The GSK3 hypothesis of Alzheimer's disease

Journal of Neurochemistry

Volumn 104, Issue 6, 2008, Pages 1433-1439

  Hooper, Claudie ^a   Killick, Richard ^a   Lovestone, Simon ^a  

^a MEDICAL RESEARCH COUNCIL   (United Kingdom)

Author keywords

amyloid; Inflammation; Insulin; Memory; Tau; Wnt

Indexed keywords

AMYLOID BETA PROTEIN; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3ALPHA; GLYCOGEN SYNTHASE KINASE 3BETA; INSULIN; TAU PROTEIN; WNT PROTEIN;

ALZHEIMER DISEASE; COGNITIVE DEFECT; ENZYME ACTIVITY; FRONTAL CORTEX; GENETIC TRANSCRIPTION; GLYCOGEN METABOLISM; HIPPOCAMPUS; HUMAN; INFLAMMATION; MEMORY DISORDER; MICROGLIA; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SHORT SURVEY; SIGNAL TRANSDUCTION;

ALZHEIMER DISEASE; GLYCOGEN SYNTHASE KINASE 3; HUMANS; SIGNAL TRANSDUCTION;

EID: 39849110726     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2007.05194.x     Document Type: Short Survey

References (75)

1. Alvarez G., Munoz-Montano J. R., Satrustegui J., Avila J., Bogonez E. and az-Nido J. (1999) Lithium protects cultured neurons against beta-amyloid-induced neurodegeneration. FEBS Lett. 453, 260-264.
2. Anderton B. H., Betts J., Blackstock W. P. et al. (2001) Sites of phosphorylation in tau and factors affecting their regulation. Biochem. Soc. Symp. 67, 73-80.
3. Asuni A. A., Hooper C., Reynolds C. H., Lovestone S., Anderton B. H. and Killick R. (2006) GSK3alpha exhibits beta-catenin and tau directed kinase activities that are modulated by Wnt. Eur. J. Neurosci. 24, 3387-3392.
4. Baki L., Shioi J., Wen P., Shao Z., Schwarzman A., Gama-Sosa M., Neve R. and Robakis N. K. (2004) PS1 activates PI3K thus inhibiting GSK-3 activity and tau overphosphorylation: effects of FAD mutations. EMBO J. 23, 2586-2596.
5. Bhat R. V., Shanley J., Correll M. P., Fieles W. E., Keith R. A., Scott C. W. and Lee C. M. (2000) Regulation and localization of tyrosine216 phosphorylation of glycogen synthase kinase-3beta in cellular and animal models of neuronal degeneration. Proc. Natl. Acad. Sci USA 97, 11074-11079.
6. Biessels G. J. and Kappelle L. J. (2005) Increased risk of Alzheimer's disease in Type II diabetes: insulin resistance of the brain or insulininduced amyloid pathology? Biochem. Soc. Trans. 33, 1041-1044.
7. Bijur G. N. and Jope R. S. (2001) Proapoptotic stimuli induce nuclear accumulation of glycogen synthase kinase-3 beta. J. Biol. Chem. 276, 37436-37442.
8. Blalock E. M., Geddes J. W., Chen K. C., Porter N. M., Markesbery W. R. and Landfield P. W. (2004) Incipient Alzheimer's disease: microarray correlation analyses reveal major transcriptional and tumor suppressor responses. PNAS 101, 2173-2178.
9. Brion J. P., Anderton B. H., Authelet M., Dayanandan R., Leroy K., Lovestone S., Octave J. N., Pradier L., Touchet N. and Tremp G. (2001) Neurofibrillary tangles and tau phosphorylation. Biochem. Soc. Symp. 0, 81-88.
10. Bullock B. P. and Habener J. F. (1998) Phosphorylation of the cAMP response element binding protein CREB by cAMP-dependent protein kinase A and glycogen synthase kinase-3 alters DNAbinding affinity, conformation, and increases net charge. Biochemistry 37, 3795-3809.
11. Caricasole A., Copani A., Caraci F., Aronica E., Rozemuller A. J., Caruso A., Storto M., Gaviraghi G., Terstappen G. C. and Nicoletti F. (2004) Induction of Dickkopf-1, a negative modulator of the Wnt pathway, is associated with neuronal degeneration in Alzheimer's brain. J. Neurosci. 24, 6021-6027.
