Deconstructing GSK-3: The fine regulation of its activity

International Journal of Alzheimer's Disease

Volumn , Issue , 2011, Pages

  Medina, Miguel ^a   Wandosell, Francisco ^b  

^a Noscira SA   (Spain)

^b CSIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3; TIDEGLUSIB;

ALZHEIMER DISEASE; CELLULAR DISTRIBUTION; DRUG TARGETING; HUMAN; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN COMPLEX FORMATION; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

EID: 79959222357     PISSN: None     EISSN: 20900252     Source Type: Journal    
DOI: 10.4061/2011/479249     Document Type: Review

References (154)

1. Rylatt D. B., Aitken A., Bilham T., Condon G. D., Embi N., Cohen P., Glycogen synthase from rabbit skeletal muscle. Amino acid sequence at the sites phosphorylated by glycogen synthase kinase-3, and extension of the N-terminal sequence containing the site phosphorylated by phosphorylase kinase European Journal of Biochemistry 1980 107 2 529 537
2. Ferkey D. M., Kimelman D., Glycogen synthase kinase-3 mutagenesis identifies a common binding domain for GBP and axin Journal of Biological Chemistry 2002 277 18 16147 16152 (Pubitemid 34967901)
3. Alessi D. R., Caudwell F. B., Andjelkovic M., Hemmings B. A., Cohen P., Molecular basis for the substrate specificity of protein kinase B; comparison with MAPKAP kinase-1 and p70 S6 kinase FEBS Letters 1996 399 3 333 338 (Pubitemid 26426877)
4. Hanger D. P., Hughes K., Woodgett J. R., Brion J. P., Anderton B. H., Glycogen synthase kinase-3 induces Alzheimer's disease-like phosphorylation of tau: generation of paired helical filament epitopes and neuronal localisation of the kinase Neuroscience Letters 1992 147 1 58 62
5. Cohen P., The Croonian Lecture 1998. Identification of a protein kinase cascade of major importance in insulin signal transduction Philosophical Transactions of the Royal Society B 1999 354 1382 485 495 (Pubitemid 29363323)
6. Hart M. J., De Los Santos R., Albert I. N., Rubinfeld B., Polakis P., Downregulation of -catenin by human Axin and its association with the APC tumor suppressor, -catenin and GSK3 Current Biology 1998 8 10 573 581 (Pubitemid 28222891)
7. Garrido J. J., Simn D., Varea O., Wandosell F., GSK3 alpha and GSK3 beta are necessary for axon formation FEBS Letters 2007 581 8 1579 1586 (Pubitemid 46528923)
8. Lucas F. R., Salinas P. C., WNT-7a induces axonal remodeling and increases synapsin I levels in cerebellar neurons Developmental Biology 1997 192 1 31 44 (Pubitemid 28015644)
9. Pap M., Cooper G. M., Role of glycogen synthase kinase-3 in the phosphatidylinositol 3- kinase/Akt cell survival pathway Journal of Biological Chemistry 1998 273 32 19929 19932 (Pubitemid 28377539)
10. Lucas J. J., Hernndez F., Gmez-Ramos P., Morn M. A., Hen R., Avila J., Decreased nuclear -catenin, tau hyperphosphorylation and neurodegeneration in GSK-3 conditional transgenic mice EMBO Journal 2001 20 1-2 27 39 (Pubitemid 32099099)
11. Ishiguro K., Shiratsuchi A., Sato S., Omori A., Arioka M., Kobayashi S., Uchida T., Imahori K., Glycogen synthase kinase 3 is identical to tau protein kinase I generating several epitopes of paired helical filaments FEBS Letters 1993 325 3 167 172 (Pubitemid 23186470)
12. Lovestone S., Reynolds C. H., Latimer D., Davis D. R., Anderton B. H., Gallo J. M., Hanger D., Mulot S., Marquardt B., Stabel S., Woodgett J. R., Miller C. C. J., Alzheimer's disease-like phosphorylation of the microtubule-associated protein tau by glycogen synthase kinase-3 in transfected mammalian cells Current Biology 1994 4 12 1077 1086 (Pubitemid 124001594)
13. Prez M., Rojo A. I., Wandosell F., Daz-Nido J., Avila J., Prion peptide induces neuronal cell death through a pathway involving glycogen synthase kinase 3 Biochemical Journal 2003 372 1 129 136 (Pubitemid 36609614)
14. Kim L., Liu J., Kimmel A. R., The novel tyrosine kinase ZAK1 activates GSK3 to direct cell fate specification Cell 1999 99 4 399 408
15. Itoh K., Tang T. L., Neel B. G., Sokol S. Y., Specific modulation of ectodermal cell fates in Xenopus embryos by glycogen synthase kinase Development 1995 121 12 3979 3988 (Pubitemid 26007349)
16. Ruel L., Bourouis M., Heitzler P., Pantesco V., Simpson P., Drosophila shaggy kinase and rat glycogen synthase kinase-3 have conserved activities and act downstream of Notch Nature 1993 362 6420 557 560 (Pubitemid 23113033)
