's disease

Neurobiology of Disease

Volumn 45, Issue 1, 2012, Pages 425-437

  DaRocha Souto, B ^a   Coma, M ^a   Perez Nievas B G ^a   Scotton, T C ^a   Siao, M ^a   Sanchez Ferrer P ^a   Hashimoto, T ^a   Fan, Z ^a   Hudry, E ^a   Barroeta, I ^b   Sereno L ^b   Rodriguez M ^b   Sanchez M B ^b   Hyman, B T ^a   Gomez Isla T ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; BRAIN DERIVED NEUROTROPHIC FACTOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 INHIBITOR; TAU PROTEIN;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; CELL LOSS; CONTROLLED STUDY; DRUG EFFICACY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENE EXPRESSION; MOUSE; NERVE CELL; NERVE CELL LESION; NERVE CELL PLASTICITY; NERVE DEGENERATION; NEUROTOXICITY; NONHUMAN; PATHOGENESIS; PHARMACOLOGICAL BLOCKING; PHENOTYPE; PRIORITY JOURNAL;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; BRAIN; CELLS, CULTURED; DENDRITIC SPINES; GLYCOGEN SYNTHASE KINASE 3; MICE; MICE, TRANSGENIC; NEURITES; NEURONS; TAU PROTEINS;

EID: 81955167913     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2011.09.002     Document Type: Article

References (62)