12. Chen J., Park C. S. and Tang S. J. (2006) Activity-dependent synaptic Wnt release regulates hippocampal long term potentiation. J. Biol. Chem. 281, 11910-11916.
13. Cho J. H. and Johnson G. V. (2003) Glycogen synthase kinase 3beta phosphorylates tau at both primed and unprimed sites. Differential impact on microtubule binding. J. Biol. Chem. 278, 187-193.
14. Christie R. H., Freeman M. and Hyman B. T. (1996) Expression of the macrophage scavenger receptor, a multifunctional lipoprotein receptor, in microglia associated with senile plaques in Alzheimer's disease. Am. J. Pathol. 148, 399-403.
15. Cole A. R., Knebel A., Morrice N. A., Robertson L. A., Irving A. J., Connolly C. N. and Sutherland C. (2004) GSK-3 phosphorylation of the Alzheimer epitope within collapsin response mediator proteins regulates axon elongation in primary neurons. J. Biol. Chem. 279, 50176-50180.
16. Dale T. C. (1998) Signal transduction by the Wnt family of ligands. Biochem. J. 329 (Pt 2), 209-223.
17. De Ferrari G. V., Papassotiropoulos A., Biechele T. et al. (2007) Common genetic variation within the low-density lipoprotein receptorrelated Protein 6 and late-onset Alzheimer's disease. PNAS 104, 9434-9439.
18. Doble B. W. and Woodgett J. R. (2003) GSK-3: tricks of the trade for a multi-tasking kinase. J. Cell Sci. 116, 1175-1186.
19. Doble B. W., Patel S., Wood G. A., Kockeritz L. K. and Woodgett J. R. (2007) Functional redundancy of GSK-3alpha and GSK-3beta in Wnt/beta-catenin signaling shown by using an allelic series of embryonic stem cell lines. Dev. Cell 12, 957-971.
20. Engel T., Goni-Oliver P., Lucas J. J., Avila J. and Hernandez F. (2006) Chronic lithium administration to FTDP-17 tau and GSK-3beta overexpressing mice prevents tau hyperphosphorylation and neurofibrillary tangle formation, but pre-formed neurofibrillary tangles do not revert. J. Neurochem. 99, 1445-1455.
21. Hamilton G., Proitsi P., Jehu L., Morgan A., Williams J., O'Donovan M. C., Owen M. J., Powell J. F. and Lovestone S. (2007) Candidate gene association study of insulin signaling genes and Alzheimer's disease: evidence for SOS2, PCK1, and PPAR-gamma as susceptibility loci. Am. J Med Genet B Neuropsychiatr. Genet 144, 508-516.
22. Hanger D. P., Hughes K., Woodgett J. R., Brion J. P. and Anderton B. H. (1992) Glycogen synthase kinase-3 induces Alzheimer's diseaselike phosphorylation of tau: generation of paired helical filament epitopes and neuronal localisation of the kinase. Neurosci. Lett. 147, 58-62.
23. Hansen T. O., Rehfeld J. F. and Nielsen F. C. (2004) GSK-3beta reduces cAMP-induced cholecystokinin gene expression by inhibiting CREB binding. Neuroreport 15, 841-845.
24. Hardy J. (2006) A hundred years of Alzheimer's disease research. Neuron 52, 3-13.
25. Hernandez F., Borrell J., Guaza C., Avila J. and Lucas J. J. (2002) Spatial learning deficit in transgenic mice that conditionally over-express GSK-3beta in the brain but do not form tau filaments. J. Neurochem. 83, 1529-1533.
26. Hoeflich K. P., Luo J., Rubie E. A., Tsao M. S., Jin O. and Woodgett J. R. (2000) Requirement for glycogen synthase kinase- 3beta in cell survival and NF-kappaB activation. Nature 406, 86-90.
