Tau phosphorylation and neuronal apoptosis induced by the blockade of PP2A preferentially involve GSK3β

Neurochemistry International

Volumn 59, Issue 2, 2011, Pages 235-250

  Martin, Ludovic ^a   Page, Guylene ^b   Terro, Faraj ^a,c  

^a UNIVERSITÉ DE LIMOGES   (France)

^b UNIVERSITÉ DE POITIERS   (France)

^c Hôpital de la Mre et de l'Enfant   (France)

Author keywords

Apoptosis; GSK3 ; PP2A; Tau neurons

Indexed keywords

6 BROMOINDIRUBIN 3' (2 BROMOETHYL) OXIME; CASPASE 3; CYCLIN DEPENDENT KINASE 5; GLYCOGEN SYNTHASE KINASE 3 INHIBITOR; GLYCOGEN SYNTHASE KINASE 3BETA; HARMINE; LITHIUM CHLORIDE; OKADAIC ACID; PHOSPHOPROTEIN PHOSPHATASE 2A; ROSCOVITINE; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; TAU PROTEIN; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DRUG INHIBITION; IMMUNOFLUORESCENCE; IN VITRO STUDY; IN VIVO STUDY; NERVE CELL NECROSIS; NERVE DEGENERATION; NEUROBLASTOMA CELL; NEUROPROTECTION; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; RNA INTERFERENCE; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; GLYCOGEN SYNTHASE KINASE 3; NEURONS; PHOSPHORYLATION; PROTEIN PHOSPHATASE 2; RATS; RATS, WISTAR; TAU PROTEINS;

EID: 79960360530     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2011.05.010     Document Type: Article

References (95)