17. Frame S., Cohen P., GSK3 takes centre stage more than 20 years after its discovery Biochemical Journal 2001 359 1 1 16 (Pubitemid 32939202)
18. Grimes C. A., Jope R. S., The multifaceted roles of glycogen synthase kinase 3 in cellular signaling Progress in Neurobiology 2001 65 4 391 426 (Pubitemid 32781670)
19. Woodgett J. R., Molecular cloning and expression of glycogen synthase kinase-3/Factor A EMBO Journal 1990 9 8 2431 2438
20. Mukai F., Ishiguro K., Sano Y., Fujita S. C., Aternative splicing isoform of tau protein kinase I/glycogen synthase kinase 3 Journal of Neurochemistry 2002 81 5 1073 1083 (Pubitemid 34809290)
21. Dajani R., Fraser E., Roe S. M., Young N., Good V., Dale T. C., Pearl L. H., Crystal structure of glycogen synthase kinase 3 : structural basis for phosphate-primed substrate specificity and autoinhibition Cell 2001 105 6 721 732 (Pubitemid 32635102)
22. Ter Haar E., Coll J. T., Austen D. A., Hsiao H. M., Swenson L., Jain J., Structure of GSK3 reveals a primed phosphorylation mechanism Nature Structural Biology 2001 8 7 593 596 (Pubitemid 32613006)
23. Noble W., Planel E., Zehr C., Olm V., Meyerson J., Suleman F., Gaynor K., Wang L., LaFrancois J., Feinstein B., Burns M., Krishnamurthy P., Wen YI., Bhat R., Lewis J., Dickson D., Duff K., Inhibition of glycogen synthase kinase-3 by lithium correlates with reduced tauopathy and degeneration in vivo Proceedings of the National Academy of Sciences of the United States of America 2005 102 19 6990 6995 (Pubitemid 40675429)
24. Bain J., Plater L., Elliott M., Shpiro N., Hastie C. J., Mclauchlan H., Klevernic I., Arthur J. S. C., Alessi D. R., Cohen P., The selectivity of protein kinase inhibitors: a further update Biochemical Journal 2007 408 3 297 315
25. Fraser E., Young N., Dajani R., Franca-Koh J., Ryves J., Williams R. S. B., Yeo M., Webster M. T., Richardson C., Smalley M. J., Pearl L. H., Harwood A., Dale T. C., Identification of the Axin and Frat binding region of glycogen synthase kinase-3 Journal of Biological Chemistry 2002 277 3 2176 2185 (Pubitemid 34968804)
26. Dajani R., Fraser E., Roe S. M., Yeo M., Good V. M., Thompson V., Dale T. C., Pearl L. H., Structural basis for recruitment of glycogen synthase kinase 3 to the axin-APC scaffold complex EMBO Journal 2003 22 3 494 501 (Pubitemid 36193594)
27. Wang Q. M., Fiol C. J., DePaoli-Roach A. A., Roach P. J., Glycogen synthase kinase-3 is a dual specificity kinase differentially regulated by tyrosine and serine/threonine phosphorylation Journal of Biological Chemistry 1994 269 20 14566 14574
28. Harwood A. J., Regulation of GSK-3: a cellular multiprocessor Cell 2001 105 7 821 824 (Pubitemid 32635083)
29. Sutherland C., Leighton I. A., Cohen P., Inactivation of glycogen synthase kinase-3 by phosphorylation: new kinase connections in insulin and growth-factor signalling Biochemical Journal 1993 296 1 15 19 (Pubitemid 23344723)
30. Stambolic V., Woodgett J. R., Mitogen inactivation of glycogen synthase kinase-3 in intact cells via serine 9 phosphorylation Biochemical Journal 1994 303 3 701 704 (Pubitemid 24325998)
31. Frame S., Cohen P., Biondi R. M., A common phosphate binding site explains the unique substrate specificity of GSK3 and its inactivation by phosphorylation Molecular Cell 2001 7 6 1321 1327 (Pubitemid 32607364)
32. Delcommenne M., Tan C., Gray V., Rue L., Woodgett J., Dedhar S., Phosphoinositide-3-OH kinase-dependent regulation of glycogen synthase kinase 3 and protein kinase B/AKT by the integrin-linked kinase Proceedings of the National Academy of Sciences of the United States of America 1998 95 19 11211 11216 (Pubitemid 28450107)
33. Fang X., Yu S. X., Lu Y., Bast R. C., Woodgett J. R., Mills G. B., Phosphorylation and inactivation of glycogen synthase kinase 3 by protein kinase A Proceedings of the National Academy of Sciences of the United States of America 2000 97 22 11960 11965
34. Cardona-Gomez P., Perez M., Avila J., Garcia-Segura L. M., Wandosell F., Estradiol inhibits GSK3 and regulates interaction of estrogen receptors, GSK3, and beta-catenin in the hippocampus Molecular and Cellular Neuroscience 2004 25 3 363 373 (Pubitemid 38366402)