27. Hooper C., Markevich V., Plattner F. et al. (2007) Glycogen synthase kinase-3 inhibition is integral to long-term potentiation. Eur. J. Neurosci. 25, 81-86.
28. Hoshi M., Takashima A., Noguchi K., Murayama M., Sato M., Kondo S., Saitoh Y., Ishiguro K., Hoshino T. and Imahori K. (1996) Regulation of mitochondrial pyruvate dehydrogenase activity by tau protein kinase I/glycogen synthase kinase 3beta in brain. Proc. Natl. Acad. Sci USA 93, 2719-2723.
29. Huelsken J. and Behrens J. (2002) The Wnt signalling pathway. J. Cell Sci. 115, 3977-3978.
30. Hye A., Kerr F., Archer N., Foy C., Poppe M., Brown R., Hamilton G., Powell J., Anderton B. and Lovestone S. (2005) Glycogen synthase kinase-3 is increased in white cells early in Alzheimer's disease. Neurosci. Lett. 373, 1-4.
31. Imahori K. and Uchida T. (1997) Physiology and pathology of tau protein kinases in relation to Alzheimer's disease. J Biochem. (Tokyo) 121, 179-188.
32. Ishiguro K., Omori A., Takamatsu M., Sato K., Arioka M., Uchida T. and Imahori K. (1992) Phosphorylation sites on tau by tau protein kinase I, a bovine derived kinase generating an epitope of paired helical filaments. Neurosci. Lett. 148, 202-206.
33. Jope R. S., Yuskaitis C. J. and Beurel E. (2007) Glycogen synthase kinase-3 (GSK3): inflammation, diseases, and therapeutics. Neurochem. Res. 32, 577-595.
34. Joshi S. N. and Crutcher K. A. (1998) Rat microglia exhibit increased density on Alzheimer's plaques in vitro. Exp. Neurol. 149, 42-50.
35. Koivisto L., Hakkinen L., Matsumoto K., McCulloch C. A., Yamada K. M. and Larjava H. (2004) Glycogen synthase kinase-3 regulates cytoskeleton and translocation of Rac1 in long cellular extensions of human keratinocytes. Exp. Cell Res. 293, 68-80.
36. Leroy K., Yilmaz Z. and Brion J. P. (2007) 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. 33, 43-55.
37. Lesort M., Jope R. S. and Johnson G. V. (1999) Insulin transiently increases tau phosphorylation: involvement of glycogen synthase kinase-3beta and Fyn tyrosine kinase. J. Neurochem. 72, 576-584.
38. Lizcano J. M. and Alessi D. R. (2002) The insulin signalling pathway. Curr. Biol. 12, R236-R238.
39. Lovestone S., Reynolds C. H., Latimer D., Davis D. R., Anderton B. H., Gallo J. M., Hanger D., Mulot S., Marquardt B. and Stabel S. (1994) Alzheimer's disease-like phosphorylation of the microtubule- associated protein tau by glycogen synthase kinase-3 in transfected mammalian cells. Curr. Biol. 4, 1077-1086.
40. Lucas J. J., Hernandez F., Gomez-Ramos P., Moran M. A., Hen R. and Avila J. (2001) Decreased nuclear beta-catenin, tau hyperphosphorylation and neurodegeneration in GSK-3beta conditional transgenic mice. EMBO J. 20, 27-39.
41. MacAulay K., Doble B. W., Patel S., Hansotia T., Sinclair E. M., Drucker D. J., Nagy A. and Woodgett J. R. (2007) Glycogen synthase kinase 3alpha-specific regulation of murine hepatic glycogen metabolism. Cell Metab 6, 329-337.
42. Mateo I., Infante J., Llorca J., Rodriguez E., Berciano J. and Combarros O. (2006) Association between glycogen synthase kinase-3beta genetic polymorphism and late-onset Alzheimer's disease. Dement. Geriatr. Cogn Disord. 21, 228-232.
43. McGeer P. L. and McGeer E. G. (1996) Anti-inflammatory drugs in the fight against Alzheimer's disease. Ann. NY Acad. Sci 777, 213-220.