1. A. Alvarez, R. Toro, A. Caceres, and R.B. Maccioni Inhibition of tau phosphorylating protein kinase CDK5 prevents beta-amyloid-induced neuronal death FEBS Lett. 459 1999 421 426 (Pubitemid 29467380)
2. B.H. Anderton, J. Betts, W.P. Blackstock, J.P. Brion, S. Chapman, and J. Connell Sites of phosphorylation in tau and factors affecting their regulation Biochem. Soc. Symp. 73 2001 80
3. H.K. Arnold, and R.C. Sears A tumor suppressor role for PP2A-B56alpha through negative regulation of c-Myc and other key oncoproteins Cancer Metastasis Rev. 27 2008 147 158
4. D.O. Azorsa, R.H. Robeson, D. Frost, B. Meec hoovet, G.R. Brautigam, and C. Dickey High-content siRNA screening of the kinome identifies kinases involved in Alzheimer's disease-related tau hyperphosphorylation BMC Genomics 11 2010 25
5. K. Baumann, E.M. Mandelkow, J. Biernat, H. Piwnica-Worms, and E. Mandelkow Abnormal Alzheimer-like phosphorylation of tau-protein by cyclin-dependent kinases cdk2 and cdk5 FEBS Lett. 336 1993 417 424 (Pubitemid 24036992)
6. K. Bettayeb, N. Oumata, A. Echalier, Y. Ferandin, J.A. Endicott, and H. Galons CR8 a potent and selective, roscovitine-derived inhibitor of cyclin-dependent kinases Oncogene 27 2008 5797 5807
7. J.P. Brion, B.H. Anderton, M. Authelet, R. Dayanandan, K. Leroy, and S. Lovestone Neurofibrillary tangles and tau phosphorylation Biochem. Soc. Symp. 81 2001 88
8. H. Chen, and S.E. Antonarakis Localisation of a human homologue of the Drosophila mnb and rat Dyrk genes to chromosome 21q22.2 Hum. Genet. 99 1997 262 265 (Pubitemid 27073333)
9. S. Chen, B. Li, I. Grundke-Iqbal, and K. Iqbal I1PP2A affects tau phosphorylation via association with the catalytic subunit of protein phosphatase 2A J. Biol. Chem. 283 2008 10513 10521
10. J.C. Cruz, H.C. Tseng, J.A. Goldman, H. Shih, and L.H. Tsai Aberrant Cdk5 activation by p25 triggers pathological events leading to neurodegeneration and neurofibrillary tangles Neuron 40 2003 471 483 (Pubitemid 37494698)
11. Y. Ding, A. Qiao, and G.H. Fan Indirubin-3′-monoxime rescues spatial memory deficits and attenuates beta-amyloid-associated neuropathology in a mouse model of Alzheimer's disease Neurobiol. Dis. 39 2 2010 156 168
12. T. Engel, P. Goni-Oliver, J.J. Lucas, J. Avila, and F. Hernandez 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 2006 1445 1455 (Pubitemid 44924224)
13. T. Engel, J.J. Lucas, P. Gomez-Ramos, M.A. Moran, J. Avila, and F. Hernandez Co-expression of FTDP-17 tau and GSK-3beta in transgenic mice induce tau polymerization and neurodegeneration Neurobiol. Aging 27 2006 1258 1268 (Pubitemid 44088576)
14. V. Fotaki, M. Dierssen, S. Alcantara, S. Martinez, E. Marti, and C. Casas Dyrk1A haploinsufficiency affects viability and causes developmental delay and abnormal brain morphology in mice Mol. Cell Biol. 22 2002 6636 6647
15. S. Frame, P. Cohen, and R.M. Biondi A common phosphate binding site explains the unique substrate specificity of GSK3 and its inactivation by phosphorylation Mol. Cell 7 2001 1321 1327 (Pubitemid 32607364)
16. A. Garcia, X. Cayla, J. Guergnon, F. Dessauge, V. Hospital, and M.P. Rebollo Serine/threonine protein phosphatases PP1 and PP2A are key players in apoptosis Biochimie 85 2003 721 726 (Pubitemid 37383789)