35. Ding Q., Xia W., Liu J. C., Yang J. Y., Lee D. F., Xia J., Bartholomeusz G., Li Y., Pan Y., Li Z., Bargou R. C., Qin J., Lai C. C., Tsai F. J., Tsai C. H., Hung M. C., Erk associates with and primes GSK-3 for its inactivation resulting in upregulation of -catenin Molecular Cell 2005 19 2 159 170 (Pubitemid 41019664)
36. Thornton T. M., Pedraza-Alva G., Deng B., Wood C. D., Aronshtam A., Clements J. L., Sabio G., Davis R. J., Matthews D. E., Doble B., Rincon M., Phosphorylation by p38 MAPK as an alternative pathway for GSK3 inactivation Science 2008 320 5876 667 670 (Pubitemid 351928349)
37. Sayas C. L., Moreno-Flores M. T., Avila J., Wandosell F., The neurite retraction induced by lysophosphatidic acid increases Alzheimer's disease-like Tau phosphorylation Journal of Biological Chemistry 1999 274 52 37046 37052
38. Lesort M., Jope R. S., Johnson G. V. W., Insulin transiently increases tau phosphorylation: involvement of glycogen synthase kinase-3 and Fyn tyrosine kinase Journal of Neurochemistry 1999 72 2 576 584 (Pubitemid 29055219)
39. Hartigan J. A., Xiong W. C., Johnson G. V. W., Glycogen synthase kinase 3 is tyrosine phosphorylated by PYK2 Biochemical and Biophysical Research Communications 2001 284 2 485 489 (Pubitemid 32918003)
40. Kim L., Harwood A., Kimmel A. R., Receptor-dependent and tyrosine phosphatase-mediated inhibition of GSK3 regulates cell fate choice Developmental Cell 2002 3 4 523 532 (Pubitemid 35252261)
41. Cole A., Frame S., Cohen P., Further evidence that the tyrosine phosphorylation of glycogen synthase kinase-3 (GSK3) in mammalian cells is an autophosphorylation event Biochemical Journal 2004 377 1 249 255 (Pubitemid 38114452)
42. Cohen P., Goedert M., GSK3 inhibitors: development and therapeutic potential Nature Reviews Drug Discovery 2004 3 6 479 487 (Pubitemid 38807530)
43. Buch I., Fishelovitch D., London N., Raveh B., Wolfson H. J., Nussinov R., Allosteric regulation of glycogen synthase kinase 3: A theoretical study Biochemistry 2010 49 51 10890 10901
44. Simn D., Benitez M. J., Gimenez-Cassina A., Garrido J. J., Bhat R. V., Daz-Nido J., Wandosell F., Pharmacological inhibition of GSK-3 is not strictly correlated with a decrease in tyrosine phosphorylation of residues 216/279 Journal of Neuroscience Research 2008 86 3 668 674 (Pubitemid 351204481)
45. Muoz-Montao J. R., Moreno F. J., Avila J., Daz-Nido J., Lithium inhibits Alzheimer's disease-like tau protein phosphorylation in neurons FEBS Letters 1997 411 2-3 183 188 (Pubitemid 27301451)
46. Takashima A., Honda T., Yasutake K., Michel G., Murayama O., Murayama M., Ishiguro K., Yamaguchi H., Activation of tau protein kinase I/glycogen synthase kinase-3 by amyloid peptide (25-35) enhances phosphorylation of tau in hippocampal neurons Neuroscience Research 1998 31 4 317 323 (Pubitemid 28446014)
47. Moon R. T., Kohn A. D., De Ferrari G. V., Kaykas A., WNT and -catenin signalling: diseases and therapies Nature Reviews Genetics 2004 5 9 691 701 (Pubitemid 39150127)
48. Aberle H., Bauer A., Stappert J., Kispert A., Kemler R., α-catenin is a target for the ubiquitin-proteasome pathway EMBO Journal 1997 16 13 3797 3804
49. Castao Z., Gordon-Weeks P. R., Kypta R. M., The neuron-specific isoform of glycogen synthase kinase-3 is required for axon growth Journal of Neurochemistry 2010 113 1 117 130
50. Li L., Yuan H., Weaver C. D., Mao J., Farr G. H., Sussman D. J., Jonkers J., Kimelman D., Wu D., Axin and Frat1 interact with Dvl and GSK, bridging Dvl to GSK in Wnt-mediated regulation of LEF-1 EMBO Journal 1999 18 15 4233 4240 (Pubitemid 29364125)
51. Yost C., Farr G. H., Pierce S. B., Ferkey D. M., Chen M. M., Kimelman D., GBP, an inhibitor of GSK-3, is implicated in Xenopus development and oncogenesis Cell 1998 93 6 1031 1041 (Pubitemid 28280796)
52. Stoothoff W. H., Cho J.-H., McDonald R. P., Johnson G. V.W., FRAT-2 preferentially increases glycogen synthase kinase 3 -mediated phosphorylation of primed sites, which results in enhanced tau phosphorylation Journal of Biological Chemistry 2005 280 1 270 276 (Pubitemid 40164989)
53. Van Amerongen R., Nawijn M., Franca-Koh J., Zevenhoven J., Van Der Gulden H., Jonkers J., Berns A., Frat is dispensable for canonical Wnt signaling in mammals Genes and Development 2005 19 4 425 430 (Pubitemid 40256273)