44. Mudher A., Shepherd D., Newman T. A. et al. (2004) GSK-3beta inhibition reverses axonal transport defects and behavioural phenotypes in Drosophila. Mol. Psychiatry 9, 522-530.
45. Mukai F., Ishiguro K., Sano Y. and Fujita S. C. (2002) Alternative splicing isoform of tau protein kinase I/glycogen synthase kinase 3beta. J. Neurochem. 81, 1073-1083.
46. Noble W., Planel E., Zehr C. et al. (2005) Inhibition of glycogen synthase kinase-3 by lithium correlates with reduced tauopathy and degeneration in vivo. Proc. Natl. Acad. Sci. USA 102, 6990-6995.
47. Nusse R. (2005) Wnt signaling in disease and in development. Cell Res. 15, 28-32.
48. Pei J. J., Tanaka T., Tung Y. C., Braak E., Iqbal K. and Grundke-Iqbal I. (1997) Distribution, levels, and activity of glycogen synthase kinase- 3 in the Alzheimer disease brain. J. Neuropathol. Exp. Neurol. 56, 70-78.
49. Pei J. J., Braak E., Braak H., Grundke-Iqbal I., Iqbal K., Winblad B. and Cowburn R. F. (1999) Distribution of active glycogen synthase kinase 3beta (GSK-3beta) in brains staged for Alzheimer disease neurofibrillary changes. J. Neuropathol. Exp. Neurol. 58, 1010-1019.
50. Peineau S., Taghibiglou C., Bradley C. et al. (2007) LTP Inhibits LTD in the Hippocampus via Regulation of GSK3beta. Neuron 53, 703-717.
51. Phiel C. J., Wilson C. A., Lee V. M. and Klein P. S. (2003) GSK-3alpha regulates production of Alzheimer's disease amyloid-beta peptides. Nature 423, 435-439.
52. Reger M. A., Watson G. S., Green P. S. et al. (2007) Intranasal insulin improves cognition and modulates {beta}-amyloid in early AD. Neurology (Epub ahead of print).
53. Reiman E. M., Webster J. A., Myers A. J. et al. (2007) GAB2 alleles modify Alzheimer's risk in APOE epsilon4 carriers. Neuron 54, 713-720.
54. Robinson S. R., Bishop G. M. and Munch G. (2003) Alzheimer vaccine: amyloid-beta on trial. Bioessays 25, 283-288.
55. Rockenstein E., Torrance M., Adame A., Mante M., Bar-on P., Rose J. B., Crews L. and Masliah E. (2007) Neuroprotective effects of regulators of the glycogen synthase kinase-3beta signaling pathway in a transgenic model of Alzheimer's disease are associated with reduced amyloid precursor protein phosphorylation. J. Neurosci. 27, 1981-1991.
56. Rodionova E., Conzelmann M., Maraskovsky E., Hess M., Kirsch M., Giese T., Ho A. D., Zoller M., Dreger P. and Luft T. (2007) GSK-3 mediates differentiation and activation of proinflammatory dendritic cells. Blood 109, 1584-1592.
57. Rubinfeld B., Albert I., Porfiri E., Fiol C., Munemitsu S. and Polakis P. (1996) Binding of GSK3beta to the APC-beta-catenin complex and regulation of complex assembly. Science 272, 1023-1026.
58. Saltiel A. R. and Kahn C. R. (2001) Insulin signalling and the regulation of glucose and lipid metabolism. Nature 414, 799-806.
59. Sanna P. P., Cammalleri M., Berton F., Simpson C., Lutjens R., Bloom F. E. and Francesconi W. (2002) Phosphatidylinositol 3-kinase is required for the expression but not for the induction or the maintenance of long-term potentiation in the hippocampal CA1 region. J. Neurosci. 22, 3359-3365.
60. Schaffer B., Wiedau-Pazos M. and Geschwind D. H. (2003) Gene structure and alternative splicing of glycogen synthase kinase 3 beta (GSK-3beta) in neural and non-neural tissues. Gene 302, 73-81.