17. M.M. Gehringer, and L.R. Microcystin Okadaic acid-induced cellular effects: a dualistic response FEBS Lett. 557 2004 1 8 (Pubitemid 38120319)
18. N. Gockler, G. Jofre, C. Papadopoulos, U. Soppa, F.J. Tejedor, and W. Becker Harmine specifically inhibits protein kinase DYRK1A and interferes with neurite formation FEBS J. 276 2009 6324 6337
19. M. Goedert, M.G. Spillantini, R. Jakes, D. Rutherford, and R.A. Crowther Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease Neuron 3 1989 519 526
20. A. Gomez-Ramos, J. Dominguez, D. Zafra, H. Corominola, R. Gomis, and J.J. Guinovart Sodium tungstate decreases the phosphorylation of tau through GSK3 inactivation J. Neurosci. Res. 83 2006 264 273 (Pubitemid 43184390)
21. R. Gomez-Sintes, F. Hernandez, A. Bortolozzi, F. Artigas, J. Avila, and P. Zaratin Neuronal apoptosis and reversible motor deficit in dominant-negative GSK-3 conditional transgenic mice EMBO J. 26 2007 2743 2754 (Pubitemid 46884288)
22. C.X. Gong, and K. Iqbal Hyperphosphorylation of microtubule-associated protein tau: a promising therapeutic target for Alzheimer disease Curr. Med. Chem. 15 2008 2321 2328
23. C.X. Gong, T.J. Singh, I. Grundke-Iqbal, and K. Iqbal Phosphoprotein phosphatase activities in Alzheimer disease brain J. Neurochem. 61 1993 921 927 (Pubitemid 23241228)
24. C.X. Gong, S. Shaikh, J.Z. Wang, T. Zaidi, I. Grundke-Iqbal, and K. Iqbal Phosphatase activity toward abnormally phosphorylated tau: decrease in Alzheimer disease brain J. Neurochem. 65 1995 732 738
25. P. Goni-Oliver, J.J. Lucas, J. Avila, and F. Hernandez N-terminal cleavage of GSK-3 by calpain: a new form of GSK-3 regulation J. Biol. Chem. 282 2007 22406 22413 (Pubitemid 47267365)
26. D.P. Hanger, H.L. Byers, S. Wray, K.Y. Leung, M.J. Saxton, and A. Seereeram Novel phosphorylation sites in tau from Alzheimer brain support a role for casein kinase 1 in disease pathogenesis J. Biol. Chem. 282 2007 23645 23654 (Pubitemid 47311907)
27. D.P. Hanger, B.H. Anderton, and W. Noble Tau phosphorylation: the therapeutic challenge for neurodegenerative disease Trends Mol. Med. 15 2009 112 119
28. F. Hernandez, E. Langa, R. Cuadros, and J. Avila Villanueva N. Regulation of GSK3 isoforms by phosphatases PP1 and PP2A Mol. Cell Biochem. 344 2010 211 215
29. S. Hu, A.N. Begum, M.R. Jones, M.S. Oh, W.K. Beech, and B.H. Beech GSK3 inhibitors show benefits in an Alzheimer's disease (AD) model of neurodegeneration but adverse effects in control animals Neurobiol. Dis. 33 2009 193 206
30. K. Iqbal, F. Liu, C.X. Gong, C. Alonso Adel, and I. Grundke-Iqbal Mechanisms of tau-induced neurodegeneration Acta Neuropathol. 118 2009 53 69
31. V. Janssens, J. Goris, and C. Van Hoof PP2A: the expected tumor suppressor Curr. Opin. Genet Dev. 15 2005 34 41 (Pubitemid 40127629)
32. H. Kamei, T. Saito, M. Ozawa, Y. Fujita, A. Asada, and J.A. Bibb Suppression of calpain-dependent cleavage of the CDK5 activator p35 to p25 by site-specific phosphorylation J. Biol. Chem. 282 2007 1687 1694 (Pubitemid 47076684)
33. J.E. Kang, S.A. Choi, J.B. Park, and K.C. Chung Regulation of the proapoptotic activity of huntingtin interacting protein 1 by Dyrk1 and caspase-3 in hippocampal neuroprogenitor cells J. Neurosci. Res. 81 2005 62 72 (Pubitemid 41139111)
34. H. Kim, S.O. Sablin, and R.R. Ramsay Inhibition of monoamine oxidase A by beta-carboline derivatives Arch. Biochem. Biophys. 337 1997 137 142 (Pubitemid 27198065)