54. Chou H. Y., Howng S. L., Cheng T. S., Hsiao Y. L., Lieu A. S., Loh J. K., Hwang S. L., Lin C. C., Hsu C. M., Wang C., Lee C. I., Lu P. J., Chou C. K., Huang C. Y., Hong YI. R., GSKIP is homologous to the axin GSK3 interaction domain and functions as a negative regulator of GSK3 Biochemistry 2006 45 38 11379 11389 (Pubitemid 44453986)
55. Alonso A. D. C., Li B., Grundke-Iqbal I., Iqbal K., Polymerization of hyperphosphorylated tau into filaments eliminates its inhibitory activity Proceedings of the National Academy of Sciences of the United States of America 2006 103 23 8864 8869 (Pubitemid 43878109)
56. Noble W., Olm V., Takata K., Casey E., Mary O., Meyerson J., Gaynor K., LaFrancois J., Wang L., Kondo T., Davies P., Burns M., Veeranna., Nixon R., Dickson D., Matsuoka Y., Ahlijanian M., Lau L. F., Duff K., Cdk5 is a key factor in tau aggregation and tangle formation in vivo Neuron 2003 38 4 555 565 (Pubitemid 36645031)
57. Sengupta A., Wu Q., Grundke-Iqbal I., Iqbal K., Singh T. J., Potentiation of GSK-3-catalyzed Alzheimer-like phosphorylation of human tau by cdk5 Molecular and Cellular Biochemistry 1997 167 1-2 99 105 (Pubitemid 27081337)
58. Nishimura I., Yang Y., Lu B., PAR-1 kinase plays an initiator role in a temporally ordered phosphorylation process that confers tau toxicity in Drosophila Cell 2004 116 5 671 682 (Pubitemid 38326726)
59. Amit S., Hatzubai A., Birman Y., Andersen J. S., Ben-Shushan E., Mann M., Ben-Neriah Y., Alkalay I., Axin-mediated CKI phosphorylation of -catenin at Ser 45: a molecular switch for the Wnt pathway Genes and Development 2002 16 9 1066 1076 (Pubitemid 34507196)
60. Liu S. J., Zhang A. H., Li H. L., Wang Q., Deng H. M., Netzer W. J., Xu H., Wang J. Z., Overactivation of glycogen synthase kinase-3 by inhibition of phosphoinositol-3 kinase and protein kinase C leads to hyperphosphorylation of tau and impairment of spatial memory Journal of Neurochemistry 2003 87 6 1333 1344 (Pubitemid 38020568)
61. Twomey C., McCarthy J. V., Presenilin-1 is an unprimed glycogen synthase kinase-3 substrate FEBS Letters 2006 580 17 4015 4020 (Pubitemid 44037562)
62. Soutar M. P. M., Kim W.-Y., Williamson R., Peggie M., Hastie C. J., McLauchlan H., Snider W. D., Gordon-Weeks P. R., Sutherland C., Evidence that glycogen synthase kinase-3 isoforms have distinct substrate preference in the brain Journal of Neurochemistry 2010 115 4 974 983
63. Takahashi M., Tomizawa K., Kato R., Sato K., Uchida T., Fujita S. C., Imahori K., Localization and developmental changes of protein kinase I/glycogen synthase kinase-3 in rat brain Journal of Neurochemistry 1994 63 1 245 255 (Pubitemid 24184925)
64. Eickholt B. J., Walsh F. S., Doherty P., An inactive pool of GSK-3 at the leading edge of growth cones is implicated in Semaphorin 3A signaling Journal of Cell Biology 2002 157 2 211 217 (Pubitemid 34839818)
65. Zhou F. Q., Zhou J., Dedhar S., Wu Y. H., Snider W. D., NGF-induced axon growth is mediated by localized inactivation of GSK-3 and functions of the microtubule plus end binding protein APC Neuron 2004 42 6 897 912 (Pubitemid 38798229)
66. Watcharasit P., Bijur G. N., Zmijewski J. W., Song L., Zmijewska A., Chen X., Johnson G. V. W., Jope R. S., Direct, activating interaction between glycogen synthase kinase-3 and p53 after DNA damage Proceedings of the National Academy of Sciences of the United States of America 2002 99 12 7951 7955 (Pubitemid 34650986)
67. Bijur G. N., Jope R. S., Glycogen synthase kinase-3 beta is highly activated in nuclei and mitochondria Neuroreport 2003 14 18 2415 2419
68. Morel C., Carlson S. M., White F. M., Davis R. J., Mcl-1 integrates the opposing actions of signaling pathways that mediate survival and apoptosis Molecular and Cellular Biology 2009 29 14 3845 3852
69. Gimenez-Cassina A., Lim F., Cerrato T., Palomo G. M., Diaz-Nido J., Mitochondrial hexokinase II promotes neuronal survival and acts downstream of glycogen synthase kinase-3 Journal of Biological Chemistry 2009 284 5 3001 3011
70. Cohen P., Frame S., The renaissance of GSK3 Nature Reviews Molecular Cell Biology 2001 2 10 769 776 (Pubitemid 33679839)
71. Xu C., Kim N. G., Gumbiner B. M., Regulation of protein stability by GSK3 mediated phosphorylation Cell Cycle 2009 8 24 4032 4039
72. Avila J., Lucas J. J., Prez M., Hernndez F., Role of tau protein in both physiological and pathological conditions Physiological Reviews 2004 84 2 361 384 (Pubitemid 38365487)
