Glycogen synthase kinase-3 is associated with neuronal and glial hyperphosphorylated tau deposits in Alzheimer's diasese, Pick's disease, progressive supranuclear palsy and corticobasal degeneration

Acta Neuropathologica

Volumn 104, Issue 6, 2002, Pages 583-591

  Ferrer, I ^a,b   Barrachina, M ^b   Puig, B ^b  

^a HOSPITAL UNIVERSITARI DE BELLVITGE   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Alzheimer's disease; Corticobasal degeneration; Pick's disease; Progressive supranuclear palsy; Tau

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3ALPHA; GLYCOGEN SYNTHASE KINASE 3BETA; PROTEIN ANTIBODY; TAU PROTEIN;

ADULT; AGED; ALZHEIMER DISEASE; ARTICLE; ASTROCYTE; CLINICAL ARTICLE; COILED BODY; CONTROLLED STUDY; CORTICOBASAL DEGENERATION; CROSS REACTION; DISEASE ASSOCIATION; DYSTROPHY; ENZYME INACTIVATION; ENZYME PHOSPHORYLATION; FEMALE; GLIA CELL; HUMAN; IMMUNOHISTOCHEMISTRY; MALE; NERVE PROJECTION; NEURITE; NEUROFIBRILLARY TANGLE; NEUROPATHOLOGY; NEUROPIL THREAD; NIEMANN PICK DISEASE; OLIGODENDROGLIA; PRIORITY JOURNAL; PROGRESSIVE SUPRANUCLEAR PALSY; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SENILE PLAQUE; WESTERN BLOTTING;

EID: 0036942843     PISSN: 00016322     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00401-002-0587-8     Document Type: Article

References (44)