1. Akiyama H., et al. Pin1 promotes production of Alzheimer's amyloid beta from beta-cleaved amyloid precursor protein. Biochem. Biophys. Res. Commun. 2005, 336:521-529.
2. Aplin A.E., et al. Effect of increased glycogen synthase kinase-3 activity upon the maturation of the amyloid precursor protein in transfected cells. Neuroreport 1997, 8:639-643.
3. Bao Y., et al. Activation of peroxisome proliferator-activated receptor gamma inhibits endothelin-1-induced cardiac hypertrophy via the calcineurin/NFAT signaling pathway. Mol. Cell. Biochem. 2008, 317:189-196.
4. Barco A., et al. Expression of constitutively active CREB protein facilitates the late phase of long-term potentiation by enhancing synaptic capture. Cell 2002, 108:689-703.
5. Beurel E., Jope R.S. The paradoxical pro- and anti-apoptotic actions of GSK3 in the intrinsic and extrinsic apoptosis signaling pathways. Prog. Neurobiol. 2006, 79:173-189.
6. Beurel E., et al. Innate and adaptive immune responses regulated by glycogen synthase kinase-3 (GSK3). Trends Immunol. 2010, 31:24-31.
7. Bhat R.V., et al. Regulation and localization of tyrosine216 phosphorylation of glycogen synthase kinase-3beta in cellular and animal models of neuronal degeneration. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:11074-11079.
8. Bhat R.V., et al. Regulation and localization of tyrosine216 phosphorylation of glycogen synthase kinase-3beta in cellular and animal models of neuronal degeneration. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:11074-11079.
9. Bijur G.N., Jope R.S. Glycogen synthase kinase-3 beta is highly activated in nuclei and mitochondria. Neuroreport 2003, 14:2415-2419.
10. Bijur G.N., et al. Glycogen synthase kinase-3beta facilitates staurosporine- and heat shock-induced apoptosis. Protection by lithium. J. Biol. Chem. 2000, 275:7583-7590.
11. Bito H., Takemoto-Kimura S. Ca(2+)/CREB/CBP-dependent gene regulation: a shared mechanism critical in long-term synaptic plasticity and neuronal survival. Cell Calcium 2003, 34:425-430.
12. Blalock E.M., et al. Incipient Alzheimer's disease: microarray correlation analyses reveal major transcriptional and tumor suppressor responses. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:2173-2178.
13. Bourne J., Harris K.M. Do thin spines learn to be mushroom spines that remember?. Curr. Opin. Neurobiol. 2007, 17:381-386.
14. Chapleau C.A., et al. The actions of BDNF on dendritic spine density and morphology in organotypic slice cultures depend on the presence of serum in culture media. J. Neurosci. Methods. 2008, 169:182-190.
15. Coma M., et al. Triflusal reduces dense-core plaque load, associated axonal alterations and inflammatory changes, and rescues cognition in a transgenic mouse model of Alzheimer's disease. Neurobiol. Dis. 2010, 38:482-491.
16. D'Amore J.D., et al. In vivo multiphoton imaging of a transgenic mouse model of Alzheimer disease reveals marked thioflavine-S-associated alterations in neurite trajectories. J. Neuropathol. Exp. Neurol. 2003, 62:137-145.
17. DaRocha-Souto B., et al. Brain oligomeric beta-amyloid but not total amyloid plaque burden correlates with neuronal loss and astrocyte inflammatory response in amyloid precursor protein/tau transgenic mice. J. Neuropathol. Exp. Neurol. 2011, 70:360-376.
18. Gomez-Isla T., et al. Clinical and pathological correlates of apolipoprotein E epsilon 4 in Alzheimer's disease. Ann. Neurol. 1996, 39:62-70.
19. Grimes C.A., Jope R.S. The multifaceted roles of glycogen synthase kinase 3beta in cellular signaling. Prog. Neurobiol. 2001, 65:391-426.
20. Hardy J., Allsop D. Amyloid deposition as the central event in the aetiology of Alzheimer's disease. Trends Pharmacol. Sci. 1991, 12:383-388.
21. Hardy J., Selkoe D.J. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 2002, 297:353-356.
22. Hashimoto T., et al. CLAC: a novel Alzheimer amyloid plaque component derived from a transmembrane precursor, CLAC-P/collagen type XXV. EMBO J. 2002, 21:1524-1534.
23. Hernandez F., et al. Spatial learning deficit in transgenic mice that conditionally over-express GSK-3beta in the brain but do not form tau filaments. J. Neurochem. 2002, 83:1529-1533.
24. Hetman M., et al. Role of glycogen synthase kinase-3beta in neuronal apoptosis induced by trophic withdrawal. J. Neurosci. 2000, 20:2567-2574.
25. Hooper C., et al. The GSK3 hypothesis of Alzheimer's disease. J. Neurochem. 2008, 104:1433-1439.
26. Hsiao K., et al. Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 1996, 274:99-102.
27. Irizarry M.C., et al. Abeta deposition is associated with neuropil changes, but not with overt neuronal loss in the human amyloid precursor protein V717F (PDAPP) transgenic mouse. J. Neurosci. 1997, 17:7053-7059.
28. Johnson-Wood K., et al. Amyloid precursor protein processing and A beta42 deposition in a transgenic mouse model of Alzheimer disease. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:1550-1555.
29. Jope R.S., et al. Glycogen synthase kinase-3 (GSK3): inflammation, diseases, and therapeutics. Neurochem. Res. 2007, 32:577-595.
30. Josselyn S.A., Nguyen P.V. CREB, synapses and memory disorders: past progress and future challenges. Curr. Drug Targets CNS Neurol. Disord. 2005, 4:481-497.
31. Kim J.W., et al. Glycogen synthase kinase 3 beta is a natural activator of mitogen-activated protein kinase/extracellular signal-regulated kinase kinase kinase 1 (MEKK1). J. Biol. Chem. 2003, 278:13995-14001.