73. Bijur G. N., Jope R. S., Proapoptotic stimuli induce nuclear accumulation of glycogen synthase kinase-3 beta Journal of Biological Chemistry 2001 276 40 37436 37442
74. Taelman V. F., Dobrowolski R., Plouhinec J.-L., Fuentealba L. C., Vorwald P. P., Gumper I., Sabatini D. D., De Robertis E. M., Wnt signaling requires sequestration of Glycogen Synthase Kinase 3 inside multivesicular endosomes Cell 2010 143 7 1136 1148
75. Goi-Oliver P., Lucas J. J., Avila J., Hernndez F., N-terminal cleavage of GSK-3 by calpain: a new form of GSK-3 regulation Journal of Biological Chemistry 2007 282 31 22406 22413 (Pubitemid 47267365)
76. Goi-Oliver P., Avila J., Hernndez F., Calpain-mediated truncation of GSK-3 in post-mortem brain samples Journal of Neuroscience Research 2009 87 5 1156 1161
77. Abe K., Takeichi M., NMDA-receptor activation induces calpain-mediated beta-catenin cleavages for triggering gene expression Neuron 2007 53 3 387 397 (Pubitemid 46178410)
78. Kandasamy A. D., Schulz R., Glycogen synthase kinase-3 is activated by matrix metalloproteinase-2 mediated proteolysis in cardiomyoblasts Cardiovascular Research 2009 83 4 698 706
79. Cohen P., The coordinated control of metabolic pathways by broad-specificity protein kinases and phosphatases Current Topics in Cellular Regulation 1985 27 23 37
80. Cross D. A. E., Alessi D. R., Cohen P., Andjelkovich M., Hemmings B. A., Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B Nature 1995 378 6559 785 789 (Pubitemid 26004411)
81. Crowder R. J., Freeman R. S., Glycogen synthase kinase-3 activity is critical for neuronal death caused by inhibiting phosphatidylinositol 3-kinase or Akt but not for death caused by nerve growth factor withdrawal Journal of Biological Chemistry 2000 275 44 34266 34271
82. Mai L., Jope R. S., Li X., BDNF-mediated signal transduction is modulated by GSK3 and mood stabilizing agents Journal of Neurochemistry 2002 82 1 75 83 (Pubitemid 34755251)
83. He X., Saint-Jeanneti J.-P., Woodgett J. R., Varmas H. E., Dawld I. B., Glycogen synthase kinase-3 and dorsoventral patterning in Xenopus embryos Nature 1995 374 6523 617 622
84. Siegfried E., Chou T. B., Perrimon N., Wingless signaling acts through zeste-white 3, the Drosophila homolog of glycogen synthase kinase-3, to regulate engrailed and establish cell fate Cell 1992 71 7 1167 1179 (Pubitemid 23016551)
85. Salinas P. C., Signaling at the vertebrate synapse: new roles for embryonic morphogens? Journal of Neurobiology 2005 64 4 435 445 (Pubitemid 41114051)
86. He X., Semenov M., Tamai K., Zeng X., LDL receptor-related proteins 5 and 6 in Wnt/ -catenin signaling: arrows point the way Development 2004 131 8 1663 1677 (Pubitemid 38559836)
87. van Amerongen R., Nusse R., Towards an integrated view of Wnt signaling in development Development 2009 136 19 3205 3214
88. Hur E. M., Zhou F. Q., GSK3 signalling in neural development Nature Reviews Neuroscience 2010 11 539 551
89. Zeng X., Tamai K., Doble B., Li S., Huang H., Habas R., Okamura H., Woodgett J., He X., A dual-kinase mechanism for Wnt co-receptor phosphorylation and activation Nature 2005 438 7069 873 877 (Pubitemid 41753071)
90. Niehrs C., Shen J., Regulation of Lrp6 phosphorylation Cellular and Molecular Life Sciences 2010 67 2551 2562
91. Kim N. G., Xu C., Gumbiner B. M., Identification of targets of the Wnt pathway destruction complex in addition to -catenin Proceedings of the National Academy of Sciences of the United States of America 2009 106 13 5165 5170
92. Hsu W., Zeng L., Costantini F., Identification of a domain of axin that binds to the serine/threonine protein phosphatase 2A and a self-binding domain Journal of Biological Chemistry 1999 274 6 3439 3445 (Pubitemid 29077183)
93. Seeling J. M., Miller J. R., Gil R., Moon R. T., White R., Virshup D. M., Regulation of -catenin signaling by the B56 subunit of protein phosphatase 2A Science 1999 283 5410 2089 2091
94. Beato M., Klug J., Steroid hormone receptors: an update Human Reproduction Update 2000 6 3 225 236 (Pubitemid 30348891)
95. Beato M., Snchez-Pacheco A., Interaction of steroid hormone receptors with the transcription initiation complex Endocrine Reviews 1996 17 6 587 609 (Pubitemid 26425258)