35. R. Kimura, K. Kamino, M. Yamamoto, A. Nuripa, T. Kida, and H. Kazui The DYRK1A gene, encoded in chromosome 21 Down syndrome critical region, bridges between beta-amyloid production and tau phosphorylation in Alzheimer disease Hum. Mol. Genet. 16 2007 15 23 (Pubitemid 46152541)
36. S. Kins, A. Crameri, D.R. Evans, B.A. Hemmings, R.M. Nitsch, and J. Gotz Reduced protein phosphatase 2A activity induces hyperphosphorylation and altered compartmentalization of tau in transgenic mice J. Biol. Chem. 276 2001 38193 38200
37. P.S. Klein, and D.A. Melton A molecular mechanism for the effect of lithium on development Proc. Natl. Acad. Sci. USA 93 1996 8455 8459 (Pubitemid 26269579)
38. L. Kockeritz, B. Doble, S. Patel, and J.R. Woodgett Glycogen synthase kinase-3-an overview of an over-achieving protein kinase Curr. Drug Targets 7 2006 1377 1388 (Pubitemid 44718298)
39. E. Kopke, Y.C. Tung, S. Shaikh, A.C. Alonso, K. Iqbal, and I. Grundke-Iqbal Microtubule-associated protein tau. Abnormal phosphorylation of a non-paired helical filament pool in Alzheimer disease J. Biol. Chem. 268 1993 24374 24384 (Pubitemid 23335430)
40. S. Kosuga, E. Tashiro, T. Kajioka, M. Ueki, Y. Shimizu, and M. Imoto GSK-3beta directly phosphorylates and activates MARK2/PAR-1 J. Biol. Chem. 280 2005 42715 42722 (Pubitemid 43049231)
41. G. Kroemer, L. Galluzzi, P. Vandenabeele, J. Abrams, E.S. Alnemri, and E.H. Baehrecke Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009 Cell Death Differ. 16 2009 3 11
42. A. Laguna, S. Aranda, M.J. Barallobre, R. Barhoum, E. Fernandez, and V. Fotaki The protein kinase DYRK1A regulates caspase-9-mediated apoptosis during retina development Dev. Cell 15 2008 841 853
43. T. Li, and H.K. Paudel Glycogen synthase kinase 3beta phosphorylates Alzheimer's disease-specific Ser396 of microtubule-associated protein tau by a sequential mechanism Biochemistry 45 2006 3125 3133 (Pubitemid 43376331)
44. X. Li, H.J. Yost, D.M. Virshup, and J.M. Seeling Protein phosphatase 2A and its B56 regulatory subunit inhibit Wnt signaling in Xenopus EMBO J. 20 2001 4122 4131 (Pubitemid 32751828)
45. Y.W. Lim, S.Y. Yoon, J.E. Choi, S.M. Kim, H.S. Lee, and H. Choe Maintained activity of glycogen synthase kinase-3beta despite of its phosphorylation at serine-9 in okadaic acid-induced neurodegenerative model Biochem. Biophys. Res. Commun. 395 2010 207 212
46. C.F. Lin, C.L. Chen, C.W. Chiang, M.S. Jan, W.C. Huang, and Y.S. Lin GSK-3beta acts downstream of PP2A and the PI 3-kinase-Akt pathway, and upstream of caspase-2 in ceramide-induced mitochondrial apoptosis J. Cell Sci. 120 2007 2935 2943
47. G. Lindwall, and R.D. Cole Phosphorylation affects the ability of tau protein to promote microtubule assembly J. Biol. Chem. 259 1984 5301 5305 (Pubitemid 14140641)
48. F. Liu, I. Grundke-Iqbal, K. Iqbal, and C.X. Gong Contributions of protein phosphatases PP1, PP2A, PP2B and PP5 to the regulation of tau phosphorylation Eur. J. Neurosci. 22 2005 1942 1950 (Pubitemid 41579384)
49. F. Liu, Z. Liang, J. Wegiel, Y.W. Hwang, K. Iqbal, and I. Grundke-Iqbal Overexpression of Dyrk1A contributes to neurofibrillary degeneration in Down syndrome FASEB J. 22 2008 3224 3233