32. Knowles R.B., et al. Demonstration by fluorescence resonance energy transfer of a close association between activated MAP kinase and neurofibrillary tangles: implications for MAP kinase activation in Alzheimer disease. J. Neuropathol. Exp. Neurol. 1999, 58:1090-1098.
33. Koffie R.M., et al. Oligomeric amyloid beta associates with postsynaptic densities and correlates with excitatory synapse loss near senile plaques. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:4012-4017.
34. Kosik K.S. Cellular aspects of Alzheimer neurofibrillary pathology. Prog. Clin. Biol. Res. 1992, 379:183-193.
35. Lee E.B., et al. Targeting amyloid-beta peptide (Abeta) oligomers by passive immunization with a conformation-selective monoclonal antibody improves learning and memory in Abeta precursor protein (APP) transgenic mice. J. Biol. Chem. 2006, 281:4292-4299.
36. Leroy K., et al. Increased level of active GSK-3beta in Alzheimer's disease and accumulation in argyrophilic grains and in neurones at different stages of neurofibrillary degeneration. Neuropathol. Appl. Neurobiol. 2007, 33:43-55.
37. Li M., et al. Cyclic AMP promotes neuronal survival by phosphorylation of glycogen synthase kinase 3beta. Mol. Cell. Biol. 2000, 20:9356-9363.
38. Lombardo J.A., et al. Amyloid-beta antibody treatment leads to rapid normalization of plaque-induced neuritic alterations. J. Neurosci. 2003, 23:10879-10883.
39. Lonze B.E., Ginty D.D. Function and regulation of CREB family transcription factors in the nervous system. Neuron 2002, 35:605-623.
40. Lucas J.J., et al. Decreased nuclear beta-catenin, tau hyperphosphorylation and neurodegeneration in GSK-3beta conditional transgenic mice. EMBO J. 2001, 20:27-39.
41. Luna-Medina R., et al. NP031112, a thiadiazolidinone compound, prevents inflammation and neurodegeneration under excitotoxic conditions: potential therapeutic role in brain disorders. J. Neurosci. 2007, 27:5766-5776.
42. Martinez A., et al. First non-ATP competitive glycogen synthase kinase 3 beta (GSK-3beta) inhibitors: thiadiazolidinones (TDZD) as potential drugs for the treatment of Alzheimer's disease. J. Med. Chem. 2002, 45:1292-1299.
43. Pap M., Cooper G.M. Role of glycogen synthase kinase-3 in the phosphatidylinositol 3-Kinase/Akt cell survival pathway. J. Biol. Chem. 1998, 273:19929-19932.
44. Pei J.J., et al. Distribution, levels, and activity of glycogen synthase kinase-3 in the Alzheimer disease brain. J. Neuropathol. Exp. Neurol. 1997, 56:70-78.
45. Perez M., et al. Characterization of a double (amyloid precursor protein-tau) transgenic: tau phosphorylation and aggregation. Neuroscience 2005, 130:339-347.
46. Peters A., Kaiserman-Abramof I.R. The small pyramidal neuron of the rat cerebral cortex. The perikaryon, dendrites and spines. Am. J. Anat. 1970, 127:321-355.
47. Phiel C.J., et al. GSK-3alpha regulates production of Alzheimer's disease amyloid-beta peptides. Nature 2003, 423:435-439.
48. Pittenger C., Kandel E. A genetic switch for long-term memory. C. R. Acad. Sci. III 1998, 321:91-96.
49. Ribe E.M., et al. Accelerated amyloid deposition, neurofibrillary degeneration and neuronal loss in double mutant APP/tau transgenic mice. Neurobiol. Dis. 2005, 20:814-822.
50. Ryan K.A., Pimplikar S.W. Activation of GSK-3 and phosphorylation of CRMP2 in transgenic mice expressing APP intracellular domain. J. Cell Biol. 2005, 171:327-335.
51. Sereno L., et al. A novel GSK-3beta inhibitor reduces Alzheimer's pathology and rescues neuronal loss in vivo. Neurobiol. Dis. 2009, 35:359-367.
52. Shankar G.M., et al. Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat. Med. 2008, 14:837-842.
53. Snider B.J., et al. Cerebrospinal fluid biomarkers and rate of cognitive decline in very mild dementia of the Alzheimer type. Arch. Neurol. 2009, 66:638-645.
54. Sofola O., et al. Inhibition of GSK-3 ameliorates Abeta pathology in an adult-onset Drosophila model of Alzheimer's disease. PLoS Genet. 2010, 6.
55. Spires T.L., et al. Activity-dependent regulation of synapse and dendritic spine morphology in developing barrel cortex requires phospholipase C-beta1 signalling. Cereb. Cortex. 2005, 15:385-393.
56. Spires-Jones T.L., et al. Passive immunotherapy rapidly increases structural plasticity in a mouse model of Alzheimer disease. Neurobiol. Dis. 2009, 33:213-220.
57. Takashima A., et al. Presenilin 1 associates with glycogen synthase kinase-3beta and its substrate tau. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:9637-9641.
58. Townsend M., et al. Effects of secreted oligomers of amyloid beta-protein on hippocampal synaptic plasticity: a potent role for trimers. J. Physiol. 2006, 572:477-492.
59. Trachtenberg J.T., et al. Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 2002, 420:788-794.
60. Woodgett J.R. Molecular cloning and expression of glycogen synthase kinase-3/factor A. EMBO J. 1990, 9:2431-2438.
61. Wu H.Y., et al. Amyloid beta induces the morphological neurodegenerative triad of spine loss, dendritic simplification, and neuritic dystrophies through calcineurin activation. J. Neurosci. 2010, 30:2636-2649.
62. Yang X.Y., et al. Activation of human T lymphocytes is inhibited by peroxisome proliferator-activated receptor gamma (PPARgamma) agonists. PPARgamma co-association with transcription factor NFAT. J. Biol. Chem. 2000, 275:4541-4544.