96. Mendez P., Azcoitia I., Garcia-Segura L. M., Interdependence of oestrogen and insulin-like growth factor-I in the brain: potential for analysing neuroprotective mechanisms Journal of Endocrinology 2005 185 1 11 17 (Pubitemid 40585063)
97. Mendez P., Azcoitia I. N., Garcia-Segura L. M., Estrogen receptor alpha forms estrogen-dependent multimolecular complexes with insulin-like growth factor receptor and phosphatidylinositol 3-kinase in the adult rat brain Molecular Brain Research 2003 112 1-2 170 176 (Pubitemid 36369259)
98. Varea O., Garrido J. J., Dopazo A., Mendez P., Garcia-Segura L. M., Wandosell F., Estradiol activates -catenin dependent transcription in neurons PLoS ONE 2009 4 4
99. Varea O., Arevalo M. A., Garrido J. J., Garcia-Segura L. M., Wandosell F., Mendez P., Interaction of estrogen receptors with insulin-like growth factor-I and Wnt signaling in the nervous system Steroids 2010 75 8-9 565 569
100. Tigyi G., Fischer D. J., Sebk A., Marshall F., Dyer D. L., Miledi R., Lysophosphatidic acid-induced neurite retraction in PC12 cells: neurite-protective effects of cyclic AMP signaling Journal of Neurochemistry 1996 66 2 549 558
101. Kranenburg O., Poland M., Van Horck F. P. G., Drechsel D., Hall A., Moolenaar W. H., Activation of RhoA by lysophosphatidic acid and G (12/13) subunits in neuronal cells: induction of neurite retraction Molecular Biology of the Cell 1999 10 6 1851 1857
102. Chun J., Goetzl E. J., Hla T., Igarashi Y., Lynch K. R., Moolenaar W., Pyne S., Tigyi G., International Union of Pharmacology. XXXIV. Lysophospholipid receptor nomenclature Pharmacological Reviews 2002 54 2 265 269 (Pubitemid 34575716)
103. Lin M. E., Herr D. R., Chun J., Lysophosphatidic acid (LPA) receptors: signaling properties and disease relevance Prostaglandins and Other Lipid Mediators 2010 91 3-4 130 138
104. Sayas C. L., Moreno-Flores M. T., Avila J., Wandosell F., The neurite retraction induced by lysophosphatidic acid increases Alzheimer's disease-like Tau phosphorylation Journal of Biological Chemistry 1999 274 52 37046 37052
105. Sayas C. L., Avila J., Wandosell F., Glycogen synthase kinase-3 is activated in neuronal cells by G 12 and G 13 by Rho-independent and Rho-dependent mechanisms Journal of Neuroscience 2002 22 16 6863 6875 (Pubitemid 35379144)
106. Sayas C. L., vila J., Wandosell F., Regulation of neuronal cytoskeleton by lysophosphatidic acid: role of GSK-3 Biochimica et Biophysica Acta 2002 1582 13 144 153 (Pubitemid 34634123)
107. Beffert U., Morfini G., Bock H. H., Reyna H., Brady S. T., Herz J., Reelin-mediated signaling locally regulates protein kinase B/Akt and glycogen synthase kinase 3 Journal of Biological Chemistry 2002 277 51 49958 49964 (Pubitemid 36014446)
108. Del Ro J. A., Gonzlez-Billault C., Urea J. M., Jimnez E. M., Barallobre M. J., Pascual M., Pujadas L., Sim S., La Torre A., Wandosell F., vila J., Soriano E., MAP1B is required for netrin 1 signaling in neuronal migration and axonal guidance Current Biology 2004 14 10 840 850 (Pubitemid 38800905)
109. Gonzlez-Billault C., Del Ro J. A., Urea J. M., Jimnez-Mateos E. M., Barallobre M. J., Pascual M., Pujadas L., Sim S., La Torre A., Gavin R., Wandosell F., Soriano E., vila J., A role of MAP1B in reelin-dependent neuronal migration Cerebral Cortex 2005 15 8 1134 1145 (Pubitemid 41373606)
110. Martnez A., Castro A., Medina M., Glycogen Synthase Kinase 3 (GSK-3) and Its Inhibitors-Drug discovery and Development 2006 New York, NY, USA John Wiley Sons Wiley Series, Drug Discovery and Development
111. Klein P. S., Melton D. A., A molecular mechanism for the effect of lithium on development Proceedings of the National Academy of Sciences of the United States of America 1996 93 16 8455 8459 (Pubitemid 26269579)
112. Li-Smerin Y., Levitan E. S., Johnson J. W., Free intracellular Mg concentration and inhibition of NMDA responses in cultured rat neurons Journal of Physiology 2001 533 3 729 743 (Pubitemid 32600528)
113. Chen G., Huang L. D., Jiang Y. M., Manji H. K., The mood-stabilizing agent valproate inhibits the activity of glycogen synthase kinase-3 Journal of Neurochemistry 1999 72 3 1327 1330 (Pubitemid 29085050)
114. Rosenberg G., The mechanisms of action of valproate in neuropsychiatric disorders: can we see the forest for the trees? Cellular and Molecular Life Sciences 2007 64 16 2090 2103 (Pubitemid 350092420)