1. Alessi DR, James SR, Downess CP, Holmes AB, Gaffney PR, Reese CB, Cohen P (1997) Characterisation a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase βα. Curr Biol 7:261-269
2. Atzori C, Guetti B, Piva R, Srinivasan AN, Zolo P, Delisle MB, Mirra SS, Migheli A (2001) Activation of JNK/p38 pathway occurs in diseases characterized by tau protein pathology and is related to tau phosphorylation but not to apoptosis. J Neuropathol Exp Neurol 60:1190-1197
3. Buée L, Delacourte A (1999) Comparative biochemistry of tau in progressive supranuclear palsy, corticobasal degeneration, FTDP-17 and Pick's disease. Brain Pathol 9:681-693
4. Buéc L, Bussière T, Buée-Scherrer V, Delacourte A, Hof PR (2000) Tau isoforms, phosphorylation and role in neurodegenerative disorders. Brain Res Rev 33:95-130
5. Cohen P, Frame S (2001) The renaissance of GSK3. Nat Rev 2:769-776
6. Cross D, Culbert AA, Chalmers KA, Facci L, Skaper SD, Reith AD (2001) Selective small-molecule inhibitors of glycogen synthase kinase-3 activity protect primary neurones from death. J Neurochem 77:94-102
7. Crowther RA, Goedert M (2000) Abnormal tau-containing filaments in neurodegenerative diseases. J Struct Biol 130:271-279
8. Fang X Yu SX, Lu Y, Bast RC Jr, Woodgett JR, Mills GB (2000) Phosphorylation and inactivation of glycogen synthase kinase 3 by protein kinase A. Proc Natl Acad Sci USA 97: 11960-11965
9. Feany MB, Dickson DW (1996) Neurodegenerative disorders with extensive tau pathology: a comparative study and review. Ann Neurol 40:139-148
10. Ferrer I, Blanco R, Carmona M, Puig B (2001) Phosphorylated mitogen-activated protein kinase (MAPK/ERK-P), protein kinase of 38 kDa (p38-P), stress-activated protein kinase (SAPK/JNK-P), and calcium/calmodulin-dependent kinase II (CaM kinase II) are differentially expressed in tau deposits in neurons and glial cells in tauopathies. J Neural Transm 108: 1397-1415
11. Ferrer I, Blanco R, Carmona M, Ribera R, Goutan E, Puig B, Rey MJ, Cardozo A, Viñals F, Ribalta T (2001) Phosphorylated MAP kinase (ERK1, ERK2) expression is associated with early tau deposition in neurones and glial cells, but not with increased nuclear DNA vulnerability and cell death, in Alzheimer disease, Pick's disease, progressive supranuclear palsy and corticobasal degeneration. Brain Pathol 11:144-158
12. Frame S, Cohen P, Biondi RM (2001) A common phosphate binding site explains the unique substrate specificity of GSK3 and its inactivation by phosphorylation. Mol Cell 7:1321-1327
13. Godemann R, Biernat J, Mandelkow E, Mandelkow EM (1999) Phosphorylation of tau protein by recombinant GSK-3beta: pronounced phosphorylation at select Ser-Thr-Pro motifs but no phosphorylation at Ser262 in the repeat domain. FEBS Lett 454:157-164
14. Goedert M, Spillantini MG, Cairns NJ, Crowtler RA (1992) Tau proteins of Alzheimer paired helical filaments: abnormal phosphorylation of all six brain isoforms. Neuron 8:159-168
15. Goedert M, Spillantini MG, Davis SW (1998) Filamentous nerve cell inclusions in neurodegenerative diseases. Curr Opin Neurobiol 8:619-632
16. Hanger DP, Hughes K, Woodgett JR, Brion JP, Anderton BH (1992) Glycogen synthase kinase-3 induces Alzheimer's disease-like phosphorylation of tau: generation of paired helical filament epitopes and neuronal localisation of the kinase. Neurosci Lett 147:58-62
17. Illenberger S, Zheng-Fischhofer Q, Preuss U, Stamer K, Bauman K, Trinczek B, Biernat J, Godemann R, Mandelkow EM, Mandelkow E (1998) The endogenous and cell cycle-dependent phosphorylation of tau protein in living cells: implications for Alzheimer's disease. Mol Biol Cell 9:1495-1512
18. Komori T (1999) Tau-positive glial inclusions in progressive supranuclear palsy, corticobasal degeneration and Pick's disease. Brain Pathol 9:663-679
19. Knowles RB, Chin J, Ruff CT, Hyman BT (1999) 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 58:1090-1098
20. Lee VMY, Goedert M, Trojanowski JQ (2001) Neurodegenerative tauopathies. Annu Rev Neurosci 24:1121-1159
21. Leroy K, Boutajangout A, Authelet M, Woodgett JR, Anderton BH, Brion JP (2002) The active form of glycogen synthase kinase-3β is associated with granulovacuolar degeneration in neurons in Alzheimer's disease. Acta Neuropathol 103:91-99
22. Lovestone S, Reynolds CH (1997) The phosphorylation of tau: a critical stage in neurodevelopment and neurodegenerative processes. Neuroscience 78:309-324
23. Lucas JJ, Hernandez F, Gomez-Ramos P, Morán MA, Hen R, Avila J (2001) Decreased nuclear beta-catenin, tau hyperphosphorylation and neurodegeneration in GSK-3β conditional transgenic mice. EMBO J 20:27-39