50. G.P. Liu, Y. Zhang, X.Q. Yao, C.E. Zhang, J. Fang, and Q. Wang Activation of glycogen synthase kinase-3 inhibits protein phosphatase-2A and the underlying mechanisms Neurobiol. Aging 29 2008 1348 1358 (Pubitemid 351970605)
51. R. Liu, X.W. Zhou, H. Tanila, C. Bjorkdahl, J.Z. Wang, and Z.Z. Guan Phosphorylated PP2A (tyrosine 307) is associated with Alzheimer neurofibrillary pathology J. Cell Mol. Med. 12 2008 241 257 (Pubitemid 351430466)
52. J.P. Lopes, C.R. Oliveira, and P. Agostinho Neurodegeneration in an Abeta-induced model of Alzheimer's disease: the role of Cdk5 Aging Cell 9 2010 64 77
53. J.J. Lucas, F. Hernandez, P. Gomez-Ramos, M.A. Moran, R. Hen, and J. Avila Decreased nuclear beta-catenin, tau hyperphosphorylation and neurodegeneration in GSK-3beta conditional transgenic mice EMBO J. 20 2001 27 39 (Pubitemid 32099099)
54. E.T. Lund, R. McKenna, D.B. Evans, S.K. Sharma, and W.R. Mathews Characterization of the in vitro phosphorylation of human tau by tau protein kinase II (cdk5/p20) using mass spectrometry J. Neurochem. 76 2001 1221 1232 (Pubitemid 32167395)
55. L. Martin, A. Magnaudeix, F. Esclaire, C. Yardin, and F. Terro Inhibition of glycogen synthase kinase-3beta downregulates total tau proteins in cultured neurons and its reversal by the blockade of protein phosphatase-2A Brain Res. 1252 2009 66 75
56. L. Martin, X. Latypova, and F. Terro Post-translational modifications of tau protein: implications for Alzheimer's disease Neurochem. Int. 58 2011 458 471
57. M.P. Mazanetz, and P.M. Fischer Untangling tau hyperphosphorylation in drug design for neurodegenerative diseases Nat. Rev. Drug Discov. 6 2007 464 479 (Pubitemid 47064569)
58. L. Meijer, A.L. Skaltsounis, P. Magiatis, P. Polychronopoulos, M. Knockaert, and M. Leost GSK-3-selective inhibitors derived from Tyrian purple indirubins Chem. Biol. 10 2003 1255 1266 (Pubitemid 38050973)
59. V. Meske, F. Albert, and T.G. Ohm Coupling of mammalian target of rapamycin with phosphoinositide 3-kinase signaling pathway regulates protein phosphatase 2A- and glycogen synthase kinase-3-dependent phosphorylation of Tau J. Biol. Chem. 283 2008 100 109
60. F.J. Moreno, M. Medina, M. Perez, E. Montejo de Garcini, and J. Avila Glycogen synthase kinase 3 phosphorylates recombinant human tau protein at serine-262 in the presence of heparin (or tubulin) FEBS Lett. 372 1995 65 68
61. J. Papkoff, and M. Aikawa WNT-1 and HGF regulate GSK3 beta activity and beta-catenin signaling in mammary epithelial cells Biochem. Biophys. Res. Commun. 247 1998 851 858 (Pubitemid 28418480)
62. J.J. Pei, E. Braak, H. Braak, I. Grundke-Iqbal, K. Iqbal, and B. Winblad Distribution of active glycogen synthase kinase 3beta (GSK-3beta) in brains staged for Alzheimer disease neurofibrillary changes J. Neuropathol. Exp. Neurol. 58 1999 1010 1019 (Pubitemid 29441929)
63. S. Peineau, C. Taghibiglou, C. Bradley, T.P. Wong, L. Liu, and J. Lu LTP inhibits LTD in the hippocampus via regulation of GSK3beta Neuron 53 2007 703 717 (Pubitemid 46283369)
64. E. Planel, K. Yasutake, S.C. Fujita, and K. Ishiguro Inhibition of protein phosphatase 2A overrides tau protein kinase I/glycogen synthase kinase 3 beta and cyclin-dependent kinase 5 inhibition and results in tau hyperphosphorylation in the hippocampus of starved mouse J. Biol. Chem. 276 2001 34298 34306