115. Jope R. S., Anti-bipolar therapy: mechanism of action of lithium Molecular Psychiatry 1999 4 2 117 128 (Pubitemid 29163975)
116. York J. D., Ponder J. W., Majerus P. W., Definition of a metal-dependent/Li(+)-inhibited phosphomonoesterase protein family based upon a conserved three-dimensional core structure Proceedings of the National Academy of Sciences of the United States of America 1995 92 11 5149 5153
117. Ray W. J., Szymanki E. S., Ng L., The binding of lithium and of anionic metabolites to phosphoglucomutase Biochimica et Biophysica Acta 1978 522 2 434 442 (Pubitemid 8274356)
118. Shaldubina A., Agam G., Belmaker R. H., The mechanism of lithium action: state of the art, ten years later Progress in Neuro-Psychopharmacology and Biological Psychiatry 2001 25 4 855 866 (Pubitemid 32374970)
119. Gould T. D., Manji H. K., Signaling networks in the pathophysiology and treatment of mood disorders Journal of Psychosomatic Research 2002 53 2 687 697 (Pubitemid 36292448)
120. Phiel C. J., Wilson C. A., Lee V. M. Y., Klein P. S., GSK-3 regulates production of Alzheimer's disease amyloid- peptides Nature 2003 423 6938 435 439 (Pubitemid 36626994)
121. Li X., Bijur G. N., Jope R. S., Glycogen synthase kinase-3, mood stabilizers, and neuroprotection Bipolar Disorders 2002 4 2 137 144 (Pubitemid 34411276)
122. Rowe M. K., Wiest C., Chuang D. M., GSK-3 is a viable potential target for therapeutic intervention in bipolar disorder Neuroscience and Biobehavioral Reviews 2007 31 6 920 931 (Pubitemid 47285347)
123. Yang S. D., Yu J. S., Lee T. T., Yang C. C., Ni M. H., Yang Y. Y., Dysfunction of protein kinase FA/GSK-3 in lymphocytes of patients with schizophrenic disorder Journal of Cellular Biochemistry 1995 59 1 108 116
124. Kozlovsky N., Belmaker R. H., Agam G., Low GSK-3 immunoreactivity in postmortem frontal cortex of schizophrenic patients American Journal of Psychiatry 2000 157 5 831 833 (Pubitemid 30249669)
125. Lipina T. V., Kaidanovich-Beilin O., Patel S., Wang M., Clapcote S. J., Liu F., Woodgett J. R., Roder J. C., Genetic and pharmacological evidence for schizophrenia-related Disc1 interaction with GSK-3 Synapse 2011 65 3 234 248
126. Pei J. J., Tanaka T., Tung Y. C., Braak E., Iqbal K., Grundke-Iqbal I., Distribution, levels, and activity of glycogen synthase kinase-3 in the Alzheimer disease brain Journal of Neuropathology and Experimental Neurology 1997 56 1 70 78 (Pubitemid 127470328)
127. Leroy K., Boutajangout A., Authelet M., Woodgett J. R., Anderton B. H., Brion J. P., The active form of glycogen synthase kinase-3 is associated with granulovacuolar degeneration in neurons in Alzheimers's disease Acta Neuropathologica 2002 103 2 91 99 (Pubitemid 36067485)
128. Medina M., Avila J., Glycogen synthase kinase-3 (GSK-3) inhibitors for the treatment of Alzheimer's disease Current Pharmaceutical Design 2010 16 25 2790 2798
129. Hooper C., Killick R., Lovestone S., The GSK3 hypothesis of Alzheimer's disease Journal of Neurochemistry 2008 104 6 1433 1439 (Pubitemid 351316776)
130. Muyllaert D., Kremer A., Jaworski T., Borghgraef P., Devijver H., Croes S., Dewachter I., Van Leuven F., Glycogen synthase kinase-3, or a link between amyloid and tau pathology? Genes, Brain and Behavior 2008 7 supplement 1 57 66
131. Takashima A., Noguchi K., Michel G., Mercken M., Hoshi M., Ishiguro K., Imahori K., Exposure of rat hippocampal neurons to amyloid peptide (25-35) induces the inactivation of phosphatidyl inositol-3 kinase and the activation of tau protein kinase I/glycogen synthase kinase-3 β Neuroscience Letters 1996 203 1 33 36
132. Ferreira A., Lu Q., Orecchio L., Kosik K. S., Selective phosphorylation of adult tau isoforms in mature hippocampal neurons exposed to fibrillar a Molecular and Cellular Neurosciences 1997 9 3 220 234 (Pubitemid 27323434)
133. Takashima A., Noguchi K., Sato K., Hoshino T., Imahori K., tau Protein kinase I is essential for amyloid β-protein-induced neurotoxicity Proceedings of the National Academy of Sciences of the United States of America 1993 90 16 7789 7793 (Pubitemid 23250036)
134. Busciglio J., Lorenzo A., Yeh J., Yankner B. A., α-Amyloid fibrils induce tau phosphorylation and loss of microtubule binding Neuron 1995 14 4 879 888