24. Mandelkow EM, Drewes G, Biernat J, Gustke N, Van Lint J, Vandenheede JR, Mandelkow E (1992) Glycogen synthase kinase-3 and the Alzheimer-like state of microtubule-associated protein tau. FEBS Lett 314:315-321
25. Muñoz-Montano JR, Moreno FJ, Avila J, Diaz-Nido J (1997) Lithium inhibits Alzheimers disease-like tau protein phosphorylation in neurons. FEBS Lett 411:183-188
26. Pei JJ, Grundke-Iqbal I, Iqbal K, Bogdanovic N, Winblad B, Cowburn RF (1998) Accumulation of cyclin-dependent kinase 5 (cdk5) in neurons with early stages of Alzheimer's disease neurofibrillary degeneration. Brain Res 29:267-277
27. Pei JJ, Braak E, Braak H, Grundke-Iqbal I, Iqbal K, Winblad B, Cowburn RF (1999) Distribution of glycogen synthase kinase 3 beta (GSK-3β) for Alzheimer disease neurofibrillary tangle. J Neuropathol Exp Neurol 58:1010-1119
28. Perry G, Roder H, Nunomura A, Takeda A, Friedlich AL, Zhu X, Raina AL, Holbrook N, Siedlak SL, Harris PLR, Smith MA (1999) Activation of neuronal extracellular receptor kinase (ERK) in Alzheimer disease links oxidative stress to abnormal tau phosphorylation. NeuroReport 10:2411-2415
29. Reynolds CH, Betts JC, Blackstock WP, Nebreda AR, Anderton BH (2000) Phosphorylation sites on tau identified by nanoelectrospray mass spectrometry: differences in vitro between the mitogen-activated protein kinases ERK2, c-Jun N-terminal kinase and p38, and glycogen synthase kinase-3β. J Neurochem 74:1587-1595
30. Schwab C, DeMaggio AJ, Ghoshal N, Binder LI, Kuret J, McGeer PL (2000) Casein kinase 1 delta is associated with pathological accumulation of tau in several neurodegenerative diseases. Neurobiol Aging 21:503-510
31. Sengupta A, Wu Q, Grundke-Iqbal I, Iqbal K, Singh TJ (1997) Potentiation of GSK-3-catalyzed Alzheimer-like phosphorylation of human tau by cdk5. Mol Cell Biochem 167:99-105
32. Shaw M, Cohen P (1999) Role of protein kinase B and the MAP kinase cascade in mediating the EGF-dependent inhibition of glycogen synthase kinase 3 in Swiss 3T3 cells. FEBS Lett 461:120-124
33. Singh TJ, Haque N, Grundke Iqbal I, Iqbal K (1995) Rapid Alzheimer-like phosphorylation of tau by the synergestic actions of non-proline-dependent protein kinases and GSK-3. FEBS Lett 358:267-272
34. Singh TJ, Zaidi T, Grundke-Iqbal I, Iqbal K (1995) Modulation of GSK-3-catalyzed phosphorylation of microtubule-associated protein tau by non-proline-dependent protein kinases. FEBS Lett 358:4-8
35. Sperber BR, Leight S, Goedert M, Lee VM (1995) Glycogen synthase kinase-3 beta phosphorylates tau protein at multiple sites in intact cells. Neurosci Lett 197:149-153
36. Spittaels K, Van den Haute C, Van Dorpe J, Geerts H, Mercken M, Sciot R, Van Lammel A, Loos R, Van Leuven F (2000) Glycogen synthase kinase-3β phosphorylates protein τ and rescues the axonopathy in the central nervous system of human four-repeat τ transgenic mice. J Biol Chem 275:413440-413449
37. Stambolic A, Woodgett JR (1994) Mitogen inactivation of glycogen synthase kinase-3β in intact cells via serine 9 phosphorylation. Biochem J 303:701-704
38. Tolnay M, Probst A (1999) Review: tau protein: pathology in Alzheimer's disease and related disorders. Neuropathol Appl Neurobiol 25:171-187
39. Utton MA, Vandecandelaere A, Wagner U, Reynolds CH, Gibb GM, Miller CC, Bayley PM, Anderton BH (1997) Phosphorylation of tau by glycogen synthase kinase 3beta affects the ability of tau to promote microtubule self-assembly. Biochem J 323:741-747
40. Xiao J, Perry G, Troncoso J, Monteriro MJ (1996) Calcium-calmodulin-dependent kinase II is associated with paired helical filaments of Alzheimer's disease. J Neuropathol Exp Neurol 55:954-963
41. Yamaguchi H, Ishiguro K, Uchida T, Takashima A, Lemere CA, Imahori K (1996) Preferential labeling of Alzheimer neurofibrillary tangles with antisera for tau protein kinase (TPK) I/glycogen synthase kinase-3beta and cyclin-dependent kinase 5, a component of TPK II. Acta Neuropathol 92:232-241
42. Zheng-Fischhöfer Q, Biernat J, Mandelkow EM, Illenberger S, Godemann R, Mandelkow E (1998) Sequential phosphorylation of Tau by glycogen synthase kinase 3beta and protein kinase A at Thr212 and Ser214 generates the Alzheimer-specific epitope of antibody AT100 and requires a paired-helical-filament-like conformation. Eur J Biochem 252:542-552
43. Zhu X, Rottkamp CA, Boux H, Takeda A, Perry G, Smith MA (2000) Activation of p38 kinase links tau phosphorylation, oxidative stress, and cell cycle-related events in Alzheimer disease. J Neuropathol Exp Neurol 59:880-888
44. Zhu X, Raina AK, Rottkamp CA, Aliev G, Perry G, Boux H, Smith MA (2001) Activation and re-distribution of c-Jun N-terminal kinase/stress activated protein kinase in degenerating neurons in Alzheimer's disease. J Neurochem 76:435-441