61. Schenk D. B., Seubert P., Grundman M. and Black R. (2005) A beta immunotherapy: Lessons learned for potential treatment of Alzheimer's disease. Neurodegener. Dis. 2, 255-260.
62. Solano D. C., Sironi M. A. R. I., Bonfini C. L. A. U., Solerte S. B., Govoni S. T. E. F. and RACCHI M. A. R. C. (2000) Insulin regulates soluble amyloid precursor protein release via phosphatidyl inositol 3 kinase-dependent pathway. FASEB J. 14, 1015-1022.
63. Stalder M., Phinney A., Probst A., Sommer B., Staufenbiel M. and Jucker M. (1999) Association of microglia with amyloid plaques in brains of APP23 transgenic mice. Am. J. Pathol. 154, 1673-1684.
64. Sun X., Sato S., Murayama O., Murayama M., Park J.-M., Yamaguchi H. and Takashima A. (2002) Lithium inhibits amyloid secretion in COS7 cells transfected with amyloid precursor protein C100. Neurosci. Lett. 321, 61-64.
65. Swatton J. E., Sellers L. A., Faull R. L. M., Holland A., Iritani S. and Bahn S. (2004) Increased MAP kinase activity in Alzheimer's and Down syndrome but not in schizophrenia human brain. Eur. J. Neurosci. 19, 2711-2719.
66. Takashima A., Noguchi K., Sato K., Hoshino T. and Imahori K. (1993) Tau protein kinase I is essential for amyloid beta-protein-induced neurotoxicity. Proc. Natl Acad. Sci. USA 90, 7789-7793.
67. Takashima A., Noguchi K., Michel G., Mercken M., Hoshi M., Ishiguro K. and Imahori K. (1996) Exposure of rat hippocampal neurons to amyloid beta peptide (25-35) induces the inactivation of phosphatidyl inositol-3 kinase and the activation of tau protein kinase I/ glycogen synthase kinase-3 beta. Neurosci. Lett. 203, 33-36.
68. Takashima A., Murayama M., Murayama O. et al. (1998) Presenilin 1 associates with glycogen synthase kinase-3beta and its substrate tau. Proc. Natl. Acad. Sci USA 95, 9637-9641.
69. Troussard A. A., Tan C., Yoganathan T. N. and Dedhar S. (1999) Cellextracellular matrix interactions stimulate the AP-1 transcription factor in an integrin-linked kinase- and glycogen synthase kinase 3- dependent manner. Mol. Cell. Biol. 19, 7420-7427.
70. Turenne G. A. and Price B. D. (2001) Glycogen synthase kinase3 beta phosphorylates serine 33 of p53 and activates p53's transcriptional activity. BMC Cell Biol. 2, 12.
71. Vehmas A. K., Kawas C. H., Stewart W. F. and Troncoso J. C. (2003) Immune reactive cells in senile plaques and cognitive decline in Alzheimer's disease. Neurobiol. Aging 24, 321-331.
72. Welsh G. I. and Proud C. G. (1993) Glycogen synthase kinase-3 is rapidly inactivated in response to insulin and phosphorylates eukaryotic initiation factor eIF-2B. Biochem. J. 294 (Pt 3), 625-629.
73. Woodgett J. R. and Ohashi P. S. (2005) GSK3: an in-Toll-erant protein kinase? Nat. Immunol. 6, 751-752.
74. Yamaguchi H., Ishiguro K., Uchida T., Takashima A., Lemere C. A. and Imahori K. (1996) Preferential labeling of Alzheimer neurofibrillary tangles with antisera for tau protein kinase (TPK) I/glycogen synthase kinase-3 beta and cyclin-dependent kinase 5, a component of TPK II. Acta Neuropathol. (Berl) 92, 232-241.
75. Zhao L., Teter B., Morihara T., Lim G. P., Ambegaokar S. S., Ubeda O. J., Frautschy S. A. and Cole G. M. (2004) Insulin-degrading enzyme as a downstream target of insulin receptor signaling cascade: implications for Alzheimer's disease intervention. J. Neurosci. 24, 11120-11126.