135. Prez M., Ribe E., Rubio A., Lim F., Morn M. A., Ramos P. G., Ferrer I., Isla M. T. G., Avila J., Characterization of a double (amyloid precursor protein-tau) transgenic: tau phosphorylation and aggregation Neuroscience 2005 130 2 339 347 (Pubitemid 40125472)
136. Rib E. M., Prez M., Puig B., Gich I., Lim F., Cuadrado M., Sesma T., Catena S., Snchez B., Nieto M., Gmez-Ramos P., Morn M. A., Cabodevilla F., Samaranch L., Ortiz L., Prez A., Ferrer I., Avila J., Gmez-Isla T., Accelerated amyloid deposition, neurofibrillary degeneration and neuronal loss in double mutant APP/tau transgenic mice Neurobiology of Disease 2005 20 3 814 822 (Pubitemid 41619357)
137. Aplin A. E., Gibb G. M., Jacobsen J. S., Gallo J. M., Anderton B. H., In vitro phosphorylation of the cytoplasmic domain of the amyloid precursor protein by glycogen synthase kinase-3 Journal of Neurochemistry 1996 67 2 699 707 (Pubitemid 26255667)
138. Rockenstein E., Torrance M., Adame A., Mante M., Bar-on P., Rose J. B., Crews L., Masliah E., Neuroprotective effects of regulators of the glycogen synthase kinase-3 signaling pathway in a transgenic model of Alzheimer's disease are associated with reduced amyloid precursor protein phosphorylation Journal of Neuroscience 2007 27 8 1981 1991
139. Hernndez F., Avila J., Tauopathies Cellular and Molecular Life Sciences 2007 64 17 2219 2233 (Pubitemid 47347961)
140. Medina M., Recent developments in tau-based therapeutics for neurodegenerative diseases Recent Patents on CNS Drug Discovery 2011 6 1 20 30
141. Caccamo A., Oddo S., Tran L. X., LaFerla F. M., Lithium reduces tau phosphorylation but not A or working memory deficits in a transgenic model with both plaques and tangles American Journal of Pathology 2007 170 5 1669 1675 (Pubitemid 47339311)
142. Bhat R. V., Shanley J., Correll M. P., Fieles W. E., Keith R. A., Scott C. W., Lee C. M., Regulation and localization of tyrosine phosphorylation of glycogen synthase kinase-3 in cellular and animal models of neuronal degeneration Proceedings of the National Academy of Sciences of the United States of America 2000 97 20 11074 11079
143. Nonaka S., Chuang D. M., Neuroprotective effects of chronic lithium on focal cerebral ischemia in rats NeuroReport 1998 9 9 2081 2084 (Pubitemid 28300570)
144. Koh S. H., Yoo A. R., Chang D. I., Hwang S. J., Kim S. H., Inhibition of GSK-3 reduces infarct volume and improves neurobehavioral functions Biochemical and Biophysical Research Communications 2008 371 4 894 899
145. Garcea G., Manson M. M., Neal C. P., Pattenden C. J., Sutton C. D., Dennison A. R., Berry D. P., Glycogen synthase kinase-3 beta; A new target in pancreatic cancer? Current Cancer Drug Targets 2007 7 3 209 215 (Pubitemid 46699072)
146. Obligado S. H., Ibraghimov-Beskrovnaya O., Zuk A., Meijer L., Nelson P. J., CDK/GSK-3 inhibitors as therapeutic agents for parenchymal renal diseases Kidney International 2008 73 6 684 690 (Pubitemid 351323251)
147. Dewhurst S., Maggirwar S. B., Schifitto G., Gendelman H. E., Gelbard H. A., Glycogen synthase kinase 3 beta (GSK-3 ) as a therapeutic target in neuroAIDS Journal of Neuroimmune Pharmacology 2007 2 1 93 96
148. Dugo L., Collin M., Thiemermann C., Glycogen synthase kinase 3 as a target for the therapy of shock and inflammation Shock 2007 27 2 113 123 (Pubitemid 46105826)
149. Jope R. S., Yuskaitis C. J., Beurel E., Glycogen synthase kinase-3 (GSK3): inflammation, diseases, and therapeutics Neurochemical Research 2007 32 4-5 577 595 (Pubitemid 46481289)
150. Miyashita K., Nakada M., Shakoori A., Ishigaki Y., Shimasaki T., Motoo Y., Kawakami K., Minamoto T., An emerging strategy for cancer treatment targeting aberrant glycogen synthase kinase 3 β Anti-Cancer Agents in Medicinal Chemistry 2009 9 10 1114 1122
151. Thotala D. K., Hallahan D. E., Yazlovitskaya E. M., Inhibition of glycogen synthase kinase 3 attenuates neurocognitive dysfunction resulting from cranial irradiation Cancer Research 2008 68 14 5859 5868
152. Mishra R., Glycogen synthase kinase 3 beta: can it be a target for oral cancer Molecular Cancer 2010 9 144
153. Medina M., Castro A., Glycogen synthase kinase-3 (GSK-3) inhibitors reach the clinic Current Opinion in Drug Discovery and Development 2008 11 4 533 543 (Pubitemid 351950847)
154. del Ser T., Phase IIa clinical trial on Alzheimers disease with NP12, a GSK-3 inhibitor Alzheimers Dementia 2010 6 S147