65. F. Plattner, M. Angelo, and K.P. Giese The roles of cyclin-dependent kinase 5 and glycogen synthase kinase 3 in tau hyperphosphorylation J. Biol. Chem. 281 2006 25457 25465 (Pubitemid 44401934)
66. W. Qian, J. Shi, X. Yin, K. Iqbal, I. Grundke-Iqbal, and C.X. Gong PP2A regulates tau phosphorylation directly and also indirectly via activating GSK-3beta J. Alzheimers Dis. 19 2010 1221 1229
67. A. Rametti, F. Esclaire, C. Yardin, N. Cogne, and F. Terro Lithium down-regulates tau in cultured cortical neurons: a possible mechanism of neuroprotection Neurosci. Lett. 434 2008 93 98
68. S.R. Ryoo, H.K. Jeong, C. Radnaabazar, J.J. Yoo, H.J. Cho, and H.W. Lee DYRK1A-mediated hyperphosphorylation of TauA functional link between Down syndrome and Alzheimer disease J. Biol. Chem. 282 2007 34850 34857 (Pubitemid 350232475)
69. A. Seifert, L.A. Allan, and P.R. Clarke DYRK1A phosphorylates caspase 9 at an inhibitory site and is potently inhibited in human cells by harmine FEBS J. 275 2008 6268 6280
70. M.L. Selenica, H.S. Jensen, A.K. Larsen, M.L. Pedersen, L. Helboe, and M. Leist Efficacy of small-molecule glycogen synthase kinase-3 inhibitors in the postnatal rat model of tau hyperphosphorylation Br. J. Pharmacol. 152 2007 959 979 (Pubitemid 350100498)
71. A. Sengupta, Q. Wu, I. Grundke-Iqbal, K. Iqbal, and T.J. Singh Potentiation of GSK-3-catalyzed Alzheimer-like phosphorylation of human tau by cdk5 Mol. Cell Biochem. 167 1997 99 105 (Pubitemid 27081337)
72. N. Sergeant, A. Bretteville, M. Hamdane, M.L. Caillet-Boudin, P. Grognet, S. Bombois, D. Blum, A. Delacourte, F. Pasquier, E. Vanmechelen, S. Schraen-Maschke, and L. Buée Biochemistry of Tau in Alzheimer's disease and related neurological disorders Expert Rev. Proteomics 5 2008 207 224 (Pubitemid 351670926)
73. P. Seubert, M. Mawal-Dewan, R. Barbour, R. Jakes, M. Goedert, and G.V. Johnson Detection of phosphorylated Ser262 in fetal tau, adult tau, and paired helical filament tau J. Biol. Chem. 270 1995 18917 18922
74. W.J. Song, L.R. Sternberg, C. Kasten-Sportes, M.L. Keuren, S.H. Chung, and A.C. Slack Isolation of human and murine homologues of the Drosophila minibrain gene: human homologue maps to 21q22.2 in the Down syndrome "critical region" Genomics 38 1996 331 339 (Pubitemid 27030122)
75. V. Stambolic, and J.R. Woodgett Mitogen inactivation of glycogen synthase kinase-3 beta in intact cells via serine 9 phosphorylation Biochem J 303 3 1994 701 704 (Pubitemid 24325998)
76. G.I. Szendrei, V.M. Lee, and L. Otvos Jr Recognition of the minimal epitope of monoclonal antibody Tau-1 depends upon the presence of a phosphate group but not its location J Neurosci Res 34 1993 243 249 (Pubitemid 23037325)
77. H. Tanimukai, I. Grundke-Iqbal, and K. Iqbal Up-regulation of inhibitors of protein phosphatase-2A in Alzheimer's disease Am J Pathol 166 2005 1761 1771 (Pubitemid 40734399)
78. D. Terwel, D. Muyllaert, I. Dewachter, P. Borghgraef, S. Croes, and H. Devijver Amyloid activates GSK-3beta to aggravate neuronal tauopathy in bigenic mice Am J Pathol 172 2008 786 798 (Pubitemid 351354550)
79. G.A. Turenne, and B.D. Price Glycogen synthase kinase3 beta phosphorylates serine 33 of p53 and activates p53's transcriptional activity BMC Cell Biol 2 2001 12
80. C. Van Hoof, and J. Goris Phosphatases in apoptosis: to be or not to be, PP2A is in the heart of the question Biochim Biophys Acta 1640 2003 97 104 (Pubitemid 36555695)
81. V. Vogelsberg-Ragaglia, T. Schuck, J.Q. Trojanowski, and V.M. Lee PP2A mRNA expression is quantitatively decreased in Alzheimer's disease hippocampus Exp Neurol 168 2001 402 412 (Pubitemid 32289776)
82. K. Vougogiannopoulou, Y. Ferandin, K. Bettayeb, V. Myrianthopoulos, O. Lozach, and Y. Fan Soluble 3', 6-substituted indirubins with enhanced selectivity toward glycogen synthase kinase -3 alter circadian period J Med Chem 51 2008 6421 6431
83. Y. Wada, K. Ishiguro, T.J. Itoh, T. Uchida, H. Hotani, and T. Saito Microtubule-stimulated phosphorylation of tau at Ser202 and Thr205 by cdk5 decreases its microtubule nucleation activity J Biochem 124 1998 738 746 (Pubitemid 28488152)
84. Q.M. Wang, C.J. Fiol, A.A. DePaoli-Roach, and P.J. Roach Glycogen synthase kinase-3 beta is a dual specificity kinase differentially regulated by tyrosine and serine/threonine phosphorylation J Biol Chem 269 1994 14566 14574
85. J.Z. Wang, I. Grundke-Iqbal, and K. Iqbal Kinases and phosphatases and tau sites involved in Alzheimer neurofibrillary degeneration Eur J Neurosci 25 2007 59 68 (Pubitemid 46098893)
86. Y. Wang, J.X. Zhang, X.X. Du, L. Zhao, Q. Tian, and L.Q. Zhu Temporal correlation of the memory deficit with Alzheimer-like lesions induced by activation of glycogen synthase kinase-3 J Neurochem 106 2008 2364 2374
87. J. Wegiel, H.M. Wisniewski, J. Dziewiatkowski, E.R. Popovitch, and M. Tarnawski Differential susceptibility to neurofibrillary pathology among patients with Down syndrome Dementia 7 1996 135 141
88. J.R. Woodgett Molecular cloning and expression of glycogen synthase kinase-3/factor A EMBO J 9 1990 2431 2438
89. Y.L. Woods, P. Cohen, W. Becker, R. Jakes, M. Goedert, and X. Wang The kinase DYRK phosphorylates protein-synthesis initiation factor eIF2Bepsilon at Ser539 and the microtubule-associated protein tau at Thr212: potential role for DYRK as a glycogen synthase kinase 3-priming kinase Biochem J 355 2001 609 615 (Pubitemid 32434076)
90. C. Yost, M. Torres, J.R. Miller, E. Huang, D. Kimelman, and R.T. Moon The axis-inducing activity, stability, and subcellular distribution of beta-catenin is regulated in Xenopus embryos by glycogen synthase kinase 3 Genes Dev 10 1996 1443 1454 (Pubitemid 26260702)
91. J.Y. Yu, J. Taylor, S.L. DeRuiter, A.B. Vojtek, and D.L. Turner Simultaneous inhibition of GSK3alpha and GSK3beta using hairpin siRNA expression vectors Mol Ther 7 2003 228 236 (Pubitemid 36395358)
92. S. Zahler, S. Tietze, F. Totzke, M. Kubbutat, L. Meijer, and A.M. Vollmar Inverse in silico screening for identification of kinase inhibitor targets Chem Biol 14 2007 1207 1214 (Pubitemid 350102244)
93. Zhang, W.; Yang, J.; Liu, Y.; Chen, X.; Yu, T.; Jia, J.; et al.; 2009. PR55alpha, a regulatory subunit of PP2A, specifically regulates PP2A-mediated beta-catenin dephosphorylation. J Biol Chem.
94. Y.L. Zheng, S. Kesavapany, M. Gravell, R.S. Hamilton, M. Schubert, and N. Amin A Cdk5 inhibitory peptide reduces tau hyperphosphorylation and apoptosis in neurons EMBO J 24 2005 209 220 (Pubitemid 40188478)
95. X.W. Zhou, B. Winblad, Z. Guan, and J.J. Pei Interactions between glycogen synthase kinase 3beta, protein kinase B, and protein phosphatase 2A in tau phosphorylation in mouse N2a neuroblastoma cells J Alzheimers Dis 17 2009 929 937